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Species Loss in Fragments of Tropical Rain Forest: A Review of the Evidence Author(s): I. M.

Turner Source: Journal of Applied Ecology, Vol. 33, No. 2 (Apr., 1996), pp. 200-209 Published by: British Ecological Society Stable URL: Accessed: 04/10/2010 05:37
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Journal of AppliedEcology 1996,33,



of Specieslossinfragments tropical forest: rain a review theevidence of

Department Botany, of National UniversitySingapore, of Singapore 119260

Summary 1. A review theliterature of showsthatin nearly casestropical forest all rain fragmentation led to a local loss of species. has in Isolatedfragments suffer reductions species richness time with after excision from and continuous forest, small fragments often have fewer speciesrecorded the same effort observation for of thanlarge fragments areasofcontinuous or forest. 2. Birds havebeenthemostfrequently studied taxonomic with group respect the to effects tropical of forest fragmentation. 3. Themechanisms fragmentation-related of extinction include deleterious the effects of human disturbance and during after deforestation, reduction population the of in sizes,thereduction immigration forest of rates, edgeeffects, changes community structure and and of (second- higher-order effects) theimmigrationexotic species. 4. Therelative of obscure. importance these mechanisms remains 5. Animals thatare large, sparsely patchily or or distributed, very specialized and intolerant thevegetation of surrounding fragments, particularly are proneto local extinction. 6. The largenumber indigenous of speciesthatare verysparsely distributed and intolerant conditions of outside forest the makeevergreen tropical rainforest parto loss ticularly susceptible species through fragmentation. to 7. Muchmore research needed study is to what probably major the threat global is biodiversity. habitatfragmentation, conservation Key-words: biodiversity, biology, extinction,
species richness.

Journal AppliedEcology(1996)33,200-209 of

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is and aboutthegenetic community so little known of rain in to diversity tropical forest relation habitat is the richness inevitably fragmentation species that There belittle can doubt the that lowland forests the of I avoided major focus thereview.havedeliberately of wettropics themostspecies-rich all terrestrial are of to papers. aimsarefirst survey My purely theoretical of ecosystems. Unfortunately, masterpiecesbiothese as to somesuggestions to thefacts secondly make and are logicaldiversity complexity undertheconand in of generalizations. whatthey imply terms possible tinuing threat destruction of from humanactivity. Tropicalforest clearance and conversion root are causes of thecurrent globalbiodiversity yet crisis, fragments rain Biodiversity intropical forest loss surprisingly scientific our understanding thelink of involves conthe in often between deforestation species and extinctions Deforestation thetropics tropical with to forest ones is very & of continuous poor(Simon1986;Heywood Stuart 1992; version landscapes of Smithet al. 1993; Heywood et al. 1994). with remnant forest patches in a matrix nonset This manipulation tropical This paperreviews studies theeffects frag- forestvegetation. of of of on of rain environments consequences biodiversity for at mentation thebiological diversity tropical has level. forest. Whilst that is both landscape theforest-fragment Facthe and recognizing biological diversity of and at exhibited levels aboveandbelow ofthe that species, torssuchas fragment degree isolation size, Introduction

201 L.M. Turner

timesinceexcision from continuous the forest may directly influence biodiversity a fragment the of and hence, a complex in manner, biodiversity the the of collection fragments occupies landscape. of that the Studies biological of in diversity fragmentstropof icalrain forest listed Table1.Initial are in impressions from collating theseinclude thatof a strong bias toward research birdsand thelargenumber on of studies comeoutofoneparticular to project, namely theBiological Dynamics ForestFragments of (for-

merly Minimum Critical ofEcosystems) Size Project, basednearManausinAmazonian Brazil. Non-avian taxahavereceived attention; little plants, surprisingly, and invertebrates, particularly sitesotherthan at beenstudied thecontext in Manaus,haverarely of tropical forest fragmentation. heavy This reliance on one taxonomicgroup (birds) and one locality (Manaus)for conclusions abouttheinfluence fragof mentation the biodiversity tropical on of forest is unsatisfactory, itrequires since of acceptance thelar-

Table1. Summary ofstudies species table on richness fragmented in tropical forest rain Study BierregaardLovejoy & 1989 Malcolm 1988 Locality Manaus, Brazil Manaus, Brazil Taxonomic group Forest birds Small mammals Landscape/fragmentTimesince size(s) fragmentation 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, ha 1400 2 x 60-80ha,3600ha Fragments totalling 700ha 87ha 1500 ha 0-3 years 2 months-3 years

Zimmerman & Bierregaard 1986 Powell Powell1987, & et Becker al. 1991 Klein1989 Fonseca Souza& de Brown 1994 Willis 1979

Manaus, Brazil Brazil Manaus, Manaus, Brazil Manaus, Brazil Sao Paulo,Brazil

Forest frogs bees Euglossine Dung& carrion beetles Termites Forest birds Small mammals

? <2 years, years 8 2-6 years Isolated 1980 in > 100years 20 years 40-90years ? 60-70years

da Fonseca Robinson Atlantic & forest, Brazil Kattan al. 1994 et

SanAntonio, Colombia Forest birds

Leck1979 Rio Palenque, Ecuador Forest birds Willis 1974; Karr1982a Barro Colorado Island, Forest birds Panama et Leigh al. 1993 Gatun Lake,Panama Trees Daily& Ehrlich 1995 Estrada al. 1993a,b, et 1994 Askins al. 1992 et Las Cruces, CostaRica Los Tuxtlas, Mexico StThomas StJohn, & US Virgin Islands Puerto Rico Eastern Usambara Tanzania Mountains, Singapore

Brash1987 Newmark 1989 Corlett Turner et 1992, al. 1994 & Thiollay Meyburg 1988 Diamondetal. 1987

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, 1-2000 ha bats, mammals non-flying Winter-resident Twoislands compared, > 100years 71 km2 birds migratory (38% forested) vs.50 km2(88% forested) Landbirds 8628km2, 6% > 100years 99 forest primary cleared, mostly 32-7% forest cover Forest birds 0 1-30ha, 1520 ha 50-100 years 620kM2,99-8% 100-150 years forest primary c. clearance, 5% forest cover Several centuries 530,15000, 25000, 36000& 50000ha 86 ha 50 years

Vertebrates, plants


Forest falcons

? 1996British Pahl etal. 1988 Ecological Society, Laurance 1994 1990, Journal Applied of Ecology, 200-209 33,

