Biodiversity conservation in human-modified Amazonian forest landscapes

14 Pages·2010·1.12 MB·English

by  Carlos A. Peres

BiologicalConservation143(2010)2314–2327
ContentslistsavailableatScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Biodiversity conservation in human-modified Amazonian forest landscapes
Carlos A. Peresa,*, Toby A. Gardnerb, Jos Barlowc, Jansen Zuanond, Fernanda Michalskie,
Alexander C. Leesa, Ima C.G. Vieiraf, Fatima M.S. Moreirag, Kenneth J. Feeleyh
aSchoolofEnvironmentalSciences,UniversityofEastAnglia,NorwichNR47TJ,UK
bDepartmentofZoology,UniversityofCambridge,CambridgeCB23EJ,UK
cLancasterEnvironmentCentre,LancasterUniversity,LancasterLA14YW,UK
dCoordenaçãodePesquisasemBiologiaAquática,InstitutoNacionaldePesquisasdaAmazônia,Manaus,Amazonas,Brazil
eDepartamentodeEcologia,UniversidadeEstadualPaulista,RioClaro,SP,Brazil
fCoordenaçãodeBotânica,MuseuParaenseEmílioGoeldi,CP399,Belém,Pará,Brazil
gDepartamentodeCiênciadoSolo,UniversidadeFederaldeLavras,Lavras,MinasGerais,Brazil
hDepartmentofBiologicalSciences,FloridaInternationalUniversity,andTheCenterforTropicalPlantConservation,FairchildTropicalBotanicGarden,FL,USA
a r t i c l e i n f o a b s t r a c t
Articlehistory: Amazonia(sensulato)isbyfarthelargesttropicalforestregion,buthassuccumbedtothehighestabso-
Received9November2009 luteratesoftropicaldeforestationandforestdegradation,drivenbyrapidfrontierexpansion,road-build-
Receivedinrevisedform22January2010 ing, and spontaneous or government-subsidized migration. The large area-through-time and paleo-
Accepted22January2010
climaticstabilityofAmazonianforestsmayhelpexplainthehighregionaltolocalscaleplantandanimal
Availableonline19February2010
species diversity of true forest specialists and high ecological sensitivity to contemporary land-use
change.Wedescribetheprevailingformsofanthropogenicdisturbancethataffectforestorganismsin
Keywords:
thecontextofthegeographicandevolutionarybackgroundthathasshapedthedegreetowhichforest
Amazonia
speciesmayberesilienttoenvironmentalchange.ThefateofAmazonianbiodiversitywillpartlydepend
Andes
upontheinteractionbetweenland-useandclimatechange,andtheextenttowhichseasonally-dryfor-
Biodiversity
Deforestation estscanretainimmunityagainstcatastrophicrecurrentwildfires.Thisreviewillustratestheimportance
Forestdisturbance ofconsideringinteractionsbetweendifferentformsofforestdisturbancetodevelopeffectiveconserva-
Human-dominatedlandscapes tionpolicy.Weconcludewithsomeconsiderationsofthepolicyagendanecessarytoprotectforestcover
Landuse andforestbiodiversityatameaningfulscaleacrosstheAmazonianbiome.
(cid:2)2010ElsevierLtd.Allrightsreserved.
1.Introduction terrestrial vascular plant species (e.g. Hubbell et al., 2008),
although the spatial turnover of species assemblages at different
LowlandandAndeanAmazoniaexhibitthegreatestexpression scalesremainspoorlyunderstood.SinglelocalitiesofSWAmazonia
oftropicalbiodiversityonEarthandthehighestabsoluteratesof can sustain the highest alpha-diversity documented to date any-
tropicaldeforestation(Hansenetal.,2008).Amazonia(sensulato) where on Earth for several taxonomic groups, including woody
stretches from sea level to >6000m across nine of the 12 South plants(Gentry,1988),butterflies(EmmelandAustin,1990),lizards
Americancountriesandencompassestheworld’slargestriverba- (Dixon and Soini, 1986) and nonvolant mammals (Peres, 1999a).
sin and most extensive unbroken tracts of tropical forests. The LowlandforestsofcentralAmazoniacanalsorivalorexceedlevels
hydrological boundaries of the Amazon basin and neighbouring ofalpha-diversityoftheupperAmazon(e.g.Cohn-Haftetal.,1997;
forestedwatersheds,includingtheTocantins,Orinocoandsmaller Oliveira and Mori, 1999). Yet Amazonian biodiversity is not
river basins across the Guianan Shields, amount to (cid:2)7.6mil- homogenousevenatsmalltointermediatespatialscalesforboth
lionkm2 (Goulding et al., 2003). This accounts for over 90% of forest (Tuomisto et al., 1995) and aquatic organisms (Fernandes
remainingSouthAmericantropicalforests,withBrazilianAmazo- etal.,2004).Forexample,adjacentseasonallyfloodedandunfloo-
niaalonecomprising(cid:2)30%oftheworld’scurrentprimarytropical dedforestsexhibithighlevelsofspeciesturnoverfortrees(terSte-
rainforests(FAO,2006). ege et al., 2003) and many faunal taxa including frogs (Gascon
TheAmazonianforestand freshwaterbiomecontainssomeof etal.,2000),smallmammals(Malcolmetal.,2005)andlargeforest
thehighestknownlevelsofbiologicaldiversityincluding>50,000 vertebrates (Haugaasen and Peres, 2005), as well as pronounced
changes in community composition (Balslev et al., 1987; Pitman
etal.,2008).Plant–animalinteractionsalsomatchlandscape-scale
* Corresponding author. School of Environmental Sciences, University of East
edaphic mosaics (Fine et al., 2004). Moreover, many habitat
Anglia,NorwichNR47TJ,UK.Tel.:[phone].
specialists are restricted to a small fraction of their hypothetical
E-mailaddress:[email protected](C.A.Peres).
0006-3207/$-seefrontmatter(cid:2)2010ElsevierLtd.Allrightsreserved.
doi:10.1016/j.biocon.2010.01.021
C.A.Peresetal./BiologicalConservation143(2010)2314–2327 2315
geographicrangeandrequirelargeforestareascontainingasuffi- expected from fringe Amazonian sites along ecotone boundaries
cient number of minor habitat enclaves to maintain a viable thatweredynamiconamillennialscale(Mayleetal.,2000).Large
(meta)populationsize. areasofaridsavannasincoreAmazoniaarefurtherquestionedby
Bioticdiversityatallscalesisincreasinglythreatenedbyavari- carbonisotoperatiosinfandepositsindicatingthatHyleanforests
etyofhuman-inducedstructuralimpacts,rangingfromsmalltree- were never replaced by tropical grasslands (Kastner and Goñi,
fall gaps generated by highly diffuse logging operations to large- 2003). Forest stability since at least the early Miocene, which
scale clear-cuts advancing into cheap or previously unclaimed wasfurtherprotectedbyregional-scalewatercyclingandtheAn-
publicforestlands.Yetanintegrativeunderstandingofhowarbo- deanrain-shadow,contributedtothegenerationofrelativelyhigh
real, terrestrial and aquatic species in tropical forest biomes re- levels of local diversity and low extinction rates of forest species
spond to different threat processes remains elusive. Forest loss compared to more arid tropical landmasses (Bush, 1994; Morley,
cannowbemappedforvastregionsatasquare-meterresolution, 2000;Stroppetal.,2009).Ingeneral,thelargerarea-through-time
yet estimates of forest biodiversity loss – at the scale of species, andpaleo-climaticstabilityofAmazonianforestsmayexplaintheir
populationsorgenes–atbestremainsaninexactscience(e.g.Fee- relatively high regional species diversity compared to Africa and
leyandSilman,2008).Thisreviewbeginswithabriefsynopsisof Asia(FineandRee,2006).Thisisnottodenyfrequentchangesin
the biogeographic history through which the Amazonian forest landscape evolution, particularly in sedimentary processes that
biota evolved. We then assess the degree to which natural and contributedto the Plio–Pleistocene to Holocene formation of flu-
pre-Columbian human disturbance has played a role in shaping vialsystemsthatcontinuetomouldtheAmazonianbiota(Rossetti
thecomparativeresilienceofthisbiotatocontemporaryformsof etal.,2005).However,theevolutionaryhistoryofthevastmajority
anthropogenicdisturbance.Next,webrieflyreviewhowforestbio- ofAmazonianspecieshasbeenpredominantlyshapedbyextensive
diversity responds to a broad spectrum of disturbances currently closed-canopymoistforestcover,althoughevidencefrommolecu-
affecting lowland and Andean Amazonia. Finally, we discuss the lar phylogenies and palynology suggest that lowland tropical
predicament of Amazonian forest biodiversity under rapidly deciduousforestsmayhavewaxedandwanedinpartsofAmazo-
changingclimateandland-usescenarios,andthepolicyagendare- niaduringglacialperiodsattheexpenseofevergreenforests(Pen-
quiredtoaddressthe dauntingchallengesofconservation inthis ningtonetal.,2000).
