Belowground foundations of tropical forest restoration

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Biotropica. 2024;56:e13296.  
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https://doi.org/10.1111/btp.13296
wileyonlinelibrary.com/journal/btp
Received:21August2023
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Revised:7N ovember2 023
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Accepted :12Decemb er2023
DOI:10.1111/btp.13296
COMMENTARY
Belowground foundations of tropical forest restoration
Lindsay A. McCulloch1,2 | Cecilia M. Prada1 | Wenying Liao1 | Marijn Bauters3,4 |
Lauren Church1 | Ming Yang Lee5 | Laura Toro6,7 | Viktor Van de Velde3 |
Anita Weissflog7 | Michelle Wong8,9 | Benton N. Taylor1
1Depar tmentofOrganismicandEvolutionaryBiology,Harvar dUniver sity,Cambridge,Massa chusetts,USA
2Nationa lCenterforAtmosphericResearch,NationalOceanographican dAtmosp hericA genc y,Boulder,Col orado,USA
3IsotopeB ioscienceLab orator y(ISOFYS),DepartmentofGreenChemistr yandTechn ology,GhentUniversit y,Ghent,B elgium
4ResearchGroupPLECO(Plant sandEcosystem s),Depar tmentofBiolog y,UniversityofAntwerp,Wilrijk,Belgium
5AsianSchooloftheEnvironment,NanyangTechnologicalUniversit y,Singapore,Singapore
6Depar tmentofPlantandMicrobialBiology,Univer sityofM innesota,St.Paul,Mi nnesot a,USA
7SchooloftheEnvironment ,YaleUniversity,NewH aven,Connecticut,USA
8CaryInstit uteofEcosystemStudies,M illbro ok,NewYork ,USA
9Depar tmentofEcologyandEvolut ionar yBiology,YaleUniversity,NewH aven,Connect icut,U SA
Correspondence
LindsayA.McC ulloch,DepartmentofOrga nismicandEvoluti onar yBiolog y,HarvardUnive rsit y,Cambridge1300CentreSt .Roslin dale,MA02131,USA.
Email:la.mcculloch9@gmail.com
Funding information
OrganizationForTropicalSt udies,Grant /AwardNumber:Rex fordDau benmireFellowshipFund514/564;NOA AClimateandGlobalChangePostd octor al
Fellowsh ip,Grant/AwardNum ber:NA18NWS4 6200 43B
Associate Editor:JenniferPowers
Handling Editor: Jayashree Ratnam
Tropical fores ts are exper iencing dras tic human land u se changes
suchthat currently half of theworld's tropical forests are regener-
atingsecondary forests (FAO,2020). Thishasspurred immensein-
terest inrestorationefforts,suchasARF100,theBorneoInitiative,
Initiative20x 20,andForestStewardshipCouncil,toaidthe natural
regenerationoftropicalforests(UNEP&CBD,2018;UNIQUE,2020;
Vergaraetal.,2015).Restor at io nr ange sf romp assive toac tivestr at-
egies, such as natural regeneration to active species selectionand
inoculationwith nativesoil.However,restoration efforts areof ten
not effective (Lindenmayer,2020) . One of the reaso ns is the lack
of connection with ecologicaltheor y and processes(e.g., compe-
tition, dispersal, succession), par ticularly with belowground pro-
cesses.Belowgroundprocessesarerelativelyunderstudied(Averill
etal.,2022;Seidl&Turner,2022;Werdenetal.,2022),yettheinter-
actionsofplantroots,soilmicrobes,andsoilpropertiesdrivecritical
belowgroundecosystemser vicessuchaserosioncontrol,waterand
nutrientcycling, and soil carbon sequestration. Attention to these
critical interactions has the potential to substantially increase the
success of restoration efforts. Here we highlight the most import-
ant belowground processes for active tropical forest restoration
(Figure 1),whenspecificrestorationpracticesshouldbeconsidered,
andsuggestkeyresearchpriorities.
