The Case of Aspen and Soil Carbon in North America

15 Pages·2017·0.89 MB·English

Article
A Tree Species Effect on Soil That Is Consistent
Across the Species’ Range: The Case of Aspen and
Soil Carbon in North America
JérômeLaganière1,*,AntraBocˇa2,HelgaVanMiegroet2andDavidParé1
1 NaturalResourcesCanada,CanadianForestService,LaurentianForestryCentre,1055duP.E.P.S.,
P.O.Box10380,Stn.Sainte-Foy,QuébecQCG1V4C7,Canada;[email protected]
2 DepartmentofWildlandResourcesandEcologyCenter,UtahStateUniversity,5230OldMainHill,Logan,
UT84322-5230,USA;[email protected](A.B.);[email protected](H.V.M.)
* Correspondence:[email protected];Tel.:[phone];Fax:[phone]
AcademicEditor:LaurentAugusto
Received:15February2017;Accepted:5April2017;Published:8April2017
Abstract: TremblingaspencoversalargegeographicrangeinNorthAmerica,andpreviousstudies
reportedthatabetterunderstandingofitssingularinfluenceonsoilpropertiesandprocessesisof
highrelevanceforglobalchangequestions. Hereweinvestigatethepotentialimpactofashiftin
aspenabundanceonsoilcarbonsequestrationandsoilcarbonstabilityatthecontinentalscaleby
conductingasystematicliteraturereviewusing23publishedstudies. Ourreviewshowsthataspen’s
effect on soil carbon is relatively consistent throughout the species range. Aspen stores less C in
theforestfloorbutsimilaramountsinthemineralsoilrelativetoconifers. However,arobustset
ofindicatorsofsoilCstability,forexample,degreeoforgano-mineralassociations,proportionof
readily-availableorlabileCestimatedduringlong-termsoilincubationsorusinghot-waterextraction,
patternofsoilCdistribution,andtemperaturesensitivityofsoilheterotrophicrespiration,revealsthat
thesoilorganiccarbon(SOC)stockunderaspenismorestable,renderingitmoreprotectedagainst
environmentalchangesandsoildisturbances. Therefore,ourcontinental-scaleanalysishighlights
thatanincreaseintheabundanceoftremblingaspeninNorthAmericanforestsmayincreasethe
resistanceandresilienceofsoilCstocksagainstglobalchanges.
Keywords: trembling aspen; coniferous tree species; soil organic matter; soil carbon reservoirs;
carbonstability;NorthAmerica
1. Introduction
Tremblingaspen(PopulustremuloidesMichx.) coversalargegeographicrangeinNorthAmerica
(Figure 1), and is found on a great variety of soils, mainly Alfisols, Spodosols, Inceptisols [1],
and Mollisols [2,3]. Its abundance within a forest stand has been found to positively affect stand
productivity,totalabovegroundbiomass,soilrespiration,andnutrientcyclinginborealmixedwood
forestsofvariouscomposition[4–6]. InwesternandmidwesternUSA,aspenhasalsobeenassociated
withincreasedlevelsofunderstoryplantspeciesdiversity[5,7]. Enhancedlevelsofavifauna,mammal,
andmacroinvertebratebiodiversityhavealsobeenreportedinaspenstandscomparedtoadjacent
coniferstands[8,9]. Furthermore,inthesemi-aridwesternUSA,aspenhasapositiveeffectonsnow
accumulationandwaterretention[10],anissueofmajorimportanceinregionsthatdependonsnow
asawatersource.
As a pioneer species, aspen has developed mechanisms for quickly occupying suitable areas
throughfastseeddispersalandvegetativesuckering,whichareoftenenhancedbydisturbanceslike
fire[11]. Becauseofitswidespreaddistributionanditspositiveeffectsonmanyecosystemservices,
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Forests 2017, 8, 113   2 of 14 
southern end of its distribution range, reported cases of aspen decline became a research focus as 
early as 1942 [13], and this has continued throughout the last century [14–17]. Overall, herbivory by 
defoliators, like the forest tent caterpillar and ungulate browsing, changes in disturbance regimes 
(such as fire exclusion), and a drier climate can affect aspen distribution and abundance. A study by 
Worrall et al. [18] recently concluded that aspen distribution might change in the future due to aspen 
disappearing from areas currently on the edge of its climatic niche where water availability will no 
longer be sufficient to ensure its survival. This is mostly predicted to happen in its southern 
distribution range, but the northern areas are also expected to see climate‐induced changes. While a 
drier climate will limit the survival of aspen in many areas (especially in the southwest), in areas 
with more suitable edaphic conditions (mostly in the north), a drier climate will most likely promote 
more fires [19], thereby, in fact, creating more favourable conditions for aspen stand establishment 
[20–23]. Furthermore, increased rates of insect disturbance or forest harvesting can also potentially 
Forests2017,8,113 2of15
benefit aspen abundance in such areas [24,25].  
Apart from aboveground forest characteristics, the effect of aspen on soil characteristics is less 
aspwenellh ausnrdeecresitvoeodd.c oInns idvieerwab loef atpteontetniotinali nctlihmeastcei eanntidfi cmliatenraagteumree,netv einndausceeadr lychaasn1g9e2s 5i[n1 2f]o.rAesttt he
souctohmerpnoseintidono, fthites edfifsetcrti bouf ttiroene rsapnegceie,sr espoiol rotergdacnaics ecsaorbfoans p(SeOnCd)e csltionreagbee chaams ereacerievseeda rinchcrefoasceuds as
earalytteanst1io9n4 2i[n1 3r]e,caenndt thyeisarhsa s[2c6o,n27ti]n. uCedontshidroeurignhgo  uthtet helalragset caemntouurnyt [1o4f –1c7a]r.bOonv esrtaolrl,edh eribni vsooriyl, by
understanding species induced SOC patterns can give us crucial insights into the potential impact of 
defoliators, like the forest tent caterpillar and ungulate browsing, changes in disturbance regimes
a shift in aspen abundance on SOC sequestration and the continental carbon balance.  
