Species Loss in Fragments of Tropical Rain Forest: A Review of the

Journalof
AppliedEcology
1996,33,
200-209
ESSAY REVIEW
oftropicalrainforest:
Specieslossinfragments
a reviewoftheevidence
I.M. TURNER
Department
ofBotany,
NationalUniversity
ofSingapore,
Singapore
119260
Summary
1. A reviewof theliterature
showsthatin nearlyall casestropicalrainforestfragmentation
has led to a local loss of species.Isolatedfragments
in
suffer
reductions
speciesrichness
withtimeafterexcisionfromcontinuous
and smallfragments
forest,
oftenhave fewerspeciesrecordedforthe same effort
of observation
thanlarge
fragments
or areasofcontinuous
forest.
2. Birdshavebeenthemostfrequently
studiedtaxonomic
groupwithrespectto the
effects
oftropicalforest
fragmentation.
3. Themechanisms
offragmentation-related
extinction
includethedeleterious
effects
of humandisturbance
duringand afterdeforestation,
thereduction
of population
sizes,thereduction
ofimmigration
rates,forest
edgeeffects,
changesin community
structure
andtheimmigration
ofexoticspecies.
(second-andhigher-order
effects)
4. Therelative
ofthesemechanisms
obscure.
importance
remains
5. Animalsthatare large,sparselyor patchilydistributed,
or veryspecializedand
intolerant
of thevegetation
surrounding
fragments,
are particularly
proneto local
extinction.
6. The largenumberof indigenous
speciesthatare verysparselydistributed
and
intolerant
of conditions
outsidetheforestmakeevergreen
tropicalrainforestparto specieslossthrough
ticularly
susceptible
fragmentation.
toglobal
7. Muchmoreresearch
is neededto studywhatis probably
themajorthreat
biodiversity.
habitatfragmentation,
conservation
Key-words:biodiversity,
biology,extinction,
species richness.
JournalofAppliedEcology(1996)33,200-209
so littleis knownaboutthegeneticand community
oftropicalrainforest
in relationto habitat
diversity
is inevitably
the
fragmentation
thatspeciesrichness
Therecanbelittle
doubtthatthelowlandforests
ofthe
I havedeliberately
avoided
majorfocusofthereview.
wettropicsarethemostspecies-rich
ofall terrestrial
to survey
papers.Myaimsarefirst
purelytheoretical
ofbioecosystems.
Unfortunately,
thesemasterpieces
as to
tomakesomesuggestions
thefactsandsecondly
are undertheconlogicaldiversity
and complexity
whattheyimplyin termsofpossiblegeneralizations.
tinuingthreatof destruction
fromhumanactivity.
Tropicalforestclearanceand conversion
are root
causes of thecurrent
globalbiodiversity
crisis,yet
fragments
rainforest
Biodiversity
lossintropical
surprisingly
our scientific
understanding
of thelink
in thetropicsofteninvolvestheconbetween
deforestation
andspeciesextinctions Deforestation
tropical
to ones
forest
is verypoor(Simon1986;Heywood& Stuart1992; versionoflandscapeswithcontinuous
Smithet al. 1993; Heywood et al. 1994).
withremnant
forest
patchessetin a matrixof nonThis paperreviewsstudiesof theeffects
of frag- forestvegetation.This manipulationof tropical
on thebiologicaldiversity
oftropicalrain environments
forbiodiversity
at
mentation
has consequences
level.Facforest.
Whilstrecognizing
thatbiologicaldiversity
is
boththelandscapeandtheforest-fragment
atlevelsaboveandbelowthatofthespecies, torssuchas fragment
exhibited
size,degreeof isolationand
Introduction
? 1996 British
Ecological Society
200
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All use subject to JSTOR Terms and Conditions
201
L.M. Turner
timesinceexcisionfromthecontinuous
forestmay
directly
influence
thebiodiversity
ofa fragment
and
hence,in a complexmanner,
thebiodiversity
of the
collection
offragments
thatoccupiesthelandscape.
Studiesofbiologicaldiversity
infragments
oftropicalrainforest
arelistedinTable1.Initialimpressions
fromcollatingtheseincludethatof a strongbias
towardresearchon birdsand thelargenumberof
studiesto comeoutofoneparticular
project,
namely
theBiologicalDynamicsof ForestFragments
(for-
merly
Minimum
CriticalSizeofEcosystems)
Project,
basednearManausinAmazonianBrazil.Non-avian
taxahavereceived
little
attention;
plants,surprisingly,
and invertebrates,
particularly
at sitesotherthan
Manaus,haverarelybeenstudiedin thecontextof
tropicalforest
fragmentation.