region. Thehistoricaldominanceofforestintheneotropics,andpartic-
ularly Amazonia, is supported by the extant vertebrate fauna,
which exhibit the highest degree of morphological specialization
2.Geographicandpaleoecologicalcontext toarboreality in forest environmentsdominatedby a continuous
canopy(EmmonsandGentry,1983),andisrelativelydepauperate
Since the breakup of Gondwanaland, much of northern South in terrestrial species when compared to paleotropical forest lin-
Americaemergedasthelargestcontinuousexpanseofclosed-can- eages (Cristoffer and Peres, 2003). For example, prehensile tails
opytropicalforestworldwide.Putsimply,Amazoniaisacolossal evolved independently at least five times in neotropical forest
mid-domain basin close to sea-level in a major continent that is mammals, including primates (Cebus and all ateline genera), ro-
bothwidestjustsouthoftheEquatorandflankedbyamassiveoro- dents (Sphiggurus and Coendou), carnivores (Potos), xenarthrans
graphicwall of westernupliftingmountains ensuringcontinuous (TamanduaandCyclopes)andallSouthAmericangeneraofmarsu-
precipitationrecycling.Although(cid:2)87%oftheentireAmazonbasin pials. Different Amazonian forest localities also hold the highest
consistsoflowlandforest<500masl,some45%oftheAndeswithin global alpha-diversity of true forest specialists for many faunal
the Amazon watershed lies at submontane elevations (500– taxa, including primates (Peres and Janson, 1999), birds (Stotz
2000masl) and the remainder between 2000 and 4000masl et al., 1996), frogs (Duellman, 2005), lizards (Pianka and Vitt,
(although several peaks in Peru extend much higher). The 2003),andmanyarthropodtaxathatwehavebarelybeguntodoc-
(cid:2)623,000km2AndeanAmazonsourcesasmuchas95%ofthesus- ument.Theseandmanyotherintercontinentaldifferencesinfau-
pendedsedimentsandnutrientsolutesexportedtotheAmazonian nal adaptation to a forest environment are likely due to the
floodplains(Meadeetal.,1985).Indeed,thegeochemistryandbio- antiquity and sheer extent of closed-canopy Amazonian forests
physical macromosaic of lowland Amazonia has been profoundly (Fjeldså,1994; Richardson etal., 2001; de Vivo and Carmignotto,
shapedbyAndeanerosionforover10millionyears(McClainand 2004).
Naiman, 2008), creating significant basin-wide gradients of pri-
mary(Malhietal.,2004) andsecondary(Peres,2008) forestpro-
ductivity, thereby setting key preconditions to any large-scale 3.Pre-Columbianforestdisturbance
planforconservingbasin-wideforestbiodiversity.
BeyondtheisolationandreconnectionofSouthAmerica,impor- South America is the last major ice-free continent to be colo-
tantgeoclimaticeventsshapingAmazoniaincludetheAndeanup- nized by humans, and the overall impact of paleoindians—which
lift,theextensivemarineincursionsoftheMiocene,theformation inAmazoniamayhavenumberedonlyfewerthan5millionprior
oftheOrinocoandAmazondrainages,andthedry–wetclimatecy- tothediffusionofEuropeanepidemicsandwidespreadpopulation
clesofthePlio–Pleistocene.However,theduration,magnitudeand collapse—onforestintegritywasatbestmodest(Meggers,1954).
consequencesoftheseeventsremainhighlycontroversial(Hoorn, Theearliestpre-historicpotteryexcavatedinAmazonia(Taperin-
2006).Largelyunequivocalgeologicalandpaleobotanicalevidence ha, lower Tapajós) dates from (cid:2)7000BP (Roosevelt et al., 1991),
hasshownthatmostoftheAmazonlowlandshasremainedunder butdensely-settledorganizedchiefdomsassociatedwithelaborate
forestthroughoutatleastthelasttwoglacialandinterglacialcy- materialcultureweresmall(20–50ha,Heckenbergeretal.,2008),
cles,ratherthanfragmentedbyopenvegetationaspostulatedby few and far apart. Unlike parts of central-west Africa, most of
thenowwidelydiscreditedPleistocenerefugiahypothesis(Haber- Amazonia is not sufficiently nutrient-rich to support persistent
leandMaslin,1999;Colinvauxetal.,2000).Sweepingconjectures game harvest by hunter–gatherers (Fa and Peres, 2001), who by
ofaridityandsavannaclimatesarelargelybasedonliberalinter- necessity typically pursue a lifestyle characterized by recurrent
pretationsofincompletebiogeographicevidencebecauseofeither nomadism and frequent resettlement. In fact, contrary to several
circularityinthesamplingeffortofmoderncodistributions(Nelson interpretationsofBalée’s(1989)‘anthropogenicforest’hypothesis,
etal.,1990)orevidencefromfossilpollenfromwindblowngrasses >85%ofAmazoniaalmostcertainlydidnotsustainpermanentset-
andherbs(e.g.vanderHammenandAbsy,1994),whichwouldbe tlementspracticingperennialagriculture.Patchesofblackanthro-
2316 C.A.Peresetal./BiologicalConservation143(2010)2314–2327
pogenic soils (known as terra preta), albeit poorly mapped, are associated with forest fragmentation processes are the most fre-
highlyskewedgeographicallyandlikelyrestrictedto<5%oftheba- quentformsofhumandisturbance,althoughthespatialextentof
sin (Bechtold, 2009). Large-scale landscaping and enrichment of these perturbations remain highly skewed (Skole and Tucker,
forest composition near sedentary settlements was therefore re- 1993;Asneretal.,2005).Naturalandhuman-inducedformsoffor-
strictedtoarelativelysmallpartofseasonally-dryAmazonia,such est-canopydisturbancediffermarkedlyintheirseverity,totalex-
as the Baures region of Bolivia (Erickson, 2000) and parts of the tent, grain size, periodicity, and permanence so that forest
upperXingúregion(Heckenbergeretal.,2008).Forexample,dense topologies that had been typically perforated by low-density
clusters of at least two tree species that are widely regarded as fine-grained disturbance events on evolutionary timescales are
‘anthropogenicforest’indicatorscanbecreatedbyedaphiccondi- now being exposed to large-scale ‘shredding’ and coarse-scale
tionscombinedwithnaturalseeddispersalagentsincludingagou- edge-effectsresultingfromfragmentation,shrinkageandattrition
tis(Brazil-nuttreeBertholletiaexcelsa:PeresandBaider,1997)and asforestssuccumbtootherland-usesundervaryingscenariosof
tapirs(aguajepalmMauritiaflexuosa:Fragosoetal.,2003).Infact, landscape configuration. Moreover, cryptic below-canopy distur-
thereisnoevidencesuggestingthatlargeareasawayfrommajor bance, such as widespread overhunting of vertebrate game and
rivers,ormoreaseasonalpartsofwesternAmazonia,weresignifi- over-harvesting of a range of other non-timber resources, alters
cantlyalteredbyhumandisturbance(BushandSilman,2007).In thelong-termdynamicsofvasttractsofforeststhatotherwisere-
anycase,whilesomepre-historicsiteswereintensivelymodified, main undisturbed (Peres and Lake, 2003; Terborgh et al., 2008).
thespatiotemporalscaleofthepre-Columbianhumanfootprintin Rarelytheseprocessesoperateinisolation,sothatinteractionsbe-
muchofAmazonia,particularlyinremoteinterfluvialregions,was tweenspatiallycorrelatedpatternsofhabitatloss,habitatdegrada-
virtually undetectable (cf. Gloor et al., 2009), thereby offering a tion and non-structural forest disturbance can accelerate or
poorhistoricalanalogueforthescaleofhumanperturbationwit- aggravate therate of populationdeclines and localextinctionsof
nessedtoday. forestinteriorspecies(LauranceandPeres,2006).
