Synthesis of the first 10 years of long-term ecological research in Amazonian Forest ecosystem: implications for conservation and management

h ttp://ww w . n a t u r e z a e c o n s e r v a c a o . c o m . b r

Natureza

&

Conservação

Brazilian

Journal

of

Nature

Conservation

SupportedbyBoticárioGroupFoundationforNatureProtection

Essays

and

Perspectives

Synthesis

of

the

first

10

years

of

long-term

ecological

research

in

Amazonian

Forest

ecosystem

–

implications

for

conservation

and

management

Fernanda

V.

Costa

a,∗

,

Flávia

R.C.

Costa

a

,

William

E.

Magnusson

a

,

Elizabeth

Franklin

a

,

Jansen

Zuanon

a

,

Renato

Cintra

a

,

Flávio

Luizão

a

,

José

Luís

C.

Camargo

a,b

,

Ana

Andrade

b

,

William

F.

Laurance

b,c

,

Fabricio

Baccaro

e,a

,

Jorge

Luiz

Pereira

Souza

a

,

Helder

Espírito-Santo

d a_{InstitutoNacionaldePesquisasdaAmazônia(INPA),Manaus,AM,Brazil}

b_{BiologicalDynamicsofForestFragmentsProject,InstitutoNacionaldePesquisasdaAmazônia(INPA),Manaus,AM,Brazil}

c_{CentreforTropicalEnvironmentalandSustainabilityScience&CollegeofMarineandEnvironmentalSciences,JamesCookUniversity,}

Cairns,Australia

d_{PostgraduateEcologyProgram,InstitutoNacionaldePesquisasdaAmazônia(INPA),Manaus,AM,Brazil}

e_{UniversidadeFederaldoAmazonas(UFAM),Manaus,Amazonas,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received26November2014 Accepted11March2015 Availableonline5May2015

Keywords: Globalchanges Habitatloss Long-termstudies Spatial-temporalvariations Selectivelogging

a

b

s

t

r

a

c

t

Wepresentasynthesisofthefirst10yearsofLongTermEcologicalResearchprojectin AmazonianForest.Weelucidatethenaturaldynamicsofforestecosystemprocessesand associatedbiota,anditschangescausedbydistinctpressuresofselectivetimberextraction andforestfragmentation.Wefoundthat,forbothplantsandanimals,densitiesof individ-ualsanddistributionofspeciesassemblagesarespatiallyheterogeneousatthemesoscale, eveninrelativelyundisturbedforests,andthatassociationswithtopo-edaphicvariables allowpredictionofaconsiderablepartofthisvariation.Forbiologicalgroupswhose dynam-icswerestudiedintheshort-term,levelsofchangeinspeciescompositionanddensities wererelativelyhigh,andthesechangesweregenerallyintunewithspatial environmen-talvariation.Theimpactofselectiveloggingonassemblagesandecosystemprocesseswas normallymoderate,andaround19yearswereneededforrecoveringforestbiomassandtree sizedistribution.Continuedstudiesareneededtodeterminethetimerequiredfor recuper-ationoftimberstocksandpre-loggingfloristiccomposition.Selectiveloggingappearstobe compatiblewiththebiodiversityconservation,butreductionandbetterplanningofroad accessmaybemoreimportantthanplannedloggingintensities.Habitat-loss’impacton organismsandecosystemprocessesislargeandlong-lasting,sinceitinducesthelossof manytaxonomicgroupsandspecies,highertreemortalityandacceleratedforestdynamics. Therewasanegativesynergybetweentheimpactsofhabitatlossandclimaticchanges,and abetterunderstandingoftheseprocessescanonlybeobtainedthroughlong-termresearch. ©2015Associac¸ãoBrasileiradeCiênciaEcológicaeConservac¸ão.PublishedbyElsevier EditoraLtda.Allrightsreserved.

∗ _{Correspondingauthor.}

E-mailaddresses:[email protected],[email protected](F.V.Costa). http://dx.doi.org/10.1016/j.ncon.2015.03.002

Introduction

Growth ofhuman populationsand economicactivities are transformingtropicalforestsinto amosaic ofaltered envi-ronments, pastures and isolated forest fragments, with severeconsequencesforbiodiversity(Bierregaardetal.,1992;

Lauranceetal.,2011).ThedestructionofAmazonianforests

grew exponentially during the 1970sand 1980s (Fearnside,

1987,1990),andcontinuestoimpactdynamicsoffauna,flora

andecosystemprocesses.

Humanactivitiesintropicalforestareasrangefrom selec-tivetimberextractionwithmoderateenvironmentalimpacts to complete deforestation for agro-pastoral and industrial activities (Laurance and Vasconcelos,2009). Understanding howandtowhatextenttropicalforestecosystemsrespond todifferentanthropogenicactivitiesprovidesusanimportant baseforenvironmentalplanning,managementand monitor-ing,allessentialforthepromotionofsustainabledevelopment oftropicalenvironments,suchasAmazonia.

Inresponsetothesechallenges,researchersoftheNational Institute for Amazonian Research (INPA) included Central AmazoniaintheBrazilianprogramforLongTermEcological Research–LTER(hereafterreferencedasLTER-Site#1) estab-lishedbytheBrazilianNationalResearchCouncil(CNPq).The aimoftheprogramistocollectandorganizedataonthe struc-ture and functioning ofthe principal Brazilianecosystems inorder togenerate aknowledge basetoevaluate biologi-caldiversity,andsubsequentlyproposeplansforsustainable useandconservation.TheLTER-Site#1(Fig.1)istheoldest

AmazoniansiteintheBrazilianLTERprogram,andincludes threeforestreservesmanagedbyINPAthatdifferinlanduse intensity.Allsitesarecoveredbyevergreendenseterra-firme forest.

