Amazonian fragments and global change

25 Pages·2017·0.33 MB·English

Biol.Rev.(2017),pp.000–000. 1
doi:10.1111/brv.12343
An Amazonian rainforest and its fragments
as a laboratory of global change
William F. Laurance1,2∗, Jose´ L. C. Camargo2, Philip M. Fearnside3,
Thomas E. Lovejoy2,4, G. Bruce Williamson2,5, Rita C. G. Mesquita2,3,
Christoph F. J. Meyer2,6,7, Paulo E. D. Bobrowiec8 and Susan G. W. Laurance1,2
1CentreforTropicalEnvironmentalandSustainabilityScience(TESS)andCollegeofScienceandEngineering,JamesCookUniversity,Cairns
4878,Australia
2BiologicalDynamicsofForestFragmentsProject,NationalInstituteforAmazonianResearch(INPA)andSmithsonianTropicalResearch
Institute,Manaus69067-375,Brazil
3DepartmentofEnvironmentalDynamics,NationalInstituteforAmazonianResearch(INPA),Manaus69067-375,Brazil
4DepartmentofEnvironmentalScienceandPolicy,GeorgeMasonUniversity,Fairfax,VA22030,U.S.A.
5DepartmentofBiologicalSciences,LouisianaStateUniversity,BatonRouge,LA70803,U.S.A.
6CentreforEcology,EvolutionandEnvironmentalChanges,UniversityofLisbon,1749-016,Lisbon,Portugal
7SchoolofEnvironmentandLifeSciences,UniversityofSalford,SalfordM54WT,U.K.
8BiodiversityCoordination,NationalInstituteforAmazonianResearch(INPA),Manaus69067-375,Brazil
ABSTRACT
Wesynthesizefindingsfromoneoftheworld’slargestandlongest-runningexperimentalinvestigations,theBiological
DynamicsofForestFragmentsProject(BDFFP).Spanninganareaof∼1000km2incentralAmazonia,theBDFFPwas
initiallydesignedtoevaluatetheeffectsoffragmentareaonrainforestbiodiversityandecologicalprocesses.However,
overits38-yearhistorytodatetheprojecthasfartranscendeditsoriginalmission,andnowfocusesmorebroadlyon
landscapedynamics,forestregeneration,regional-andglobal-changephenomena,andtheirpotentialinteractionsand
implications for Amazonian forest conservation. The project has yielded a wealth of insights into the ecological and
environmental changes in fragmented forests. For instance, many rainforest species are naturally rare and hence are
either missing entirely from many fragments or so sparsely represented as to have little chance of long-term survival.
Additionally, edge effects are a prominent driver of fragment dynamics, strongly affecting forest microclimate, tree
mortality,carbonstorageandadiversityoffauna.
Evenwithinourcontrolledstudyarea,thelandscapehasbeenhighlydynamic:forexample,thematrixofvegetation
surrounding fragments has changed markedly over time, succeeding from large cattle pastures or forest clearcuts
to secondary regrowth forest. This, in turn, has influenced the dynamics of plant and animal communities and
their trajectories of change over time. In general, fauna and flora have responded differently to fragmentation: the
most locally extinction-prone animal species are those that have both large area requirements and low tolerance
of the modified habitats surrounding fragments, whereas the most vulnerable plants are those that respond
poorly to edge effects or chronic forest disturbances, and that rely on vulnerable animals for seed dispersal or
pollination.
Relative to intact forests, most fragments are hyperdynamic, with unstable or fluctuating populations of species
in response to a variety of external vicissitudes. Rare weather events such as droughts, windstorms and floods have
had strong impacts on fragments and left lasting legacies of change. Both forest fragments and the intact forests in
our study area appear to be influenced by larger-scale environmental drivers operating at regional or global scales.
These drivers are apparently increasing forest productivity and have led to concerted, widespread increases in forest
dynamics and plant growth, shifts in tree-community composition, and increases in liana (woody vine) abundance.
* Addressforcorrespondence(Tel:[phone];E-mail:[email protected])
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
2 WilliamF.Lauranceandothers
Suchlarge-scaledriversarelikelytointeractsynergisticallywithhabitatfragmentation,exacerbatingitseffectsforsome
species and ecological phenomena. Hence, the impacts of fragmentation on Amazonian biodiversity and ecosystem
processesappeartobeaconsequencenotonlyoflocalsitefeaturesbutalsoofbroaderchangesoccurringatlandscape,
regionalandevenglobalscales.
Key words: Amazonia, biodiversity, carbon storage, climate change, drought, ecosystem services, edge effects,
environmentalsynergisms,habitatfragmentation,naturereserves.
