Plant compensation to grazing and soil carbon dynamics in a tropical grassland.

0.58 MB·English

by  Ritchie, Mark E.

Plant compensation to grazing and soil
carbon dynamics in a tropical grassland
MarkE.Ritchie
DepartmentofBiology,SyracuseUniversity,Syracuse,NY,USA
ABSTRACT
Theeffectsofgrazingonsoilorganiccarbon(SOC)dynamics,particularlyinthe
tropics,arestillpoorlyunderstood.Plantcompensationtograzing,wherebyplants
maintainleafarea(Cinputcapacity)despiteconsumption(Cremoval)bygrazers,
hasbeendemonstratedintropicalgrasslandsbutitsinfluenceonSOCislargelyun-
explored.Here,theeffectofgrazingonplantleafareaindex(LAI)wasmeasuredin
afieldexperimentinSerengetiNationalPark,Tanzania.LAIchangedlittleforgraz-
ingintensitiesupto70%.TheresponsecurveofLAIversusgrazingintensitywas
usedinamassbalancemodel,calledSNAP,ofSOCdynamicsbasedonprevious
datafromtheSerengeti.ThemodelpredictedSOCtoincreaseatintermediategraz-
ingintensity,butthentodeclinerapidlyatthehighestgrazingintensities.TheSNAP
modelpredictionswerecomparedwithobservedSOCstocksinthe24grazedplots
ofa10-yeargrazingexclosureexperimentateightsitesacrosstheparkthatvaried
inmeanannualrainfall,soiltexture,grazingintensityandplantligninandcellulose.
ThemodelpredictedcurrentSOCstocksverywell(R2 > 0:75),andsuggeststhat
compensatoryplantresponsestograzingareanimportantmeansofhowherbivores
mightmaintainorincreaseSOCintropicalgrasslands.
Subjects Ecology,EcosystemScience,EnvironmentalSciences,SoilScience
Keywords Herbivory,Grazing,Plants,Compensation,Leafarea,Soilcarbon,Modeling,Grasslands,
Tropical,Serengeti
INTRODUCTION
Submitted 20August2013
Accepted 5December2013 Soilorganiccarbon(SOC)ingrasslandsandsavannasrepresentsoneofthelargest
Published 28January2014 reservoirsofcarbononearth(Conant etal.,2001;Lal etal.,2007).Duetowidespread
Correspondingauthor unsustainablelanduseduetoovergrazing,lossofnativeherbivores,excessivefires,and
MarkE.Ritchie,[email protected]
thepotentialtoreversetheimpactsoftheseuses,SOCisoneofthemoreimportant
Academiceditor
potentialsinksofgreenhousegasesintheefforttomitigateclimatechange(Mannetje,
JianguoWu
2007;Ellis&Ramankutty,2008;Smithetal.,2008).Amajorquestioniswhat
AdditionalInformationand
Declarationscanbefoundon managementpracticesingrasslands,intheformofgrazing,fire,fertilization,
page22 re-vegetationandrestoration,etc.,canleadtonetsequestrationofcarbon.
DOI10.7717/peerj.233 Recentreviewsdemonstratethatherbivorescanhavedramaticallydifferenteffectson
soilorganiccarbon(SOC),bothpositiveandnegative,dependingonsoiltype,
Copyright
2014Ritchie precipitation,plantspeciescompositionandgrazingintensity(Milchunas&Lauenroth,
Distributedunder 1993;Derner&Schuman,2007;Pineiroetal.,2010;McSherry&Ritchie,2013).These
Creative-CommonsCC-BY3.0 resultshavebeenobtainedlargelyintemperategrasslandsgrazedbylivestock(McSherry
&Ritchie,2013),andrelativelylittleisknownaboutgrazingimpactsonSOCintropical
OPENACCESS
HowtocitethisarticleRitchie(2014),Plantcompensationtograzingandsoilcarbondynamicsinatropicalgrassland.PeerJ2:e233;
DOI10.7717/peerj.233
grasslands.Inthetropicsandincertaintemperateclimates,plantspeciescompositionis
dominatedbywarm-season(C4)grassesthat,amongotheradaptationstograzing,invest
heavilyinrhizomesandotherstorageorgansthatallowthemtorespondquicklytoboth
rainfallanddefoliation(McNaughton,1985;Milchunas&Lauenroth,1993;Dubeux etal.,
2007).Compensatoryresponsestograzingcaninvolvesacrificingstemsforleavesand
thusmaintainleafareaandpotentialcarboninputsdespitecarbonoff-takebyherbivores
(Anderson,Dong&McNaughton,2006;Zheng etal.,2010;Ziter&MacDougall,2013).