Botanic birds Bogor Garden, Breeding Indonesia Australia Arboreal 2-> 28 years Queensland, marsupials 24-74 ha Australia Arboreal 10 Queensland, forest: 50-80years marsupials, Continuous small mammals of ha fragments1-4-590

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thatbirdsand Amazonian gelyuntested assumption represent themajor taxa and all forest Braziltruly in of In communities tropicalforest. addition,withthe excised focusoftheManaus projectbeingon recently forest patches,fewstudiesare leftto provideinforthat mationon fragments have been isolatedfordecades or longer. overtimein the have showndeclines Severalstudies a or of forest birdswithin fragment diversity resident (Willis 1974, 1979; Leck 1979; group of fragments Diamond,Bishop& van Balen 1987;Kattan,Alvareza Lopez & Giraldo 1994). Leck (1979) reported loss a of25 speciesofbirdfrom highly isolated87-haforest fragment Rio Palenque in Ecuador) injust 5 years. (at Nearlya third thespecieshave beenlostin 80 years of froma fragmented area of montane forestat San AntoniointheColombianAndes(Kattanetal. 1994). bird BarroColorado Island,Panama,lost45 breeding half century a protectedarea as species in its first of (Willis 1974), though32 of thesewere specialists forest forest and thatweredisplaced margin secondary on of because of successional development theforest in theisland.Out of62 birdspeciesbreeding theBogor Botanical Garden (containingmany mature forest a Indonesia,durtrees, thoughhardly properforest), ing 1932-52, 20 had disappearedby 1980-85, four wereclose to extinction and fivemore had declined at noticeably (Diamond et al. 1987). Small fragments in increases forest birddiversity Manaus showedbrief and densityafterisolation as displaced birds took in forest patches,but thesemeasures refuge remnant soon fellto levels below those recordedbeforeiso& lation (Lovejoy et al. 1986; Bierregaard Lovejoy 1989). of forest Otherstudieshave contrasted fragments different sizes, oftenincludingdata gatheredfrom foresttractsfor comparison.It is a fairly extensive contains trivial resultto show thata small fragment fewerspecies of a certaintaxon than a large one, but manyof thesestudieshave shownthatdiversity is measuredwiththe same samplingeffort lower in in size variesverygreatly smallfragments. Fragment these studies,being largelydependenton the taxocomnomic group in question. Tree community less positionhas been studiedin fragments than 1ha in extent(Leigh et al. 1993), whereasforestraptor in of has diversity been investigated blocks of forest 50 000 ha (Thiollay& Meyburg 1988),indicating up to the veryelasticnatureof the conceptof forest fragment. The studiesat Manaus have shownthatsmallfragbirds ments contain fewerspecies of understorey al. 1986),smallmammals 1988; (Malcolm (Lovejoy et et et (Bierregaard al. Bierregaard al. 1992),primates & Bierregaard 1986),dung 1992),frogs (Zimmerman and carrion beetles (Klein 1989), euglossine bees (Powell & Powell 1987; Becker, Moure & Peralta 1991)and termites (Fonseca de Souza & Brown1994) or than largerfragments areas in continuousforest.

Similar resultshave been found in other tropical that for localities:generally fragments have been isoperiodsoftime(Willis1979;Thiollay latedforgreater & & Meyburg1988;Pahl, Winter Heinsohn1988;da Fonseca & Robinson1990;Laurance 1990;Newmark 1991;Estrada,Coates-Estrada& Meritt1993a, 1994; Estradaetal. 1993b;Leighetal. 1993;Laurance 1994; 2-9 Daily & Ehrlich1995). For instance, understorey in bird species were captured during mist-netting less seven50-100-year-old fragments than3 ha in area Tanzania; while in theEasternUsambaraMountains, 26 species were caught over a similarperiod in a nearby (Newmark1991). 520-hafragment Thereare also somedata forspeciesloss associated with deforestation a larger spatial scale. Brash on that (1987) reported theloss of99 6% ofPuertoRico's had primary forest beenassociatedwitha 12% loss of a land birdspecies.Singaporehas undergone similar a (99 degreeof deforestation 8%) and suffered higher et levelof speciesloss (Corlett1992;Turner al. 1994), of estimates whichinclude26% of thevascularplant avifaunaand 44% -ofthe flora,28% of the resident Islands St fish. speciesof freshwater In theUS Virgin thanSt Thomas,had more beingsmaller John, despite birds(mostly warblers) migrant speciesof wintering and in greater abundances(Askins,Ewert& Norton because St Johnstillhad 88% 1992).This is probably forest coveras opposed to 38% on St Thomas. makesit difficult refute to of Analysis theliterature leads to the thatforest thehypothesis fragmentation thoughfewstudiescan be local loss of biodiversity, rigorousin theirmethsaid to have been entirely the regarding extentto which odology,particularly studand observations werereplicated. Further better to ies are to be encouraged.But it is also necessary communities tropicalrainforest stepbeyondtreating from perthe as merespeciestotals.It is imperative, biolspectivesof both ecologistsand conservation of mechanisms the ogists,to understand underlying to identify and groups fragments speciesloss in forest to thatare particularly susceptible extinction.

of Mechanisms speciesloss in forest fragments

oftenleads to It has been shownthatfragmentation of the local extinction speciesbut we need to know if the mechanism extinction we are to tryto stop of or to studythe process as a means of gaining this, Severalpossibilities intocommunity structure. insight are available, at least some of which are covered below.

because by chance Some specieswillbe exterminated their habitats within the landscape will all be patternsare usually destroyed.Species distribution landscape and this patchyin the tropicalrain-forest speciesbeingexterincreases likelihood certain the of

203 I.M. Turner

minatedby fragmentation (Diamond 1980; Fonseca de Souza & Brown1994). the fragThere is a tendencyto oversimplify landmentation process by viewingthe fragmented patches of scape as a deforested matrixcontaining forest.Realityis much more complex. undisturbed the remnant Deforestation will undoubtedlyaffect will be fragments: treeswill be felled,watercourses altered,animals will be hunted,fireor smoke will to penetrate fragments. the These eventsare all likely be deleterious biodiversity: to indeeddisturbed fragments at Los Tuxtlas, Mexico, had a significantly mammalsthan undislower diversity non-flying of turbedones (Estrada et al. 1994); but theeventsdefy analysiswithin any simpleecologicalmodel of diversityloss.

