increasing soil carbon storage: mechanisms, effects of ...for these mechanisms in global models and...

REVIEWARTICLE

Increasing soil carbon storage mechanisms effects of agriculturalpractices and proxies A review

Marie-France Dignac1 amp Delphine Derrien2amp Pierre Barreacute3 amp Seacutebastien Barot4 amp

Lauric Ceacutecillon5amp Claire Chenu1

amp Tiphaine Chevallier6 amp Greacutegoire T Freschet7 amp

Patricia Garnier1 amp Bertrand Guenet8 amp Mickaeumll Hedde1 amp Katja Klumpp9amp

Gwenaeumllle Lashermes10 amp Pierre-Alain Maron11amp Naoise Nunan4

amp Catherine Roumet7 amp

Isabelle Basile-Doelsch12

Accepted 9 March 2017 Published online 7 April 2017 INRA and Springer-Verlag France 2017

Abstract The international 4 per 1000 initiative aims atsupporting states and non-governmental stakeholders in theirefforts towards a better management of soil carbon (C) stocksThese stocks depend on soil C inputs and outputs They arethe result of fine spatial scale interconnected mechanismswhich stabilisedestabilise organic matter-borne C Since2016 the CarboSMS consortium federates French researchersworking on these mechanisms and their effects on C stocks ina local and global change setting (land use agricultural prac-tices climatic and soil conditions etc) This article is a syn-thesis of this consortiumrsquos first seminar In the first part we

present recent advances in the understanding of soil Cstabilisation mechanisms comprising biotic and abiotic pro-cesses which occur concomitantly and interact Soil organicC stocks are altered by biotic activities of plants (the mainsource of C through litter and root systems) microorganisms(fungi and bacteria) and lsquoecosystem engineersrsquo (earthwormstermites ants) In the meantime abiotic processes related tothe soil-physical structure porosity and mineral fraction alsomodify these stocks In the second part we show how agri-cultural practices affect soil C stocks By acting on both bioticand abiotic mechanisms land use and management practices

This synthesis of the CarboSMS French consortiumrsquos first seminar wasalready published in French Derrien D Dignac M-F Basile-Doelsch IBarot S Ceacutecillon L Chenu C Chevallier T Freschet GT Garnier PGuenet B Hedde M Klumpp K Lashermes G Maron P-A Nunan NRoumet C Barreacute P (2016) Stocker du C dans les sols Quels meacutecanismesquelles pratiques agricoles quels indicateurs Etude et Gestion des Sols23193ndash223We prepared this English version in accordance with Dr DominiqueArrouays chief editor of Etude et Gestion des Sols

Marie-France Dignacmarie-francedignacinrafr

1 UMR ECOSYS INRA AgroParisTech Universiteacute Paris-SaclayF-78850 Thiverval-Grignon France

2 Biogeacuteochimie des Ecosystegravemes Forestiers INRAF-54280 Champenoux France

3 Laboratoire de Geacuteologie de lrsquoENS PSL Research University UMR8538 of CNRS 24 rue Lhomond F-75231 cedex 05 Paris France

4 UMR iEES-Paris (CNRS UPMC INRA IRD) 4 place JussieuF-75005 Paris France

5 Universiteacute Grenoble Alpes Irstea UR EMGR 2 rue de laPapeterie-BP 76 F-38402 St-Martin-drsquoHegraveres France

6 EcoampSols (IRD Montpellier SupAgro Cirad INRA) CampusSupAgro Bldg 12 F-34060 Montpellier France

7 Centre drsquoEcologie Fonctionnelle et Evolutive UMR 5175 (CNRSUniversiteacute de Montpellier Universiteacute Paul-Valeacutery MontpellierEPHE) 1919 route de Mende F-34293 Montpellier France

8 Laboratoire des Sciences du Climat et de lrsquoEnvironnement(LSCEIPSL CEA CNRS UVSQ Universiteacute Paris-Saclay)F-91191 Gif-sur-Yvette France

9 INRA UREP F-63039 Clermont-Ferrand France10 UMR FARE (INRA URCA) F-51100 Reims France11 Agroeacutecologie AgroSup Dijon INRA University Bourgogne

Franche-Comteacute F-21000 Dijon France12 Aix-Marseille Universiteacute CNRS IRD Coll France INRA

CEREGE F-13545 Aix-en-Provence France

Agron Sustain Dev (2017) 37 14DOI 101007s13593-017-0421-2

(choice of plant species and density plant residue exportsamendments fertilisation tillage etc) drive soil spatiotempo-ral organic inputs and organic matter sensitivity tomineralisation Interaction between the different mechanismsand their effects on C stocks are revealed by meta-analysesand long-term field studies The third part addresses upscalingissues This is a cause for major concern since soil organic Cstabilisation mechanisms are most often studied at fine spatialscales (mmndashμm) under controlled conditions while agricul-tural practices are implemented at the plot scale We discusssome proxies and models describing specific mechanisms andtheir action in different soil and climatic contexts and showhow they should be taken into account in large scale modelsto improve change predictions in soil C stocks Finally thisliterature review highlights some future research prospectsgeared towards preserving or even increasing C stocks ourfocus being put on the mechanisms the effects of agriculturalpractices on them and C stock prediction models

Keywords Soil organic C C dynamics Stabilisationmechanisms Mineralisation Agricultural practices

Indicators Models Macrofauna Microorganisms Litter

Root inputs Organomineral associations Porosity

Contents1 Introduction2 Soil C storage mechanisms state of the art

21 Action of living biomass on soil organic Cdynamics211 Plants rhizosphere and soil organic C stor-

agemdashimportance of root systems212 Impact of living organisms on soil C seques-

trationmdashthe macrofauna case213 Diversity and physiology of microorgan-

ismsmdashdrivers of soil C dynamics22 Abiotic soil organic C stabilisation mechanisms

221 Localisation in the physical structure of soil222 C stabilisation mechanisms involving

organomineral interactions3 Mechanisms of OM dynamics affected by agricultural

practices31 Review of the main agricultural practices32 Impact of agricultural practises on soil organic C

storage4 How could a better accounting of OM stabilisation

mechanisms improve the prediction of soil organic Cstock evolution41 Finding indicators to improve prediction of chang-

es in soil organic C stocks42 Better integration of OM stabilisation mechanisms

in large-scale C dynamics models

43 Modelling OM mineralisation at the micro-scalecould help in describing macroscopic C fluxes

44 Data needed to constrain various approaches toenhance prediction of soil C stock evolutionpatterns

5 ConclusionAcknowledgmentsReferences

1 Introduction

The increasing atmospheric concentration of greenhouse gas-es (GHG) particularly those containing carbon (CO2 CH4) isa consequence of human activities and is associated with cli-mate change Anthropogenic carbon emissions are partiallybalanced by carbon (C) sinks in oceans vegetation and soil(Le Queacutereacute et al 2015) Soils contain approximately threetimes more C than the atmosphere (2400 vs 800 GtC)(Jobbaacutegy and Jackson 2000) in the form of organic C bornein organic matter (OM) On decadal time scales soils canserve as a C sink or source depending on their properties onthe climate land use etc (Eglin et al 2010)

Global models linking the atmospheric CO2 concentrationto temperature show that a 35ndash4 Gtyear decrease in atmo-spheric C would limit the temperature increase to +152 degC by2050 (Meinshausen et al 2009 Minasny et al 2017) ie thethreshold beyond which climate change would have a signif-icant impact (IPCC 2013) This annual decrease in the atmo-spheric CO2 concentration could be fulfilled by annually in-creasing C stocks in the top 30 cm soil horizon by 04 (4 per1000) (Balesdent and Arrouays 1999 Paustian et al 2016)

In this context the 4 per 1000mdashCarbon Sequestration inSoils for Food Security and the Climate initiative launched byFrance in 2015 ahead of COP21 in Paris (http4p1000org)aims to bring together governmental and non-governmentalstakeholders devoted to improving soil C stock managementPositive effects on food security and climate change are ex-pected through the collective objective of increasing C stockson a global scale in agricultural areas (croplands grasslandsforests) on which human action can be oriented towards Cstorage (Paustian et al 2016) Indeed increasing soil OMstocks is also beneficial for soil fertility since OMmineralisation might be a source of nutriments for plantsBut this requires implementing agricultural practices adaptedto local conditions that will increase soil C inputs with out-puts remaining stable or decreasing thus maximising soil Cstorage

Soil OM is not homogeneous and some OM is quicklymineralised after entering the soil while some persists for verylong periods (Schmidt et al 2011) Conceptual pools weresometimes associated to functional pools tentatively separatedfrom soils according to chemical or physical fractionation

14 Page 2 of 27 Agron Sustain Dev (2017) 37 14

(eg Balesdent 1996 Zimmermann et al 2007 Crow et al2007Moni et al 2012) In recent years the significance of thechemical fractions obtained after the so-called humic sub-stances separation have been questioned since they are prob-ably artefacts formed during the drastic chemical extractiontreatment (Schmidt et al 2011) Reconciliating conceptualand experimental pools of soil C with different dynamicsis still a matter of research especially when soil organicmatter is now accepted as a continuum of organic mole-cules possibly associated with minerals (Lehmann andKleber 2015)

Three soil conceptual C pools are generally defined accord-ing to their degradation rate (Fig 1) (von Luumltzow et al 2008)Labile OM turnover occurs within a day to a year OM turn-over in the intermediate pool occurs within a few years todecades Both pools originate predominantly from plant ani-mal bacterial and fungal residues The intermediate pool isalso supplied by OM degradation products from the labilepool This OM pool is rather active with rather fast turnoverso it is highly influenced by soil management practicesFinally the turnover of the stable OM pool occurs on timescales ranging from decades to centuries It originates fromlabile and intermediate pools and involves most of the soilorganic C (Torn et al 2009) It consists of plant animal bac-terial or fungal residues and microbial metabolic productsOM in the stable pool can be found in aggregates andoradsorbed on mineral surfaces

The challenge for the 4 per 1000 initiative is to increase thesize of the intermediate and stable C pools in order to maxi-mise the sustainability of additional C storage ie maximisingthe residence time of this additional C in soil C storagerelease in these reservoirs is driven by biotic and abiotic mech-anisms that operate at fine spatial scales within the soilorganomineral matrix It is essential to understand these mech-anisms and interactions so as to be able to anticipate andcontrol changes in soil C contents in an ever-evolving envi-ronment (changes in land use agricultural practices climatic

or edaphic conditions etc) Many research groups are ad-dressing these scientific challenges while striving to overcomescientific knowledge gaps on these mechanisms However itis hard to compare this information on various spatiotemporalscales which has led to the creation of a national researchnetwork in France (to be expanded internationally) to federatethe strengths of our scientific community on this issue

The CarboSMS (Carbon StabilizationMechanisms in Soil)research network was launched in late 2015 and currentlyconsists of about 110 members Some 70 researchers attendedthe CarboSMS kickoff meeting at the Ecole NormaleSupeacuterieure (ENS) in Paris on 10 March 2016 The presentarticle summarises the outcome of this meeting In the firstpart we present recent advances on the mechanisms involvedin soil organic C sequestration and then discuss the effects ofagricultural practices on these mechanisms in the second partFinally in the third part we show how it is essential to accountfor these mechanisms in global models and define indicatorsto describe C dynamics in order to enhance the prediction ofthe patterns of change of soil organic C stocks

2 Soil C storage mechanisms state of the art

Two main types of mechanisms influence the stabilisationdestabilisation of soil organic C biotic mechanisms relatedto living soil biomass and soil biodiversity (plants fauna mi-croorganisms) and abiotic mechanisms (localisation in the soilphysical structure and degradationstabilisation hotspotsorganomineral interactions) For the sake of clarity thesemechanisms will be discussed successively in the followingsection although they occur simultaneously in soils combin-ing or neutralising their effects

21 Action of living biomass on soil organic C dynamics

211 Plants rhizosphere and soil organic Cstoragemdashimportance of root systems

The effects of plants on soil OM are twofold First as auto-trophic organisms plants are the main source of soil organic Cthrough their litter production (shoots and roots) root exu-dates (released through passive and active mechanisms) andvia symbiotic (nitrogen-fixing and mycorrhizal) associationsSecond plants contribute to soil OM stabilisation mechanismsby producing poorly degradable compounds and by promot-ing stable aggregate formation By limiting erosion plantsalso contribute to soil OM conservation

Plants have a broad range of root systems and their influ-ence on soil OM varies with the plant species and root func-tional traits (ie architecture morphology physiology chem-ical composition and symbiotic associations Fig 2)

Fig 1 Conceptual pools of soil C depending on its turnover time labileintermediate and stable pools

Agron Sustain Dev (2017) 37 14 Page 3 of 27 14

OM fluxes from plants to soils C inputs to the soil consist ofabove- and belowground litter (leaves branches stemrootshellip) but also of rhizodeposits and of compounds thatare directly transferred to mycorrhizal fungi Root litter con-tributes about one third of total litter inputs in grassland soilsand half in forest soils (Freschet et al 2013) Rhizodepositionrepresents about 11 of the C assimilated by plants or 27 ofthat allocated to roots (Jones et al 2009 Balesdent et al2011) The type and intensity of mycorrhizal associationsand therefore of C transfers to mycelial hyphae depend re-spectively on the plant phylogenetic identity and on soil fac-tors especially on the availability of soil nutrients(Soudzilovskaia et al 2015)

Some recent and debated studies suggest that belowgroundinputs largely contribute to OM which is stabilised in soils onthe medium to long term (Balesdent and Balabane 1996Kuzyakov and Domanski 2000 Mendez-Millan et al 2010Clemmensen et al 2015) especially in deeper soil horizons(Rasse et al 2005 Rumpel and Koumlgel-Knabner 2011Mendez-Millan et al 2012) In particular the study by

Jobbaacutegy and Jackson (2000) showed that the vertical rootdistribution corresponds to that of soil organic C for differentplant species and soil types Indeed root litter decompositionis generally 30 slower than leaf decomposition (Birousteet al 2012 Freschet et al 2013) In addition abovegroundlitter inputs are only partly transferred into the mineral soil(Garten 2009) where the decomposition rate decreases withincreasing depth (Garcia-Pausas et al 2012 Poirier et al2014 Prieto et al 2016)

The contribution of belowground input to C storage occursthrough the persistence of plant residues or via the stimulationof soil microbial activity and the increase of the contributionof microbial necromass to the slow cycling soil OM pools(Beniston et al 2014 DuPont et al 2014 Lange et al 2015Morrieumln et al 2017)

The architecture and rooting profile of species are thuscritical traits that control the amount and location of C inputsin the soil profile Amongst herbaceous plants monocots gen-erally produce greater root biomass than forbs (Poorter et al2015) and have higher fine root densities (Craine et al 2003)

Fig 2 Differences in functional traits and symbiotic associations between different plant species influence soil organic matter stabilisation Adaptedfrom Freschet et al (in press)


suggesting larger C inputs to soil Lange et al (2015) alsodemonstrated that higher plant diversity increases rhizospherecarbon inputs

Quality of OM inputs and impact on their decompositionrate The chemical composition [eg concentration in C ligninsnitrogen (N) and manganese (Mn)] of aboveground and below-ground litter inputs and root exudates varies markedly betweenplant species and influences OM decomposition kinetics on timescales ranging from year to decade (Jones et al 2009 Machinetet al 2011 Birouste et al 2012) It is commonly recognised that ahigh lignin content leads to the accumulation of particulate OMin the soil (Cotrufo et al 2015) and increases the plant residuecontribution to the intermediate OM pool (Fig 1) The litter Mncontent stimulates lignin degradation through the formation ofMn peroxidases involved in lignin oxidation (Berg 2014Keiluweit et al 2015a) High N levels in plant litter and residuesgenerally increase their initial decomposition rate and result inthe accumulation of microbial residues that persist in the soil Atthe same time high N levels in plant residues inhibit the specificdecomposition of lignins (Berg et al 2010 Dignac et al 2002Martins and Angers 2015) probably due to the recombination ofNwith partially decomposed lignin molecules (Berg et al 2010)

The type and intensity of mycorrhizal associations stronglyinfluence the OM fate in soils (Fig 2) (Clemmensen et al2013 2015) Roots colonised by ectomycorrhiza as well asmycelial hyphae from both ecto- and endomycorrhiza decom-pose more slowly than non-mycorrhizal roots (Langley et al2006) Moreover mycorrhizal hyphae differ in their morpho-logical (diffuse vs rhizomorphic) and biochemical (hyalinevs melanised) characteristics (Fernandez and Kennedy2015) Melanised compounds could be involved in fungalOM persistence in soils (Fernandez et al 2016) Several recentstudies suggest that the chemical composition of OM inputs maynot explain their persistence in soils beyond a decade but has animpact on the C pool cycling over year to decade Over longertime scales this persistence would depend more on environmen-tal conditions (Amelung et al 2008 Derrien et al 2006Thevenot et al 2010 Schmidt et al 2011 Andreetta et al2013 Lehmann and Kleber 2015 Mathieu et al 2015)