(such as fire exclusion), and a drier climate can affect aspen distribution and abundance. A study
The objective of this paper is to assess whether trembling aspen has an effect on the amount and 
byWorralletal.[18]recentlyconcludedthataspendistributionmightchangeinthefuturedueto
nature of soil carbon relative to conifers, and whether this effect is consistent across the species’ 
aspendisappearingfromareascurrentlyontheedgeofitsclimaticnichewherewateravailability
continental range, such that it can be extrapolated across North America. We also aim at identifying 
willnolongerbesufficienttoensureitssurvival. Thisismostlypredictedtohappeninitssouthern
factors potentially responsible for inconsistencies among studies regarding the magnitude or the 
distributionrange,butthenorthernareasarealsoexpectedtoseeclimate-inducedchanges. Whilea
direction of the observed aspen effects (none, positive, negative). In our analysis, soil properties and 
drierclimatewilllimitthesurvivalofaspeninmanyareas(especiallyinthesouthwest),inareaswith
processes other than carbon (e.g., nutrient availability, pH) were also considered when possible, but 
moresuitableedaphicconditions(mostlyinthenorth),adrierclimatewillmostlikelypromotemore
the main focus was to assess the effect of aspen on soil carbon storage and stability against C losses 
fires[19],thereby,infact,creatingmorefavourableconditionsforaspenstandestablishment[20–23].
(i.e., the relative persistence of that C in the soil). To achieve this, we conducted a systematic 
Furlittheerarmtuorer er,eivniecwre,a dseedfinreadte asso af itnrasencstpadriesntut rabnadn cimepoarrftoiarle sstumhamrvaerys tionf gexciasntinagls orepseoatrecnht,i aulsliyngb e2n3e fit
asppeunbalibsuhendd astnucdeieins csouncdhuacrteeads in[2 N4,o2r5t]h. America, and summarized the outcomes. 

Figure 1. Geographic distribution of trembling aspen (Populus tremuloides Michx.) and location of the 
Figure1.Geographicdistributionoftremblingaspen(PopulustremuloidesMichx.)andlocationofthe
study sites covered by this literature review. 
studysitescoveredbythisliteraturereview.
2. Material and Methods 
Apartfromabovegroundforestcharacteristics,theeffectofaspenonsoilcharacteristicsisless
wel2l.1u.n Sdtuerdsyt oAordea. Inviewofpotentialclimateandmanagementinducedchangesinforestcomposition,
theeffectoftreespeciessoilorganiccarbon(SOC)storagehasreceivedincreasedattentioninrecent
Trembling aspen is the most widely distributed tree in North America, growing from Alaska to 
years[26,27]. Consideringthelargeamountofcarbonstoredinsoil,understandingspeciesinduced
central  Mexico  [1].  The  species is  widespread  across  all  provinces  of  Canada,  in  Alaska,  in 
SOCpatternscangiveuscrucialinsightsintothepotentialimpactofashiftinaspenabundanceon

SOCsequestrationandthecontinentalcarbonbalance.
The objective of this paper is to assess whether trembling aspen has an effect on the amount
andnatureofsoilcarbonrelativetoconifers,andwhetherthiseffectisconsistentacrossthespecies’
continentalrange,suchthatitcanbeextrapolatedacrossNorthAmerica. Wealsoaimatidentifying
factors potentially responsible for inconsistencies among studies regarding the magnitude or the
directionoftheobservedaspeneffects(none,positive,negative). Inouranalysis,soilpropertiesand
processesotherthancarbon(e.g.,nutrientavailability,pH)werealsoconsideredwhenpossible,but
themainfocuswastoassesstheeffectofaspenonsoilcarbonstorageandstabilityagainstClosses
(i.e.,therelativepersistenceofthatCinthesoil). Toachievethis,weconductedasystematicliterature
review, defined as a transparent and impartial summary of existing research, using 23 published
studiesconductedinNorthAmerica,andsummarizedtheoutcomes.
Forests2017,8,113 3of15
2. MaterialandMethods
2.1. StudyArea
TremblingaspenisthemostwidelydistributedtreeinNorthAmerica,growingfromAlaskato
centralMexico[1].ThespeciesiswidespreadacrossallprovincesofCanada,inAlaska,innorth-eastern
UnitedStatesaswellasinwesternstates, whereitgrowsmainlyathighaltitudes(Figure1). The
tremblingaspendistributionrangeontheNorthAmericancontinentwastakenasthestudylimitsfor
ourliteraturereview.
2.2. DataCollection
The available literature on the influence of aspen on soil carbon was compiled using Scopus,
WebofScience,ResearchGate,aswellasGoogleScholar. Keywordsusedduringthebibliographic
searchwere: aspen,soilcarbon,soilorganicmatter. Inordertobeincludedinouranalysis,studieshad
tomeetthreecriteria:(1)reportsoilorganiccarbon(ororganicmatter)concentration,content(orstock),
and/orastabilityindicator;(2)compareaspenwithoneormoreconiferousspeciesestablishedon
similar site conditions (paired-sites preferably); (3) perform statistical analysis and report results.