CONTENTS
I. Introduction .............................................................................................. 3
II. Larger-scaledrivers ...................................................................................... 3
(1) Landscape-scalephenomena ......................................................................... 3
(2) Regional-scalephenomena ........................................................................... 4
(3) Global-scalephenomena ............................................................................. 4
III. Studyareaandkeydatasets .............................................................................. 5
(1) Studyarea ............................................................................................ 5
(2) Uniquedatasets ...................................................................................... 6
IV. Changesinintactforests .................................................................................. 6
(1) Unexpectedtrends ................................................................................... 6
(2) Potentialenvironmentaldrivers ...................................................................... 6
V. Consequencesoffragmentsize ........................................................................... 7
(1) Sampleeffects ........................................................................................ 8
(2) Areaeffects ........................................................................................... 8
VI. Edgeeffects ............................................................................................... 8
(1) Foresthydrology ...................................................................................... 8
(2) Strikingdiversityofedgeeffects ...................................................................... 9
(3) Impactsofmultipleedges ............................................................................. 9
(4) Effectsofedgeageandadjoiningvegetation .......................................................... 9
VII. Forestisolationandthematrix ........................................................................... 9
(1) Matrixstructureandcomposition .................................................................... 10
(2) Factorsinfluencingthematrix ........................................................................ 10
(3) Narrowforestclearings ............................................................................... 11
VIII. Dynamicsofforestfragments ............................................................................. 11
(1) Raredisturbances .................................................................................... 12
(2) Hyperdynamism ...................................................................................... 12
(3) Divergingtrajectoriesoffragments ................................................................... 13
(4) Ecologicaldistortions ................................................................................. 13
(5) Forestcarbondynamics .............................................................................. 14
IX. Speciesresponsestofragmentation ....................................................................... 14
(1) Non-randomextinctions .............................................................................. 14
(2) Non-neutralextinctions .............................................................................. 14
(3) Keycorrelatesofanimalvulnerability ................................................................ 15
(4) Keycorrelatesofplantvulnerability .................................................................. 16
X. Horizonsfornewresearch ............................................................................... 16
XI. Generallessons ........................................................................................... 17
(1) Valuesoflong-termresearch ......................................................................... 17
(2) Trainingisvital ....................................................................................... 17
XII. Lessonsforconservation .................................................................................. 17
(1) TheBDFFPisabest-casescenario ................................................................... 17
(2) Reservesshouldbelargeandnumerous .............................................................. 18
(3) Nofragmentisunimportant .......................................................................... 18
(4) Woundedlandscapescanrecover .................................................................... 18
XIII. Fragmentationandlarger-scaledrivers ................................................................... 18
(1) Interactingdrivers .................................................................................... 18
(2) TheAmazonandclimatechange .................................................................... 19
XIV. Conclusions .............................................................................................. 20
XV. Acknowledgements ....................................................................................... 20
XVI. References ................................................................................................ 20
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
Amazonianfragmentsandglobalchange 3
I. INTRODUCTION
The Biological Dynamics of Forest Fragments Project
(BDFFP) is the world’s largest and longest-running
experimental study of habitat fragmentation (Lovejoy etal.,
1986; Bierregaard etal., 1992; Laurance etal., 2002, 2011).
LocatedincentralAmazonia(Fig.1),theBDFFPhasevolved
since its inception in 1979 into an epicentre for long-term
research. Beyond this, its research mission has gradually
broadenedtoincludenotonlyforestfragmentationbutalso
studies of forest regeneration, landscape dynamics, climatic
Fig. 1. Map of the Biological Dynamics of Forest Fragments
variation, regional- and global-change phenomena and a
ProjectincentralAmazonia.
varietyofinterdisciplinaryresearchtopics.
The BDFFP is strategically located at the heart of the
Amazon, the world’s largest tropical forest. The Amazon being altered by large-scale agriculture (Fearnside, 2001;
itselfliesattheintersectionofkeyquestionsinglobalchange, Gibbs etal., 2010), industrial logging (Asner etal., 2005),
both for research and for action. It is believed to be one of proliferating roads (Laurance etal., 2001a; Fearnside, 2002,
the major regions that will be most impacted by projected 2007; Killeen, 2007), increasing biofuel production (Butler
climaticchange(Salazar,Nobre&Oyama,2007;Dai,2012; & Laurance, 2009), hydroelectric dams (Fearnside, 2016b)
IPCC, 2013; Nobre etal., 2016). If effectively conserved andoil,gasandminingdevelopments(Fineretal.,2008).
and managed, the Amazon has the potential to contribute LargeexpansesoftheAmazonhavealreadybeencleared,
markedlytoeffortstolimitclimatechangeduringthenarrow resultinginconsiderablefragmentation.Bytheearly1990s,
window of time we have remaining to avert ‘dangerous’ the area of forest that was fragmented (<100km2) or
global warming (Fearnside, 2000, 2016a; Houghton, Byers vulnerable to edge effects (<1km from edge) was over
& Nassikas, 2015). Because of its enormous carbon-storage 150% greater than the area that had been deforested
capacity,itisalsooneoftheplacesonEarthwheresharply (Skole & Tucker, 1993). From 1999 to 2002, deforestation
reducing greenhouse-gas emissions could be achieved by and industrial selective logging in Brazilian Amazonia,
limitingforestlossanddegradation,therebydeliveringgreat respectively,created∼32000and∼38000kmofnewforest
globalbenefitsforhumankind(Stickleretal.,2009). edgeannually(Broadbentetal.,2008).Prevailinglandusesin
Today, the BDFFP is one of the most enduring, Amazonia,suchascattleranchingandsmall-scalefarming,
influential and highly cited environmental investigations typicallyproducelandscapesdominatedbysmall(<400ha)
in the world (Gardner etal., 2009; Peres etal., 2010; and irregularly shaped forest fragments (Fig. 2) (Cochrane
Pitman etal., 2011). Its wide-ranging research has involved & Laurance, 2002; Broadbent etal., 2008). Such fragments
hundreds of Brazilian and international investigators and areespeciallyvulnerabletoawidearrayofedgeeffectsand
thousandsofstudentsandothertrainees.Herewesynthesize otherexternalvicissitudes(Bierregaardetal.,1992;Laurance
the contributions of this singular project to the study of etal.,2002,2011).