Impact of plant residue inputs on soil OM degradation(priming effect) Fresh OM inputs that are easily used by soilmicrobial decomposers such as root exudates leachates andthe labile portion of litter can also stimulate native soil OMdegradation This so-called priming effect can be explained bythree potentially co-occurring mechanisms (Loumlhnis 1926Fontaine et al 2004 2007 Blagodatskaya and Kuzyakov2008) (1) increased activity and development of microbialcommunities specialised in acquiring labile resources (r-strategists) resulting in increased soil enzymatic activities withpotentially negative effects on soil OM storage (2) stimula-tion of microbial communities adapted to the degradation of

less degradable substrates (K-strategists) which depends onthe nutrient availability in soils (Fontaine et al 2011 Derrienet al 2014) and (3) the action of root exudates (eg oxalicacid) disrupting soil organomineral associations and providingmicroorganisms with access to previously stabilised organiccompounds (Keiluweit et al 2015b)

Aggregate stability and soil layer cohesion Plants contributeto the formation of stable aggregates (OM protected from degra-dation see Section 221 below) in soil through fine roots andmycorrhizal associations (Tisdall and Oades 1982) High fine rootand mycelial hyphae densities improve aggregate stability (Fig 2)(Wu et al 2014 Erktan et al 2016) through different mechanisms(1) increased production of root exudates such as polysaccharideswhich act as a glue between soil particles (2) better soil particletrapping facilitated by the entanglement of roots and hyphae (3)increased wetting-drying cycle frequency in soil in relation to wa-ter acquisition by roots (4) input of plant residues containingspecific constituents (eg hemicellulose suberin or phenolic com-pounds) that contribute to macroaggregate stability and (5) stimu-lation of the production of microbial metabolites involved inmicroaggregate stability (Martens 2000 von Luumltzow et al 2008Martins and Angers 2015) These processes vary between plantspecies but also depend on mycorrhizal fungi (Rillig et al 2015)Hyphae with a diffuse morphology thus promoting soilndashhyphalinteractions could therefore have a greater impact on soil aggre-gate formation than hyphae of rhizomorphic types (Fernandez andKennedy 2015) Finally polysaccharides secreted by N2-fixingbacteria also have a positive effect on soil aggregate formation(Martins and Angers 2015)

Vegetation also contributes indirectly to soil C storagerelease by affecting soil physical structure The density andpermanence of aboveground plant cover as well as the plantrsquosability to accumulate litter protect topsoil from structuralbreakdown under the action of rainfall (Fig 2) (LeBissonnais et al 2005) Species with high root length density(eg monocot species) and high root branching intensity (egannual species) within topsoil also limits surface erosion andwater runoff by promoting soil particle trapping (Gyssels et al2005) High root length density and fast root turnover alsopromote the formation of galleries that increase the soil poros-ity and limit water runoff (Gyssels et al 2005) However thisalso increases soil moisture and may improve conditions forsoil OM decomposition in deeper soil horizons Finally spe-cies with deep root systems high root length density and highroot branching intensity can improve the cohesion betweensoil layers and limit landslides (Stokes et al 2009)

In conclusion plants influence labile intermediate and sta-ble soil C pools The effects of plants on soil OM stabilisationand protection seem to be mostly positive although the bal-ance between positive and negative effects (ie over-mineralisation) will differ according to interactions betweenplants and the soil abiotic and biotic conditions For instance


plantndashmicrobe plantndashplant plantndashanimal (herbivory-related)and plantndashsoil interactions and their effects on C stabilisationmechanisms have yet to be extensively exploredFurthermore although chemical recalcitrance has been shownto have little influence on long-term soil C stabilisation(Marschner et al 2008 Schmidt et al 2011 Dungait et al2012) it may influence the intermediate C pool (Fig 1) andthe secondary consumptiontransformation of these OMs bymacro- and microorganisms (Moorhead et al 2014) Thesearch for new indicators of C dynamics linked to the chem-ical composition of plant tissues could improve our knowl-edge on these mechanisms In this context another majorchallenge is to gain greater insight into the role of the func-tional diversity of plants and of their symbionts in soil OMstabilisationdestabilisation mechanisms This challenge re-quires stronger interactions between soil science plant andmicrobial ecology and the development of long-term compar-ative laboratory and field studies before testing the relevanceof these mechanisms in models To this aim experimentalplatforms (eg Ecotrons) and stable isotope techniques to dif-ferentiate C fluxes would help to gain insight into how thespatial distribution of roots and their symbionts can influenceOM stabilisation through mechanisms related to soil physicalproperties as presented in the Section 22 of this review

212 Impact of living organisms on soil C sequestrationmdashthemacrofauna case

The diversity of organisms hosted in soils is huge in terms ofsize and function encompassing megafauna macrofauna mi-crofauna and microorganisms Soil macrofauna includes or-ganisms larger than 2 mm with high taxonomic diversity in-cluding millipedes (diplopoda and centipedes) woodliceearthworms some springtails numerous spiders and insects(ants beetles termites) in addition to vertebrates such as ro-dents (mice) and insectivores (moles shrews) Functionallythese animals can be grouped according to their diet(zoophagous herbivorous root-feeding saprophagous soil-feeding etc) or to their impact on their physical and chemicalenvironment The best known group includes lsquoecosystem en-gineersrsquo (earthworms ants and termites) These organismsoften represent a large biomass in soils (individually for earth-worms or socially for termites and ants) having a substantialinfluence on soil OM dynamics (Chevallier et al 2001)(Fig 3)

Processes promotingC stabilization In tropical and temperateregions it is widely recognised that long-termOM stabilisation iscontrolled by interactions between microorganisms (fungi andbacteria) ecosystem engineers (roots earthworms termites ants)and the soil mineral matrix (Lavelle 1997) Ecosystem engineersact by fragmenting litter incorporating it into the soil profile

mixing soil by bioturbation in the profile and influencing dis-solved OM transport (Bohlen et al 2004)

Ecosystem engineers also promote C stabilisation byforming biogenic structures (biostructures such as castingsgalleries veneers fungi wheels termite or ant hills) The Cin these structures can be stabilised through organomineralassociations depending on ingested OM composition (Vidalet al 2016) The type shape and characteristics of these bio-genic structures vary depending on species land-use patternsand seasons (Decaeumlns et al 2001 Hedde et al 2005 Moraet al 2005) The C distribution in these structures eg con-centration decreasing from the centre outwards varies be-tween species For a given species the C distribution in bio-genic structures varies according to their habitats and dependson the soil depth (Don et al 2008 Jimeacutenez et al 2008) Thephysical degradation rate of these structures influences Cstabilisation time scale as well as nutrient release and avail-ability in soils (Le Bayon and Binet 2006 Mariani et al2007a Mariani et al 2007b Jouquet et al 2011)Furthermore the type of OM (macro-debris particulatematter or microbial metabolites) and its location (intra- orinter-aggregate) which differ between ecosystem engineersare also drivers of C dynamics in these biogenic structures(Six et al 2000 Bossuyt et al 2004 Six et al 2004Bossuyt et al 2005)

Processes promoting C mineralisation The transit of soilparticles through the gut of macrofaunal organisms promotescontact between microbes and OM leading to alteration of thechemical structure of the OM This alteration occurs (1) byselective digestion of peptide compounds which alters theirstability (Shan et al 2010) (2) through biochemical changesdue to a succession of extreme pH or redox conditions(Brauman 2000) or (3) by physical remodelling of the parti-cles (West et al 1991) Many groups of soil fauna are known

Fig 3 Earthworm activity affects organic matter dynamics via litterconsumption and soil particle ingestion


to stimulate microbial activity and OM mineralisation in theshort term (Brown 1995 Winding et al 1997)

Micro- and meso-fauna also contribute to the decomposi-tion of litter and plant debris in that their activity regulates theactivity of the soil microbial communities For example thegrazing of bacterial-feeding protozoa or nematodes tends toreduce the microbial density However it also stimulates theactivity of the microbial communities which tends to increaseOM mineralisation rate This is known as the microbial loopprinciple (Bonkowski 2004)

In conclusion trophic activity and the production ofbiostructures by soil fauna especially by the ecosystem engi-neers impact soil C dynamics OM mineralisation is oftenstimulated in the short term but stabilised in the longer termAs a result the quantitative effects are highly variable (Fig 3)Further research is necessary to gain insight into and predictthese effects while taking the functional traits of the organ-isms and their environment into greater account At largerspatiotemporal scales the functional domain defined by theproperties of biogenic structures (eg termitospheremyrmecosphere or drilosphere) strongly influences C storagein the soil profile which affects the overall ecosystemfunctioning

There is also a lack of knowledge about (1) the impact ofthe biochemical quality of OM on its use by soil organismssince the OM they ingest is chosen not only according to itsdegradability but also to its stoichiometric composition inrelation to decomposer needs and (2) the digestive systemof organisms its effect on microorganism selection and theeffect of this selection on biogenic structures Little is alsoknown about the effect of changes in environmental condi-tions (water and nutrient availability) on biogenic structuresResearch on the effects of cultivation practices (tillage pesti-cide use etc) on the soil fauna density and on their trophicinteractions that affect soil C stabilisation would also be nec-essary (see Section 3)

Finally future research on C stabilisation mechanisms insoil hostingmacrofauna should assess the balance between thebeneficial effects of these organisms on C storage and theirnegative effects due to the GHG they emit (CH4 N2O)(Lubbers et al 2013 Chapuis-Lardy et al 2010) In the longterm research projects should also consider the ability of soilfauna to generally positively influence plant biomass produc-tion (Scheu 2003) thus likely increasing soil OM inputs (seeSection 211)

213 Diversity and physiology of microorganismsmdashdriversof soil C dynamics

Within soil decomposers microorganisms are the most taxo-nomically and functionally diversified component (Torsvikand Oslashvrearings 2002 Curtis and Sloan 2005) It is estimated that1 g of soil can host up to 1 billion bacteria representing

1 million species (Gans et al 2005) and up to 1 million fungicomprising up to 10000 species (Hawksworth 1991 Bardgett2005) However the number of neighbouringmicroorganismswith which a single bacterium interacts within a distance ofabout 20 μm is relatively limited (120 cells on average)(Raynaud and Nunan 2014)

By their activity microorganisms play a very importantrole in the ecosystem services provided by soils At the eco-system scale soil microorganisms are vital with regard to (1)nutrient recycling (N phosphorus sulphur potassium etc)essential for plant growth and ecosystem dynamics (2) soilOM storage crucial for preserving the soil structure and fer-tility and (3) soil OM degradation which could dramaticallychange the global climate equilibrium (van der Heijden et al2008) Furthermore microorganisms are the main source oforganic compounds stabilised in the long term (compared toplants) (eg Simpson et al 2007 Schimel and Schaeffer2012) as indicated by studies using molecular biomarkerssuch as sugars and amino sugars proteins and lipids(Derrien et al 2006 Miltner et al 2012)

The soil microbial compartment despite its central role in soilOM transformation is still often considered as a group of ubiq-uitous organisms with high functional redundancy (Nannipieriet al 2003) on the basis of the postulate put forward byBeijerinck (1913) that lsquoeverything is everywhere but the envi-ronment selectsrsquo As such microbial communities are still oftenincluded in compartment models of soil C dynamics as a func-tional black box generating fluxes whose intensity depends onlyon abiotic factors such as temperature humidity pH etc thusexcluding the hypothesis that the diversity and composition ofmicrobial communities as well as trophic interactions (competi-tion commensalism etc) between populations can play a func-tional role (McGill 1996 Gignoux et al 2001)

This vision could be partly explained by the technical lim-itations that have long hindered the characterisation of the vastdiversity of microbial communities in soils thus preventing(1) the identification of microbial populations involved in soilOM degradation and (2) the assessment of the role of micro-bial diversity in soil OM transformation However significantprogress has been made (Fig 4) especially since the begin-ning of the lsquoomicsrsquo era and the advent of molecular toolswhich are currently able to characterise the taxonomic andfunctional diversity of communities in situ and without apriori (Maron et al 2011 Nagy et al 2016) Recent studiesusing these tools have suggested that microbial diversity is animportant parameter that can modulate soil OM turnover andthus the balance between soil C storage and atmospheric CO2

emissions (Tardy et al 2015 Ho et al 2014 Baumann et al2013 Bell et al 2005) Future studies should improve theoverall understanding of microbial mechanisms involved inthis balance (complementary niches facilitation etc)However other studies have indicated that diversity does nothave a role in the balance between C storage and CO2


emissions (Wertz et al 2006 Wertz et al 2007 Griffiths et al2001 and Griffiths et al 2008) Long-term studies at experi-mental sites but also in monitoring networks at national orinternational scales (Gardi et al 2009) will help to gain insightinto the spatiotemporal variability of processes related to mi-crobial diversity and their impact on soil organic C storage

Advances in microbial ecological knowledge are crucialfor understanding how microorganisms use C and thereforeimpact its long-term fate in soil (Schimel and Schaeffer 2012)A substantial proportion of soil C originates from labile com-pounds metabolised by microorganisms and stabilised as mi-crobial residues in organomineral complexes (Miltner et al2012 Clemmensen et al 2013 Cotrufo et al 2015 Haddixet al 2016) The C use efficiency of microorganisms is used toestimate for a given substrate the ratio between mineralised Cand C incorporated in soil OM This C use efficiency variesdepending on the microbial species and their physiology nu-trient availability (N phosphorus sulphur etc) necessary formicrobial metabolism interactions with the soil matrix and theenvironmental conditions (temperature pH moisture etc)(Manzoni et al 2012 Mooshammer et al 2014 Geyer et al2016 Lashermes et al 2016) Moreover it is likely to changedepending on the climatic and atmospheric conditions(Allison et al 2010 Schimel 2013 Sistla et al 2014)

Considering the major contribution of microbial com-munities in processes driving soil C dynamics managingthe microbial component could be a lever for optimising

soil C storage (Jastrow et al 2007) Future researchshould aim at classifying the impacts of climate parame-ters land-use patterns and microbial diversity on C stor-age while also focussing on improving the models byexplicitly incorporating microbial diversity to improvethe prediction of soil C dynamics

22 Abiotic soil organic C stabilisation mechanisms

221 Localisation in the physical structure of soil

Soil is a heterogeneous environment which has an impact onsoil organic C dynamics At the landscape scale soil heteroge-neity is driven by the soil texture and mineralogy and by topol-ogy and management practices At the plot scale agriculturalpractices and plant species are the determinants of heterogene-ity (Etema andWardle 2002 Chevallier et al 2000) At the fineprocess scale the degree of heterogeneity depends on the soilphysical structure which corresponds to the spatial arrange-ment of solid particles (mineral particles OM) and pores inwhich fluids decomposers and soluble compounds circulate(Chenu and Stotzky 2002 Monard et al 2012)Understanding how the soil physical structure affects OM dy-namics is crucial with a view to preserving or even increasingorganic C stocks in soils On the one hand climate change andespecially the water regime affects the environmental

Fig 4 History and methodological developments in microbial ecology Excerpt from Maron et al (2007) with permission of Springer


conditions at the microbial habitat scale while on the otherland use and agricultural practices markedly affect the soilstructure

As mentioned above biotic processes can have a greateffect on aggregation plants with their roots macrofaunawhen they digest organic and mineral soil components togeth-er and microbes by acting on their close organomineral envi-ronment at the nanoscale Abiotic C stabilisation mechanismsare thus highly linked to biotic mechanisms

Soil organic C dynamics are slowed down by inclusion inaggregates From the mid-twentieth century experimentalstudies have demonstrated that aggregation decreases the soilOM mineralisation rate (Rovira and Greacen 1957)Experiments were designed to measure CO2 production aftergrinding of soil aggregates and to compare it to the CO2 emit-ted by the same soil with preserved aggregates The resultsshowed that grinding increased soil organic C mineralisationand that the rate increased with the fineness of the grindingSince then many studies based on physical fractionationmethods have helped to isolate different types of soil aggre-gates and understand their roles in protecting OM Byanalysing samples of soils that had undergone conversionfrom a C3 to a C4 photosynthesis type of vegetation (or thereverse) and using the difference in C isotopic compositionbetweenOM fromC3 and C4 plant types it was shown that (1)the C residence time was greater when plant debris was in-cluded in aggregates than when it was not associated withaggregates and (2) the C residence time in micro-aggregates(lt50 μm)was longer than in macro-aggregates (gt50μm) (egGolchin et al 1994 Besnard et al 1996 Six et al 1998 Sixand Jastrow 2002 Chevallier et al 2004) However the struc-tural difference between micro- and macro-aggregates mightnot be the only factor that could explain these contrasted OMmineralisation rates because (1) the OM nature and qualitymay differ in micro- and macro-aggregates (2) micro- andmacro-aggregates might host different microbial communities(Hemkemeyer et al 2015) and (3) the stability of macro- andmicro-aggregates which regulates the OM storage duration isnot the same (Plante and McGill 2002) However aggregatesand especially micro-aggregates are used as fractions to indi-cate the degree of physical protection of C as estimates of thepools involved in the compartment models on C dynamics atmulti-annual time scales (eg Zimmermann et al 2007 forRothC) Conceptual models describing C dynamics in differ-ent aggregates considering aggregate formation-destructioncycles have recently emerged but their parameterisation isnot yet possible since these models are too complex and notsufficiently constrained (Stamati et al 2013)