Secondly,C4grassesgenerallycontainhigherlevelsofligninandcellulose(Bartonetal.,
1976),whicharegenerallyrecalcitranttodecomposition,andproduceextensive
abovegroundlitterthatfrequentlyburnsduringextendeddryseasons(Trollope,1982;
McNaughton,Stronach&Georgiadis,1998;Sankaran,Ratnam&Hanan,2008).Thirdly,
benigntemperaturesallowfortheprevalenceofmacro-decomposers,suchastermites
anddungbeetles,torapidlyincorporatesenescedplantmaterialandherbivoredunginto
soil(Hanski&Cambefort,1991;Freymannetal.,2008;Dungait etal.,2009;Risch,
Anderson&Schutz,2012).Thesefeaturesmaydramaticallyalterherbivoreimpactson
SOCintropicalgrasslandsascomparedtotemperategrasslandswithequivalent
precipitationandsoiltype(McSherry&Ritchie,2013).
Ofthesethreeimportantfeatures,theconsequenceofplantcompensationforsoil
carbonisprobablytheleastwellunderstood.Leafareaindex(leafarea/areasampled),or
LAI,hasbeenshowntodecreaseinresponsetograzinginsomecontextsbutnotothers
(Anderson,Dong&McNaughton,2006;Zhaoetal.,2009;Cruz etal.,2010;Zheng etal.,
2010;Ziter&MacDougall,2013).StudiesinSerengetiNationalPark(McNaughton,1985;
McNaughton,Milchunas&Frank,1996)andwestAfrica(deMazancourt,Loreau&
Abbadie,1999)haveshownbiomasscompensationtograzing,butnotcompensationfor
lostleafareaspecifically.Furthermore,thequantitativemannerinwhichLAIchangesas
aresponsetovaryinggrazingintensityhasnotbeenfullyexplored.Amajorquestionis
whetherLAIcanbemaintainedorevenincreasewithincreasinggrazingintensityandat
whatlevelofgrazingintensityitdeclines.
TheresponseofLAItoherbivorymaybeakeydriverofsoilcarbonresponseto
grazing.Leafareaishighlycorrelatedwithgrossphotosynthesisandnetcarbon(C)
assimilation(Craineetal.,2001;Ellsworthetal.,2004;Reich,Wright&Lusk,2007).
MaintenanceofleafareafollowingdefoliationpotentiallyallowsCinputsintoimportant
carbonpools,suchasbiomassandSOC,tobelittleaffectedbyherbivory,whilelossof
leafareacandramaticallyreduceCinputs.Becausemostcurrentsoilcarbondynamic
modelslackanexplicitaccountingofherbivoreimpactsonleafarea(Paustian,Parton&
Persson,1992;Schimel etal.,1994;Partonetal.,1995),therelativeimportanceofleaf
area-relatedCinputsrelativetoClossesfromfire,decomposition,andherbivore
consumptionhavenotbeenexplored.
Thegoalofthispaperistoshowhowleafareaindex(LAI),orleafarea/areasampled,
andplantallocationtostemandleafchangeswithgrazingintensityinatropicalsavanna
andthentoexplorehowsuchpossiblecompensatoryresponsesmightaffectsoilcarbon
dynamics.Hence,thispaper(1)presentstheresultsofa2-yeargrazingexclosure
Ritchie(2014),PeerJ,10.7717/peerj.233 2/27
experimentinSerengetiNationalParktomeasureeffectsofvaryinggrazingintensityon
plantLAIandproportionofbiomassallocatedtostemsvs.leaves,(2)developsamodelof
soilcarbondynamicsbasedonextensivepastresearchintheSerengetiasaframeworkfor
evaluatingtheimpactofLAIresponsetograzing,and(3)comparespredictionsofthis
modelwithobservedsoilcarbonstocksacrosstheeightsitesofa9-yeargrazingexclosure
experimentinwhichkeymodelinputparameterswereindependentlymeasured.
