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Europ.J.Agronomy34 (2011) 197–210 ContentslistsavailableatScienceDirect European Journal of Agronomy journal homepage: www.elsevier.com/locate/eja Review Facing up to the paradigm of ecological intensification in agronomy: Revisiting methods, concepts and knowledge ThierryDoréa,∗,DavidMakowskib,EricMalézieuxc,NathalieMunier-Jolaind, MarcTchamitchiane,PabloTittonellf aAgroParisTech,INRA,UMR211,F-78850Thiverval-Grignon,France bINRA,AgroParisTech,UMR211,F-78850Thiverval-Grignon,France cCIRAD,URHortSys,BoulevarddelaLironde,TAB-103/PS4,34398MontpellierCedex,France dINRA,UMR102GénétiqueetEcophysiologiedesLégumineuses,17rueSully,BP86510,F-21065DijonCedex,France eINRA,UnitéEcodéveloppement,CentrePACA,F-84914AvignonCedex9,France fCIRAD-Persyst,SystèmesdeCultureAnnuels,TAB-102/02AvenueAgropolis,34898MontpellierCedex5,France a r t i c l e i n f o a b s t r a c t Articlehistory: Agricultureisfacinguptoanincreasingnumberofchallenges,includingtheneedtoensurevarious Received18October2010 ecosystemservicesandtoresolveapparentconflictsbetweenthem.Oneofthewaysforwardforagricul- Receivedinrevisedform5February2011 turecurrentlybeingdebatedisasetofprinciplesgroupedtogetherundertheumbrellaterm“ecological Accepted16February2011 intensification”.Inpublishedstudies,ecologicalintensificationhasgenerallybeenconsideredtobebased essentiallyontheuseofbiologicalregulationtomanageagroecosystems,atfield,farmandlandscape Keywords: scales.Weproposeherefiveadditionalavenuesthatagronomicresearchcouldfollowtostrengthen Agroecology theecologicalintensificationofcurrentfarmingsystems.Webeginbyassumingthatprogressinplant Agroecosystem sciencesoverthelasttwodecadesprovidesnewinsightofpotentialusetoagronomists.Potentiallyuse- Plantscience Farmers’knowledge fulnewdevelopmentsinplantscienceincludeadvancesinthefieldsofenergyconversionbyplants, Meta-analysis nitrogenuseefficiencyanddefencemechanismsagainstpests.Wethensuggestthatnaturalecosys- Comparativeanalysis temsmayalsoprovidesourcesofinspirationforcroppingsystemdesign,intermsoftheirstructureand functionontheonehand,andfarmers’knowledgeontheother.Naturalecosystemsdisplayanum- berofinterestingpropertiesthatcouldbeincorporatedintoagroecosystems.Wediscussthevalueand limitationsofattemptingto‘mimic’theirstructureandfunction,whileconsideringthedifferencesin objectivesandconstraintsbetweenthesetwotypesofsystem.Farmersdevelopextensiveknowledge ofthesystemstheymanage.Wediscusswaysinwhichthisknowledgecouldbecombinedwith,orfed intoscientificknowledgeandinnovation,andtheextenttowhichthisislikelytobepossible.Thetwo remainingavenuesconcernmethods.Wesuggestthatagronomistsmakemoreuseofmeta-analysisand comparativesystemstudies,thesetwotypesofmethodsbeingcommonlyusedinotherdisciplinesbut barelyusedinagronomy.Meta-analysiswouldmakeitpossibletoquantifyvariationsofcroppingsystem performancesininteractionwithsoilandclimateconditionsmoreaccuratelyacrossenvironmentsand socio-economiccontexts.Comparativeanalysiswouldhelptoidentifythestructuralcharacteristicsof croppingandfarmingsystemsunderlyingpropertiesofinterest.Suchanalysiscanbeperformedwith setsofperformanceindicatorsandmethodsborrowedfromecologyforanalysesofthestructureand organisationofthesesystems.Thesefiveapproachesshouldmakeitpossibletodeepenourknowledge ofagroecosystemsforaction. © 2011 Elsevier B.V. All rights reserved. Contents 1. Introduction.......................................................................................................................................... 198 2. Diversifyingsourcesofknowledgetoguideecologicalintensification............................................................................. 199 2.1. Mobilizingadvancesinplantsciences....................................................................................................... 199 ∗ Correspondingauthor.Tel.:+33130815245;fax:+33130815425. E-mailaddress:[email protected](T.Doré). 1161-0301/$–seefrontmatter© 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.eja.2011.02.006 198 T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 2.1.1. Anewlookatthebasics............................................................................................................ 199 2.1.2. Thecultivatedplantanditsbiologicalenvironment............................................................................... 199 2.1.3. Waystoimprovetheuseofplantsciencesforecologicalintensification......................................................... 200 2.2. Learninglessonsfromthefunctioningofnaturalecosystems............................................................................... 201 2.2.1. Whatdoes“Mimickingnaturalecosystems”mean?............................................................................... 201 2.2.2. Agroecosystemsascomplexsocio-ecologicalsystems............................................................................ 202 2.3. Farmers’knowledgeandlayexpertisevalorisationandintegrationintoscientificknowledge............................................ 203 2.3.1. Valueoffarmers’knowledgeforagronomy........................................................................................ 203 2.3.2. Qualificationandvalidationoflayexpertiseandknowledgeexpression......................................................... 204 3. Methodsforsynthesizinginformation.............................................................................................................. 204 3.1. Meta-analysisandagronomy................................................................................................................ 205 3.2. Comparativeanalysisofagroecosystems.................................................................................................... 205 3.2.1. Comparativeanalysisbasedonmultipleindicators............................................................................... 206 3.2.2. Analysingthestructureandfunctioningofagroecosystems...................................................................... 206 4. Overalldiscussionandconclusion................................................................................................................... 207 Acknowledgement................................................................................................................................... 208 References........................................................................................................................................... 208 1. Introduction age.Thisapproachfocusesprincipallyonthefateoffertilisersand their use by crops. Witt et al. (2006) applied a similar approach Newagriculturalsystemsarerequiredtoallowagricultureto to oil palm plantations. According to Chevassus au Louis and satisfytheincreasinglydiverseexpectationsofsociety.Fordecades, Griffon (2008) and a number of other authors (Affholder et al., agronomyhasproducedknowledgeanddesignedagroecosystems 2008; Mikolasek et al., 2009; Hubert et al., 2010; Bommel et al., formaximisingtheproductionofprimaryfoodandfibre,eitherfor 2010), ecological intensification is a pathway towards the pro- directconsumptionorforindustrialuse.Agriculturalproduction duction of more agricultural product, the production of “new” issues have recently been expanded to include other ecosystem things (ecosystem services) and different means of production services(Zhangetal.,2007).Likeothernaturalandsemi-artificial (environmentally friendly). According to Chevassus au Louis and ecosystems,agroecosystemscanprovideservices,suchascarbon Griffon (2008), ecological intensification is based on “intensifi- sequestration,pollination,orwaterfiltration.Thecapacityofagri- cation in the use of the natural functionalities that ecosystems culturetoprovidesuchservicesis,ofcourse,notalwaysguaranteed, offer”. Though relatively vague, this definition remains a possi- and there are many examples of adverse effects of agricultural ble starting point for the consideration of alternative pathways practicesontheenvironment,leadingtoecologicaldisservicesof of development for agriculture. This