Decomposers act on organic substrates in the soil porenetwork OM mineralisation requires contact between the sub-strates and decomposing microorganisms or their enzymes at

themicrometre scale of themicrobial habitat (Chenu and Stotzky2002) Several recently developed techniques have helped gaininsight into the mechanisms by which the physical structure ofsoil regulates OM mineralisation Microtomography helps esti-mate the size and shape of the pores and their degree of connec-tivity Nanoscale secondary ion mass spectrometry (nanoSIMS)and synchrotron radiation [scanning transmission x-ray micro-scope (STXM) and near edge x-ray absorption fine structure(NEXAFS)] imaging can locate OM and microorganisms atthe micrometre scale while also providing chemical informationcomplementary to that obtained through fluorescence microsco-py studies of thin soil sections (Raynaud andNunan 2014) It hasbeen shown that OM-decomposer co-localisation acceleratesbiodegradation (Vieubleacute Gonod et al 2003 Pinheiro et al2015 Don et al 2013) while accessibility of OM to microbesmight be a major driver of soil C dynamics (Dungait et al 2012)This contact can occur by substrate and enzyme diffusion andadvection or via microorganism growth and mobility (Fig 5)Furthermore the local environmental conditions (oxygen pHwater content etc) at the micrometre scale have to be favourablefor microorganism activity The soil structure controls biodegra-dation at the micrometre scale (Juarez et al 2013) Themineralisation rates of simple substrates thus depend on the sizeof the pores in which they are located (Killham et al 1993Ruamps et al 2011) and could be related to the different micro-bial communities present in these habitats (Hemkemeyer et al2015 Hatton et al 2015)

In conclusion by combining experimental approaches in-volving microcosms isotopic labelling 3D imaging andmodelling significant progress should be achieved in thecoming years in understanding how the soil structure controlsOM dynamics and incorporating these controls into modelsStudies at fine spatial scales will be particularly useful to link

Fig 5 Organic matter biodegradation requires direct contact betweenmicroorganisms or their extracellular enzymes and organic substratesand local conditions favourable for microorganisms This transmissionelectron microscopy image of a thin soil section shows that even at themicrometric scale microorganisms and organic materials can bephysically separated (Chenu et al 2014a)


C storage mechanisms to the soil C saturation concept asdiscussed in the third part of this review (Section 4)

222 C stabilisation mechanisms involving organomineralinteractions

Mineral protection of soil OMmdashan old story The idea thatsoil OM can be protected from the mineralising activity ofmicroorganisms by soilminerals emergedmore than 200 yearsago (Thaer 1811 in Feller and Chenu 2012) This protectionhas been included in soil C dynamics models for over 70 years(Henin and Dupuis 1945) Smaller minerals mainly containedin the clay particle-size fraction (less than 2 μm) most effi-ciently protect OM This particle-size class consists of a vari-ety of minerals clay minerals (phyllosilicates) as well as dif-ferent forms ofmetallic oxyhydroxides and poorly crystallisedaluminosilicates (allophane or imogolite types) These finelydivided minerals protect OM by adsorption (eg Jones andEdwards 1998) or by trapping OM within sub-micron aggre-gates thus physically protecting it from the degrading actionof soil microorganisms (Chenu and Plante 2006) The OMdegradation rate is also decreased and stabilisation increasedwhen organic molecules are located in parts of the pore net-work (neck diameter between 10 and 1000 nm) that are satu-rated with water thus limiting oxygen and enzyme diffusion(Zimmerman et al 2004 Chevallier et al 2010)

Chemical interactions and heterogeneous soil OM distri-bution OM adsorption by soil minerals may derive from dif-ferent types of interaction anionic ligand exchange cationicligand exchange cationic bridges or so-called weak interac-tions (including van der Waals forces hydrogen bonding hy-drophobic interactions) The type of interactions involved de-pends on the mineral phases and OM chemical functions (vonLuumltzow et al 2006) Although theoretically these differenttypes of interactions are expected it is however very difficultto directly observe them in soil samples and to highlight anychemical specificity of organomineral interactions using cur-rent state-of-the-art techniques (Lutfalla 2015)

Moreover direct observations on natural samples usingmicroscopic techniques combined with increasingly powerfulcharacterisation tools (atomic force microscopy nanoSIMSSTXMndashNEXAFS etc) showed that OM is adsorbed on min-eral surfaces in the form of patches and does not cover theentire particle surface (eg Ransom et al 1998 Chenu andPlante 2006 Remusat et al 2012 Theng 2012 Rumpel et al2015) An isotopic labelling study further revealed that newlyadsorbed OM preferentially binds to existing patches and notto free mineral surfaces (Vogel et al 2014) These resultssuggest that the capacity of different minerals to protect OMwould depend on their ability to adsorb a large number ofpatches This could explain why the correlation between

specific mineral surfaces and their ability to protect OM ispoor or nonexistent (Koumlgel-Knabner et al 2008)

High importance of low-crystallised mineral forms andmineral weathering Andosol observations chemical extrac-tion results and fine-scale observations suggest that poorlycrystallised mineral forms (pedogenic oxides and amorphousor slightly crystallised aluminosilicates) are particularly effi-cient in stabilising soil OM (Torn et al 1997 Kleber et al2015) They complex soil organic compounds to formorganomineral nano-complexes (noted here nanoCOMx) afew nanometres to a few hundreds of nanometres in sizewhich contain high C concentrations They can be observedby direct transmission electron microscopy analysis (Wenet al 2014) Close correlations between the metallicoxyhydroxide and C contents have been highlighted usingindirect chemical extraction methods (Bruun et al 2010Mikutta et al 2006) thus demonstrating the importance ofnanoCOMx for soil OM stabilisation NanoCOMx havemainly been studied in controlled conditions whereby theyare synthesised by adsorption and co-precipitation (especiallyfor Fe and Al) in batch experiments but further research isneeded on the identification and quantification of these mech-anisms in soils (Kleber et al 2015)

Andosols which have a particularly high OM content arethe systems of choice for studying nanoCOMx formation insoils (Torn et al 1997) The weathering of primary mineralphases produces partially crystallised phases (proto-imogolites) which complex the OM before reaching theirfinal crystalline growth stages (imogolite andor allophane)These proto-imogoliteOM interactions thus have a dual feed-back effect (1) they stabilise organic compounds over periodsof up to several thousands of years (Basile-Doelsch et al2005) and (2) they stop crystal growth of the secondary min-eral phases (Levard et al 2012) Based on these mechanismsa new conceptual model of soil OM stabilisation was pro-posed to highlight the synergy between the continuous alter-ation of minerals and nanoCOMx formation dynamics(Basile-Doelsch et al 2015) (Fig 6) The findings of somestudies carried out on mineral surfaces tend to confirm thismodel (Bonneville et al 2011 Kawano and Tomita 2001)Future research is needed to validate this model on variousmineralogical phases in different soil types

Finally unlike crystallised minerals the kinetics of alter-ation of poorly crystallised minerals in soils may span just afew years to decades which is of the same order of magnitudeas the time scales at which C dynamics are considered in theclimate change context Contrary to general opinion OMmineralisation in organomineral complexes could well bedue to destabilisation of mineral phases which are no longerregarded as immutable at yearly to decadal timescalesKeiluweit et al (2015b) showed for example that some oxa-late type constituents of root exudates destabilised

14 0 of 27 Agron Sustain Dev (2017) 37 14

oxyhydroxide minerals and released initially complexed na-tive OM These compounds which become accessible to mi-croorganisms may be mineralised The destabilisation ofnanoCOMx mineral components has also been shown in ag-ricultural systems (Wen et al 2014) and in some cases asso-ciated with substantial OM loss

Until recently analytical methods have not been effectiveto achieve sufficiently detailed characterisation of the organiccomponent of organomineral complexes to highlight differ-ences depending on the mineral phases to which they areassociated Future research on organomineral complexes willbenefit from recent progress in analytical methods To en-hance integration of theoretical knowledge of these com-plexes future studies on their formation and dynamics willhave to move from the laboratory to the field in order tounderstand how these mechanisms are affected by agriculturalpractices

3 Mechanisms of OM dynamics affectedby agricultural practices

The soil C stock depends primarily on land-use patterns ForFrench soils Martin et al (2011) showed that the 0 to 30 cmmineral horizons contained on average 80 tC haminus1 under forestand grassland 50 tC haminus1 under crops and 35 tC haminus1 in vine-yard soils (Table 1) Any land-use change therefore has amarked effect on the C stock Meta-analyses on this subjecthave shownmassive C loss following the cultivation of forestsand grasslands The meta-analysis of Guo and Gifford (2002)based on 74 publications showed that soil C decreases whencropland replaces native forest (minus42) and pasture (minus59) It

also revealed a drop in C stocks from plantations to grassland(minus10) and from native forest to plantations (minus13) Therapid decrease in C stocks in cultivated soils can be explainedby the generally lower C inputs (Lal et al 2004) and faster OMmineralisation rates due to more intense tillage which mixesdeeper soil horizons and partly destroys the aggregation (Weiet al 2014) However soil C stocks increase after conversionfrom native forest to pasture (+8) crop to pasture (19)crop to plantation (+18) or crop to secondary forest (+53)(Guo and Gifford 2002) Observations by Attard et al (2016)showed the asymmetry of the mechanisms the loss of organicC stocks after cultivation of grassland soil was fast while thereplenishment of these stocks was slow because it depends onthe slow installation and growth of plant roots in the previous-ly cultivated soil Furthermore recent observations showedthat C stock evolution related to land-use changes aremediated by soil parent material (Barreacute et al 2017) the dif-ferences in soil C stocks between old forests and croplandswere higher on calcareous bedrocks than on loess deposits

Operationally these results concerning the impacts of land-use changes on soil C stocks underline the fact that the spatialpatterns of land-use or rotations must be considered with cau-tion However soil C stocks also depend on the agriculturalpractices implemented which determine the input and outputC fluxes in soils depending on soil and climatic conditionsThe following section identifies the main agricultural practicesand examines their impact on the soil C stock

31 Review of the main agricultural practices

Variousmanagement operations (Table 1) can be implementeddepending on the land use The following categories can be

Fig 6 Conceptual models of organomineral interactions differing withregard to the mineral surface properties a In conventional modelsorganic compounds form a series of layers and the turnover ratedecreases when the molecule gets closer to the mineral surface b Themodel proposed by Basile-Doelsch et al (2015) considers that the

alteration of minerals generates nanometre amorphous minerals Theirhigh reactivity and specific surface area promote their interactions withorganic compounds (excerpt from Basile-Doelsch et al 2015 withpermission of ACS Publications)


Tab

le1

Specificities

ofdifferenttypes

ofland

use(non-exhaustivelist)inmetropolitan

France

(croplandsurban

gardensgrasslandsvineyardsforestsandagroforestry

system

s)interm

sof

Ccontent

soilandclim

aticconditionsvegetatio

nsoilstructureresiduemanagem

entexogenousorganicmatterinputsandotherpracticesand

theirspatiotemporalvariability[com

piledon

thebasisof

interviews

with

adozenprofessionalsworking

atthecrossroadbetweenacadem

iaandagricultu

re(agriculturaltechnicalinstitu

tesFrenchNationalF

orestryOfficeetc)]

Forests

Grasslands

Agroforestry

Croplands

Vineyards

Urban

gardens

Average

stocks

(tCha

minus1of

0ndash30

cmM

artin

etal2011)

8080

Not

mentio

ned

5035

Variable

Ccontents(g

kgminus1

soil

Joim

eletal2016)

Average

[minndashm

ax]

3383[148ndash159]

2982[449ndash243]

1692[257ndash5820]

1121[341ndash393]

2815[979ndash5930]

Soilandclim

aticconditions

Poor

acidicsoils

sometim

esflooded

Eventually

soils

onslopes

diversity

ofclim

ates

Diverse

Markedhuman

actio

nOften

basicsoilandwarm

clim

ates

Strong

artificialisation

Plantspecies

Highbiodiversity

includinglegumes

Avoidcompetitionbetween

tree

speciesandcrops

Low

biodiversity

Potentially

grassbandsin

theranks

Aestheticcriterion

Residue

managem

ent

Depends

onexportof

harvestresidues

(brancheslt7cm

indiam

eter)

Depends

ongrazingand

mow

ingintensity

Exporto

fwoodbiom

ass

(exceptleaves)and

cropsresidues

are

sometim

esreturned

tothesoil

Exporto

fharvestresidues

aresometim

esreturned

tothesoil

Leavesandcrushedshoots

eventually

returned

tothesoil

Exporto

ffallenleaves

and

mow

inglawns

Exogenous

OM

inputs

Manure

Eventually

Contributionof

exogenous

OM

from

urbanareaor

manure

Noexogenousinput

Large

inputsof

exogenous

OM

from

urbanorigin

Practices

modifying

soil

physicalstructure

Stum

pandeventualtillage

whenplantin

gcompactionafterheavy

engine

trafficatthinning

(every

10years

approxim

ately)

Often

aggregated

structure

sometim

estillage

Tillageor

no-tillagein

tree

rows

Tillageor

no-tillage

Soilscratchingeventually

decompaction

Packedw

aterproof

volumes

constrainedby

thepipe

network

Otherpractices

Fertilisatio

nrarely

practicedamendm

entif

treesdecline

Fertilisatio

nirrigation

associations

with

legumes

Fertilisationirrigatio

ninorganicam

endm

entpesticides

Temporalspecificity

Forestrevolutio

nabout

60ndash200

years

Sometim

esleys

Cdynamicsmustb

eratio

nalised

accordingto

forestrevolutio

nduratio

n

Annualcropssom

etim

esinterm

ediatecrops

Rapidly

changing

physical

andchem

icalproperties

Spatialh

eterogeneity

Related

toroot

distribution

organicsurfacehorizon

Especially

relatedto

grazingintensity

Lines

oftreeson

grass

bands

Eventually

hedges

and

grassbands

Vinerowsandeventually

grassinter-rows

Veryheterogeneous

alignm

ento

ftrees

fragmented

discontin

uous


distinguished choice of plant species vegetation densityplant export intensity (crop residues returned to the soil orexported grazingmowing of grasslands export of harvestresidues in forest ecosystems etc) addition of exogenousOM irrigation fertilisation tillage etc These practices main-ly control the spatiotemporal distribution of OM inputs to soilalong with the sensitivity of OM to mineralisation both ofwhich affect soil OM stocks (Jastrow et al 2007)

Choice of plant species The choice of plant species has aneffect on the chemical quality of soil OM (Rumpel et al 2009Armas-Herrera et al 2016) and modifies the processesgoverning the dynamics of soil organic C In forests for ex-ample although aboveground litter production is similar forsoftwood and hardwood trees the litter degradation mecha-nisms differ (Berg and Ekbohm 1991 Osono and Takeda2006) In deciduous forest litter generally decomposes fasterand the residues are more deeply incorporated in the soil pro-file because of the biochemical properties of their tissues andtheir impact on the soil chemistry thus impacting for exam-ple the presence and activity of earthworms (Augusto et al2015) As noted above (Section 212) these organisms have astrong influence on soil OM dynamics In grasslands le-gumendashgrass associations promote soil C storage (Li et al2016) In agricultural systems varieties allocating more re-sources to the harvested part (grain) are often selected to in-crease yields This selection decreases the biomass allocatedto vegetative parts including roots which contribute morethan other plant organs to the intermediate OM pool(Section 211)

Soil OM inputs The intensity of plant harvesting for planta-tion management directly impacts plant-derived soil OM in-puts (leaf litter crop residues roots etc) In grasslands theseinputs depend on the number of grazing animals and the mow-ing frequency (Conant et al 2001) in agricultural systems oncrop residue export (Saffih-Hdadi and Mary 2008) in forestson the thinning regime and the exportation of branches of lessthan 7 cm diameter (called harvest residues) (Jandl et al2006) inputs in urban soils depend on the mowing frequencyin parks and on the removal of fallen leaves (Qian and Follett

2002 Lal and Augustin 2011) Exogenous OM is sometimesadded to reduce chemical input and to recycle wasteExogenous OM may be animal manure (Chotte et al 2013)compost or sewage sludge (Hargreaves et al 2008 Lashermeset al 2009) or pyrogenic residues (biochar) (Steiner et al2007 Andrew et al 2013)

The frequency and spatial distributionlocalisation of soilOM inputs differ amongst land uses It is assumed that vege-tation cover present throughout the year increases soil OMinputs as it is the case for permanent grassland under grassbands or when intermediate crops are cultivated during thewinter season C dynamics in soils under ley grasslands showa legacy grassland effect during cropping years leading tolonger residence times of C in their fine fractions comparedto continuously cropped soils (Panettieri et al 2017) Soil OMinputs in forests are also a function of the age of trees at cutting(input of younger trees being lower than input of older ones)Spatially the distribution of plant inputs may be modulated(Fig 7) by seeding (or planting) density by the localised ad-dition of composts by planting of grass bands in vineyards bygrowing hedges in croplands or rows of trees in agroforestrysystems or by aesthetic management of parks and gardens inurban areas (Freschet et al 2008 Strohbach et al 2012 Kulaket al 2013 Cardinael et al 2015)

These practices can increase the quantities of C added tothe soil but the extent to which they also affect C stabilisationmechanisms is unclear Additional soil OM mineralisationcan for example be observed following a fresh OM input(see the priming effect paragraph Section 211)

Practices that stimulate both primary production and de-composer activity Tillage soil decompaction after heavy ma-chinery passages or removal of stumps after clear-cutting aforest stand are also practices that impact not only primaryproduction and soil OM inputs but also OM mineralisationand therefore soil to atmosphere C fluxes These operationsaffect soil properties likely including its structure decompos-er activity (Lienhard et al 2013) and consequently soil organicC stocks (see Section 2) Primary production and decomposeractivity are also impacted by facilities for soil and water con-servation in dry areas by the use of inorganic amendments or

a bFig 7 The spatial distribution oforganic matter can be modulatedby localised compost inputs (aMadagascar) or by setting uprows of trees in the plots (bAgroforestry Melle France)Source T Chevallier and RCardinael


by systematic fertilisation in some cropping regions or in ur-ban gardens (Miller et al 2005 Edmondson et al 2012)However for economic reasons fertilisation practices are verylimited in forests or in poor agricultural areas