Thisheavyrelianceon
one taxonomicgroup (birds) and one locality
(Manaus)forconclusions
abouttheinfluence
offragmentation
on the biodiversity
of tropicalforestis
unsatisfactory,
sinceitrequires
ofthelaracceptance
Table1. Summary
tableofstudies
on speciesrichness
infragmented
tropical
rainforest
Study
Locality
Taxonomic
group
Bierregaard
& Lovejoy
1989
Malcolm1988
Manaus,Brazil
Forestbirds
Manaus,Brazil
Smallmammals
Zimmerman
&
Bierregaard
1986
Powell& Powell1987,
Beckeretal. 1991
Klein1989
Manaus,Brazil
Forestfrogs
Manaus,Brazil
bees
Euglossine
Manaus,Brazil
Fonsecade Souza&
Brown1994
Willis1979
Manaus,Brazil
Dung& carrion
beetles
Termites
Sao Paulo,Brazil
Forestbirds
da Fonseca& Robinson Atlantic
forest,
Brazil
1990
Kattanetal. 1994
Smallmammals
SanAntonio,
Colombia Forestbirds
Leck1979
Rio Palenque,Ecuador Forestbirds
Willis1974;Karr1982a BarroColoradoIsland, Forestbirds
Panama
Leighetal. 1993
GatunLake,Panama
Trees
Las Cruces,CostaRica
Estradaetal. 1993a,b,
1994
Los Tuxtlas,Mexico
Askinsetal. 1992
StThomas& StJohn,
US Virgin
Islands
Brash1987
PuertoRico
Newmark
1989
Eastern
Usambara
Tanzania
Mountains,
Singapore
Vertebrates,
plants
Java
Forestfalcons
Thiollay& Meyburg
1988
Diamondetal. 1987
? 1996British
Pahl etal. 1988
EcologicalSociety, Laurance1990,1994
Journal
ofApplied
Ecology,
33,200-209
3 x 1 ha,3 x 10ha and
continuous
1x 100ha,3 x 10ha
isolated;
3x 10ha,3x 100ha
non-isolated
1 ha, 10ha and
continuous
1 ha, 10ha, 100ha,
forest
continuous
1 ha, 10ha and
continuous
1 ha, 10ha and
continuous
21 ha, < 250ha,
1400ha
2 x 60-80ha,3600ha
Fragments
totalling
700ha
87ha
1500ha
0-3 years
2 months-3
years
?
<2 years,8 years
2-6 years
Isolatedin 1980
> 100years
20 years
40-90years
?
60-70years
6 x < 1 ha islands,
70-80years
continuous
forest
7 at 3-30ha, 1 of
Butterflies
18-33years
227ha
of
Frugivorous
mammals35 fragments
5-35years
& birds,bats,
1-2000ha
mammals
non-flying
Winter-resident Twoislandscompared, > 100years
71 km2(38% forested)
birds
migratory
vs.50 km2(88%
forested)
Landbirds
8628km2,99 6%
> 100years
forest
primary
cleared, mostly
32-7% forest
cover
Forestbirds
0 1-30ha, 1520ha
50-100years
Daily& Ehrlich1995
Corlett1992,Turner
et
al. 1994
Landscape/fragmentTimesince
size(s)
fragmentation
620kM2,99-8%
100-150years
forest
primary
c. 5% forest
clearance,
cover
Severalcenturies
530,15000,25000,
36000& 50000ha
86 ha
50 years
birds
BogorBotanicGarden, Breeding
Indonesia
Australia Arboreal
2-> 28 years
Queensland,
marsupials 24-74 ha
Australia Arboreal
10
Queensland,
forest:
50-80years
marsupials, Continuous
smallmammals
of1-4-590ha
fragments
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202
Speciesloss inrain
forest
?) 1996British
Ecological Society,
ofApplied
Journal
Ecology,33, 200-209
gelyuntestedassumptionthatbirdsand Amazonian
all themajor taxa and
forestin Braziltrulyrepresent
communitiesof tropicalforest.In addition,withthe
excised
focusoftheManaus projectbeingon recently
forestpatches,fewstudiesare leftto provideinforthathave been isolatedfordecmationon fragments
ades or longer.
Severalstudieshave showndeclinesovertimein the
or
of residentforestbirdswithina fragment
diversity
group of fragments(Willis 1974, 1979; Leck 1979;
Diamond,Bishop& van Balen 1987;Kattan,AlvarezLopez & Giraldo 1994). Leck (1979) reporteda loss
of25 speciesofbirdfroma highlyisolated87-haforest
fragment
(at Rio Palenque in Ecuador) injust 5 years.
Nearlya thirdofthespecieshave beenlostin 80 years
froma fragmentedarea of montane forestat San
AntoniointheColombianAndes(Kattanetal. 1994).
BarroColorado Island,Panama,lost45 breedingbird
species in its firsthalf centuryas a protectedarea
(Willis 1974), though32 of thesewere specialistsof
secondaryforestand forestmarginthatweredisplaced
because of successionaldevelopmentof theforeston
theisland.Out of62 birdspeciesbreedingintheBogor
Botanical Garden (containingmany mature forest
trees,thoughhardlya properforest),Indonesia,during 1932-52, 20 had disappearedby 1980-85, four
wereclose to extinctionand fivemore had declined
at
noticeably(Diamond et al. 1987). Small fragments
Manaus showedbriefincreasesin forestbirddiversity
and densityafterisolation as displaced birds took
refugein remnantforestpatches,but thesemeasures
soon fellto levels below those recordedbeforeisolation (Lovejoy et al. 1986; Bierregaard& Lovejoy
1989).
of
Otherstudieshave contrastedforestfragments
different
sizes, oftenincludingdata gatheredfrom
extensiveforesttractsfor comparison.It is a fairly
contains
trivialresultto show thata small fragment
fewerspecies of a certaintaxon than a large one,
but manyof thesestudieshave shownthatdiversity
measuredwiththe same samplingeffortis lower in
smallfragments.
Fragmentsize variesverygreatlyin
these studies,being largelydependenton the taxonomic group in question. Tree communitycomless than 1ha
positionhas been studiedin fragments
in extent(Leigh et al. 1993), whereasforestraptor
in blocks of forestof
has been investigated
diversity
50
000
ha
&
up to
(Thiollay Meyburg1988),indicating
the veryelasticnatureof the conceptof forestfragment.