TheDuckeForestReserve(RFD)islocated26kmnorthof Manaus(2◦5547.80S;59◦5830.34W),andcovers10.000ha (10×10km).Thisareadoesnotsufferenvironmentalimpact withinitsborders,butissurroundedbyurbansprawlfrom Manauscity.Allstudieswereconductedinpermanentplots regularly distributed acrossthe landscape. The Experimen-tal ForestManagementStation(ZF2)islocatedabout 90km northeastofManaus(2◦38S,60◦11W),andwassubmittedto selectiveloggingtreatmentsin4-haplots,arrangedinthree blocks.Eachblockhasonecontrolunloggedplot,threeplots loggedin1987,andoneplotloggedin1993toassesstheeffect oftimeaftertimberextraction.Theloggedplotsexperienced differentintensitiesoftimberextraction.Alltheseplotswere establishedintheuplandflatterrain(“plateau”),tominimize topographiceffects.ThereservesoftheBiologicalDynamicsof theForestsFragmentsProject(PDBFF)aresituated80kmfrom Manaus andspanabout1.000km2_{.Thestudyareaincludes} 11 forest fragments (fiveof1ha, four of10ha, and twoof 100ha),andexpansesofnearbycontinuousforestthatserveas experimentalcontrols.Intheearly1980s,thefragmentswere isolated from nearbyintactforestbydistancesof80–650m byclearingandburningthesurroundingforest.Moststudies performedinPDBFFassessedtheeffectoffragmentation com-ponents–sizeoffragmentsandedgeeffect–onbiodiversity, ratherthanevaluatingfragmentationasalandscapeprocess asproposedbyFahrig(2003,2013).

Fig.1–LocationofLTER-Site#1incentralAmazonia,andthepositionofthestudiedareasonnorthofManuscity.(1)Ducke

ForestReserve(RFD),(2)ExperimentalForestManagementStation(ZF2)and(3)ReservesofBiologicalDynamicsofForest

[image:2.612.132.459.425.712.2]

Table1–TablesummarizingLTER-Site#1areaswithitsrespectivestudiedgroupsandenvironmentalcharacteristics affectedbyeachpredictorofchangeevaluated.

Area Predictorofchange Studiedgrouporcharacteristicaffected

DUCKE

Soiltexture/topography Plantbiomass,treemortality,wooddecomposition,nutrientcontent Plantcomposition(palms,herbs,shrubs,treesandlianas)

Fungirichnessandabundance(leaflitterfungi)

Animalcomposition–vertebrates(birds,primates,lizards,snakesandamphibians)and soilinvertebrates(ants,pseudoscorpions,mitesandtermites)

Distancefromriparianzone Plant(palms,herbs,shrubs,treesandlianas)andbirdcomposition Vegetationstructure

WaterandWatershed properties

Animalcomposition(birds,snakes,frogs) Wooddecomposition

Compositionofaquaticfauna(fishandinvertebrates) Floristiccomposition

Time Treebiomass,treemortality

Fungirichnessandabundance(leaflitterfungi) Vertebrates(fish)andinvertebrates(pseudoscorpions)

ZF2

Skiddertrails Richnessandcompositionofunderstoryherbs

Loggingintensity Treeregeneration,biomass,treespeciesrichness,volumeoftimberspecies Nutrients

Timeafterlogging PopulationabundancesofVertebrates(lizards,frogs)andinvertebrates(antsand termites)

Treespeciesrichness,treebiomass,deadbiomass,understoryherbs Vertebrates(understorybirds)

Soilproperties/topography Treebiomass

Plantcomposition(understoryandtreespecies,lianasandpalms)

PDBFF

Plantlitter,arborealbiomass,treemortality GlobalClimatechange

Edgeeffects

Climaticattributes(light,desiccation,heatandwinds)

Ecosystemprocess(germination,pollination,dispersionandherbivory) Habitat

loss

Micro-climaticregime,waterflow

Forestdynamics(plantmortality,recruitment,andgrowth,gapformation) CompositionandrichnessofVertebrates(birds,primates,mammals,fishandfrogs) andinvertebrates(buterfliesandaquaticinsects)

Plantcomposition(palms,trees)

Since these areas are similar in terms of experimental designs (samples collected with standardized protocols in permanentnonfloodedevergreen rainforestplots)wewere encouraged tosynthesize the information carriedout dur-ingthelast10yearsofresearchbytheBrazilianLTER-Site#1 (1999–2009).Here,wepresentasynthesisofthemain stud-iesundertakeninthisperiod,coveringrelationshipsbetween ecosystemprocessesandassociatedbiotawithdifferentland uses,suchaschangesinnaturalforestlandscapes,impacts causedbyselectivelogging,andintenseforestfragmentation. Thebiologicalgroupsstudiedandenvironmental character-isticsaffectedbyeachpredictorofchangeevaluatedineach areaaresummarizedinTable1.

Biodiversity

and

ecosystem

processes

vary

within

the

mesoscale

topography

Thetropicalforestischaracterizedbyamplenaturalvariation generatedbydifferences insoilcharacteristics,topography, climateandvegetationstructure.StudiesinRFDatLTER-Site #1,Central Amazonia,have shownthat withinmesoscales (10.000ha), soil and topography gradients are the princi-pal factors responsible for differences between landscape elements.

Thelocaltopography,consistingofplateaus, slopesand stream valleys,clearly influencessoil texture and nutrient

distribution. Soilclaycontent ishighonplateaus and low-lyingareashavesandysoils(Araújoetal.,2002;Luizãoetal., 2004).Thenitrogenconcentration(N)inleaves,plantlitterand theuppersoilstratumwerefoundtobelowerinvalleysthan onslopesandplateaus.Thecarbonconcentration(C)didnot varywithtopography,resultinginhighC/Nratiosinvalley bot-toms.ThelowquantitiesofNcirculatinginvalleysarelikely attributabletosandysoilsandseasonalflooding(Araújoetal.,

2002;Luizãoetal.,2004).