Themodelofcarbondynamics,calledSNAP(referringtoitsorigininSerengeti
NationalPark)accountsexplicitlyforfixedcarbon,asdeterminedbyLAI,soiltexture
andrainfall,anditsallocationtorootsversusshoots,anditsfate:decomposition,
consumptionbyherbivores,combustioninfireorresidenceinalong-termrecalcitrant
SOCpool.Themodelhasfiveinputvariables:meanannualrainfall,grazingintensity,fire
frequency,abovegroundproportionofcelluloseClignin,andsoiltexture(percentsand),
basedonthesuggestedmostimportantfatesofstablecarbonintheSerengetiecosystem
(McNaughton,1985;McNaughton,Banyikwa&McNaughton,1998;McNaughton,Stronach
&Georgiadis,1998;Holdoetal.,2007,Holdoetal.,2009).Themodelanditsfunctional
relationshipsarepopulatedwithparametervaluesavailablefromasubstantialliterature
ongrazing,plants,soils,andmicrobesfromSerengetiNationalParkplussomeadditional
newdataongrazingintensity,plantligninandcelluloseandsoilmoisturegatheredfrom
along-term(9year)grazingexperimentacrosseightsitesinSerengetiNationalParkthat
varyingrazingintensity,rainfall,soiltexture,firehistory,andplantspeciescomposition.
Toevaluatetheroleofplantcompensation,asensitivityanalysisofmodelparameters,
includinggrazingintensity,intheSNAPmodelisconducted.Themodelalsoisusedto
makedeductivepredictionsofcurrentsoilcarbonstocksundertheassumptionofamass
balancesteady-stateresultingfromthepersistenceofmeanrainfall,plantligninand
cellulose,soiltexture,firehistory,andgrazingintensityconditionsoveranextended
periodofprioryears.Thesepredictionsarethencomparedwithobservedsoilcarbon
measuredingrazedplotsofthe9-yearexclosureexperimentusinglinearregression,with
testsforoverallmodelfit(R2)andtestsfordifferencesinslopefromavalueof1andan
interceptvalueofzero.Thisanalysisprovidesanexplicitandquantitativetestofthe
hypothesisthatplantcompensatoryresponsesareimportantintheinfluenceof
herbivoresonsoilcarbon.
Thisapproachappliesadeductive(Belovsky,1984;Belovsky,1994;Overmars,deGroot
&Huigen,2007)ratherthaninductive(Burnham&Anderson,2004)evaluationofthe
impactofpossibleplantcompensation.Theuseofadeductivemodelexplicitlycombines
thelogically-derivedhypothesizedmechanismsbywhichdifferentfactorsmightdrive
soilcarbondynamicsbasedonpriorknowledgeoftheSerengeti.Asensitivityanalysisof
themodelassessestherelativeimportanceofagivenvariableorparameterrelativeto
others.Theadvantageofadeductiveapproachisthatitavoidstheuncertaintyin
inferencederivedfromassociatingsoilcarbondynamicswithmultiple,possibly
auto-correlated,independentvariablesinaninductiveapproach(Burnham&Anderson,
2004).Further,adeductivemodelbuildsinnon-linearityofrelationships,whichislargely
avoidedininductiveapproachesbutmaybelikelytooccurintherelationshipbetween
Ritchie(2014),PeerJ,10.7717/peerj.233 3/27
LAIandgrazing(McNaughton,1985;deMazancourt,Loreau&Abbadie,1999;Anderson,
Dong&McNaughton,2006).
MATERIALS AND METHODS
Study area
MostofthedatapresentedinthisstudywerecollectedinSerengetiNationalPark(SNP),
Tanzania.SNPcontainsnearly3millionmigratorywildebeest(Connochaetestaurinus),
zebra(Equusburchelli),andThomson’sgazelles(Gazellathomsoni),plusmultiplespecies
ofresidentherbivores>10kginsize,alldistributedheterogeneously(Andersonetal.,
2010)over25,000km2(ameandensityof120/km2)(McNaughton,1985;Sinclair etal.,
2007).Theseherbivoresconsumeamajorfraction(mean61.8%(cid:6)12.2SEM)of
abovegroundprimaryproduction(McNaughton,1985).VegetationisdominatedbyC
4
grasses,featuringThemedatriandrainmorelightlygrazedareasandDigitaria
macroblepharaandPennisetummenzianuminmoreheavilygrazedareas.TheSerengeti
regionfeaturesapronouncedrainfallgradientdrivenmixedsomewhatindependently
withasoilgradientofsilty,organicmatter-richsoilsinthesoutheasttoclaysoilsinthe
westandsandy,lownutrientsoilsinthenorth(Andersonetal.,2007;Sinclair etal.,2007;
Andersonetal.,2010).Theclustereddistributionofresidentherbivores(Andersonetal.,
2010)andvariablemovementsofmigratoryspeciesresultsinhighlyvariablehistorical
grazingintensityacrossthelandscape.Strongpreferencesbyherbivoresforplantsfound
atthetopratherthanbottomofslopesplusatendencytoavoidtheedgesofwoodlands
resultsinvariablegrazingintensityoverdistancesof<50m(Gwynne&Bell,1968;
Anderson,Dong&McNaughton,2006;Andersonetal.,2007).