32 Impact of agricultural practices on soil organic Cstorage

French experimental field studies on long-term variationsin soil C stocksNumerous studies have already been conduct-ed on the effects of agricultural practices on soil C storageWepresent the results of three recently published experimentslocated in France spanning decadal to multi-decadal periodsOne study concerns forests under conventional managementwhile two were focused on large-scale cropping systems withexogenous OM amendments or reduced tillage

Changes in C stocks in forest soils were monitored in theFrench Permanent Plot Network for the Monitoring of ForestEcosystems (RENECOFOR) by repeated measurements in 102plots managed by the French National Forestry Office at 15-yearintervals (Jonard et al 2017) The observations revealed an av-erage annual increase in C stock of 034 t haminus1 yearminus1 Thisprecisely corresponds to a 4permil annual increase (average stocksin lit ter and in the top 40 cm soil horizon were816 tC haminus1 = 034816 = 0004) The stock increase was largerin coniferous than in deciduous forests (Jonard et al 2017) andwas not linked to increased aboveground inputsWeak linkswerenoted with the litter quality (CN) the history and managementof the stand (regular vs irregular forests)

The effects of the addition of exogenous OM were studied inthe Qualiagro long-term field experiment located atFeucherolles near Paris (France) Various composts andmanureswere applied at a rate of 4 t haminus1 every other year The soil Ccontents measured every other year for 15 years showed signif-icant C accumulation ie 020ndash050 tC haminus1 yearminus1 for soilamended with manure and urban compost (Peltre et al 2012)These organic amendments thus had a positive effect on C stor-age in addition to economic and agronomic benefits (improve-ment of soil fertility and physical structure) However negativeeffects were observed particularly related to fluxes of elementsother than C Organic amendments often contain large quantitiesof N and P thus inducing a risk of over-fertilisation N2O emis-sion and NH3 volatilisation Organic amendments also present arisk associated with the organic contaminants metal contami-nants or pathogens that they may contain (Smith 2009) It isnecessary to better characterise the OM input the reversibilityof its accumulation and effects on the dynamics of other elements(N P etc) in order to better understand and predict the positiveand negative effects of waste-derived organic amendments(Noirot-Cosson et al 2016)

The long-term effects of tillage were studied for 41 years ina large-scale cropping area in the Paris Basin (Boigneville)(Dimassi et al 2014) In this field experiment no significant

effects of tillage or crop management were observed on Cstocks over 41 years Reducing tillage however resulted inrapid soil C accumulation in the first 4 years and then the Cstocks only slightly changed over the next 24 years(+217 tC haminus1 with reduced tillage +131 tC haminus1 with notillage) but additional stored C was later lost (Dimassi et al2014) The lack of ploughing caused soil OM stratificationand changes in soil functioning nutrient availability soil wa-ter holding capacity microbial diversity the amount of fresh Cincorporated in the soil and accordingly the priming effectThe water regime could be the determining factor of Cstoragedestocking in these situations OM mineralisationwas favoured during wet years or when the soils were irrigat-ed particularly at the surface where the majority of C accu-mulated when ploughing was stopped Conversely C accu-mulated during dry years As already suggested by Balesdentet al (2000) this study highlighted the importance of identi-fying quantifying and classifying the different mechanismsaccording to the soil and climatic conditions in order to beable to model and predict soil organic C stocks under differentagricultural and forestry practices

Meta-analyses Meta-analyses are useful for comparing re-sults obtained in various long-term studies in similar exper-imental fields to determine whether the processes triggeredby a specific agricultural practice are widespread Hereafterwe present some examples of recently published meta-analyses on the impacts of irrigation (Zhou et al 2016)tillage (Virto et al 2012) liming (Paradelo et al 2015) andfertilisation (Han et al 2016 Yue et al 2016) on soil Cstocks

The findings of a meta-analysis by Zhou et al (2016) sug-gested that the water availability changed the plant C alloca-tion and the soil OM turnover Drought led to an increase inthe rootshoot ratio and a decrease in heterotrophic soil respi-ration while irrigation led to an increase in soil respiration butalso to higher biomass inputs

Regarding soil tillage the meta-analysis of Virto et al(2012) shows the same trends as the long-term observationby Dimassi et al (2014) No-tillage had little effect on the soilorganic C stocks (see also Luo et al 2010) However second-ary practices of no-till cropping systems (implemented to off-set the lack of tillage as the choice of cropped species and thenumber of rotations) showed positive effects on C storage(Virto et al 2012)

Paradelo et al (2015) reviewed the results of 29 studiesconsidering the effects of liming on soil C stocks Theirmeta-analysis did not reveal an unambiguous effect of limingon C storage The compiled studies had been carried out undera wide range of experimental conditions Moreover they didnot allow quantification of the three key processes driving thedynamics of organic C in soils affected by liming crop


production decomposer activity and soil structure (seeSection 2)

Yue et al (2016) compared 60 studies on the impact of Ninputs on C stocks Their meta-analysis highlighted an in-crease in soil C inputs and no change in output fluxes relatedto increased N inputs Regarding organic C stocks the resultsshowed an increase in C in the organic horizons and the soilsolution but no change in the C stock in the mineral soilhorizons contrary to the findings of the meta-analysis on for-est soils conducted by Janssens et al (2010) However meta-analyses average the results obtained in different contexts andwith different timescales which may overlook effects thatcould be observed at a given site The meta-analysis of Hanet al (2016) confirmed the results of Yue et al (2016) Iffertilisation is complemented by organic amendments thenthe increase in C stocks would be even higher since organicamendments directly contribute to soil OM stocks

In conclusion due to the lack of knowledge on the mech-anisms impacted by agricultural practices it is hard to predicttheir effects on soil C stocks Agricultural practices whichincrease soil OM inputs are often considered to have a posi-tive impact on C storage (Pellerin et al 2013 Chenu et al2014b Paustian et al 2016) However their impact on mech-anisms that contribute to the storagedestocking of soil C (seeSection 2) are not yet clearly understood Meta-analyses andlong-term field studies showed that the relative intensity ofmechanisms contributing to storage and those contributingto destocking may change over time These studies alsoshowed that it is essential to understand how the soil andclimatic conditions modulate soil organic C stabilisationmechanisms

In addition while considering practices in terms of the Ccycle and increased soil C stocks the importance of interac-tions with cycles of other nutrients present in OM (N P Setc) should not be overlooked Finally regardless of the landuse it should be kept in mind that the main challenge for allagricultural stakeholders is to ensure a production level thatwill provide enough food in the context of world populationgrowth and sufficient income for farmers while maintainingemployment Preserving or increasing OM stocks are alsolevers with regard to these issues (Manlay et al 2016)

4 How could a better accounting of OM stabilisationmechanisms improve the prediction of soil organic Cstock evolution

Working at the scale of mechanisms often implies working atfine spatial scales (mmndashμm) only assessing the potential roleof specific mechanisms and studying them in specific condi-tions (laboratory experiments or experiments in specific soiland climatic conditions) Predicting changes in the soil organ-ic C stock through the understanding of mechanisms raises at

least two crucial related issues that will be discussed in thissection (1) upscaling (from μm3 to dm3 and then to the plotlandscape and global scale) and (2) validation (from the po-tential action of a mechanism to its quantitative expression indifferent soil and climatic contexts) Regarding the upscalingissue there are at least three possibilities (1) finding an indi-cator that describes one or more mechanisms (2) introducingmore mechanisms in soil organic C dynamics models (RothCor Century types) or (3) identifying variables measured at themicroscopic scale that allow through appropriate modellingprediction of macroscopic trends Each of these approachesmust then be validated on suitable datasets (Fig 8)

41 Finding indicators to improve prediction of changesin soil organic C stocks

Several indicators have or could be developed to improve theprediction of soil organic C stocks particularly in a context ofland use and practice changes (see IPCC 2006 detailing themethod currently used to estimate changes in soil C stocks)

The most currently discussed indicator is probably the Csaturation deficit Hassink (1997) proposed that the proportionof the fine fraction (lt20 μm) of a soil implies an upper limit toits capacity to store stable C This theoretical limit can becalcu la ted (C s a t ) by par t ic le-s ize measurements(Csat = 409 + 037 times (clay + fine silt)) (Hassink 1997)Sequestration by the fine fraction is due to the physical andphysicochemical protection provided by finely divided min-erals (see Section 222) The C saturation deficit is obtainedby subtracting this theoretical Csat value from the actual OMconcentration in the fine fraction of the soil This indicator hasrecently been used to draw the first map of the potential oforganic C storage in the fine fraction in the 0ndash30 cm horizonof French soils (Angers et al 2011) However this indicator ofthe potential gain of soil organic C has so far never beenvalidated and its relevance for predicting C stock patternsconsecutive to a change in land use or farming practices re-mains to be evaluated (OrsquoRourke et al 2015)

Another approach somewhat similar to that of Hassink(1997) was proposed to assess French soil C storage capacityReacutemy and Marin-Laflegraveche (1974) defined some benchmarkOM levels according to clay and carbonate soil contentsRoussel et al (2001) used this chart to estimate the OM deficitcompared to the benchmark OM contents for French soils Theauthors thus subtracted OM contents referenced in the FrenchSoil Analysis Database (BDAT) from the benchmark OM con-tents listed on the chart proposed by Reacutemy andMarin-Laflegraveche(1974) However the link between the potential of OM gainand the OM deficit calculated using the Reacutemy and Marin-Laflegraveche (1974) chart remains to be validated and the area ofvalidity of this chart is still an open issue (Roussel et al 2001)

Conversely indicators of the risk of soil organic C losscould be developed For example C in a soil with a high


particulate OM content may be more rapidly lost compared toC in a soil that has a greater portion of C associated with themineral matrix (Arrouays 1994 Jolivet et al 2003)Particulate OM contents which are easily measured bystandardised methods could thus be an indicator of the poten-tial for soil C loss Other studies suggest that the biogeochem-ical stability of C might be connected to its thermal stability(Plante et al 2011 Saenger et al 2013 2015 Barreacute et al2016) In this case thermal measurements could serve as aproxy for assessing the amount of organic C that may be lostfollowing a land use or cropping practice change Using ther-mal measurements to assess the C sequestration potentialcould also be considered

Other indicators based on biotic mechanisms of soil organ-ic C sequestration (see Section 21) could probably be usedsuch as the bacteriafungi ratio or indicators based on soilfauna vegetation or litter layer Soil type and mineralogy arealso potential relevant indicators (Mathieu et al 2015 Khomoet al 2016) It should be kept in mind that the measurement ofthese indicators should be rapid and inexpensive to enablethem to be tested in a large variety of soil and climatic con-texts Finally the indicator necessarily represents the seques-tration mechanisms in partial and degraded form but its pre-dictive value will only be satisfactory if it has a sound scien-tific basis and has been subject to a specific validation processThese conditions have currently not been met for any indica-tor thus broadening the prospects for research validation andimplementation of such indicators of soil C stock changes In

addition selecting relevant indicators for C storage initiativesis still a complicated task Indeed indicators could trace the Cstorage potential of soils (like those described above) or othervariables such as the storage rate input fluxes averagemineralisation rate mean residence time in soil etc

42 Better integration of OM stabilisation mechanismsin large-scale C dynamics models

The prediction of the evolution of C stocks by Earth-systemmodels is very uncertain (eg Friedlingstein et al 2006) Acomparison of Earth-system models showed for a given an-thropogenic GHG emission change scenario that thesemodels can predict a soil organic C stock evolutionary patternfor the twenty-first century ranging from minus50 to +300 GtC(Eglin et al 2010) The difference between the extremes ofthe predicted values corresponds to about 40 of the currentatmospheric C stock A better prediction of the evolution ofthe atmospheric CO2 concentration is crucial to reduce uncer-tainties about soil C stock changes Soil C stabilisation mech-anisms are not yet taken into sufficient consideration in large-scale models (Luo et al 2016) In particular biological regu-lation (macrofauna microorganisms) and soil structure(Wieder et al 2015) are barely taken into account in thesemodels despite the fact that they are major drivers of soil Cdynamics as noted above (see Section 2)

Furthermore most of these models fail to reproduce theinteractions between primary production and organic C

Fig 8 From the identification of stabilisation mechanisms to their effective consideration to improve the prediction of soil organic C stock evolution


residence time in soils These two variables control theamount of C stored in soils but independently (Todd-Brownet al 2013) However explicitly integrating stabilisationmechanisms into these models is a difficult task We must firstfind a suitable mathematical formalism to describe the mech-anism to be added incorporate it into the model and testwhether the model performance has actually been improved

By this approach various studies have been aimed at intro-ducing the priming effect in C dynamics models (Guenet et al2013 Perveen et al 2014) An equation describing the soilOMmineralisation rate as a function of the fresh OM contentproposed by Wutzler and Reichstein (2008) and adapted byGuenet et al (2013) was introduced in the ORCHIDEE mod-el This function actually improved the performance of themodel for representing incubation data from laboratory exper-iments Simulations based on various scenarios highlightedthat soil storage capacities predicted by the two versions ofthe model could differ by up to 12GtC (ie 08 tC haminus1) for thetwenty-first century (Guenet et al submitted)

The explicit representation of all sequestration mechanismsin Earth-system models is not yet possible since it would ne-cessitate excessively long calculation times and since the equa-tions needed to describe many mechanisms have yet to be ac-curately formulated They could however be quickly improvedby increasing the number of comparisons between statisticaland mechanistic models and by testing the mechanistic modelson databases that exist or are under development

However the lack of precise data still hampers the use andimprovement of models especially at large spatial scales andin the vertical profile (Mathieu et al 2015 He et al 2016 Balesdent et al in press) There are indeed very strong uncer-tainties with regard to C stock estimates and the input data ofthese models (soil parameters land use C inputs etc) Theprogress achieved in the GlobalSoilMap project in developingwell-resolved global maps of soil characteristics (Arrouayset al 2014) is also essential for improving the representationof sequestration mechanisms in Earth-system models

43 Modelling OMmineralisation at the micro-scale couldhelp describing macroscopic C fluxes

Another approach is to precisely describe soil OMmineralisation in micro-scale models and investigatehow these models could usefully fuel C dynamics modelsoperating at larger scales (plot landscape global) Forexample a few models have emerged during the past de-cade explicitly describing the functioning of soil micro-organisms in interaction with their substrates their envi-ronment and soil OM (Schimel and Weintraub 2003Fontaine and Barot 2005 Moorhead and Sinsabaugh2006 Allison 2012) Some of these models include therepresentation of several functional groups of microorgan-isms (eg copiotrophic and oligotrophic categories) with

homogeneous ecological functioning features These newmodels including microbial processes are more consistentwith the actual processes and can be more generally ap-plied for various environmental situations However theyare more complex often theoretical and not calibrated(Guisan and Zimmermann 2000) One current challengeis to improve their predictive accuracy by testing them onsuitable experimental observations (Schmidt et al 2011)This requires research conducted on various scales (pop-ulations communities ecosystems) to (1) prioritize keyfactors for predicting soil C dynamics and interactionswith nutrient cycles and (2) integrate robust and simpli-fied functions in larger scale models

A new generation of mechanistic models has also emergedthat take the effects of the soil physical structure on the activityof decomposers and on C mineralisation into account Thesemodels include an explicit 2D or 3D description of the porenetwork based on computer tomography images (Monga et al2008 2014 Falconer et al 2007 2015 Pajor et al 2010Resat et al 2012 Vogel et al 2015) They operate over shorttime scales and have been validated for simplified systemsThese models should facilitate the classification of variablescontrolling C dynamics in order to define soil structure de-scriptors other than those currently used in models at the plotscale so as to improve them

An effective strategy could be to use emerging propertiesfrom micro-scale models that explicitly take fine-scale soilheterogeneity into account to fuel ecosystem modelsOtherwise simplified versions of fine-scale models that cap-ture fine-scale soil heterogeneity could be designed and inte-grated in ecosystem models However such upscaling frommicrometre to plot and then global scales is a difficult taskspanning a vast field of research

44 Data needed to constrain various approachesto enhance prediction of soil C stock evolution patterns

Irrespective of the approach used to connect thestabilisation mechanisms to the evolution of soil C stocksthe predictions must be compared to field data Changes inC stocks are hard to detect in the short term (lt10 years)which is a methodological challenge for the implementa-tion of the 4 per 1000 programme The detection of chang-es in soil C stocks currently involves repeated analysesover time in long-term field studies (Fornara et al 2011)or chronosequences (Poumlplau et al 2011) In addition toassess whether predictions of a particular approach couldbe generalised it would be useful to compare the predic-tions to data collected for different plant covers in varioussoil and climatic contexts As such networks of long-termfield experiments and soil monitoring programmes men-tioned above (Section 3) are particularly useful For in-stance at sites equipped with flux towers C stocks soil


properties and site management history are monitored inaddition to ecosystem to atmosphere gas fluxes Many suchsites have been developed in recent years and there arecurrently about 600 worldwide for a variety of ecosystemsthus enabling relevant data synthesis For example a re-cent study evaluated changes in primary production ingrasslands according to the nitrogen fertilisation and cli-mate (annual rainfall and temperature) conditions(Gilmanov et al 2010 Soussana et al 2010) while alsoassessing organic C sequestration in grassland soils ac-cording to the nitrogen fertilisation harvested biomass (ag-ricultural practices) and soil and weather conditions Othersyntheses of data from flux tower sites showed that the Cbalances were instead controlled by management practicesin young forests and by climate variations in mature forests(Kowalski et al 2004) Soil organic C storage was found toincrease with the number of days of plant growth (Granieret al 2000)

