The conservation value of small, isolated fragments of lowland tropical rain forest

REVIEWS 31 Kawecki, T.J. (1995) Demography of source-sink populations and the evolution of ecological niches, Euol. Ecol. 9,38-44 32 Holt, R.D.and Gomulkiewicz, R. How does immigration influence local adaptation? A re-examination of a familiar paradhfm,Am. Nat. (in press) 33 Fretwell, SF. (1972) Populations in a Seasonal Environment, Princeton University Press 34 Dias, PC. et al. (1994) Blue tits in meditetranean habitat mosaics,

41 Reille, M. (1984) Origine de la veg&ation actuelle de la Come sud-orientale; auaiyse pollinique de cinq marais cotiers, Pollen Spores 26,43-60 42 Van Balen, J.H. (1973) A comparative study of the breeding ecology of the great tit Parus major in different habitats, Ardea 61, l-59 43 Anon. (1988) Dkpaflement de la Haute-Corse et de la Gorse-Sud. RBultats du DeuxiPme Inventaire Forestier, (1987-1988), Ministere

Ardea 82,363-372 35

36

37

38 39

40

Meller, A.P. (1995) Developmental stability and ideai despotic distribution of blackbirds in a patchy environment, Oikos 72, 228-234 Keddy, P.A. (1981) Fxperimentai demography of the sand-dune annual Cakife edentuh, growing along au environmental gradient in Nova Scotia, J. Ecol. 69,615-630 Pulliam, H.R. and Danielson, B.J. (1991) Sources, sinks and habitat selection: a landscape perspective on population dynamics, Am. Nat. 137(Suppl.), S50-566 Thompson, J.D. (1991) Phenotypic plasticity as a component of evolutionary change, Trends Ecol. Euol. 6,246-249 Dias, P.C. and Blondel, J. Local specialization and maladaptation in Mediterranean blue tits Parus caeruleus, Oecologia (in press) Holt, R.D. (1996) Adaptive evolution in a source-sink environment: direct and indirect effects of density-dependence on niche evolution, Oikos 75,182-192

44

45 46 47 48

49

de I’Agriculture et du Developpement Rural, lnventaire Forestier National, France Lambrechts, M. and Dias, P.C. (1993) Difference in the onset of laying between island and mainland Mediterranean blue tits Par-us caerufeus: phenotypic plasticity or genetic differences? Ibis 135, 451-455 Hutchinson, GE. (1958) Concluding remarks, Cold Spring Harbor Symp. Quant. Biol. 22,415-427 Lebreton, J-D. and Gonzalez-Davila, G. (1993) An introduction to models of subdivided populations, J. Biol. Syst. 1,389-423 Danielson, B.J. (1992) Habitat selection, interspecific interactions and landscape composition, Euol. Ecol. 6,399-411 Gaggiotti, O.E. and Smouse, P.E. (1996) Stochastic migration and maintenance of genetic variation in sink populations, Am. Nat. 147,919-945 Wootton, J.T. and Bell, D.A.(1992) A metapopuiation model of the peregrine falcon in California: viability and management strategies, Ecol. Appl. 2,307-321

The conservationvalue of small, isolated fragmentsof lowlandtropicalrainforest I.M. Turner and Richard T. Corlett