habitat fragmentation, including its broader consequences Changesinforestcovercanhaveimportanteffectsonlocal
for Amazonian ecosystems and biota. We emphasize that climateandvegetation.Habitatfragmentationcanpromote
many of the local impacts of fragmentation in the Amazon forest desiccation via phenomena such as the ‘vegetation
arebeingmodifiedorexacerbatedbyenvironmentalchanges breeze’ (Fig. 3). This occurs because fragmentation leads
occurring at wider landscape, regional and even global to the juxtaposition of cleared and forested lands, which
scales.Weassertthattheeffectsoffragmentationcannotbe differ greatly in their physical characteristics. Air above
fully understood without considering the influence of these forests is cooled by evaporation and especially plant
larger-scalephenomena. evapotranspiration,butsuchcoolingisgreatlyreducedabove
clearings(Avissar&Schmidt,1998).Asaresult,theairabove
clearingsheatsupandrises,reducinglocalairpressureand
drawing moist air from the surrounding forests into the
II. LARGER-SCALEDRIVERS
clearing. As the rising air cools, its moisture condenses into
convectivecloudsthatcanproducerainfallovertheclearing
(1) Landscape-scalephenomena
(Avissar&Liu,1996).Theairisthenrecycledascool,dryair
Thecorrelatedprocessesofforestlossandfragmentationare backovertheforest.Inthisway,clearingsofafewhundred
among the greatest threats to tropical biodiversity (Lovejoy hectaresormorecandrawmoistureawayfromnearbyforests
etal., 1986; Ewers & Didham, 2006; Laurance & Peres, (W.F.Laurance,2004b;Cochrane&Laurance,2008;Nobre
2006; Gibson etal., 2011). Amazonia harbours more than etal., 2016). In eastern Amazonia, satellite observations
halfoftheworld’ssurvivingtropicalforest,andiscurrently of canopy water content suggest such desiccating effects
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
4 WilliamF.Lauranceandothers
greaterwindspeeds(fromreducedsurfacedrag),whichcould
affectmoistureconvergenceandcirculation(Walker,Sud&
Atlas,1995;Sud,Yang&Walker,1996).Itisevenpossible
that moderate forest loss and fragmentation could increase
net regional precipitation in the near term, as a result of
increasingconvectionalstormsdrivenbyvegetationbreezes,
although the main effect would be to remove moisture
fromforestsandredistributeitoveradjoiningclearings.The
greatestconcernisthatifdeforestationreachessomecritical
threshold,Amazonianrainfallmightdeclineabruptlyasthe
regional hydrological system collapses (Avissar etal., 2002;
Nobreetal.,2016).
Massive smoke plumes produced by forest and pasture
fires cause two additional effects of forest loss. Smoke
hypersaturates the atmosphere with cloud condensation
nuclei (microscopic particles in aerosol form) that bind
with airborne water molecules and thereby inhibit the
formation of raindrops (Rosenfeld, 1999). In addition,
by absorbing solar radiation, smoke plumes warm the
atmosphere,inhibitingcloudformation.Asaresultofthese
two effects, large fires can create rain shadows that extend
Fig. 2. Habitat fragmentation in eastern Amazonia caused for hundreds or even thousands of kilometers downwind
by a (A) forest-colonization project (Tailaˆndia) and (B) cattle (Freitas,SilvaDias&SilvaDias,2000).Thiscanbeaserious
ranching(Paragominas).Forestsareblackandclearedareasare threat to forests because tropical fires are lit during the
grey. Each image shows an area of about 600km2 (adapted criticaldry-seasonmonths,whenplantsarealreadymoisture
fromCochrane&Laurance,2002).
stressedandmostvulnerabletofire.
can penetrate 1.0–2.7km into fragmented forests (Briant,
(3) Global-scalephenomena
Gond & Laurance, 2010). This moisture-robbing function
of clearings, in concert with frequent burning in adjoining Howwillglobal-changedriversaffecttheAmazon?Although
pastures, could help to explain why fragmented forests are model predictions for future climates in Amazonia vary
sovulnerabletodestructive,edge-relatedfires(Cochrane& considerably, it is generally expected that parts of the
Laurance,2002,2008;Barlowetal.,2006). basin will become hotter and drier under projected global
warming(IPCC,2013;Nobreetal.,2016).Whatthisportends
for the Amazon is a matter of some controversy. Earlier
(2) Regional-scalephenomena
studies assuming CO concentrations about twice those in
2
Extensiveforestclearingreducestherateofevapotranspira- the pre-industrial atmosphere, notably by the UK Hadley
tionbecausepasturegrassesandcroplandshavefarlessleaf Centre, projected disastrous forest die-offs (Cox etal., 2000,
areaandshallowerrootsthandorainforests(Jippetal.,1998). 2004). However, this conclusion has been countered by
Atregionalscales,decliningevapotranspirationcouldreduce new models from the same research group, suggesting the
rainfallandcloudcoverandincreasealbedoandsoil-surface Amazonforestwillremainalmostentirelyintactatuptofour
temperatures. Moisture recycling via evapotranspiration is timespre-industrialCO levels(Coxetal.,2013;Goodetal.,
2
exceptionally important in the hydrological regime of the 2013; Huntingford etal., 2013). The main difference is that
Amazon (Salati & Vose, 1984; Eltahir & Bras, 1994), espe- thenewermodelsincludeCO -fertilizationeffects(Kimball
2
ciallyduringthedryseason(Malhietal.,2008),becausethe etal.,1993),whichareassumedtoincreaseplantgrowthand
forestisbothvastandfarfromthenearestocean. water-useefficiency.Thisisbecausethehigheratmospheric
However, the regional consequences of large-scale CO concentrationshouldallowplantstoconservewaterby
2
deforestationarefarfromfullyunderstood.Somemodelling decreasing the duration of stomatal-opening periods while
studies suggest that Amazonian deforestation could reduce stilltakinginadequateCO forphotosynthesis.