4.Contemporaryforestdisturbance 5.Biodiversityresponsestoland-usechange
Amazonian forests have been repeatedly subjected to millen- Wecompiledatotalof62plantandanimalcommunitystudies
nial-scale natural disturbances including floodplain erosion inforestlandscapesofAmazoniaandthetropicalAndesthatexam-
through lateral river-channel migration (Salo et al., 1986), flood- ined assemblage-wide ecological responses to different modes of
pulses(Hessetal.,2003),windstorm-inducedblowdownscausing structuralforestconversionordegradation(seeTable1andrefer-
large-scale tree mortality (Nelson et al., 1994) and episodic fires encelistinSupplementaryMaterials).Thespatialextentofpastre-
(Sanford et al., 1985). However, the spatiotemporal scale of this search efforts is restricted to a negligible portion of this region
background disturbance regime bears little resemblance to pres- (Fig.2),withparticularconcentrationofeffortinasmallnumber
ent-day patterns of anthropogenic forest conversion/degradation, ofwell-studiedlocalities,includingtheBiologicalDynamicsofFor-
whichhave rapidly accelerated since the road-buildingand fron- est Fragmentation Project (PDBFF), north of Manaus, Brazil, the
tier-colonizationprojectsofthe1970s.ConsideringallnineAma- Bragantina region (eastern Pará), and more recently, a pulpwood
zonian countries, 63.8(cid:3)106ha of forest were lost to different forestrylandscapeinnortheasternPará(JariProject).Thereisalso
land-usesbetween1990and2007,but76.1%ofthisdeforestation a clear mismatch between the geographic distribution of forest
occurred in Brazil alone, 95% of which in the Brazilian Amazon conversion/degradation across Amazoniancountries and the spa-
(Fig. 1). During the same period, however, the fastest relative tial allocation of ecological research effort. Furthermore, most
deforestation rate was observed in Ecuador, which lost nearly studieshaveexaminedonlyasingletaxonomicgroup,andcross-
25%ofitsmontaneandlowlandforest. taxa landscape-scale studies sampling five or more taxa within
Clear-cutting from slash-and-burn agriculture, selective log- the same sites are currently restricted to only five sites. Studies
ging,large-scaleforestconversionintocattleranches,foodcrops, ontheimpactofforestreplacementwithcattlepastureandcrop-
and exotic-tree monocultures, and the isolation and edge effects landsondifferenttaxaarelargelylackingfromvastareasofdefor-
Fig.1. AbsoluteandrelativeextentofforestlossacrossallnineAmazoniancountries:(a)Horizontalbarsrepresentthetotalforestcoverin1990;blackbarsindicatethe
amountofforestcoverremainingby2007.(b)Proportionalforestlossoverthesameperiodcalculatedfordifferentyearsintermsofthe1990baseline.Countriesareordered
byeither(a)theirtotalextentof1990forestcover,or(b)fromthelowesttothehighestproportionalforestloss.DatafromtheUN’sFoodandAgricultureOrganization(http://
faostat.fao.org/default.aspx).
Table1
Listofbiodiversitystudiesinhuman-modifiedforestlandscapesofthelowlandandAndeanAmazon.Geographiccoordinateswereunavailableforsomestudies,butobtainedfromGoogleEarthonthebasisofapublishedorunpublished
map.ReferencesarelistedintheSupplementaryMaterials.
Source Natureofstudy Taxonomicgroup Land-usesotherthanprimaryforest Biodiversitymetric Geographiclocation
Taxonomic Land-use Primary
coverage coverage forest
Ackermanetal. Single Multiple Yes Termites Palm-basedagroforestry,home-gardenagroforestry Overallspeciesrichness,species 02(cid:3)3100400S,60(cid:3)0104800W
(2009) diversity,communitycomposition
Adams(1997) Single Multiple Yes Bats Forestfragments,secondaryforest Overallspeciesrichness,species 01(cid:3)110S,47(cid:3)190W
diversity
Andradeand Single Single Yes Birds Secondaryforests Overallspeciesrichness,community 01(cid:3)080S,70(cid:3)120W
Rubio-Torgler composition
(1994)
Armbrechtetal. Single Multiple No Ants Forest,Polygenericshadedcoffee,Monogenericshadedcoffee, Overallspeciesrichness,species 05(cid:3)080–05(cid:3)450N,75(cid:3)450–
(2005) Suncoffee diversity 75(cid:3)560W
Barlowetal. Single Multiple Yes Butterflies Secondaryforest,Eucalyptusplantation Overallspeciesrichness,restricted 00(cid:3)2700000–01(cid:3)3000000S,
(2007a,2008) speciesrichness,community 51(cid:3)4000000–53(cid:3)2000000W
composition
Barlowetal. Single Multiple Yes Birds Secondaryforest,Eucalyptusplantation Overallspeciesrichness,community 00(cid:3)2700000–01(cid:3)3000000S, C
.A
(2007b) composition 51(cid:3)4000000–53(cid:3)2000000W .
