Ciro Gardi and Simon Jeffery

Soil Biodiversity

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A-23759-EN-C

ISSN 1018-5593

EUR 23759 EN

Soil BiodiversityCiro Gardi and Simon Jeffery

The mission of the JRC-IES is to provide scientific-technical support to the European Union’s policies for the protection and sustainable development of the European and global environment.

European CommissionJoint Research CentreInstitute for Environment and SustainabilityLand Management & Natural Hazards Unit

Authors: Ciro Gardi, Simon JefferyDesign: José-Joaquín Blasco

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EUR 23759 ENISBN 978-92-79-11289-8ISSN 1018-5593DOI 10.2788/7831

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Table of contents

Soil Biodiversity 5Measuresofsoilbiodiversity 5OrganismsoftheSoil 6

The Functions of Soil Biodiversity 7Nutrientcycling 7Soilformationandweathering 8Wasterecycling 8Homeforotherorganisms 9Functionalredundancy 9Resistancevs.Resilience 10

The Economics of Soil Biodiversity 11

Soil Biodiversity and Sustainable Agriculture 13Organicmattercyclingandhumification 13Fertilityregulationandnutrientuptake 14Pestanddiseasecontrol 14Soilstructureandsoil-waterrelationships 14Pollination 15

Soil Biodiversity and Biotechnology 16Bioremediation 16Antibiotics 16Antibiotic resistance 17Biocontrolofpests 17

Soil Biodiversity at the Extreme 19Temperature 19Hot 19Cold 19Dry 19SolarRadiation 20Mechanismsforcopingwithextremes 20Cryptobiosis 20Use of proteins 20Cyst formation 20

Soil Biodiversity and Climate Change 21TheImpactofSoilBiodiversityonCO

2 21

TheImpactofSoilBiodiversityonotherGreenhouseGases 22

References 23

Whatisbiodiversity?Biodiversityhasdifferentmean-ingsdependingonthesituationbeingdiscussedandthe target audience. For example, the Oxford English Dictionary defines biodiversity as being “The varietyofplantandanimallifeintheworldorinaparticularhabitat”.Thisisdefinitionisclearlysufficientfornon-specialists.However,whenlookingmorespecificallyatbiodiversity,itbecomesevidentthatthoughtneedstobe given to other groups such as fungi, bacteria andarchea.Assoilissuchasdiversesystemwhenconsid-eredbiologically (aswellasphysicallyor chemically)itisnecessarytoincludealltaxonomicgroups.There-fore, throughout this booklet, when referring to “soilbiodiversity”itwillbeinreferencetothevarietyofall living organismsfoundwithinthesoilsystem.

Thesoilsystemisdynamic,highlyheterogeneousandextremelycomplex.Soilitselfconsistsofamineralpor-tioncontainingmainlysilicaandamixtureoftracemet-als, and an organic matter portion containing a largevarietyofdifferentorganiccompounds,aswellaswaterandvastarrayofdifferentorganisms.Soilcanexistasavarietyoftextures;withthetexturebeingaproductofchangesintherelativeproportionsofsand,siltandclay.Itcancontainareasofrelativedryness,andincludesmi-croporeswhicharealmostalwayswaterfilledapartfromintimesofextremedrought.Theproportionandtypeoforganicmattervariesbothwithdepth,andspatially.

This high level of heterogeneity means that soil con-tains an extremely large number of ecological nicheswhichhavegivenrisetoastaggeringarrayofbiodiver-sity.Usingataxonomicapproachtomeasurebiodiver-sity,itisoftensaidthatmorethanhalftheworld’ses-timated10millionspeciesofplant,animalandinsectslive in the tropical rainforests. However, when thisapproach is applied to the soil, the level of diversityisoftenquotedasbeing in the rangeofhundredsofthousandstopossiblymillionsofspecieslivinginjust1handfulofsoil!

Measures of soil biodiversity

Measurementsofthelevelofsoilbiodiversityinagivenareaareimportantasahighlevelofspeciesdiversityisthoughttoindicateahealthyenvironment.Nospe-cificindicesexist,orneedtobedevelopedforthesoilsystem as biodiversity indices are applicable acrossthe entire range of ecosystems without the need formodification.However,eachhasitsownstrengthsandweaknesses.

Thesimplestmeasuresofbiodiversityare:

• Species richness, normally denoted “S”, which isthetotalnumberofspeciesfoundinanecosystemorsample.

• Species evenness, normallydenoted“E”,which isameasureofhowsimilartheabundancesofdifferentspeciesareinacommunity.Speciesevennessrangesfromzerotoone.Whenevennessisclosetozero,itin-dicatesthatdistributionoforganismswithinthecom-munityisnoteven,i.e.mostoftheindividualsbelongto one, or a few, species or taxa. When evenness isclosetoone,itindicatesthatthedistributionoforgan-ismswithinthecommunityiseven,i.e.eachspeciesortaxaconsistofasimilarnumberofindividuals.

Clearly, thesetwomeasuresofbiodiversityaremuchmore informative when combined than when usedalone.

Othermethodswhichareoftheusedtoquantifybiodi-versityinanecosystemare:

Simpson’s index (D) gives the probability that tworandomlyselectedindividualsbelongtotwodifferentspecies/categories.Itisoftenusedtoquantifythebio-diversityofagivenhabitatandtakesintoaccountboththenumberofspeciesandtherelativeabundanceofeachspeciespresent.

Simpson’sindexiscalculatedasfollows:

WhereSisthenumberofspecies, Nisthetotalpercentagecoverortotalnumber oforganisms, nisthepercentagecoverofaspeciesornumber oforganismsofaspecies.

IthasbeennotedthattheSimpsonIndexcan,insomesituations,providemisleadingresultswithsomeareaswhichclearlyhave lowlevelsofbiodiversityhavingadisproportionately higher index. This situation is un-common, however, and the Simpson Index normallyprovidesarealisticmeasureofbiodiversitywithalowindexequatingtoarelativelyhighlevelofbiodiversityandahighindexrelatingtoarelativelylotlevelofbio-diversity.

Shannon-Wiener index (H1) (alsooftenreferredtoastheShannonIndex)isameasureoftheorderordisor-der inaparticularsystemwhichcanbeusedandap-pliedtoecologicalsystems.Whenappliedinecology,inordertoquantifylevelsofbiodiversity,theShannonindex takes into account both species richness andtheproportionofeachspecieswithinazone.Ahigherindexisanindicationthateithertherearearelativelyhighnumberofuniquespeciesorthatthereisrelative-lyhighspeciesevenness.

TheShannonindexiscalculatedasfollows:

Soil Biodiversity

5

pi is the relative abundance of each species. This is

calculated as the proportion of individuals in a spe-ciescomparedtothetotalnumberofindividualsinthecommunity:

niisthenumberofindividualsinspeciesi.

NisthetotalnumberofallindividualsSisthenumberofspecies.

Organisms of the soil

Aspreviouslystated,thesoilenvironmentishometoanincrediblediversityoforganisms.Addedtothat,theorganismswhichare found therearealsooftenexistat astonishingly high levels of abundance. The levelof abundance and diversity varies from soil to soil,dependingonfactorssuchasorganicmattercontent,soiltexture,pHandsoilmanagementpractices.Belowistheapproximateabundanceanddiversityoforgan-ismsdividedintogroupingsaccordingtosize,typicallyfoundinahandfuloftemperategrasslandsoil.

MicrofaunaSizerange:1-100mm

MesofaunaSizerange:100mm-2mm

MegafaunaSizerange:‹2mm

Bacteria100billioncellsfrom10.000species

Tardigrades Earthworms

Fungi50kmofhyphaefrom500’sofspecies

Collemobla Ants

Protozoa100.000cellsfrom100’sofspecies

Mites Woodlice

Nematodes10.000individualsfrom100’sofspecies

Combined1.000’sindividualsfrom100’sofspecies

Combined100’sindividualsfrom10’sofspecies

Thereasonthatsuchaslargeabundanceoforganismscanbefoundin justonehandfulofsoil isduetotheporespacefoundwithinsoilwhichiswheretheorgan-ismslive.Whileitmayappeartobesolid,soilnormallycontainsa largeamountofporespaceand in fact, insome soils, the pore space can make up 50% of thetotal volume of the ‘soil’. The pore space itself cangenerally be divided up between air and water filledspace,withtheexceptionofintimesofwaterlogging

orextremedrought.Thesurfaceareaofthisporespacecanexceed24,000m2in1gofclaysoils,withthetotalsurfaceareadecreasingwith increasingsiltandsandcontent.Thisdemonstratesthat,atthescaleofmicro-organisms,thereishugeamountofspacetofunctionasahabitatfororganismsinsoil,andthisisthereasonthatarelativelysmallamountofsoilcanbehometosuchavastarrayandabundanceoflife.