Levels of nitrogen mineralization and nitrification were significantly lower in soils of valleys, with N immobiliza-tionmainlyobservedduringtherainyseason(Luizãoetal., 2004). The production of fine plant litter(maximum stem width≤2cm)anditsdecompositionwereslightlygreaterin plateausascomparedtovalleys(Luizãoetal.,2004).Therefore, athicklayerofleavesaccumulatesoversandysoilsduetothe scarcityofnutrientsfoundinthesesoils,whichthenresults inrelativelyslowerdecompositionrates.Thelocaltopography (plateau,slopeandvalley)clearlyinfluencesthelitterandsoil nutrientdistribution.Thesedifferencesshouldbeconsidered intheconstructionofmodelspredictingcarbonemissionrates thatusedataondecompositionintheirestimates.

[image:3.612.52.552.79.424.2]

inclay-richsoilsofplateauswhilepalmbiomassisgreater insandysoilsofslopesandvalleys.InthePDBFFareas,tree biomassincreaseswiththequantityofclayinsoilsaswell assoilfertility,mainlyduetonitrogen(Lauranceetal.,1999). However,thecorrelationbetweenbiomassandnitrogenmay be due to the contribution of leaves to soil nitrogen, and notcausedbysoilnitrogencontent.Sincesoilvariablesare markedlyinfluencedbylocaltopography,thesestudiesshow theimportanceoftakingintoaccounttopographytoimprove ourcurrentestimatesofcarbonstocksoverlargeareasinthe Amazon,anditcanbeeasilyassessedusingsatelliteimagery. Theprocessofwooddecompositionislargelyindependent ofsoilcharacteristics,topography,and vegetationstructure

inRFD (Toledoet al., 2009). The absence of a relationship

betweenwooddecompositionandvariablesinfluencingtree biomassanddecompositionofplantlitterindicatesan asym-metrybetweenproductivityanddecomposition,whichshould intheorybringaboutagreateraccumulationofdeadwood invalleys,whereratesoftreemortalitywerereportedtobe greater(Toledoetal.,2012).AccordingtoToledoetal.(2012), thegreaterproportionoftreedeathduetouprootinginvalleys waslikelytoberelatedtorestrictionsonrootestablishment duetoanoxicsupersaturatedsoils,andthereducedneedfor finerootsbecauseofthegreateravailabilityofphosphorous invalleysoils.Together,thesefactorsfavorlowinvestmentin subterraneanbiomassinvalleys.

Biodiversitydistributionfollowssimilarpatternstothose observedforecosystemprocesses.Studiesdemonstratethat thecompositionofplantsinmanyfunctionalgroupsstudied inRFD(herbs,palms,shrubs,treesandlianas),aswellasfungi, isstronglyassociatedwithedaphicconditions,changing grad-uallyalongthetopographicgradientthatextendsfromsandy, poorandpoorly-drainedsoilsofvalleystomoreclay-richand well-drainedsoilsofplateaus(Costaetal.,2005,2009;Kinupp

andMagnusson,2005;Braga-Netoetal.,2008;Druckeretal.,

2008;Schiettiet al., 2013; Rodrigueset al., 2014).Similarly,

studies from non-fragmented areas of the PDBFF reserves show that topography and soilfertility affect the distribu-tionofunderstoryplants(Harmsetal.,2004),lianas(Laurance et al., 2001), arboreal successional species(Lauranceet al.,

2006a),andthecompositionofthetreecommunity(Bohlman

etal.,2008;Lauranceetal.,2010).

Someanimal groups, especiallythose assumed to have limiteddispersal–suchasamphibians(Meninetal.,2008)and soilinvertebrates(Araújo,2007;Franklinetal.,2007;Oliveira

etal.,2009;Dambros,2010;Souzaetal.,2012)–displayed

dis-tributionstosomedegreeassociatedwithtopographyandsoil characteristics.Thereisevidencethatabundanceand diver-sityofedaphicarthropodsareassociatedwithdifferentlevels ofC,P,Na andCainlitterand/orinsoil.Thispattern sug-geststhatqualityofsubstratemaylimitthesoilmesofauna inDuckeReserve.Approximatelyhalfoftheantspecieswere foundsolelyinvalleysor onlyonplateaus, suggestingthat themajorityare habitatspecialistsand dependofsoil tex-ture,whichisrelatedtomoisturecontent(Oliveiraetal.,2009). Pseudoscorpions,however,werenotfoundtobesensitiveto environmentalfactors,suchasterraintopography, percent-ageofclay insoils, quantityofplant litterorsoilpH, and assuch,canbeconsideredhabitatgeneralists(Aguiaretal.,

2006).

Groupswithamplegeographicdistribution,suchaslizards

(Pinto,2008a)andsnakes(Fragaetal.,2011)werealsofound

tobelittleaffectedbytopographicandsoilvariablespresent inthemesoscalecontextatRFD.Similarly,VidalandCintra

(2006)showedthatthetopographicgradientcharacterizedby

plateaus–slopes–lowlands(60–140mofaltitude)hadlittle effectontheoccurrence,sizeandgroupdensityofthe pri-mateSaguinusbicolor(Sauim-de-coleira,anendangeredspecies). However,owlsandbirdspeciescompositionchangesalongthe topographicgradient,andalsoinrelationtoleaflitterdepth and distance to forest streams. Compositional differences werealsofoundintheaviancommunityintheeasternand westernwaterbasinsthatcomposethereserve.Theseresults suggestthatalthoughmostbirdspeciesoccurthroughoutthe mesoscale,manyspeciestrackdifferencesinthelandscape andforeststructure(BarrosandCintra,2009;CintraandNaka,

2012).