definition is much broader agriculture(Matsonetal.,1997;Swintonetal.,2007).Disservices thanthatofCassman(Cassman,1999),andprovidesaninteresting mayincludedecreasesinwaterandairqualityoracontributionto havenforscientistspromotingtheuseofbiologicalregulationin biodiversityloss.Asagroecosystemsareecosystemscontrolledby agroecosystems. humans,adoptingthecorrectapproachtoawiderangeofproduc- Manyarticleshavebeenpublishedonbiologicalregulationin tionissuesrequiresanunderstandingofthewayinwhichnatural agroecosystems,mostlyundertheheading“agroecology”,andnew andhuman-drivenorforcedprocessesinteractwithintheecosys- papers are continuing to appear. Research on this topic remains tem. highlynecessary,andisprobablyachallengeformostagronomists Agronomistshavearguedthatthemissionsofmulti-objective familiarwithindividualphysicaland/orchemicalaspectsofagroe- agriculture could best be achieved by making better use of cosystems. However, ecological intensification calls for both a biologicalregulationmechanismsatdifferentlevels:cropmanage- widerdiversificationofsourcesofknowledgeandthedevelopment ment,croppingsystemdesign,landscapelayoutandmanagement of new data analysis methods. Agronomists have, until recently, (Matsonetal.,1997;Médièneetal.,2011).Thisassumesthatbiolog- reliedessentiallyontheirownscientificoutput.Prototyping(e.g., icalmechanismsareabletoreplacechemicalorphysicalinputs,or Vereijken,1997;Lanc¸onetal.,2007;Debaekeetal.,2009)andthe tointeractfavourablywiththem,playingthesameagronomicrole model-based design of agricultural systems (e.g., Rossing et al., withoutexternalcosts,includingenvironmentalcostsinparticu- 1997; Bergez et al., 2010) are fed by results processed through lar.Theuseofbiologicalregulationinagroecosystemstoachieve simulationstudies,statisticalhypothesistestingandgroupanaly- bothahighleveloffoodproductionandtoprovideecosystemser- sis,fromresearchgroupsworkingmostlyatexperimentalstations vices, apparently opposite aims, has been placed at the core of (Fig. 1). We argue here that agronomists would be placed in a what is increasingly called “ecological intensification”. The Food betterpositiontotackleecologicalintensificationiftheydiversi- and Agriculture Organisation (FAO, 2009) recently defined “eco- fiedtheirsourcesofknowledgeandthemethodsusedtocompile, logicalintensification”(or“sustainableintensification”)withinthe organiseandanalysesuchknowledge.Thediversificationofknowl- frameworkoforganicagricultureas“Maximizationofprimarypro- edge sources may include (i) making use of recent advances in duction per unit area without compromising the ability of the plantsciences,(ii)learninglessonsfromthefunctioningofnatural systemtosustainitsproductivecapacity”.Theexpression“ecolog- ecosystems, guiding the design and management of acroecosys- icalintensification”wasalreadyinusemorethantwodecadesago tems and (iii) embracing local farmers’ knowledge. Methods for (Egger,1986),whenitreferredtoakindofecologicalengineering assessingthesesourcesofknowledgearenecessarilydiverse,and inagropastoralsystemsinAfrica,replacingsomeperennialspecies couldbeextendedtodataminingandthemeta-analysisoflarge toimprovesoilorganicmattercontent. datasets containing heterogeneous information and comparative AmorerecentuseoftheexpressionbyCassman(1999)focused analyses of agroecosystems at different scales. We present here on cereal production and highlighted the need for progress in theargumentsforfurtheragronomicresearchinthesetworelated plant and soil science to achieve a continuous increase in cereal domains:sourcesofknowledgeforagronomistsanddataprocess- yields (intensification) without environmental (ecological) dam- ingmethods. T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 199 Data Analysis & Sources of generation synthesis knowledge Existing Modelling Simulation studies agronomic knowledge On station Statistical s Plant sciences experiments hypothesis testing on em e st (genetics, g sy ecophysiology) Oexnp-efarrimments Glorcoaul pv aalunaatlyiosnis & nowled ms for sign Natural ve k ste de ecosystem Surveys, Meta-analysis & data- vati osy functioning participatory mining nno oec research I gr a Farmers’ Comparative studies of knowledge agroecosystems Fig.1. Summaryofnewavenuesofagronomicresearchforecologicalintensification. 2. Diversifyingsourcesofknowledgetoguideecological by agronomists. Nevertheless, results recently obtained in plant intensification sciencessuggestthatthissimpleparadigmcouldbeimproved,as shownforexamplebyZhuetal.(2010),whoanalysedthewaysin 2.1. Mobilizingadvancesinplantsciences whichimprovementsinphotosynthesisefficiencycouldcontribute totherequiredincreaseinyields. Therehasbeentremendousprogressinplantsciencesinrecent Nutrient use efficiency is also clearly a key point in ecologi- decades,withdetailedelucidationofthegeneticandenvironmen- calintensification.Oneofthemostimportantissuesisdecreasing taldeterminismofplantdevelopment,growthandreproduction. the use of nitrogen fertilisers, to decrease greenhouse gas emis- This progress was made possible, in particular, by increases in sions,toreducethedependenceofagricultureonfossilfuelsand ourabilitytodissectcellularandmolecularprocesses,supported topreventhealthandenvironmentaldisorders,withoutdecreasing byexponentialprogressinlaboratorytechniquesandthecapac- productivity(Gallowayetal.,2008;Spiertz,2010).Plantscientists itytoanalysemassesofgenomicdata(e.g.,TardieuandTuberosa, haveinvestigatedindetailtheexchangesofnitrogenbetweenroots 2010).Thisknowledgeaboutthehighlycomplexlifeofplantshas and their environment (Jackson et al., 2008). Glass (2003) sum- often been developed in a simplified environment, far removed marisedthefactorsdecreasingnitrogenabsorptionefficiency,on from the reality of farmers’ fields. This has led to a widening of the basis of molecular knowledge and empirical data. Decreases the gap between the research objectives of plant scientists and innitrogentransporteractivityandratesofnitrateabsorptionfol- agronomists.Wehighlightbriefly,withafewexamples,waysin lowincreasesinsoilammoniumconcentration,lowtemperature whichagronomistscouldmakeuseofadvancesinplantsciences andincidentradiation.Thesemechanismsmayaccount,atleastin todesignecologicallyintensivecroppingsystems. part,forthehighvariabilityoffertiliserefficiencyobservedinfield experiments.Theyalsoprovideuswithopportunitiestoimprove nitrogenmanagementinthesoil.Moregenerally,thewaysinwhich 2.1.1. Anewlookatthebasics plantsmakeuseofadaptationmechanismstodealwithmineral Agronomistsinvolvedinthedesignandevaluationofcropping depletionhavebeenextensivelystudiedonaphysiologicalbasis systemsoftenmakeuseofasimplifiedcropdescription(Monteith, (GrossmanandTakahashi,2001).Agronomistscouldmakeuseof 1977),despitetheavailabilityofmoremechanisticmodelssimu- this work to define the limits within which plant environments latingcanopyphotosynthesis(Spittersetal.,1986;Spitters,1986; mustbecontainedtoavoidunfavourableplantreactions. dePury and Farquhar, 1997). In this simplified description, the canopy,representedasa“bigleaf”,interceptsphotosynthetically activeradiationandconvertsittobiomass.Branchingisgenerally 2.1.2. Thecultivatedplantanditsbiologicalenvironment consideredtobetheoutcomeofinterplantcompetition.Mineral Sincethemiddleofthelastcentury,thegradual“artificialisa- nutritionisrepresentedasasimplefluxfromsoiltoplantroots, tion”ofagriculturehasledtoagronomistspayinglessattentionto depending on soil mineral and water contents. Such simplified thebiologicalcomponentsoffields.Agroecologyhasemergedasa representations have proved sufficient and highly successful for reactionagainstthisexcessivesimplificationofthesystem,placing cropping system design. Moreover, the more sophisticated rep- thebiologicalcomponentbackattheheartofthesystem(Altieri, resentations of the basic processes of plant life implemented in 1989), and resulting in the development of an “agroecosystem” more complex models do not necessarily improve the ability of view(Conway,1987).Nevertheless,commonagronomicpractices