Design
PlantcompensationtograzingwasassessedneartheSerengetiWildlifeResearchCentre
◦ ′ ◦ ′
nearSeronera(34 50 Eand2 25 S)insidethePark.TheareaisopenAcaciatortilis
savannawoodland,withdominantgrassesThemedatriandraandDigitaria
macroblephara,andhostsresidentherdsofimpala(Aepycerosmelampus),buffalo
(Synceruscaffer),andThomson’sgazelles(Gazellathomsoni),amongothers,andis
routinelyvisitedbytheannualwildebeestandzebramigration.Plantresponsestograzing
weremeasuredinsideandoutsideofgrazingexclosuresestablished2yearspreviouslyina
10haopengrasslandwithlessthan5%treecoverneartheSerengetiWildlifeResearch
Centre(2-yearexclosureexperiment).Theproportionofbiomassasstemversusleafwas
measuredforallplantsclippedfromsixrandomlyselected15(cid:2)15cmquadrats,three
insideandthreeoutsideeachoftwelveexclosuresofvarioussize(10(cid:21)200m2)erected
between2009and2010toprotectexperimentalgardensornutrientaddition
experiments.LAI,proportionofstem,andabovegroundbiomassweremeasuredinthe
unused‘‘bufferzone’’justinsideeachfenceandtheninquadrats4mperpendicularto
eachfencepairedwitheachquadratinsidethefence.Theobjectivewastoencounter
differentlocalizedgrazingintensitiesthatresultedfromsamplingbeneaththornyshrubs
orotherplantprotectionsversuspatcheswithhighlypreferredforagespecies.
Ritchie(2014),PeerJ,10.7717/peerj.233 4/27
Togenerateadditionalinputdataforamodelofsoilcarbondynamics,alonger-term(9
year)grazingexclosureexperimentestablishedbySamMcNaughtonin1999(Anderson,
Ritchie&McNaughton,2007)wasusedtoprovidedataonsoilmoistureasafunctionof
rainfall,andindependentmeasuresofgrazingintensity,plantligninandcellulose,and
SOCtotesttheSOCdynamicmodel.Alineofsixplots(4(cid:2)4m),spaced10mapartina
linetransectwereestablishedinOctober1999ateachof8siteslocated10ormorekm
apart,ingrasslandareasvisitedalmostentirelybygrazing,ratherthanbrowsing,ungulate
species(Anderson,Ritchie&McNaughton,2007).Siteswerechosentobewithin1kmof
large,permanentconcentrationsofgrazingherbivores(Andersonetal.,2010)andvaried
considerablyinannualrainfall,soiltype,andfirefrequency.Threerandomlyselected
plotswithinthetransectateachsitewerefencedwith2mhigh,8cmmeshwire.These
fenceseffectivelyexcludedallgrazingmammals>10kg,sinceanimalspreferredtogo
aroundratherthanjumpfences.Theremainingthreeplotsateachsitewereunfenced
controls.Woodyvegetationatourexperimentalsiteswastypicallysparse(lessthan10
woodyplants/ha)butherbaceouslegumes,suchasIndigoferavolkensii,wereubiquitous
andreasonablyabundant(>2%cover)atallourstudysites.Oureightsitesincludedtwo
onthetreelessshortgrassplainsofsoutheasternSNP,andtheothersixsiteswere
representativeofwoodysavannasbroadlydistributedacrossSNP(Ruess&Seagle,1994).
Measurements
Theeffectofgrazingonplant(grass)allocationtoleafversusstemandonleafareaindex,
LAI(cm2leaf=cm2groundarea)wasassessed.Clippedplantsforallplantspeciesina
quadratweretakenbacktothelaband,whilefresh,laidoutandtracedongraphpaper,
◦
andthenleaveswereclippedfromstemsandstored,driedat45 C,andweighed
separately(aswithfieldbiomass).Theproportionofleafforeachquadratwascalculated,
alongwithLAI(totalleafarea(cm2)dividedbyquadratarea(cm2)).
Anotherkeyvariable,GI(grazingintensity)varieslocallyandwasestimatedinboth
the2-yearand9-yearexperimentsasthefractionaldifferenceinstandingaboveground
biomass(AGB):GI D 1(cid:0)AGB =ABG (Anderson,Ritchie&McNaughton,2007).GIis
g ug
anindirectmeasureofthefractionofannualproductionconsumedbygrazers
(McNaughton,1985;McNaughton,Milchunas&Frank,1996).AGBwasmeasuredby
clippingandweighingallabovegroundplantmaterial,excludinglitter,afterdryingat
◦
45 Cforthreedaystoconstantmass.AGBwasmeasuredinthe2-yearexclosure
experimentinthepairedquadratsinsideandoutsideexclosuresusedtomeasureLAI.