At present, consideration the demographic a of and geneticeffects the restriction population size of of throughthe fragmentation tropical forestmust of remain sincevery relevant few data largely theoretical a will have been published. theory, smallfragment In supporta smallerpopulationof a givenspeciesthan a largerone. As a fragment gets verysmall, popuwill lationswillfallbelowviablelevelsand extinction ensue. Tiny relictpatchesmay contain 'ecologically extinct'populations of species doomed because of their smallsize. Smallpopulations maybe moreliable to fluctuations which will inevitablyinclude local from extinctions; and theywill also tend to suffer and inbreeding thatreducegenetic varidrift genetic ation, increasehomozygosity and, in the long term, reducefitness (Caughley1994;Mills & Smouse 1994). However,Leung,Dickman & Moore (1993) did not in in of find anyreduction heterozygosity populations in therodent (2-5, Melomys cervinipes smallfragments in 7 5 and 97 5 ha) ofrainforest northern Queensland, isolated for more than 60 years by clearance for pastures,comparedwitha populationfroma large forest tract.However,an islandpopulationdid show reduced heterozygosity, showing that migration in betweenthe fragments the agricultural landscape was occurring and thatit helpedto maintaingenetic diversity.

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If thedeforested is to matrix inhospitable forest specof ies there be little no immigration individuals will or afterisolation. Studies have to colonize fragments shown that many forestspecies will not cross even smalldeforested zones (Dale etal. 1994):for relatively beetleswere markedly affected a by example,forest 100-in-wide breakin treecover(Klein 1989),as were forest birds (Bierregaard al. 1992). Isolation diset tancehas been shownto influence speciesrichness the of tropical forestfragments (Estrada et al. 1993a;

of Laurance 1994).The failure manyanimalsto move the can betweenfragments also restrict immigration of plantspecieswhentheseanimalsincludeseed disif persers;gene flowwill also be restricted theyare Certainanimal speciesmay be relatively pollinators. nomadic, or migrateseasonally throughthe forest (Loiselle & Blake 1992). If theyavoid crossingopen habitats to areas,theyare unlikely utilizefragmented patches value of isolated forest so the conservation willdiminish. may play a major role in The natureof thematrix the between forest fragments. determining movement open water(causinghillThe possibilities rangefrom tops to become islands because of the floodingof to valleysafterdam construction) secondaryforest Few forest animalsmay be or tree-crop plantations. but willingor able to cross the former, many may utilizethe latter.There are reportsthat some small patches of rain forestin Malaysia contain a surof includinglarge high diversity wildlife, prisingly mammals, apparently because they receive little by and are surrounded extensive humandisturbance Hall treeplantations (Bennet& Caldecott1981;Duff, that & Marsh 1984).Thisraisesthepossibility swathes form valuforest plantedtreesmight or of secondary of able corridors increasethe connectedness prito and maryfragments maintainhigherrates of immigration to them. With regard to tropical wildlife, studin of comesfrom evidence favour thishypothesis ies on mammals(Laurance 1990; Leung et al. 1993; Estrada et al. 1994) and butterflies (Daily & Ehrlich fromthe paucityof mam1995) and by implication in malianrain-forest fragspecialists theunconnected in Australia of ments monsoonforest Northern (Bowman & Woinarski1994). is phenomImmigration probably an important of enonforthemaintenance highlocal levelsofdiverhave Studiesof treediversity sityin tropicalforests. shownthat a substantial portionof the speciesin a tropicalrain forestplot are rare, i.e. sparselyrepresented(Hubbell & Foster 1983; Gentry1988), as mustbe where manyspeciesare packed so indeedthey in. The fewlong-term studiesof tropicaltreepopuis in lationsshowthatthere turnover thecomposition in area offorest oftherarespeciescomplement a given (Hubbell & Foster 1983;Primack& Hall 1992). Rare rates per tree species oftenexhibithigherturnover individualin theirpopulationsthan common ones, at least in Sarawak (Primack& Hall 1992). Thus a in of fraction thediversity a plot is supconsiderable transient of populations raretrees(Hubpliedbytiny the bell & Foster 1986). In isolated fragments rare rapidly and not be species will die out relatively of speciesbecauseofa failure immireplacedbyother gration.

are The edges of forestfragments the boundaries and and between forest non-forest are thustransition

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zones betweenthe two. The relativeimportance of edges increasesas fragment decreases,and edge size effects may becomehighly influential. Such phenomena havebeenreviewed recently Murcia(1995). For by instance, forest microclimate strongly is influenced by distanceto theperiphery a fragment. of These effects of appear to be properties theedge and not restricted to fragments. Roads passingthrough forest produce similar as effects, maylargegaps in theforest canopy. The talland relatively continuous evergreen canopy of therainforest shadestheforest interior producing 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 temhave perature,and decreases in relativehumidity, been recordedwhen forest edges are comparedwith interiors on (Kapos 1989; Brown 1993). Such effects the microclimate have been shown to extendup to 40 m inwardsfrom forest the boundaryin fragments at Manaus (Kapos 1989). Othershave reported less dramaticeffects (7-12 m, MacDougall & Kellman 1992; 15-25m, Williams-Linera1990), ameliorated over timeas the new edge of a forest develops.Repetitionof measurements 4 after yearsat the Manaus site showed a less markedand more complex edge influence microclimate on (Camargo & Kapos 1995). At a largerspatialscale, remotesensing has revealed thatthe edges of forest blocks have averagecanopy temperatures to 2 C0 warmerthan centralareas up (Nichol 1994). in environment Edge phenomena thephysical may have directeffects the forest on community, though these much welldocumented. altered are less The microclimatemay be unsuitableforcertainspecies,effecsize further some for tivelyreducingthe fragment forestanimals, increasingmortality rates of forest to plantsneartheedgeand reducing recruitment their near edges populations.Changes in foreststructure have been found.These includea greater treedensity (Williams-Linera1990, 1993), an increased underand of storey reduced overstorey density foliage (Malcolm 1994),a greater and mortality rate of resulting disturbance (Lovejoy et al. 1986; Laurance 1991a; of Leighetal. 1993),and a higher density disturbanceassociatedspecies(Laurance 1991 though latter the a), was not foundbyWilliams-Linera (1990). Newlycreated edgesexposetreesunusedto strong windsto the turbulent outsidetheforest, thusincreasatmosphere from windthrow ing mortality (Lovejoy et al. 1986). Thisprocess erodethefragment, further may reducing itseffective size. An edge-related phenomenonthat has received much attention the temperate in zone is increased predationat birds' nests. Fewer studieshave been conductedin the tropics.Burkey(1993) has shown