Carewastakentoavoidduplicatingresultsfromsimilardatasetsreportedindifferentpublications.
Due to the low number of studies reporting the influence of aspen on comparable SOC variables
(concentration vs. content, forest floor vs. mineral horizons, different soil sampling depths, etc.),
wewereunabletoapplystatisticalmethodstoourdataset(meta-analysis). Indeed,onlysixstudies
reportedforestfloorCconcentrationandtwelvereportedCcontent. Inaddition,thedifferenttypesof
soilcarbonstabilityindicatorsusedamongstudiesprecludeddirectcomparisonofresponseratios. For
example,itisimpossibletocompareQ values(proxyfortemperaturesensitivityofsoilrespiration
10
andmicrobialdecomposition)withproportionofmineral-associatedcarbonorwithSOCthatismore
easilydecomposable(incubation)orsoluble(hot-waterextraction). Thesystematicliteraturereview
yielded23references,totalling93cases(TableA1). Thewidespreadgeographicdistributionofstudies
acrossNorthAmericawasconsideredagoodcoverageofthetremblingaspenrange(Figure1).
3. Results
Soil C concentration remains largely unaffected by the presence of aspen relative to conifers.
AllcasesreportingCconcentrationsinforestfloorandmineralsoilshownosingulareffectofaspen,
exceptinonestudywhereforestfloorCconcentrationislowerunderaspenthanunderconifer(Table1).
ForestfloorCcontentislowerunderaspenthanunderconiferintwothirdsofthestudies(14outof
21cases),whileinmostcasesnovegetationeffectsaredetectedintheSOCcontentofthemineralsoil
(18outof25). ThestabilityofSOC,asexpressedbythevarietyofCstabilityindicatorsusedinthe
differentstudies,isforthemajorityofthecaseshigherunderaspenthanunderconifer,especiallyin
themineralsoil(13outof19). TotalSOCstorage(FF+MIN)isgenerallynotdifferentamongvegetation
types. Theseindicatorsaredegreeoforgano-mineralassociations,proportionofreadily-availableor
labileCestimatedduringlong-termsoilincubationsorusinghot-waterextraction,patternofsoilC
distribution,andtemperaturesensitivityofsoilheterotrophicrespiration. Therearealsocases(twoout
offive)pointingtowardahigherstabilityintheforestfloor,albeitlesspronouncedthaninthemineral
soil. NoneofthestudiesshowadeclineinSOCstabilityforaspenineithersoillayer.
Thepotentialfactorsthatcouldmodulateaspeneffectwerenotfullyindependentoverthefull
geographicextentofthestudy.Forexampleconiferspeciesdistributionco-variedstronglywithclimate
(Table A1). Nevertheless, the most robust trends that were observed, specifically the absence of a
specieseffectonCconcentrationsandonmineralsoilCcontent;thenegativeeffectofaspenonforest
floorCstocksaswellitspositiveeffectonmineralsoilCstability,werefoundoverthefullgeographical
rangecoveredbythedataset(TableA1). Moreover, studieswithoppositeresultsregardingaspen
effectswerefrequentlyfoundwithinasamegeographicarea(TableA1). Theseresultssuggestthatthe
directionandimportanceoftheaspeneffectsaredependentonlocalconditionsorspecificityofthe
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experimentaldesignssuchassitehistory,localdrainageconditionsortimesincestandestablishment.
Unfortunatelythelackoflargescalegeographicpatternsinaspeneffectsdoesnotallowtoidentify
factorsresponsiblefortheimportanceordirectionoftheseeffects.
Table1.Numberofcaseswherethepresenceofaspencausedanincrease,adecrease,ornochangein
forestfloor(FF)andmineral(MIN)soilCconcentration,content,andstabilityrelativetoconifers.
CConcentration CContent CStability
Effect
FF MIN FF MIN FF+MIN FF MIN
Increase 0 0 1 2 1 2 13
Decrease 1 0 14 5 0 0 0
Noeffect 10 12 6 18 5 3 6
Totalnumberofcases 11 12 21 25 6 5 19
Boldhighlightsthemaineffectineachcolumn.Dataextractedfrom23papers.
4. Discussion
4.1. AspenDoesNotIncreaseSoilCButPromotesItsStability
ThesizeoftheSOCstockisgenerallynotsignificantlydifferentbetweenaspenandconiferstands.
While aspen tends to store less C in the forest floor relative to conifers, mineral soil C storage is
generallysimilar,makingtotalSOCstoragenotsignificantlydifferentamongforesttypes,giventhe
largevariabilityofsoilcarboncontentsinthemineralsoilandtherelativelylowcontributionofforest
floortototalsoilcarbonstorage.AnotableexceptiontothispatternisfoundintheIntermountainWest,
whereSOCstocksarehigherunderaspeninsitesinNorthernandSouthernUtah[3,28]. However,
thereisstrongevidencethataspenpromotesSOCstabilityintheentiresoilprofile,butespeciallyin
themineralsoil. Indeed,Cstabilityinthemineralsoilisclearlyhigherinaspenstandsrelativeto
coniferstandsin70%ofthestudies,withnostudiesshowingadeclineinSOCstabilityassociated
withthepresenceofaspen. Amultitudeofindicatorsserveasproxiesfordeterminingthishigherlevel
ofCprotectioninaspensoilsthatpointatthemechanismsofstabilization. TheCO releasedduring
2
long-termsoilincubationsathightemperature,andexpressedasafractionoftotalSOC,serveasthe
mostdirectindicatorofSOCreadilyavailabletomicrobes(i.e.,labileSOC).Numerousstudiesshow
thatSOCunderaspenisindeedlessdecomposablerelativetoconifers[3,29,30],althoughtwostudies
didnotdetectanydifferencesamongstandtypes[31,32]. ArecentmultisitestudyinUtah[28]further
supports lower SOC lability under aspen, as indicated by hot water extractions. The temperature
sensitivityofsoilheterotrophicrespiration,relevantforpredictingsoilClossesinawarmerworld,is
alsolowerinaspenthaninsprucestands,indicatingthatenhancedsoilClossesinresponsetoclimate
warmingmaybelesspronouncedinaspenstandsthaninconiferousones[33].