Belowground processes are of ten mediated by microorganisms,
whichcreatecritical links between plants and soil (Figure 1b). These
plant–microbial interactions can occur via established symbioses
wheremicrobesarephysicallyconne ctedtoplantroots(e.g.,symbiotic
nitrogen-fixingbacteriaandmycorrhizalfungi)orviathefree-livingsoil
microbialcommunity(e.g.,throughrootexudationandsoilpathogens).
Interac tions betwee n roots and soil mic robes often dri ve reciprocal
effectsbetweenplants and the soil,called plant–soilfeedbacks(PSF),
which canmakethe local soil either more (positive PSF) or less(neg-
ative PSF) favorable toparticular plant species.These plant–microbe
inte rac t io nsare im p or t a nt fo rfo re s tr ecove r y,a sh igh li ghted by ag lob al
analysisshowingplantbiomassrecovered64%fasterafterinoculating
plantswithmicrobiomesfromnativeecosystems(Averilletal.,2022).
Disentangling the multitude of plant–soil–microbe interactions
and their impact s on the many belowground processes relevant to
tr op ica lfo re s tr est ora tionc anb ec hal le ngi ng.Wes t ruc t ur eou ra r ticle 
around several keyrestoration objectives: soil stabilization and c ar-
bonstorage,nutrient cyclingrecovery and forestgrowth, and forest
diversityandmultifunctionality.Herewedefineforestmultifunction-
ality as:aforestecosystemthatcan providea mixofenvironmental,
©2024AssociationforTropicalBiolog yandConserv ation.

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ecological, economic, and social services and goods (Mansourian
etal.,2005).Foreachoftheserestorationobjectives,wehighlightthe
management strategies that can impact the respective belowground
players an d processes , and call for m ore inclusio n of plant–soil–mi-
crobe interactions in restoration research and practice.
1 | SOIL STABILIZATION AND CARBON
STOR AGE
Oneobjectiveofrestorationissoilstabilizationtopreventerosion
a n df u r t h e r d eg r a d a t i o n ,w h i l e pr o m o t i n gc a r b o n s t or a g e . I nc r e a s e d
carbon storage can be observed in less than a decade when above-
groundcarbonismeasuredinrestoredareas(Philipsonetal.,2020),
withchangesinsoilcarbonstocksoccurringupto40 years(Holl&
Zahawi,2014;Jonesetal.,2 019;Zaninietal.,2021).However,the
trajec tories of soil st abilization ( Ford et al., 2016), plant survival
(Werden et al., 2022), and soilcarbonstorage(Craig et al., 2018)
in regenerating forests are affec ted by the belowground plant
growthstrategiesoftheselectedplantspecies(Figure 1c).Forex-
ample,specieswiththickfinerootsanddeeprootstructureshave
been linked to slower growth rates andplantestablishment, both
ofwhich increase the amountofcarbon storedin the ecosystem
(Werdenetal.,2022).Theem ergenceofglob alroottraitdatabase s
(e.g., Iversen et al., 2017)havehighlightedfunctional groupsthat
can help restoration practitioners select species that aid in recov-
ery. However, fur ther linking and t ranslating t raits to ecos ystem
functionisnecessaryforsuccessfulrestoration.
