The Case of Aspen and Soil Carbon in North America PDF
Preview The Case of Aspen and Soil Carbon in North America
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.:+1-418-648-4329;Fax:+1-418-648-5849 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, Forests2017,8,113;doi:10.3390/f8040113 www.mdpi.com/journal/forests 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 Forests2017,8,113 4of15 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 Forests2017,8,113 5of15 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 Forests2017,8,113 6of15 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. Forests2017,8,113 9of15 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.
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