thatthe chance of bait chickeneggs beingfoundby higher rainforest at egg-eating animalsis significantly in edges thaninteriors Belize and Mexico. However, Gibbs (1991) foundthat,whileboundariesbetween primary and secondary forest Costa Rica showed in thisedge effect, periphery primary of forest meetthe from ing open pasturedid not differ significantly the in is forest interior ratesofeggattack.Nest predation probably higherin fragments compared with continuous forest (Loiselle& Hoppes 1983;Sieving1992). This maybe due to thepresence nestpredators of that are eitheredge specialistsor avoiders of the forest interior. that Brash(1987) reported thenest-predatory birdMegaropsfuscatus a warblefly and chick-parasite were found at greaterabundancesin smallerforest on nestsmay be a fragments PuertoRico. Loss from to on major influence recruitment bird populations and mightbe paralleledby predationon adult birds and otherforest vertebrates. In conclusion, fragment edgesmaybe inhospitable to some, and possiblya majorityof, forestspecies in reduction fragment and size, leadingto an effective making fragmentshape (via peripheryto area of relationships) important an determinant fragment quality. However, edges may not be universally The choice of breeding adverseto forest organisms. pool by fivespeciesof forest frogin Brazil appeared unaffected forest by edges(Gascon 1993) and several in speciesofsmallmammalincreased abundancenear themargins forest in of fragments Queensland(Laurance 1994), possibly because these rodents found in at superior foraging thedense,tangledgrowth the The hemiepiphyte forest Oreopanaxcapitatus fringe. to (Araliaceae) was restricted edge zones in thelower of montaneforest Mexico (Williams-Linera 1992).



If certain animalor plantgroupsare moresusceptible to local extinction than through fragmentation others, within fragment the a changein community structure lead to further is highly whichmay ultimately likely, second-and changesand moreextinctions, producing A the effects. good exampleinvolves loss higher-order of army ants from neotropical forest fragments (Lovejoy et al. 1986). The ant coloniesrequirelarge areas (> 30 ha) offorest supplysufficient The to food. of the ants fromsmallerfragments is disappearance withtherapid loss of a smalland specialassociated ized group of insectivorous birds that followarmy ant colonies feedingon insects disturbedby the ants swarming (Willis1974,1979;Lovejoyetal. 1986). littleresearch has Despite thisexample,relatively beenconducted higher-order on but a number effects, of anecdotal cases point to fragmentation-related as changes in community structure being of great importanceand interest(Terborgh 1992). Habitat fragmentation likelyto affect is most severely those

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animalswithrequirements verylargeareas of for IMMIGRATION OF EXOTICS undisturbed forest. Largecarnivores particularly are landscape is of matrix a fragmented The deforested susceptible local extermination to through fragthe of becausefew the by often dominated alienspecies, mentation tropical of forest, aregenerally and under exposed of are native species tolerant theextremely from strong additional pressure other human activimaybe a tendareas.There in conditions thecleared ties. Theabsence megapredators of is liableto release to the for to exotics start invade fragments. ency these control vertebrate on herbivore medium- smalland to to forest areasarelessvulnerable invasion Continuous sizedcarnivore (mesopredator) populations, though conditions may not favour becauseenvironmental of are larger species theformer unlikely be allowed to will of much theforest be of establishmentthealiens; to increase greatly becausethey frequently are also and of outside rangeof dispersal thosespecies; the of A of theprey human hunters. scarcity predators to may theundisturbed community be resistant the in mayleadto a reduction diversity theprey of fauna establishment exoticspecies.The considerably of as one or a fewspecies and cometo dominate outof susceptibilityoceanicislandcommunities, greater the compete rest.This suggestion explainthe may to by with thoseofcontinents, disruption compared in of forest low diversity smallmammals 60-80-ha & Mueller-Dombois indi1989) exotic (Loope species fragments theAtlantic in coastforests Brazil(da of resistthat indeed havean inherent cates communities Fonseca& Robinson1990)and a morestructured of ance to invasion. Whitmore (1991),in a review less (apparently randomly assembled) small mammal in cited the invasive tropics, plants thehumid woody in in community smallfragments Queensland (Laurin in forest case of Pittosporum undulatum montane ance1994).Mesopredator the release, namely expanof forest Jamaica the sole example undisturbed as sionofmesopredator populations after reduction or small fragments invaded. However, successfully being of removal megapredator control, been has implicated within & Crome1989) are range(Willson dispersal inincreased predation tropical in nest forest fragments may and thestrong ofalieninvaders overwhelm tide (Loiselle& Hoppes 1983;Sieving1992; Laurance, 1992). the native 1983; Simberloff community (Janzen & Garesche Payne1993). of in The greater frequency disturbance and around Verysmallfragments lose mostof their may ver(Laurance their invasion may fragments also favour tebrate faunaand thiscan affect floristic the com1991a). of et position theforest. Leigh al. (1993)hypothesized thatthetiny islandsin Lake Gatun,Panama,had of becomedominated a handful large-seeded, by Extinction proneness in wind-throw-resistantthatthrive theabsence trees to extinction ofmammalian For are same seed-predators. these islands, Somespecies more susceptible rapid oftropical forest than in the rain Adler (1994)found strong asynchronyreproductive through fragmentation ofmamIn the of Australia, proneness between activity fragmented populations thefru- others. tropical to related to rodentProechimys This malsto extinction givorous semispinosus. he appears be inversely in matrix to the towards conditions theprevailing ascribed floristic differences between islands tolerance of of landscape(Laurance that ledtodiffering had temporal patterns resource vegetation the fragmented vertebrate fruand 1990, Mexico, availability. Asynchrony reduce might migration 1991b).AtLos Tuxtlas, low In forest withlow population densities, mobility between geneflow populations. larger frag- givores to were mostsusceptible the in and habitats ments small mammals increase abundance and specialized may terwith etal. 1993b), seed fragmentation (Estrada act as efficient and seedling predators, greatly habitat of a likelihood mammals tree restrial exhibiting greater influencing regeneration (Laurance 1994). or than rainforest often is identified an eco- local extinction volantspecies birds.Fragas Tropical mammals has on with system a heavy dependence mutualistic species mentation ledto thelossofthelargest et of for in interactions itsstability. Manyplant species the at Los Tuxtlas (Estrada al. 1994).In a study the as are on of faunasof islandsof theSunda Shelfthat rain forest reliant animals agents dispersal mammal Asian continent havebeen linked landtothe foreither by pollenor seedsor both.If habitat frag- would that showed of the causestheextinction certain mentation Heaney(1984) important during Pleistocene, or this islandswerecharacterized a sharp by pollinating seed-dispersing animals, couldsev- the smallest of limit of in reduction thenumber largecarnivore species. erely regeneration theseplantspeciesand Bond These called so islands notbedirectly vortex land-bridge may hence initiate extinction an (Howe 1984; in but results illustrate to this to evidence support process 1994).However, fragments, the analogous forest large tropical forest limited rain is (Bond1994; Bowman premise thatonlyvery & thegenerally accepted of populations toppredcan areasofforest maintain Woinarski 1994). Mostplant species appear tobe not so specialized either in their pollinators dispersers ators. or by avifaunas classified majorecoas to be affected rapidly fragmentation-related For neotropical by are in forests extinction, though reproductively unsuccessful popu- logicalguild,extinctions fragmented to lations trees of maypersist centuries for becauseof in summarized Table 2. It is difficult distinguish thelongevity their of members. from data. Thismaybe because the anycleartrend