When forests are converted from dif ferent land uses, the soil's
physical, chemical, and biological properties change, leading to shift s
in fungal s pecies com position an d diversit y (Jones et a l., 2003; Wubs 
et al., 2016). To ensure successful establishment, the proportion of
arbuscular versus ectomycorrhizal trees should be selected based
on the nati ve or reference eco system. Pla nts form nutr ient acquirin g
FIGURE 1 Graphicaldepictionof
how(a)restorationactionsthatexplicitly
consider(b)importantbelowground
element scanrestore(c)keybelowground
processesduringtropicalforest
regeneration. Key belowground elements
(roottrait s,mycorrhizae,nitrogen-
fixingbacteria[N-fixers],andothersoil
microbes)influencesoilstabilization
andcarbonstorage,nutrientcycling
recoveryandforestgrowth,andforest
diversit yandmultifunc tionality.Various
roottraitsandmycorrhizaecanpromote
thestabilizationofsoilandprotect
against erosion while also contributing
tosoilcarbonstorage.Mycorrhizaeand
N-fixerssupporttherecoveryofnutrient
cyclingandforestgrowthovertimefor
reforestedareasinthetropics.Further,
plant–soilfeedbacks(PSF)cansupport
thediversityandmultifunctionalityof
tropicalforeststhroughbothpositiveand
negativePSF.Thebelowgroundprocesses
that are mediated by these belowground
characteristicscanbeinfluencedthrough
restorationactions(depictedhereinthe
topleftwithahandaddingseedsfrom
selectedplantspecies,seedsinoculated
withmicrobialsymbionts,and/orsoil
inoculumdependingontheneedsofthe
forestbeingrestored).
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symbioses with arbuscular and/or ectomycorrhizal fungi. Arbuscular
mycorrhiz al fungi grow into root ce lls and send hyphae in to the soil
to scavenge fo r available nutr ients and ecto mycorrhizal fun gi form a
sheath around roots and breakdown organic material themselves to
access soilnutrients (Phillips et al., 2013).Successful establishment of
treesandtheirmycorrhizalfungiwilllikelyhavebeneficialeffectsonsoil
proper ties that facilitate carbon storage andnutrient cyclingthrough-
outregeneration, asfoundinotherecosystems(Asmelashetal.,2016;
Policellietal.,2020). Myc orrhizalsymbiose scans tabi lizesoilsviahy ph al 
networks and increase carbon storage via production ofcompounds
suchasglycoproteins(glomalin),whichslowdowndecomposition(Rillig
etal.,20 01; Figure 1b,c).Morespecifically,arbuscularmycorrhizaltrees
stimulate fast carbon cycling and mineral-associated organic matter
formation, whileec tomycorrhizaltrees drive slow decompositionand
buildupofsurfaceorganiclayers(Craigetal.,2018;Pradaetal.,2021).
When implementing active restoration, practitioners should
considerrestoringnativemycorrhizalcommunities.Providingnative
soilin oculu mi ncrea sesfu nga lb io mas sa nd abu nd anc ew hi leals oe n-
hancingabovegroundplantprocesses(Maltz&Treseder,2015;Wubs
etal.,2016; Figure 1a).However,wecautionthatmanycommercially
availablemycorrhizalinoculacontainnon-nativeandunsuitablemy-
corrhiz al taxa for mos t tropical fore st restorati on project s. These
inocula couldbeineffective or detriment al tothe goal of restoring
healthy native soil microbial communities and successful regener-
ation. Usin g native soil fo r mycorrhizal inocu lum can be be neficial
andprovideasuiteoffungalsymbiontslocaltotheregion.However,
practitionersmaywanttoexperimentwithwheretheysourcetheir
local so il inoculum fro m before full imp lementati on, as plants' re -
sponses t o soil inoculu m depend on t he successio nal stage of th e
ecosystemthattheinoculumwascollec tedfrom(Allenetal.,2003).
2 | NUTRIENT CYCLING RECOVERY AND
FOREST GROWTH
Recovery of soil b iogeochemic al cycling se rves as a key prer equi-
site to abovegr ound biomass regene ration, and soil microbes are
essential to biogeochemical cycling. The standing paradigm indi-
catesthattropicalsecondaryforeststransitionfromnitrogen(N)to
phosphorus(P)limitation(Powers&Marín-Spiotta,2017; Figure 1c),
and both mycorrhizae andN-fixing bacteria play an important role
inthesenutrientcycles.Forexample,mycorrhizalfungicanincrease
the connectivity andavailability of nutrient pools in anecosystem
by accessin g various for ms of nutrien ts, such as P, that can not be
accessed by plants (Smith & Read, 2010), thereby increasing plant
biomass,height,andspeciesrichness(Neuenkampetal.,2019).