Another interesting example is the use of Free-Air CO2

Enrichment experimental systems which artificially increasethe atmospheric CO2 concentration Such experiments havebeen developed for several years now and have generatedessential information on the response of ecosystems to in-creased atmospheric CO2 concentrations (Ainsworth andLong 2005) Regarding the soil they have shown that C stockincreases when nitrogen is available and does not vary whennitrogen is limiting despite increased input via litter produc-tion (Hungate et al 2009) These data were compared withlarge-scale model outputs for different output variables(Walker et al 2015)

Networks of sites thus enable us to estimate the importanceof stabilisation mechanisms for C storage to classify them (byexploring databases) and to validate approaches designed toimprove prediction of soil C stock evolutionary patternsHowever changes in soil C stocks are often not observablefor several years after a changemdashthis key factor highlights thefact that such sites must absolutely be maintained in the longterm

In conclusion enhanced integration of soil OMstabilisation mechanisms in models to improve predictionsof the evolution of soil C stocks is not easy Several ap-proaches could be proposed each with their positive and neg-ative features Building soil C storage indicators based onmechanisms is the simplest approach but they may have verylimited predictive value if they have a weak scientific basisdue to the excessive uncertainty level Finding a suitable androbust formalism to incorporate the mechanisms in large-scalemodels is often a major research challenge in itself Linkingstabilisation mechanisms and modelling of soil C stock dy-namics requires collaboration of scientific communitiesconducting research on mechanisms and modellingmdashthis isthe only way to accurately assess medium- and long-termvariations in soil organic C stocks in a changing environment

5 Conclusion

The currently favoured solution of the 4 per 1000 initiative toincrease soil C stocks is to increase soil C input fluxes throughmanagement practices adapted to local conditions Thesepractices not only influence soil C inputs but also soil Cstabilisation and destabilisation mechanisms and therefore soilC outputs

Recent studies have improved the overall understanding ofbiotic and abiotic mechanisms involved in soil organic Cstabilisationdestabilisation Belowground plant contributionshave a major role in soil C storagedestocking Contrary toaboveground litter that might be quickly mineralised rootinputs could greatly contribute to C inputs that may bestabilised in soils although they may also induce over-mineralisation of native OM especially when nutrient re-sources are limited Plant residues supply intermediate andlabile soil C pools and through their chemical compositioncontrol their dynamics They also indirectly act on the stable Cpool by promoting aggregate formation through roots andmycorrhizal associationsMicroorganisms and soil fauna havea central role in soil C storagedestocking mechanisms be-cause they consume and transform OM Their metabolic ac-tivity produces CO2 and CH4 (destocking) when they con-sume applied (exogenous) and native (endogenous) OMHowever the action of soil organisms is generally consideredto produce secondary compounds that ultimately contribute tosoil C stabilisation either via their chemical recalcitrance orvia the interactions they establish with mineral soil ions andsurfaces Soil organisms are also essential for nutrientrecycling and preserving ecosystem balance and biodiversityAll of these co-benefits tend to indicate that soils with highbiological activity have a higher C storage potential Howevertheir management requires increased knowledge on theinteracting mechanisms and is more operationally difficultThe 4 per 1000 initiative will have to consider these antagonistbiotic mechanisms in its recommendations in order to balancehigher soil C stabilization with respect to C mineralisation

The action of decomposers on OM depends on the arrange-ment between particles (inorganic and organic) and on thenetwork of pores in which the fluids decomposers and theirenzymes circulate Recent studies have also highlighted thecentral role of mineral phases in protecting OM However itappears that all mineral surfaces do not have the same abilityto protect organic compounds and that organomineral com-plexes evolve over time due to weathering processes Recentlydeveloped tools should lead to significant progress in the un-derstanding and modelling of the influence of the soil matrixstructure on soil C storagedestocking

The effects of OM stabilisation mechanisms must bestudied throughout the soil profile including deep soilhorizons (up to parent material) since plant root systemshave a very high impact C dynamics models should


therefore not be limited to the soil surface since deep soilsare also impacted by agricultural practices and land-usepatterns These models should try to find indicators thatexplicitly take the different soil compartments into ac-count and no longer consider the microbial componentas a lsquoblack boxrsquo while also considering the soil faunaResearch on the validation of indicators of these mecha-nisms is essential in order to take the complexity of theequation involving biological factors physical interac-tions soil and climate conditions land-use patterns prac-tices and management into account

This review highlighted three essential needs for future re-search on soil C storage long-term monitoring of experimentalsites reliable and precisely resolved data (soil parameters land-use patterns and practices) particularly at large spatial scalesand multidisciplinary interactions between researchers in thefields of soil science and ecology Indeed although the differentmechanisms are often studied separately they should be studiedtogether as they are related These complex interactions drive Cdynamics Finally it is crucial to strengthen interactions be-tween operational and academic communities in order to accu-rately identify the challenges that still need to be addressed toenhance the overall understanding of the impact of agriculturalpractices on soil C storage to disseminate new knowledge andtranslate it into practical recommendations

Acknowledgments The authors thank all participants of theCarboSMS network meeting of 10 March 2016 We also thank everyonewe interviewed on the links between practices and mechanisms (ManuelBlouin Camille Breacuteal Aureacutelie Cambou Patrice Cannavo MarieCastagnet Annie Duparque Sabine Houot Thomas Lerch DominiqueMasse Anne-Sophie Perrin Noeacutemie Pousse Thomas Turini and LaureVidal-Beaudet) This review was conducted with the financial support ofResMO (French research network on organic matter) ENS-PSL theGeoscience Department of ENS CNRS INSU INRA ANR-Dedycasand ANR-Soilμ3D GTF and CR were supported by the EC2CO-MULTIVERS project (BIOHEFECT-MICROBIEN program CNRS-INSU) We also thank Dr Eric Lichtfouse (Springer) and DrDominique Arrouays (Etude et Gestion des Sols) for authorising us tosubmit this English version of the article already published in French inEtude et Gestion des Sols (Derrien et al 2016)

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Clemmensen KE Finlay RD Dahlberg A Stenlid J Wardle DA LindahlBD (2015) Carbon sequestration is related to mycorrhizal fungalcommunity shifts during long-term succession in boreal forestsNew Phytol 2051525ndash1536 doi101111nph13208

Conant RT Paustian K Elliott ET (2001) Grassland management and con-version into grassland effects on soil carbon Ecol Appl 11343ndash355doi1018901051-0761(2001)011[0343GMACIG]20CO2

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Curtis TP SloanWT (2005) Exploringmicrobial diversitymdasha vast belowScience 3091331ndash1333 doi101126science1118176

Decaeumlns T Galvis JH Amezquita E (2001) Properties of the structurescreated by ecological engineers at the soil surface of a Colombiansavanna Comptes Rendus de lrsquoAcadeacutemie des Sciences de ParisSeacuterie IIImdashSciences de la Vie 324465ndash477 doi101016S0764-4469(01)01313-0

Derrien D Dignac M-F Basile-Doelsch I Barot S Ceacutecillon L Chenu CChevallier T Freschet GT Garnier P Guenet B Hedde M KlumppK Lashermes G Maron P-A Nunan N Roumet C Barreacute P (2016)Stocker du C dans les sols Quels meacutecanismes quelles pratiquesagricoles quels indicateurs Etude et Gestion des Sols 23193ndash223

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Derrien D Plain C Courty P-E Gelhaye L Moerdijk-Poortvliet TCWThomas F Versini A Zeller B Koutika LS Boschker HTS EpronD(2014) Does the addition of labile substrate destabilise old soil or-ganic matter Soil Biol Biochem 76149ndash160 doi101016jsoilbio201404030

Dignac M-F Koumlgel-Knabner I Michel K Matzner E Knicker H (2002)Chemistry of soil organic matter as related to CN in Norway spruceforest (Picea abies (L) karst) floors and mineral soils J Plant NutrSoil Sci 165281ndash289 doi1010021522-2624(200206)1653lt281AID-JPLN281gt30CO2-A

Dimassi B Mary B Wylleman R Labreuche J Couture D Piraux FCohan JP (2014) Long-term effect of contrasted tillage and cropmanagement on soil carbon dynamics during 41 years AgricEcosyst Environ 188134ndash146 doi101016jagee201402014

Don A Steinberg B Schoumlning I Pritsch K Joschko M Gleixner GSchulze E-D (2008) Organic carbon sequestration in earthwormburrows Soil Biol Biochem 401803ndash1812 doi101016jsoilbio200803003

Don A Riedenbeck C Gleixner G (2013) Unexpected control of soilcarbon turnover by soil carbon concentration Environ Chem Lett11407ndash413 doi101007s10311-013-0433-3

Dungait JAJ Hopkins DW Gregory AS Whitmore AP (2012) Soil or-ganic matter turnover is governed by accessibility not recalcitranceGlob Chang Biol 181781ndash2088 doi101111j1365-2486201202665x

DuPont ST Beniston J Glover JD Hodson A Culman SW Lal R FerrisH (2014) Root traits and soil properties in harvested perennial grass-land annual wheat and never-tilled annual wheat Plant Soil 381405ndash420 doi101007s11104-014-2145-2

Edmondson JI Davies ZG McHugh N Gaston KJ Leake JR (2012)Organic carbon hidden in urban ecosystems Scientific Reportsdoi101038srep00963

Eglin T Ciais P Piao SL Barre P BellassenV Cadule P Chenu C GasserT Koven C Reichstein M Smith P (2010) Historical and futureperspectives of global soil carbon response to climate and land-usechanges Tellus-B 62700ndash718 doi101111j1600-0889201000499x

Erktan A Ceacutecillon L Graf F Roumet C Legout C Rey F (2016) Increasein soil aggregate stability along a Mediterranean successional gradi-ent in severely eroded gully bed ecosystems combined effects ofsoil root traits and plant community characteristics Plant Soil 398121ndash137 doi101007s11104-015-2647-6

Etema C Wardle DA (2002) Spatial soil ecology Trends Ecol Evol 17177ndash183 doi101016S0169-5347(02)02496-5

Falconer RE Bown JL White NA Crawford JW (2007) Biomassrecycling a key to efficient foraging by fungal colonies Oikos1161558ndash1568 doi101111j0030-1299200715885x

Falconer RE Battaia G Schmidt S Baveye P Chenu C Otten W (2015)Microscale heterogeneity explains experimental variability and non-linearity in soil organic matter mineralisation PLoS One 101ndash12doi101371journalpone0123774

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Fernandez CW Kennedy PG (2015) Moving beyond the black-box fun-gal traits community structure and carbon sequestration in forestsoils New Phytol 2051378ndash1380 doi101111nph13289

Fernandez CW Langley JA Chapman S McCormack ML Koide RT(2016) The decomposition of ectomycorrhizal fungal necromassSoil Biol Biochem 9338ndash49 doi101016jsoilbio201510017

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Fontaine S Henault C Aamor A Bdioui N Bloor JMG Maire V MaryB Revaillot S Maron PA (2011) Fungi mediate long term seques-tration of carbon and nitrogen in soil through their priming effectSoil Biol Biochem 4386ndash96 doi101016jsoilbio201009017

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Freschet GT Cornwell WK Wardle DA Elumeeva TG Liu W JacksonBG Onipchenko VG Soudzilovskaia NA Tao JP Cornelissen JHC(2013) Linking litter decomposition of above and belowground or-gans to plant-soil feedbacks worldwide J Ecol 101943ndash952 doi1011111365-274512092

Freschet GT Violle Roumet C Garnier E (in press) Interactions entre lesol et la veacutegeacutetation structure des communauteacutes de plantes etfonctionnement du sol In Lemanceau P amp Blouin M (Eds) Les solsau coeur de la zone critique Ecologie

Friedlingstein P Cox P Betts R Bopp L Von BlohW Brovkin V CaduleP Doney S Eby M Fung I Bala G John J Jones C Joos F Kato TKawamiya M Knorr W Lindsay K Matthews HD Raddatz T


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Gans J Wolinsky M Dunbar J (2005) Computational improvementsreveal great bacterial diversity and high metal toxicity in soilScience 3091387ndash1390 doi101126science1112665

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Geyer KM Kyker-Snowman E Grandy AS Frey SD (2016) Microbialcarbon use efficiency accounting for population community andecosystem-scale controls over the fate of metabolized organic matterBiogeochemistry 127173ndash188 doi101007s10533-016-0191-y

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Gilmanov TG Aires L Barcza Z Baron VS Belelli L Beringer JBillesbach D Bonal D Bradford J Ceschia E Cook D CorradiC Frank A Gianelle D Gimeno C Gruenwald T Guo HQHanan N Haszpra L Heilman J Jacobs A Jones MB JohnsonDA Kiely G Li SG Magliulo V Moors E Nagy Z Nasyrov MOwensby C Pinter K Pio C Reichstein M Sanz MJ Scott RSoussana J-F Stoy PC Svejcar T Tuba Z Zhou GS (2010)Productivity respiration and light-response parameters of worldgrassland and agroecosystems derived from flux-tower measure-ments Rangel Ecol Manag 6316ndash39 doi101046j1466-822X2001t01-1-00250x

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Griffiths BS Ritz K Wheatley R Kuan HL Boag B Christensen SEkelund F Sorensen SJ Muller S Bloem J (2001) An examinationof the biodiversity-ecosystem function relationship in arable soilmicrobial communities Soil Biol Biochem 331713ndash1722 doi101016S0038-0717(01)00094-3

Griffiths BS Hallett PD Kuan HL Gregory AS Watts CW WhitmoreAP (2008) Functional resilience of soil microbial communities de-pends on both soil structure and microbial community compositionBiol Fertil Soils 44745ndash754 doi101007s00374-007-0257-z

Guenet B Eglin T Vasilyeva N Peylin P Ciais P Chenu C (2013) Therelative importance of decomposition and transport mechanisms inaccounting for soil organic carbon profiles Biogeosciences 102379ndash2392 doi105194bg-10-2379-2013

Guenet B Camino-Serrano M Ciais P Tifafi M Maignan F Soong JLJanssens IA (submitted) Impact of priming on global carbon emis-sions from soils

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Haddix ML Paul EA Cotrufo MF (2016) Dual differential isotope la-beling shows the preferential movement of labile plant constituentsinto mineral bonded soil organic matter Glob Chang Biol 222301ndash2312 doi101111gcb13237

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Hatton P-J Remusat L Zeller B Brewer EA Derrien D (2015)NanoSIMS investigation of glycine-derived C and N retention withsoil organo-mineral associations Biogeochemistry 125303ndash313doi101007s10533-015-0138-8

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He Y Trumbore SE Torn MS Harden JW Vaughn LJ Allison SDRanderson JT (2016) Radiocarbon constraints imply reduced carbonuptake by soils during the 21st century Science 3531419ndash1424doi101126scienceaad4273

Hedde M Lavelle P Joffre R Jimenez JJ Decaens T (2005) Specificfunctional signature in soil macro-invertebrate biostructures FunctEcol 19785ndash793 doi101111j1365-2435200501026x

van der Heijden MG Bardgett RD van Straalen NM (2008) The unseenmajority soil microbes as drivers of plant diversity and productivityin terrestrial ecosystems Ecol Lett 11296ndash310 doi101111j1461-0248200701139x

Hemkemeyer M Christensen BT Martens R Tebbe CC (2015) Soilparticle size fractions harbour distinct microbial communities anddiffer in potential for microbial mineralisation of organic pollutantsSoil Biol Biochem 90255ndash265 doi101016jsoilbio201508018

Henin S Dupuis M (1945) Essai de balance de la matiegravere organique dusol Annales Agronomiques 16ndash26

Ho A de Roy K Thas O De Neve J Hoefman S Vandamme P HeylenK Boon N (2014) The more the merrier heterotroph richness stim-ulates methanotrophic activity ISME J 81945ndash1948 doi101038ismej201474

Hungate BA van Groeningen K-J Six J Jastrow JD Luo YQ de GraaffMA van Kessel C Osenberg CW (2009) Assessing the effect ofelevated carbon dioxide on soil carbon a comparison of four meta-analyses Glob Chang Biol 152020ndash2034 doi101111j1365-2486200901866x

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IPCC (2013) Climate change 2013 the physical science basisContribution of Working Group I to the Fifth Assessment Reportof the Intergovernmental Panel

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Janssens IA Dieleman W Luyssaert S Subke JA Reichstein MCeulemans R Ciais P Dolman AJ Grace J Matteucci G PapaleD Piao SL Schulze ED Tang J LawBE (2010) Reduction of forestsoil respiration in response to nitrogen deposition Nat Geosci 3315ndash322 doi101038ngeo844


Jastrow JD Amonette JE Bailey VL (2007) Mechanisms controlling soilcarbon turnover and their potential application for enhancing carbonsequestration Clim Chang 805ndash23 doi101007s10584-006-9178-3