206 Species loss in rain forest

Table2. Avifaunal extinctions a percentage their as of guild rain for neotropical forest Data from five sites. Brash (1987)
and Kattan et al. (1994)

Guild Site Brazil Panama Ecuador Colombia Puerto Rico Raptors Insectivores Frugivores 54 22 56 33 14 74 22 18 31 7 57 16 33 36 22

species indioecious mammal-dispersed compared and because poorperthe forest, possibly with continuous in and of sistence smallpopulations theformer the of these disadvantage two limited dispersal thelatter of functional groups plants.


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for havebeenconducted us to conEnoughstudies rain thatthefragmentationtropical of cludesafely to though forest a majorthreat local biodiversity, is from human the increased pressure wildlife greater on in may landscapes makea major activity fragmented thestudies cover forests a widerange spatial over of to impact. Variousmechcontribution thenegative scale.A number authors of haveemphasized heavy a of anisms responsible the are for localextinction speclossamong raptors largefrugivores and (Leck 1979; it ies in fragmented but,as yet, is notpossible forest Willis 1979; Brash 1987; Kattan et al. 1994). Brash of factors toquantify relative the importance different (1987) pointsout thatthismaybe a phenomenon edge size, forest such as restriction population of exacerbated direct by human pressure these on specof Rareandpatchily species. effects invasion exotic or ies.Largefrugivores generally require extensive forest for with requirements a and distributed species, those in order havesufficient to sustain to fruit their popuseemparticularly habitats largerangeor specialist lations.Fragmentation oftenleads to local domito Tolerance thematrix of susceptible fragmentation. nation smaller by generalist frugivores aremore that is associated conditions a characteristic frequently tolerant thematrix of vegetation able to switch and in forest. that with species can survive fragmented in diets thus opportunistically, flourishingthealtered a to that tropical all It is probably mistake assume landscape(Willis1979). In their literature review, similar rain forest in will communities react anexactly Johns Skorupa(1987) also identified & largefruand In resistance resiliwayto fragmentation.their as givores theecological groupofprimates was that enceto fragmentation, maydiffer forests significantly in mostsensitive forest to disturbance. However, a or continents over much smallerspatial between of study neotropical land-bridge islandsGotelli& RicoandSingapore provide interesting scales. Puerto for Graves(1990) could findno evidence greater in respect. islands Both have suffered comparisons this extinction bird proneness among larger-bodied specfrom a similar massive ofprimary loss forest, mostly ies. Successful colonizers suchislands of tendto be but century deforestation, Singapore's nineteenth thatare widespread continents on species (Faaborg has beenmoreseriously Of reduced. the that endemic 1979), possibly indicating narrowly spec- biodiversity twoislands, Puerto Rico has a considerably greater iesmaybe particularly to susceptible fragmentationhave forests which extensive secondary related extinction. appearsto be thecase for coverfrom This native woody species (Lugo beencolonized many by inCostaRica(Thomas1991). et butterflies Katten al. also has largeareas of secondary that at of (1994)reported birdspecies theedges their 1988).Singapore forest often yet fragments, containing primary forest, or tolerance were geographical range ecological parforests relatively species-poor remain its secondary to sensitive habitat ticularly fragmentation. However, et of than century succession a more (Turner al. that varia- after Karr(1982b) found forest for birds strong comthat Ricanforest in size bility population was a moreimportant pre- 1994),indicating thePuerto than munity be moreresilient theSingaporean may than of dictor extinction probability wasrarity. for the include greater one. Explanations thismight Turneret al. (1994) identified orchidsas epiphytic on islandof absolutesize of fragments the larger to having beenparticularly susceptible forest fragin selection Puerto Rico and a stronger pressure favin for mentation Singapore. reasons their The extincour of fragmentation to brought bearon tolerance, tionproneness a matter speculation. are for Changes Ricanbiotathrough thePuerto greater geographical in forest microclimate fragmentation be to with may a and the greater but have blame, epiphytic pteridophytes beenmuch isolation, moreseasonalclimate of winds hurCaribbean to lesssusceptible localextinction (Turner al. 1994). likelihood catastrophic inthe et ricane belt. Meave & Kellman(1994) notedthatnatural fragcan a Onlyextensive tracts forest contain full of of in ments* riparian forest Belize appear depauperate and biotaofa region of *Natural fragments are those patchesforest of surrounded complement theindigenous for from disruption guarantees security of bynon-forest vegetation recent where human activity was therefore not primary the agency responsibletheir for formation and such tractsmustbe the first priority conserof is notresponsible their for maintenance as fragments. vationists. is imperative prevent A if fragmentation It to universally and tenable succint definition of natural fragment tropical I that evergreen at all possible. wouldargue may bepossible, they not but clearly from fragdiffer the sensitive fragmentation to are ments arethe that focus this of review, were which created forests particularly inhistorically times people recent by clearing forest. of species bothvery are because large a portion their