P
Barlowetal. Single Single Yes Birds Burntforests Overallspeciesrichness,community 02(cid:3)440S,55(cid:3)410W ere
(2002) composition s
e
Bernardand Single Multiple Yes Bats Forestfragments,Savannahs Overallspeciesrichness,community 02(cid:3)300S,54(cid:3)570W ta
Fenton(2002) composition l./
Borges(2007) Single Single Yes Birds Diversesecondaryforests Overallspeciesrichness,species 01(cid:3)540S,61(cid:3)270W Bio
diversity,communitycomposition log
Borgesand Single Single No Birds Secondaryforest Overallspeciesrichness,species 02(cid:3)200S,60(cid:3)000W ica
l
Stouffer(1999) diversity,communitycomposition C
o
Carvalhoand Single Single Yes Ants Edgehabitat Overallspeciesrichness,species 02(cid:3)200S,60(cid:3)000W n
Vasconcelos diversity,communitycomposition serv
Cas(c1a9n9t9e-)Marín Single Multiple Yes Epiphytes Diversesecondaryforests Overallspeciesrichness,species 10(cid:3)1701000N,84(cid:3)4704000W ation
etal.(2006) diversity,communitycomposition 14
Castro-Arellano Single Single Yes Bats Loggedforests Overallspeciesrichness,species 03(cid:3)2103600S,54(cid:3)5700000W 3(2
etal.(2007) diversity,communitycomposition 0
1
Cochraneand Single Single Yes Woodyplants Burnedforest Overallspeciesrichness,species 12.03(cid:3)S,44.03(cid:3)W 0)
Schulze(1999) diversity 23
DaSilvaetal. Single Multiple No Birds Secondaryforests,Pastures Overallspeciesrichness 02(cid:3)590S,47(cid:3)310W 14
–
(1996) 23
DeAlmeidaetal. Single Multiple No Birds Secondaryforest,Eucalyptusplantation,Forestfragments Overallspeciesrichness 04(cid:3)5900500–05(cid:3)1100500S, 27
(2004) 47(cid:3)3902900–48(cid:3)1603800W
Diasetal.(2009) Single Single Yes Fish Streamsinloggedforests Overallspeciesrichness,community 02(cid:3)570N,58(cid:3)420W
composition
Fiedleretal. Single Single Yes Moths Edgehabitat Overallspeciesrichness,species 00(cid:3)080S,113(cid:3)400W,
(2007) diversity,communitycomposition 04(cid:3)050S,79(cid:3)100W
Freitas(2008) Single Single Yes Mammals Loggedforests Restrictedspeciesrichness 02(cid:3)430–03(cid:3)040S,58(cid:3)310–
58(cid:3)570W
Gardneretal. Single Multiple Yes Dungbeetles Secondaryforests,Eucalyptusplantations Overallspeciesrichness,species 00(cid:3)270–01(cid:3)300S,51(cid:3)400–
(2008) diversity,communitycomposition 53(cid:3)200W
Gardneretal. Multiple Multiple Yes Amphibians,lizards Secondaryforests,Eucalyptusplantations Overallspeciesrichness,community 00(cid:3)270–01(cid:3)300S,51(cid:3)400–
(2007) composition 53(cid:3)200W
Haugaasenetal. Multiple Single Yes Birds,arthropods Burntforests Overallspeciesrichness,community 02(cid:3)440S,55(cid:3)410W
(2003) composition
Hawesetal. Single Multiple Yes Moths Secondaryforest,Eucalyptusplantation Overallspeciesrichness,species 00(cid:3)530S,52(cid:3)360W
(2009) diversity,communitycomposition
Hungetal.(2008) Single Multiple Yes Arachnids Secondaryforest,Eucalyptusplantation Overallspeciesrichness,species 00(cid:3)2700000–01(cid:3)3000000S,
diversity,communitycomposition 51(cid:3)4000000–53(cid:3)2000000W
(continuedonnextpage) 23
1
7
Table1(continued) 23
1
8
Source Natureofstudy Taxonomicgroup Land-usesotherthanprimaryforest Biodiversitymetric Geographiclocation
Taxonomic Land-use Primary
coverage coverage forest
Kattanetal. Single Single Yes Birds Forestfragments Overallspeciesrichness,community 10(cid:3)1904300N,
(1994) composition 74(cid:3)5202200W
Klingbeil Single Single Yes Bats Forestfragments Overallspeciesrichness,species 03(cid:3)750S,73(cid:3)240W
andWillig diversity,communitycomposition
(2009)
Kösteretal. Single Multiple Yes Epiphytes Forestfragments,Secondaryforests,Isolatedremnanttreesin Overallspeciesrichness,species 00(cid:3)250S,79(cid:3)010W
(2009) pasture diversity
Lauranceetal. Single Single Yes Trees Forestfragments Restrictedspeciesrichness 02(cid:3)300S,60(cid:3)W
(2006)
Leck1979 Single Single No Birds Forestfragment Overallspeciesrichness 0(cid:3)350S,79(cid:3)220W
LeesandPeres Single Single Yes Birds Forestfragments Overallspeciesrichness,community 09(cid:3)530S,56(cid:3)280W
(2006) composition
LeesandPeres Single Single Yes BirdsandMammals Riparianforestcorridors Overallspeciesrichness,community 09(cid:3)530S,56(cid:3)280W
(2008) composition
Limaetal.(2009) Multiple Multiple Yes Nitrogen-fixingbacteria Secondaryforest,agroforestry,subsistencecrops,pastures Overallspeciesrichness,community 4.41(cid:3)S,69.94(cid:3)W C.A
composition .P
Martínezetal. Single Multiple No Earthworms Matureforest,Pasture Overallspeciesrichness,species 02(cid:3)420–02(cid:3)520N,76(cid:3)300– ere
(2006) diversity 76(cid:3)330W se
Mathieuetal. Multiple Multiple Yes Soilmacrofauna Ricecrops,Fallows,Pastures Overallspeciesrichness,species 05(cid:3)160S,49(cid:3)500W ta
(2005) diversity,communitycomposition l./
B
Michalskietal. Single Single Yes Trees Forestfragments Overallspeciesrichness,community 09(cid:3)530S,56(cid:3)280W io
(2007) composition log
Michalskiand Single Single Yes Mammals Forestfragments Overallspeciesrichness 09(cid:3)530S,56(cid:3)280W ica
l
Peres(2007) C
o
Mitjaetal.(2008) Multiple Multiple No Herbaceous,woodyplants Ricefields,pastures Overallspeciesrichness,community 05(cid:3)1600800S,49(cid:3)5002900W nse
composition rv
a
Moreiraetal. Multiple Multiple Yes Soilmesoandmacrofauna, Secondaryforest,agroforestry,subsistencecrops,pastures Overallspeciesrichness,community 4.41(cid:3)S,69.94(cid:3)W tio
(unpublished microbialcommunities composition n
1
data) 4
3
MurielandKattan Single Multiple No Butterflies Shadecoffeeplantation,suncoffeeplantation Overallspeciesrichness,species 05(cid:3)450–05(cid:3)550N,75(cid:3)360– (2
(2009) diversity,communitycomposition 76(cid:3)020W 01
Nepstadetal. Multiple Multiple Yes Plants,ants,birds,bats Secondaryforest,abandonedpasture,activepasture Overallspeciesrichnessandcomposition 02(cid:3)590S,47(cid:3)310W 0)
2
(1996) 3
1
Nöskeetal. Multiple Multiple Yes Epiphytes,moths Disturbedforest,Isolatedtreesinpasture Overallspeciesrichness,species 03(cid:3)590S,79(cid:3)040W 4–
(2008) diversity,communitycomposition 23
Numaetal. Single Multiple No Bats Forestfragments,Shadedcoffeeplantation,Associatedcoffee Overallspeciesrichness 04(cid:3)100–04(cid:3)400N,75(cid:3)350– 27
(2005) plantation 75(cid:3)500W
O’Deaand Single Multiple Yes Birds Secondaryforest,Agriculturalland Overallspeciesrichness,species 00(cid:3)040S–00(cid:3)070N,
Whittaker diversity,communitycomposition 78(cid:3)360–78(cid:3)460W
(2007)
Parryetal.(2007) Multiple Single Yes Largemammals,large Secondaryforests Overallspeciesrichness,community 00(cid:3)530S,52(cid:3)360W
birds composition
Peresetal.(2003) Multiple Single Yes Birds,mammals Burntforests Overallspeciesrichness,community 02(cid:3)5905800S,56(cid:3)0503600W
composition
Presleyetal. Single Single Yes Bats Loggedforests Overallspeciesrichness,community 03(cid:3)360S,54(cid:3)950W
(2008) composition