The studiesat Manaus have shownthatsmallfragments contain fewerspecies of understoreybirds
(Lovejoy et al. 1986),smallmammals(Malcolm 1988;
Bierregaardet al. 1992),primates(Bierregaardet al.
1992),frogs(Zimmerman& Bierregaard1986),dung
and carrion beetles (Klein 1989), euglossine bees
(Powell & Powell 1987; Becker, Moure & Peralta
1991)and termites
(Fonseca de Souza & Brown1994)
or areas in continuousforest.
than largerfragments
Similar resultshave been found in other tropical
thathave been isolocalities:generallyforfragments
latedforgreaterperiodsoftime(Willis1979;Thiollay
& Meyburg1988;Pahl, Winter& Heinsohn1988;da
Fonseca & Robinson1990;Laurance 1990;Newmark
1991;Estrada,Coates-Estrada& Meritt1993a, 1994;
Estradaetal. 1993b;Leighetal. 1993;Laurance 1994;
Daily & Ehrlich1995). For instance,2-9 understorey
in
bird species were captured during mist-netting
lessthan3 ha in area
seven50-100-year-old
fragments
in theEasternUsambaraMountains,Tanzania; while
26 species were caught over a similarperiod in a
nearby(Newmark1991).
520-hafragment
Thereare also somedata forspeciesloss associated
with deforestationon a larger spatial scale. Brash
(1987) reportedthattheloss of99 6% ofPuertoRico's
primaryforesthad beenassociatedwitha 12% loss of
land birdspecies.Singaporehas undergonea similar
a higher
(99 8%) and suffered
degreeof deforestation
levelof speciesloss (Corlett1992;Turneret al. 1994),
estimatesof whichinclude26% of thevascularplant
flora,28% of the residentavifaunaand 44% -ofthe
fish.In theUS VirginIslands St
speciesof freshwater
John,despitebeingsmallerthanSt Thomas,had more
migrantbirds(mostlywarblers)
speciesof wintering
and in greaterabundances(Askins,Ewert& Norton
1992).This is probablybecause St Johnstillhad 88%
forestcoveras opposed to 38% on St Thomas.
makesit difficult
to refute
Analysisof theliterature
leads to the
thehypothesisthatforestfragmentation
thoughfewstudiescan be
local loss of biodiversity,
said to have been entirelyrigorousin theirmethodology,particularlyregardingthe extentto which
observationswerereplicated.Furtherand betterstudies are to be encouraged.But it is also necessaryto
stepbeyondtreatingtropicalrainforestcommunities
fromtheperas merespeciestotals.It is imperative,
spectivesof both ecologistsand conservationbiolmechanismsof
ogists,to understandthe underlying
to
and identify
groups
speciesloss in forestfragments
thatare particularly
susceptibleto extinction.
Mechanismsofspeciesloss in forestfragments
oftenleads to
It has been shownthatfragmentation
the local extinctionof speciesbut we need to know
the mechanismof extinctionif we are to tryto stop
this,or to studythe process as a means of gaining
Severalpossibilities
structure.
insightintocommunity
are available, at least some of which are covered
below.
DEFORESTATION-RELATED
DISTURBANCE
because by chance
Some specieswillbe exterminated
their habitats within the landscape will all be
destroyed.Species distributionpatternsare usually
landscape and this
patchyin the tropicalrain-forest
increasesthelikelihoodofcertainspeciesbeingexter-
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203
I.M. Turner
minatedby fragmentation
(Diamond 1980; Fonseca
de Souza & Brown1994).
There is a tendencyto oversimplifythe fraglandmentationprocess by viewingthe fragmented
scape as a deforestedmatrixcontainingpatches of
undisturbedforest.Realityis much more complex.
Deforestationwill undoubtedlyaffectthe remnant
fragments:
treeswill be felled,watercourseswill be
altered,animals will be hunted,fireor smoke will
penetratethefragments.
These eventsare all likelyto
be deleteriousto biodiversity:
indeeddisturbedfragments at Los Tuxtlas, Mexico, had a significantly
mammalsthan undislower diversityof non-flying
turbedones (Estrada et al. 1994); but theeventsdefy
analysiswithinany simpleecologicalmodel of diversityloss.
RESTRICTION
OF POPULATION
SIZE
At present,a considerationof the demographicand
geneticeffectsof the restrictionof population size
throughthe fragmentation
of tropical forestmust
remainlargelytheoreticalsinceveryfewrelevantdata
will
have been published.In theory,a smallfragment
supporta smallerpopulationof a givenspeciesthan
a largerone. As a fragmentgets verysmall, popuwill
lationswillfallbelowviablelevelsand extinction
ensue. Tiny relictpatchesmay contain 'ecologically
extinct'populations of species doomed because of
theirsmallsize. Smallpopulationsmaybe moreliable
to fluctuationswhich will inevitablyinclude local
extinctions;and theywill also tend to sufferfrom
geneticdriftand inbreedingthatreducegeneticvariation, increasehomozygosity
and, in the long term,
reducefitness(Caughley1994;Mills & Smouse 1994).