207 I.M. Turner

sparsely distributed through community also the and intolerant open sites.Thus,boththeabsolutenumof ber of species and the proportionof the complete biota under threatfromfragmentation greater are thanforany otherbiome.Nowhereelse is theresuch a sharp distinction betweenhighlydiverseprimary forest and thespecies-poor earlysuccessional matrix. This however,does not mean that already fragmented tropical forests shouldbe ignored neglected or (Turneret al. 1994). Many forest typesin thehumid tropicsnow occur onlyas fragmented remnants: e.g. the Atlanticrain forestof Brazil, and the tropical of dryforests CentralAmericaand Indo-China.Even small fragments continueto possess relatively high levelsof diversity manyyearsafterexcision(Turner et al. 1994). Certainspecies may be able to survive indefinitely fragmented in landscapes. For example, Robbinset al. (1987, 1992) foundthatmanymigrant birds made good use of fragmented forestsin the & Neotropics;Stouffer Bierregaard (1995) discovered in to thatunderstorey hummingbirds, starkcontrast insectivorous species,persistin diversity and abundance in small fragments Manaus; and Ferrari& at thattwo threatened Diego (1995) reported speciesof and primate, were Callithrixflaviceps Alouattafusca, in of surviving many small fragments the Atlantic of trees coast forests Brazil.Even singleremnant may conserve,at least in the shortterm,some epiphytic orchidspecies(Williams-Linera, Sosa & Platas 1995). Meave & Kellman (1994) argued that, because naturalfragments tropicalrainforest of possesshigh forest need levelsofplantdiversity, fragmentation not This viewmaybe necessarily lead to mass extinction. thesenaturalforest overoptimistic: patchesmayhave similarto those of equivalentareas speciesnumbers in continuousforest thatregion,but theydo not in of approachthevery highdiversity thecorerainforest blocks. Undoubtedlythe natural fragment assemblages were derivedover a long period of timeand from humaninterference. have notsuffered damaging of Man-made fragments rain forest are literally created 'overnight'and will contain a community, elements of which have over many generations little selection for tolreceived pressure fragmentation erance.

geneticdiversity small populations.Probablythe of most interesting area of researchwill be into the of second- and higher-order effects fragmentation. but These willpresent greatchallengeto ecologists a for areofhighpotential pureas wellas appliedscience. the and One approach to understanding diversity communitystructureof tropical forestmight be experiments of throughthe natural deconstruction will habitatfragmentation. Major difficulties include findingthe right controls for such observations, of the unravelling multiplicity factorsinvolved,and the inevitable stochasticity even chaos of natural or of systems.The effectiveness corridorsand buffer of zones in ameliorating negative-impacts fragthe The ultimate attention. mentation also needs critical rain willbe to resynthesize species-rich forchallenge studestfrom tattered its remnants. Emphasison field suffers greatly ies is important. This area of research bothfrom emotional the of hyperbole theill-informed of and fromthe academic hypertrophy theoreticians and modellers. to upon how muchof Finally,it is salutary reflect theecologicalresearch ~Vhich providedthefounhas rainforest dationsforourtheories concerning tropical communities was actually conducted in fragments suchas BarroColorado Island,Panama. Acknowledgements TimWhitmore, I am very to grateful RichardCorlett, Kang Nee, PeterGrubb and Bill Laurance fortheir of comments earlier on drafts thispaper. constructive

and fragmentation isoAdler,G.H. (1994) Tropical forest amonganimalpopulationsof lationpromote asynchrony rodent. Ecology,63, 903Journal Animal of a frugivorous 911. Askins,R.A., Ewert,D.N. & Norton, R.L. (1992) Abunin and migrants fragmented continuous danceofwintering Islands.Ecologyand Conservation forests theUS Virgin in Landbirds (eds J.M. Hagan & D. ofNeotropical Migrant Press, Institution W. Johnston), 197-206.Smithsonian pp. Washington. Becker, Moure,J.S.& Peralta,F.J.A.(1991) More about P., Bioeuglossine bees in Amazonian forestfragments. tropica, 586-591. 23, Bennet,E.L. & Caldecott,J.O. (1981) Unexpectedabundance: the trees and wildlifeof the Lima Belas Estate 57, ForestReserve,near Slim River,Perak. The Planter, 516-519. of Bierregaard, R.O. & Lovejoy,T.E. (1989) Effects forest bird fragmentation Amazonianunderstory communion ties.Acta Amaz6nica, 215-241. 19, Bierregaard, R.O., Lovejoy, T.E., Kapos, V., dos Santos, R.W. (1992) The biologicaldynamics A.A. & Hutchings, of tropicalrainforest 42, fragments. BioScience, 859-866. matter? Assessingthe Bond, W.J. (1994) Do mutualisms on disruption plant impact of pollinatorand disperser Transactions the of RoyalSociety, extinction. Philosophical SeriesB, 344, 83-90. Bowman, D.J.M.S. & Woinarski, J.C.Z. (1994) Bio-

Wheredo we go from here?

We know so littleabout this enormousand urgent has to be problemthat more researchundoubtedly done. I would emphasize further workon forest fragmentsthathave been isolatedfora considerable period oftime.It is information thelongterm on viability offragments, on thenature thenewequilibrium and of value willreachthatwillbe ofgreatest pointthatthey in planning conservationstrategies.Research prioritiesmustincludestudiesto identify those groups which,in the long term, mostaffected habitat are by fragmentation, researchinto the dynamicsand and

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208 Speciesloss inrain forest