Jimeacutenez JJ Decaeumlns T Lavelle P (2008) C and N concentrations inbiogenic structures of a soil-feeding termite and a fungus-growingant in the Colombian savannas Appl Soil Ecol 40120-128 doi101016japsoil200803009

Jobbaacutegy EG Jackson RB (2000) The vertical distribution of soil organiccarbon and its relation to climate and vegetation Ecol Appl 10423ndash436 doi1018901051-0761(2000)010[0423TVDOSO]20CO2

Joimel S Cortet J Jolivet CC Saby NPA Chenot ED Branchu PConsalegraves JN Lefort C Schwartz C (2016) Physico-chemical char-acteristics of topsoil for contrasted forest agricultural urban andindustrial land uses in France Sci Total Environ 54540ndash47 doi101016jscitotenv201512035

Jolivet C Arrouays D Leacutevegraveque J Andreux F Chenu C (2003) Organiccarbon dynamics in soil particle-size separates of temperate forestSpodosols converted to maize cropping Eur J Soil Sci 54257ndash268doi101046j1365-2389200300541x

Jonard M Nicolas M Coomes DA Caignet I Saenger A Ponette Q(2017) Forest soils in France are sequestering substantial amountsof carbon Sci Total Environ 574616ndash628 doi101016jscitotenv201609028

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Jouquet P Ngo TP Nguyen HH Henry-des-Tureaux T Chevallier T DucTT (2011) Laboratory investigation of organic matter mineralizationand nutrient leaching from earthworm casts produced by Amynthaskhami Appl Soil Ecol 4724ndash30 doi101016japsoil201011004

Juarez S Nunan N Duday A-C Pouteau V Schmidt S Hapca S ChenuC (2013) Effects of different soil structures on the decomposition ofnative and added organic carbon Eur J Soil Biol 5881ndash90 doi101016jejsobi201306005

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Keiluweit M Nico P Harmon ME Mao J Pett-Ridge J Kleber M(2015a) Long-term litter decomposition controlled by manganeseredox cycling Proceedings of the National Academy of Sciences1125253ndash5260 doi101073pnas1508945112

Keiluweit M Bougoure JJ Nico PS Pett-Ridge J Weber PK Kleber M(2015b) Mineral protection of soil carbon counteracted by root ex-udates Nat Clim Chang 5588ndash595 doi101038nclimate2580

Khomo L Trumbore S Bern C R Chadwick OA (2016) Timescales of Cturnover in soils with mixed crystalline mineralogies KrugerNational Park South Africa SOIL Discussions doi105194soil-2016-31

Killham K Amato M Ladd JN (1993) Effect of substrate location in soiland soil pore-water regime on carbon turnover Soil Biol Biochem2557ndash62 doi1010160038-0717(93)90241-3

Kleber M Sollins P Sutton R (2007) A conceptual model of organo-mineral interactions in soils self-assembly of organic molecularfragments into zonal s tructures on mineral surfacesBiogeochemistry 859ndash24 doi101007s10533-007-9103-5

Kleber M Eusterhues K Keiluweit M Mikutta C Mikutta R Nico PS(2015) Chapter onemdashmineral-organic associations formation prop-erties and relevance in soil environments In Donald LS (Ed)Advances in agronomy Academic Press pp 1ndash140

Koumlchy M Hiederer R Freibauer A (2015) Global distribution of soilorganic carbonmdashpart 1 masses and frequency distributions of

SOC stocks for the tropics permafrost regions wetlands and theworld Soil 1351ndash365 doi105194soil-1-351-2015

Koumlgel-Knabner I Guggenberger G Kleber M Kandeler E Kalbitz KScheu S Eusterhues K Leinweber P (2008) Organo-mineral asso-ciations in temperate soils integrating biology mineralogy and or-ganic matter chemistry J Plant Nutr Soil Sci 17161ndash82 doi101002jpln200700048

Kowalski AS Loustau D Berbigier P Manca G Tedeschi V BorghettiM Valentini R Kolari P Berninger F Rannik U Hari P RaymentM Mencuccini M Moncrieff J Grace J (2004) Paired comparisonsof carbon exchange between undisturbed and regenerating stands infour managed forests in Europe Glob Chang Biol 101707ndash1723doi101111j1365-2486200400846x

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Kuzyakov Y Domanski G (2000) Carbon input by plants into the soilReview Journal of Plant Nutrition and Soil Science 163421ndash431doi1010021522-2624(200008)1634lt421AID-JPLN421gt30CO2-R

Lal R Augustin B (Eds) (2011) Carbon sequestration in urban ecosys-tems Springer Science amp Business Media

Lal R Griffin M Apt J Lave L Morgan MG (2004) Managing soilcarbon Science 304393 doi101126science1093079

Lange M Eisenhauer N Sierra CA Bessler H Engels C Griffiths RIMellado-Vaacutezquez PG Malik AA Roy J Scheu S Steinbeiss SThomson BC Trumbore SE Gleixner G (2015) Plant diversity in-creases soil microbial activity and soil carbon storage Nat Commun66707 doi101038ncomms7707

Langley JA Chapman SK Hungate BA (2006) Ectomycorrhizal coloni-zation slows root decomposition the post-mortem fungal legacyEcol Lett 9955ndash959 doi101111j1461-0248200600948x

Lashermes G Nicolardot B Parnaudeau V Thuries L Chaussod RGuillotin ML Lineres M Mary B Metzger L Morvan T TricaudA Villette C Houot S (2009) Indicator of potential residual carbonin soils after exogenous organic matter application Eur J Soil Sci 60297ndash310 doi101111j1365-2389200801110x

Lashermes G Gainvors-Claisse A Recous S Bertrand I (2016)Enzymatic strategies and carbon use efficiency of a litter-decomposing fungus grown on maize leaves stems and rootsFront Microbiol doi103389fmicb201601315

Lavelle P (1997) Faunal activities and soil processes adaptive strategiesthat determine ecosystem function Adv Ecol Res 2793ndash132 doi101016S0065-2504(08)60007-0

Le Bayon RC Binet F (2006) Earthworms change the distribution andavailability of phosphorous in organic substrates Soil Biol Biochem38235ndash246 doi101016jsoilbio200505013

Le Bissonnais Y Cerdan O Lecomte V Benkhadra H Souchegravere VMartin P (2005) Variability of soil surface characteristics influencingrunoff and interrill erosion Catena 62111ndash124 doi101016jcatena200505001

Le Queacutereacute C Moriarty R Andrew RM Peters GP Ciais P FriedlingsteinP Jones SD Sitch S Tans P Arneth A Boden TA Bopp L Bozec YCanadell JG Chini LP Chevallier F Cosca CE Harris I HoppemaM Houghton RA House JI Jain AK Johannessen T Kato EKeeling RF Kitidis V Goldewijk KK Koven C Landa CSLandschutzer P Lenton A Lima ID Marland G Mathis JT MetzlN Nojiri Y Olsen A Ono T Peng S Peters W Pfeil B Poulter BRaupach MR Regnier P Rodenbeck C Saito S Salisbury JESchuster U Schwinger J Seferian R Segschneider J Steinhoff TStocker BD Sutton AJ Takahashi T Tilbrook B van der Werf GRViovy N Wang YP Wanninkhof R Wiltshire A Zeng N (2015)Global carbon budget 2014 Earth System Science Data 747ndash85doi105194essd-7-349-2015


Lehmann J Kleber M (2015) The contentious nature of soil organicmatter Nature 52860ndash68 doi101038nature16069

Levard C Doelsch E Basile-Doelsch I Abidin Z Miche H Masion ARose J Borschneck D Bottero JY (2012) Structure and distributionof allophanes imogolite and proto-imogolite in volcanic soilsGeoderma 183-184100ndash108 doi101016jgeoderma201203015

Li Q Yu PJ Li GD Zhou DW (2016) Grass-legume ratio can change soilcarbon and nitrogen storage in a temperate steppe grassland SoilTillage Res 15723ndash31 doi101016jstill201508021

Lienhard P Terrat S Mathieu O Levecircque J Chemidlin Preacutevost-Boureacute NNowak V Reacutegnier T Faivre C Sayphoummie S Panyasiri K TivetF Ranjard L Maron P-A (2013) Soil microbial diversity and Cturnover modified by tillage and cropping in Laos tropical grasslandEnviron Chem Lett 11391ndash398 doi101007s10311-013-0420-8

Loumlhnis F (1926) Nitrogen availability of green manures Soil Sci 22253ndash290

Lubbers IM van Groenigen KJ Fonte SJ Six J Brussaard L vanGroenigen JW (2013) Greenhouse-gas emissions from soils in-creased by earthworms Nat Clim Chang 31ndash8 doi101038NCLIMATE1692

Luo Z Wang E Sun OJ (2010) Can no-tillage stimulate carbon seques-tration in agricultural soils A meta-analysis of paired experimentsagriculture Ecosystems and Environment 139224ndash231 doi101016jagee201008006

Luo Y Ahlstroumlm A Allison SD Batjes NH Brovkin V Carvalhais NChappell A Ciais P Davidson EA Finzi A Georgiou K Guenet BHararuk O Harden JW Il Y Hopkins F Jiang L Koven C JacksonRB Jones CD Lara MJ Liang J McGuire AD Parton W Peng CRanderson JT Salazar A Sierra CA Smith MJ Tian H Todd-Brown KEO Deacutechireacute M van Groenigen KJ Wang YP Ouest TOWei Y Wieder WR Xia J Xia X Xiaofeng X Zhou T (2016)Toward more realistic projections of soil carbon dynamics by earthsystem models Glob Biogeochem Cycles 3040ndash56 doi1010022015GB005239

Lutfalla S (2015) Persistance agrave long terme des matiegraveres organiques dansles sols caracteacuterisation chimique et controcircle mineacuteralogique Thegravesede doctorat en Sciences de lrsquoEnvironnement Universiteacute Paris Saclay

von Luumltzow M Koumlgel-Knabner I Ludwig B Matzner E Flessa HEkschmitt K Guggenberg G Marschner B Kalbitz K (2008)Stabilization mechanisms of organic matter in four temperate soilsdevelopment and application of a conceptual model J Plant NutrSoil Sci 171111ndash124 doi101002jpln200700047

Machinet GE Bertrand I Barriere Y Chabbert B Recous S (2011)Impact of plant cell wall network on biodegradation in soil role oflignin composition and phenolic acids in roots from 16 maize geno-types Soil Biol Biochem 431544ndash1552 doi101016jsoilbio201104002

Manlay RJ Freschet GT Abbadie L Barbier B Chotte J-L Feller CLeroy M Serpantieacute G (2016) Seacutequestration du C et usage durabledes terres en savane ouest-africaine synergie ou antagonisme InSall S BernouxM BrossardM (Eds) Carbone des sols drsquoAfrique etde Madagascar et pratiques de gestion

Manzoni S Taylor P Richter A Porporato A Agren GI (2012)Environmental and stoichiometric controls on microbial carbon-use efficiency in soils New Phytol 19679ndash91 doi101111j1469-8137201204225x

Mariani L Jimenez JJ AsakawaN Thomas RJ Decaens T (2007a)Whathappens to earthworm casts in the soil A field study of C and Ndynamics in neotropical savannahs Soil Biol Biochem 39757ndash767doi101016jsoilbio200609023

Mariani L Jimenez JJ Torres EA Amezquita E Decaens T (2007b)Rainfall impact effects on ageing casts of a tropical anecic earthwormEur J Soil Sci 581525ndash1534 doi101111j1365-2389200700960x

Maron PA Ranjard L Mougel C Lemanceau P (2007) Metaproteomicsa new approach for studying functional microbial ecology MicrobEcol 53486ndash493 doi101007s00248-006-9196-8

Maron PA Mougel C Ranjard L (2011) Soil microbial diversity spatialoverview driving factors and functional interest Comptes Rendusde lAcadeacutemie des Sciences Paris Biologie Seacuterie II 334403ndash411doi101016jcrvi201012003

Marschner B Brodowski S Dreves A Gleixner G Gude A Grootes PMHamer U Heim A Jandl G Ji R Kaiser K Kalbitz K Kramer CLeinweber P Rethemeyer J Schaumlffer A Schmidt MWI Schwark LWiesenberg GLB (2008) How relevant is recalcitrance for the sta-bilization of organic matter in soils J Plant Nutr Soil Sci 17191ndash110 doi101002jpln200700049

Martens DA (2000) Plant residue biochemistry regulates soil carbon cy-cling and carbon sequestration Soil Biol Biochem 32361ndash369 doi101016S0038-0717(99)00162-5

Martin MP Wattenbach M Smith P Meersmans J Jolivet C Boulonne LArrouaysD (2011) Spatial distribution of soil organic carbon stocks inFrance Biogeosciences 81053ndash1065 doi105194bg-8-1053-2011

Martins MR Angers DA (2015) Different plant types for different soilecosystem services Geoderma 237-238266ndash269 doi101016jgeoderma201409013

Mathieu JA Hatteacute C Balesdent J Parent E (2015) Deep soil carbondynamics are driven more by soil type than by climate a worldwidemeta-analysis of radiocarbon profiles Glob Chang Biol 214278ndash4292 doi101111gcb13012

McGill WB (1996) In Evaluation of soil organic matter models edsPowlson DS Smith P Smith JU (Springer Rothamsted) pp 111ndash132

MeinshausenMMeinshausen N HareW Raper SC Frieler K Knutti RFrame DJ Allen MR (2009) Greenhouse-gas emission targets forlimiting global warming to 2degC Nature 4581158ndash1162 doi101038nature08017

Mendez-Millan M Dignac M-F Rumpel C Rasse DP Derenne S (2010)Molecular dynamics of shoot vs root biomarkers in an agriculturalsoil estimated by natural abundance 13C labelling Soil BiolBiochem 42169ndash177 doi101016jsoilbio200910010

Mendez-Millan M Dignac M-F Rumpel C Rasse DP Bardoux GDerenne S (2012) Contribution of maize root derived-C to soil or-ganic carbon throughout an agricultural soil profile assessed bycompound-specific 13C analysis Org Geochem 421502ndash1511doi101016jorggeochem201102008

Mikutta R Kleber M Torn M Jahn R (2006) Stabilization of soil organicmatter association with minerals or chemical recalcitranceBiogeochemistry 7725ndash56 doi101007s10533-005-0712-6

Miller AE Schimel JP Meixner T Sickman JO Melack JM (2005)Episodic rewetting enhances carbon and nitrogen release from chap-arral soils Soil Biol Biochem 372195ndash2204 doi101016jsoilbio200503021

Miltner A Bombach P Schmidt-Brucken B Kastner M (2012) SOMgenesi s mic robia l b iomass as a s igni f icant source Biogeochemistry 11141ndash55 doi101007s10533-011-9658-z

Minasny B Malone BP McBratney AB Angers DA Arrouays DChambers A Chaplot V Chen Z-S Cheng K Das BS Fielda DJGimona A Hedley CB Hong SY Mandal B Marchant BP MartinM McConkey BG Mulder VL ORourke S Richer-de-Forges ACOdeh I Padarian J Paustian K Pan G Poggio L Savin I StolbovoyV Stockmann U Sulaeman Y Tsui C-C Varinggen T-G vanWesemaelBWinowiecki L (2017) Soil carbon 4 per mille Geoderma 29259ndash86 doi101016jgeoderma201701002

Monard C Mchergui C Nunan N Martin-Laurent F Vieubleacute-Gonod L(2012) Impact of soil matric potential on the fine-scale spatial dis-tribution and activity of specific microbial degrader communitiesFEMS Microbiol Ecol 81673ndash683 doi101111j1574-6941201201398x

Monga O Bousso M Garnier P Pot V (2008) 3-D geometrical structuresand biological activity application to soil organic matter microbialdecomposition in pore space Ecol Model 216291ndash302 doi101016jecolmodel200804015


Monga O Garnier P Pot V Coucheney E Nunan N Otten W Chenu C(2014) Simulating microbial degradation of organic matter in a sim-ple porous system using the 3-D diffusion-based model MOSAICBiogeosciences 112201ndash2209 doi105194bg-11-2201-2014

Moni C Derrien D Hatton PJ Zeller B Kleber M (2012) Density frac-tions versus size separates does physical fractionation isolate func-tional soil compartments Biogeosciences 95181ndash5197 doi105194bg-9-5181-2012

Moorhead DL Sinsabaugh RL (2006) A theoretical model of litter decayand microbial interaction Ecol Monogr 76151ndash174 doi1018900012-9615(2006)0765B0151ATMOLD5D20CO2

Moorhead D Lashermes G Recous S Bertrand I (2014) Interactingmicrobe and litter quality controls on litter decomposition a model-ing analysis PLoS One doi101371journalpone0108769

Mooshammer M Wanek W Zechmeister-Boltenstern S Richter A(2014) Stoichiometric imbalances between terrestrial decomposercommunities and their resources mechanisms and implications ofmicrobial adaptations to their resources Front Microbiol doi103389fmicb201400022

Mora P Miambi E Jimenez JJ Decaens T Rouland C (2005) Functionalcomplement of biogenic structures produced by earthworms ter-mites and ants in the neotropical savannas Soil Biol Biochem 371043ndash1048 doi101016jsoilbio200410019