cropmodelstopredictbehaviourinarangeoffluctuatingcondi- stilllargelyignorebiologicalinteractionsincultivatedfields,and tions.Suchrepresentationshavethereforebeenusedonlyrarely agroecologists often emphasise the need for an empirical and 200 T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 holisticapproachtoagroecosystems.Newfindingsinplantsciences ofplantmicro-organismsinplant×plantinteractions(Sanonetal., concerningtherelationshipsbetweentheplantanditssurrounding 2009;Lietal.,2008)andthecompetitionofmicrobialcommunities bioticenvironmenthaverecentlyemergedandareofgreatinterest. promotingbothplantgrowthandhealth(Lemanceauetal.,2009) Studiesofinteractionsbetweenrootsandsoilmicro-andmacro- illustratethebenefitsthatagronomistsmayobtainfromadvances organismshaverevealedtheexistenceofprocessesofparamount inresearchonplant–micro-organisminteractionsforrhizosphere importanceforagronomists.Someoftheseinteractionsarevery engineeringandmanagement(Ryanetal.,2009).Beyondtheques- familiar to agronomists, including nitrogen fixation by symbio- tion of production, Jackson et al. (2008), focusing on nitrogen, sis between Rhizobium sp. and leguminous or non-leguminous derived from current knowledge on root/micro-organism inter- (Mehboob et al., 2009) plants. Other associations, such as that actions the trends in ecosystem services supplied by cropping between other endophytic di-azotrophic bacteria and grasses or systems in different agricultural situations. Thanks to the deep cereals,alsoexistandmaybeofinterest,aspointedoutbyReis insightnowavailable,thecontributionofagronomistsatsystem etal.(2000).Plantsmaybeinjuredbysoilpathogenicorganisms, level can be built on mechanistic rather than empirical knowl- but they may also benefit from organisms present in the rhizo- edge,asdemonstratedbycertainexamplesinprecisionagriculture sphere, through improvements in growth and mineral nutrition, (Welbaumetal.,2004). an increase in resistance to unfavourable abiotic conditions, and Interactions between aerial parts of the plant and the sur- protectionagainstoranincreaseinresistancetopathogens(Sturz rounding biotic environment have also been described in detail andNowak,2000;KiersandDenison,2008). in recent years. The metabolic pathways by which plants react Whatever the types of organisms considered, the species bothlocallyandsystemicallytoinfectionorwoundingareincreas- or plant genotype drives selection of the bacterial community ingly well known (de Bruxelles and Roberts, 2001; Kessler and and determines the benefits of plant–rhizosphere mutualism. Baldwin, 2002). Some result in the production of volatile sub- Improvements in the genomic characterisation of rhizobacterial stances,whichplayaroleinherbivorerepulsionorplant-to-plant communities have made it possible to demonstrate that plant signalling. These findings are promising for genetic engineer- genotype influences bacterial assemblages by modifying exuda- ing approaches, provided that the genetic basis of the metabolic tionpatterns(Micallefetal.,2009).Anunderstandingoftheplant pathwayscanbeidentified(DudarevaandPichersky,2008).How- genomewouldmakeitpossibletodeterminethegeneticbasisof ever, cropping system may also play a role, as the expression themechanismandtomakeuseofgeneticvariantsforthemanage- ofthemetabolicpathwaysinvolvedindirectorindirectdefence mentandmanipulationoftherhizospherecommunity(Ryanetal., probably depends on interactions between genotype and envi- 2009; Wissuwa et al., 2009). These rhizosphere associations and ronment (Le Bot et al., 2009). Moreover, it may be possible theirbenefitstothecropalsodependstronglyoncroppingsystem, to elicit some of these pathways deliberately, with appropriate so it would seem reasonable to conclude that adapted cropping techniques. systems(includingcroprotationandcropmanagementmeasures) couldalsoincreaseefficiency.TheefficacyoftheRhizobium/legume 2.1.3. Waystoimprovetheuseofplantsciencesforecological associationisalsohighlydependentoncroppingsystem,through intensification theeffectsofpracticesonthephysicalandchemicalpropertiesof Theprecedingtwosectionsdonotprovideadetailedreviewof soilsandtheirwaterstatus(Sprentetal.,1987).Theseeffectsare theextensiveliteratureinplantsciences.Instead,theydealwith well known, but should be considered in the light of the recent afewexamplesofrecentprogressandthepossiblebenefitsthat developmentoflegumenodulationgenomics(Staceyetal.,2006). agronomistscouldderivefromtheseadvances(seeTable1).These SturzandNowak(2000)haveenlargedtheirvisiontotheoverall examplesdemonstratethatcloserconsiderationoftheresultsof communities of endophytic rhizobacteria with potentially bene- plant sciences could help agronomists to reach their objectives, ficialeffectsoncropgrowththroughanincreaseinresistanceto pavingthewayforhigherlevelsofproduction,betterqualityprod- unfavourableabioticconditionsandtopathogenaggression,and ucts, and less harmful consequences for the environment. Other throughimprovementsingrowthandmineralnutrition.Theagro- advancesinplantsciences,concerningplantarchitecture,leafand nomicbenefitsoftheseassociationswithendophyticrhizobacteria rootmorphogenesis(McSteenandLeyser,2005;WangandLi,2008; depend on the survival of bacterial communities, which in turn Walteretal.,2009),floralbiology(e.g.,Bossetal.,2004),therole dependsonsoilandcropmanagement(BowenandRovira,1999; ofaquaporins(e.g.,Maureletal.,2008),cellseparationprocesses Acosta-Martinezetal.,2008).Oneofthewaysbywhichcropman- (Robertsetal.,2002)andlongdistancesignalswithinplants(Lough agementcanmodulatetheevolutionofmicrobialcommunities,is and Lucas, 2006), for example, are also of great potential inter- itseffectonrootexudates.Inadditiontoalteringthephysicaland esttoagronomistsworkingonecologicalintensification,asthey chemicalpropertiesofthesoil,rootexudateshavebeenshownto mighthelpcropstoavoidortoresistdeleteriousstresses.How- affectbothsoilmicro-organismcommunitiesandothereukaryotes ever,majoreffortsarestillrequiredtoscale-uptheresultsfrom (Bertinetal.,2003).Baisetal.(2004,2006)reviewedthenature individualgenes,cellsororganstothecanopy,andtotestthesta- ofthechemicalsinvolvedandthecorrespondinginteractionpro- bilityofbiologicalresultsinawiderangeofagriculturalconditions. cesses for various ecological roles. However, one of the aspects Itisalsoimportanttocheckthatadvancesinoneareaarenotasso- of crop/soil community interactions most frequently ignored by ciatedwithseveredrawbacksinothers.However,thesefindings agronomistsisprobablytheroleofthecommonmycorrhizalnet- arenonethelessprecioustoagronomists,whowillneedtouseall works (CMNs), which may be affected directly or indirectly by themeansavailabletoconstructnovel,moreresource-useefficient soiltillage,fertilisers,pesticideuseandaerialplantmanagement and/orproductivecroppingsystems. (Pietikäinen and Kytöviita, 2007). The networks that these fungi Finally, there are many different drivers of change in ecolog- establish between plants may provide a major route for mineral ical intensification (see introduction and subsequent sections). transferfromplanttoplant(Heetal.,2003).vanderHeijdenand Innovative systems that have already been developed in the Horton(2009)recentlyreviewedthepossibilitiesforCMNforma- domain of ecological intensification, such as the use of mix- tionbetweendifferentplantspecies,theirecologicalsignificance turesofcultivarsorspecies,agroforestryandno-tillagesystems, andthebenefitsgenerated.Theyfoundthatthereweremanypos- would certainly benefit from the knowledge provided by plant sibilities for CMN development, but that there were also large sciences.However,thesesystemswillthemselvesraisenewques- differences in the benefits accrued, particularly in terms of pro- tions and issue new challenges to plant science. For example, motionofthegrowthofinterconnectedplants.Similarly,therole although progress has been made in this area, plant sciences T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 201 Table1 Examplesofrecentresultsfromplantsciencesusefulinagronomy. Topicsinplantsciences Keyreferences Potentialagronomicbenefits Plantarchitecture Zhuetal.