However,Leung,Dickman & Moore (1993) did not
in populationsof
findanyreductionin heterozygosity
in smallfragments
therodentMelomyscervinipes
(2-5,
7 5 and 97 5 ha) ofrainforestin northern
Queensland,
isolated for more than 60 years by clearance for
pastures,comparedwitha populationfroma large
foresttract.However,an islandpopulationdid show
reduced heterozygosity,showing that migration
in the agriculturallandscape
betweenthe fragments
was occurringand thatit helpedto maintaingenetic
diversity.
PREVENTION
OR REDUCTION
OF
IMMIGRATION
? 1996 British
Ecological Society,
JournalofApplied
Ecology,33, 200-209
If thedeforested
matrixis inhospitableto forestspecofindividuals
ies therewillbe littleor no immigration
to colonize fragmentsafterisolation. Studies have
shown that many forestspecies will not cross even
smalldeforested
zones (Dale etal. 1994):for
relatively
example,forestbeetleswere markedlyaffectedby a
100-in-wide
breakin treecover(Klein 1989),as were
forestbirds (Bierregaardet al. 1992). Isolation distancehas been shownto influence
thespeciesrichness
of tropical forestfragments(Estrada et al. 1993a;
Laurance 1994).The failureofmanyanimalsto move
can also restrictthe immigration
betweenfragments
of plantspecieswhentheseanimalsincludeseed disif theyare
persers;gene flowwill also be restricted
pollinators.Certainanimal speciesmay be relatively
nomadic, or migrateseasonally throughthe forest
(Loiselle & Blake 1992). If theyavoid crossingopen
habitats
areas,theyare unlikelyto utilizefragmented
so the conservationvalue of isolated forestpatches
willdiminish.
The natureof thematrixmay play a major role in
themovementbetweenforestfragments.
determining
The possibilitiesrangefromopen water(causinghilltops to become islands because of the floodingof
valleysafterdam construction)to secondaryforest
or tree-cropplantations.Few forestanimalsmay be
willingor able to cross the former,but many may
utilizethe latter.There are reportsthat some small
patches of rain forestin Malaysia contain a surprisinglyhigh diversityof wildlife,includinglarge
mammals, apparently because they receive little
humandisturbanceand are surroundedby extensive
treeplantations(Bennet& Caldecott1981;Duff,Hall
thatswathes
& Marsh 1984).Thisraisesthepossibility
forest
or
trees
of secondary
mightformvaluplanted
able corridorsto increasethe connectednessof priand maintainhigherrates of immimaryfragments
gration to them. With regard to tropical wildlife,
comesfromstudevidencein favourofthishypothesis
ies on mammals(Laurance 1990; Leung et al. 1993;
Estrada et al. 1994) and butterflies
(Daily & Ehrlich
1995) and by implicationfromthe paucityof mammalianrain-forest
specialistsin theunconnectedfragmentsofmonsoonforestinNorthernAustralia(Bowman & Woinarski1994).
Immigrationis probably an importantphenomenonforthemaintenanceofhighlocal levelsofdiverhave
sityin tropicalforests.Studiesof treediversity
shownthat a substantialportionof the speciesin a
tropicalrain forestplot are rare, i.e. sparselyrepresented(Hubbell & Foster 1983; Gentry1988), as
indeedtheymustbe whereso manyspeciesare packed
in. The fewlong-termstudiesof tropicaltreepopulationsshowthatthereis turnoverin thecomposition
ina givenarea offorest
oftherarespeciescomplement
(Hubbell & Foster 1983;Primack& Hall 1992). Rare
tree species oftenexhibithigherturnoverrates per
individualin theirpopulationsthan common ones,
at least in Sarawak (Primack& Hall 1992). Thus a
in a plot is supconsiderablefractionof thediversity
populationsofraretrees(Hubpliedbytinytransient
bell & Foster 1986). In isolated fragmentsthe rare
species will die out relativelyrapidly and not be
replacedbyotherspeciesbecauseofa failureofimmigration.
EDGE
EFFECTS
The edges of forestfragmentsare the boundaries
and are thustransition
betweenforestand non-forest
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204
Speciesloss in rain
forest
? 1996British
Ecological Society,
JournalofApplied
Ecology,33, 200-209
zones betweenthe two. The relativeimportanceof
edges increasesas fragment
size decreases,and edge
effects
may becomehighlyinfluential.
Such phenomena havebeenreviewedrecently
byMurcia(1995). For
instance,forestmicroclimate
is strongly
influenced
by
distanceto theperiphery
of a fragment.
These effects
appear to be propertiesof theedge and not restricted
to fragments.
Roads passingthroughforestproduce
similareffects,
as maylargegaps in theforestcanopy.
The talland relatively
continuousevergreen
canopy
of therainforestshadestheforestinteriorproducing
a comparatively
dark,cool and humidmicroclimate
(Fetcher,Oberbauer& Strain1985).Thus,a fragment
edge will produce a gradient in microclimatic
conditions,though not necessarilya simple one
(Malcolm 1994; Murcia 1995). Increases in photosynthetically active radiation (Williams-Linera
1990; MacDougall & Kellman 1992) and air temperature,and decreases in relativehumidity,have
been recordedwhen forestedges are comparedwith
interiors(Kapos 1989; Brown 1993). Such effectson
the microclimatehave been shown to extendup to
40 m inwardsfromthe forestboundaryin fragments
at Manaus (Kapos 1989). Othershave reportedless
dramaticeffects(7-12 m, MacDougall & Kellman
1992; 15-25m, Williams-Linera1990), ameliorated
over timeas the new edge of a forestdevelops.Repetitionof measurements
after4 yearsat the Manaus
site showed a less markedand more complex edge
influenceon microclimate
(Camargo & Kapos 1995).