2
basin-wide precipitation by roughly 20–30%, but these Other global-change phenomena, such as extreme
estimates rely on a simplistic assumption of complete, climatic events, could also potentially have important
uniformforestclearing(e.g.Nobre,Sellers&Shukla,1991; impacts.Forinstance,droughtsintheAmazonarenormally
Dickinson & Kennedy, 1992; Lean & Rowntree, 1993). associated with El Nin˜o events and are strongest in the
Model results based on actual (circa 1988) deforestation southern, eastern and north-central Amazon – areas of the
patterns in Brazilian Amazonia have been less dramatic, basin that already experience pronounced dry seasons.
with deforested regions predicted to experience modest However, severe droughts in 2005 and 2010 arose from
(6–8%) declines in rainfall, moderate (18–33%) reductions a completely different cause – exceptionally high Atlantic
in evapotranspiration, higher soil-surface temperatures and sea-surface temperatures, which caused the rain-bearing
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
Amazonianfragmentsandglobalchange 5
Fig.3. Thevegetation-breezephenomenon,whichcanpromoteforestdesiccationinthegeneralvicinityofpasturesandclearings
(fromCochrane&Laurance,2008).
inter-tropical convergence zone to shift northward (Lewis The study area includes three large cattle ranches
etal.,2011).Theresultingdroughtsaffectednotjustthedrier, (∼5000haeach)containing11forestfragments(fiveof1ha,
more seasonal parts of the basin but also its wettest areas fourof10haandtwoof100ha),andlargeexpansesofnearby
in central and western Amazonia. Because plant species in continuousforestthatserveasexperimentalcontrols(Fig.1).
thesewetareasareadaptedtoperenniallyhumidconditions, Intheearly1980s,thefragmentswereisolatedfromnearby
thenewdroughtscausedmassiveplantmortality,killingtens intactforestbydistancesof80–650mthroughclearingand
of millions of trees while releasing several billion tonnes of burning of the surrounding forest. A key advantage was
atmospheric carbon emissions (Lewis etal., 2011; Marengo that pre-fragmentation censuses were conducted for many
etal.,2012).Withmountingevidencethatclimaticextremes animalandplantgroups(e.g.trees,understoreybirds,small
couldbecomemorefrequentandintenseinawarmingworld mammals,primates,frogs,manyinvertebratetaxa),thereby
(Veraetal.,2006;Herringetal.,2015;Jime´nez-Mun˜ozetal., allowing long-term changes in these groups to be assessed
2016),couldtheAmazonbedrivenintoanewkindofclimatic far more confidently than in most other fragmentation
dynamic – oneforwhichitsecosystemsandbiodiversityare studies.
poorlyadapted?
Because of poor soils and low productivity, the ranches
surroundingtheBDFFPfragmentswerelargelyabandoned,
especially after government fiscal incentives dried up from
III. STUDYAREAANDKEYDATASETS
1988 onwards. Secondary forests – initially dominated by
Vismia spp. in areas that were cleared and burned,
(1) Studyarea and by Cecropia spp. in areas that were cleared without
TheexperimentallandscapeoftheBDFFPspans∼1000km2 fire – proliferatedinmanyformerlyforestedareas(Mesquita
in area and is located 80km north of Manaus, Brazil. etal.,2001).Someregeneratingareasinitiallydominatedby
The topography is relatively flat (80–160m elevation) Cecropia later grew into structurally well-developed (>20m
but dissected by numerous stream gullies. The heavily tall), species-rich secondary forests (Longworth etal., 2014).
weathered, nutrient-poor soils of the study area are typical Vismia-dominated regrowth, however, which is relatively
oflargeexpansesoftheAmazonBasin.Rainfallrangesfrom species poor, is maturing far more slowly (Norden etal.,
1900 to 3500mm annually with a moderately strong dry 2011;Williamsonetal.,2014).
seasonfromJunetoOctober.Theforestcanopyis30–37m Tohelpmaintainisolationoftheexperimentalfragments,
tall, with emergent trees to 55m. Species richness of trees 100m-wide strips of regrowth were cleared and burned
[≥10cm diameter at breast height (dbh)] often exceeds around each fragment on 4–5 occasions, most recently in
280speciesha−1, which is among the highest known tree 2013–2014.However,humandisturbancesthataffectmany
diversityintheworld(DeOliveira&Mori,1999;Laurance fragmented landscapes in the Amazon, such as major fires,
etal.,2010b).Comparablyhighlevelsofdiversityareseenin logging and hunting (Michalski & Peres, 2005), are largely
manyotherplantandanimaltaxa. preventedattheBDFFP.
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
6 WilliamF.Lauranceandothers
(2) Uniquedatasets controls (Lovejoy etal., 1986; Bierregaard etal., 1992). The
firstisthatstandardizedcensusesofmanyplantandanimal
The BDFFP sustains some of the longest-running and
taxawereconductedineachexperimentalfragmentbeforeit
highest-quality environmental data sets in the Amazon.
wasisolatedfromthesurroundingforest.Thesecondisthat
This includes a network of 69 1-ha forest-dynamics plots
dozens of ‘control’ sites in nearby intact forests have been
arrayed across intact and fragmented forests in the study
monitoredforupto38years,toassessthetemporaldynamics
area, which has been monitored since the early 1980s, and
of these sites. The intact-forest sites were expected to vary
apermanent25-haplotinintactforestestablishedin2005.
randomly over time or respond to occasional vicissitudes
Theseplotshavemadeimportantcontributionstoreducing
suchasdroughts,butnottochangeovertimeinadirectional
uncertaintiesinbiomassandcarbon-storageestimatesforthe
manner.