ThequadratinsidetheexclosurewasassignedGI D 0,andthepairedquadratoutsidethe
exclosurewasassignedGIbasedonthedifferenceinAGBbetweenthepairedquadrats.
Inthe9-yearexclosureexperiment,biomasswasclippedfromfour15(cid:2)15cmquadrats
withineachgrazedandexclosureplotinlateMayorJuneattheendofthewetseasonin
2006,2009,and2010.Biomassmeasuredineachofthethreegrazedplotsateachsitewas
comparedtobiomassineachoftheirnearestneighborexclosureplots(Anderson,Ritchie
&McNaughton,2007),yieldingthreeestimatesofgrazingintensityateachsite.
Tomeasureligninpluscellulosefraction(LIGCELL),driedplantmaterialfromthe
entireclippedquadratwasgroundthrougha0.9mm(40mesh)screeninaWileymill
Ritchie(2014),PeerJ,10.7717/peerj.233 5/27
andthensubjectedtoasulfuricacidhydrolysismethod(Sluiter etal.,2010),i.e.,
sequentialdigestioninfirstneutraldetergentmanufacturedbyAnkomTechnologyCorp.,
Macedon,NewYork,USA(sodiumlaurylsulfate,50.02%,EDTAdisodium,dehydrate,
31.03%.,sodiumborate,decahydrate11.35%,andsodiumphosphate,dibasic,anhydrous,
7.6%),followedbyAnkommanufacturedaciddetergent(20gcetyltrimethylammonium
bromide(CTAB)dilutedin1L1.00NH SO ),andthenin72%sulfuricacid,followed
2 4
◦
finallybyashinginamufflefurnaceat500 Cfor24h.Ligninandcellulosefractionswere
inferredbythemasslostbetweentheremainderfollowingneutraldetergentdigestion
andtheremainderafterashing,expressedasaproportionoftheoriginalsamplemass.
Annualrainfalloverthe9yearsofthestudywasobtainedfromraingaugedataat23
sitescollectedbytheSerengetiEcologicalMonitoringProgram(Andersonetal.,2007).
FirefrequencywasdeterminedbyinterpretingMODISsatellitevisibleandnearinfra-red
imagery(Dempewolf etal.,2007)forJuly(cid:21)Octoberfor2000(cid:21)2008togeneratemapsof
fireoccurrenceforeachyearwitharesolutionof250m.GrazingexperimentsiteGPS
⃝
locationswereoverlaidwithfiremapsforeachyearinaGIS(ArcGIS9.1byESRIR)to
determinethenumberoftimesasiteburnedovertheperiod2000(cid:21)2008.
Effectsofprecipitationonsoilmoistureandnumberofdaysinwhichmicrobeswere
likelytobeactive(WETDAYS)weredeterminedfromfieldmeasurementsofsoil
moistureinthelong-termexperiment(unpublisheddatagenerouslyprovidedbySam
McNaughton).Fivecmdiametersoilcoresweretakentoadepthof10cmeachmonth
fromDecember1999toJune2002(atotalof31days)ateachofthreegrazedplotsatthe
eightsitesofthelong-termSerengetigrazingexperiment.Moisturecontentwas
determinedgravimetricallyandmonthlyrainfallwasmeasuredfromraingauges
mountedon1mtallfencepostsateachsite.Arecentreview(Manzoni,Schimel&
Porporato,2012)suggeststhat,insemi-aridsoils,microbialactivityceaseswhenwater
potentialdropsbelow(cid:0)14cmH O.Waterpotentialwasconvertedintosoilmoisture,
2
calibratedforthetextureofSerengetisoils(Table1)(Cosby etal.,1984)andsuggested
thatManzoni,Schimel&Porporato(2012)thresholdcorrespondedonaverageto10%
gravimetricwatercontent.Thenumberofdaysateachoftheeightsitesthatsoilmoisture
was10%orhigherwasdeterminedandthenusedtobuildaregressiontoestimatethe
numberofdaysperyearwithactivesoilmicrobesasafunctionofannualrainfall.