At a largerspatialscale, remotesensinghas revealed
thatthe edges of forestblocks have averagecanopy
temperatures
up to 2 C0 warmerthan centralareas
(Nichol 1994).
Edge phenomenain thephysicalenvironment
may
have directeffectson the forestcommunity,
though
thesearemuchlesswelldocumented.
The alteredmicroclimatemay be unsuitableforcertainspecies,effectivelyreducingthe fragmentsize furtherfor some
forestanimals, increasingmortalityrates of forest
to their
plantsneartheedgeand reducingrecruitment
populations.Changes in foreststructurenear edges
have been found.These includea greatertreedensity
(Williams-Linera1990, 1993), an increased understoreyand reducedoverstorey
densityoffoliage(Malcolm 1994),a greatermortalityand rate of resulting
disturbance(Lovejoy et al. 1986; Laurance 1991a;
Leighetal. 1993),and a higherdensityofdisturbanceassociatedspecies(Laurance 1991a), thoughthelatter
was not foundbyWilliams-Linera
(1990). Newlycreated edgesexposetreesunusedto strongwindsto the
turbulent
atmosphereoutsidetheforest,thusincreasing mortalityfromwindthrow(Lovejoy et al. 1986).
Thisprocessmayerodethefragment,
reducingfurther
itseffective
size.
An edge-relatedphenomenonthat has received
much attentionin the temperatezone is increased
predationat birds' nests. Fewer studieshave been
conductedin the tropics.Burkey(1993) has shown
thatthe chance of bait chickeneggs beingfoundby
higherat rainforest
egg-eating
animalsis significantly
edges thaninteriorsin Belize and Mexico. However,
Gibbs (1991) foundthat,whileboundariesbetween
primaryand secondaryforestin Costa Rica showed
thisedge effect,
of primaryforestmeettheperiphery
fromthe
ing open pasturedid not differ
significantly
forestinteriorin ratesofeggattack.Nest predationis
probably higherin fragmentscompared with continuousforest(Loiselle& Hoppes 1983;Sieving1992).
This maybe due to thepresenceofnestpredatorsthat
are eitheredge specialistsor avoiders of the forest
interior.
Brash(1987) reportedthatthenest-predatory
birdMegaropsfuscatus
and a warbleflychick-parasite
were found at greaterabundancesin smallerforest
on PuertoRico. Loss fromnestsmay be a
fragments
to bird populations
major influenceon recruitment
and mightbe paralleledby predationon adult birds
and otherforestvertebrates.
In conclusion,fragment
edgesmaybe inhospitable
to some, and possiblya majorityof, forestspecies
reductionin fragment
size,and
leadingto an effective
making fragmentshape (via peripheryto area
of fragment
relationships)an importantdeterminant
quality. However, edges may not be universally
adverseto forestorganisms.The choice of breeding
pool by fivespeciesof forestfrogin Brazil appeared
unaffected
by forestedges(Gascon 1993) and several
speciesofsmallmammalincreasedin abundancenear
themarginsof forestfragments
in Queensland(Laurance 1994), possibly because these rodents found
superiorforagingin thedense,tangledgrowthat the
forestfringe.The hemiepiphyte
Oreopanaxcapitatus
to edge zones in thelower
(Araliaceae) was restricted
montaneforestof Mexico (Williams-Linera1992).
HIGHER-ORDER
EFFECTS
If certainanimalor plantgroupsare moresusceptible
to local extinction
thanothers,
throughfragmentation
withinthefragment
a changein community
structure
lead to further
is highlylikely,whichmay ultimately
changesand moreextinctions,
producingsecond-and
A good exampleinvolvestheloss
effects.
higher-order
of army ants from neotropical forest fragments
(Lovejoy et al. 1986). The ant coloniesrequirelarge
areas (> 30 ha) offorestto supplysufficient
food.The
of
the
from
smaller
is
ants
fragments
disappearance
with
loss
of
a
small
and
the
associated
specialrapid
ized group of insectivorousbirds that followarmy
ant colonies feedingon insects disturbedby the
swarmingants(Willis1974,1979;Lovejoyetal. 1986).
Despite thisexample,relativelylittleresearchhas
beenconductedon higher-order
but a number
effects,
of anecdotal cases point to fragmentation-related
changes in communitystructureas being of great
importanceand interest(Terborgh 1992). Habitat
fragmentation
is likelyto affectmost severelythose
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205
L.M. Turner
? 1996 British
Ecological Society,
ofApplied
Journal
Ecology,33, 200-209
animalswithrequirements
forverylargeareas of
IMMIGRATION OF EXOTICS
undisturbed
forest.