Rondonetal. Single Single Yes Trees Secondaryforest Overallspeciesrichness,community 04(cid:3)540S,73(cid:3)390W
(2009) composition
Rossietal.(2006) Multiple Single No Soilmacrofauna Pastures Overallspeciesrichness,species 05(cid:3)160S,49(cid:3)500W
diversity
Sampaioetal. Single Single Yes Bats Forestfragments Overallspeciesrichness,community 02(cid:3)240–02(cid:3)250S,59(cid:3)430–
(2003) composition 59(cid:3)450W
Sampaioetal.(in Single Multiple Yes Largemammals Loggedforest;Forestfragmentsisolatedbyscrubsavannah Overallspeciesrichness,community 2(cid:3)340S,54(cid:3)540W;2(cid:3)80S,
revision) composition 54(cid:3)540W
C.A.Peresetal./BiologicalConservation143(2010)2314–2327 2319
estationwithintheBrazilianstatesofMatoGrosso,Rondônia,and
– Pará,despiteunprecedentedagriculturalexpansionduringthelast
09
71(cid:3) two decades. In sum, all but a few human-modified Amazonian
W W4 W W W W W W W landscapesare yet tobeinvestigated,and regardless ofsampling
05016(cid:3) 04731(cid:3)0339S,(cid:3) 06011(cid:3) 05457(cid:3) 04719(cid:3) 62.89(cid:3) 0.13W(cid:3) 07821(cid:3) 07324(cid:3) 05456(cid:3) ianfteewnsiltoycaelxitiisetsin.gresearchefforthasbeenheavilyskewedtowards
00750S,(cid:3) 0S,0259(cid:3)00111–0(cid:3)04833W(cid:3)00238S,(cid:3) 0S,0230(cid:3) 0S,0111(cid:3) 10.34S,(cid:3) 3.36S,6(cid:3) 0S,0000(cid:3) 0S,0374(cid:3) 0S,0321(cid:3) niaNreexstu,lwtinegreivniedwiftfehreenptrecvoanilsinegqupeantcteersnstooflalannddsc-uapseeinstrAumctauzroe-,
andthewaysinwhichexistingresearchrevealshowarboreal,ter-
on restrial and aquatic species in forest environments respond to
Overallspeciesrichness,communitycompositionOverallspeciesrichnessandcompositiOverallspeciesrichness Overallspeciesrichness,communitycompositionOverallspeciesrichness,speciesdiversity,communitycompositionOverallspeciesrichness,speciesdiversity,communitycompositionOverallspeciesrichness,speciesdiversity,communitycompositionAbundance,functionalcommunitycompositionOverallspeciesrichness,speciesdiversity,communitycomposition Overallspeciesrichness Overallspeciesrichness,speciesdiversity,communitycomposition t5oflSflmauhe.lo1rdoselwg.eeT-tmecgeSiim-ntaelr.ytiolcgvrebtweecifefevtrtrlrioihovottimgeyhmstlg—irybniosnitynlpnphogiivagfenciacognagreelnl—v>dtifinah3tonfhgee0orgaaerMmtBiescntsraihosstasnstsazaontiontlpomihfdayteAonaarmprcbikAeocaaeromucztfusoakoalnbrgnyzatlrioestaodinnuoifeifonnaxfifrondtcrar>uaensn9lcsttd0attaist%ttvufoeiresrosadafaccli(totsIsuhBmttpirreGnaeemtgEreietuf,oahavdil2lsrleliy0ohtny0ugdur6gaieeifn)hps--.
dynamics. The extent of logging disturbance in Amazonia has
mi- thereforebeenvastlyunderestimated,butoftenexceedsthetotal
Sed deforestedarea(Asneretal.,2005).Timberofftakestypicallydrive
Selectivelyloggedforest,Clear-cutforest,Pasture Secondaryforest,abandonedpasture,activepastureForestfragments Loggedforests Forestfragments Forestfragments,secondaryforest Secondaryforest Secondaryforest Closedmixedforest,Closedacaciaforest,Forestedge,closedsecondary,Woodland,Isolatedtreesingrasslan Agriculture,Secondaryforests Loggedforests vsfeohaaffidtncaroheatntnepaaeraervetenmbdtdeceaadYwestritsllp,ptreciaau.ytoob,aeatgrtrlrsfntryoeoo2pieiri,knsnacnwla0i.tttisttgelghgf0Fryra,-tesemouor6pilhfsmruoniefroc)izaeencu.ttroiotlefenuanmmocgieTfxrnoltorhgglehlaalaanssfyngiemrtcilnrniittiooounhrnoaeygddpneffrtagxgnialeastaenertlleiumnloaarnededg,oolnnsgecdrgeUtafiantgddielsvgnhdoeorit-ebenimoagelxgustnihgnrapgesfooit(potdeeditanodArhnirrrsnesaiirmgegftvsshitlo(hcame.ehciseusrroipesort(e.nymagr1nsonAt(plui.9fooRftsamtetcboVy9hislinotltdecrysa1aaeud-ereiansz)dimrraosrlmicoAdeii.nftnef,ogsonp-mdpiattufn2utuaaiuonaaisec0anscnatrrcpdnesezt0odebldtsello8ssceaoybbcnttbo)wtnossiiyh,meeocfuicaaientasrdediclysttpennot.sihei,epeavonn(cid:2)dcassl2ritersaelepcui3i0.ceisrsoc,nartc0lsa0utoireel2ghaioisl9btfaatv0ygsiny)arsndreep0r.teeisxgilohen0(eqceltcsBfce)gosuaueaua.ifasgdlnaceonwrCltrgclsefncsurlooiaeieoiaerstrpnvnctreslwstseoyygeeess--tt,
damaged for every tree extracted in a logging frontier of eastern
es Pará.Aquaticsystemsembeddedwithinloggedforestsmayretain
at a relatively rich macroinvertebrate fauna, but their fish assem-
m
pri blagesstillbecomemoredepauperateandlessfunctionallydiverse
es nts es es, (Nessimian et al., 2008). Reduced-impact logging (RIL) tech-
Dungbeetl BirdsMammals Ants Ants Woodypla Dungbeetl Dungbeetl Epiphytes Bats Birds nedxaiqtmruaaecgst—eivwaenhdiincmdhuasaytrreryeswiunildteAinlmyoanezxloytnomilale—indgorraesdatislayceprrnreodibmulceiseiimntghpiasscutcssotoallinantabebirolae-l
diversity (e.g. Azevedo-Ramos et al., 2006; Wunderle et al.,
2006). Nevertheless, some taxa appear to be sensitive to even
Yes YesNo Yes Yes Yes Yes Yes No Yes Yes low-intensity logging. For example, changes in canopy cover and
understorey foliage density are detrimental for bats through
e e e e knock-oneffectsonforagingandecholocation.Studiesonbatsat
Multipl MultiplSingle Single Single Single Single Single Multipl Multipl Single trwesoersveepsa)rahtaevReILshsiotwesninththaetBwrahzilieliacnoAmmmaoznonsp(TeacpieasjóaspapnedarKatyoapbóe
unaffected or even benefit from logging, certain guilds and rarer
e species are either absent or found in reduced abundances in RIL
Single SingleSingle Single Single Single Single Multipl Single Single Single sbieteaslt(ePreetderisneftorael.s,t2s0s0u6b;jePcrteesdletyoeRtILalw.,i2t0h0c8h)a.nFigsehsfianubnoatshchanabailtsaot
conditions and assemblage composition lagging for several years
Scheffler(2005) Silvaetal.(1996)Stoneetal.(2009) Vasconcelosetal.(2000)Vasconcelosetal.(2006)Vieira(1996) Vulinec(2002) Vulinecetal.(2006)WernerandGradstein(2009)Willigetal.(2007)Wunderleetal.(2006) aptinofattrdeeDerrrdea-lrswotepogliragtoeteinetlihdtgahebhrreleeatrahsecsrolboeanenatceistvlns.ueFfsldaiyiriocssminctn,osgiwnnfrAtoioitrmnmhuiametzehdopxenia(scDietatixinsnacgsoebpfseiotttsuideoadilnlvei.e,ecosr2tisf0fvioot0eyrn9,lae)oi.ttgslgihesiaondsrgtitf-tficthoecrmruemle-t
study (Azevedo-Ramos et al., 2006), all Amazonian biodiversity
2320 C.A.Peresetal./BiologicalConservation143(2010)2314–2327
Fig.2. Distributionofsingletaxonormulti-taxastudiesonbiodiversityresponsestoland-usechangeinlowlandAmazoniaandthetropicalAndes(seeTable1andreferences
inSupplementaryMaterials).Grayareasindicatetheextentofdeforestationsincetheearly1970sto2007inBrazilandPeru.Whitecirclesaresizedproportionallytothetotal
numberofplant,invertebrateandvertebratetaxonomicgroupsinvestigatedateachsite;e.g.atotalof22taxahavebeenexaminedinthemoststudiedsite(Biological
DynamicsofForestFragmentationProject,Manaus,Brazil).Thickdark-graycontourindicatesthephytogeographicboundariesofAmazonia(sensulato).Narrowblackcontour
withinBrazilindicatesthepoliticalboundariesof‘LegalAmazonia’.(Forinterpretationofthereferencestocolourinthisfigurelegend,thereaderisreferredtotheweb
versionofthisarticle.)