AcrossthevariousSOCfractionationtechniques,SOCassociatedwiththeclayandsiltparticles
is considered most stable, as the organo-mineral associations confer one of the strongest chemical
protectionmechanismsagainstClossesviamicrobialdecomposition,leaching,anderosion[34–37].
Thelightfractionoruncomplexedorganicmatterfraction,ontheotherhand,hasnochemicalbond
betweenCandmineralsurfacesandisconsideredtobemoreresponsivetoenvironmentalchangesand
soildisturbances[34,36].WhencomparingSOCfractionsbetweenaspenandconifersoils,considerably
moremineral-associatedSOC(uptoone-third)isfoundinthetopsoilunderaspen[28,38]inseasonally
drymontanesitesofwesternUSA,whileconifersstoreaslightlyhigherproportionofSOCinthelight
fraction[28]. Similarly,inthemoremesicclimateofeasternCanada,aspenstoreproportionallyless
SOCintheuncomplexedorganicmatterfraction[39].
Moreover,thelocationoftheCstoredwithinthesoilprofilealsohasimplicationsforlong-term
stability of SOC. Deep soil layers are generally colder, less aerated, sometimes waterlogged,
and generally more nutrient-limited relative to surface layers, thereby limiting microbial biomass,
microbialactivity,andassociatedClosses[37]. TheSOClocatedintheforestfloor,incontrast,ismore
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vulnerabletoenvironmentalperturbations,fire,andmanagementactivities[40–42]. Thus,soildepth
becomescriticalinassessingSOCstoragepotential[43].
WhiletherearecasespointingtowardahigherCstabilityofaspenintheforestfloor,albeitless
pronouncedthaninthemineralsoil(twocasesoutoffive),itshouldbenotedthatthesedatapoints
arederivedfromthesamestudyconductedindifferentregionsofCanadawithdifferentconiferous
species[30].
Collectively,theavailabledatashowthataspendoesnotconsistentlyalterthesizeofthetotal
SOCstock. PresenceofaspenisoftenassociatedwithadecreaseinforestfloorCcontent,andashiftof
SOCtolowerdepthsinthesoilprofilecomparedtonearbyconifers. Thisisconsistentwithpublished
synthesisreportsindicatingthatbroadleavesstorelessCintheforestfloorlayerrelativetoconifers,
whileeffectsinthemineralsoilareinconclusive[26,27,44]. Aspenpresence,however,facilitatesSOC
stability,whichmayincreasetheresistanceandresilienceofsoilCstockstoglobalchanges.
4.2. DriversofAspenEffectsonSoilCarbonStability
4.2.1. LitterQuantity
Theproductivityoftheforestecosystemandtherelatedfluxesofdetritusfromvarioussources
intothesoilmayinfluenceSOCaccumulationandstabilization. Aspenisoftencharacterizedbyhigher
productivitythanotherspeciesgrowinginthesameenvironment[6,45],resultinginagreaterinfluxof
abovegroundandbelowgrounddetritusintothesoil. ArecentcomparativestudyinUtahindicates
annual overstory foliage C inputs of 724 ± 175 kg C·ha−1 for aspen vs. 475 ± 82 kg C·ha−1 for
conifers[28]. Thisissimilartoobservationsincentral-easternCanada,comparingtotalaboveground
inputs(foliar+woodylitter): intheOntariosites, averageannualinputsare1325 ± 36kgC·ha−1
foraspen,1136±67kgC·ha−1 forjackpine,and1119±51kgC·ha−1 formixedconiferousstands,
whereasintheQuebecsites,annualinputsare1233±57kgC·ha−1foraspenand926±129kgC·ha−1
forblacksprucestands[30]. Whilelitterfallunderaspenissubstantiallyhigherthanunderconifers,
thelinkbetweenlitterfallquantityandSOCstabilityinthemineralsoilisnotstraightforward. Infact,
consideringthegrowingevidenceofhighersubstratequalitypositivelyaffectingCstabilizationin
mineralsoil(e.g.,[46,47]),itisdifficulttodifferentiatebetweentheeffectsofquantityandqualitywhen
comparingaspenandconifer. Inaddition,doublinglitterinputswithoutchanginglitterqualityin
a20-yearcontrolledexperimenthadnoeffectonSOCstability[48]inaNorthernhardwoodforest,
suggestingthatlitterqualityisastrongerdriverthanlitteramounts.
Muchlessisknownaboutrootdetritusinputs. Finerootproductionconstitutesanimportant
portion (one-third to three-quarters) of annual net primary productivity (), and due to their short
lifespan,rootscontinuouslycontributetothesoilorganicmatter()pool[49]. Aspenexhibitslarge
intraspecificvariationinrootmorphologicaltraitsduetogenetic,biotic,andabioticfactors[50–52]. When
comparingaspenfinerootbiomasstothatofconifers,thefindingsarenotconsistent. Forexample,
BauhusandMessier[53]andLaganièreetal.[6]shownodifferencesbetweenaspenandconiferstands
intheCanadianborealforest,asdoesAyresetal.[54]forthetop10cmofsoilatasiteinColorado,
whileBocˇaandVanMiegroet[28]reportmuchhigherfinerootbiomassunderconifersinUtah.