I

Deforestation Is occurring at an alarming areas undergoing rapid rates of t has been estimated that by rate in the lowland tropics. In many deforestation4. 1990,24% of the lowland tropitropical regions, rain forest Is restricted cal rain forest on Earth had Large, undisturbed areas of been cleared’, largely to create to small (400 ha), isolated fragments. lowland tropical rain forest must agricultural land. The rate of tropiWhile only the preservation of large areas be one of the highest priorities for cal deforestation continues to of tropical raln forest can safeguard the conservation. Yet, as outlined complete blota, recent research has acceleratelJ. In many countries of above, many tropical nations now have few, if any, such areas rethe humid tropics, the loss of pri- shown that a substantial number of forest species can persist for decades in maining. What these countries mary lowland forest far exceeds fragmented forest, though large the global average, and lowland usually do possess are many scatrain forest only occurs as isolated vertebrates are susceptible to habitat tered and isolated fragments of forest: the vast majority of which remnants. According to the 1990 fragmentation. Inevitably, small fragments will become the last refuges of many are small-less than 100ha (1 lo+) estimates of the Food and Agriculrainforest species that are on the brink ture Organizationl, roughly one in - and heavily disturbed, often of extlnctlon. In areas with little rain four tropical rainforest countries being located on steep slopes or forest remaining, fragments can be the poor soils5. Are such fragments surveyed had less than 30% of ‘seeds’ from which to re-establish worth conserving? A positive retheir original lowland rainforest area remaining, including such extensive forest. sponse to the same question has already been given for tropical dry large nations as Thailand and the forest6 and various wildlife habiPhilippines. Regions within certain Ian Turner is at the School of Biological Sciences, tats in the USAT.Recent research is countries may also be more seNational University of Singapore, Singapore 119260 helping to elucidate an appropriverely affected than others. For ([email protected]); Richard Corlett is at the instance, the Atlantic coastal forate response for lowland tropical Dept of Ecology and Biodiversity, University of rain forest. ests of Brazil are currently estiHong Kong, Pokfulam Road, Hong Kong mated to occupy only 12%of their ([email protected]). original area3. Long-term viability of small fragments of lowland tropical Lowland tropical rain forests are the most species-rich of terresrain forest The diversity of lowland tropical rain forest is so great trial ecosystems. Therefore, their destruction must be seen as the greatest threat to the biological diversity of the that no complete biological inventory for an area of forest planet. It is already clear, for example, that many globally has yet been made, and probably only a minority of its spethreatened bird species are restricted to tropical forest ties have been described taxonomically. Fragments of forest

330

0

1996, Elsevier Science Lid

PII: SO169_5347(96)10046X

TREE uol. 1 I. no. 8 August

1996

REVIEWS will contain many species at the time when they first become isolated, but the number will diminish over time after isolation owing to a variety of factors (see Box 1). Genetic diversity will probably be eroded in line with species diversity, but this has, to date, received little scientific attention in tropical forestsa. If small remnant fragments of lowland tropical rain forest can be shown to lose much of their biodiversity rapidly, there would be little to argue in favour of their conservation. Unfortunately, there have been relatively few studies of the biodiversity of small fragments of lowland rain forest that have been isolated for more than a decade. Instead, the mostdetailed studies of tropical forest fragmentation have come from the Biological Dynamics of Forest Fragments Project (based near Manaus in Amazonian Brazil). These studies have followed the biodiversity and community structure of small, mostly 1 and 10ha fragments before and after isolation from continuous fores@. Publications concerning studies spanning the first decade of isolation are now appearinglosll, but it is probably still too early to pinpoint the likely longterm effects of fragmentation. The Manaus set-up is also rather untypical of the severe fragmentation with which we are particularly concerned here. The fragments at Manaus are separated from large areas of continuous forest by very short distances (sometimes ~100m) and the cleared forest areas have generally been allowed to develop secondary forest, thus rapidly reforming a continuous canopy link to the extensive forest. Bukit Timah Nature Reserve in Singapore is probably the best-studied, long-term, small tropical rainforest fragment in the world. The reserve contains 50 ha of primary lowland forest that has been isolated for at least 130 years (see Box 2). It maintains a primary forest character despite the extinction of many of its larger vertebrate species. However, the Singapore Botanic Gardens’ Jungle, a much smaller remnant (4 ha) of tropical rain forest that has been isolated for a similar length of time as Bukit Timah, has lost half of its native plant species over the past century or ~012.The Gardens’ Jungle has become heavily dominated by one tree species, Calophylfumfen-ugineum,and in other areas the proliferation of climbers appears to be preventing tree regeneration. Tiny (~1 ha) islands formed from forested hill tops, when Lake Gatun in Panama was created about 80 years ago, have become dominated by a few species of large-seeded treel3. A similar pattern of reduced species-richness and simplification of the community structure has been shown in studies on vertebrates in long-term, small isolates14-17;and recently, also for butterfliesi8. Some species can persist in small isolated fragments of rain forest, however. For instance, bird species thought to be extinct have been newly rediscovered in relict forest patches on Cebu, one of the islands of the Philippinesig, and threatened primates can be found in many fragments of forest in Atlantic Brazil*O.Even individual relic trees from tropical forest have been shown to harbour a wide diversity of epiphytic plant specieszl. Clearly, species of large mammals cannot persist within small fragments. A number of other characteristics have also been associated with proneness to local extinction owing to habitat fragmentation in tropical forest animals. These include intolerance of the conditions outside the forestz2, a high degree of specialization, possession of a narrow geographic rangeQ24,and a naturally variable population size25. What is, as yet, poorly understood is what proportion of the original rainforest community can maintain viable populations in isolated fragments. Many species may be persisting for long periods after isolation purely by the longevity of individuals that are no longer reproducing. TREE vol.