(2010) Increasedradiationinterception Walteretal.(2009) dePuryandFarquhar(1997) Photosynthesisefficiency WangandLi(2008) Canopypatterntargetforcropmanagement Increaseinyield Identificationofgenotypesadaptedforcropmixture Exchangesofnitrogenbetween Jacksonetal.,2008 Improvedfertiliseruseefficiency rootsandenvironment Roleoforganicanionexudation Glass(2003) Improvednitrogenmanagement Ryanetal.(2001) Interactionbetweenrootsand Mehboobetal.(2009) Improvedmineralnutrition soilorganisms Brussaardetal.(2007) Roleofcommonmycorrhizal Micallefetal.(2009) Improvedcropgrowth networks Ryanetal.(2009) Adaptationofcropmanagement SturzandNowak(2000) vanderHeijdenandHorton(2009) Interactionbetweenaerial deBruxellesandRoberts(2001) Managementofnaturaldefencesforimprovedresistancetopests partsoftheplantand environment results are still often obtained in highly simplified systems and 2.2.1. Whatdoes“Mimickingnaturalecosystems”mean? therefore cannot easily be translated to multispecies systems. Therehavebeenonlyafewpracticalattemptstodesignagroe- Above-ground competition for light and below-ground competi- cosystems from nature. Jackson and Jackson (1999) aimed to tion for water are major processes in ecological intensification developsustainablecroppingsystemsbymimickingthemid-grass thatrequirestudyinsystemsincludingfacilitationbetweenplants American prairie, creating crop mixtures analogous to the vege- (Long and Nair, 1999; Zhang et al., 2008; Malézieux et al., tation structure of the prairie. Traditional agroecosystems in the 2009). tropics, long unknown or disparaged by some agronomists, are frequently based on the integrated management of local natural 2.2. Learninglessonsfromthefunctioningofnaturalecosystems resourcesand,inmanycases,onthemanagementoflocalbiodi- versity.Thesesystemsmayalsobeconsideredtoresultfromthe Strategies for agroecosystem design and management may observationofnearbynaturalecosystemsbygenerationsoffarm- be derived from the observation of natural ecosystems, guid- ers, who have aimed to mimic the functioning and structure of ing alternative agronomic practices. Several authors (e.g., Ewel, thesenaturalsystems.Forexample,slashandburnsystemscanbe 1999;Altieri,2002;Jackson,2002;Vandemeer,2003;Malézieux, consideredtomimicnaturebehaviourafterfire.Agroforestrysys- 2011)havealreadysuggestedthatnaturalecosystemsmayprovide temsinthehumidtropicsmimicthestructureandfunctioningof appropriatemodelsforagroecosystemdesigntoachievebothenvi- rainforests.AccordingtoEwel(1999),humidtropicalecosystems ronmentalandsocialgoalswhileensuringlong-termsustainability. appeartobeparticularlysuitableforapplicationofthe“mimicry This idea is based on the assumption that natural ecosystems ofNature”concept.Agroforestrysystemsinthehumidtropicsare are adapted to local constraints, due to a long process of natu- basedonthetropicalrainforestmodel.Theycombineseveralstrata, ral selection (Dawson and Fry, 1998; Ewel, 1999). It is therefore haveahighlevelofspeciesdiversityandareverywidespreadin assumedthattheincorporationofcertaincharacteristicsofnatu- Asia,Oceania,AfricaandLatinAmerica.Suchsystemsprovideboth ral ecosystems into agroecosystems would improve some of the subsistence for local populations and major environmental and propertiesofagroecosystems,suchasproductivity(Fukai,1993), socio-economicservices(Sanchez,1995;Nair,2001).Lyinghalfway stability (Aerts, 1999; Schulte et al., 2003) and resilience (Lefroy betweenagro-andforestecosystems,agroforestrysystemscom- etal.,1999).Thesefeaturesareparticularlyusefulfordealingwith bine annual and perennial, herbaceous and woody species, in a pestoutbreaks(Trenbath,1993)andincreasingenergyefficiency moreorlesscomplexwholeintermsofthenumberofplantspecies inacontextofthedepletionoffossilfuels(Hatfield,1997).Asim- andpractices(Torquebiau,2007).ThedamaragroforestsofSuma- ilar reasoning was followed in the framework of Ecoagriculture, tra,orthecocoa-basedagroforestsofCameroonorCostaRica,are proposed by McNeely and Scherr (2003), which places biodiver- originalwaysinwhichfarmingcommunitiesusenaturalresources sity at the heart of strategies to conserve and restore ecosystem inhumanreconstructionsofboth“natural”andproductiveecosys- services,increasewildpopulationsinagroecosystems,andsustain temsfromnaturalecosystems(Michonetal.,1995,2007;Schroth agriculturalproduction.Anillustrationofthismimicryisprovided etal.,2001,2004). forcroppingsystemsinFig.2withanemphasisoncropprotection. Thescientificfoundationsofthemimicryparadigm,however, Innaturalecosystems,thevariousanimalandplantspeciesinteract remaintobestudiedthoroughly(Malézieux,2011).Thepotential throughpopulationdynamicsandtrophicnetworks,providingthe of this approach to generate innovative agroecosystems in prac- finalecosystemwithservices,suchaspollination.Instandardcrop- ticealsoremainslargelyunknown.Ewel(1999)andvanNoordwijk pingsystems,theseinteractionsmayleadtopestdamageoncrops, andOng(1999)proposedtwoprinciplesforthedesignofagroe- whichmaybemanagedwithvariouscontrolmethodstolimityield cosystemsbasedonnaturalecosystemmimicry.Accordingtothe loss.Anincreaseinplantspeciesdiversityinsystemsmimicking firstoftheseprinciples,agroecosystemsshouldmimicthestructure naturalecosystemscouldallownaturalenemiestocontrolpests andfunctionofnaturalecosystemsexistinginagivenpedoclimatic andgenerateecosystemservices. zone.Accordingtothesecond,agroecosystemsshouldalsomimic 202 T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 Cropping system Agroecosytem "inspired by Natural ecosystem natural ecosystems" Cultivated biota Biota Crop(cultivar) (plant species/cultivars) (plant species) Crop rotation Spatial arrangement over time Spatial arrangement CCrrooppmmaannaaggeemmeenntt Management over time Associated biota Pests Pests Fauna Natural enemies Chemical, genetic and cultural Population dynamics Population dynamics Trophic networks Trophic networks control Yield(s) Yield Ecosystem services EEccoossyysstteemmsseerrvviicceess Fig.2. Acomparisonofnaturalecosystems,conventionalcroppingsystemsandagroecosystemsinspiredfromnaturalecosystems,withanemphasisoncropprotection. the diversity of species existing in natural ecosystems, thereby foroptimisingnutrientmanagementinareasworkedbyhumans, maintainingthediversityofnaturalecosystemsinthegivenzone. communityecologyinnaturalecosystemsmayfacilitatethedesign Thefirstoftheseprinciplesisclearenough,butmustbeextended ofnewcropprotectionstrategiesandanunderstandingoffacilita- tobeeffective.Indeed,therearemanyfunctions,andstructurecan tionwithinnaturalecosystemsshouldmakeiteasiertomakeuseof beassessedatdifferentscales.Furthermore,basingagroecosytem thisprocessinagroecosystems.Finally,approachesbasedonmim- designsolelyonnaturalecosystemspresentinthesameareamay ickingnaturalecosystemswillinevitablybeconfrontedwiththe betoolimiting:somegoodideasmightemergefromthestudyof “aimproblem”.Naturalecosystemsprovidemanyservicesbutare verydistantsystems. not targeted. Agroecosystems, by contrast, are designed to opti- Accordingtothesecondprinciple,theredesignofagroecosys- misedifferentaspectsandtoachievedifferentgoals.Consequently tems in more ecologically intensive configurations implies their approachesmimickingnaturalecosystemsarelimitedbycertain diversification.Thishasbeenthecase,forexample,inCuba,where agriculturalobligations,suchastheremovalofthemineralscon- small- and medium-scale farmers have tended to diversify their tainedinagriculturalproducts.Someinsightmaybegainedfrom productionsystemsinresponsetotheirlimitedaccesstoortotal regardingagroecosystemsascomplexsystemswithmanysimul- lackofagriculturalinputstosustainproductivity(Funes-Monzote taneousfeedbackloopsincludingadimensionabsentfromnatural et al., 2009). The resulting diversified systems are energetically ecosystems:humanagency. more efficient, less dependent on external inputs, more produc- tive,adaptableandresilient.Thediversificationofagroecosystems 2.2.2. Agroecosystemsascomplexsocio-ecologicalsystems withinthemimicryparadigmmaybeachievedbyincreasingthe