Amazon (e.g. Phillips etal., 1998; Nascimento & Laurance,
Amajorsurprise,however,isthattheBDFFPcontrolshave
2002; Baker etal., 2004). For example, in comparison to
changed in several concerted ways (Laurance etal., 2014a).
the 3000 1-ha plots surveyed by the RADAMBRASIL
Beforeinterpretinghowfragmentationhasalteredecological
Project (Nogueira etal., 2008, 2015), the BDFFP plots
communities in the BDFFP, it is first important to identify
include data on nearly all other forest components such
howtheintact-forestsiteshavechanged,asthesewidespread
assmaller(1–30cmdiameter)trees,palms,lianas,strangler
effects are presumably altering the forest fragments as well.
figs, understorey vegetation and dead biomass (Nascimento
Thelong-termmonitoringoftensofthousandsoftreesand
& Laurance, 2002, 2004). These data allow assessment
populations of many other plant and animal groups has
of spatial variability in aboveground biomass with a high
allowed researchers to identify synchronous changes in the
degreeofconfidence.Forexample,theabovegroundbiomass
undisturbedforestsattheintactsites,andtoattempttoinfer
of trees varies considerably among the 69 1-ha plots in
the BDFFP landscape (mean±S.D.=356±47Mgha−1; theirenvironmentalcauses.
How have the intact forests changed? Over the past
Laurance etal., 1999). This high variability demonstrates
2–3decades, we have found that (i) forest dynamics (tree
aneedformanyplotsthatarespatiallystratified,ratherthan
mortality and recruitment) have accelerated significantly
onlyafewplotsof1haorsmallerscatteredirregularlyaround
overtime(W.F.Lauranceetal.,2004b,2014a;S.G.Laurance
the Amazon, for calibrating satellite imagery for biomass
etal., 2009); (ii) tree-community composition has shifted,
mapping,andforestimatinggreenhouse-gasemissionsfrom
generallyinfavouroffaster-growingcanopytreesandagainst
ongoingdeforestation(seeFearnside,2016a).
shade-tolerantsubcanopytrees(W.F.Lauranceetal.,2004b,
Floristic data from the BDFFP are exceptional for
2005);(iii)growthrateshaveincreasedforthelargemajority
their high quality of species identification, allowing better
(84%)oftreegenerainourstudyarea(Fig.4)(W.F.Laurance
matching with plant functional and phylogenetic traits
etal., 2004b); (iv) aboveground tree biomass has increased
such as wood density and tree form (e.g. Fearnside, 1997;
significantly over time (although tree-stem numbers have
Nogueira, Nelson & Fearnside, 2005; Chave etal., 2006;
not changed significantly; S.G. Laurance etal., 2009); and
Nogueira etal., 2007; Souza etal., 2016). Given their broad
(v) lianas have increased markedly in abundance (Fig. 5)
spatial extent and temporal depth, these data have also
(Lauranceetal.,2014a,b).
contributedtoknowledgeofthediversityofAmazonianplant
speciesandtheirrelationshipstosoiltextureandchemistry,
(2) Potentialenvironmentaldrivers
topography, forest dynamics and climatic variables at
both landscape and regional scales (e.g. Bohlman etal., Why are the intact forests changing? The causes of such
2008; S.G. Laurance etal., 2009; Laurance, Andrade & changes are incompletely understood (Lewis, Malhi &
Laurance, 2010a; Laurance etal., 2010b; ter Steege etal., Phillips, 2004a; Lewis etal., 2009b) and often controversial
2013). Biodiversity and ecosystem processes represent part (Clark, 2004; Fearnside, 2004). Nonetheless, the trends we
of what is lost when the forest is destroyed or degraded. detected appear broadly consistent with those observed
Understanding these processes is essential for assessing not elsewhere in many Amazonian (Phillips & Gentry, 1994;
only the vulnerability of forests, but also their potential Phillipsetal.,1998,2002;Bakeretal.,2004;Lewisetal.,2004b;
resilience in the face of global change and their rates of Schnitzer&Bongers,2011)andAfrican(Lewisetal.,2009b)
recovery following various perturbations (Williamson etal., tropical forests. These trends are consistent with ecological
2014; Souza etal., 2016). Data sets for a number of faunal patterns expected from rising forest productivity, including
groups, such as birds, amphibians, primates and major faster plant growth, increasing forest biomass, intensifying
invertebratetaxa,areofcomparablequalityandduration. competitionleadingtogreaterplantmortalityandturnover,
and increasing abundances of plant species that can attain
highgrowthratesorareadvantagedindynamicforests(W.F.
Lauranceetal.,2004b;Lewisetal.,2004b,2009b).
IV. CHANGESININTACTFORESTS
Themostfrequentlyinvokeddriverofrisingtropicalforest
productivity is CO fertilization (e.g. Lewis etal., 2004a,
(1) Unexpectedtrends 2
2009a). This is because many plants show faster growth
Aspartofitsoriginalmissiontoassesslong-termchangesin under enriched CO (Oberbauer, Strain & Fletcher, 1985;
2
fragmentedforests,theBDFFPhastwotypesofexperimental Granados & Ko¨rner, 2002; Ko¨rner, 2004) and because
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
Amazonianfragmentsandglobalchange 7
Fig.5. Increaseinabundanceoflianasinintact-forestplotsof
Fig. 4. Rates of tree growth in intact forests of the theBiologicalDynamicsofForestFragmentsProject(BDFFP)
BiologicalDynamicsofForestFragmentsProject(BDFFP)have (fromLauranceetal.,2014b).Thesolidlineshowsy=xwhereas
acceleratedovertimeforthelargemajority(84%)oftreegenera thedottedlineisalinearregressionfittedtothedata.