1 I, no. 8 August

1996

Box 1. Mechanisms of deterioration in isolated fragments of lowland tropical rain forests Deforestation-related disturbance During and after isolation, human activity will often involve harvesting plant material (including timber), hunting animals, the diversion of water courses, and the intrusion of fire or smoke into fragments. Restriction of population size A small area of forest will only be able to support small populations of most species. Small populations are more likely to fluctuate to below demographic viability and to lose genetic diversity through genetic drift and inbreeding. Reduction In immigration Many rainforest animals are reluctant to cross open areas. This reduces the rate of immigration of individuals into isolated fragments, making the re-establishment of extinct species unlikely and increasing the genetic isolation of fragmented populations. Forest edge effects The edges of fragments, particularly where they meet non-forest vegetation, rep resent major transition zones. The internal microclimate of the forest is frequently hotter, drier and brighter near to the edge. Tree mortality may increase near new edges. These changes can adversely affect forest species. Higher-order effects The losses of certain species within a fragment may have knock-on effects. For instance, the loss of large carnivores may allow increases in some species of smaller carnivores, which, in turn, could have detrimental affects on the species they predate. Immigration of alien species Few of the rainforest species are tolerant of the open conditions of agricultural or early successional sites. Such sites are dominated by a group of common, often pantropical, species. These come to surround fragments and may start to invade and outcompete the indigenous species in the fragments.

Natural fragments: are they relevant? In areas of the tropics where the climate is near the limits of seasonal dryness that will support true rain forest, the forest becomes confined to certain parts of the landscape, typically along rivers and streams or on patches of certain soil types. Such natural rainforest fragments have been found to exhibit a relatively high diversity of tree species26v27, though their vertebrate faunas, particularly mammal species, may be limited. The high diversity of natural fragments has been put forward, admittedly with certain reservations, as a hopeful sign that artificial fragments of tropical rain forest may be able to support, indefinitely, a reasonable array of species?, particularly plants and invertebrates. However, it must be remembered that natural fragments have developed over thousands of years, allowing for the selection of species and genotypes suited to life in isolated patches of forest. The virtually instantaneous formation of man-made fragments from extensive lowland forest is likely to be a much more dramatic event and may exclude a greater proportion of the community. Yet, Hong Kong has retained a large number of tropical forest plant species despite near total deforestation and defaunation, which took place over 300 years ago28.Thus, there are grounds for believing that a substantial element of the rainforest plant community may be relatively resistant to fragmentation, and that dire predictions of plant extinction, through loss of pollinating and seed-dispersing vertebrates from fragments, may be overly pessimistic*‘. We clearly need more studies of the major processes of diversity loss in forest remnants to identify which are the most serious. Fragments are better than nothing Many rainforest species have an absolute requirement for the survival of rain forest. Human-dominated agricultural landscapes in the wet tropics contain a high biodiversity, though mostly consisting of a group of abundant, pantropical, cultivated, weedy or anthropic specie@. The presence of fragments of original forest will significantly enhance the diversity of the landscape and increase the likelihood of the 331