Asatestofthenewsoilcarbonmodel,SOCwasmeasuredatthesametimeasbiomass
ineachplotfrom8.3cmdiameter(cid:2)40cmdeepcoresfromeachofthethreebiomass
quadratsperplot.Eachcorewasspreadonaportabletabletopandcrushedwitharolling
pintobreakupsoilaggregates.Allpebbles,rocks,andvisiblerootswereremoved,and
thensoilwassievedthrough0.7mmmesh.Coresofknownvolumewerepooled,stored
◦
insealedplasticbags,andthendriedfor6daysat45 Candthenweighedtodetermine
bulkdensity(gsoil/cm3).BothSOCandnitrogencontentsweredeterminedwiththe
Walkley-BlackmethodattheSoilsAnalysisLaboratoryatSokoineUniversityof
AgricultureinMorogoro,Tanzania.Reportederrorwas(cid:6)0.004g/gC.Soilcomposition
(sand,siltandclayfractions)wasdeterminedbyamicropipettemethod.Soilcarbon
densitywasmeasuredbymultiplyingSOCcontentbybulkdensity(g/m2)to40cmdepth
Ritchie(2014),PeerJ,10.7717/peerj.233 6/27
Table1VariablesandkeyparametersintheSNAPmodel,theirunits,andsourcesofdata.
Parameter Units Type Source
ANPPmax gm(cid:0)2yr(cid:0)1 Literature Maximumabovegroundproduction(McNaughton,1985)
ANPPest gm(cid:0)2yr(cid:0)1 Model Grazer-modifiedANPP
BNPPest gm(cid:0)2yr(cid:0)1 Literature Belowground production (McNaughton, Banyikwa & Mc-
Naughton,1998)(Fig.3B)
DDSOC gCm(cid:0)2yr(cid:0)1 Model Dung-derivedSOC
FIRE #/yr Measured Numberoffiresperyear,monitored(Table4)
GI proportion Measured 1-(grazedbiomass/ungrazedbiomass)(Table4)
LAI - Measured LeafAreaIndex(dimensionless);Thisstudy(Fig.2B)
LIGCELL proportion Measured CelluloseClignin(%)abovegroundbiomass,(Table4)
MRESP gCm(cid:0)2d(cid:0)1 Literature (Ruess&Seagle,1994)(Fig.3D)
PL proportion Measured Proportionleaf;Thisstudy(Fig.2A)
PDSOC gCm(cid:0)2yr(cid:0)1 Model Plant-derivedSOC
RAIN mm/yr Interpolated Meanannualrainfall(Andersonetal.,2010)(Table4)
SAND% percent Measured Fromastandardsoilanalysis,measured(Table4)
WETDAYS dyr(cid:0)1 Measured #dayswithsoil>10%water;Thisstudy(Fig.3C)
WHC proportion Literature Waterholdingcapacity(Ruess&Seagle,1994)(Fig.3A)
Table2ParametersforMonteCarlosimulations.Parametersandtheirerrorsusedinpredictingsoilcarbon
stocksinSerengetigrasslandsandintheMonteCarlosimulations.
Parameter Input Coefficient
B0 SE B1 SE B2 SE
PL GI 0.597 0.061 0.24 0.023
LAI GI 1.15 0.027 (cid:0)0.015 0.0011 4.6 0.2
ANPPmax RAIN (cid:0)27.5 17.6 0.84 0.07
WHC SAND% 1.04 0.05 (cid:0)0.0070 0.0008
BNPPest RAIN 958.8 165.0 (cid:0)0.82 0.27
WETDAYS RAIN (cid:0)0.025 0.033 0.00043 0.00006
MRESP SOC (cid:0)0.58 0.45 0.00044 0.00007
CARBON N/A 0.45 0.02
ofthepooledcoresineachplot.A40cmdepthwasused,asthistypicallycorrespondsto
thedepthof>90%ofroots(McNaughton,Stronach&Georgiadis,1998),andmultiple
sitesfeaturedahardpanordenseclaylayerat40(cid:21)50cmthatpreventedreasonable
samplingtogreaterdepths.
Literature data and re-analyses
Literaturedata,mostlyfrompriorstudiesinSerengeti,werere-analyzedtospecifically
estimatesoilwaterholdingcapacity(WHC),abovegroundproduction,belowground
production,andsoilmicrobialrespirationofcarbon.Forsourcesandunitsofliterature
data,seeTable1.TherelationshipsusedarereportedintheResultsandDiscussion
(Table2).