Regarding aquaticfauna ofRFD, Mendonc¸a et al. (2005) showedthatfishspeciescompositionvariesbetweendrainage basins,andthatthis differenceisassociatedwithvariation inwaterchemistry,currentvelocitiesand substrate proper-ties.TheridgethatrunsdownthemiddleofRFDseparates thesetwomajorwaterbasins,withstreamstotheeast flow-ingtotributariesoftheAmazonRiverandthosetothewestto theNegroRiver(Mendonc¸aetal.,2005).Someterrestrialplant groups alsohadspecies restrictedtooneor anotherwater basin(Costaetal.,2005;Garcia,2005;KinuppandMagnusson, 2005).However,itisdifficulttoidentifywhichfactorsaccount forthis difference sincethereislittle variationin soiland other environmentalfactors betweendrainage basins.The onlyimportantdifferencebetweenwatershedsisthe avail-ablephosphoruscontent,whichmaybelinkedtothedrainage patterns.Sincethesewatershedsareseparatedbylowridges, theydonotrepresentbarrierstodispersalforsomegroups

(Costaetal.,2005).

Studieshaveshownthat,whileextremelyinterestingfor somequestions,itisnotgenerallyeconomicallyviabletofocus on exhaustivelists ofmegadiversegroups ofinvertebrates, suchasoribatidmitesandants.Forstudiesdesignedtodetect environmentalchanges,itisbettertoevaluatechangesinthe presence ofmorecommon species (Moraes et al., 2011) or evenuse reduced-samplingtechniques (Souza et al.,2009). For example,not sorting the less frequentspecies didnot severelyaffecttheobservedpatternofsimilarityamong sam-pleplots,indicatingthatmoreabundantspeciescanbeused assubstitutesforlessabundantspeciesinbiomonitoring stud-ies.Inaddition,thesamplingeffortreductiondidnotaffectthe capacitytodetecttheeffectofsoilpHforthecommunityof antgenera(Souzaetal.,2009).

10% of species turnover

Water table level 60

50

40

30

20

10

0

All life forms Trees

Shrubs 90% of species

turnover

Saturated zone

Horizontal distance from nearest drainage (m)

Height abo

v

e

the nearest dr

ainage (m)

Fig.2–Representationofthepositionswheremostchangesinplantcompositionoccursinrelationtothesmallforest

streams.Watertablefluctuationzoneisshowningray.Theblackarrowhighlightedisthemaximumextensionofthe

riparianarea(350m),givenlimitsdetectedinplantspeciescomposition.

AdaptedfromSchiettietal.(2013).

touselocalmicroclimatesmightbemorerelevantforfuture survivalthantheirgeneralassociationswithclimateatlarge scales(Antonellietal.,2010).

The

importance

of

the

riparian

zone

DiversestudiesinLTER-Site#1haveshownthatspecies com-position ofdistinct assemblages such as plants, frogs and tadpoles,snakesandbirds,variesinrelationtodistancefrom waterbodies(Druckeretal.,2008;Rodriguesetal.,2010;Fraga

etal.,2011;Buenoetal., 2012;Schiettietal., 2013).InRFD,

Druckeretal.(2008)showedthatthefloristiccompositionof

understoryherbsisdistinctfrom thatfoundupto approxi-mately100mhorizontallyfromtheedgeofstreams,orabove about70mabovedrainages,varyingslightlywiththesizeof thestreamvalley.Asaresult,theonlydistincthabitat recog-nizedbymostspeciesappearstoberestrictedtoareasaround streams.Furtheraway,differencesaresubtleandthepattern variesamongspecies.

Schiettietal.(2013)showedthatthefloristiccomposition

ofherbs,shrubs,palms, treesand lianasvary considerably betweenvalleys,butisrelativelyconstantinareasofhigher elevation(Fig.2).Mostchangesinspeciescomposition(about 90%)occur up todistancesbetween 8and 18min vertical drainageheight,dependingonthegroupofplants.This ver-tical interval is equivalent to a distance of approximately 60–250mhorizontally from waterways. Similarly,frogs and theirtadpoles(Rodriguesetal.,2010),understorybirds(Bueno etal.,2012)andsnakes(Fragaetal.,2011)studiedinRFDalso appeartorecognizeariparianzonesimilarinwidth (approxi-mately100–200m)tothatestimatedforunderstoryherbsand theotherplantgroups.

UnderBrazilianlaw,thewidthofprotectedriparian vegeta-tiondependsonthewidthofthewaterbody.Thislegislation mandatesprotectionofareaswithin30mforstreamsupto

10mwide, suchasthose that occurin theDuckeReserve. Our studiesshowed that this riparianarea issmallerthan thatrecognizedbymostanimalandplantgroups,andthat awidthof100–250mwouldbemoreappropriatefor conser-vationpurposes. Thestudies alsoshowed thataminimum verticaldistancefrom theclosestdrainageareawouldbea bettercriteriontoprotectbiodiversitythanprotectionbased onlyonahorizontaldistance.Thecriticalverticaldistance from drainage areas for conservations purposesshould be defined by the zone of groundwater fluctuation, and this willvaryamongAmazonianlandscapesdependingon topo-graphic variation, precipitation regime and soil properties. Thedifferencesinspeciescompositionbetweenriparianareas inadjacent smallwatershedsalsoindicate thateach small watershedhasanovelcontributionintermsofspeciestothe regionaldiversity.Thesefindingssupportourclaimthat nar-rowprotectedareas,asBrazilianlawprescribes,willnotbe sufficienttoprotectthemajorityofspecies.