REVIEWS survival of the indigenous biota, or at least a portion of it. At Los Tuxtlas in Mexico, 40%of the vertebrate frugivore species were confined to the forest fragments in the landscaper6. Certain animal groups are able to persist in fragments; for example, understorey hummingbird communities in Amazonian Brazil were not greatly affected by fragmentationlo, at least in the short-term. Even tiny remnant and regrowth patches can provide valuable habitat for some forest birdr6JOJrand forest mammal speciesuJ2. Forest insects may also be able to make use of linear remnants or native trees planted outside primary forestl8Ja. But near-complete deforestation will exterminate virtually all of the native species, as has happened with forest vertebrates in Hong Kong*s. Fragments may also be of benefit to migratory animals as sites that provide food and shelter for specific periods of the year. Certainly, neotropical migrant birds have been found to make use of small tropical forest fragment+. Improving the likelihood of maintaining fragment biodlversity Several factors influence the number of species that are likely to survive in a forest fragment. Size and degree of isolation are important, but frequency and intensity of human disturbance and the nature of the surrounding vegetation may play a major role as well. Anecdotal accounts of surprisingly rich wildlife in long-isolated fragments of lowland rain forest in Malaysias5J6point to low human disturbance and buffer zones of tree vegetation as being important in maintaining the forest biodiversity. Recent studies of understorey insectivorous birds in isolated fragments in BraziP have indicated that the rapid establishment of tall secondary forest around small fragments linking them back to more extensive primary forest areas greatly accelerates the recovery of the avian insectivore community to something close to the pie-isolation situation. Such studies need to be repeated for fragments that have a greater degree of isolation and time since excision, but these results give some hope that there are feasible management options for maintaining the species richness of fragments of lowland tropical rain forest. Fragments in conservation strategies Given the enormous biodiversity of tropical rain forest, it is obvious that exsitu conservation methodologies will not be able to cope with the present threats to species and genetypes from the lowland tropics-not that the resources would be available to employ these methods anyway, in what are generally underdeveloped nations. Small fragments will provide a safety net for a significant number of species and their genetic diversityar; a breathing space for conservationists to plan strategies for preventing the loss of the species concerned. Intervention management can then be focused on species that are particularly sensitive to fragmentation such as large carnivores and epiphytic orchidss’. Fragments can also act as sources for recolonization of nearby areas undergoing succession6. Many rainforest species possess limited powers of dispersal, and re-establishment of primary species in secondary forest may be virtually impossible if no fragments occur within a short distance of the site. Our studies in Singapore and Hong Kong*Qr indicate that natural succession is very slow to incorporate primary forest specialists, though in both places succession is generally taking place on highly degraded land. Even when the secondary forest is directly contiguous with the primary fragment, lack of dispersal is possibly preventing the arrival of many species. Others have reported that secondary forests can accrete diversity quite rapidly38.39,but these data 332

Box 2. Bukit Timah Nature Reserve, Singapore: a fragment of primary lowland rain forest isolated for many years The tallest hill (163 m a.s.1.) in Singapore, Bukit Timah, is mostly covered with 164 ha of tropical forest-the Bukit Timah Nature Reserveal. The upper slopes of the hill support about 50 ha of primary dipterocarp forest from which nearly 900 plant species have been recordedQ43. Bukit Timah has been isolated from other areas of primary forest since at least 1860 (Ref. 44). The rest of the reserve consists of secondary forest of various types. This was contiguous with a much larger area of mostly secondary forest in the centre of Singapore Island until 1985 when an eight-lane highway was built, severing this link‘u. The loss of 99.8% of primary forest in Singapore over the past 150years44 has led to the loss of a substantial fraction of the native biota, including 26% of the vascular plant flora, 28% of the resident avifauna and 44% of the species of freshwater fish37.44. Bukit Timah, therefore, no longer con tains large carnivores such as tiger (Panthera tigris corbetti) or leopard (Panthera pardus fusca), large herbivores such as the banded langur (Presbflis femoralis femoralis), sambur (Cervus unicolor equinus) and barking deer (Muntiacus muntjak peninsulae), and many forest bird species have become extinct, such as the hornbills (Bucerotidae), trogons (Jrogonidae), broadbills (Eurylaimidae) and all but one barbet (Capitonidae)41. The reserve contains two telecommunication installations served by a single-lane road, an extensive network of trails and several abandoned quarries; it receives many thousands of human visitors each year. Despite all this, most of the primary forest areas still have the appearance of the interior of extensive forest tract+. The only exotic plant species to have invaded the primary forest widely is the small melastomataceous shrub Clidemia hirta37. Bukit Timah demonstrates that isolated fragments of lowland tropical rain forest do have more than a temporary ecological viability.