Fig.3. Changesintotalforestandnon-forestcoverrecordedwithinprivaterurallandholdingsacrossdifferentstatesofBrazilianAmazoniafrom1996to2006;(MT)Mato
Grosso,(PA)Pará,(TO)Tocantins,(RO)Rondônia,(AM)Amazonas,(AC)Acre,(RR)Roraima,and(AP)Amapá.Croplandsincludealltypesofsubsistenceandcashcrops;cattle
pasturesincludeallmanagedandunmanagedpastorallands,stockedprimarilybyvaryingdensitiesofbovinecattle.Horizontalbarsininsetgraphindicatethetotalarea(in
106km2)ofeachstate.DataadaptedfromtheBrazilianAgriculturalCensus(IBGE,2006),whichunderestimatesforestconversiontoagricultureintheprivatesectorbecause
manylegalordefactopropertiesarenotcapturedbyofficialcensusstatistics.
studies on logging have not had access to pre-impact data, such importanceofdifferentmanagementoptions,includingdifferences
thatobservationsmaybeconfoundedbynaturalspatialheteroge- inloggingintensity,lengthofrotationcycle,roadplanningandthe
neityinspeciesdistributions.Second,thepotentialimpactsoflog- spatialdistributionofno-takesites.Thefactthatmanyspeciesre-
ging may occur across temporal scales much longer than the sponsestologgingaredissipatedacrosslargeareasandoverlong
duration of field studies. Finally, logging impacts usually interact time-lags means that the development of minimum certification
withotherhuman-induceddisturbancessuchasfireandover-har- standardsforecologicallyresponsibleforestmanagementrequires
vesting of non-timber resources (e.g. Nepstad et al., 2008). The ahighlycoordinatedprogramofresearchandmonitoringacrossa
challenge for future research will be to tease apart the relative widenetworkofstudysites.
C.A.Peresetal./BiologicalConservation143(2010)2314–2327 2321
5.2.Wildfiredisturbance ofthedominantproductionsystems.Mostworktodatehasbeen
oncattlepastures,withfewbiodiversitystudiesincroplandsout-
Since Uhl and Buschbacher’s (1985) seminal paper, it has be- side small-scale slash-and-burn farming (see Table 1). Although
come well established that human-induced forest degradation cattlepasturesencompasshighlevelsofheterogeneityassociated
through logging and fragmentation can operate synergistically withagesincedeforestation,andthetypeandintensityofmanage-
withabnormalclimaticeventstoincreasethefrequencyandsever- ment (Dias-Filho and Ferreira, 2008), the replacement of closed-
ity of fires in Amazonianforests. Extreme supra-annual droughts canopy forest with open farmland has predictably severe conse-
triggered by ENSO events and elevated Atlantic sea-surface tem- quences for forest biodiversity. Compared to primary forest, pas-
peratures play a critical role in triggering extensive forest fires tures are invariably dominated by a highly impoverished subset
when combined with anthropogenic ignition sources from slash- ofgeneralistoredge-tolerantforestspecies,open-areaspecialists
and-burnagricultureandcattleranching(Aragãoetal.,2008).In- orexotics.Forexample,ofthe53dungbeetlespeciesinanintact
deed, fires can result in wholesale phase-shifts in the structure southeasternAmazonianforestsite(Scheffler,2005),only13were
and composition of Amazonian forests (Barlow and Peres, 2008), foundinpastures,ofwhich87%ofcapturesconsistedofonespe-
comprisingakeymechanismforapossibleclimate-mediatedfor- cies.InthecentralAmazon,nativeearthwormswereeitherabsent
estdieback(Malhietal.,2009). orrareinpastures,insteadbeingreplacedbylargenumbersofan
Evenlow-intensityfiresoftenhavealargeimpactonbiodiver- exoticperegrinespecies(Decaensetal.,2004).Onlythreeoutof47
sity, inducing high levels of tree mortality (up to 50% of trees frugivorous bird species forayed into active pasture from neigh-
P10cmDBH)andsignificantlossestofaunalcommunities,includ- bouringsecondaryforests,whereas18speciesusedalimited80-
ing disturbance-sensitive birds and primates (e.g. Peres et al., m strip of scrubby pasture along the forest edge (Silva et al.,
2003; Barlow and Peres, 2004a, b). Fires also lead to ecosystem 1996).Wholesalechangesinaquatichabitatsalsooccurindefor-
instability and destabilising feedback cycles, as once-burned for- ested areas, with streams becoming shallower, wider, hotter and
ests become more likely to burn again (Cochrane et al., 1999). sustaininglowerprimaryproductivityandlessspecies-richmacr-
Theserecurrentfireshavemuchgreatereffectsonforestbiodiver- oinvertebrateandfishassemblages,inwhichlargelyinsectivorous
sity than initial fires, including a 100% turnover of bird species ichthyofaunasshifttoassemblagesdominatedbydetritivoresand
compositionbetweentwice-burned andunburnedprimaryforest periphyticalgae–grazers(BojsenandBarriga,2002).Invasiveallo-
(Barlow and Peres, 2004b). Each subsequent fire appears to lead chthonousfish species from floodplainareas downrivermay also
to both a dramatic shift in tree species composition (Barlow and becomeabundant(Nessimianetal.,2008).
Peres, 2008) and an associated collapse in forest biomass (Peres, Functional groups of soil organisms – including prokaryotes,
1999b;Cochraneetal.,1999;BarlowandPeres,2004a). nitrogen-fixingnodulatingbacteria,arbuscularmycorrhizalfungi,
Because fire occurrenceis stronglylinked to human activities, pathogenic and antagonist fungi, earthworms, ants, beetles and
fires are likely to have a particularly importantrole in degrading termites–werecomparedacrossdifferentland-usesinaheteroge-
thebiodiversityvalueoffragmentedlandscapes.Surface-firedistur- neous landscape near Benjamin Constant, western Brazilian
bance is a significant predictor of species richness in forest frag- Amazonia, including primary forest, young secondary forests
ments for forest-dependent birds (Lees and Peres, 2006) and (<12yrs-old) recovering from slash-and-burn plots, agroforestry
mammals (Michalski and Peres, 2007). In addition, burned frag- homegardens,foodcrops,andpasture(Fidalgoetal.,2005).Under
mentsareunlikelytoberecolonizedbydisturbance-sensitivespe- current conditions, slash-and-burn successional mosaics sur-
cies if entire, isolated fragments burn. However, the spatio- roundedbylargeareasofprimaryforestretainedthehighestlevels
temporal variation in the causes and consequences of fires, and of soil fertility and species diversity for macro and mesofauna.
howfiresinteractwithotherformsofforestdegradationandacross However,soilmicrobialcommunitiesincattlepasturesandcrop-
differentspatialscalesremainpoorlyunderstood(BarlowandSilve- land were among the most diverse (Leal et al., 2009; Lima et al.,
ira,2009).ThisinformationisvitaltobetterpredictAmazon-wide 2009), showing that these land-uses did not deplete microbial
implicationsoffires,identifyvulnerability,anddefineandhighlight diversity.