Smaller size > larger size

6

Problemsarisewhenwetrytousethetaxonomicap-proach to quantify soil biodiversity, especially whenwemoveintothemicroscopicworldofbacteria.Firstly,onlyasmallpercentageofsoilbacteria,probably<10%,arecurrentlyculturableinthelaboratoryandthislim-itstheamountofresearchthatcanbeundertakenonthem in a laboratory. Added to this, as bacteria canswaplargeamountsofDNAbetweenthemselves,theverydefinitionofwhatmakesa‘species’isunclearforbacteria.Indeed,thereisnowidelyacceptedconsen-susfordefining‘species’inbacterialsystematics.

Moreimportantly,wewouldbedramaticallyunderes-timatingthevalueofsoilbiodiversityifweweretouseonlythetaxonomicapproach.Itisthediversityoftheprocesses, the “functional diversity”, carried out bythe soil biota which gives soil biodiversity such highvalue.

Soilorganismsperformmanyimportantfunctionssuchasplayinga largerole in thecyclingofnutrients.Forexample,thisincludesthemovingcarbonfromthesoiltotheatmospherethroughmicrobialdecompositionofsoil organic matter and a complete understanding ofthisfunctionishighlypertinentinthisageofgrowingconcernoveratmosphericcarbondioxidelevels.Otherfunctions include the aiding of soil fertility throughinputofnitrogenandcarbon into thesoil,aswellasaffectingandmaintainingsoilstructure.Thesoilbiotaalsoaidsthecleaningofwatersuppliesaswaterfiltersdownthroughthesoil,aswellastheremovalofpollut-antsfromthesoilthroughdegradation.

Itisclearthatthesoilbiotaperformsmanyvitalrolescoveringavastrangeofprocessesandfunctioningatarangeofdifferentscalesfromthemicro,sub-aggre-gate scale up to the global scale. Soil biodiversity istherefore known to play a very important role withintheglobalsystem,andongoingresearchcontinuestohighlightthispoint.

Nutrient cycling

Allglobalnutrientcyclescontainanedaphicphasetoagreaterorlesserextent.Manyofthecyclesarehighlycomplex,involvingarangeofenzymesandbiochemi-calprocesswhicharenotgoingtobediscussedhereindepth.However,anoverviewoftheprocesseswhichoccur and are reliant on the soil biota are presentedbelow.

Oneofthemostwidelydiscussednutrientcyclesinre-centtimesisthecarboncyclebecauseofitspertinencetothetheoryofclimatechange.Thecarboncycleoc-curs when carbon dioxide (CO

2) is fixed into organic

formthroughtheprocessofphotosynthesis.Plantsaremostfamousforperformingthisprocess,butarange

ofmicrobialorganismsincludingalgae,cyanobacteriaandsomeotherformsofbacteriaarealsocapableofphotosynthesis.Inthecarboncycle,thisfixedcarboncanmoveupthroughtrophiclevelsasphotosyntheticorganisms,or“primaryproducers”,aregrazeduponby“primaryconsumers”suchasherbivores,andtheseinturncanbepredatedby“secondaryconsumers”andsoon.

Thecarbonthatwasinitiallyfixedbyphotoautotrophsisreturnedtothesoilorganicmatterwhentheorganismsdie,orthroughexcreta.Thiscarbon,whichformspartoftheorganicmatterofthesoil,canthenfollowoneoftwopathways.Itcanbesubjecttomicrobialdecompo-sitionwherebymicrobesusetheorganicsubstanceasan energy source and the carbon is returned back totheatmosphereintheformonrespiredCO

2.However,

thereareseveralfactorsormechanismswhichcanin-crease,sometimesdramatically,theresidencetimeofcarboninsoils.Onefactoristhelevelofrecalcitranceofthecarbonform.Forexample,short-chaincarbohy-drates are highly labile and do not generally remainin soils for long. However, more complex molecules,especiallyligningsandtanninsaremuchmorerecalci-trantandcanremaininsoilsformanyyears.

Other mechanisms exist by which carbon can remaininthesoilforextendedperiodsoftime,possiblycen-turies.Oneexampleofthisispeatbogswhich,duetotheirwaterloggednature,havehighlyrestrictedgase-ousexchangebetweentheatmosphereandbogitself.Thismeansthatsubsurfaceareasofpeatbogsbecomeanaerobicandacidicandthisseverelyrestrictsthemi-crobialdecompositionoftheorganicmatter.

Inmineralsoils,however,itislesscommonforwaterlogging to occur and so prevent microbial decay. Inthesesoils,itismorecommonforittobeinaccessibil-ityoforganicmattertomicrobialattackwhichpreventsitsdecay.Thiscanoccurbecausetheorganicmatterisstuckbetweensoilaggregatesmeaningitisprotectedfromaccessbymicrobes,becauseitisinmicro-poreswhicharetoosmall formicrobestoenter,or justbe-cause, on the micro-scale, there are no microorgan-ismsinthevicinitywhicharecapableofdecomposingthe substance. This means that the organic mattercontentofamineralsoilcanberelativelystableuntiladisturbanceprocesssuchastillageoccurs.Thisthenexposespreviouslyprotectedorganicmattertoattackandsocausesaflushofmicrobialbiomassasthisnew-lyreleasedenergysourceisutilizedbythesoilmicro-biota,andalsoleadstoareductioninthesoilorganicmattercontentofsoils.

Thenitrogencyclereliesheavilyonthesoilbiota.Thelargestpoolofnitrogen is theatmospherewith isal-

The functions of Soil Biodiversity

6 7

most 80% nitrogen. Gaseous nitrogen is not able tobeutilisedbythemajorityoftheorganismsonEarth,including plants. It first requires ‘fixing’ by microor-ganisms, through the actions of free living microbessuchascyanobacteriaandvariousgeneraofbacteriaandactinomycetes,orbysymbioticmicrobessuchasRhizobium which form root nodules in legumes. Thisnitrogen fixation process converts gaseous nitrogenintoammoniawhichcanbeutilizedbyplantsoralargefraction of this ammonia is also converted into otherplant available forms first into nitrite (NO

2-) and then

intonitrate(NO3-

).

Conversionofnitrogenproductssuchasnitratesandnitritesbacktonitrogengasoccursthroughaprocessknownasdenitrification.Thisprocessoccursinanaer-obicconditionswherebacteriausenitrogen,duetotheabsenceofoxygen,foranaerobicrespiration.

Thenitrogencyclehasveryimportantagriculturalandenvironmentalimplicationsasitaffectsbothsoilfertil-ity, due to the fact that nitrogen is often the limitingnutrient for crop growth, and it can also be a sourceofthegreenhousegasN

2O.Forthesereasons,among

others,thenitrogencyclehasbecomeamajorresearchtopic in recent years. This has shed new light on theprocesses and organisms involved in the cycle. Forexample,overthepastfewyears,researchhasuncov-eredthevariousrolesplayedbyarcheainthenitrogencycleanddemonstratedthattheyareabletoperformbothassimilatoryprocesses,suchasnitrogenfixationandnitrateassimilation,aswellasdissimilatoryrolessuchasnitraterespirationanddenitrification(Cabelloet al.,2004).

Therearemanyothernutrientswhicharevitalforlifeon this planet which have important edaphic phasesreliantonthesoilbiota,generallyforthedecomposi-tionalstagesof thecycle. Forexample,phosphorousis an important element for life on Earth and is usedforseveraldifferentbiologicalprocesses,aswellasbe-ingavitalpartofbothDNAandRNA.Whileplantsarethemostimportantorganismsregardingtheuptakeofphosphorousfromwaterandsoil,andmakingitavail-ableupthroughthedifferenttrophiclevels,itisagainthe soil microbiota which release phosphorous backinto theenvironment throughdecompositionofdeadplantsandanimals.

Soil formation and weathering

Soil forming processes occur as part of a complexfeedback cycle between the mineral fraction of soils,theenvironment,andthebiotawithinthesoilsystem.Soil formation starts when rocks start to breakdownthroughweathering,overmanyyears.Thetypeofrockwhichweathersandfromwhichthesoilformsisknownasthe“parentmaterial”.

Early colonizers, such as lichens and other photoau-totrophic organisms, fix carbon dioxide from the at-mosphere as they grow and start to establish smallamountsoforganicmatterwhichotherorganismscan

utilise as an energy source. Overtime, the amount oforganicmatterbuildsupasmorecarbonisputintothesystemthroughphotosynthesis,allowingotherorgan-isms to colonise the system. Once there is sufficientorganic matter and other nutrients available, higherplantsareabletocolonisethesoilwhichcanthenaidand speed up the soil forming process through theirrootsgrowingintocracksinrocksandcausingcrackstoexpandtherebyincreasingthesurfaceareaexposedtoweathering.

Weatheringistheprimarysourceofessentialelementsfororganismswithinthesoilsystem,withtheexceptionofnitrogenandcarbon.Feedbackcyclesexistbetweenthesoilbiotaandtheweatheringprocesswhereby,asweathering occurs, essential elements are released,aiding growth within the soil biota. This in turn addsto theweatheringprocessas thesoilbiota increasesweatheringrates.Fungi,particularlysaprotrophicandmutualisticfungi,havebeenshowntoincreaseratesofmineralweatheringandarethoughttobeimportantinweatheringatecologicalandevolutionarytimescales(Hofflandet al.,2004),andhenceinfluencethecyclesofseveralnutrientswithinthesoilsystem.Weatheringhasalsobeenshowntobeacceleratedbyearthworms,includingevidenceofthetransformationofsmectitetoillite(Carpenteret al., 2007).Thishighlightsthecriti-calrolethatsoilorganismsplaywithinsoil formationprocesses.