In additi on to mycorrhizal f ungi, restor ation pract itioners have
long recognized the potential benefits of plants that form rela-
tionship s with N-fixing bacte ria (hereafte r referred to as N-fixers ;
Figure 1b)because of their ability to bring new N into the ecosys-
temand growfastasseedlings(Chaeretal.,2011).Thisiscriticalas
theN cycle can take more than 52 yearstofullyrecover(Amazonas
et al., 2011). By e nhancing soi l N from the deco mposition of t heir
N-richt issues(Bink ley& Giardina, 1997), N-fixers can co unteract
largeNlossesfromdisturbances(BooneKauffmanetal.,1995;Neill
etal.,2006)andincreasebioavailableNtomeetthehighplantNde-
mandinearlysuccessionalstages(Battermanetal.,2013;Levy-Varon
etal., 2019). However,practitioners shouldnotonly plantNfixers,
asNfixerscancompetewithneighboringtrees,negativelyaf fecting
regener ation (Taylor et al., 2 017), and inc rease soil N2O emissions
ifNavailabilityanddemandbecomeunbalanced(Kou-Giesbrecht&
Menge,2019). Wesuggestthatactive plantingofNfixerswilllikely
bemorecriticalinN-limitedecosystems(Smith-Martinetal.,2 017),
suchasmontanetropicalforests( Tanneretal., 1998) orhighly dis-
turbed o r degrade d ecosyste ms, and less s o where N is abu ndant,
suchashighly-weathered,stableoxisols(Huddelletal.,2022;Wong
etal.,2020)orregions withhighNdepositionthat may increaseN
availabilityintheenvironment(Kou-Giesbrecht&Menge,2019).
Soilcation(positivelycharged)nutrient s,suchascalcium,influence
soi l p H a n d n u t r ientm o v e m e n t i nthes o i l . T h e s e c a t i o n sc a nalsob e n e g -
ativelyimpactedbyland-usechangeandmayrequirespecialattention
inrestorationeffort s(Bauters etal.,2021;Bauters,Grau, etal.,2022;
Bauters,Janssens, et al., 2022,Figure 1c).Cationsarepredominantly
stored in woodybiomass,thus thesenutrients are depleted from the
ecosystemwhenbiomassisremovedfromnativeforests.Givencation
inputsaregenerallylow,thelong-termimpactsofcationdepletionwar-
rantfurtherstudyandtheconsiderationofcationamendmentsduring
active restorationto soils that are particularlydepleted,inaddition to
themorecommonfertilizeramendmentsofnitrogen,phosphorus,and
potassium(Fajardoetal.,2013;Toroetal.,2024).
3 | FOREST DIVERSITY AND MULTI FUN
CTI ONA LITY
Plant–soilfeedbacksare alsoimpor tant forincreasingdiversityand
multifunctionality of recoveringforests (Figure 1c), supporting the
resilien cy of these trop ical forest s (Bennett & K lironomos, 2 019).
Positive (mutualistic) and negative(pathogenic)PSFcanaffecttree
species' establishment (Sarmiento et al., 2017) and performance
(Eck et al., 2019; Manganet al., 2010) by making the environment
favorableforspecificplantgroups,affectingtheirlocalabundances
(Figure 1b,c). For example, as succession proceeds, tree species
may experience strong negative PSF (pathogen pressure) where
and when they peak in abundance during succession, as host-
specificmicrobiotamaybelocallyabundant(Bagchietal.,2014;Liu
et al., 2015). Thus, both positive and negative PSF c an affect tree
diversit yinmatureforests(Bagchietal.,2014; Comitaetal.,2014;
Corralesetal.,2016;Manganetal.,2 010)andcontext-dependency
ofPSFmaystronglycontributetosuccessionaltrajectories.