potentialtippingpointsbeyondwhichthefloraandfaunatypicalof Despite thelow intrinsicvalue ofthe agro-pastoralmatrix for
closed-canopyAmazonianforestmaybeunabletorecover. forest biodiversity, farm management decisions and land-use
choices can have severe repercussions for conservation through
5.3.Agro-pastoralmatrix their indirect influence on species persistence in adjacent forest
remnants. Perhaps the most serious negative indirect effects of
Agriculturalexpansionforlocal,nationalandinternationalmar- agriculture on forest biodiversity is the spread of forest wildfires
kets is a major driver of Amazonian deforestation and land-use originating from land-clearing or careless pasture management
change. Extensive ranching of some (cid:2)71million head of cattle (Morton et al., 2008). Less well understood impacts come from
occupying74Mhaofpasturesisthedominantagro-pastoralactiv- theleakageintofreshwatersystemsoftheheavycocktailofcrop-
ity in Brazilian Amazonia, accounting for (cid:2)80% of the deforested landpesticidesandherbicides(Fearnside,2001),particularlyinthe
area(Greenpeace,2009).However,recentdecadeshavewitnessed floodplaincultivationofannualcrops.Atthemorelocalscale,agri-
arapidnorthwardexpansionofmechanisedmonocultures,replac- cultureandcattleranchingcandetrimentallyaffecttheintegrityof
ingbothabandonedpastures(SimonandGaragorry,2005)andpri- forestfragmentsviaspill-overandedgeeffects.Forexample,cattle
mary and secondary forests (Morton et al., 2006). Major overgrazing in remnantriparianforest stripscan significantlyre-
Amazonian agricultural commodities now include soybean, cas- ducethespeciesrichnessofforestbirds(LeesandPeres,2008).
sava, maize, bananas, beans, rice and coffee (Fearnside, 2001). In ApriorityareaofconservationresearchinAmazonianagricul-
2006, agricultural areas in private landholdings in Brazilian turallandscapesistheimportanceofland-usehistoryandintensi-
Amazonia had increased by (cid:2)23Mha within one decade to fication on the prospects for regeneration and biodiversity
(cid:2)69.7Mha (79.5% as cattle pastures and 20.5% as croplands; recoveryonabandonedfarmland,andthepotentialforirreversible
Fig. 3). Yet (cid:2)54.5Mha was deforested in almost the same period ecologicalchangefollowingintensiveuse.AndradeandRubiotor-
(1998–2007), suggesting that over half of all deforestation oc- gler(1994)suggestedthatshifting-agriculturecanprovideasus-
curredinpreviouslyunclaimedpubliclands. tainable form of land-use in the Colombian Amazon given that
Setagainstthescaleofagro-pastoralexpansionintheAmazon bird communities sampled in fields abandoned for only 10years
therehasbeenrelativelylittleresearchonthebiodiversityimpacts were indistinguishable from those in neighbouring forest areas.
2322 C.A.Peresetal./BiologicalConservation143(2010)2314–2327
However, this form of small-scale agriculture contrasts starkly secondarysuccessionpathways,undermultiplecyclesofland-use
withslowrecoverytrajectoriessuchasthoseineasternBrazilian abandonment and forest regrowth (e.g. Moran et al., 1996; Perz
Amazoniawheredegradedscrublandshaveoftenbeensubjectto and Skole, 2003). Biodiversity recovery in Amazonian secondary
decades of non-forest land-use, such as intensive cattle grazing, forestsisofpotentiallyhighconservationvalue,notleastbecause
andmaybekilometresapartfromthenearestpatchesofremaining of the vast fallow areas that are currently regenerating (Asner
forest (Uhl et al., 1988). The development of improved conserva- et al., 2009). On the basis of 26 Landsat scenes scattered across
tionstrategiesinAmazonianagriculturallandscapesdependscrit- themostdeforestedregionofBrazilianAmazonia,Almeida(2008)
ically on understanding the extent to which the biodiversity estimatedthat19.4%ofallforestlandareathathadbeenconverted
benefitsoflocalreforestationandbiodiversityoffsetschemesand by2006(680,000km2)wassecond-growthundervaryingstagesof
proposed low-impact farming techniques (e.g. silvopastoralism, regeneration. However, a 10-yr time-series of these images re-
Castro et al., 2008) are effective in the context of such regional vealedthatthissecond-growthwasalmostinvariablyshort-lived,
andhistoricalconstraints. withameanhalf-lifeshorterthan5yrs,whichissomewhathigher
thanpreviousestimatesfor1978–2002(Neeffetal.,2006).
5.4.Edge-dominatedandfragmentedforests Yetbiodiversityrecoveryintropicalsecondaryforestscritically
accruesslowdividends(Chazdonetal.,2009).InlowlandAmazo-
Forestfragmentationisanumbrellatermforthesimultaneous nia, even relatively old secondary forests exhibit limited species
shrinkage of forest area, sub-division of large forest blocks, and accumulation. For example, relatively long-lived (20–40yr-old)
proliferationofforestedges(LindenmayerandFischer,2007).Edge secondaryforestsofeasternAmazoniacontainedonly40.3–41.8%
habitatsareexpandingonamassivescale.Forexample,6.4%ofall ofthe268treespeciesP5cmDBHofanadjacentprimaryforest,
remaining forest within a 1.12millionkm2 study area (covering and those were largely regenerating vegetatively through respr-
>80% of the deforestation and selective logging in the Brazilian outs(Vieira,1996).Moreover,84%oftheseprimaryforesttreespe-
Amazon) falls within 100m of a forest edge (Broadbent et al., ciesreliedonanimalseed-dispersalvectors,suggestingthattheir
2008).Thedetrimentaleffectsofforestfragmentationincludeele- absencecanthwarttheinfluxofold-growthtreespeciesintosec-
vatedtreemortality(Laurance,2000),changesinspeciescomposi- ondaryforests(VieiraandProctor,2007). IntheJarilandscapeof
tionandmutualisticor trophicinteractions (PeresandMichalski, northeastern Pará, where 15 vertebrate, invertebrate and plant
2006;Crameretal.,2007),andsynergismswithotherdriversoflo- taxa were sampled across five primary and five secondary forest
calextinctionssuchaswildfiresusceptibility(Alencaretal.,2004), (14–19yr-old)sites,59%ofover1000speciesrecordedinprimary
elevatedhuntingpressure(Peres,2001)andconversiontoagricul- forest also occurred in secondary forests (Barlow et al., 2007).
ture(Mortonetal.,2006).Landtenuredynamicsalsosignificantly However,manyofthesespecieswererecordedonlyonce,andthis
affects forest retention. Although poorer smallholders tend to figurefellto46%whensingletonswereexcludedfromsecondary
clear-cutalargerproportionoftheirlandholdings,largeproperties forestsamples.Foranumberofreasons,thedatafromJarirepre-
(>100ha)stillaccountfor58%ofoveralldeforestationinnorthern sentabest-casescenarioofbiodiversityrecoveryasmostAmazo-
MatoGrosso,Brazil(Oliveira-FilhoandMetzger,2006). nian secondary forests are much younger, farther removed from
Speciesrichnessinisolatedforestfragmentsisprimarilyafunc- remnant patches of primary forest, more heavily disturbed, and
tionoffragmentsize,largelybecausemanymammals(Michalski carrythelegacyofalessbenignland-useandmanagementhistory
and Peres, 2007), birds (Stoufferand Bierregaard, 1995; Lees and that is often exacerbated by additional biophysical constraints
Peres, 2006), and several arthropod taxa (Powell and Powell, such as fire-mediated nutrient depletion and local extinction of
1987;BrownandHutchings,1997;Didham,1997)arehighlysen- animalseed-dispersalvectors.