Largecarnivores
areparticularly
landscapeis
matrixof a fragmented
The deforested
susceptible
to local extermination
through
thefragbyalienspecies,becausefewofthe
oftendominated
mentation
oftropicalforest,
and aregenerally
under
exposed
of theextremely
nativespeciesare tolerant
fromotherhumanactivistrongadditionalpressure
intheclearedareas.Theremaybe a tendconditions
ties.Theabsenceofmegapredators
is liableto release
encyfortheseexoticsto starttoinvadethefragments.
control
onvertebrate
herbivore
andmediumtosmalltoinvasion
forest
areasarelessvulnerable
Continuous
sizedcarnivore
(mesopredator)
populations,
though
conditionsmay not favour
becauseenvironmental
areunlikely
largerspeciesoftheformer
tobe allowed
willbe
ofthealiens;muchoftheforest
establishment
to increasegreatly
becausetheyare frequently
also
outsidetherangeof dispersalof thosespecies;and
A scarcity
of predators
thepreyof humanhunters.
to the
maybe resistant
theundisturbed
community
a
in
mayleadto reduction
ofdiversity thepreyfauna
establishment
of exoticspecies.The considerably
as one or a fewspeciescometo dominateand outof oceanicislandcommunities,
susceptibility
greater
competetherest.This suggestion
mayexplainthe
to disruption
by
comparedwiththoseofcontinents,
of smallmammalsin 60-80-haforest
low diversity
&
Mueller-Dombois
1989)
indiexoticspecies(Loope
fragments
in theAtlanticcoastforests
of Brazil(da
resistindeedhavean inherent
catesthatcommunities
Fonseca& Robinson1990)and a morestructured
ance to invasion.Whitmore
(1991),in a reviewof
lessrandomly
(apparently
assembled)
smallmammal
citedthe
invasive
woodyplantsin thehumidtropics,
in
in
community smallfragments Queensland
(Laurin montaneforestin
case of Pittosporum
undulatum
ance1994).Mesopredator
release,namelytheexpanforest
Jamaicaas the sole exampleof undisturbed
sionofmesopredator
populations
afterreduction
or
smallfragments
invaded.However,
beingsuccessfully
ofmegapredator
removal
control,
hasbeenimplicated
are withindispersalrange(Willson& Crome1989)
inincreased
intropical
nestpredation
forest
fragments
mayoverwhelm
and thestrong
tideofalieninvaders
(Loiselle& Hoppes 1983;Sieving1992; Laurance,
1992).
thenativecommunity
(Janzen1983;Simberloff
Garesche& Payne1993).
of disturbance
in and around
The greater
frequency
Verysmallfragments
maylose mostof theirvermayalso favourtheirinvasion(Laurance
fragments
tebratefaunaand thiscan affectthefloristic
com1991a).
oftheforest.
position
Leighetal. (1993)hypothesized
thatthetinyislandsin Lake Gatun,Panama,had
becomedominatedby a handfulof large-seeded,
Extinctionproneness
in theabsence
wind-throw-resistant
treesthatthrive
to rapidextinction
ofmammalian
Forthesesameislands, Somespeciesaremoresusceptible
seed-predators.
oftropical
than
inreproductive through
thefragmentation
rainforest
Adler(1994)foundstrong
asynchrony
of
mamtheproneness
of thefru- others.In tropicalAustralia,
betweenfragmented
activity
populations
relatedto
This he
malsto extinction
givorousrodentProechimys
semispinosus.
appearsto be inversely
in theprevailing
matrix
towardsconditions
ascribedto floristic
differences
betweentheislands tolerance
ofresource vegetation
of the fragmented
landscape(Laurance
thathadledtodiffering
temporal
patterns
fruand
1990,1991b).AtLos Tuxtlas,Mexico,vertebrate
availability.
Asynchrony
mightreducemigration
low mobility
In largerforest
geneflowbetween
populations.
frag- givoreswithlow populationdensities,
to
inabundance
and
habitatswerethemostsusceptible
mentssmallmammals
and specialized
mayincrease
terwith
et
seed and seedlingpredators,
(Estrada al. 1993b),
act as efficient
greatly habitatfragmentation
a greaterlikelihoodof
mammalsexhibiting
treeregeneration
restrial
influencing
(Laurance1994).
thanvolantspeciesor birds.Fragas an eco- local extinction
Tropicalrainforestis oftenidentified
mammals
has ledto thelossofthelargest
onmutualistic
witha heavydependence
system
species mentation
foritsstability.
interactions
Manyplantspeciesinthe at Los Tuxtlas(Estradaetal. 1994).In a studyofthe
arereliant
onanimalsas agentsofdispersal mammalfaunasof islandsof theSunda Shelfthat
rainforest
foreitherpollenor seedsor both.If habitatfrag- wouldhavebeenlinkedbylandtotheAsiancontinent
ofcertainimportant duringthePleistocene,
causestheextinction
mentation
Heaney(1984) showedthat
orseed-dispersing
by a sharp
pollinating
animals,thiscouldsev- the smallestislandswerecharacterized
of theseplantspeciesand
in thenumberof largecarnivore
reduction
species.
erelylimitregeneration
islandsmaynotbedirectly
vortex(Howe 1984;Bond Theseso calledland-bridge
henceinitiate
an extinction
buttheresults
illustrate
1994).However,evidenceto supportthisprocessin
fragments,
analogoustoforest
tropicalrainforest
is limited
(Bond1994;Bowman&
thegenerally
acceptedpremisethatonlyverylarge
oftoppredpopulations
canmaintain
areasofforest
Woinarski
1994).Mostplantspeciesappearnottobe
so specialized
in eithertheirpollinators
or dispersers ators.
bymajorecoavifaunasclassified
as to be affected
rapidlyby fragmentation-related For neotropical
in fragmented
forestsare
extinction,
thoughreproductively
unsuccessful
popu- logicalguild,extinctions
to distinguish
lationsof treesmaypersistforcenturies
becauseof
in Table 2. It is difficult
summarized
thelongevity
oftheirmembers.
anycleartrendfromthedata. Thismaybe because
This content downloaded on Fri, 8 Mar 2013 14:23:34 PM
All use subject to JSTOR Terms and Conditions
206
Species loss in rain
forest
Table2. Avifaunal
extinctions
as a percentage
oftheirguild
rainforest
forfiveneotropical
sites.Data fromBrash(1987)
and Kattan et al. (1994)
Guild
? 1996British
EcologicalSociety,
JournalofApplied
Ecology,33, 200-209
Site
Raptors InsectivoresFrugivores
Brazil
Panama
Ecuador
Colombia
PuertoRico
54
22
56
33
14
74
22
18
31
7
57
16
33
36
22
speciescompared
indioeciousandmammal-dispersed
becausethepoorperforest,
possibly
withcontinuous
and the
of theformer
sistencein smallpopulations
ofthelatterdisadvantage
thesetwo
limited
dispersal
functional
groupsofplants.