Waste recycling

Saprotrophicorganisms,alsoknownasdecomposers,usedeadorganisms,ordeadpartsoforganismssuchas leaves, tocarryouttheprocessofdecomposition.This is a heterotrophic process whereby the sapro-trophs get their energy and nutrients from organicsubstrates.Theprimarydecomposersarebacteriaandfungialthoughsomesoilinvertebratessuchasearth-wormsarealsodecomposers.

Othersoilinvertebratessuchasmillipedesandcollem-bolaareoftenincorrectlyreferredtoasdecomposers.Thesearemorecorrectlycalleddetritivoresastheyarenotable todigest thewiderangeofcompoundsthatfungi and bacteria are capable of digesting. Nor aretheycapableofdecomposingorganicmatterascom-pletelyasbacteriaandfungiandleavebehindorganicsubstanceswhichcanthanundergofurtherdecompo-sitionintoinorganicmaterial.

Bacteria are generally the primary decomposers ofdead organisms and fungi are generally the primarydecomposers of plant litter. When organic matterbecomes available, either in the form of dead organ-isms,faeces,orthroughadisturbanceeventreleasingpreviously inaccessibleorganicmatter,suchaswhenagriculturalfieldsaretilled,bacteriacanbecapableofrapidgrowthandreproduction,especiallyiftheorgan-icmattercontainsrelativelysimplechemicalbonds.

Fungiareabletodegrademuchmorecomplexchemi-calbonds including ligninandcellulose.Additionally,

8

asthemajorityofsaprotrophicfungigrowasabranch-ingnetworkofhypahetheyareabletopenetratelargerpiecesoforganicmatterasopposedtobeingrestrictedtogrowingonthesurface.Thegrowthoffilamentousfungiisaffectedbythespatialdistributionofsubstratewithinthesoil.Whensubstrateissparselydistributed,fungicanchangetheirforagingstrategytoexplorativegrowth,wherebytheygrowsparselyinordertoexploreaslargeanareaaspossibletoincreasethelikelihoodoflocatingsuitablesubstrate.Uponcontactwithasuit-ablesubstratefungicanchangetheirgrowthform,be-comingmuchdenserwhensuitablesubstrateisavail-able toprovidenutrients,allowing themtomaximizeuseoftheresourceinthecompetitivesoilenvironment(RitzandYoung2004).

Fungi usually dominate in forest ecosystems, wherethelitterismainlyplantbasedandsocontainsahighproportion of lignin and cellulose. However, due totheirfilamentousnature,mostsaprotrophic fungiareeasily damaged by physical disturbance events suchaswhenagriculturalfieldsaresubjectedtotillage.Forthisreason,bacteriagenerallydominateinagriculturalsystems.

Home for other organisms

One very important function of soils is as a habitatforotherorganisms.Whilemostpeopleareawareoflargeranimalswhichusethesoilasahome,suchasmoles, rabbits and foxes, many of these are thoughtofaspests.However,thesoilisalsoahomeformanyotherlessobviousorganisms,includinglarvalstageofgloballyimportantanimalgroupssuchaspollinators.Disturbance events, both anthropogenic such as till-age,andnatural,suchaserosionevents,can reducehabitatavailabilityfortheseimportantgroups.Pollina-tors are often keystone species for ecosystems, andtheirremovalcanleadtothecollapseofsomeecosys-tems(Bond2001).

Functional Redundancy

Thephenomenonoffunctionalredundancyreliesonthefactthatdifferentspeciesareabletoperformthesamefunctionalroleinangivenecosystem.Thismeansthatchangesinspeciesdiversitymaynotaffectecosystemfunctioningasotherspeciesareabletotakeoverthefunctionalroleofspecieswhichhavebeenlostfromtheecosystem.Functionalredundancyispossiblebecauseitoccurs through theoverlapof functionalprocessescarriedoutbydifferentorganismswhichinhabitdiffer-entniches.Thisisdifferentfromcompetition,whichiswheretwodifferentorganismscompeteforaresourcewhichisinlimitedsupply.

Oneexampleofaprocesswherefunctionalredundan-cymayoccurwithinanecosystemisnitrogenfixation.As supplies of nitrogen from the atmosphere are allbutinfinitefromtheviewpointofsoilmicroorganisms,thereisnocompetitionforthisresource.Theremaybeseveral diverse species of microorganism in the soilenvironmentfixingnitrogen, forexamplecyanobacte-

ria,Rhizobiumandsomeactinomycetes.Lossofoneofthosespeciesorgroupsoforganismswouldnotmeanthatthenitrogencyclestopswithinthatecosystemasotherorganismsarealsopresentandperformingthatrole. This means that there is functional redundancywith regard to nitrogen fixation within this exampleecosystem.

Tofurtherexplaintheconceptoffunctionalredundan-cy,considerthefollowingschematic.

Eachellipserepresentstherangeoffunctionsthatcanbeperformedbyonepartofagivensoilcommunity,beitacertainspeciesorgroupoforganisms.

Whilstsomefunctionscanbecarriedoutonlybyapartofthecommunity,overlapbetweenthefunctionsthateachgroupperformsexits.

If one part of the community is removed, then someofthefunctionsperformedbythatcommunityislost.However,duetotheoverlapinfunctionsperformedbydifferentcommunities,notallfunctionsarelost.ThisisFunctionalRedundancy.

However, it is important to note that some functionscarried out in soil have more functional redundancythanothers.Forexample:

a) High levels of functional redundancy exist. E.g. Breakdown of some forms of organic matter bymanyspeciesofsoilinvertebrates,fungiandbacteria.

a b c

8 9

b) Some levels of function redundancy exists.E.g.NitrogenfixationbyRhizobium, Cyanobacteria,ac-tinomycetes.

c) No Functional redundancy exists. Loss of this part of the community means completelossofthisfunction.E.g.breakdownofsomehighlyre-calcitrantorxenobioticcompounds.

Resistance vs. Resilience

Otherimportantconceptswhendiscussingtheeffectsof soil biodiversity on soil ecosystem functioning (orbiodiversityonecosystemfunctioningingeneral),aretheconceptsofresistanceversusresilience.

Resistance refers to a community’s ability to ‘resist’theeffectsofadisturbanceevent.Inasoilsystemthiscan includebothnaturalphenomenasuchasanero-sionevent,orbeanthropogenicsuchasapplicationofpesticideortillage.Thelevelofresistanceinthecom-munityisameasureofhowmuchecosystemfunction-ing is reduced following a disturbance event. A com-munity with high levels of resistance will be affectedlessbysuchaneventthanacommunitywithlowlevelsofresistance.

Resilience,ontheotherhand,referstoacommunity’sabilitytorecoverbacktopre-eventlevelsoffunction-ingafteradisturbance.Aresilientcommunitywillrela-tively rapidly regain pre-disturbance event levels offunctioningwhereasacommunitywhichhaslowlevelsofresiliencewilltakemuchlonger,ifindeediteverre-coverstopre-disturbanceeventlevels.

Itisimportanttonotethatthetwophenomena,resist-anceandresilienceareindependent,meaningacom-munitywithhighorlowlevelsofresistancemayhaveeitherhighorlowlevelsofresilience.

Forexample:

The above figure shows the effect of a disturbanceeventonthreedifferenthypotheticalsoilcommunities.CommunityAshowsrelativelyhighlevelsofresistancebut low levels of resilience and over the time frameshowndosenotrecoverbacktopre-disturbancelevelsoffunctioning.CommunityBshowsrelativelylowlevelsofresistance,butmuchhigherlevelsofresilienceandsoonafter thedisturbanceevent is functioningagainat pre-disturbance levels. Community C shows bothlowlevelsofresistanceandlowlevelsofresilienceanditspossiblethatthefunctioningofthiscommunitywilldramaticallyandpermanentlyreduced.

Thisdemonstrateshowanidenticaldisturbanceeventcanleadtoverydifferentoutcomeswithregardtodif-ferentsoilcommunitiesandhighlightsthedifficultiesandimportanceofhavingthemaximumamountofin-formation possible regarding a soil community whenattempting to assess the possible environmental im-pact of given disturbance event. Some systems willpossiblybeaffectedverylittlewhereasothersystemsmaybedramaticallyaffectedbythesamedisturbanceevent.

Leve

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Am

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Res

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Am

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=R

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Time

Disturbance event

C

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10

Soilbiodiversitycarriesarangeofvaluesthatdependontheperspectivefromwhichtheyarebeingconsid-ered.Theseinclude:

•Functional value,relatingtothenaturalservicesthatthesoilbiotaprovides,theassociatedpreservationofecosystemstructureand integrity,andultimately thefunctioning of the planetary system via connectionswiththeatmosphereandhydrosphere.