Overall,evidencestronglyindicatesthatPSFsincreaseandmain-
taintropicalforestdiversity.Diverseforestshaveahigher capacity
toservemultiplefunctions,aremoreresilienttofuturedisturbances
(Messieretal.,2022,Figure 1c),andhavehighercarbonstoragepo-
tential.However,directincorporationofPSFsintoforestrestoration
plansisinitsinfancy,andthecomplexityofthesefeedbacksmakes
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McCULLOCH e t al.
theirmanagementdifficult,particularlyinthediverseforestsofthe
tropics.Atthe broadscale, restorationefforts targeted at increas-
ing soil he alth and micr obial diver sity can e nhance PSFs an d their
subsequentsupport ofdiverse, multifunctionaltropicalforests.For
example,evennativesoilinoculationsthatbringsoilpathogensmay
bebeneficialoverallbypromotingtreespeciesdiversity.Iflocalsoil
inoculumisbeingused,collectingfrommultipleareasandhomoge-
nizingbeforeimplementationcouldmaximizethebenefitsofPSF.If
activerestorationincludesselectingseedsorseedlingsforplanting,
it is impor tant that practitioners select species that are not just di-
versephylogeneticallybutalsowithrespecttotheirfunctionaltypes
tomaximizetheresilienceand func tion oftherestored area.Given
the vast diversit y of tropical forest ecosystems, small pilot studies
maybebeneficialforinformingwhichplantspecies toprioritizefor
plantingbeforelarge-scaleeffortsareimplemented.
4 | NEX T STEPS IN BELOWGROUND
TROPICAL FOREST RESTORATION
Inadditiontobiogeochemicalandecologicalbelowgroundprocesses
thatsupportsuccessful restoration,wemustbalancethe economic
andsocialneedsofrestorationareasduringthenextdecade(United
Nations,& WorldBank, 2022).Strongerpartnershipsbetweensci-
entistsandrestorationpractitionerswillhelpachievethisgoal(Holl
&Brancalion,2022;Powers,2022).Practitionersvalueinexpensive
managementstrategiesandtangibleresult s(e.g.,numberofplanted
trees, t ree surv ival, amou nt of biomass st ored) that c an be imple-
mented at la rge scales (H oll & Branc alion, 2022). However, scien-
tistsoftenfocusonmeasuringmorecomplexmetricsofrestoration
success at smaller scales(e.g., pollination,belowground carbonse-
questration,nutrientcycling;Melietal.,2017 ).Giventhismismatch,
effortstoidentifyaccessible,inexpensivemetricsthatrepresentthe
recoveryof belowground processes,andinparticularthe potential
ofsoil microbestofacilitateandsupport restorationeffortswillbe
critical to meet global restoration targets.
Microbiome interventions, such as inoculating plants prior to
planting o r transferr ing soil from int act ecosyste ms, are promisin g
to o l sto a cce l e r ater e gene r a t iona n drec o veryo f e cos y s t e mp r o c esse s 
(Averilletal.,2022; Figure 1a).However,theimplementationofthese
strategies in tropical forests should be carefully evaluated based
onplant–microberelationships, ecosystemtype(e.g.,dominanceof
ectomycorrhizal symbionts inm ontaneforest s andarbuscular my-
corrhizal symbionts in lowland forests) and initial biogeochemical
conditions(Neuenkampetal.,2019).Moreover,extensiveknowledge
aboutbeneficialsourcesofinocula(Maltz&Treseder,2015)andana l-
yses that compare the cost-effectiveness of topsoil transplantsand
commercially available microbes at large scales are needed to suc-
cessfullyrestoretropicalforests(Brancalionetal.,2 019).