InthestudybySteeleetal.[51],deadrootscomprisefrom24%to47%oftotalfinerootbiomass,and
finerootturnoverisnotdifferentbetweenaspen,jackpine,andblackspruce.Sincesoilconditionswere
notsimilaramongstands,theseresultsmustbeevaluatedwithcaution. BocˇaandVanMiegroet[28]
reportthatdeadrootbiomasscomprises32%ofaspenand36%ofconifertotalfinerootbiomass,while
Laganièreetal.[6]indicateahigherproportionofdeadvs. totalfinerootbiomassunderaspenstands
(29%)relativetojackpine(18%)ormixedconiferstands(17%). Finéretal.[55]reportthataspenfine
rootsdecomposesignificantlyfasterthanthoseofadjacentconifers. Blocketal.[56]alsoreportedthat
aspenfinerootsarerelativelyshort-lived,withlifespansrangingfrom30to300days. Considering
similarorlowertotalrootbiomass(althoughwithvariableproportionofdeadroots)andthesimilar
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turnoverrates(rootproduction/totalrootbiomass),rootdetritusinputperseisunabletoexplainthe
morestableSOCinaspensoils.
4.2.2. LitterQuality
Thechemistryofabovegroundandbelowgrounddetritalinputsvariesamongtreespeciesand
associated understory, and can affect SOC stability via many mechanisms, including biochemical
recalcitranceorchemicalsorption. Whenaspenfoliageorrootlitteriscomparedtothatofconifers,a
generallyconsistentpatternemergesatthecontinentalscale,pointingtowardhigherqualityofCinputs
underaspen. Indeed,theC/Nratio,theacid-insolubleresidueorKlasonlignin,aswellasthelignin
monomerVphenolaresignificantlylowerinaspenfoliagelitterthaninconiferneedles[28,54,57–59],
althoughlitterchemistrymayvarydependingonbioticandabioticconditions[60,61]. LowerC/N
ratioofaspenrootlitteralsoindicateshigherdetritusqualityandfasterdegradationpotential[28,29].
Multipleexperimentshaveshownthatlitterfromaspendecomposesatahigherratethanthatfrom
conifers,atleastinearlystagesofdecomposition[59,62]. Also,theforestfloormaterialunderaspen
hasbeencalculatedtohavealowermeanresidencetimethanlitterunderconifers[28,63]. Ithasbeen
hypothesizedthatthefasteralitterisdecomposedthemorerecalcitrantandcomplextheremaining
organic matter will be [64,65]. Indeed, Giardina et al. [29] reported that high quality aspen litter
can eventually result in low quality SOC relative to lodgepole pine, as indicated by cumulative
carbonemissionsinincubatedsoilsfromnorthernColorado. Long-termaspen-coniferfoliarlitter
decompositionexperimentsalsotendtosupportthishypothesis. Aspenfoliageinitiallydecomposes
atafasterratethanconiferlitter,butdecompositionratesconvergeafterafewyears,sothatmass
remainingofaspeniscomparabletoconiferspeciesorhigherinsomecases[57,62]. Whilethequality
oflitterinputsaffectsSOCstabilityintheforestfloorviarecalcitrance,othermechanismsmayoperate
moreindirectly,conferringgreaterstabilitytoSOCinthemineralsoilunderaspen.
Astrikingdifferencebetweenaspenandconiferforestsobservedinthenorthernregionsisthe
higherpHandhigherCacontentofaspenlitter,generatinghighersoilpHandexchangeablebase
cationconditionsinthevicinityofaspentrees[4,66,67]. Redistributionofsoilnutrientsfromrelatively
deepmineralsoilhorizonstotheupperforestfloorlayerviaanabundantlitterfallhasoftenbeen
documented,andaspenhasbeenidentifiedasaCapump[68,69]. Calciumcanplayaroleinaggregate
stability [36,70]. In addition, higher Ca levels have been found to reduce the output of dissolved
organiccarbon(DOC)andmineralizableSOC[71,72].
Moreover,thegeneralhigherpalatability,pH,andnutrientcontentsofbroadleaflitterrelative
to conifer needles are favourable to macrofauna [73,74]. For example, a microcosm experiment
demonstrated that aspen litter, as well as humus derived from aspen trees, was more favourable
to earthworms [59]. Earthworms participate actively in the formation and stabilization of soil
aggregates[75–77]. Therefore,themorefavourablesoilconditionsformacrofaunalorganismsunder
aspenmaybeconducivetogreaterSOCstabilisation. Itisnoteworthythatthesespecies-inducedsoil
chemistryeffectsarenotobservedinthesouthernpartoftheaspenrange,inseasonallydrymontane
sites. ThelackofmeaningfuldifferencesinpHofaspenandconifersoilsintheIntermountainWest
canpotentiallybeexplainedbythelackofexcessiveleachingandbasestrippingintheseseasonally
drysoils,ortheinputofdustfromthesurroundingdesertareas[78]. Also,asnotedbythelackof
anysightingsofearthwormsinthisarea(e.g.,[54]),earthwormactivitydoesnotseemtoplayarolein
SOCredistributionandstabilizationattheselocations,probablyduetothedrysoilconditions.