• Utilitarian (“direct use”) value, which covers thecommercialandsubsistencebenefitsofsoilorganismstohumankind.

•Intrinsic (“non-use”) value,whichcomprisessocial,aesthetic,culturalandethicalbenefits

•Bequest (“serependic”) value, relatingtofuture,butas yet unknown, value of biodiversity to future plan-etaryfunctionorgenerationsofhumankind.

Pimentelet al.,(1997)attemptedtocalculatetheeco-nomicvalueofbiodiversity, includingthatofsoilbio-diversity.Thiswasdoneusingrelativelyconservativeestimates and assumptions. Those processes whicharedependentonthesoilbiotaarelistedbelow:

Activity Soil biodiversityinvolved in such activity

World economy benefits of biodiversity (xs109/year)

Waste recycling Varioussaprohyticandlitterfeedinginverte-brates(detritivores),fungi,bacteria,actinomyc-etesandothermicroorganisms

760

Soil formation Diversesoilbiotafacilitatesoilformation,e.g.earthworms,termites,fungi,etc.

25

Nitrogen fixation Biologicalnitrogenfixationbydiazotrophbacte-ria

90

Bioremediation of chemicals Maintainingbiodiversityinsoilsandwaterisimperativetothecontinuedandimprovedeffec-tivenessofbioremediationandbiotreatment

121

Biotechnology Nearlyhalfofthecurrenteconomicbenefitofbiotechnologyrelatedtoagricultureinvolv-ingnitrogenfixingbacteria,pharmaceuticalindustry,etc.

6

Biocontrol of pests Soilprovidemicrohabitatsfornaturalenemiesofpest,soilbiota(e.g.mycorrhizas)contributetohostplantresistanceandplantpathogenscontrol

160

Pollination Manypollinatorsmayhaveedaphicphaseintheirlife-cycle

200

Other wild food Forex.mushrooms,earthworms,smallarthro-pods,etc.

180

Total 1.542

Thisconservativeestimateshowstheannualvalueofecosystemservicesprovidedbysoilbiodiversitytobe$1.5 trillion (Pimentelet al., 1997).Thisamount risesto$13trilliononceecosystemgoodsuchascropsandtimberareincluded(Constanza1997).Thisisapproxi-mately25%ofthecombinedglobalGDPof2007!(esti-matedtobe$54.3trillion:WorldBank2007).

This demonstrates the vast economic benefits of soilbiodiversity and its conservation. Preventing the de-cline of soil biodiversity must therefore be of para-mountimportance.Lossofsoilbiodiversityequatesto

alossofvalueofthesoilsystembywhicheverofthefourperspectivesareusedforevaluation.

Whilst any reduction in soil biodiversity may not im-mediatelyequatetoalossvalueduetothepreviouslydiscussed phenomena of functional redundancy, thismay still occur if levels of functional redundancy arelow. Even where levels of functional redundancy arerelativelyhigh,anylossofsoilbiodiversitywillreducethefunctionalredundancyofthesoilsystem,therebyreducingitsresistance,andsoleaveitmorevulnerabletofurtherlossofvaluethoughdisturbanceevents.In

The economics of Soil Biodiversity

10 11

someoftheworstcasescenarios,intheeventthatthelossofbiodiversity fromthesoil removesakeystonespecies(thatbeingaspecieswhichplaysacriticalroleinagivenecosystem),acollapseofmultiplefunctionsandconcurrentlossofecosystemservicesmayoccur,dramaticallyreducingthevalueofthesystem.

Thebiodiversityofthesoilsystemisclearlyofimmenseeconomicimportance.Thesoilecosystemisincrediblycomplex and is still far from being fully understood.

Caremustbetakenthatitsexploitationforshorttermeconomicgaindoesnotturnintoamassivelongtermeconomic(andecological)loss.Thiscanonlybedonewithconfidenceifwecompletelyunderstandsoilbio-diversity, its interaction with the soil system and theprocessescarriedout.Thishighlightstheneedforfur-therresearchinthisdepauperatebuthighlypertinentareaofscience.

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Agriculture is the science of cultivating soil, produc-ingcrops,andraisinglivestock.Sinceitsdevelopmentroughly 10,000 years ago, agriculture has achievedunprecedented progress and success, being able tofeed an ever increasing global population. Farmersthroughouttheworldhaverespondedtothechallengeofrisinghumanneedsbyincreasingthetotalandperarea production levels every year. This agriculturalmiracleisduetotheintensification,concentrationandspecialisation of agriculture, relying upon new tech-nologiesofagriculturalchemicals(fertilizersandpes-ticides), mechanisation, and plant breeding (hybridsandGMO’s).Modernagriculture,however,hasseveralundesirablesideeffects,oftenresultinginreduceden-vironmental quality and natural resources as well ashealthconcernsandeconomicinsecurityforthetradi-tionalfamilyfarm.Thishasledtowhatisknowntodayasaglobal“SustainableAgriculture”movement.

The most important negative effects of conventionalagricultureare,forexample:

• the indiscriminate use of pesticides and chemicalfertilizerswhichaffectshumanhealth,wildlifepopula-tionsandthequalityoftheenvironment;

•theexcessiverelianceonsyntheticfertilizers,andtheimproperuseanddisposalofanimalwastesisleadingtothebreakupofnaturalnutrientcycles,affectingalsowaterqualityandwildlifeinaquatichabitats;

•thetrendtowardlargerfarmsandplantation-typemo-noculturesisleadingtoalossofglobalbiodiversity;

• inadequate farming management practices can ledtheincreaseinsoilerosionrates,resultinginthelossofproductivefarmlandinmanypartsoftheworldandassociated off-site problems such as waterway con-tamination;

• unsustainable irrigation programs throughout theworld are resulting in a depletion of freshwater re-sourcesandinanundesirablebuildupofsalinityandtoxicmineral levels inoneoutoffivehectaresunderirrigation.

Sustainable agriculture represents a possible way toavoid,ortoreduce,theabovelistedimpacts.Inparticu-larsustainableagriculturereferstotheabilityofafarmto produce food indefinitely, without causing severeorirreversibledamagetoecosystemhealth.Asforthemoregeneralconceptof“sustainability”,threekeyis-suesareinvolved:environmental(thelong-termeffectsof various practices on soil properties and processesessentialforcropproductivity),socialandeconomical.Soilbiodiversityisessentialforagricultureandfoodse-curity and its proper management will aid agriculturebeingcarriedoutusingsustainablemethods.

Theidentificationoftherolesofthesoilbiotaonsoilfertilityregulationandplantproductionhasbeendif-ficult(Anderson,1994),andstillmanyofthefunctionsassociatedtodifferentgroupsareunknown.Thisisof-tenduetoscaleproblemsinresearch,wherecropper-formanceismeasuredatplotscaleandoveragrowingseason,whichintegratesacross(andthusdilutes)thegenerallysmallerscale,shortertermspecificeffectsofthesoilbiota(Lavelle2000).Inaddition,it isdifficulttodetermine thevarious interactionsbetweenaboveandbelowgroundbiodiversity.Nevertheless,thereareexamplesofbothpositiveandnegativeeffectsofsomefunctional groups, particularly microorganisms, phy-toparasites/pathogensandrhyzophages,plantroots,andmacrofaunaonplantproduction.

Thebeneficialeffectsofsoilorganismsonagriculturalproductivityandecologicalfunctioninginclude:

•organicmatterdecompositionandsoilaggregation;

•breakdownoftoxiccompounds,bothmetabolicby-productsoforganismsandagrochemicals;

• inorganic transformations that make available ni-trates,sulphates,andphosphatesaswellasessentialelementssuchasironandmanganese;

•nitrogenfixationintoformsusablebyhigherplants.

Organic matter cycling and humification

Thedecompositionandtransformationoforganicmat-ter in terrestrial ecosystems relies essentially on soilorganisms.Thiscatabolicprocessiscomplementarytophotosynthesis,andintermsofecosystemsservices,has comparable importance. In other words, we canconsiderthe“recycling”activityofthesoilbiotatobeasimportantastheproductionofneworganicmateri-als.

Decompositioninvolvesthephysicalfragmentationoforganic matter, generally operated by small inverte-brates,butalsothechemicaldegradation,transforma-tion and the translocation of organic substrates. Thephysicaldecompositionisthefirstphaseoftheproc-essanditisfollowedbytheactionofenzymesmainlyproducedbysoilmicroorganisms.

From the transformation of the organic matter in thesoil,apeculiarclassoforganicsubstancesisproduced:thehumus.Thisbroadandheterogeneouscategoryoforganic compounds is not only a long term reservoirofsoil fertility,butalsoplaysanessential role in thecreationandstabilisationofsoilstructure,andintheregulationofsoil-waterinteractions.