(fromW.F.Lauranceetal.,2004b).Datashownaremeanrates
oftrunk-diametergrowthforgenerathatincreasedordecreased
The notable increases in liana abundance in our intact
significantlyinabundanceovertimeintheplots,aswellasthose
forests (Laurance etal., 2014b) might arise because lianas
thatshowednosignificanttrend.Interval1is1984–1991,and
interval2is1992–1999. appear to exploit rising CO2 concentrations and drier
conditions more effectively than do trees (Condon, Sasek
&Strain,1992;Granados&Ko¨rner,2002;butseeMarvin
atmospheric CO levels have risen rapidly, especially in
2 etal.,2015).Treeswithheavylianainfestationsareknownto
recent decades. This view is supported by compelling
exhibitelevatedmortalityandreducedgrowth(Ingwelletal.,
evidenceofalargecarbonsinkinthebiosphere(Ballantyne
2010).Notably,inourstudyarea,lianaabundanceisstrongly
etal.,2013),asubstantialpartofwhichappearstobeonland
and negatively correlated with live tree biomass (Fig. 6)
(Sarmientoetal.,2010)andinthetropics(Lewisetal.,2009a;
(Laurance etal., 2001b). Liana increases over time have
Huntingfordetal.,2013).
alsobeenobservedintropicalforestsinwesternAmazonia,
Other explanations for the rising productivity, however,
the Guianas, Central America and elsewhere (Schnitzer &
are not implausible. For instance, droughts can influence
Bongers, 2011), with rising atmospheric CO and possibly
forestdynamicsandcompositionandappeartobeincreasing 2
increasing drought being the most frequent explanations
in parts of the Amazon (Lewis etal., 2009a; Marengo etal.,
(see Laurance etal., 2014b and references therein). This
2011; Chou etal., 2013; Fu etal., 2013). The increase in
potentially negative effect of CO enrichment on forest
forest dynamics we observed in intact forests appears to be 2
biomass via increasing liana infestations is not included in
driven primarily by rising tree mortality, with recruitment
thelatestHadleyCentremodels(Coxetal.,2013;Goodetal.,
and growth often lagging behind periods of high mortality.
2013;Huntingfordetal.,2013),andcouldcanceloutsomeof
Thesemortalitypulsesarepositivelyassociatedwithseveral
thecarbon-storagebenefitssuggestedforahigh-CO future
factors, including El Nin˜o droughts and increasing rainfall 2
(Ko¨rner,2004,2017).
seasonality(S.G.Lauranceetal.,2009).
Hence,forwhateverthereasonorreasons,itisapparent
Additionally, multi-decadal shifts in solar radiation or
that the intact forests in our study area are changing in
cloudiness could potentially increase forest productivity,
a variety of ways. Such changes are likely to interact
although evidence for such shifts in the tropics is limited
with, and potentially complicate or amplify, the impacts
(Lewisetal.,2009a).Recoveryfrompastdisturbancehasalso
offragmentationontropicalforestcommunities.
beenhypothesizedtounderliechangesatsometropicalforest
sites, but there is no evidence of widespread disturbance in
our study area (W.F. Laurance etal., 2004b, 2005) aside
from charcoal fragments that are at least four centuries old V. CONSEQUENCESOFFRAGMENTSIZE
(Bassini & Becker, 1990; Fearnside & Leal Filho, 2001),
possibly indicating major fires during past mega-El Nin˜o TheBDFFP’soriginalmissionfocusesonassessingtheeffects
events(Meggers,1994). of fragment area on Amazonian forests and fauna, and on
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
8 WilliamF.Lauranceandothers
even with constant sampling effort across all fragments.
Such declines are evident in leaf bryophytes (Zartman,
2003), tree seedlings (Benítez-Malvido & Martinez-Ramos,
2003b), palms (Scariot, 1999), understorey insectivorous
birds (Stratford & Stouffer, 1999; Ferraz etal., 2007), bats
(Sampaio, 2000; Rocha etal., 2017), primates (Gilbert &
Setz, 2001; Boyle & Smith, 2010b) and larger herbivorous
mammals (Timo, 2003), among others. For such groups,
smaller fragments (<100ha) are often unable to support
viable populations. A few groups, such as ant-defended
plants and their ant mutualists, show no significant
decline in diversity with fragment area (Bruna etal.,
2005).
Fragment size also influences the rate of species losses,
withsmallerfragmentslosingspeciesmorequickly(Lovejoy
etal., 1986; Stouffer, Strong & Naka, 2008). Assuming that
the surrounding matrix is hostile to bird movements and
precludes colonization, Ferraz etal. (2003) estimated that a
1000-fold increase in fragment area would be needed to
Fig.6. Negativeassociationbetweenlianaabundanceandthe
slow the rate of local species extinctions by 10-fold. Even a
aboveground biomass of live trees in Biological Dynamics of
fragment of 10000 ha in area would be expected to lose a
ForestFragmentsProject(BDFFP)forest-dynamicsplots(from
substantialpartofitsbirdfaunawithinonecentury(Ferraz
Lauranceetal.,2001b).
etal., 2003). Similarly, long-term mark–recapture studies
suggestthatverylargefragmentswillbeneededtomaintain
keyecologicalandecosystemprocesses.Herewesummarize fully intact assemblages of certain faunal groups, such as
major findings and conservation lessons that have been ant-following birds, which forage over large areas of forest
gleanedtodate. (VanHoutanetal.,2007).
(1) Sampleeffects
Many species in Amazonian forests are rare or patchily VI. EDGEEFFECTS
distributed. This phenomenon is especially pronounced
in the large expanses of the basin that overlay heavily AnimportantinsightfromtheBDFFPistheextenttowhich
weathered, nutrient-poor soils (e.g. Radtke, da Fonseca & edgeeffects – physicalandbioticchangesassociatedwiththe
Williamson, 2008). In these areas resources such as fruits, abrupt,artificialmarginsofhabitatfragments–influencethe
flowersandnectararetypicallyscarceandplantsareheavily dynamicsandcompositionofplantandanimalcommunities.
defendedagainstherbivoreattack(Laurance,2001). Herewesummarizekeyfindingsfromthiswork.