Finally,higherqualitysubstrates,whileleadingtofasterforestfloordecompositionrates,also
couldresultinhighermicrobialutilization,andcould,therefore,contributetogreaterSOCstabilisation
withinthestablemineral-associatedfractionduetohighermicrobialbiomass,andmoremicrobial
by-products[79]. Indeed,spectralanalysisofUtahsoilsseemstoindicatethattheCcompoundsof
mineral-associatedSOCarerathersimpleinstructure(e.g.,polysaccharidesratherthanaromatics)and
likelyofmicrobialorigin(RománDobarco,Unpublisheddata;seeS1forMaterialsandMethods).
Forests2017,8,113 7of15
Thus,inthelong-term,SOCderivedfromhigh-qualitylittercanresultingreaterSOCstorage
andstabilization. Thedocumentedfasterdecompositionofaspenfoliarandrootlitter,potentiallydue
toalowerC/Nratioandloweracid-insolubleresidues,coupledwiththefindingsthataspensoilslose
lessSOCthroughheterotrophicdegradationduringincubations[3,29,30]supportthishypothesisfor
aspen-coniferforests.
4.2.3. TheImportanceofUnderstory
AnotherimportantaspectoftreespeciesinfluenceonSOCstabilityismediatedthroughtheassociated
understory cover. Understory plants growing in aspen forests can constitute an important above-
andbelowgroundCfluxtothesoilsystem[28]. Aspenstandshavebeenshowntosupporthigher
understoryplantspeciesbiomass,diversity,andproductivitycomparedwithadjacentconifers[6,7,80].
Understorycompositioncanhaveastrongimpactonsoilcharacteristicsthatmaybeevengreater
thanthatimpartedbyoverstorycomposition. Forexample,thebryophytelayerusuallyestablished
underconifersisamajorconstituentofsoilorganicmatterinborealforests[81–83]. Bryophytesalter
microclimateconditionsbyincreasingsoilmoisturecontent,andreducingsoiltemperatureaswellas
litterdecompositionrate[84,85]. Anincreasingabundanceofaspeninconifer-dominatedforestshas
beenassociatedwithadecreaseinbryophyteabundance,reductionoftheforestfloorthicknessand
soilmoisture,andanincreaseinsoilpH[73,86].Thedevelopmentofabryophytederivedorganiclayer
underborealconiferstandscreatesaSOCreservoiroflowstability. Indeed,inspiteofremarkablylow
decompositionrates[87–89],bryophytederivedorganiclayerhaslittlecontactwithmineralparticles
because,unlikevascularplants,itdoesnotgrowrootsintothemineralsoilandhencethereislittle
possibilityfororgano-mineralinteractions[39]. Inaddition,theaccumulationofthislayercangenerate
cool and wet soil conditions that slow down organic matter decomposition [30]. However, such
conditionsthatmaintainSOCmaynotberesilienttoadisturbanceorachangeinspeciescomposition
thatwouldpreventbryophytegrowth.
Interestingly, the above-mentioned effects mediated by the associated understory vegetation
couldnoteasilyhavebeenobservedincommongardenstudiesorinintensiveplantations,wherethe
understoryplantcompositionisusuallystronglyaltered. Thisfurtherunderscoresthehighvalueand
thecomplementaryroleofusingnaturalforestsorextensiveplantationswhenstudyingtheeffectof
treespeciesonsoilpropertiesandprocesses.
4.2.4. RootingPatternandRhizosphereProcesses
TheverticaldistributionofrootbiomassiscloselylinkedtothedistributionofSOCwithdepth[90].
Therefore,differencesinrootingdepthpatternsamongtreespeciesmayaffecttheverticalplacement
ofSOCwithinthesoilprofile,withimplicationsforSOCstability. Whilenotmuchdataareavailable
onrootingpatterns,StrongandLaRoi[91]documentedtheroot-systemmorphologyofsomeboreal
species,showingthataspenrootsarewelldistributedthroughoutthesoilprofileandcanreach1m
indepth. Bycomparison,therootsofblacksprucerarelygobeyondadepthof30cm,andmostof
themarelocatedattheorganic-mineralinterface. Thismayexplain,inpart,whythepresenceofaspen
is associated with a decrease in forest floor C content and proportionally higher amounts of SOC
indeeper,moreprotectedsoilhorizons. However,inUtah,BocˇaandVanMiegroet[28]foundroot
biomassCtobepositivelycorrelatedwiththelightfraction(i.e.,thelessstablefractionofSOC).
Wearenotawareofastudythathasexploredtheextenttowhichaspenandconifertreesdirectly
affectsoilCturnoverandmicrobialbiomassthroughtheirrhizodeposits. Higherspecificrootlength
(SRL)ofaspencomparedtoconifers[50,51,53,92,93]suggestsahighervolumeofsoilexploitedand
affectedbyrhizosphereprocesseslikerootexudationanddetritusinput[94]. Thiscouldsuggestmore
dynamicbelowgroundprocessesunderaspen.
Rootdynamicsareaffectedbythetypeofassociatedmycorrhiza;forexample,thedecomposition
rateofectomycorrhizal(ECM)rootshasbeenreportedtobeslowerthanthatofnon-ECMroots[95].
Most conifers have ECM associations, while aspen have ECM and arbuscular mycorrhizal (AM)
Forests2017,8,113 8of15
associations,withECMdominatinginthetopsoilclosesttothelitterlayer,andAMmoredominantin
thedeepersoil[96]. Brzosteketal.[97]founddifferencesinrootexudationandformofNproduced
when comparing two ECM and two AM tree species. The quantification and characterization
of root exudates, and the microbial activity around them, as well as detritus turnover, and the
interactions between rhizosphere and detritusphere, present directions for future research aimed
atbetterunderstandingthemechanismsofhowaspenbelowgroundprocessesaffecttheformation
andpreservationofmorestableSOCthanconifers.