Agroecosystemsaresystemsthatcombinesociologicalandeco- numberofmicroorganisms,plantandanimalspeciesrelevantto logicaldynamics,ininteraction.Incomplex,dynamicandspatially agriculture over space and time, or through agrobiodiversity, a heterogeneoussystems,interactionstakeplaceoverscalesgenerat- subset of general biodiversity (Brookfield et al., 2003). However, ingemergentpropertiesandself-regulatorymechanisms(Holling, natural ecosystem mimicry cannot mean reproducing the diver- 1973).Thesemechanismsoftenmanifestascross-scalefeedback, sity observed in natural ecosystems, for at least three reasons. or panarchy (Gunderson and Holling, 2002), and societies con- First,recentreviewsofexistingknowledgeinecologyhavedemon- tribute to system regulation through adaptive management. For stratedthatfunctionalcompositioncontrolsecosystemfunctioning example,insmallholderagriculturalsystemsmakinguseofcom- morefrequentlythanspeciesdiversity(Hooperetal.,2005).Asour munally shared resources, buffering and regulatory mechanisms purposeistoimproveagroecosystemfunctioningthroughecologi- often emerge from collective action (Meinzen-Dick et al., 2004). calintensification,andnottoconservenaturalspeciesbiodiversity This is why agroecosystems may be defined as socio-ecological persewithinagroecosystems,agronomistsshouldconcentrateon systems,orcyberneticsystemssteeredbyhumanstoattaincer- identificationoftheleveloffunctionalbiodiversityresultinginthe tain goals (see Conway, 1987). The capacity of farmers to adapt expressionofinterestingproperties.AspointedoutbyMain(1999), playsamajorroleinsystemresilienceand,byanalogytothecon- whoaddressedthequestionofhowmuchbiodiversityisenough ceptofinformaleconomies(deSoto,2000),regulatorymechanisms in the context of agroecosystems mimicking nature, the level of operateasinformalresourceflowsthatareoftenunaccountedfor diversityconsideredadequatestronglydependsonthegoalsand inagroecosystemsanalysis(Tittonelletal.,2009).Justasnatural criteriausedforevaluation.Moreover,interestingpropertiesmay ecosystemshavea“memory”asadirectconsequenceoftheirhis- arise from the spatial and temporal organisation of the species tory,sodoagroecosystems,exceptthatsomeofthatmemorylies ratherthanpurelyfromtheirnumber.Forexample,lessonscanbe inhumanagency(Tittonell,2007). learnedfromstudiesofnaturalecosystemsaddressingagronomic A wider definition of agroecosystem diversification, more topics:nutrientcyclingwithinacomplexlandscapemaybeuseful compatible with the socio-ecological nature of complex T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 203 agroecosystems, must consider not only species diversity, but Table2 also the diversity of agricultural practices and rural knowledge Examplesoffarmers’knowledgepotentiallyusefulinagronomy. adaptedto/derivedfromlocalpedoclimaticconditions.Theselieat Sourcesofknowledge Keyreferences Potentialagronomic thecoreofhumanagencyandrepresentnewsourcesofknowledge benefit foragronomicresearch(seebelow).Agroecosystemdiversification Localecological ChalmersandFabricius Explainingchangesin in its broadest sense thus concerns the diversity of livelihood knowledge (2007) agriculturalsystems strategiesatacertainlocation,diverselanduse,managementand Traditionalfarming SinghandSureja Designofsustainable marketingstrategies,theintegrationofproductionactivities(e.g., systems (2008) farmingsystems crop-livestock interactions), spatial and temporal associations of Abbonaetal.(2007) Understandingof cropsandcropcultivars,andthemaintenanceofgeneticagrobio- ecologicalprocesses diversityinthesystem.Theefficiencyofuseofnatural,economic Localknowledgeand Ballardetal.(2008) Assessmentof and social resources in agroecosystems—which goes beyond the indicatorsfor managementpractices partial use efficiency of a certain single input—and desirable assessingforest forforests management properties, such as stability and resilience, are based on one or Farmer’sindicators Tchamitchianetal. Indicatorswith moreofthesecategoriesofdiversity.Newavenuesforagronomy supportingdecision (2006) expandeddomainsof tostrengthenagroecologicalintensificationshouldgobeyondthe making validity cultivatedfieldorthemixtureofspeciesinagivenlandscape.They shouldexploredesirablepropertiesandmechanismsthatoperate atthescaleofcomplexsocio-ecologicalsystems,i.e.thattakeinto investigatedfarmers’knowledge.Thestudiesthathavebeencar- accountsociologicalandecologicaldynamicsandinteractionsin riedoutinthisdomainhavemostlyassessedthevalidityofthis agroecosystems. knowledge(e.g.,Grossman,2003;Friedmanetal.,2007;Graceetal., 2009) or considered the local adaptation of more generic solu- 2.3. Farmers’knowledgeandlayexpertisevalorisationand tions(e.g.,Steiner,1998;Affholderetal.,2010).However,farmers’ integrationintoscientificknowledge knowledgeisnotonlyofvalueforapplicationandfortheadap- tationofagronomicknowledgetoaparticularcase.Itcanalsobe Farmers do not rely exclusively on the results and output of usedtoextendtheavailablescientificagronomicknowledge(see agronomicresearchtooperatetheiragroecosystems.Theymake theexamplespresentedinTable2).Wewilldefendthispointand use of much wider knowledge, based on their own experiences discussthevariousissuesitraisesbelow. and on exchanges with other farmers and advisers, thus build- ing their own expertise. This expertise is rooted in the need to 2.3.1. Valueoffarmers’knowledgeforagronomy actwhateverthelevelofagronomicknowledgeavailable:sound We will analyse separately the lay expertise (resulting from anddetailedorunreliableandpatchy.Itisalsodependentonthe farmers’ activities and interactions with their own systems) and characteristics(environmental,economic,social)ofthesituationin the more traditional knowledge that some farmers or societies whichitisconstructed.AccordingtoPrior(2003),wemayconsider havedevelopedovertime.Thevalueoflayexpertiseforagronomy farmers to be lay experts (although this denomination entails an andfordevelopment(supporttofarmers)hasbeenrecognisedfor antinomy):expertsbecauseoftheirexperience-basedknowledge sometime(e.g.,Barzmanetal.,1996;BaarsanddeVries,1999). andlaybecausethisknowledgeislimitedinscopeanddoesnot Thislayexpertisecanhelptoenlargecurrentagronomicknowl- givefarmersthebroaderanddeductiveunderstandingcharacteris- edgeinvariousways.First,farmersoperatetheiragroecosystem ticofscientificorexpertknowledge.Recognitionofthevalueoflay evenintheabsenceofappropriateknowledge,becausetheyhave expertiseisbothanecessityandachallengeinmanydomains,such to.Theythereforedevelopexperience-basedknowledgethatcan as medicine (e.g., adapting treatments according to the patient’s fillinsomeofthegapsinscientificknowledge.However,asmen- reactions,bothasobservedbydoctorsandasinterpretedbythe tioned above, this experience-based knowledge is often limited patient) and industry (particularly for fault detection in plant or tothefarmer’sownparticularcase,whereasscientificknowledge machineoperation).However,althoughthevalueofthislayexper- shouldbemoregeneral. tise is recognised, it is not used to build or extend the current Second, some traditional practices are based on the observa- scientificknowledge,buttoadaptitsapplicationinlocalsituations tion of natural ecosystems (Chalmers and Fabricius, 2007; Reed (Henderson,2010). et al., 2007), which, as we have seen, may be of value for eco- Farmers can observe not only their own production systems, logicalintensification.ChalmersandFabricius(2007),forexample, butalsoothersystems(bothagriculturalandnatural)andinter- showedthatlocalexperts,usingtheirecologicalknowledge,were actionsbetweenthesesystems.Theycanalsogainexperimental abletoputforwardexplanationsforchangesintheirsystem,some knowledge in their own systems. They are often willing to do ofwhichwerealsoprovidedbyscientificknowledge.However,the so and therefore carry out experiments in the operation of their local experts also had other explanations rooted in a more gen- own agroecosystem, evaluating the response of the system to eralunderstandingofthesystem.Traditionalfarmingsystemscan theirdecisions.Thisgeneratesdifferenttypesofknowledge.When