Conclusions
forus to conEnoughstudieshavebeenconducted
of tropicalrain
cludesafelythatthefragmentation
though
forest
is a majorthreatto local biodiversity,
from
greater
human
theincreased
pressure
onwildlife
in fragmented
landscapesmaymakea major
activity
thestudiescoverforests
overa widerangeofspatial
to thenegativeimpact.Variousmechcontribution
scale.A number
ofauthorshaveemphasized
a heavy
ofspecanismsareresponsible
forthelocalextinction
lossamongraptorsand largefrugivores
(Leck 1979;
ies in fragmented
forest
but,as yet,itis notpossible
Willis 1979; Brash 1987; Kattan et al. 1994). Brash
ofdifferent
factors
toquantify
therelative
importance
(1987) pointsout thatthismaybe a phenomenon
such as restriction
of populationsize, forestedge
exacerbated
bydirecthumanpressure
on thesespeceffects
orinvasionofexoticspecies.Rareandpatchily
ies.Largefrugivores
generally
require
extensive
forest
fora
distributed
species,andthosewithrequirements
in orderto havesufficient
fruit
to sustaintheirpopulargerangeor specialisthabitatsseemparticularly
lations.Fragmentation
oftenleads to local domito fragmentation.
Toleranceofthematrix
susceptible
nationbysmallergeneralist
frugivores
thataremore
associated
conditionsis a characteristic
frequently
tolerant
ofthematrixvegetation
and able to switch
infragmented
forest.
withspeciesthatcan survive
in thealtered
dietsopportunistically,
thusflourishing
a mistake
to assumethatall tropical
It is probably
landscape(Willis1979). In theirliterature
review,
similar
rainforest
willreactinanexactly
communities
Johns& Skorupa(1987) also identified
largefruand resiliIn theirresistance
wayto fragmentation.
givoresas theecologicalgroupofprimates
thatwas
enceto fragmentation,
forests
maydiffer
significantly
mostsensitive
to forestdisturbance.
However,in a
or over much smallerspatial
betweencontinents
studyof neotropical
land-bridge
islandsGotelli&
provideinteresting
scales.PuertoRicoandSingapore
Graves(1990) could findno evidencefor greater
inthisrespect.
Bothislandshavesuffered
comparisons
extinction
birdspecproneness
amonglarger-bodied
from
a similar
massivelossofprimary
forest,
mostly
ies. Successful
colonizersof suchislandstendto be
but Singapore's
centurydeforestation,
nineteenth
on continents
speciesthatare widespread
(Faaborg
has beenmoreseriously
reduced.Of the
thatnarrowly
endemic
1979),possibly
indicating
spec- biodiversity
has
a
two
Puerto
Rico
considerably
greater
islands,
iesmaybe particularly
to fragmentationsusceptible
have
forests
which
cover
from
extensive
secondary
relatedextinction.
This appearsto be thecase for
native
woody
species
(Lugo
been
colonized
by
many
inCostaRica(Thomas1991).Kattenetal.
butterflies
thatbirdspeciesat theedgesoftheir 1988).Singaporealso has largeareas of secondary
(1994)reported
forest
oftencontaining
yet
fragments,
primary
werepar- forest,
geographical
rangeor ecologicaltolerance
forests
relatively
species-poor
remain
its
secondary
to habitatfragmentation.
sensitive
ticularly
However,
ofsuccession
(Turneret al.
varia- aftermorethana century
Karr(1982b)foundforforest
birdsthatstrong
thatthePuertoRicanforestcombilityin populationsizewas a moreimportant
pre- 1994),indicating
thantheSingaporean
be
more
resilient
munity
may
thanwasrarity.
dictorofextinction
probability
for
this
includethegreater
one.
might
Explanations
Turneret al. (1994) identified
epiphyticorchidsas
on
size
of
the
absolute
largerislandof
fragments
to forestfraghavingbeenparticularly
susceptible
in fava
selection
Puerto
Rico
and
pressure
stronger
inSingapore.
mentation
Thereasonsfortheirextincon
our
of
to
bear
brought
tolerance,
fragmentation
tionproneness
area matter
forspeculation.
Changes
thePuertoRicanbiotathrough
greater
geographical
in forest
microclimate
withfragmentation
maybe to
havebeenmuch isolation,a moreseasonalclimateand the greater
blame,butepiphytic
pteridophytes
ofcatastrophic
windsintheCaribbean
hurtolocalextinction
lesssusceptible
(Turner
etal. 1994). likelihood
ricane
belt.