Thefindingthatareasofhighestcompositionalchangeand mostdistinct fromothers inthe environment(about200m horizontallyoneachsideofstream,and8–18mverticallyfrom the riparianzone)arethose directlyaffected by groundwa-terfluctuationalsohasimplicationsforpredictingtheeffects ofclimate change.If the climatebecomesdrier in Amazo-nia, water storage in the soil and groundwater levels will decrease.Thiswillreducethesizeofriparianareasandcause changesinspeciescompositionsduetodifferencesindrought tolerance(Engelbrechtetal.,2007).Themajorityof tropical-forestspeciesarenotcapableofdispersingoverlongdistances

(Clarketal.,2005;Colwelletal.,2008;Terborgh etal.,2011)

and plantsalreadyconfinedtonarrowzonesneardrainage areaswillhavelittlerecoursetomigratetosimilar environ-ments.Thesespeciesmayalsobecomethreatenedbypressure fromspeciesofhigherareasthatwillbeabletoinvadeareas aroundstreamsasthegroundwaterleveldrops(Schiettietal.,

[image:5.612.100.504.63.254.2]

Spatial

and

temporal

variation

in

biodiversity

and

ecosystem

processes

Biodiversityandecosystemprocessesvarynotonlyinspace, butalsointime,andthistemporaldynamiccanalsoberelated toenvironmentalcharacteristics.Understandingthevariation oftemporaldynamicsinthelandscapeisimportantfor mod-elingscenariosforclimatechangeandconservationplanning. Astudy offish assemblies inRFD streams showedthat speciescomposition and fish abundance vary betweenthe dryandwetseason,withrichness(20%)andabundance(30%) being higher in the dry season. However, the composition tendstoreturntoitsoriginalstateattheonsetofthenextdry season,duetothecommonestspeciesthataccountforthe sta-bilityoffishassembliesoverthelongterm.Changesinspecies composition observedbetween seasonsappeartobe asso-ciatedwithlateralmigrationoffishtotemporarypoolsand othermicro-habitatsduringthefloodperiod(Espírito-Santo

etal.,2009,2013).Theseobservationsaresimilartolateralfish

migrationpatterns associatedwith largeAmazonianrivers (Junketal.,1989).

Braga-Netoandcollaborators(2008)foundthatspeciesof

leaf-litterfungirespondtotheinteractionbetweenedaphic conditions,whichvaryinspace,andtoprecipitation,which variesintime.Thenumberoffruitingmorphospeciesvaries alonganedaphicgradientonlyduringthedriestperiods,being lowerinclay-richanddriersoils.Duringtherainiestperiods oftheyear,humidity islesslimiting,resultinginasimilar numberofspeciesfruitingalongtheedaphicgradient.

Comparisonsbetween older studies (Adis and Mahnert,

1990,1993)andmorerecentones(Aguiaretal.,2006)on

pseu-doscorpionsshowedthatthesepredatorshaveaconsistent patternofabundanceanddiversityoverdecades.Thisresult suggeststhat distributionsofspeciesintheseassemblages arestableoverthelongterm,contrastingwiththevariations observedintheshorttermforotherorganisms.

Castilhoet al.(2010)showedthatthe short-termrateof

biomasschangeinRFDwaspredominatelypositiveinplotson clay-richandmorefertilesoils,andpredominatelynegativein plotswithsandyandinfertilesoilsduringthefirstmonitoring period(2001–2003),butnotinthesecond(2002–2004)(Castilho etal.,2010).Therefore,incontrasttoresultsofseveralrecent studies,thatdidnottakeintoaccounttheinteractionbetween climateandsoils,thatstudysuggeststhatlargeareasof Ama-zoniawithsandysoilsmaylosebiomassundertheconditions predictedbymostclimate-changemodels.Thepersistenceof thiseffectthroughtimestillneedstobeverified.

Theeffectsofsoilandtopographyontreemortalityalso vary temporally.Soil and topographyexplainabout 25% of thespatialvariationinsmall-tree(<30cmDBH)mortality dur-ing a period with heavy rain storms, while no effect was detectedduringaperiodoffewerstorms(Toledoetal.,2012). Themagnitudeofthe effectofsoilandtopographyontree mortalityalsoincreasedafterstorms.Ingeneral,plotswith lessfertilesoilsonsteepslopesorsandysoilsinvalleyshad greatertreemortalitythanthoseonwell-drainedclayeysoils ontheplateaus(Toledoetal.,2012).Infact,thehigher propor-tionofuprooteddeadtreesinvalleysinAmazoniahasbeen attributedtopoorsoildrainage,sincewaterexcessinthese

areasrestrictsrootestablishment,productivityoffineroots androotingdepth(EspeletaandClark,2007).

The dynamics of populations, species assemblages and ecosystem processesvary spatiallyon the landscapescale. Mostofthosestudiesreportedthatdynamicsdifferbetween differentlandscapeelements,suchasclayplateausandsandy valleys.Knowledgeofthesevariationsinnaturaldynamics acrossspaceiscrucialtointerpretchangesindynamicsdueto anthropogenicdisturbances.Wedemonstratethatlocal con-trolplotsthatdonotcoverthelandscapevariationwillfailto providethebaselinetowhichperturbationsshouldbe com-pared.

The

effects

of

selective

timber

extraction

on

biodiversity

and

ecosystem

processes

are

moderate

ExperimentaltimberextractioninZF2wasconductedinplots thatunderwentdifferenttimbercuttingtreatments:low(25%), moderate(50%),high(75%)andacontroltreatmentgroupthat correspondstotheprimaryforestswithoutwoodextraction

(HiguchiandBiot,1997).Theintensityofloggingineachplot

corresponded tothe reductioninvolumeofall commercial treesspecieswithDBH≥10cm.