Ritchie(2014),PeerJ,10.7717/peerj.233 7/27
Figure1 Hypotheticalmajorfatesofcarbonintropicalgrassland,asthebasisforapracticalsoil
carbondynamicmodel.Netfixedcarbonbecomesresidentsoilorganiccarbon(SOC)throughtwoma-
jorpathways:plant-derivedSOCnotconsumedbymicrobes(insoilorthegutsofmacro-decomposers
liketermites)(heavysolidarrows),anddung-derivedSOC(heavyshort-dashedarrows)notassimilated
bygrazersandgutorsoilmicrobes.Allothercarboniscombustedthroughfire(blackarrow),orrespired
bygrazersandmicrobesinsoilorthegutsofmacro-decomposers(longdashedarrows).
Model development
Theflowoffixedcarbonthroughhypotheticaltropicalgrasslandwasdescribedaccording
tofourcriteria.First,massbalancewasassumed,sothatallfixedcarbonresidedinpools,
suchasbiomassorSOC,orsufferedthefateofbeingcombusted,consumed,orrespired.
Second,thisflowwasdescribedintheminimumnumberoffluxesandpoolsnecessaryto
accountforthefateofcarbon(Fig.1).Third,themostparsimonioussetofinputvariables
thatcoulddescribethechangesinthesepoolswasused.Finally,atimestepofoneyear
withadistinctwetanddryseasoneachyearwasassumed,withproductionandgrazing
resultinginastandingbiomassatthebeginningofthedryseasoneachyearthat
subsequentlyeithercombustediftherewasfireorwasotherwisedecomposed.More
complicatedtimedynamicsofdailyorseasonalchangeshavebeenusedrecently(Holdo
etal.,2007,2009),butthisintroducespossiblyunnecessarycomplexity.Above-and
belowgroundproductionarethereforeseasonalaccumulationsofbiomassasmodifiedby
averagegrazingintensityoverthecourseofthewetseason.Biomassnotconsumedby
herbivoresmaythenburnatsomefrequencyduringthedryseason.Theseassumptions
ledtoarelativelysimplesetofpathwaysforstablecarbon(Fig.1):(1)inputintosoil
organicmatterfromdecomposingshootsorroots,(2)combustioninfire,or(3)input
intosoilorganicmatterthroughdung.Allnon-ligninorcellulosecompoundswere
assumedtoturnoverwithin1(cid:21)2yearsorless(Ruess&Seagle,1994)andwere
consequentlyignored.
Themodelwasbasedonfourmajorassumptions.First,tropicalgrassespotentially
exhibitcompensatoryresponsestodefoliationthatmaintainsimilarleafarea,andthus
photosyntheticcapacity,acrossabroadrangeofgrazingintensities(McNaughton,1985).
Second,thelargestcarboninputstothesoilorganicmatterpooloccurthrough
Ritchie(2014),PeerJ,10.7717/peerj.233 8/27
decompositionofabove-andbelowgroundbiomassandthroughincorporationof
herbivoredungintosoil.Third,themajorlossesofSOCderivefromcombustion(fire),
herbivorerespirationandsoilmicrobialrespiration.Finally,allplantCinplanttissue
otherthanligninandcellulosewasassumedtobeassimilatedandrespiredbyherbivores,
microbesinsoilorthegutsofmacro-decomposers.Ligninandcellulosearethemost
recalcitrantformsofcarbontodecomposition,andlikelyaccountforthemajority
(>90%)oflong-livedSOC(Ganjegunteetal.,2005;Frank,Pontes&McFarlane,2012).
TheSOC(g/m2to40cmdepth)measuredin2009inthegrazedplotsinthelong-term
grazingexperimentrepresentedSOC underthereasonableassumptionthatconditions
eq
intheseplotshadbeenapproximatelysimilarintermsofwildlifeuse,plantspecies
composition,andclimatesince1979(Sinclair etal.,2007;Holdoetal.,2009).Theaverage
ofgrazingintensitiesmeasuredin2006,2009,and2010wasassumedtoreflecthistorical
long-termgrazing.Theotherinputvariableseitherwerealreadyalong-termaverage
(RAIN,FIRE)orareunchangedbylanduse(SAND%).
Statistics
TheassociationbetweenLAIandgrazingintensity(GI)wastestedwithlinearregression
inSPSSversion19(IBM,Armonk,NewYork,USA).Non-linearrelationshipswerealso
explored,andbasedontheappearanceofthedata,theRscript‘‘nls’’wasusedwitha
functionB (cid:0)B exp.(cid:0)B GI),whereB arefittedcoefficients.LinearregressioninSPSS
0 1 2 i
wasusedtobuildregressionrelationshipsfromliteraturedata(Table2)andtocompare
observedSOCtopredictedSOC fromtheSNAPmodel.Inthecomparisonofthe
eq
observedandpredictedSOC,thehypothesesthattheinterceptoftheregressionlinewas
equaltozeroandthattheslopewasequaltoonewereevaluatedwithz-tests.