While evidence suggests that active management of below-
ground processes c an provide substantial restoration benefits,
our understanding of these processes lags far behind that of abo-
veground forest dynamics. Here,wepropose several next stepsto
advance our understanding of belowground processes and tropical
forestrestorationsuccess:
• Researchers designing projects about active restoration should
partner and communicate with local restoration practitioners be-
forehandtoensure theirresearchobjectives willprovide action-
ableinformationtoimprovelocalrestorationef forts.
• Moretargetedstudiesareneededtodeterminethelong-termef-
fectsofarbuscularversusectomycorrhizaldominanceoncarbon
andnutrientcycling inrestoredforestsandfurtherevaluate the
feasibilityofactivelymanagingmycorrhizaldominanceataresto-
ration site.
• Often,Nfixersareprioritizedinactiverestorationeffort s,despite
equivocalevidencethattheybenefitforestregrowth.Futurework
shouldfocuson understandingthecontextinwhich prioritizing
plantingNfixersisadvantageousversuscounterproductive.
• C ations represent important and potentially limiting nutrients
outsideofNandPforforestrestorationandtheeffectsofcation
fertilizationwarrant sfurtherstudy.
• For belowgr ound trait-based (i.e. ro oting depth, r oot thicknes s)
approaches to be widely adopted in futurerestoration projects,
agreatereffortisneededtocharacterizethebelowgroundfunc-
tionaldiversit yacrossthetropicstopredictspecies'performances
underawiderangeofenvironmentalanddisturbancegradients.
• Clear,specific, and accessiblecommunicationis particularlyim-
portantfor studiesfocusingonbelowgroundprocesses,as these
are often n ot explicitly i ncluded in many re storation goa ls. For
example,valuableinformationtopractitionerscouldincludebut
is not limited to seedling size (root: shoot ratio), belowground
traitsand their potential associated functions, fertilizer addition
amounts and composition used in experiments, microbial inoc-
ulations,reasoning for plantspecies selec tion andtheir primary
microbialsymbionts(N-fixingbacteria,mycorrhizaltype,etc.).
There is agreat push from governments, NGOs, stakeholders,
andthepublictorestoredegradedecosystems,particularlytropical
foreststhatplayanoutsizedrolein globalcarbon,water,andnutri-
entcycling.Herewe argue thatbelowgrounddynamics,particularly
plant–microbeinteractions,arefundamentalcomponentsofsuccess-
fultropicalforestrestorationthataretoooftenoverlooked.Further,
webelieve it is important to balancethe ecological,economic ,and
socialneedsofrestoredareas.Thus,bytranslatingbelowgroundre-
searchfromthescientificcommunityintopreciseandpracticalland
man agementst ra tegie sforr es torationp ra ctit io nerstofollow,future
restorationprojectsmaybemoreef fectivelyimplemented.
ACKNOWLEDGMENTS
We are grateful to the Association for Tropical Biology and
Conversation for suppor ting the symposium: “Tropical forest restora-
tion: Role of soilbiota-root symbioses”that inspiredthis commentary
and attendees who contributed their ideas and comment s during the
discus si on .A uth or sLA MandCMPweresupp ort edby th eO rga nizatio n
for Tropical Stu dies under the Re xford Daube nmire Fellowshi p Fund
17447429, 2024, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/btp.13296 by NANYANG TECHNOLOGICAL UNIVERSITY, Wiley Online Library on [25/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

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McCULLOCH e t al.
(Fund 514/564), and L AM was als o suppor ted by the NOA A Climate
andGlobalChangePostdoctoralFellowshipProgram,administeredby
UCAR'sCooperative Programs for theAdvancement of Ear th System
Science(CPAESS)underaward#NA18NWS4620043B.Wewouldlike
tothan ktheTaylorLabgroupforth eirfeedbac konane ar lydraftofthis 
commentary.
DATA AVA I L AB ILI T Y STATE M EN T
Nonewdatawaspresentedinthisarticle.
ORCID
Lindsay A. McCulloch https://orcid.org/0000-0001-6868-2632
Marijn Bauters https://orcid.org/0000-0003-0978-6639
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