Thestudiesintheareaofselectiveloggingindicatethat mostofthetreebiomasshadrecoveredby19yearsafter cut-ting. However,inthisperiod,commercialspeciesrecovered only66–88%oftheoriginalwoodvolume,suggestingthatmore time is needed forrecuperation ofthe timber stocksafter exploration(Pinto,2008b).Thecompositionoftheforeststill differsmuchfromtheoriginal,withcommercialspecies hav-inglower basalarea.Theextractionoflargetreesmaylead tochangesinthelongterm,becauseestablishmentofmany commercial hardwoodspeciesisslow.Logging significantly increasedrichnessofthetreeregeneratinglayerinrelationto controlplots(Magnussonetal.,1999)andaffectedtheoverall similarityinspeciescompositionamongplots,butthe mag-nitude of the effect was small comparedto the difference betweenonecontrolplotandallotherplots(Magnussonetal.,

1999).

Pinto (2008b) suggested that a cycle of30 years is

fea-sible for the forests to be managed again, if no external or internaldisturbanceoccurs.A compilationofstudiesin the BrazilianAtlanticforest(Liebschetal., 2008)estimated atleastahundredyears torecoverpre-disturbance propor-tions ofanimal-dispersedtreespecies(80%ofthespecies), non-pioneertreespecies(90%)andunderstoryspecies(50%). ConsideringthatthestudyatZF2wasfocusedoncommercial treespeciesandwascarriedoutundercontrolledconditions ofdisturbance,weemphasizethatthis estimateofatleast 30yearsisapplicableonlytocommercialplantsandactions fortimber management.Morestudies onlong termeffects ofloggingshouldbedonetopredictthetimenecessaryfor recuperationoftheinitialtreespeciescomposition.

accumulated vegetative residues that decomposed in the yearsfollowingcutting,contributingwithcarbonand nutri-ents to the soil, as well as CO2 to the atmosphere. The liberationofnutrientsfromcoarseleaflitterandwood decom-positionincreasedtheconcentrationofpotassium,calcium and magnesium available in the soils in the two years followinglogging.Necromassincreased,andthereforethe res-pirationratealsoincreasedinthefirstfiveyearsanduptoat least15yearsaftercutting.Pinto(2008c)comparedthe nutri-entcontentandstocksintreesoftwosecondaryforestsof differentagesandhistoryoflanduse.Treesinthesecondary growthafterlogging(forestof23yearsage)hadhigher nutri-entcontents(N,K,Ca,Mg,Na)thantreesinsecondaryforests developedafterclearcutting(forestof14yearage),showing theimportanceofusehistoryandtimeafterdisturbancefor theecosystemprocesses.

CostaandMagnusson(2002) examinedthe effectof

dif-ferentloggingintensities,timesinceloggingandtheskidder tracksonthecompositionanddiversityofunderstoryherbs. Nooveralldifferenceswerefoundinthecompositionofherbs betweenthedifferentloggingintensities,buttherewerelocal differencesinplantcompositionassociatedwitholdclearings andalong skiddertracks.Thecompositionand richness of herbsdidnotvarywithtimesinceloggingupto10years.Costa

and Magnusson (2002,2003) showed that selective cutting

affectsthereproductionofunderstoryplants,buttheseeffects werenotnecessarilynegative.Theabundanceand number offloweringplantspecieswasgreater 4yearsafterlogging andreturnedtocontrollevelsafter11years.Theintensityof logginghadnoimpactonthereproductionofthe understory-plantassemblages as a whole. However,for somespecies, reproductionwashigherinareaswithgreaterlogging inten-sity. Thesestudies demonstratethat managedforests with similarselectiveloggingintensitiescanbeusedforthe conser-vationofunderstoryherbspecies.Additionally,skiddertrails shouldbeminimizedsincetheycause greatestimpactover thelongtermandpermitcolonizationbyinvasivespecies.

Low-impactselectiveloggingcausedmoderateeffectson bothvertebrateandinvertebrateassemblages.Guilhermeand

Cintra(2001)showedthatthediversity,speciescomposition

andfrequencyofusebyunderstorybirdswerenotaffectedby differentloggingintensities,butwereaffectedbytimeafter logging.Theseauthorsshowedthatselectiveloggingdoesnot causegreatimpactsonbirdassemblages,andthat,insome situations,managedareascouldbeabetteroptionfor conser-vationinrelationtootherformsoflanduse.Incontrast,Lima

etal.(2001)foundthatselectiveloggingaffectedthreelizard

speciesdifferently.Theabundanceofonespeciesincreased withselectiveloggingwhileanotherspeciesdecreased.In con-trasttotheresultsforvertebrates,selectiveloggingdidnot affectthenumberofspeciesortotalabundanceofantsonthe forestground(Vasconcelosetal.,2000).However,differences inloggingintensitycausedchangesinthedensityofvarious speciesofants(Vasconcelosetal.,2000)andleaf-littertermites (Limaetal.,2000),andtheseeffectslastedformorethan10 yearsaftercutting.

Ingeneral,theeffectsofselectiveloggingweremoderate, and no species loss was recorded, even though the abun-danceofsomespeciesincreasedordecreased.Howeveritis importanttonotethat,inthesestudies,selectiveloggingwas

undertakenbyaresearchorganization,didnotexperienced forestfiresorotherdisturbancestypicallyassociatedwith ille-gallogging,anddidnotincludeanevaluationoftheimpacts ofaccessroads.Thisformofselectiveloggingappearstobe compatiblewithbiodiversityconservation,butreductionand betterplanningofaccessroadsmaybemoreimportantthan plannedloggingintensities,aconclusionalsoreachedinan areawithcommerciallogging(Diasetal.,2010).