TheSNAPsoilcarbondynamicmodelwasconstructedfromanumberofempirical
relationshipsthatcontainparameters(intercepts,slopes,etc.)estimatedwitherror.A
MonteCarloanalysis(Ogleetal.,2010)wasconductedbysamplingthenormal
distributionsinferredfrommeasuredmodelinputparametersandparametersfrom
relationshipsusedtoconstructthemodel.Thisprocesswasrepeated100timesto
generateameanands.e.m.fortheestimatedSOC foreachsiteandeachpairedgrazed
eq
andungrazedplotinthe9-yearexclosureexperiment.
RESULTS AND DISCUSSION
New and prior data analyses
Theproportionofbiomassinleavesincreasedsignificantly(P < 0:001)withincreasing
grazingintensity(Fig.2A).Inconcordancewiththispattern,LeafAreaIndex(LAI)
declinedsignificantlywithincreasinggrazingintensity(GI)accordingtolinearregression
(R2 D 0:36,dfD1,34,PD0.01).Howeveranon-linearfunction,LAI D B (cid:0)B exp
0 1
.B GI/fitthedatamuchbetter(R2 D 0:58,dfD1,33,P < 0:001)andvisiblymatched
2
bettertheconsistentlyhighLAIfoundatlowtointermediategrazingintensityandthe
dramaticdeclineinLAIaboveagrazingintensityof70%(Fig.2B).Thesetwopatterns
supportthehypothesisthatplantsmaintainCinputstotheSerengetiecosystemdespite
Ritchie(2014),PeerJ,10.7717/peerj.233 9/27
Figure2 PlantcompensatoryresponsestograzinginSerengeti.Keyrelationshipsforassessingplant
compensationtograzing:(A)proportionofleaves(PL)and(B)LeafAreaIndex(LAI,cm2=cm2)of
grazedandungrazedplants,eachasafunctionofgrazingintensity(GI).
heavyremovalsofbiomassbygrazers.ThemaintenanceofLAIacrosssuchabroadrange
ofgrazingintensitiescontrastswiththetypicalpatternofdramaticreductionsinLAIseen
mostlyintemperatesystemsunderrelativelymoderategrazingintensities(30%(cid:21)60%)
(Zhaoetal.,2009;Cruz etal.,2010;Zheng etal.,2010).Thepatterncorroboratesresults
ofenhancedproductivityundergrazing(McNaughton,1985;Milchunas&Lauenroth,
1993;Frank,Kuns&Guido,2002)thatareatleastpartlyderivedfromcompensatory
morphologicalchangesbyplantstograzing(Anderson,Dong&McNaughton,2006;Ziter
&MacDougall,2013).Despitethesepreviousresults,itisstillnotclearwhytheC grasses
4
typicallydominantintheSerengetiandelsewhereresponddifferentlytomoderately
intensegrazingthanC grasses(Derner&Schuman,2007;McSherry&Ritchie,2013).
3
Asexpected,waterholdingcapacityexhibitedastrong,significant(P < 0:001)
negativeassociationwithincreasingsandcontent(Ruess&Seagle,1994)(Fig.3A),and
rootproductionshowedasignificant(P D 0:0015)declineinassociationwithhigher
rainfall(McNaughton,Banyikwa&McNaughton,1998)(Fig.3B).Theproportionofdays
soilheldmorethan10%moistureincreasedsignificantly(P D 0:006)withmeanannual
rainfallacrosstheeightlong-termgrazingexperimentalsites(Fig.3C).Finally,maximum
microbialrespirationrateswerestronglyandsignificantly(P < 0:001)associatedwith
existingSOCstocksacrosstheSerengetilandscape(Ruess&Seagle,1994)(Fig.3D).
Regressionequationsarereportedinthefiguresandwereusedinthedevelopmentofthe
SOCdynamicmodel.
SOC dynamic model
BasedontheresultsforLAIresponsetograzing(Fig.2B),theSOCmodelforSerengeti
NationalPark(hereafterreferredtoastheSNAPmodel)wasconstructedwithfiveinput
variables:RAIN,meanannualrainfall(mm/yr);GI,grazingintensity(1-(grazed
biomass/ungrazedbiomass))(McNaughton,1985);FIRE,firefrequencyorthenumberof
firesrecorded,dividedbythenumberofyearsoverwhichfiresweremonitored;
Ritchie(2014),PeerJ,10.7717/peerj.233 10/27