Morrieumln E Hannula SE Snoek LB Helmsing NR Zweers H deHollander M Soto RL Bouffaud ML Bueacutee M Dimmers WDuyts H Geisen S Girlanda M Griffiths RI Joslashrgensen HBJensen J Plassart P Redecker D Schmelz RM Schmidt OThomson BC Tisserant E Uroz S Winding A Bailey MJBonkowski M Faber JH Martin F Lemanceau P de Boer W vanVeen JA van der Putten WH (2017) Soil networks become moreconnected and take up more carbon as nature restoration progressesNat Commun 814349 doi101038ncomms14349

Nagy LG Riley R Bergmann PJ Krizsaacuten K Martin FM Grigoriev IVCullen D Hibbett DS (2016) Genetic bases of fungal white rot wooddecay predicted by phylogenomic analysis of correlated gene-phenotype evolution Mol Biol Evol doi101093molbevmsw238

Nannipieri P Ascher MT Ceccherini MT Landi L Pietramellara GRenella G (2003) Microbial diversity and soil functions Eur J SoilSci 54655ndash670 doi101111ejss4_12398

Noirot-Cosson PE Vaudour E Gilliot J-M Gabrielle B Houot S (2016)Modelling the long-term effect of urban waste compost applicationson carbon and nitrogen dynamics in temperate cropland Soil BiolBiochem 94138ndash153 doi101016jsoilbio201511014

OrsquoRourke SM Angers DA Holden NM McBratney AB (2015) Soilorganic carbon across scales Glob Chang Biol 213561ndash3574 doi101111gcb12959

Osono T Takeda H (2006) Fungal decomposition of abies needle andBetula leaf litter Mycologia 98172ndash179 doi103852mycologia982172

Pajor R Falconer R Hapca S OttenW (2010)Modelling and quantifyingthe effect of heterogeneity in soil physical conditions on fungalgrowth Biogeosciences 73731ndash3740 doi105194bg-7-3731-2010

Panettieri M Rumpel C Dignac M-F Chabbi A (2017) Does grasslandintroduction into cropping cycles affect carbon dynamics throughchanges of allocation of soil organic matter within aggregate frac-tions Sci Total Environ 576251ndash263 doi101016jscitotenv201610073

Paradelo R Virto I Chenu C (2015) Net effect of liming on soil organiccarbon stocks a review Agric Ecosyst Environ 20298ndash107 doi101016jagee201501005

Paustian K Lehmann J Ogle S Reay D Robertson GP Smith P (2016)Climate-smart soils Nature 53249ndash57 doi101038nature17174

Pellerin S Bamiegravere L Angers D Beacuteline F Benoicirct M Butault JP ChenuC Colnenne-David C De Cara S Delame N Doreau M Dupraz PFaverdin P Garcia-Launay F Hassouna M Heacutenault C Jeuffroy

MH Klumpp K Metay A Moran D Recous S Samson E SaviniI Pardon L (2013) Quelle contribution de lrsquoagriculture franccedilaise agrave lareacuteduction des eacutemissions de gaz agrave effet de serre Potentieldrsquoatteacutenuation et coucirct de dix actions techniques Synthegravese du rapportdrsquoeacutetude INRA (France) 92 p

Peltre C Christensen BT Dragon S Icard C Kaumltterer T Houot S (2012)RothC simulation of carbon accumulation in soil after repeated ap-plication of widely different organic amendments Soil BiolBiochem 5249ndash60 doi101016jsoilbio201203023

Perveen N Barot S Alvarez G Klumpp K Martin R Rapaport AHerfurth D Louault F Fontaine S (2014) Priming effect and micro-bial diversity in ecosystem functioning and response to globalchange a modeling approach using the SYMPHONY modelGlob Chang Biol 201174ndash1190 doi101111gcb12493

Pinheiro M Garnier P Beguet J Martin-Laurent F Vieubleacute-Gonod L(2015) The millimetre-scale distribution of 24-D and its degradersdrives the fate of 24-D at the soil core scale Soil Biol Biochem 8890ndash100 doi101016jsoilbio201505008

Plante AF McGill WB (2002) Soil aggregate dynamics and the retentionof organic matter in laboratory-incubated soil with differing simu-lated tillage frequencies Soil Tillage Res 6679ndash92 doi101016S0167-1987(02)00015-6

Plante AF Fernaacutendez JM Haddix ML Steinweg JM Conant RT (2011)Biological chemical and thermal indices of soil organic matter sta-bility in four grassland soils Soil Biol Biochem 431051ndash1058 doi101016jsoilbio201101024

Poirier V Angers DA Whalen JK (2014) Formation of millimetric-scaleaggregates and associated retention of 13C-15N-labelled residues aregreater in subsoil than topsoil Soil Biol Biochem 7545ndash53 doi101016jsoilbio201403020

Poorter H Jagodzinski AM Ruiz-Peinado R Kuyah S LuoY Oleksyn JUsoltsev VA Buckley TN Reich PB Sack L (2015) How doesbiomass distribution change with size and differ among speciesAn analysis for 1200 plant species from five continents NewPhytol 2061188ndash1190 doi101111nph13571

Poumlplau C Don A Vesterdal L Leifeld J Van Wesemael BASSchumacher J Gensior A (2011) Temporal dynamics of soil organiccarbon after land-use change in the temperate zone-carbon responsefunctions as a model approach Glob Chang Biol 172415ndash2427doi101111j1365-2486201102408x

Prieto I Stokes A Roumet C (2016) Root functional parameters predictfine root decomposability at the community level J Ecol 104725ndash733 doi1011111365-274512537

Qian Y Follett RF (2002) Assessing soil carbon sequestration in turfgrasssystems using long-term soil testing data Agron J 94930ndash935

Ransom B Kim D Kastner M Wainwright S (1998) Organic matterpreservation on continental slopes importance of mineralogy andsurface area Geochimica and Cosmochimica Acta 621329ndash1345doi101016S0016-7037(98)00050-7

Rasse DP Rumpel C Dignac M-F (2005) Is soil carbon mostly rootcarbon Mechanisms for a specific stabilisation Plant Soil 269341ndash356 doi101007s11104-004-0907-y

Raynaud X NunanN (2014) Spatial ecology of bacteria at the microscalein soil PLoS One doi101371journalpone0087217

Remusat L Hatton PJ Nico PS Zeller B Kleber M Derrien D (2012)NanoSIMS study of organic matter associated with soil aggregatesadvantages limitations and combination with STXM Environ SciTechnol 463943ndash3949 doi101021es203745k

Reacutemy JC Marin-Laflegraveche A (1974) Lrsquoanalyse de terre Reacutealisation drsquounprogramme drsquointerpreacutetation automatique Annales Agronomiques25607ndash632

Resat H Bailey V McCue LA Konopka A (2012) Modeling microbialdynamics in heterogeneous environments growth on soil carbonsources Microb Ecol 63883ndash897 doi101007s00248-011-9965-x

Rillig MC Aguilar-Trigueros CA Bergmann J Verbruggen EVeresoglou SD Lehmann A (2015) Plant root and mycorrhizal


fungal traits for understanding soil aggregation New Phytol 2051385ndash1388 doi101111nph13045

Roussel O Bourmeau EWalter C (2001) Evaluation du deacuteficit enmatiegravereorganique des sols franccedilais et des besoins potentiels enamendements organiques Etude et Gestion des Sols 865ndash81

Rovira AD Greacen EL (1957) The effect of aggregate disruption on theactivity of microorganisms in soil Aust J Agric Res 8659ndash673

Ruamps LS Nunan N Chenu C (2011) Microbial biogeography at thesoil pore scale Soil Biol Biochem 43280ndash286 doi101016jsoilbio201010010

Rumpel C Koumlgel-Knabner I (2011) Deep soil organic mattermdasha key butpoorly understood component of terrestrial C cycle Plant Soil 338143ndash158 doi101007s11104-010-0391-5

Rumpel C Chabbi A Nunan N Dignac M-F (2009) Impact of landusechange on the molecular composition of soil organic matter J AnalAppl Pyrolysis 85431ndash434 doi101016jjaap200810011

Rumpel C Baumann K Remusat L Dignac M-F Barreacute P Deldicque DGlasser G Lieberwirth I Chabbi A (2015) Nanoscale evidence ofcontrasted processes for root-derived organic matter stabilization bymineral interactions depending on soil depth Soil Biol Biochem 8582ndash88 doi101016jsoilbio201502017

Saenger A Ceacutecillon L Sebag D Brun JJ (2013) Soil organic carbonquantity chemistry and thermal stability in a mountainous land-scape a rock-Eval pyrolysis survey Org Geochem 54101ndash114doi101016jorggeochem201210008

Saenger A Ceacutecillon L Poulenard P Bureau F De Danieli S GonzalezJM Brun JJ (2015) Surveying the carbon pools of mountain soils acomparison of physical fractionation and rock-Eval pyrolysisGeoderma 241279ndash288 doi101016jgeoderma201412001

Saffih-Hdadi KMary B (2008)Modeling consequences of straw residuesexport on soil organic carbon Soil Biol Biochem 40594ndash607 doi101016jsoilbio200708022

Scheu S (2003) Effects of earthworms on plant growth patterns andperspectives Pedobiologia 47846ndash856 doi1010780031-4056-00270

Schimel J (2013) Soil carbon microbes and global carbon Nat ClimChang 3867ndash868 doi101038nclimate2015

Schimel J Schaeffer SM (2012) Microbial control over carbon cycling insoil Front Microbiol doi103389fmicb201200348

Schimel JP Weintraub MN (2003) The implications of exoenzyme activ-ity on microbial carbon and nitrogen limitation in soil a theoreticalmodel Soil Biol Biochem 35549ndash563 doi101016S0038-0717(03)00015-4

Schmidt MWI Torn MS Abiven S Dittmar T Guggenberg G JanssensIA Kleber M Koumlgel-Knabner I Lehmann J Manning MNannipieri P Rasse DP Weiner S Trumbore SE (2011)Persistence of soil organic matter as an ecosystem property Nature47849ndash56 doi101038nature10386

Shan J Brune A Ji R (2010) Selective digestion of the proteinaceouscomponent of humic substances by the geophagous earthwormsMetaphire guillelmi and Amynthas corrugatus Soil Biol Biochem421455ndash1462 doi101016jsoilbio201005008

Simpson AJ Simpson MJ Smith E Kelleher BBP (2007) Microbiallyderived inputs to soil organic matter are current estimates too lowEnviron Sci Technol 418070ndash8076 doi101021es071217x

Sistla SA Rastetter EB Schimel JP (2014) Responses of a tundra systemto warming using SCAMPS a stoichiometrically coupled acclimat-ing microbe-plant-soil model Ecol Monogr 84151ndash170 doi10189012-21191

Six J Jastrow JD (2002) Organic matter turnover Encyclopedia of SoilScience pp936ndash942

Six J Elliott ET Paustian K Doran JW (1998) Aggregation and soilorganic matter accumulation in cultivated and native grassland soilsSoil Sci Soc Am J 621367ndash1377 doi102136sssaj199803615995006200050032x

Six J Elliott ET Paustian K (2000) Soil macroaggregates turnover andmicroaggregates formation a mechanism for C sequestration underno-tillage agriculture Soil Biol Biochem 322099ndash2103 doi101016S0038-0717(00)00179-6

Six J Bossuyt H Degryze S Denef K (2004) A history of research on thelink between (micro)aggregates soil biota and soil organic matterdynamics Soil Tillage Res 797ndash31 doi101016jstill200403008

Smith SR (2009) A critical review of the bioavailability and impacts ofheavy metals in municipal solid waste composts compared to sew-age sludge Environ Int 35142ndash156 doi101016jenvint200806009

Soudzilovskaia NA Douma JC AkhmetzhanovaAA van Bodegom PMCornwell WK Moens EJ Treseder KK Tibbett M Wang YPCornelissen JHC (2015) Global patterns of plant root colonizationintensity by mycorrhizal fungi explained by climate and soil chem-istry Glob Ecol Biogeogr 24371ndash382 doi101111geb12272

Soussana JF Tallec T Blanfort V (2010) Mitigating the greenhouse gasbalance of ruminant production systems through carbon sequestra-t ion in grasslands Animal 4334ndash350 doi 101017S1751731109990784

Stamati FE Nikolaidis NP Banwart S Blum WEH (2013) A coupledcarbon aggregation and structure turnover (CAST) model for top-soils Geoderma 211-21251ndash64 doi101016jgeoderma201306014

Steiner C BlumWEH ZechW deMacedo JLV Teixeira WG LehmannJ Nehls T (2007) Long term effects of manure charcoal and mineralfertilization on crop production and fertility on a highly weatheredcentral Amazonian upland soil Plant Soil 291275ndash290 doi101007s11104-007-9193-9

Stokes A Atger C Bengough A Fourcaud T Sidle R (2009) Desirableplant root traits for protecting natural and engineered slopes againstlandslides Plant Soil 3241ndash30 doi101007s11104-009-0159-y

Strohbach MW Arnold E Haase D (2012) The carbon footprint of urbangreen spacemdasha life cycle approach Landsc Urban Plan 104220ndash229 doi101016jlandurbplan201110013

Tardy V Spor A Mathieu O Leveque J Terrat S Plassart P Regnier TBardgett RD van der Putten WH Roggero PP Seddaiu G BagellaS Lemanceau P Ranjard L Maron PA (2015) Shifts in microbialdiversity through land use intensity as drivers of carbon mineraliza-tion in soil Soil Biol Biochem 90204ndash213 doi101016jsoilbio201508010

Thaer A (1811) Principes raisonneacutes drsquoagriculture Traduit de lrsquoallemandpar EVB Crud JJ Prechoud Ed Paris 4 t pp 1811ndash1816

Theng BKG (2012) Formation and properties of clay-polymer com-plexes Book series Developments in Clay Science vol 4

Thevenot M Dignac M-F Rumpel C (2010) Fate of lignins in soil areview Soil Biol Biochem 421200ndash1211 doi101016jsoilbio201003017

Tisdall JM Oades JM (1982) Organic matter and water stable aggregatesin soil Soil Sci 23821ndash825

Todd-Brown KEO Randerson JT Post WM Hoffman FM Tarnocai CSchuur EAG Allison SD (2013) Causes of variation in soil carbonsimulations from CMIP5 Earth system models and comparison withobservations Biogeosciences 101717ndash1736 doi105194bg-10-1717-2013

Torn MS Trumbore SE Chadwick OA Vitousek PM Hendricks DM(1997) Mineral control of soil organic carbon storage and turnoverNature 389170ndash173 doi10103838260

Torn MS Swanston CW Castanha C Trumbore SE (2009) Storage andturnover of organic matter in soil In Biophysico-chemical process-es involving natural nonliving organic matter in environmental sys-tems (Senesi N Xing B Huang PM eds) Chap 6 pp 219ndash272 JohnWiley amp Sons Inc doi1010029780470494950ch6

Torsvik V Oslashvrearings L (2002) Microbial diversity and function in soil fromgenes to ecosystems Curr Opin Microbiol 5240ndash245 doi101016S1369-5274(02)00324-7


Vidal A Quenea K Alexis M Derenne S (2016) Molecular fate of rootand shoot litter on incorporation and decomposition in earthwormcasts Org Geochem 1011ndash10 doi101016jorggeochem201608003

Vieubleacute Gonod L Chenu C Soulas G (2003) Spatial variability of 24-dichlorophenoxy acetic acid (24-D) mineralisation potential at amillimetre scale in soil Soil Biol Biochem 35373ndash382 doi101016S0038-0717(02)00287-0

Virto I Barre P Burlot A Chenu C (2012) Carbon input differences as themain factor explaining the variability in soil organic C storage in no-tilled compared to inversion tilled agrosystems Biogeochemistry10817ndash26 doi101007s10533-011-9600-4

Vogel C Mueller CW Houmlschen C Buegger F Heister K Schulz SSchloter M Koumlgel-Knabner I (2014) Submicron structures providepreferential spots for carbon and nitrogen sequestration in soils NatCommun doi101038ncomms3947

Vogel L Makowski D Garnier P Vieubleacute-Gonod L Raynaud X NunanN Coquet Y Chenu C Falconer R Pot V (2015) Modeling theeffect of soil meso- and macropores topology on the biodegradationof a soluble carbon substrate AdvWater Resour 8487ndash102 doi101016jadvwatres201505020

von Luumltzow M Koumlgel-Knabner I Ludwig B Matzner E Flessa HEkschmitt K Guggenberg G Marschner B Kalbitz K (2008)Stabilization mechanisms of organic matter in four temperate soilsDevelopment and application of a conceptual model J Plant NutrSoil Sci 171111ndash124 doi101002jpln200700047

Walker AP Zaehle S Medlyn BE De Kauwe MG Asao S Hickler TNorby RJ (2015) Predicting long-term carbon sequestration in re-sponse to CO2 enrichment how and why do current ecosystemmodels differ Glob Biogeochem Cycles 51ndash20 doi1010022014GB004995

Wei X Shao M Gale W Li L (2014) Global pattern of soil carbon lossesdue to the conversion of forests to agricultural land ScientificReports doi101038srep04062

Wen Y Li H Xiao J Wang C Shen Q Ran W He X Zhou Q Yu G(2014) Insights into complexation of dissolved organic matter andAl(III) and nanominerals formation in soils under contrasting fertil-izations using two-dimensional correlation spectroscopy and highresolution-transmission electron microscopy techniquesChemosphere 111441ndash449 doi101016jchemosphere201403078

