Species Loss in Fragments of Tropical Rain Forest: A Review of the
Transcription
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 This content downloaded on Fri, 8 Mar 2013 14:23:34 PM 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 This content downloaded on Fri, 8 Mar 2013 14:23:34 PM All use subject to JSTOR Terms and Conditions 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- This content downloaded on Fri, 8 Mar 2013 14:23:34 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Fri, 8 Mar 2013 14:23:34 PM All use subject to JSTOR Terms and Conditions 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 This content downloaded on Fri, 8 Mar 2013 14:23:34 PM All use subject to JSTOR Terms and Conditions 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. 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