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of geography Australianmonsoon rainforest mammals: implications theconservation rainforest for of mammals. PacificConservation Biology, 98-106. 1, Brash,A.R. (1987) The history avianextinction forest of and conversion Puerto Rico. Biological Conservation, on 39, 97-111. Brown, (1993) The implications climate N. of and gap microclimate for seedling growthconditions in a Bornean lowlandrain forest. Journal TropicalEcology,9, 153of 168. Burkey, T.V. (1993) Edge effects seed and egg predation in at twoneotropical rainforest sites. BiologicalConservation, 66, 139-143. Camargo,J.L.C. & Kapos, V. (1995) Complexedge effects on soil moisture and microclimate centralAmazonian in forest. Journal Tropical of Ecology,11, 205-221. Caughley, G. (1994) Directionsin conservationbiology. Journal AnimalEcology,63, 215-244. of Corlett,R.T. (1992) The ecological transformation Sinof gapore,1819-1990.Journal Biogeography, 411-420. of 19, da Fonseca, G.A.B. & Robinson, J.G. (1990) Forest size and structure: and competitive predatory effects small on mammalcommunities. BiologicalConservation, 26553, 294. Daily, G.C. & Ehrlich,P.R. (1995) Preservation bioof in diversity small rainforest patches: rapid evaluations using butterfly and trapping.Biodiversity Conservation, 4, 35-55. H.L. & O'Neill, R.V. Dale, V.H., Pearson,S.M., Offerman, (1994) Relating patternsof land-use change to faunal in Amazon. Conservation biodiversity theCentral Biology, 8, 1027-1036. of Diamond,J.M. (1980) Patchydistributions tropical birds. Conservation PerBiology: an Evolutionary-Ecological spective(eds M. E. Soul6 & B. A. Wilcox), pp. 57-74. SinauerAssociates,Sunderland. Diamond, J.M., Bishop,K.D. & van Balen, S. (1987) Bird in survival an isolatedJavanwoodland:islandor mirror? Conservation Biology, 132-142. 1, of Duff,A.B., Hall, R.A. & Marsh, C.W. (1984) A survey in wildlife and around a commercialtree plantationin Sabah. MalaysianForester, 197-213. 47, Estrada,A., Coates-Estrada,R. & Meritt,D. (1993a) Bat and rainforest speciesrichness abundancein tropical fragat ments and in agricultural habitats Los Tuxtlas,Mexico. Ecography, 309-318. 16, Estrada,A., Coates-Estrada,R., Meritt, Montiel,S. & D., of Curiel,D. (1993b) Patterns frugivore speciesrichness habiand abundancein forest islandsand in agricultural tatsat Los Tuxtlas,Mexico. Vegetatio, 245-257. 107/108, Estrada, A., Coates-Estrada,R. & Meritt,D. (1994) Non and landscapechangesin thetropical rain mammals flying forest regionofLos Tuxtlas,Mexico. Ecography, 22917, 241.of on Faaborg,J.(1979) Qualitative patterns avianextinction islands:lessonsforconservation. neotropical land-bridge Journal Applied of Ecology,16, 99-107. Ferrari,S.F. & Diego, V.H. (1995) Habitat fragmentation and primate in of conservation theAtlantic forest eastern Minas Gerais,Brazil.Oryx,29, 192-196. Fetcher,N., Oberbauer,S.F. & Strain,B.R. (1985) Vegetationeffects microclimate lowlandtropical on in forests in Costa Rica. International Journal Biometeorology, of 29, 145-155. of Fonseca de Souza, O.F. & Brown,V.K. (1994) Effects on habitatfragmentation Amazonian termite communities.Journal TropicalEcology,10, 197-206. of Gascon, C. (1993) Breeding-habitat by fiveAmazonian use frogs forest at edge.Biodiversity Conservation, 438and 2, 444. Gentry, A.H. (1988) Changes in plantcommunity diversity

and floristic composition on environmental and geographical gradients.Annals of the Missouri Botanical Garden, 1-34. 75, Gibbs,J.P.(1991) Aviannestpredation tropical forest: in wet an experimental study.Oikos,60, 155-161. Gotelli, N.J.& Graves,G.R. (1990) Body sizeand theoccurrenceof avian specieson land-bridge islands.Journal of Biogeography, 315-325. 17, Heaney,L.R. (1984) Mammalianspeciesrichness islands on on theSunda Shelf, Southeast Asia. Oecologia,61, 11-17. Heywood,V.H. & Stuart, S.N. (1992) Speciesextinctions in and tropical forests. Tropical Deforestation SpeciesExtinction (eds T. C. Whitmore& J. A. Sayer), pp. 91-117. Chapman& Hall, London. Heywood, V.H., Mace, G.M., May, R.M. & Stuart,S.N. (1994) Uncertainties extinction in rates.Nature, 368, 105. Howe, H.F. (1984) Implications seed dispersal animals of by fortropical reserve management. BiologicalConservation, 30, 261-281. Hubbell,S.P. & Foster,R.B. (1983) Diversity canopytrees of in a neotropical forest and implications conservation. for TropicalRain Forest.Ecologyand Management (eds S. L. & Sutton,T. C. Whitmore A. C. Chadwick),pp. 25-41. BlackwellScientific Publications, Oxford. Janzen, D.H. (1983) No park is an island:increasein interference fromoutside as park size decreases. Oikos, 41, 402-410. A.D. & Skorupa,J.P.(1987) Responsesofrain-forest Johns, primatesto habitat disturbance: review.International a Journal Primatology, 157-191. of 8, Kapos, V. (1989) Effects isolationon thewaterstatusof of forest in patches theBrazilian Amazon.Journal Tropical of Ecology, 173-185. 5, on Karr, J.R. (1982a) Avian extinction Barro Colorado Island,Panama: a reassessment. American Naturalist, 119, 220-239. in and Karr, J.R. (1982b) Populationvariability extinction theavifaunaof a tropicalland bridge island.Ecology,63, 1975-1978. H. Kattan,G.H., Alvarez-L6pez, & Giraldo,M. (1994) Forand San estfragmentation birdextinctions: Antonioeighty yearslater.Conservation Biology, 138-146. 8, of on Klein, B.C. (1989) Effects forest fragmentation dung and carrion beetle communities Central Amazonia. in Ecology, 1715-1725. 70, Laurance, W.F. (1990) Comparative responses of five arborealmarsupials tropical to forest Jourfragmentation. nal ofMammalogy, 641-653. 71, in Laurance,W.F. (1991a) Edge effects tropicalforest fragments:applicationof a model for the design of nature reserves. BiologicalConservation, 205-219. 57, of Laurance,W.F. (1991b) Ecological correlates extinction pronenessin Australiantropical rain forestmammals. Conservation Biology, 79-89. 5, and Laurance, W.F. (1994) Rainforest fragmentation the structureof small mammal communitiesin tropical Queensland.BiologicalConservation, 23-32. 69, Laurance,W.F., Garesche,J. & Payne,C.W. (1993) Avian in and in nestpredation modified naturalhabitats tropical Queensland:an experimental study.Wildlife Research, 20, 711-723. in Leck, C.F. (1979) Avian extinctions an isolatedtropical wet-forest Ecuador. Auk,96, 343-352. preserve, Leigh, E.G., Wright, S.J.,Herre,E.A. & Putz, F.E. (1993) The decline of tree diversity newlyisolated tropical on islands:a testof a nullhypothesis some implications. and 7, Evolutionary Ecology, 76-102. Leung,L.K.-P., Dickman,C.R. & Moore, L.A. (1993) Geneticvariation fragmented in populationsof an Australian rainforest rodent,Melomys cervinipes.Pacific Conservation Biology, 58-65. 1,