Soilmacrofauna,especiallyearthworms in temperateregions,haveanimportantimpactonsoilorganicmat-

Soil Biodiversity & Sustainable Agriculture

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terdynamicsandnutrientcyclingislargelydeterminedbytheirdensityandbehavior(Lavelleet al.1997).Evenamongasinglegroupofsoilorganisms,suchasearth-worms,therecanexistvastlydifferentfeedingandliv-inghabits.Forexample:epigeicspeciesfeedandliveon the surface of soil and in the litter; aneic speciesfeedonthesurface,butliveintothesoil,buildinglargegallerynetworks;andendogeicspeciesliveandfeedwithinthesoil.

Fertility regulation and nutrient uptake

Chemical fertilitycanbedefinedastheavailabilityofnutrientsessentialfortheplants.Soilmicroorganismsplaya fundamental role insoil fertility regulation, in-creasingplantavailablenutrients,especiallynitrogenandphosphorus,andhavebeendemonstratedrepeat-edlytohavepositiveimpactsoncropyields.

Nitrogen,whichisoftenthelimitingfactorforagricul-turalproductivity,canbefixedbyseveralgroupsofsoilmicroorganisms, both symbiotic and non-symbiotic.Symbioticnitrogenfixation,operatedbybacteriaandactinomycetes, can be as high as 400 kg N ha-1 yr-1,whiletheamountofnitrogenfixedbyfreelivingbacte-riaisgenerallymuchlower.

Mycorrhizaaretheresultsofsymbiosisbetweenspe-cific soil-borne fungi and the roots of higher plants.Therearetwomaintypesofmycorrhizaknownasen-domycorrhiza and ectomycorrhiza (Smith and Read1997). Endomycorrhiza, commonly known as arbus-cularmycorrhizalfungi(AMF)physicallypentratetherootsofhigherplantsandcandirectlyaffectacquisi-tionofnutrients,suchasphosphorus,nitrogen,calci-

umandmagnesium.Thissymbiosisgenerallyenablestheplantto“explore”ahighervolumeofsoil,increas-ingthemineraluptakeseveralfold.Forexample,aninvestigation carried out on sorghum demonstratedthattheplantscanincreasethePuptakemorethanfivetimeswhenAMFarepresentattheroots(Marsh-ner1995).

The appropriate management of the soil biota is es-sentialforsustainableagriculture,wherethelimitationofexternalinputsisoneofthefundamentalprinciples.Research carried out in India has shown that the ap-propriate management of the organic materials andsoilorganisms(in thiscaseearthworms),can leadtoadramaticincreaseinteayieldsandinprofitabilityofthecrop(Senapatiet al.1999).

Pest and disease control

Plantpestsanddiseaserepresentanenormousprob-lem for agriculture production, causing both quanti-tative and qualitative damages to crop productions.MonetarylossesduetosoilbornediseasesintheU.S.areestimatedtoexceed$4billionperyear(Lumsdenet al., 1995),and lossesdue toparasiticnematodesexceed $8 billion per year (Barker et al., 1994). Fur-thermore, the cost of soil borne plant pathogens tosociety and the environment far exceeds the directcoststogrowersandconsumers.Theuseofchemicalpesticidestocontrolsoilbornepathogenshascausedsignificant changes in air and water quality, alterednaturalecosystemsresultingindirectandindirectaf-fectsonwildlife,andcausedhumanhealthproblems.

Plantdiseasesmayalsooccurinnaturalenvironments,buttheyrarelyrunrampantandcausemajorproblems.Incontrast,thethreatofdiseaseepidemicsincroppro-ductionisconstant.Thereasonsforthisarebecomingincreasinglyevident.

Plant diseases result when a susceptible host and adisease-causingpathogenmeetinafavorableenviron-ment.Ifanyoneofthesethreeconditionsisnotmet,diseasedoesnotstartorspread.Ahealthysoilcom-munityhasadiversefoodwebthathelpstokeeppestsanddiseaseundercontrolthroughcompetition,preda-tionandparasitism(Susiloet al.2004).

Soil-borne diseases often result from a reduction inthebiodiversityofsoilorganisms.Restoringbeneficialorganismsthatattack,repel,orotherwiseantagonizedisease-causingpathogenswillrenderasoildisease-suppressive. Plants growing in disease-suppressivesoilresistdiseasesmuchbetterthaninthosegrowinginsoilswhichhavealowbiologicaldiversity.Beneficialorganismscanbeaddeddirectly,or thesoilenviron-ment can be made more favorable for them, throughcorrectagronomicmanagement.

Soil structure and soil-water relationships

Agoodandstablesoilstructureisoneofthemainob-jectives of farmers. A favourable soil structure facili-tatesthegerminationandtheestablishmentofcrops,

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helps to prevent water logging, reduces the risks ofwatershortageanddroughtandmaximisesresistanceandresilienceagainstphysicaldegradation.

Soilstructure, thearrangementof theelementalpar-ticlesofthesoil,ismediatedbyorganicandinorganicsubstances (microstructure) and by living organismsactivities (meso and macrofauna burrowing, rootgrowth,etc.)orstructures(rootsandfungalhyphae).

Soil macrofauna also play an important role in soilstructure modification, through bioturbation and theproduction of biogenic structures. It is essential tohave a suitable balance between organism buildingandbreakingbiogenicstructures, inorder topreventsoil degradation processes, such as soil compaction(Barrios2007).

Theactivityofsoilmacrofaunacanhaveanimportantinfluenceonwaterandnutrientsdynamic. InaseriesofexperimentalactivitiescarriedoutinBurkinaFaso,Mando et al. (1996) and Mando and Miedema (1997)showed that by managing the application of organicmulchandmanure to thesurfaceofcrustedsoil sur-faces, itwaspossibletostimulatetheburrowingandfeedingactivitiesoftermites.Theholescreatedinthesoilsurfacehelpedpreventrunoffandaidedwaterin-filtration. It has also been demonstrated that the notillage or minimum tillage management schemes, bypromoting the activity of soil engineers, can improvethesoilphysiccharacteristics.

Pollination

Two-thirdsof theworld’scropspeciesdependon in-sectsforpollination,whichaccountsfor15to30per-cent of the food and beverages we consume. FrenchandGermanscientistshaveestimatedthattheworld-wideeconomicvalueofthepollinationserviceprovided

byinsectpollinators,mainlybees,was€153billionin2005forthemaincropsthatfeedtheworld.However,theservicesprovidedbypollinatorsarenotlimitedtoagricultureproductivity.Theyarealsokeytothefunc-tionofmany terrestrialecosystemsbecause theyen-hancenativeplantreproduction.

Several pollinating insect species (belonging to Hy-menoptera, Coleopteraandotherinsectorders),spendapartoftheir lifecycle intothesoil.Americannativebees, for example, are among the most importantcrop-pollinatingspeciesandhave threebasichabitatneeds:

•Theymusthaveaccesstoadiversityofplantswithoverlappingbloomingtimes.

•Theyneedplacestonest.Mostnativebeesaresoli-tary, and none build the wax or paper structures weassociatewithhoneybeesorwasps,butnestinsmallwarrens of tunnels and cells which they construct inthesoil.

•Theyneedprotectionfrommostpesticides. Insecti-cidesareprimarilybroad-spectrumandare thereforedeadlytobees.Furthermore,indiscriminateherbicideusecanremovemanyoftheflowersthatbeesneedforfood.

Thisdemonstratesthepositiveinteractionthatcanbeestablishedbetweensoilbiodiversityandsustainableagriculture. Sustainable agriculture, thanks to limita-tionsintheuseofxenobioticcompoundsandexternalinputs, ensures a higher level of soil biodiversity. Atthesametimetheservicesprovidedbymorecomplexandhealthysoilcommunities,feedbackandenablethefurtherreductionofexternalinputsneededbyagricul-ture.Soilbiodiversityisthereforeofvitalimportanceinincreasingthesustainabilityofagriculture.

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Thehighlevelsofbiodiversityfoundinthesoilsystemincludesorganismswhichperformawiderangeofeco-logicallyimportantfunctions.Soildwellingorganisms,aswithabovegroundorganisms,mustcompeteforre-sources,andtrytoavoidbeingpreyuntiltheymanageto reproduce. The consequences of this is that thereare many evolutionary “arms races” occurring withinthesoilsystem.This,combinedwiththehighlevelsofdiversity, means that there are an array of functionsandcompoundswithinthesoilsystemwhichcanbeuti-lizedforbiotechnologicalapplications,andpotentiallytherearemanymorefunctionsandcompoundswhichcouldbeusefulwhichareyettobediscovered.Forthisreason,anactiveareaofsoilbiologicalresearchisthatofbiotechnology.Theseareasofbiotechnological re-searchgenerallyfallintooneormoreofthefollowingareas.

Bioremediation

Thesoilbiotaishometomanydifferentdecomposers.Theseareheterotrophicorganismswhichbreakdownorganicsubstancestogainenergyandindoingsore-cyclecarbonandnitrogenbackintotheenvironment.However,thisprocesscanalsobeutilizedasaformofbiotechnologyknownasbioremediation,whichistheprocessofusingorganisms(“bio”)toreturnacontami-nated area back to its pristine state (“remediation”).Despite this broad definition, most bioremediation isactually undertaken through the use of microorgan-ismsduetotheirabilitytoutilizeavastrangeofcarbonsourcesasasubstrate.