Herein lies a key implication for understanding forest
fragmentation: given their rarity, many species may be
(1) Foresthydrology
absent from fragments not because their populations have
vanished, but because they were simply not present at The hydrological regimes of fragmented landscapes differ
the time of fragment creation – a phenomenon termed the markedly from those of intact forest (Kapos, 1989; Kapos
‘sampleeffect’(Wilcox&Murphy,1985).Suchsampleeffects etal., 1993). Pastures or crops surrounding fragments
are the hypothesized explanation for the absence of many have much lower rates of evapotranspiration than do
rare understorey bird species from fragments (Ferraz etal., forests, causing such areas to be hotter and drier than
2007).Inaddition,manybeetles(Didhametal.,1998a),bats forests (Camargo & Kapos, 1995). Field observations and
(Sampaioetal.,2003;Farnedaetal.,2015;Meyeretal.,2015; heat-flux simulations suggest that desiccating conditions
Rochaetal.,2017),ant-defendedplants(Bruna,Vasconcelos can penetrate up to 100–200m into fragments from
&Heredia,2005)andtrees(Bohlmanetal.,2008;Laurance adjoining clearings (Malcolm, 1998; Didham & Lawton,
etal.,2010b)attheBDFFPexhibithighlevelsofrarity,habitat 1999).Further,streamsinfragmentedlandscapesexperience
specializationorpatchiness. greater temporal variation in flow rate than do those in
forests, because clearings surrounding fragments have less
evapotranspirationandrainfallinterceptionandabsorption
(2) Areaeffects
by vegetation (Trancoso, 2008). Rapid runoff promotes
Understandingfragment-areaeffectshaslongbeenacentral localized flooding in the wet season and stream failure
goal of the BDFFP (Lovejoy & Oren, 1981; Lovejoy in the dry season, with potentially important impacts
etal., 1984, 1986; Pimm, 1998). The species richness of on aquatic invertebrates (Nessimian etal., 2008) and fish
many organisms declines with decreasing fragment area, assemblages.
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
Amazonianfragmentsandglobalchange 9
(2) Strikingdiversityofedgeeffects 1994), tree mortality (Laurance etal., 2006a), abundance
and species richness of tree seedlings (Benítez-Malvido,
Atleastoverthefirst3–4decadesafterisolation,edgeeffects
1998; Benítez-Malvido & Martinez-Ramos, 2003b), liana
have been among the most important drivers of ecological
abundance (Laurance etal., 2001b) and the density and
change in the BDFFP fragments. The distance to which
diversityofdisturbance-lovingpioneertrees(Lauranceetal.,
differentedgeeffectspenetrateintofragmentsvarieswidely,
2006a,b,2007).Theadditiveeffectsofnearbyedgesprobably
ranging from 10 to 300m at the BDFFP (Laurance etal.,
help to explain why small (<10ha) or irregularly shaped
2002)andconsiderablyfurther(atleast2–3km)inareasof
forest remnants are often so severely altered by forest
theAmazonwhereedge-relatedfiresarecommon(Cochrane
fragmentation(Zartman,2003;Lauranceetal.,2006a).Some
&Laurance,2002,2008;Briantetal.,2010).
fauna are likewise sensitive to multiple edges. For instance,
Edge phenomena are remarkably diverse (Fig. 7). They
the number of nearby forest edges was found to be an
include increased desiccation stress, wind shear and wind
important predictor of local bat abundance (Rocha etal.,
turbulence that sharply elevate rates of tree mortality and
2017).
damage (Laurance etal., 1997, 1998a). These in turn cause
wide-ranging alterations in the community composition of
trees (Laurance etal., 2000, 2006a,b) and lianas (Laurance (4) Effectsofedgeageandadjoiningvegetation
etal., 2001b). Such stresses may also reduce germination
When a forest edge is newly created it is open to fluxes of
(Bruna, 1999) and establishment (Uriarte etal., 2010)
wind, heat and light, creating sharp edge-interior gradients
of shade-tolerant plant species in fragments, leading to
inforestmicroclimatethatstressorkillmanyrainforesttrees
dramatic changes in the composition and abundance of
(Lovejoyetal.,1986;Sizer&Tanner,1999).Astheedgeages,
tree seedlings (Benítez-Malvido, 1998; Benítez-Malvido &
however,proliferatingvinesandlateralbranchgrowthtend
Martinez-Ramos,2003b).
to‘seal’theedge,makingitlesspermeabletomicroclimatic
Manyanimalgroups,suchasnumerousbees,wasps,flies
changes (Camargo & Kapos, 1995; Didham & Lawton,
(Fowler, Silva & Venticinque, 1993), beetles (Didham etal.,
1999).Treedeathfrommicroclimaticstressislikelytodecline
1998a,b), ants (Carvalho & Vasconcelos, 1999), butterflies
over the first few years after edge creation (D’Angelo etal.,
(Brown & Hutchings, 1997), understorey birds (Quintela,
2004) as the edge becomes less permeable, because many
1985; S.G. Laurance, 2004a) and gleaning predatory bats
drought-sensitive individuals die immediately and because
(Rocha,2016;Rochaetal.,2017),declineinabundancenear
surviving trees may acclimate to drier, hotter conditions
forest edges. Edge habitats of continuous forest and larger near the edge (Laurance etal., 2006a). Tree mortality from
fragments (100ha) have fewer species of bats and higher
wind turbulence, however, probably increases as the edge
levels of dominance by a few common species (Rocha, ages and becomes more closed because, as suggested by
2016;Rochaetal.,2017).Negativeedgeeffectsareapparent wind-tunnelmodels,downwindturbulenceincreasesifedges
even along narrow forest roads (20–30m width). Among arelesspermeable(W.F.Laurance,2004b).