Forest

fragmentation

strongly

affects

ecosystem

processes

and

associated

biota

Studiesonthecompositionanddynamicsofthetree assem-blagesinfragmentedareasofPDBFFatLTER-Site#1areoneof thelargestintermsofspatialextent(1.000km2_)and tempo-ralscale(approximately30years)anywhereintheworld.The impactofforestfragmentationontreeassemblageshasa pro-foundinfluenceonthelong-termpersistenceofanimaland plantpopulationsinfragmentedforests.Themicro-climatic regimeinfragmentsdiffersfromintactareas(Camargoand

Kapos,1995).Pastureoragriculturalareassurrounding

frag-mentshavelowerratesofevapotranspiration,andarehotter and drier. Theeffects ofdryingcan penetrate from 100to 200mintofragments,notnecessarilyfollowingalinear

pat-tern(CamargoandKapos,1995;Malcolm,1998;Didhamand

Lawton,1999).Waterbodiesinfragmentedlandscapespresent

greater temporal variationinflow than dothose in forest, duetothelowerratesofevapotranspiration(Trancoso,2008). Thesedifferencespromotelocalizedfloodinginthewet sea-son and stream failure in the dry season. Together, these climaticandhydrologicalmodificationshavelargeeffectson organisms and ecosystem processes, especially nearforest edges.

Edge effects in fragments are variable. They include increaseindesiccation,heat,light,andturbulencefromwinds amongotherclimatic factorsthatdirectly affectecosystem processes(Lauranceetal.,1997,2004a),suchasseed germi-nation andsurvivalofseedlings(Daviesetal.,1998;Bruna, 1999),pollination,seeddispersion,andherbivory(Harmsand

Dalling,1997;CordeiroandHowe,2001,2003;Terborghetal.,

2001),seedfall(DaviesandSemui, 2006;Nascimentoet al.,

2006),andnutrientcycling(Klein,1989).Fragmentationalso altersforestdynamics,increasingmortalityrates,tree dam-age and clearings formation (Ferreira and Laurance, 1997;

Lauranceetal.,1998a).Oneofthemostimportantimplications

abouttheincreaseintreemortalityisthelossoflivebiomass inthefirst100–300mofedge(Lauranceetal., 1997,1998a). Notonlydomoretreesdieinfragments,butthegreatest pro-portionofthesedeathsisalsoconstitutedbylargetreesthat makeupthelargestfractionofforestbiomass(Lauranceetal., 2000).Smallincreasesinbiomassoflianasandsmalltrees, andcoarseandfineplantlitterdonotcompensatefortheloss ofbiomasscausedbyincreasedtreemortality(Nascimento

and Laurance,2004).Mathematical modelspredictthat the

lossofbiomassincreasesabruptly infragmentswithareas between100and400ha,dependingontheshapeofthe

frag-ment(Lauranceetal.,1997,1998a).Thesemodelsalsosuggest

areascould beresponsibleforanannualemissionofmore than150milliontonsofcarbonintotheatmosphere(Laurance

etal.,1998b).

Areareductioniscommonlyassociatedwiththe impover-ishmentofbiodiversityinforestfragments.Reductionsinthe numberofspecieswithfragmentationwereobservedinalarge numberoftaxonomicgroupsincludingprimates(Gilbertand

Setz,2001;BoyleandSmith,2010),insectivorousunderstory

birds,(StratfordandStouffer,1999;Ferrazetal.,2007),palms

(Scariot,1999),andlargeherbivorousmammals(Timo,2003),

amongothers.However,smallerfragmentsdonotalwayshave fewerspeciesthanlargerfragments(Laurance,2008).Forsome taxonomicgroups,suchasbutterflies(BrownandHutchings, 1997),frogs(Tocheret al.,1997)andleaf-litterinvertebrates

(Didham,1997),speciesnumbersincreasewithfragmentation.

IncentralAmazonia,thenumberoffrogspeciesincreasedas aresultoftheresilience toedgeeffectsbythe majorityof forestspecies,andduetotheinfluxofspeciescomingfrom modifiedhabitatsurroundingfragmentedareas(Tocheretal., 1997).Similarly,thenumberofbutterflyspeciesalsoincreased aftertheisolationoffragmentsduetotheinvasionofspecies typicalofopenareas(BrownandHutchings,1997).Insmall fragments(plotsof1ha),thenumberoftreespeciesdidnot declinewithinforest fragments, dueto the recruitment of speciesfrom initialsuccessional stagesthatnormally have lowfrequencyincontinuousforests.Thisgroupofplantsis favoredbytheprocessofforestfragmentationand prolifer-atesinmany fragmentsduetothe mortalityoflarge trees

(Lauranceetal.,2006b;Nascimentoetal.,2006).The

magni-tudeoffloristicchangesinseedlingsisfasterandmoreintense thanthatobservedforadults(Benitez-Malvido,1998;Sizerand

Tanner,1999),whichmayaffectfuturegenerations.

Overall,the responsesofdifferentspeciesor taxonomic groupsto fragmentation variedconsiderably. Some species werefavoredbyforestfragmentation,suchasspecialistson clearingsformedbynaturaltree falls,which becomemore abundantinfragment borders.On theother hand, species sensitivetotheeffectsoffragmentationgenerallydonot tol-eratehabitatconditionssurroundingfragments(Gasconetal., 1999), astheyare vulnerable toedgeeffectsand incapable ofcrossingdeforestedareas(StoufferandBierregaard,1995;

Lauranceet al.,2004a),orhavelargehomeranges(Rylands

andKeuroghlian,1988;Harper,1989).