Different soil decomposers are capable of degradingdifferenttypesoforganicsubstance.Some,compoundsarenotrecalcitrantandsoaresusceptibletodecompo-sitionbyarangeoforganisms.Othercompounds,suchasligninandcellulosearehighlyrecalcitrantandonlysusceptibletobreakdownbutafewselectorganisms;brownrotfungiinthecaseofligninforexample.Thismeansthatsomenon-recalcitrantpollutantsmayonlylastashortperiodoftimeintheenvironmentandbebroken down without human intervention. However,manyorganicpollutantsarecomposedoflongchainsofcarbonandhydrogenandcanbestructurallysimilartocomplexorganiccompoundssuchas lignin.Thesecompoundsgenerallylastmuchlongerintheenviron-mentbutthesimilaritiesinstructuremeansthatfungicanoftenbeusedforthebioremediationofmanytypesofcompounds,thekeybeingdeterminationofthecor-rectfungalspeciesfortheeffectivebioremediationofagivencompound.Theincrediblediversityofbacteriameansthereareoftentypesofbacteriacapableofde-gradingcontaminantstoo.Againdeterminingthecor-recttypeofbacteriaforagivencontaminantisneces-saryformaximumeffectivenessofbioremediation.

Bioremediationoccurs,or isundertaken in, threedif-ferentforms:

•Intrinsic Bioremediation: thisprocessoccursnatu-rallyincontaminatedsoilorwaterandiscarriedoutbymicroorganismslivingatthesiteofthecontamination.Noadditionalorganismsornutrientsarerequired.

• Biostimulation: in this process, nutrients and/oroxygen are added to contaminated soil (or water) toencouragethegrowthandactivityofthemicroorgan-ismslivingatthesiteofthecontamination.

• Bioaugmentation: is the process of adding organ-isms,generallymicroorganismstosoil(orwater)toaidtheintrinsicbioremediationortointroduceorganismscapableofdegradingacontaminantwhichtheintrinsicpopulationisunableto.

Bioremediationcanbehighlyeffectiveinremovingcon-taminantsfromaffectedsites.Inonecaseanestimated38,000m3ofsoilinCanadawascontaminatedwithanoil-tarbyproductcontainingpolycyclicaromatichydro-carbons,cyanide,xylene,tolueneandheavymetalsbyagasificationplant.Afterapplicationofabacteriaandnitrogennutrientmix(acombinationofbiostimulationandbioaugmentationtechniques),thevariousconstit-uentpollutantsoftheoiltarwerereducedby40-90%injust70-90days(Warithet al.1992).

Antibiotics

Thesoilcontainsacomplexarrayoffoodwebsandin-teractions between the diverse groups of organismsfoundthere,withorganismspredatingeachotherandcompeting for resources,andassuchahostofproc-esses forbothattackandsurvivalhaveevolved.Oneoftheseistheuseofchemicalsubstancesinaformofchemical“warfare”betweensoilorganisms.Itissomeof these chemicals which, when isolated, we use formedicinalpurposesasantibiotics.

Antibiotics isolated from soil organisms include (butarenot limitedto):penicillin, isolatedfromthepeni-cillinfunguswhichisfoundinsoilsandwhich,alongwithseveralsemi-syntheticderivatives,isstillinwide

Soil Biodiversity and biotechnology

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use.Aminoglycosides,suchasstreptomycinandkan-amycin,aswellastetracyclineswereisolatedfromsoildwellingactinomycetes.Lipopeptidessuchasdapto-mycin have also been derived from Steptomyces, atype of actinomycete. Each of these antibiotics hasa different mode of action. Some attack the cellularmembranes,whereasothersattack the ribosomeorother cellular constituents. It is for this reason thatsome organisms are susceptible to some antibioticsbutnotothers,dependingonwhether theyhavethespecificformofcellularconstituentwhichtheantibi-oticattacks.

Antibiotic resistance

As well as not being susceptible to some antibiotics,microorganismsarealsooftencapableofdevelopingresistanceover time.Whilst this isoftenviewedasaproblemforclinicalmicrobiology,precedentsforvari-ousmodesofantibioticresistanceseenintheclinicalenvironmentcanoftenbefoundinthesoilenvironment.Thisisbecausesoilmicroorganismsareoftenexposedto a wide range of compounds in their local environ-ment, some of which may be harmful such as antibi-otics,andthisplacesanevolutionarypressureontheorganismstodevelopresistanceortogoextinct.It isalsonecessarythatantibioticproducersmustcontainsomeantibioticresistancemechanismsforexample,toprevent them committing suicide through productionoftheirownantibioticcompounds.

The soil environment therefore represents an impor-tantpoolforresearchintotheunderlyingmechanismsofantibioticresistance,includingpossiblemechanismswhicharenotyetseeninclinicalmicrobiology.Utilisa-tionofthisresourcetobetterimproveourunderstand-ingofthebiochemicalprocessesoccurringmayallowthe circumnavigation or reduction of further antibi-oticresistancedeveloping.Thisisanareaofresearchwhich is just starting to gain prominence (D’Costa et al., 2006; Tomasz 2006). Evolution has even takenantibiotic resistance one step further. Danatas et al., (2008) demonstrated that out of 18 antibiotics thattheytested,from8majorclassesofantibioticofbothnatural and synthetic origin, 13 to 17 supported thegrowth of bacteria when the antibiotic was availableasthesolecarbonsource.Microorganismsareclearlyhighlyadaptable, inwayswhichweareonly recentlycomingtounderstand.

Antibiotic resistance occurs because antibiotics pro-vide an evolutionary pressure on a given populationwherebythoseorganismswithnaturalresistancecansurviveandreproducewhereasthoseorganismswhichdo not have the resistance factor die. Once a resist-ancefactorhasdevelopeditcanspreadrapidlywithina population or even a community though horizontalgenetransferwhereDNAistransferredfromonebacte-riumtoanother.TransferofDNAcontainingantibioticresistance genes (as well as other genes) can occurthroughthreeprocesses:

• Transformation. When a bacterium dies and lyses(splitsopen),otherbacteriawhichareactively-growingincloseproximitycanpickupitsDNA.

• Transfection. Phage, which are viruses that infectbacteria and fungi, sometimes pick up extra genesfrom the microorganisms that they infect which arethenpassedontootherorganismswhichtheyinfect

•Conjugation. Bacteriacanfusetheircellmembranestogetherandexchangeplasmidsorfragmentsoftheirchromosomes

Theseprocessescanoccurbetweendistinct ‘species’ofbacteriameaningthatmechanismsofantibioticre-sistance may only have to evolve once and can thenspreadthroughoutanentirecommunity.

Biocontrol of pests

Biocontrolofpests is theuseofnatural ‘enemies’asbiologicalcontrolagents,suchaspredators,parasitesorpathogens,tocontrolorreducethepopulationofagivenpest. It isoftenusedasanalternativetopesti-cideuse.Broadspectrumpesticideusecanbehighlyproblematic as they often act on insects which arebeneficial to crops as well as harmful insects. Thereisalsoapossibilityof thesechemicalsbeingwashedinto groundwater or any nearby waterways causingcontamination.Biocontrolisonemethodwhichcanbeusedtoreducetheneedforlargescaleapplicationsofbroadspectrumpesticides.

When the pest is a pathogen, such as in the case ofplantdiseases,thenthebiologicalcontrolagentisof-ten referred to as an ‘antagonist’. Biological controlgenerally falls into three different types of strategy,referredtoas:

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•Conservation,wherecareistakensothatnaturalbio-logicalcontrolagentsarenoteradicatedbyotherpestcontrolprocesses;

•Classical biological control,whereabiologicalcon-trolagentisintroducedintoanareatocontrolapestspecies

•Augmentation,whichinvolvesthesupplementalre-leaseofabiologicalcontrolagent.Itisoftenthisthirdtype of biocontrol which utilizes the soil biota. Forexample,entomopathogenicnematodesareoften re-leasedatratesofmillionsorevenbillionsperacreforcontrolofcertainsoil-dwellinginsectpests

Kerr (1982) listed that the idealbiocontrolorganismsshouldincludethefollowingcharacteristics:

1.Theorganismshouldsurviveforanextendedperiodoftimeinthesoilinaninactiveoractiveform.

2. Theorganismshouldcontactthepathogeneitherdi-rectlyorindirectlybydiffusionofchemicals.

3. Multiplication in the laboratory should be simpleandinexpensive.

4.Itshouldbeamenabletoasimple,efficientandin-expensive process of packaging, distribution and ap-plication.

5.Ifpossible,itshouldbespecificforthetargetorgan-ism;themorespecificitis,thelessenvironmentupsetitwillcause.

6. Itshouldnotbeahealthhazardinitspreparation,distributionandapplication.

7. It should be active under the appropriate environ-mentalconditions.

8.Itshouldcontrolthetargetpathogenefficientlyandeconomically.