sitivetothecorrelatedeffectsofedgesandforestpatcharea.Forest
remnantscontainalimitedsubsetofanyregionalforestandaqua-
tic biota. For example, aquatic macroinvertebrates in streams 6.Loomingspectreofclimatechange
within (cid:2)10-ha forest fragments are just as species-poor as those
coursing through completely deforested areas (Nessimian et al., ApotentiallyseriousincipientthreattoAmazonianbiodiversity
2008).Thisispartlybecausesmallpatchesinevitablysamplefewer is global climate change. Over the past several decades tempera-
speciesandlesshabitatdiversitythanlargerpatches(Hailaetal., tures in the Amazon have increased by approximately
1993)whichisaggravatedbytheintrinsicrarityofmanytropical 0.025(cid:3)Cyr(cid:4)1 (Hansen et al., 2006; Malhi and Wright, 2004) but
forest species. Post-disturbance faunal relaxationmay take many slightlyfasterintheAndes(VuilleandBradley,2000).GlobalCli-
decadesuntilassemblagesinfragmentsreachaquasi-equilibrium mate Models (GCMs) predict that temperatures in these regions
(Kattan,1994;Ferrazetal.,2003).Suchspatialandtemporalsam- willriseby3–8(cid:3)Coverthenextcentury(Malhietal.,2009).Inre-
plingeffectscouldbeespeciallyimportantforAmazonianspecies, sponse to changes in temperature and climate, species assem-
whichoftenhavepatchydistributionsatvaryingspatialscalesand blages are predicted to respond with distributional shifts,
complexpatternsofendemism(e.g.ZimmermanandBierregaard, predominantly by moving upslope towards colder climates (Col-
1986; Gentry, 1992; Didham et al., 1998). Negative edge effects welletal.,2008;Chenetal.,2009).Consequently,theamountof
on forest organisms include altered microclimates (Williams- climatically suitable habitat available to many species will de-
Linera et al., 1998), fire damage (Cochrane and Laurance, 2002), crease,eveniftheyarecapableofperfectmigration,possiblylead-
elevated rates of tree mortality, and shifts in plant and animal ingtolocalorevenglobalextinction(Thomasetal.,2004).Habitat
community composition (Laurance et al., 2002). Finally, research loss will be much greater if species are unable to migrate at the
onedgeeffectsintheAmazonhasbeendisproportionatelyconcen- pace required by climate change, either due to limited dispersal
tratedwithinthePDBFFProjectnearManaus(Lovejoyetal.,1986), or interactions with other abiotic and biotic factors (Malcolm
so that the ecological impact of edges among different land-uses etal.,2006).Forestconversionandfragmentationreduceshabitat
andland-usehistoriesremainspoorlyunderstood(Fig.2). connectivity, thereby impeding geographic range readjustment.
Likewise,humanactivitiesabovethetreeline,suchascattlegraz-
5.5.Secondarygrowth ing and burning in the Andes, may prevent upslope migration
thereby hastening habitat loss and increasing extinction risk. If
Forest-replacingeconomicactivitiesofvaryingpatchsizesinthe thenumberofspeciesemigratingfromanareaexceedsthenum-
humidtropicsareusuallyshort-lived,resultinginhighlyvariable berimmigratingtherewillbelossoflocaldiversityorbioticattri-
C.A.Peresetal./BiologicalConservation143(2010)2314–2327 2323
Fig.4. Pan-Amazoniandistributionofdesignatedprotectedareas‘‘onpaper”underdifferentdenominationswithinandimmediatelyoutsidethephytogeographicboundaries
oftheregion(darkredline).Dark,intermediateandlightgreenpolygonsindicatetheboundariesofstrictlyprotectedareas,sustainabledevelopmentreserves,andofficially
recognisedindigenousterritories,respectively.Deforestedareas(by2007)outsideofparksandreservesareindicatedinorange;deforestationwithinparksisnotshown.
DataareunavailableforGuyana,SurinameandFrenchGuiana.(Forinterpretationofthereferencestocolourinthisfigurelegend,thereaderisreferredtothewebversionof
thisarticle.)
tion(Colwelletal.,2008;FeeleyandSilman,2009).Thisisapoten- levelsofendemism(Mares,1992;FjeldsåandRahbek,1998),this
tiallyseriousthreattoAmazonian–Andeanbiodiversity,sincethe largely reflects our disconcertingly large ignorance of fine- to
lowlandbiotahavefewspeciestoreplaceemigratingspeciesalong broad-scale patterns of species distributions for even the best
elevationalgradients. knownvertebratetaxasuchasbirdsandprimates(seeTable1in
Unliketemperature,thereisnoclearconsensusamongGCMsas Peres,2005).TheAmazonianforestandfreshwaterbiotaremains
tohowprecipitationwillchangeintheAmazonandtropicalAndes. severelyundersampled,anditslongevolutionaryhistoryhaslikely
However,mostmodelspredictincreaseddryingeitherduetolower generated a yet-to-be-uncovered high level of cryptic diversity
total annual precipitation or longer and more severe dry seasons (Fjeldså, 1994). Concentrations of relatively archaic lowland spe-
(Malhietal.,2008).Thesensitivityoftropicalforeststowateravail- ciesareincontrastwiththerelativelyyoungspeciesoftheeastern
abilityhasbeenwelldemonstratedthroughbothobservationaland slopesoftheAndes.Prioritiesonanyconservationagendashould
experimentalstudies.DetailedMesoamericanstudieshaveshown includemaximizingtheprotectionofphylogeneticdiversity(Cro-
thatevenrelativelyminorincreasesindryseasonlength/strength zier, 1997) and species-rich assemblages of disturbance-sensitive
mayleadtorapiddeclinesintreegrowth(Clarketal.,2009).These- old-growthlowlandforestspecialists,especiallyinareascurrently
vere Amazonian drought of 2005 decreased tree growth and ele- threatenedbyhighlevelsofdeforestation.Moreover,geologically
vatedtreemortality,resultinginlowerforestbiomassstocksand older species exposed to long periods of geoclimatic stability are
a net carbon emission (Phillips et al., 2009). These observations likely less preadapted to current environmental change and the
are supported by experimental rainfall exclusion from drought buffeting effect of a fluctuating climate, as shown for ancient
plots, which significantly increased large tree mortality (Nepstad Southeast Asian forest vertebrate species, which are both more
etal.,2007). Risingtemperaturescoupledwithdecreasedrainfall vulnerabletohabitatdegradationandhavesmallergeographicdis-
willlikelytriggermorefrequentandmoreseveredroughtsinthe tributions(Meijaardetal.,2008).
Amazon.Insomemodels,increasedhydrologicalstressispredicted Althoughtheerosionoftropicalforestbiodiversityworldwideis
totriggeralarge-scaleforestdieback,followedbypossiblereplace- most frequently associated with complete forest conversion to
ment by savannah-like habitat (Cox et al., 2004). While this has otherland-uses,amyriadofadditionalprocesseshavecontributed
beenquestionedbyseveralrecentstudies(seeCochraneandBar- towidespreadpopulationlossesatlocaltoregionalscales,includ-
ber,2009),climatechangeinconjunctionwithotherhumandistur- ingsurfacefires,forestfragmentation,selectivelogging,andover-
banceshasenormouspotentialtodrivesignificantlossesinforest harvestingofnon-timberresourcessuchasgamevertebrates(Lau-
biodiversity(Barlow and Peres,2008; Malhiet al.,2008). Specifi- rance and Peres, 2006). The combination of these threats means
cally,increasedmortalityofcanopytreesduetodryerconditions that,onewayoranother,mostoftheAmazoncanalreadybede-
may create large stocks of woody debris and open the canopy finedas‘‘human-modified”.
resultinginelevatedflammability(Nepstadetal.,2004)whichin Droughtsensitivityisamajordeterminantofspeciesdistribu-
turn will facilitate fire spread, especially if human access is en- tions of tropical forest trees (Engelbrecht et al., 2007; Butt et al.,
hancedthroughfragmentationandedgecreation. 2008)andothertaxa,particularlyinmoreaseasonalpartsoflow-
land Amazonia and Andean cloud forests. Yet virtuallythe entire
spectrum of forest disturbances highlighted in this review frac-
7.Conservationpolicyconsiderations
turesoreliminatestheprotectivestructureprovidedbytheforest
canopy, driving increased incident radiation that desiccate the
Althoughprioritizingbiodiversity conservation acrosslowland
understorey. This is often followed by wholesale compositional
Amazonia has been challenged on the grounds of putatively low