alsobeasourceofunderstandingandinspirationforthedesignof confronted with, observing or learning from natural ecosystems, sustainablefarmingsystems.SinghandSureja(2008)showed,for farmers gain knowledge similar to what is generally referred to example,howtraditionalfarmingsystemscopewithharshenvi- as local or traditional ecological knowledge (LEK or TEK, Berkes, ronmentsthroughthemanagementofawidediversityofplants 1999). Over generations, they may also build traditional knowl- providing genetic resources. Abbona et al. (2007) evaluated the edge (not specifically ecological), refined by years of adaptation sustainabilityofatraditionalvineyardsysteminArgentina,both (seeprevioussection).Whenexperimenting,theybuildamixture initsoriginallocationandinanewlyplantedarea.Theyshowed of experience-based and experimental knowledge. Many studies that the traditional system, in its original location, was indeed haveconsideredtheuseofLEK/TEK,butmosthavefocusedonthe sustainable,whereasthissystemwasnotsustainableinitsnew, useofthisknowledgefornaturalresourcemanagement(including different location. They concluded that the efficacy of the tradi- fisheriesandforestrysystems,whichmorecloselyresembleasub- tionalsystemwasdependentonthelocationinwhichandforwhich sistenceharvestingactivity)ratherthanthedesignorimprovement ithadbeendevelopedovertime.Duringthisevaluationprocess, of productive agricultural systems. Fewer studies have directly basedontheuseofindicatorsdevelopedforthisanalysisthrough 204 T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 theadaptationofexistingmethods,theseauthorsgainedinsight inwhichitwasobtained(rangesofthevariablesconsidered,for intoandanunderstandingoftheecologicalprocessesatworkin example);thisfactorcanbeusedtoanalysetheextenttowhichthe thetraditionalvineyardsystem.Theanalysisoftraditionalfarm- knowledgeobtainedisgeneric.Certaintyreferstotheconfidence ers’ practices therefore provided an opportunity to obtain new that can be attributed to the knowledge. Finally, precision mea- scientific knowledge. In a different context, Ballard et al. (2008) sureshowclosetoanumericalexpressionitispossibletogetinthe analysedtheknowledgeinvolvedinthemanagementandmoni- expressionoftheknowledge.Evencertainknowledgemaydisplay toringactivitiesofcommunity-basedforestrygroupsandtheways alowprecisionrenderingitsusepurelyhypothetical(ventilatinga inwhichlocalandscientificknowledgecomplementedeachother. greenhousedoesmodifyitstemperature,butthechangeisdifficult Theyshowedthatlocalknowledgeprovidedarapidandefficient toindicatewithprecision).Artificialintelligenceprovidesaframe- means of assessing the effects of management practices on the workforrepresentingexpertiseandanalysingtheconflictsarising forest.Thesamewasfoundforgreenhousetomatomanagement. wheninformationfromdifferentsourcesiscompared(severallay Tchamitchianetal.(2006)successfullyusedtheconceptof“crop expertsoracombinationoflayexpertiseandscientificknowledge; vigour”asanindicatorintheirexpertsystemcontrollingthedaily AmgoudandKaci,2007;Bench-CaponandDunne,2007;Alsinet greenhouseclimatefortomatoproduction.Tomatocropvigouris etal.,2008;AmgoudandPrade,2009).However,thisdomain(qual- readily assessed by growers of greenhouse tomato crops, on the itative reasoning and argumentation) is still developing and, to basisofasetofobservations:planttipcolourandshape,fruitload ourknowledge,itsconceptsandtoolshavenotyetbeenusedto onthecrop,cropoverallcolour.Scientistsrelatetheseobservations mergelayexpertiseandscientificknowledgeinagronomy(there tothegenerativetovegetativebalanceofthecropanditsability areapplicationsfordatabasefusion,assistingdebatepreparation toperformphotosynthesis(Navarreteetal.,1997),withoutbeing andindustrialplanning).Theaddedvalueoftheseapproacheslies abletomodelitformally. intheneedtoprovideanexplanationdetailingtheargumentssup- Takenasawhole,localknowledgeandlayexpertisecanprovide portingapieceofknowledge,thereforeaddressingthequestions cluestothenaturalorecologicalprocessesmostusefulinthedesign ofcertaintyandprecisionraisedabove. ofsustainablefarmingsystems,suchasthenaturalregulationof Thequalificationoflayexpertisehasbeenshowntobeanec- pestpopulationsbytheirpredators(Barzmanetal.,1996;Sinzogan essarystepinapproachesaimingtocombinethisexpertisewith et al., 2004), or management of the soil and its mineral balance scientific knowledge. Going beyond the issues of the domain of (Steiner,1998;OkobaanddeGraaff,2005;Saitoetal.,2006;Abbona validity, certainty and precision, there is the question of valida- etal.,2007).Theycanalsobeofvalueinthedesignofassessment tionofthenewknowledgeobtained.However,classicalvalidation methodsorindicatorsformonitoringtheecologicalperformances procedures cannot readily be applied, because the observations ofthesefarmingsystems. underlyingtheexperience-basedknowledgeacquiredarelacking. For example, to validate the greenhouse management rules for- 2.3.2. Qualificationandvalidationoflayexpertiseandknowledge malisedfromexpertknowledge,Tchamitchianetal.(2006)useda expression two-stepmethodratherthanadirectvalidationoftherulesthem- Although both interesting and challenging, the lay expertise selves, which was not possible. The first step involved checking of farmers (or advisers) is not easy to use. First, this lay exper- thattheapplicationoftheserulesreallydidresultinthedesired tisemustbeelicitedandrepresented.Severalmethodologieshave patternofbehaviourinthegreenhouse(asexpressedwhenbuild- beenproposedforexpertknowledgeelicitation,eitherforspecific ingtherules),withoutquestioningtheagronomicvalidityofthis applications,suchasplantdiseaseepidemics(HughesandMadden, behaviour.Thesecondstepinvolvedassessingthequalityofpro- 2002),orformoregeneralapplications(Cornelissenetal.,2003; ductionobtainedbyapplyingtheserules,thegoalbeingtoobtain Leyetal.,2010).Appropriateelicitationmethodsincludetheselec- appropriate production levels from the greenhouse. Attempts at tion of a panel of experts and the associated delimitation of the thedirectvalidationofagivenrulehaveonlymadeexplicitwhich knowledgedomainconsidered.Thechoiceofrepresentationalso piecesofagronomicknowledgecanbeusedtosupportagivenrule. influencestheelicitationprocess.Manyauthorsadvocatetheuse However,itwouldnothavebeenpossibletodesigntherulefrom offuzzymodels,whichallowtheuseoflinguistictermsandare thisidentifiedscientificknowledge,generallybecausethescopes moresuitablefortheexpressionofknowledgeinqualitativerather ofthescientificknowledgeandthatofthelayexpertiseyielding thanquantitativeterms.Bycontrast,scientificknowledgeismost theruleweredifferent. frequentlymodelledinquantitativeterms,particularlywhenthe goalistorepresenttheoperationofasystemundertheinfluence ofbothcontrolled(humandecisionsandactions)anduncontrolled 3. Methodsforsynthesizinginformation (environment)factors.Mostoftheagronomicmodelsbuilttosim- ulateagroecosystemsarenumericalmodelsinwhichthevariables Thethreemainresearchmethodscurrentlyusedbyagronomists havepointvaluesratherthanintervalorprobabilisticvalues.There (Fig. 1) are various types of field experiments, on-farm inquiries is therefore a gap between the most common representation of (e.g., Doré et al., 2008), and modelling (e.g., Rossing et al., 1997; scientificknowledgeandthatoflayexpertise,hinderingthecom- Bergez et al., 2010). Field experiments provide validated knowl- binationandmergingofthesetwotypesofknowledge.However, edge meeting the scientific rules for data acquisition. This basic differencesinrepresentationarenottheonlydifficulty.Aspointed knowledgecanbesupplementedbyinquiriesprovidingdatafrom outbyPrior(2003),layexpertsmaybewrong,eitherbecauseof real-worldagriculturalsituations(farms).Modellingcanbeused thelimitedscopeoftheirexperienceorbecausetheirconclusions toexploretheresponseofkeyagronomicandenvironmentalvari- arebasedonfalsepremises(misobservations,forexample,dueto ables, such as, for example, yield or nitrogen loss, to climate, alackofknowledgeorskills).Theirknowledgeisalsosituation- croppingsystemvariablesorsocietalchanges.Thedatagenerated