Soilbiodiversityclearlyhasmanymorecurrentandpo-tentialusesforbiotechnologyandthisisanareaongo-ingareaofresearch.Onethingisclear,foreveryorgan-ismwhichgoesextinctinthesoilenvironment,aswithotherecosystems,someasyetundiscoveredbiotech-nologyisalsopotentiallylost.Itisvital,therefore,thatsoilbiodiversityisconservedasmuchasisreasonablypossibleandthattheawarenessofthisneedisraisedwithinthescientificcommunityandpublicingeneral.

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Microorganisms have been found pretty much every-wherewehavelooked.Thisencompassesavastrangeof environments including relative extremes in tem-perature,moistureregimeandsolar radiation.Whilstmicroorganismshavebeenfoundflourishinginplacessuchasboilingvolcanicsprings,thesoilenvironmentcanalsobeaveryextremeenvironment.Soilcommu-nities have been found in many harsh environmentson Earth, from freezing Antarctica to baking deserts,including areas of extreme dryness, and exposure toUV. Communities found in such environments oftenexistatrelativelylowlevelsofbiodiversity.Theselowlevels of biodiversity can facilitate research as it canoftenbepossibletobetterelucidateinteractionsandtherelationshipsbetweenorganismsandtheirphysi-cal and chemical environments. Results and insightsfromthesesystemscanthenbeappliedtomorecom-plex systems, such as those found in soil systems intemperateandtropicalregions.

Therelativelylowlevelsofbiodiversitygenerallyfoundin extreme environments means that communitiesoften contain little or no functional redundancy. Thismeansthattheycanbeparticularlysusceptibletodis-turbance events and the removal of a vital functionfromthecommunitycanhavedramaticconsequencesforotherorganismsofthecommunitypossiblyleadingto largechanges incommunitycompositionandeco-systemprocessrates(WallandVirginia1999).

Temperature

Hot

DeathValleyisoneofthehottestplacesonEarthwithdaytimetemperaturesoftenexceeding45°Cduringthesummermonths,andtherearereportsof thegroundtemperaturereachingover93°C(Douglas2006).How-ever, although the soil biodiversity in Death Valleysoil is greatly diminished when compared to temper-atesoilsforexample,thereareextremophilicbacteriawhichthriveeventhere.

Microorganisms in hot deserts have been shown tostillfunctionregardinggeochemicalcycling.Walvoordet al.(2003)reportedthatalargereservoirofbioavail-ablenitrogen(upto104kilogramsofnitrogenperhec-tare,asnitrate)hasaccumulatedinthesubsoilzonesof hot deserts. Natural sources of nitrate in desertecosystems includesconversion fromatmosphericN

2

by N-fixing organisms as well as nitrate in precipita-tion,eoliandepositionofnitratesalts,(Walvoordet al.2003).Thisdemonstratesthatecosystemfunctioning,drivenbymicroorganisms,stilloccursevenintherela-tivelyextremetemperaturesexperiencedinthedesertenvironment.

Cold

AntarcticsoilsarethecoldestonEarth(CampbellandClaridge 1981). Mean monthly air temperatures forsome areas of Antarctica only rise above 0°C duringDecember and January and don’t rise above -20°C inJuly and August (Delille 2000). These soils representthe only known soil system where nematodes repre-sentthetopofthefoodchainandassuchtheirfoodwebsareunusuallysimple.

Asnematodesareaquaticanimals,soilwaterisamoreimportantfactoraffectingtheirsurvivalthanthecold.However,nematodesareabletoenteraformofcryp-tobiosis–beingastateinwhichallmetabolicactivityinanorganismisstopped–knownas“anhydrobiosis”whichisastateenteredintobysomeorganismsintheabsenceofwater.Organismsinthisstateareextreme-lyresilientandareabletosurviveforextendedperiodsuntilconditionsbecomefavourableonceagain.Inthisstatenematodesdonotfunctionwithregardstothecy-clingofnutrientsandthis,combinedwiththerelativelyslowmetabolicactivatesofmicroorganismsinthecoldtemperatures,andthelackofmetabolicactivityduringthecoldestmonths,contributestoanextremelyslowrateofnutrientcyclingintheAntarcticenvironment.

Microarthropods in extreme cold environments suchas that found in Antarctica survive subzero tempera-turesthroughtheuseofavarietyofstrategies.Theirbodyfluidsarekeptinaliquidstatethroughtheuseofcarbohydratecryoprotectantsandinsomecasesalsothroughtheuseofantifreezeproteins.Theseareaidedby the removal or masking of ice nucleating agentswithin their body fluids (Sinclair and Stevens 2006).These strategies prevent the freezing of bodily fluidsandconcurrentcellulardamagethatthiswouldcause.

Dry

AswellasbeingthecoldestsoilsonEarth,Antarcticais also home to the driest soils in the McMurdo DryValleys.OutsideofAntarctica,thedriestplaceontheplanetistheAtacamaDesertofChile.Here,someareasreceive less than5mmof rainfallperyearand therecanbedecadeswithnorainatall(Warren-Rhodeset al. 2006). However, limited levels of biodiversity arestillfoundhere.Inareaswithlessthan75hoursayearofavailableliquidwater,cyanobacteria,whichareca-pableofphotosynthesis,arestill found.Thisappearstobethelimitofphotosynthesiswithregardtowateravailability.Duetotherestrictionsonphotosynthesisandmetabolismimposedbythesevererestrictionsofwater,ithasbeenestimatedthatorganiccarbonwithinthesoilcommunitiesfoundinthisenvironmenthasaturnover time of 3,200 years (Warren-Rhodes et al.2006).Thiscomparedtoturnoverratesofgener

Soil Biodiversity at the extreme

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ally less than 100 years in arable soils (Yamashita et al.2006).

Solar radiation

Solar radiation is confined to the extreme surface ofsoils.Ithasbeendemonstratedthatevensandysoilswhichhaverelativelylargeporesonlyallowthetrans-mittanceof0.3%ofsolarradiationdownto2mmdeepandthistransmittanceisreducedtojust0.2%at1mmdepthinasiltyclaysoil(Benvenuti1995).

While light is vital for photosynthetic organisms, re-strictingphotosynthesistotheextremesurfaceofthesoilsystem,solarradiationalsocontainsUVwhichisharmfultolife.Hugheset al.(2003)demonstratedthatUV radiation inhibited the growth of fungal hyphae,withtheinhibitionofgrowthincreasingwithdecreas-ingwavelength.

Organismswhichareexposedtosunlightnormallypro-ducepigmentstoprotectthemselvesfromtheharmfuleffectsofUV.Forexample, increasedmelanisation iswitnessedincollembolawhichdwellnearertothesoilsurfaceasadirectcorrelationtotheirincreasedexpo-suretoUV(Hopkin1997).

Perhapscounterintuitively,Arrageet al.(1993)demon-strated that many of the subsurface microorganismstheystudiedexhibitedthesamelevelsofUVresistanceas surface microorganisms. This is perhaps a conse-quenceofthehighlydynamicnatureofthesoilsystem

meaningthatanysoilmicroorganismscannot‘rely’onbeingprotectedfromUVandmaybecomeexposedaf-ter erosion events. In order to survive such events itisnecessaryforsubsurfaceorganismstopossessthenecessaryprotectivemechanismseveniftheyarenotutilizedforthemajorityofthetime.

Mechanisms for coping with extremes

Cryptobiosis

Thecryptobioticstateischaracterisedbyanundetec-table metabolism and the induction of physiologicaland morphological changes in the organism. Someorganisms, including many species of bacteria andnematodes,areabletoenteracryptobioticstateatanystage during the lifecycle when environmental condi-tionsbecometooharshtosupportactivelife.

Organismsinthecryptobioticstatebecomeextremelyresistant to environmental conditions. Nematodes inthisstate,forexample,havebeenshowntoberesist-anttoextremelylowtemperatures,desiccationwheretherelativehumidityreaches0%,vacuumandnemati-cides.However,theyarestillabletoquicklyrevivetoanactivestatewhenfavourableenvironmentalcondi-tionsreturn(FreckmanandWomersley1983).

Use of proteins

Proteins have been shown to be able to function toprotectorganismsfromextremesofeitherheatorcold.Proteinswhichhelpprotectorganismsfromtheeffectsofheatarecalledheatshockproteins.Theseproteinsfunctionas‘chaperones’tootherproteins,aidingtheirfolding and helping to prevent denaturation whichwouldotherwisebecausedbytheheat.

Conversely, proteins which help protect organismsfromthecoldarecalledcoldshockproteins.Themodeoffunctionofcoldshockproteinsis lesscertainthanthatofheatshockproteins,butitappearsmanyareca-pableofbindingtoDNAandsopossiblyaidtheorgani-zationofthechromosomesoractasRNA‘chaperones’.Someorganismswhichareabletosurviveinsubzeroenvironmentsarealsocapableofproducingantifreezeproteins.Thesefunctionbybindingtoanyicecrystalswhichformandinhibitingtheirgrowth.