understoreybirds,for example,fiveof eightforagingguilds Regrowth forest adjoining fragment edges can also
declined significantly in abundance within 70m of narrow lessenedge-effectintensity.Microclimaticchanges(Didham
roads, evidently in response to increased light and forest & Lawton, 1999), tree mortality (Mesquita, Delamoˆnica
disturbancenearroadedges(S.G.Laurance,2004a). & Laurance, 1999) and edge avoidance by understorey
Somegroupsoforganismsremainstableorevenincrease birds (Develey & Stouffer, 2001; S.G. Laurance, Stouffer
in abundance near edges. Leaf bryophytes (Zartman & & Laurance, 2004; S.G. Laurance, 2004a) and gleaning
Nascimento, 2006), wandering spiders (Ctenus spp.; Rego, animal-eating bats (Sampaio, 2000; Meyer, Struebig &
Venticinque & Brescovit, 2007; Mestre & Gasnier, 2008) Willig, 2016; Rocha, 2016; Rocha etal., 2017) are all
and many frogs (Gascon, 1993) displayed no significant reducedwhenforestedgesarebufferedbyadjoiningregrowth
response to edges. Organisms that favour forest ecotones forest,relativetoedgesborderedbycattlepastures.Mature
ordisturbances,suchasmanyspeciesofgap-favouringand regrowth can be particularly benign for some fauna; for
frugivorous birds (S.G. Laurance, 2004a), hummingbirds example,diverseassemblagesofaerial-feedinginsectivorous
(Stouffer&Bierregaard,1995a),frugivorousbatsthatexploit bats showed similar activity patterns in primary forest
earlysuccessionalplants(Sampaio,2000;Rochaetal.,2017), and in adjoining 30-year-old secondary forests (Navarro,
light-loving butterflies (Leidner, Haddad & Lovejoy, 2010) 2014).
and fast-growing lianas (Laurance etal., 2001b), increase in
abundancenearedges,sometimesdramatically.
VII. FORESTISOLATIONANDTHEMATRIX
(3) Impactsofmultipleedges
BDFFP research demonstrates that plots near two or more Unliketrueislandsencircledbywater,habitatfragmentsare
edges suffer more severe edge effects than do those near surrounded by a matrix of modified vegetation that can be
just one edge (Fig. 8). This conclusion is supported by highly variable in space and time. Here we highlight key
studiesofedge-relatedchangesinforestmicroclimate(Kapos, factors that can influence the matrix and how, in turn, the
1989; Malcolm, 1998), vegetation structure (Malcolm, matrixinfluencesfragmentdynamicsandcomposition.
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety
10 WilliamF.Lauranceandothers
Fig.7. Thediversityofedge-effectphenomenastudiedattheBiologicalDynamicsofForestFragmentsProject(BDFFP)andthe
distancetowhicheachwasfoundtopenetrateintofragmentinteriors(adaptedfromLauranceetal.,2002).PAR,photosynthetically
activeradiation.Someenvironmentalphenomena(e.g.relativehumidity,soilmoisture)appearmorethanoncebecausetheywere
measuredbydifferentinvestigatorsusingvaryingmethods,times,and/orstudylocations.
(1) Matrixstructureandcomposition Gasnier, 2008), dung beetles (Quintero & Roslin, 2005),
euglossine bees (Becker, Moure & Peralta, 1991) and
The BDFFP landscape has experienced considerable
monkeyssuchasredhowlersAlouattaseniculus,beardedsakis
dynamism over time. In particular, secondary forests have
Chiropotes satanas and brown capuchins Cebus apella (Boyle &
gradually overgrown most pastures in the study area. This
Smith,2010b),havealsorecolonizedsomeofthefragments.
regrowthlessenstheeffectsoffragmentationforsomespecies,
The surrounding matrix also has a strong effect on
with the matrix becoming less hostile to faunal use and
plant communities in fragments by reducing edge effects
movements. Several species of insectivorous birds that had
(see Section VI), influencing the movements of pollinators
formerlydisappearedfromfragmentshaverecolonizedthem
(Dick, 2001; Dick, Etchelecu & Austerlitz, 2003) and seed
as surrounding secondary forests regenerated (Stouffer &
dispersers (Jorge, 2008; Bobrowiec & Gribel, 2010; Boyle
Bierregaard, 1995b; Stouffer etal., 2011). The rate of local
&Smith,2010b)andstronglyinfluencingtheseedrainthat
extinctionsofbirdshasalsodeclined(Stoufferetal.,2008).
arrivesinfragments.Forinstance,pioneertreesregenerating
The regenerating forest in the matrix now permits
in fragments differed strikingly in composition between
fragments as small as 100ha to support bird and bat
fragments surrounded by Cecropia-dominated regrowth and
assemblages similar to those in continuous forest (Wolfe
those encircled by Vismia-dominated regrowth (Nascimento
etal.,2015;Rochaetal.,2017).Forbats,matrixrecoveryhas
etal., 2006). In this way plant and animal communities in
resultedinmarkedcompositionalchangesinfragmentsand
fragments may increasingly tend to mirror the composition
shiftsintherankorderofthemostabundantspecies(Meyer
of the surrounding matrix (Laurance etal., 2006a,b), a
etal., 2016; Rocha, 2016). Gleaning animal-eating bats,
phenomenon observed elsewhere in the tropics (Janzen,
which formerly occurred at low abundances in fragments
1983;Diamond,Bishop&Balen,1987;Laurance,1991).
(Sampaio,2000)andyoungregrowth(Bobrowiec&Gribel,
2010), have increased over the past 10–15years as the
(2) Factorsinfluencingthematrix
surrounding regrowth has expanded and matured (Meyer
etal., 2016; Rocha, 2016; Rocha etal., 2017). A number Land-use history is a key driver of secondary succession in
of other species, including certain forest spiders (Mestre & Amazonia, resulting in distinct trajectories of regeneration
BiologicalReviews(2017)000–000©2017CambridgePhilosophicalSociety