209 I.M. Turner

Loiselle,B.A. & Blake, J.G. (1992) Populationvariationin BioScience, 838-845. 42, a tropicalbirdcommunity. Loiselle, B.A. & Hoppes, W.G. (1983) Nest predationin in insular and mainland lowland rainforest Panama. Condor, 93-95. 85, D. Loope, L.L. & Mueller-Dombois, (1989) Characteristics to of invadedislands,withspecialreference Hawaii. Bio(eds J. A. Drake, logicalInvasions:A Global Perspective H. A. Mooney, F. di Castri,R. H. Groves,F. J. Kruger, M. Rejmdnek& M. Williamson),pp. 257-280. Wiley, Chichester. Lovejoy,T.E., Bierregaard, R.O., Rylands,A.B., Malcolm, J.R.,Quintela,C.E., Harper,L.H., Brown,K.S., Powell, A.H., Powell, G.V.N., Schubart,H.O.R.-& Hays, M.B. of (1986) Edge and other effects isolation on Amazon Conservation forestfragments. Biology: the Science of (ed. M. E. Soul6), pp. 257-285. Scarcityand Diversity SinauerAssociates,Sunderland. of reductions the diversity in Lugo, A.E. (1988) Estimating forest (ed. tropical species.Biodiversity E. 0. Wilson),pp. 58-70. National AcademyPress,Washington. light MacDougall, A. & Kellman,M. (1992) The understorey of in regime and patterns treeseedlings tropicalriparian forest 19, of patches.Journal Biogeography, 667-675. Malcolm,J.R. (1988) Smallmammalabundancesin isolated forestreservesnear Manaus, and non-isolatedprimary 18, Brazil.Acta Amaz6nica, 67-83. in Malcolm, J.R. (1994) Edge effects centralAmazonian forest Ecology, 2438-2445. 75, fragments. of Meave, J.& Kellman,M. (1994) Maintenance rainforest of in diversity riparianforests tropicalsavannas: implications for species conservation during Pleistocene of 21, drought. Journal Biogeography, 121-135. Mills, L.S. & Smouse, P.E. (1994) Demographic consein populations.American quences of inbreeding remnant Naturalist, 144,412-431. in forests: impliMurcia,C. (1995) Edge effects fragmented Trends Ecologyand Evolution, in cationsforconservation. 10, 58-62. and fragmentation Newmark,W.D. (1991) Tropical forest birds in the Eastern the local extinction understorey of Tanzania. Conservation Usambara Mountains, Biology, 5, 67-78. of Nichol, J.E. (1994) An examination tropicalrain forest microclimate using GIS modelling.Global Ecology and Letters, 69-78. 4, Biogeography J.W. & Heinsohn,G. (1988) Variation Pahl, L.I., Winter, of in responsesof arborealmarsupialsto fragmentation in tropicalrainforest northeasternAustralia.Biological 46, Conservation, 71-82. Powell,A.H. & Powell,G.V.N. (1987) Populationdynamics of male euglossinebees in Amazonian forest fragments. Biotropica, 176-179. 19, and forest Primack,R.B. & Hall, P. (1992) Biodiversity 42, changein Malaysian Borneo.BioScience, 829-837. Robbins, C.S., Dowell, B.A., Dawson, D.K., Col6n, J.A, R. J., Espinoza,F., Rodriguez, Sutton, & Vargas,T. (1987) in winter birdpopulations isoComparisonofneotropical forest. Acta ffcologica, 285latedpatches versus extensive 8, 292. Robbins, C.S., Dowell, B.A., Dawson, D.K., Col6n, J.A., Estrada, R., Sutton,A., Sutton,R. & Weyer,D. (1992) land birdpopulations migrant Comparisonofneotropical

and fragments, isolatedforest forest, in wintering tropical of habitats.Ecology and Conservation Neoagricultural tropicalMigrantLandbirds(eds J. M. Hagan & D. W. Press, Johnston), pp. 207-220. SmithsonianInstitution Washington. insular and differential K.E. (1992) Nest predation Sieving, birdsofCentralPanama. forest amongselected extinction 73, Ecology, 2310-2328. D. (1992) Species-area relationships,fragSimberloff, in mentation, and extinction tropical forests.Malayan NatureJournal, 398-413. 45, and Simon,J.L. (1986) Disappearingspecies,deforestation 110,60-63. data. New Scientist, T.H. & Smith,F.D.M., May, R.M., Pellew, R., Johnson, Walter,K.R. (1993) How much do we know about the in rate?Trends Ecologyand Evolution, current extinction 8, 375-378. of R.O. (1995) Effects forest P.C. & Bierregaard, Stouffer, in hummingbirds Amaon fragmentation understorey 9, Biology, 1085-1094. zonian Brazil. Conservation in Terborgh,J. (1992) Maintenance of diversity tropical forests. Biotropica, 283-292. 24, Thiollay, J.-M. & Meyburg, B.U. (1988) Forest fragof and the conservation raptors:a surveyon mentation 44, theislandofJava.BiologicalConservation, 229-250. rangesof Thomas,C.D. (1991) Habitat use and geographic butterflies fromthe lowlands of Costa Rica. Biological 55, Conservation, 269-281. Turner,I.M., Tan, H.T.W., Wee, Y.C., Ali bin Ibrahim, of R.T. (1994) A study plantspecies Chew,P.T. & Corlett, of in extinction Singapore:lessons for the conservation Conservation 8, Biology, 705-712. tropicalbiodiversity. T.C. (1991) Invasivewoody plantsin perhumid Whitmore, tropicalclimates.Ecology of BiologicalInvasionsin the pp. Tropics P. S. Ramakrishnan), 35-40. International (ed. New Delhi. Publications, Williams-Linera,G. (1990) Vegetation structure and of conditions forest environmental edgesin Panama. Jour78, nal ofEcology, 356-373. of G. Williams-Linera, (1992) Distribution thehemiepiphyte of at Oreopanaxcapitatus theedgeand interior a Mexican lowermontaneforest. Selbyana,13, 35-38. de G. Williams-Linera, (1993) Vegetaci6n bordesde un nublado en el Parque Ecol6gica Clavijero,Xalapa, Veracruz, Mexico. Revistade Biologia Tropical, 443-453. 41, Williams-Linera, Sosa, V. & Platas, T. (1995) The fate G., of orchidsafterfragmentation a Mexican of epiphytic cloud forest. Selbyana,16, 36-40. of E.O. (1974) Populationsand local extinctions birds Willis, on Barro Colorado Island, Panama. Ecological Mono44, graphs, 153-169. of Willis,E.O. (1979) The composition avian communities Brazil.Papeis Avulin remanescent woodlotsin Southern sos de Zoologia,33, 1-25. of Willson,M.F. & Crome,F.H.J. (1989) Patterns seed rain Journal at the edge of a tropicalQueenslandrain forest. Ecology, 301-308. 5, of Tropical R.O. (1986) Relevanceof B.L. & Bierregaard, Zimmerman, and of theequilibrium theory islandbiogeography speciesAmazonia. a with case from to area relations conservation 13, Journal Biogeography, 133-143. of 1995 8 received August 1994; revision 5 Received September

? 1996British Ecological Society, of Journal Applied 33, Ecology, 200-209