Cyst formation

Many microorganisms, including bacteria, protozoaand fungi are also capable of undergoing a processcalled‘encysting’inwhichtheyform‘cysts’.Cystsarebasically dormant and resilient forms of the organ-ismscharacterisedbyverylittleornometabolismandthickercellswalls.Cystsaremoreresilienttoextremesof temperature, pH and desiccation. Once conditionsagain become favourable, the organisms are able tocomeoutoftheircystformandagainstartmetaboliz-ing,growthandreproduction.

20

Climatechangeanditspossibleeffectsiscurrentlyanareaofintensiveresearch.Theglobalsystemisincred-iblycomplexwithavirtuallyinfinitenumberofinterac-tionsoccurringatdifferenttemporalandspatialscales.Whilea reductionistapproachtounderstandingsuchalarge,complexanddynamicsystemisnotpossible,gaining a better understanding of the functions oc-curring inmanyofthedifferentecosystemsfoundontheplanetandtheirimplicationsforclimatechangeisclearlyveryimportant.

Soil is one system which has the potential to have amassiveinfluenceonclimatechangeduetothelargeamountsofcarbonstoredthere,morethantwicetheamountpresent intheatmosphere,whichisfoundinthesoilsystemintheformoforganicmatter.

Carbon dioxide is continuously removed from the at-mospherethroughphotosynthesisbyplantsandotherphotosyntheticorganismssuchasalgaeandcyanobac-teria.However,itisalsogenerallybeingemittedfromsoilsasthecarbonwhich ispresent insoil isutilizedas an energy source with CO

2 being emitted as a by-

productofrespiration.This is theessenceof thecar-boncycle,albeitinhighlysimplifiedform.

This is a schematic representation of the Carbon Cy-cle:

Although this figure is also simplified, the numbersareallwellestablishedandrelativelyuncontroversial.Figure1showsisthatifallinputsofcarbonintosinksareaddedtogether thetotalamountofcarbongoingintosinksfromtheatmosphereis213.35Gtperyear.

Conversely,whenallofthecarbonemittedintotheat-mospherefromnon-anthropogenicsourcesareadded,theytotal211.6Gtperyear.Thisequatestoanetlossofcarbonfromtheatmosphereof1.75Gtcarbon.ItisforthisreasonthattherelativelysmallfluxofCO

2from

anthropogenicsources(5.5Gtperyear)isofsuchlargeconsequence as it turns the overall carbon flux fromtheatmospherefromalossof1.75Gtperyear,toanet gainof3.75Gtcarbonperyear!

The Impact of Soil Biodiversity on CO2

The feedback between soil carbon and atmosphericCO

2 is a process which is still not fully understood.

However, it is generally accepted that the soil biotaplaysthedominantpartinthisinteraction.Soilbiologi-calprocessesthereforecanclearlyhavealargeeffecton theglobalcarboncycle.This isbecausesoilscur-rentlycontainapproximatelytwicetheamountofcar-bonasisfoundintheatmosphere,andfluxestotalinginthehundredsofgigatonnesofcarbonoccurbetweenthesoilandtheatmosphereonanannualbasis.Acom-pleteunderstandingoftheCarbonCycleisvital inin-creasingourunderstandingofthefeedbackofcarbonbetween thesoiland theatmosphereand if,orhow,thismaybecontrolled.

Bellamyet al. (2005)foundthatanestimated13milliontonsofCarbonarelostfromUKsoilsannually.Thisistheequivalentto8%oftotalUKcarbonemissions.Aslossesofsoilorganiccarbon (SOC)were found tobeindependentofsoilproperties,thishasleadtothefor-mationofthehypothesisthatthestabilityofSOCisde-pendentontheactivityanddiversityofsoilorganisms(Schulze&Freibauer2005).Thereisevidence,howev-er,thatsoilsfunctionasasinkforCO

2insomeareasas

morecarbonisputintothesoilsystemthroughphoto-synthesisthanisremovedviarespiration.

Studiesatdifferentlatitudeshaveshownthattherateofsoilorganicmatterdecompositiondoublesforevery8-9°C increase in mean annual temperature (Ladd et al., 1985).Whilethis isgreater thanthepredicted in-creasesduetoclimatechange,allotherthingsbeingequal, it is apparent that increased global tempera-tureswillspeedupsoilorganicmatterdecompositionrates.ThisthenhasthepotentialtofeedbackintoevengreaterlossesofCO

2fromsoil.

Soil biodiversity can also have indirect effects as towhethersoilfunctionsasacarbonsinkorsource.Ithasbeendemonstratedrepeatedlythatsoilbiodiversityaf-fectstheerodibilityofasoilduetoanumberofmecha-nismsincludingextracellularexudates,andphysicallybindingsoilparticlestogetherwithfungalhyphae.Thisprocessisimportantwithregardtoclimatechangeasithasbeenshownthatsoilerosioncanturnsoilfromcar-

Schematic showing the carbon cycle highlighting both quantities of carbon stored in, and fluxes of carbon moving between different global systems. Source: NASA (2008) http://earthobservatory.nasa.gov/Features/CarbonCycle/carbon_cycle4.php

Soil Biodiversity and Climate Change

Vegetation 610

Marine Biota

Dissolved OrganicCarbon < 700

Deep Ocean38.100

Fossil Fuels &Cement Production

4.000

RiversSolis 1.580

Atmosphere 750

Storage in GIC

Surface Ocean 1.020

Fluxes in GIC/yr

CO2

60

50

64

6

90

92

40 10091.6

60

1.6

121.30.5 5.5

20 21

bonsinktoacarbonsource(LalandPimentel2007).However,howlargeaneffectthisisremainscontrover-sialandisanareaofongoingresearch.

The impact of Soil Biodiversity on other Greenhouse Gases

Methane(CH4)productionalsooccursasapartofthe

carboncycle.Itisproducedbythesoilmicrobiotaun-deranaerobicconditionsthroughaprocessknownasmethanogensis. Methane is about 21 times more po-tentasagreenhousegasthancarbondioxide.

Nitrousoxide(N2O)isproducedasapartofthenitro-

gencyclethroughprocessesknownasnitrificationanddenitrificationwhicharecarriedoutbythesoilmicrobi-ota.Nitrousoxideis310timesmorepotentasagreen-housegasthancarbondioxide.

Ofthetotalsemitted,80%ofN2Oand50%ofCH4emit-

ted fromareproducedbysoilprocesses inmanagedecosystems.

Whilstthesegasesarepotentiallymorepotentgreen-housegasesthanCO

2,onlyapproximately8%ofemit-

ted greenhouse gases are CH4 and only 5% are N

2O,

with CO2 making up approximately 83% of the total

greenhousegasesemitted.Theactualpercentagecon-tributionofthesegasestoglobalwarmingcanbeseeninthefigurebelow(Source:USEPAInventoryofGreen-houseGasEmissionsandSinks).

Thisprovidesstrongevidencethatthesoilsystemhasthepotentialtoplayaveryimportantroleineithercaus-ingorhelpingtomitigatetheeffectsofclimatechange.Itisthereforeveryimportantthatwefullyunderstandthe soil system, and its feedback with greenhousesgasesintheatmosphere,toallowustomakeaccuratepredictionsregardingclimatechangeandthepossibleimpactsofvariouslandmanagementpractices.

Relative contributions of different green house gases to global warmingSource: Greenhouse Gases and Global Warming Potentials. U.S. Environmental Protection Agency (2002)

% C

ontr

ibut

ion

CO2

80

70

60

50

40

30

20

10

0CH

4N

2O Other gases

22

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24

European Commission

EUR 23759 EN – Joint Research Centre – Institute for Environment and SustainabilityTitle: Soil BiodiversityAuthor(s): Ciro Gardi and Simon JefferyLuxembourg: Office for Official Publications of the European Communities2009 – 24 pp. – 21.0 x 29.7 cmEUR – Scientific and Technical Research series – ISSN 1018-5593ISBN 978-92-79-11289-8DOI 10.2788/7831

Abstract

What is biodiversity? Biodiversity has different meanings depending on the situation being discussed and thetarget audience. For example, the Oxford English Dictionary defines biodiversity as being. The variety of plantand animal life in the world or in a particular habitat. This is definition is clearly sufficient for non-specialists.However, when looking more specifically at biodiversity, it becomes evident that thought needs to be given toother groups such as fungi, bacteria and archea. As soil is such as diverse system when considered biologically(as well as physically or chemically) it is necessary to include all taxonomic groups. Therefore, throughout thisbooklet, when referring to soil biodiversity it will be in reference to the variety of all living organisms found withinthe soil system.

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24

Ciro Gardi and Simon Jeffery

Soil Biodiversity

The mission of the JRC is to provide customer-driven scientific and technical support for the conception, develop-ment, implementation and monitoring of EU policies. As a service of the European Commission, the JRC functions as a reference centre of science and technology for the Union. Close to the policy-making process, it serves the com-mon interest of the Member States, while being independent of special interests, whether private or national.

LB-N

A-23759-EN-C

ISSN 1018-5593

EUR 23759 EN