Wertz S Degrange V Prosser JI Poly F Commeaux C Freitag TGuillaumaud N Le Roux X (2006) Maintenance of soil functioningfollowing erosion ofmicrobial diversity EnvironMicrobiol 82162ndash2169 doi101111j1462-2920200601098x

Wertz S Degrange V Prosser JI Poly F Commeaux C Guillaumaud NLe Roux X (2007) Decline of soil microbial diversity does not in-fluence the resistance and resilience of key soil microbial functionalgroups following a model disturbance Environ Microbiol 92211ndash2219 doi101111j1462-2920200701335x

West LT Hendrix PF Bruce RR (1991)Micromorphic observation of soilalteration by earthworms Agric Ecosyst Environ 34363ndash370 doi1010160167-8809(91)90121-D

Wieder W Allison SD Davidson E Georgiou K Hararuk O He YJHopkins F Luo YQ Smith MJ Sulman B Todd-Brown K WangYP Xia JY Xu XF (2015) Explicitly representing soil microbialprocesses in earth system models Glob Biogeochem Cycles 291782ndash1800 doi1010022015GB005188

Winding A Ronn R Hendriksen NB (1997) Bacteria and protozoa in soilmicrohabitats as affected by earthworms Biol Fertil Soils 24133ndash140 doi101007s003740050221

Wu Q-S Cao M-Q Zou Y-N He X-H (2014) Direct and indirect effectsof glomalin mycorrhizal hyphae and roots on aggregate stability inrhizosphere of trifoliate orange Scientific Reports doi101038srep05823

Wutzler T Reichstein M (2008) Colimitation of decomposition by sub-strate and decomposers - a comparison of model formulationsBiogeosciences 5749ndash759 doi105194bg-5-749-2008

Yue K Peng Y Peng C Yang W Peng X Wu F (2016) Stimulation ofterrestrial ecosystem carbon storage by nitrogen addition a meta-analysis Scientific Reports doi101038srep19895

Zhou X Zhou L Nie Y Fu Y Du Z Shao J Zheng Z Wang X (2016)Similar responses of soil carbon storage to drought and irrigationinterrestrial ecosystems but with contrasting mechanisms a meta-analysis Agric Ecosyst Environ 22870ndash81 doi101016jagee201604030

Zimmerman AR Chorover J Goyne KW Brantley SL (2004) Protectionof mesopore-adsorbed organic matter from enzymatic degradationEnviron Sci Technol 384542ndash4548 doi101021es035340+

Zimmermann M Leifeld J Schmidt MWI Smith P Fuhrer J (2007)Measured soil organic matter fractions can be related to pools inthe RothC model Eur J Soil Sci 58658ndash667 doi101111j1365-2389200600855x


Increasing soil carbon storage mechanisms effects of agricultural practices and proxies A review

Abstract

Introduction

Soil C storage mechanisms state of the art

Action of living biomass on soil organic C dynamics

Plants rhizosphere and soil organic C storagemdashimportance of root systems

Impact of living organisms on soil C sequestrationmdashthe macrofauna case

Diversity and physiology of microorganismsmdashdrivers of soil C dynamics

Abiotic soil organic C stabilisation mechanisms

Localisation in the physical structure of soil

C stabilisation mechanisms involving organomineral interactions

Mechanisms of OM dynamics affected by agricultural practices

Review of the main agricultural practices

Impact of agricultural practices on soil organic C storage

How could a better accounting of OM stabilisation mechanisms improve the prediction of soil organic C stock evolution

Finding indicators to improve prediction of changes in soil organic C stocks

Better integration of OM stabilisation mechanisms in large-scale C dynamics models

Modelling OM mineralisation at the micro-scale could help describing macroscopic C fluxes

Data needed to constrain various approaches to enhance prediction of soil C stock evolution patterns

Conclusion

mk3

mk4

References

(choice of plant species and density plant residue exportsamendments fertilisation tillage etc) drive soil spatiotempo-ral organic inputs and organic matter sensitivity tomineralisation Interaction between the different mechanismsand their effects on C stocks are revealed by meta-analysesand long-term field studies The third part addresses upscalingissues This is a cause for major concern since soil organic Cstabilisation mechanisms are most often studied at fine spatialscales (mmndashμm) under controlled conditions while agricul-tural practices are implemented at the plot scale We discusssome proxies and models describing specific mechanisms andtheir action in different soil and climatic contexts and showhow they should be taken into account in large scale modelsto improve change predictions in soil C stocks Finally thisliterature review highlights some future research prospectsgeared towards preserving or even increasing C stocks ourfocus being put on the mechanisms the effects of agriculturalpractices on them and C stock prediction models

Keywords Soil organic C C dynamics Stabilisationmechanisms Mineralisation Agricultural practices

Indicators Models Macrofauna Microorganisms Litter

Root inputs Organomineral associations Porosity

Contents1 Introduction2 Soil C storage mechanisms state of the art

21 Action of living biomass on soil organic Cdynamics211 Plants rhizosphere and soil organic C stor-

agemdashimportance of root systems212 Impact of living organisms on soil C seques-

trationmdashthe macrofauna case213 Diversity and physiology of microorgan-

ismsmdashdrivers of soil C dynamics22 Abiotic soil organic C stabilisation mechanisms

221 Localisation in the physical structure of soil222 C stabilisation mechanisms involving

organomineral interactions3 Mechanisms of OM dynamics affected by agricultural

practices31 Review of the main agricultural practices32 Impact of agricultural practises on soil organic C

storage4 How could a better accounting of OM stabilisation

mechanisms improve the prediction of soil organic Cstock evolution41 Finding indicators to improve prediction of chang-

es in soil organic C stocks42 Better integration of OM stabilisation mechanisms

in large-scale C dynamics models

43 Modelling OM mineralisation at the micro-scalecould help in describing macroscopic C fluxes

44 Data needed to constrain various approaches toenhance prediction of soil C stock evolutionpatterns

5 ConclusionAcknowledgmentsReferences

1 Introduction

The increasing atmospheric concentration of greenhouse gas-es (GHG) particularly those containing carbon (CO2 CH4) isa consequence of human activities and is associated with cli-mate change Anthropogenic carbon emissions are partiallybalanced by carbon (C) sinks in oceans vegetation and soil(Le Queacutereacute et al 2015) Soils contain approximately threetimes more C than the atmosphere (2400 vs 800 GtC)(Jobbaacutegy and Jackson 2000) in the form of organic C bornein organic matter (OM) On decadal time scales soils canserve as a C sink or source depending on their properties onthe climate land use etc (Eglin et al 2010)

Global models linking the atmospheric CO2 concentrationto temperature show that a 35ndash4 Gtyear decrease in atmo-spheric C would limit the temperature increase to +152 degC by2050 (Meinshausen et al 2009 Minasny et al 2017) ie thethreshold beyond which climate change would have a signif-icant impact (IPCC 2013) This annual decrease in the atmo-spheric CO2 concentration could be fulfilled by annually in-creasing C stocks in the top 30 cm soil horizon by 04 (4 per1000) (Balesdent and Arrouays 1999 Paustian et al 2016)

In this context the 4 per 1000mdashCarbon Sequestration inSoils for Food Security and the Climate initiative launched byFrance in 2015 ahead of COP21 in Paris (http4p1000org)aims to bring together governmental and non-governmentalstakeholders devoted to improving soil C stock managementPositive effects on food security and climate change are ex-pected through the collective objective of increasing C stockson a global scale in agricultural areas (croplands grasslandsforests) on which human action can be oriented towards Cstorage (Paustian et al 2016) Indeed increasing soil OMstocks is also beneficial for soil fertility since OMmineralisation might be a source of nutriments for plantsBut this requires implementing agricultural practices adaptedto local conditions that will increase soil C inputs with out-puts remaining stable or decreasing thus maximising soil Cstorage

Soil OM is not homogeneous and some OM is quicklymineralised after entering the soil while some persists for verylong periods (Schmidt et al 2011) Conceptual pools weresometimes associated to functional pools tentatively separatedfrom soils according to chemical or physical fractionation

14 of 27 Agron Sustain Dev (2017) 37 14


























































































Tab

le1

Specificities

ofdifferenttypes

ofland


France

(croplandsurban


system

s)interm

sof

Ccontent

soilandclim





piledon

thebasisof

interviews

with



iaandagricultu


tesFrenchNationalF

orestryOfficeetc)]

Forests

Grasslands

Agroforestry

Croplands

Vineyards

Urban

gardens

Average

stocks

(tCha

minus1of

0ndash30

cmM

artin

etal2011)

8080

Not

mentio

ned

5035

Variable

Ccontents(g

kgminus1

soil

Joim

eletal2016)

Average

[minndashm

ax]

3383[148ndash159]

2982[449ndash243]

1692[257ndash5820]

1121[341ndash393]

2815[979ndash5930]

Soilandclim

aticconditions

Poor

acidicsoils

sometim

esflooded

Eventually

soils

onslopes

diversity

ofclim

ates

Diverse

Markedhuman

actio

nOften

basicsoilandwarm

clim

ates

Strong

artificialisation

Plantspecies

Highbiodiversity

includinglegumes


tree

speciesandcrops

Low

biodiversity

Potentially

grassbandsin

theranks

Aestheticcriterion

Residue

managem

ent

Depends

onexportof

harvestresidues

(brancheslt7cm

indiam

eter)

Depends

ongrazingand

mow

ingintensity

Exporto

fwoodbiom

ass

(exceptleaves)and

cropsresidues

are

sometim

esreturned

tothesoil

Exporto

fharvestresidues

aresometim

esreturned

tothesoil


eventually

returned

tothesoil

Exporto

ffallenleaves

and

mow

inglawns

Exogenous

OM

inputs

Manure

Eventually

Contributionof

exogenous

OM

from

urbanareaor

manure

Noexogenousinput

Large

inputsof

exogenous

OM

from

urbanorigin

Practices

modifying

soil

physicalstructure

Stum

pandeventualtillage

whenplantin


engine

trafficatthinning

(every

10years

approxim

ately)

Often

aggregated

structure

sometim

estillage

Tillageor

no-tillagein

tree

rows

Tillageor

no-tillage


decompaction

Packedw

aterproof

volumes

constrainedby

thepipe

network

Otherpractices

Fertilisatio

nrarely

practicedamendm

entif

treesdecline

Fertilisatio

nirrigation

associations

with

legumes


ninorganicam

endm

entpesticides

Temporalspecificity

Forestrevolutio

nabout

60ndash200

years

Sometim

esleys

Cdynamicsmustb

eratio

nalised

accordingto

forestrevolutio

nduratio

n

Annualcropssom

etim

esinterm

ediatecrops

Rapidly

changing

physical

andchem

icalproperties

Spatialh

eterogeneity

Related

toroot

distribution


Especially

relatedto

grazingintensity

Lines

oftreeson

grass

bands

Eventually

hedges

and

grassbands


grassinter-rows

Veryheterogeneous

alignm

ento

ftrees

fragmented

discontin

uous





























































5 Conclusion









References






































































































































































































































































































Abstract

Introduction

















Conclusion

mk3

mk4

References













Agron Sustain Dev (2017) 37 14 of 27 14













































































Tab

le1

Specificities

ofdifferenttypes

ofland


France

(croplandsurban


system

s)interm

sof

Ccontent

soilandclim





piledon

thebasisof

interviews

with



iaandagricultu


tesFrenchNationalF

orestryOfficeetc)]

Forests

Grasslands

Agroforestry

Croplands

Vineyards

Urban

gardens

Average

stocks

(tCha

minus1of

0ndash30

cmM

artin

etal2011)

8080

Not

mentio

ned

5035

Variable

Ccontents(g

kgminus1

soil

Joim

eletal2016)

Average

[minndashm

ax]

3383[148ndash159]

2982[449ndash243]

1692[257ndash5820]

1121[341ndash393]

2815[979ndash5930]

Soilandclim

aticconditions

Poor

acidicsoils

sometim

esflooded

Eventually

soils

onslopes

diversity

ofclim

ates

Diverse

Markedhuman

actio

nOften

basicsoilandwarm

clim

ates

Strong

artificialisation

Plantspecies

Highbiodiversity

includinglegumes


tree

speciesandcrops

Low

biodiversity

Potentially

grassbandsin

theranks

Aestheticcriterion

Residue

managem

ent

Depends

onexportof

harvestresidues

(brancheslt7cm

indiam

eter)

Depends

ongrazingand

mow

ingintensity

Exporto

fwoodbiom

ass

(exceptleaves)and

cropsresidues

are

sometim

esreturned

tothesoil

Exporto

fharvestresidues

aresometim

esreturned

tothesoil


eventually

returned

tothesoil

Exporto

ffallenleaves

and

mow

inglawns

Exogenous

OM

inputs

Manure

Eventually

Contributionof

exogenous

OM

from

urbanareaor

manure

Noexogenousinput

Large

inputsof

exogenous

OM

from

urbanorigin

Practices

modifying

soil

physicalstructure

Stum

pandeventualtillage

whenplantin


engine

trafficatthinning

(every

10years

approxim

ately)

Often

aggregated

structure

sometim

estillage

Tillageor

no-tillagein

tree

rows

Tillageor

no-tillage


decompaction

Packedw

aterproof

volumes

constrainedby

thepipe

network

Otherpractices

Fertilisatio

nrarely

practicedamendm

entif

treesdecline

Fertilisatio

nirrigation

associations

with

legumes


ninorganicam

endm

entpesticides

Temporalspecificity

Forestrevolutio

nabout

60ndash200

years

Sometim

esleys

Cdynamicsmustb

eratio

nalised

accordingto

forestrevolutio

nduratio

n

Annualcropssom

etim

esinterm

ediatecrops

Rapidly

changing

physical

andchem

icalproperties

Spatialh

eterogeneity

Related

toroot

distribution


Especially

relatedto

grazingintensity

Lines

oftreeson

grass

bands

Eventually

hedges

and

grassbands


grassinter-rows

Veryheterogeneous

alignm

ento

ftrees

fragmented

discontin

uous





























































5 Conclusion









References






































































































































































































































































































Abstract

Introduction

















Conclusion

mk3

mk4

References













































































Tab

le1

Specificities

ofdifferenttypes

ofland


France

(croplandsurban


system

s)interm

sof

Ccontent

soilandclim





piledon

thebasisof

interviews

with



iaandagricultu


tesFrenchNationalF

orestryOfficeetc)]

Forests

Grasslands

Agroforestry

Croplands

Vineyards

Urban

gardens

Average

stocks

(tCha

minus1of

0ndash30

cmM

artin

etal2011)

8080

Not

mentio

ned

5035

Variable

Ccontents(g

kgminus1

soil

Joim

eletal2016)

Average

[minndashm

ax]

3383[148ndash159]

2982[449ndash243]

1692[257ndash5820]

1121[341ndash393]

2815[979ndash5930]

Soilandclim

aticconditions

Poor

acidicsoils

sometim

esflooded

Eventually

soils

onslopes

diversity

ofclim

ates

Diverse

Markedhuman

actio

nOften

basicsoilandwarm

clim

ates

Strong

artificialisation

Plantspecies

Highbiodiversity

includinglegumes


tree

speciesandcrops

Low

biodiversity

Potentially

grassbandsin

theranks

Aestheticcriterion

Residue

managem

ent

Depends

onexportof

harvestresidues

(brancheslt7cm

indiam

eter)

Depends

ongrazingand

mow

ingintensity

Exporto

fwoodbiom

ass

(exceptleaves)and

cropsresidues

are

sometim

esreturned

tothesoil

Exporto

fharvestresidues

aresometim

esreturned

tothesoil


eventually

returned

tothesoil

Exporto

ffallenleaves

and

mow

inglawns

Exogenous

OM

inputs

Manure

Eventually

Contributionof

exogenous

OM

from

urbanareaor

manure

Noexogenousinput

Large

inputsof

exogenous

OM

from

urbanorigin

Practices

modifying

soil

physicalstructure

Stum

pandeventualtillage

whenplantin


engine

trafficatthinning

(every

10years

approxim

ately)

Often

aggregated

structure

sometim

estillage

Tillageor

no-tillagein

tree

rows

Tillageor

no-tillage


decompaction

Packedw

aterproof

volumes

constrainedby

thepipe

network

Otherpractices

Fertilisatio

nrarely

practicedamendm

entif

treesdecline

Fertilisatio

nirrigation

associations

with

legumes


ninorganicam

endm

entpesticides

Temporalspecificity

Forestrevolutio

nabout

60ndash200

years

Sometim

esleys

Cdynamicsmustb

eratio

nalised

accordingto

forestrevolutio

nduratio

n

Annualcropssom

etim

esinterm

ediatecrops

Rapidly

changing

physical

andchem

icalproperties

Spatialh

eterogeneity

Related

toroot

distribution


Especially

relatedto

grazingintensity

Lines

oftreeson

grass

bands

Eventually

hedges

and

grassbands


grassinter-rows

Veryheterogeneous

alignm

ento

ftrees

fragmented

discontin

uous





























































5 Conclusion









References






































































































































































































































































































Abstract

Introduction

















Conclusion

mk3

mk4

References




























































5 Conclusion









References






































































































































































































































































































Abstract

Introduction

















Conclusion

mk3

mk4

References




References






































































































































































































































































































Abstract

Introduction

















Conclusion

mk3

mk4

References
















































































































































































































































































Abstract

Introduction

















Conclusion

mk3

mk4

References

increasing soil carbon storage: mechanisms, effects of ...for these mechanisms in global models and...

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