The main lessons learned are that small fragments (<100ha)are extremelysensitiveand tend todegradewith timedue tohigh treemortality,but if protectedfrom fires andothermajordisturbances,canbegintorecoverinjusta decadeortwo(Lauranceetal.,2011).Unfortunately,thisisnot theprevailingscenarioinBrazilianecosystems.Inthisway, wereinforcetheimportanceofthelong-termstudies, includ-ingareasisolatedformanydecades,sincefragmentationhas long-lastingeffectsonbiodiversity.

Anthropogenic

disturbances

and

global

changes

interact

synergistically

on

ecosystem

processes

Severalhypothesesontheeffectsofglobalclimatechangeon forestbiomassandspeciessubstitutionarebeingtested(Lewis

etal.,2004a).Itisstillunclearifincreasesintemperature,CO2

concentrations,nitrogendepositionorchangesinintensityof elNinoeventsarethemostimportantdriversandwhatisthe sizeoftheirimpacts.

Laurance and Williamson (2001) showed that tree

mor-talityand the decayof plantlitterfrom treesunder stress duringperiodsofextremedroughtinEl-Ni ˜noyearsincrease dramaticallyinalreadydisturbedareasoffragmentborders, ascomparedtoareasinsidefragments.Theaccumulationof combustiblematerialandthegreaterpenetrationoflightin borderscouldbethesourceofforestfiresindrieryears, espe-ciallyunderthescenariospredictedbymostclimate-change models.

ArborealbiomassincreasedovertimeinCentralAmazonia, perhapsasaresultofdirectclimatechangesorthe fertiliza-tionoftheatmospherewithCO2(Castilhoetal.,2010).Biomass change averaged +5.6Mgha−1_ano−1_{, a level in accordance} withstudiesinotherAmazonianareas.Biomasschangewas foundtobenegativelyassociatedwithprecipitation, suggest-ing thatmortalityratesincreaseinyearswithlargestorms andaffectstandingcarbonstocks(Castilhoetal.,2010). Simi-larresultsoveramuchlargerareabasedonplotsthatinclude those fromPDBFFatLTER-Site#1were obtainedbyPhillips

etal.(1998,2004),Bakeretal.(2004),Lewisetal.(2004b)and

Lauranceetal.(2004b),andthosestudiesindicatedthatareas

ofintactforestscouldbesignificantcarbonsinks.

Incontrast,physiologicalmodelsdevelopedbyChambers

et al.(2004)suggestthatupland (terrafirme)forestsarenot

efficientintheiruseofcarbon.Basedontheirmodels, car-bonemissionsviatreerespirationandfromorganicmaterial shouldbegreaterthanthephotosyntheticabsorptionbytrees. Thisfactsuggeststhattheforestgrowthprobablydoesnot respondtotheincreaseinatmosphericCO2concentration.If thisisthecase,theforestwouldnotbebehavingasacarbon sink.Thesedifferencesbetweenmodelsandresults regard-ingvegetationcomponentshowtheimportanceoflong-term investigationtotheinterpretationofresultsfromshort-term studiesandphysiologicalmodels.

Conclusions

Theresultsobtainedinthefirst10yearsofAmazonianLTER (1999–2009)showedthatdensitiesofindividualsandspecies assemblagesdistributionsarespatiallyheterogeneous,even inrelativelyundisturbedforests,andthatassociationswith topo-edaphicvariablesallowpredictionofaconsiderablepart ofthisvariation.For thebiologicalgroupswhosedynamics were studiedintheshort-term, levelsofchangeinspecies composition and density were relatively high, and in gen-eral changed in tune with the environmental variation in space.Therefore,inclusionofenvironmentalpredictorssuch astopography,soilcontentandwaterattributesallows devel-opmentofmoreprecisemodelsoffuturedynamics.

recoveryofpre-loggingassemblages.Incontrast,theimpactof forestfragmentationonorganismsandecosystemprocesses isgreatandlong-lasting.Studiesindicatethatthereisnegative synergybetweentheimpactsoffragmentationandclimatic changes,andthatabetterunderstandingoftheseprocesses canonlybeobtainedthroughlong-termresearch.

TheresultsoftheresearchinLTER-Site#1 indicatethat conservationdecisionsregardingtheAmazonforestarenot goingtobeeasy.Interventions,suchasselectivelogging,are likelytoaffectdifferentgroups,suchascommerciallyvaluable treesandinvertebrates,differently.Fragmentationhas imme-diate obvious effects onbiodiversity, but even inrelatively undisturbedareas,subtledifferencesinlandscapeelements makelargeareassuitableorunsuitableforsometaxa,which mean that it will often be necessary to undertake in situ studies to effectively plan reserve boundaries, at least for mesoscalereserves.Possiblesourcesoffundingforreserves, suchascarbontrading,arebasedonstaticmodelsofbiomass distribution, but theinteractions betweenedaphicfeatures and climatecurrentlymakepredictionsimprecise,and the insitumeasurementsarenotinaccordwiththeoretical mod-els.Systematicconservationplanningwillonlybeeffectiveif wecangeneratethedatanecessaryformodels,andthe expe-riencefromLTER-Site#1indicatesthatwearefarfromhaving adequateunderstandingofthelong-termprocesses.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

Weare gratefultofinancialandlogisticsupportgrantedby LongTermEcologicalResearchProgram(ProgramadePesquisa Ecológicade LongaDurac¸ão, PELD)through CNPq, the Pro-gramforBiodiversityResearch(PPBio)throughMinistériode Ciência,Tecnologia eInivac¸ão(MCTI), Coordinationforthe ImprovementofHigherEducationPersonnel(CAPES), Biologi-calDynamicsoftheForestsFragmentsProject(PDBFF-ST669) andSmithsonianTropicalResearchInstitute(STRI).CNPQand CAPESprovidedmanyscholarshipstothestudentsinvolved. Wealsothankalltheresearchers,students,fieldandlab assis-tantsinvolvedinthestudies,whoaretoonumeroustoname here.

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