dependentinthatitisobtainedinadomainoflowvariability(oneof arethenprocessed,mostlybyclassicalmethods,suchassimulation thegoalsofagriculturalpracticesisoftentoreducevariabilityand studies,single-experimentdataanalysis,orgroupanalysis.These diversityinagroecosystems,agoalchallengedbyecologicalinten- methodscouldprobablybecomplementedwithtwoothermeth- sification).Layexpertiseshouldthereforebequalifiedandanalysed ods: meta-analysis, involving the statistical synthesis of results independently,inseveraldifferentways:domainofvalidity,cer- fromaseriesofstudies,andcomparativeanalysesofagroecosys- taintyandprecision.Thedomainofvalidityisimportantbecause tems,involvingtheuseoflarge-scalecomparisonssimilartothose knowledgeshouldbeassociatedwithadescriptionofthedomain usedinecology(e.g.,Fortuneletal.,2009). T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 205 3.1. Meta-analysisandagronomy andwithin-studyvariances(Borensteinetal.,2009).Combina- tionoftheindividualstudyestimatesandestimationofamean Meta-analysis (e.g., Borenstein et al., 2009) is more powerful valueforthevariableofinterest,forexample,canbeachieved than a simple narrative review of a series of studies, because it bycalculatingaweightedsumofindividualestimatesderived synthesises published data in a quantitative manner and makes fromthestudiescollectedinstepii. itpossibletoassessthebetween-studyvariabilityofavariableof v. Assessment of publication bias. Publication bias occurs when interest. only studies with highly significant results are published. In Both scientific researchers and decision-makers can benefit thiscase,ameta-analysiscanleadtoabiasedconclusionand from meta-analysis in several ways (Sutton et al., 2000), as this overestimationoftheeffectofagivenfactor.The‘funnelplot’ approach provides a methodological framework for (i) explor- techniquecanbeusedtodealwiththisissue(e.g.,Borenstein ing what has already been done on a given research topic and etal.,2009). identifyingmoreclearlywherethegapsanduncertaintieslie,(ii) vi. Presentationoftheresultsandofthelevelofuncertainty. generatinganoverviewofdivergentresults,(iii)guidingdecisions basedonasystematicreviewandstatisticalanalysisofalltheavail- In the context of ecological intensification, the meta-analysis abledatarelatedtoagiventopic,(iv)broadeningtheknowledge frameworkconstitutesaninterestingalternativetodynamiccrop base and allowing replication for the testing of hypotheses, (v) models.Dynamiccropmodelscanbeusedbothtoassessthecon- addingtothecumulativedevelopmentofscience. sequencesofcroppingtechniquesandenvironmentalvariablesfor Mostmeta-analysescarriedouttodatehavebeenperformedin cropproduction(e.g.,JonesandThornton,2003)andtoassessthe medicalscience(Normand,1999;Suttonetal.,2000).Thisapproach effect of cropping systems on key environmental variables (e.g., hasbeenlesssystematicallyappliedinotherareasofresearch,such Rolland et al., 2008), two key issues for ecological intensifica- asecology(e.g.,ArnqvistandWooster,1995;Cardinaleetal.,2006), tion.However,thesemodelsincludeseveralsourcesofuncertainty and has sometimes been applied in agriculture (e.g., Bengtsson (Monodetal.,2006)andtheirpredictionsarenotalwaysreliable etal.,2005),animalscience(Sauvantetal.,2008)andplantpathol- (e.g.,Barbottinetal.,2008;Makowskietal.,2009).Webelievethat ogy(Rosenbergetal.,2004).Inagronomy,meta-analysismethods meta-analysisshouldbemoresystematicallyusedbyagronomists, have generally been used to compare the effects of different toassessandcomparetheeffectsofcroppingsystemsonproductiv- croppingtechniquesorofdifferentcroppingsystemsonyieldor ity,risksofsoilandwaterpollution,greenhousegasemissionsand biomassproduction.Forexample,MiguezandBollero(2005)used biodiversity.Aconsiderablebodyofexperimentaldataisavailable ameta-analysismethodtosummariseanddescribequantitatively forsuchpurposes(e.g.,RochetteandJanzen,2005).Suchdatacould theeffectofseveralwintercovercropsonmaizeyield.Theauthors bereviewed,combinedandanalysedwithstatisticaltechniques,to estimated the ratio of maize yield after a winter cover crop to rankcroppingsystemsasafunctionoftheirimpactonkeyenvi- maizeyieldwithnocoverfrom37publishedstudiescarriedout ronmentalvariables,suchaswaternitratecontent,greenhousegas invariousregionsoftheUSAandCanada.Inanotherstudy,Miguez emissions(e.g.,N O)andthepresence/absenceofspeciesofeco- 2 etal.(2008)studiedtheeffectsofplantingdensityandnitrogen logicalinterest(e.g.,earthworms,birds).However,meta-analysis fertiliser on the biomass production of Miscanthus × giganteus, requirestheuseofappropriatetechniquesandthevalueofameta- using31publishedstudiesincludingbiomassmeasurementsatdif- analysismaybegreatlydecreasedifthesixstepsoutlinedabove ferentdatesoverseveralyears.Drawingonpublishedstudieson arenotrigorouslyimplemented. sub-SaharanAfricanagriculture,Chikowoetal.(2010)conducted a meta-analysis of factors controlling nitrogen and phosphorus 3.2. Comparativeanalysisofagroecosystems capture and conversion efficiencies by major cereal crops. The meta-analysiscarriedoutbyBadgleyetal.(2007)didnotfocuson Information useful for the ecological intensification of agroe- aspecificcroppingtechnique,butwasperformedtocomparetwo cosystems may be obtained from comparative analyses of the agriculturalsystems:organicversusconventionalorlow-intensity. structuralandfunctionalpropertiesandperformanceofcontrast- The authors compared the yields obtained in an organic system ing agroecosystems. Similar approaches, based on temporal or withthoseobtainedinconventionalorlow-intensityfoodproduc- spatialcomparisons,areusedinotherfieldsofresearch,suchas tionsystems,basedonyielddatafrom293individualstudieson plant sciences (Wright et al., 2004; Vile et al., 2005; Mauseth, various crops. These data were used to estimate the mean yield 2006), evolution sciences (Schluessel et al., 2008) and marine ratioforvariousfoodcategories,forbothdevelopedanddeveloping ecology(FuhrmanandSteele,2008).Thecomparativeanalysisof countries. agroecosystemsandcomparisonsofagroecosystemswithnatural Diverse techniques for meta-analysis are available (e.g., ecosystemsinvolvethesimultaneousanalysisofmultiplecriteria, Borenstein et al., 2009; Sutton et al., 2000), but meta-analysis withevaluationoftheextenttowhichtheydisplayspecificsystem shouldalwaysincludethefollowingsteps: properties. Several approaches have been proposed for this pur- pose (e.g., Pannell and Glenn, 2000; de Bie, 2000; Xu and Mage, i. Definitionoftheobjectiveofthemeta-analysisandofthevari- 2001;López-Ridauraetal.,2002;Giampietro,2003),basedlargely ableofinteresttobeestimatedfromthedata(e.g.,inMiguez onconceptsformulatedmorethanadecadeago,byauthorssuch andBollero,2005,thevariableofinterestistheratioofmaize as Conway (1987) and Marten (1988). These methods evaluate yieldafterawintercovercroptomaizeyieldintheabsenceof indicators relating to the properties of agroecosystems, such as acovercrop). productivity, stability and resilience. These properties are often ii. Systematicreviewoftheliteratureand/orofthedatasetreport- interdependent and, as pointed out by Marten (1988), they are ingvaluesofthequantitiesofinterest. notuniversalandmustberedefinedundereachnewsetofcondi- iii. Analysisofdataquality(i.e.,qualityoftheexperimentaldesigns tions.Asdiscussedabove,studiesofthelocalknowledgesustaining andofthemeasurementtechniques). various mechanisms of indigenous resilience across contrasting iv. Assessment of between-study variability and heterogeneity. agroecosystems, particularly at the scale of the landscape and Evaluation of the between-study variability of the variable of its functionality (e.g., Birman et al., 2010), are also a promising interestandoftheheterogeneityoftheaccuracyofindividual startingpointforobtaininginformationusefulforecologicalinten- estimatesisanimportantstepinameta-analysisandseveral sification. In the next few paragraphs, we examine briefly some statisticalmethodshavebeenproposedtoestimatebetween- criticalissuesrelatingtothechoiceofindicatorsinmulticriteria 206 T.Doréetal./Europ.J.Agronomy34 (2011) 197–210 evaluationsandidentifyinnovativewaysoflookingattherelation- nomicsbyLeontief(1951,1966),andlaterintroducedintoecology shipbetweenstructureandfunctioninagroecosystems. byHannon(1973).Indicators,suchasaveragemutualinformation (AMI) and ascendency (A), were proposed by Ulanowicz (1997, 3.2.1. Comparativeanalysisbasedonmultipleindicators 2004)forcharacterisationofthedevelopmentcapacity(interms In practice, the implementation of multicriteria analytical ofincreasedorganisation)ofecologicalsystems,andhaverecently frameworksofteninvolvestheselectionofanumberofindicators beenusedincomparativeanalysesofagroecosystems(Rufinoetal., (or the use of a list of predetermined indicators) and of refer- 2009). This approach is known as ecological network analysis, encethresholdvaluesforeachindicator.Theselectionofindicators and Rufino et al. (2009) presented a set of indicators including is frequently biased towards the disciplinary standpoint of the AMI, A, and Finn’s cycling index, for assessment of the diversity observerorhighlyinfluencedbycertainstakeholders,so‘quality and organisation of system components governing N flows and control’methodsforevaluatingthechoiceofindicatorsarenec- food self-sufficiency in three smallholder crop-livestock systems essary.Intheirexaminationofthechoiceofindicatorsindifferent fromEthiopia,KenyaandZimbabwe.Farmsystemsareconceptu- casestudies,GrootandPacini(2010)arguedthatmulticriteriaeval- alisedasnetworks,withthehouseholdandthefarmingactivities uationsshouldinvolvetheanalysisoffourmainsystemproperties: represented as compartments and the N flows represented as performance,diversity,coherenceandconnectedness,whichcan connections between compartments. In this example, indicators beapproachedfromfourdimensions:physical,ecological,produc- assessing network size, activity, cycling, organisation and diver- tiveandsocial.Performancerelatestofunctionalpropertiesofthe sityoftheNflowswerecomparedwithindicatorsofproductivity agroecosystem,suchascapacity,stabilityandresilience.Diversity and household food self-sufficiency. This analysis revealed that relatestothestructuralpropertiessustainingsuchfunctions.Indi- although the amounts of N cycled were small and similar at all cators of coherence describe the degree of interaction between sites,resourceuseefficiencyanddependenceonexternalresources components or subsystems within an agroecosystem, and con- differed widely between these apparently ‘comparable’ agroe- nectednessdescribesinteractionswithadjacentsystems(i.e.,other cosystems.SystemperformancewaspositivelyrelatedtoNflow agroecosystems,urbanornaturalsystems,etc.).Whenseveralindi- network size, organisation and N cycling, consistent with the catorsareconsideredsimultaneously,itmaybepertinenttocheck hypothesis that increasing the organisation of resource cycling whetheralltherelevantcriteriapertainingtosystemperformance, withinresource-limitedagroecosystemsmayrenderthesesystems diversity,coherenceorconnectednessaregivenequalimportance. moreadaptableandlessvulnerable. Forexample,López-Ridauraetal.(2002)andPacinietal.(2003) Themainhypothesisunderlyingtheuseoftheseindicatorsis used two sets of indicators in two independent evaluations of that agroecosystems retain the properties of the natural ecosys- agroecosystems.Althoughbothmethodsconsideredmultiplecri- tems for which these indices were derived. Ulanowicz (2004) teriapertainingtosystemsustainability,theyweightedthevarious calculatedthevalueofseveralindicatorsofnetworksizeandorgan- systempropertiesand/ordimensionsofsustainabilitydifferently. isation,suchasthenumberofdifferentnodesandflows,theirroles In general, comparative analyses based on indicators provide and their connectivity, for a number of natural ecosystems and astaticpictureofthestatusofagroecosystemsatoneparticular agroecosystems.Thisexerciserevealedwidergapsbetweenthese point in time, without considering the underlying feedback and systemsintermsofindicatorsoforganisationthanforthemagni- system dynamics responsible for bringing the system to its cur- tudeofenergymatterandinformationflowwithinthem.Inother rentstatusandforanysubsequentchangetothatstatus.Beyond words,increasingorganisationmakesitpossibletodomuchmore comparing multiple indicators and the tradeoffs between them, with the same resources, while contributing to system stability. the comparative analysis of agroecosystems should aim to dis- Theextentandthemannerinwhichorganisationcontributesto til the relationships between relevant properties; e.g., between buildingresilienceinagroecosystemsisafascinatingresearcharea performance on the one hand, and diversity, coherence and thatremainslargelyunexplored.Existingframeworksofthinking connectednessontheother.Acommondenominatoroftheindi- about resilience in the field of ecology and nature conservation catorsusedinmulti-criteriaevaluationsistheirinterdependence mayalsobeofinteresthere(e.g.,Walkeretal.,2010).Anindirect and their dependence on the structural diversity of the agroe- measurementoftheorganisationofanagroecosystemisitsenergy cosystem. This interdependence results from the co-adaptation andentropybalance.Svirezhev(2000)proposedtheuseofthermo- of agroecosystem components over time. The structural diver- dynamicsconceptstoassessthesustainabilityofagroecosystems, sity of agroecosystems, corresponding to the diversity of system basedontheprinciplethatanecosysteminequilibriumwithits componentsandtheirinterrelationships,isonlyfunctionalwhen environmenthasacertain‘capacity’toabsorbanthropogenicstress organisedinaspecificway. thatisregulatedbyitscapacitytoexpelentropybacktowardsthe environment(the‘entropypump’).Thiscapacity,whichemerges 3.2.2. Analysingthestructureandfunctioningofagroecosystems fromvariousagroecosystemproperties,canbeusedtocharacterise Itisoftenpostulatedthattheecologicalintensificationofagroe- thestatusofanagroecosystemwithrespecttotheadjacentnatural cosystems may be achieved through gradual diversification to ecosystemfromwhichithasbeenderived. capitalise on regulatory principles and mechanisms inherent to Many of the properties of agroecosystems are often interde- natural ecosystems (see above and, for example, Altieri, 1999; pendent, together determining the vulnerability and adaptation Gliessman,2001;Wezeletal.,2009).Knowledgeofthestructural capacity of these systems in the face of external shocks and diversityofanagroecosystem,however,maynotbesufficientto stressors (Luers, 2005). Far from being postulates of a new the- explainitsbehaviour,andthewayinwhichthediversecomponents ory, these properties are discussed here as operational, working ofthesystemrelatetoeachothershouldalsobeknown.Moreover, concepts. We know that the provision of agroecosystem service unnecessarilyhighdegreesofdiversityofsystemcomponentsand functions is regulated by the intrinsic properties of these sys- flows within systems with poorly organised configurations may tems, the functionality of which can be influenced by design. In leadtoredundancy(Kauffman,1995;Ulanowicz,2004).Here,we practical terms, ‘design’ implies proposing alternative configura- examinesomemethodsforstudyingthediversityandorganisation tionsfortheorganisationofenergy,matterandinformationflows ofsystemcomponentsbasedonthetheoryofnetworksthatmay towards,withinandfromthesysteminspaceandtime.Theexam- beusedinthecomparativeanalysisofagroecosystems. plesexaminedhereindicatethat,uptoacertaincriticallevel,an Indicatorsofnetworkcomplexityandorganisationhavebeen increaseinthediversityofsystemcomponentsandinterrelation- derivedfromcommunicationscience.Theywerefirstusedineco- ships confers desirable properties on agroecosystems consistent

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tems may also provide sources of inspiration for cropping system design, in terms of their structure and function on the one We suggest that agronomists make more use of meta-analysis and . biological regulation mechanisms at different levels: crop manage- ment Many authors advocate the use.
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