Meave & Kellman(1994) notedthatnaturalfragOnlyextensive
tractsof forestcan containa full
ofriparian
inBelizeappeardepauperate
ments*
forest
biotaofa regionand
oftheindigenous
*Natural
fragments
arethose
patches
offorest
surrounded complement
for
fromdisruption
guarantees
of security
bynon-forest
vegetation
where
recent
human
activity
was therefore
nottheprimary
agency
responsible
fortheir
formation
and such tractsmustbe the firstpriorityof conseris notresponsible
fortheir
maintenance
as fragments.
A
if
fragmentation
vationists.
It is imperative
toprevent
universally
tenable
andsuccint
definition
ofnatural
fragment
tropical
I
would
argue
that
evergreen
at
all
possible.
maynotbepossible,
butthey
clearly
differ
from
thefragsensitiveto fragmentation
ments
thatarethefocusofthisreview,
which
werecreated forestsare particularly
inhistorically
recent
times
bypeople
clearing
forest.
becausea largeportionoftheirspeciesarebothvery
This content downloaded on Fri, 8 Mar 2013 14:23:34 PM
All use subject to JSTOR Terms and Conditions
207
I.M. Turner
sparselydistributed
throughthecommunity
and also
intolerantofopen sites.Thus,boththeabsolutenumber of species and the proportionof the complete
biota under threatfromfragmentation
are greater
thanforany otherbiome.Nowhereelse is theresuch
a sharp distinctionbetweenhighlydiverseprimary
forestand thespecies-poorearlysuccessionalmatrix.
This however,does not mean that already fragmentedtropicalforestsshouldbe ignoredor neglected
(Turneret al. 1994). Many foresttypesin thehumid
tropicsnow occur onlyas fragmented
remnants:e.g.
the Atlanticrain forestof Brazil, and the tropical
dryforestsofCentralAmericaand Indo-China.Even
small fragmentscontinueto possess relativelyhigh
levelsof diversity
manyyearsafterexcision(Turner
et al. 1994). Certainspecies may be able to survive
indefinitely
in fragmented
landscapes. For example,
Robbinset al. (1987, 1992) foundthatmanymigrant
birds made good use of fragmentedforestsin the
& Bierregaard(1995) discovered
Neotropics;Stouffer
in starkcontrastto
thatunderstorey
hummingbirds,
insectivorousspecies,persistin diversityand abundance in small fragments
at Manaus; and Ferrari&
Diego (1995) reportedthattwo threatenedspeciesof
and Alouattafusca,were
primate,Callithrixflaviceps
survivingin many small fragmentsof the Atlantic
coast forestsof Brazil.Even singleremnanttreesmay
conserve,at least in the shortterm,some epiphytic
orchidspecies(Williams-Linera,
Sosa & Platas 1995).
Meave & Kellman (1994) argued that, because
naturalfragments
of tropicalrainforestpossesshigh
forestfragmentation
neednot
levelsofplantdiversity,
This viewmaybe
necessarilylead to mass extinction.
thesenaturalforestpatchesmayhave
overoptimistic:
speciesnumberssimilarto those of equivalentareas
in continuousforestin thatregion,but theydo not
ofthecorerainforest
approachtheveryhighdiversity
blocks. Undoubtedlythe natural fragmentassemblages were derivedover a long period of timeand
fromdamaginghumaninterference.
have notsuffered
Man-made fragmentsof rain forest are literally
created 'overnight'and will contain a community,
elements of which have over many generations
tolreceivedlittleselectionpressureforfragmentation
erance.
Wheredo we go fromhere?
?) 1996British
EcologicalSociety,
JournalofApplied
Ecology,33, 200-209
We know so littleabout this enormousand urgent
problemthat more researchundoubtedlyhas to be
done. I would emphasizefurther
workon forestfragmentsthathave been isolatedfora considerableperiod oftime.It is information
on thelongtermviability
offragments,
and on thenatureofthenewequilibrium
pointthattheywillreachthatwillbe ofgreatestvalue
in planning conservationstrategies.Research prioritiesmustincludestudiesto identify
those groups
which,in the long term,are mostaffected
by habitat
fragmentation,
and researchinto the dynamicsand
geneticdiversityof small populations.Probablythe
most interestingarea of researchwill be into the
second- and higher-order
effectsof fragmentation.
These willpresenta greatchallengeto ecologistsbut
areofhighpotentialforpureas wellas appliedscience.
One approach to understandingthe diversityand
communitystructureof tropical forestmight be
throughthe natural deconstructionexperimentsof
willinclude
habitatfragmentation.
Major difficulties
findingthe right controls for such observations,
of factorsinvolved,and
unravellingthe multiplicity
the inevitablestochasticity
or even chaos of natural
of corridorsand buffer
systems.The effectiveness
of fragzones in amelioratingthe negative-impacts
mentationalso needs criticalattention.The ultimate
rainforspecies-rich
challengewillbe to resynthesize
estfromitstatteredremnants.Emphasison fieldstudgreatly
ies is important.This area of researchsuffers
bothfromtheemotionalhyperboleoftheill-informed
of theoreticians
and fromthe academic hypertrophy
and modellers.
Finally,it is salutaryto reflectupon how muchof
theecologicalresearch~Vhichhas providedthefoundationsforourtheoriesconcerning
tropicalrainforest
communitieswas actually conducted in fragments
suchas BarroColorado Island,Panama.
Acknowledgements
I am verygrateful
to RichardCorlett,TimWhitmore,
Kang Nee, PeterGrubb and Bill Laurance fortheir
commentson earlierdraftsofthispaper.
constructive
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