4.3. FactorsResponsibleforInconsistencies
Fromtheavailabledata,weareabletodetectaclearandconsistentpatternofenhancedsoilC
stabilityinaspensoilsthroughoutNorthAmerica,andseveralpotentialdriversofSOCstabilitycan
beidentified. Atthesametime,itappearsthatpatternsofSOCstabilizationcanvarygeographically,
suggestingthatecosystemdriversofSOCstorageandstabilizationaremodulatedbyseveralabiotic
factors,inparticularclimateandintrinsicsoilproperties(geology,texture,soildepth)inlinewiththe
conceptofinteractingsoilformingfactors[98].
Theroleofclimatecanplayoutinmanyways. InthewesternUSwateristhemainlimitingfactor
ofaspenproductivity,whileitistemperatureatitsnorthernrange[99]. Thishasseveralimplications.
Forexample,theroleofaspenasacalciumpumpandthehigherconcentrationofthiselementinfresh
litterrelativetothatofconiferlitter,whichcanenhancesoilpH,inturnaffectingthesorptionand
desorptionoforganiccompounds[100],isnotobservedinthedryportionofitsrange. Becauseof
thelimitedverticalwatermovementinthisseasonallydryarea,soilsgenerallyhaveabundantCa
reservesandahighpH,andveryfewdifferencesemergebetweenaspenandconifersoilpHandbase
saturation[3,32]. Ontheotherhand,indicatorsoflitterquality,suchashighernutrienttoCratiosand
lowerligninconcentrationsforaspen,areclearerinthewesternUS[28,54]. Woldeselassie[101]further
observedthatevenwithinthesamewatershedinnorthernUtah,SOCstocksinthemineralsoilunder
aspencanvaryconsiderablywithaspect,presumablyduetomicroclimatedifferences(temperature,
moistureavailability),andtheirimpactonCinputsandlossesthroughdecomposition. Specifically,
SOCtoadepthof40cmwassignificantlydifferent(p<0.05)amongtransectswithwestandnorth
facingaspects,whichwerewetterandhadlowersoilCstocks;whilethedriersouthandeastfacing
siteshadthehighestSOC.Thissuggeststhatdrierconditionsinthisregionineffectcanfavourgreater
Cstorage. Bycontrast,inthenorthernregions,thedevelopmentofamosslayeriscommonunder
conifersandhasatemperatureisolatingeffectonsoil,whichdelaysthedegradationoforganicmatter,
slowingdownitsmicrobialtransformationtowardsmorestableforms—amechanismnotpossiblein
dryregionslackingabryophytecover.
Geographic differences in forest productivity rates are an obvious explanatory factor for the
variability in overall SOC storage among the studies used in this analysis. Differences in forest
structurewithinthesamesitealsoseemtoinfluenceSOCstorage,whetherdirectlythroughdifferences
inproductivityorindirectlythroughitsinfluenceonunderstoryabundanceorcomposition. Thisis
illustratedinthestudiesfromNorthernUtahandSouthernUtah,whichshowedthataspentreedensity
ortreesize(anindexforcanopyopenness)significantlyimpactSOCstorageunderpureaspen[101],
whilemineral-associated(stable)SOCconcentrationispositivelycorrelatedwithaspenabundancein
mixedaspen,asexpressedbylivebasalareaofaspen[38].
Mineral soil characteristics could also influence the tree species effect. Román Dobarco and
VanMiegroet[38]showedthatsoilmineralcharacteristicscanoverrideoramplifyvegetationeffects,
astheyobservedthatdifferencesinCstocksbetweenaspenandconifersweremostpronouncedat
highsiltandclaycontents(40–70%clay+silt),whiledifferencesremainedlesspronouncedincoarser
soiltextures(<40%clay+silt). BocˇaandVanMiegroet[28]showedapositivecorrelationbetween
CconcentrationinthesoilsandextractableFeandAlthatcouldexplaindifferencesinSOCpools
betweenanorthernandsouthernUtahsite. Overall,thesefindingsunderscoretheinterplaybetween
abiotic(edaphic)andbiologicalfactorsincreatingstableSOCpools.
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5. Conclusions
Oursystematicliteraturereviewshowsthataspeneffectonsoilcarbonisrelativelyconsistent
throughoutthespeciesrange. ItshowsthataspenstoreslessCintheforestfloorbutsimilaramounts
in the mineral soil relative to conifers. However, the expression of a vegetation effect on mineral
SOCstoragemaybeconstrainedgeographicallybytheimportanceofotherbioticandabioticfactors.
Nevertheless,arobustsetofindicatorsofsoilCstability,suchasdegreeoforgano-mineralassociations,
proportion of readily-available or labile C estimated during long-term soil incubations or using
hot-waterextraction,patternofsoilCdistribution,andtemperaturesensitivityofsoilheterotrophic
respiration,revealsthatSOCunderaspenismorestableandwouldbethusmoreprotectedagainst
environmentalchangesandsoildisturbances. Therefore, ourcontinental-scaleanalysishighlights
thatanincreaseintheabundanceoftremblingaspeninNorthAmericanforestscouldbebeneficialto
theresistanceandresilienceofbelowgroundsoilCstocksagainstglobalchanges. Disentanglingthe
relativeroleofvegetationvs. abioticeffectsonSOCstabilization,oridentifyingandquantifyingthe
relativeinfluenceofindividualdrivers,remainsachallengethatshouldbetakenupbyscientists.