are generally based on small plots. Larger sample areas would probably show that the secondary forests are typically floristically monotonous and, as a whole, contain many fewer species than the primary forest2g. However, secondary forest contiguous to primary forest remnants can still play an important role in providing extra resources for certain forest animal species, facilitating their movement and ameliorating the microclimate of the fragment. One counter argument to conserving many fragments in the same area is that they may contain nested subsets of the indigenous biota40. In other words, one fragment contains much the same set of species as another, and so once one fragment is conserved, using resources to conserve more replicates of the same fragment may prove inefficient. However, even with birds and mammals, species loss from fragments may result from non-size-dependent processes, such as hunting, and the patchy distribution of plant communities in the rain forest makes it unlikely that fragments would be replicate random samples from a uniform biota. Conclusions There is unequivocal evidence that fragments of tropical forest do decline in species richness over time when they become isolated from continuous forests. The pace and duration of this decline are still poorly known, but the scanty data indicate that fragments of ~100ha can retain a relatively large proportion of their biodiversity decades after isolation. Fragments can act as last refuges for plant and animal species and may provide an opportunity for conservationists to launch last-chance attempts to rescue species from extinctionar. The majority of tropical rainforest species are relatively intolerant of conditions outside the rain forest and possess limited powers of dispersal. The presence of fragments in a landscape will allow the persistence of certain species, many more than a completely deforested landscape could support. The fragments may also be able to grow if given the TREE ool.

II,

no. 8 August

1996

REVIEWS right opportunity. This could eventually result in the reforestation of tropical landscapes. It is likely that the recreation of lowland rain forest through the coalescence of remnant fragments will be easier, both technically and economically, than starting from bare ground. We conclude that small fragments of lowland tropical rain forest are worth conserving. Unprotected fragments are being lost or irreversibly damaged every day. Evaluation and protection of such fragments should have high priority, particularly in those parts of the tropics where no other forest remains. Acknowledgements N.S. Sodhi, A. Balmford, S.J. Wright and the students of BP31 1 kindly provided some valuable comments on the paper.

References 1 FAO(1993) Forest Resources Assessment 1990: Tropical Countries, FAO Forestry Paper 112 2 Whitmore, T.C. and Sayer, J.A. (1992) Deforestation and species extinction in tropical moist forests, in Tropical Deforestation and Species Extinction (Whitmore, T.C. and Sayer, J.A., eds), pp. 1-14, Chapman &Hall 3 Brown, K.S. and Brown, G.G.(1992) Habitat alteration and species loss in Brazilian forests, in Tropical Deforestation and Species Extinction (Whitmore, T.C. and Sayer, J.A., eds), pp. 119-142, Chapman &Hall 4 Balmford, A. and Long, A. (1994) Avian endemism and forest loss, Nature 372,623-624

5 Chatelain, C., Gautier, L. and Spichiger, R. (1996) A recent history of forest fragmentation in southwestern Ivory Coast, Biodiuers. Conseru. 5,37-53

Janzen, D.H. (1988) Management of habitat fragments in a tropical dry forest growth, Ann. MO Bet Card. 75,105-l 16 Shafer, CL. (1995) Values and shortcomings of small reserves, Bioscience

45,80-88

Turner, I.M. (1996) Speciesloss in fragments of tropical rain forest: a review of the evidence, J. Appl. Ecol. 33,200-219 Bierregaard, R.O. el al. (1992) Effects of forest fragmentation on Amazonian underetory bird communities, Bioscience 42, 859-866