Acknowledgments:WethankJulienBeguinforassistancewiththegenerationofFigure1andHeatherAlexander
forprovidingcoordinatesfortheAlaskasites. WethankLaurentAugustofortheopportunitytosubmitan
invitedpaperforthisspecialissueofForests.Wearegratefultothreereviewerswhoseconstructivecomments
significantlyimprovedthismanuscript.
AuthorContributions:J.L.,D.P.,andH.V.M.designedthestudy.J.L.andA.B.conductedtheliteraturereview
andcollectedthedata.Allauthorswrotethepaper.
ConflictsofInterest:Theauthorsdeclarenoconflictofinterest.
Forests2017,8,113 10of15
AppendixA
TableA1.Descriptionofthestudiesincludedthissystematicliteraturereviewandsummaryofresults.Aspencauseseitheranincrease(+),adecrease(−),orno
change(0)inforestfloor(FF)andmineral(MIN)soilCconcentration,content,andstabilityrelativetoconifers.Whenasimilareffect(+,−,or0)isobservedmore
thanonceperreference,thenumberofcasesshowingthiseffectisindicatedinbracketsnexttotheeffectsign.
Reference Location CSpoenciifeesr1 (SYteaanrd)Age2 SDaemptphli(ncgm) SoilType (M◦CA)T3 (MmAmP)4 N FCFConcentMraItNion FCFContentMIN FF+MIN FCFStabMiliItNy Indicators5
Alban1982[68] MN Pg,Pr,Pb 39–40,41–49 FF,0–61, Alfisols 4 610 1 0,-(5) 0(2),-(4)
0–80
AlexanderandMack2016[102] AK Pm 20-100 FF,0–10 Gelisolsto n.a. 286 2–14 0(3) 0,-(2) 0(3)
Inceptisols
Ayresetal.2009[54] CO Pc,Pe n.a. 0–10 n.a. n.a. n.a. 4 0(2) 0(2)
Bauhusetal.1998[103] QC Ab+Pg 50,124 FF,0–10 Spodosols,Alfisols 0.6 823 1 0(4) 0(4)
BocˇaandVanMiegroet2017[28] UT Ptm+Al+Ac+Pf mature FF,0–50 Alfisols,Mollisols 3.2,4.5 1031,823 4 - + 0 +(3) A,B,C
FF(OA),
BuckandSt.Clair2012[104] UT Al+Pe+Ptm n.a. n.a. 10.1 201 10 0 0
0–10
Côtéetal.2000[31] QC Ab+Pg 50,124 FF,0–10 Spodosols,Alfisols 0.6 823 4 0 0 0 0 0 D
DobarcoandVanMiegroet UT Ptm+Al+Ac+Pf mature 0–15 Alfisols,Mollisols 3.2,4.5 1197,812 6,5 0(2) 0(2) 0(4),+(2) A,B,D
2014[38]
Giardinaetal.2001[29] CO Pc 40–250 0–15 n.a. 0.5 700–850 6 + D
Hannametal.2004[105] AB Pg 80–140 FF Alfisols −0.6 433 3 - 0
Hannametal.2005[106] AB Pg 80–140 FF Alfisols −0.6 433 3 - 0
Jerabkovaetal.2006[107] AB Pgmainly 70–125 FF,0–7 Alfisols −0.6 433 3 0 0 0 0
Kishchuketal.2014[108] AB Pgmainly 62–124 10–17 Alfisols −0.6 431 3 0
Laganièreetal.2009[73] QC Pm 79–89 FF Alfisols 0.8 890 3 -
Laganièreetal.2011[39] QC Pm 90 0–15 Alfisols 0.7 890 8 + A
Laganièreetal.2012[33] QC Pm 90 n/a Alfisols 0.7 890 8 + E
Laganièreetal.2013[30] QC,ON Pm,Pb 90,83 FF,0–55 Alfisols,Inseptisols 0.7,2.5 890,712 8,4 0,- 0(2),- 0(2) +(2) +(2) C,D
Lamarcheetal.2004[109] QC Pg+Pm+Ab 57–131 FF Alfisols,Spodosols 0.8 857 18 0
OlsenandVanMiegroet2010[32] UT Al+Pe mature 0–30 Alfisols 7 950 3 0 0 D
ParéandBergeron1996[4] QC Pg 49–123 FF,0–10 Alfisols 0.6 823 8 - 0
Ste-Marieetal.2007[69] QC Pb 59–89 FF,0–20 Alfisols,Spodosols 0.7 890 3 0,+ 0(2)
Weishampeletal.2009[110] MN Pb+Pr+Ab 20–58 FF,0–40 Alfisols 3 785 3–15 - 0 0
Woldeselassieetal.2012[3] UT Ptm+Pe+Al+Pc mature FF,0–60 variable 4.5 890–950 6 - 0,+ + +(3) A,C,D
1Ab,Abiesbalsamea;Ac,Abiesconcolor;Al,Abieslasiocarpa;Pb,Pinusbanksiana;Pc,Pinuscontorta;Pe,Piceaengelmannii;Pf,Pinusflexilis;Pg,Piceaglauca;Pm,Piceamariana,Pr,
Pinusresinosa;Ptm,Pseudotsugamenziesii;2n.a.,informationnotavailable;3MAT,meanannualtemperature;4MAP,meanannualprecipitation;5Stabilityindicators:A,degreeof
organo-mineralassociations;B,water-extractableC;C,patternofsoilCdistribution;D,proportionofreadily-availableorlabileCestimatedduringlong-termsoilincubations;E,
temperaturesensitivityofsoilheterotrophicrespiration.