10 Stouffer, P.C. and Bierregaard, R.O. (1995) Effects of forest fragmentation on understory hummingbirds in Amazonian Brazil, Conseru. Biol. 9, 1085-1094 11 Stouffer, PC and Bierregaard, R.O. (1995) Use of Amazonian forest fragments by understory insectivorous birds, Ecology76, 2429-2445 12 Turner, I.M. et al. A century of plant species loss from an isolated fragment of lowland tropical rain forest, Conseru. Biol. (in press) 13 Leigh, E.G. et al. (1993) The decline of tree diversity on newly isolated tropical islands: a test of a null hypothesis and some implications, Euol.Ecol.7,76-102 14 Leek,CF. (1979)Avian extinctions in an isolated tropical wet-forest preserve, Auk 96,343-352 15 Willis, E.O. (1979) The composition of avian communities in remanescent woodlots in southern Brazil, Pap&s Aoulsos Zool. 33, l-25

16 Estrada, A. et al. (1993) Patterns of frugivore species richness and abundance in forest islands and in agricultural habitats at Los Tuxtlas, Mexico, Vegetatio 107/108,245-257 17 Laurance, W.F. (1994) Rainforest fragmentation and the structure of small mammal communities in tropical Queensland, Biol. Conserv. 69,23-32

18 Daily, G.C. and Ehrlich, P.R. (1995) Preservation of biodiversity in small rainforest patches: rapid evaluations using butterfly trapping, Biodivers. Conserv. 4,35-55 19 Magsalay, P. et al. (1995) Extinction and conservation on Cebu, Nature 373,294

20 Ferrari, SF. and Diego, V.H. (1995) Habitat fragmentation and primate conservation in the Atlantic Forest of eastern Minas Gerais, Brazil, Oryx29, 192-196 TREE vol.

11, no. 8 August

1996

21 Hietz-Seifert, U., Hietz, P. and Cuevara, S. (1996) Epiphyte vegetation and diversity on remnant trees after forest clearance in southern Veracmz, Mexico, Biol. Conseru. 75,103-l 11 22 Laurance, W.F.(1991) Ecological correlates of extinction proneness in Australian tropical rain forest mammals, Conseru. Biol. 5, 78-89

23 Kattan, G.H.,Alvarez-L6pez, H. and Giraldo, M. (1994) Forest fragmentation and bird extinctions: San Antonio eighty years later, Conseru. Biol. 8, 138-146 24 Thomas, C.D. (1991) Habitat use and geographic ranges of butterflies from the lowlands of Costa Rica, Biol. Conseru. 55,

269-281 25 Karr, J.R. (1982) Population variability and extinction in the avifauna of a tropical land bridge island, Ecology 63,1975-1978 26 Meave, J. and Kellman, M. (1994) Maintenance of rain forest diversity in rfparian forests of tropical savannas: implications for species conservation during Pleistocene drought, J. Biogeogr. 21, 121-135

27 Bowman, D.M.J.S.and Woinarski, J.C.Z. (1994) Biogeography of Australian monsoon rainforest mammals: implications for the conservation of rainforest mammals, Pacific Conserv. Biol. 1,98-106 28 Corlett, R.T. and Turner, 1.M.Long-termsurvival in tropical forest remnants in Singapore and Hong Kong, in Tropical Forest Remnants: Ecology, Management and Conservation of Fragmented Communities (Laurance, W.F., Bierregaard, R.O. and Moritz, C., eds),

University of Chicago Press (in press) 29 Corlett, R.T. (1995) Tropical secondary forests, Prog.Pbys. Ceogr. 19,159-172 30 Crome, F., Isaacs, .I. and Moore, L. (1994) The utility to birds and mammals of remnant riparian vegetation and associated windbreaks in the tropical Queensland uplands, Pacific Consero. Biol. 1,328-343 31 Warkentin, I.G., Greenberg, R. and Salgado Ortiz, J. (1995) Songbird use of gallery woodlands in recently cleared and older settled landscapes of the Selva Lacandona, Chiapas, Mexico, Conseru. Biol. 9,1095-1106

32 Estrada, A., Coates-Estrada, R. and Meritt, D. (1994) Non flying mammals and landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico, Ecography 17,229-241 of rain forest vegetation as potential 33 Hill, C.J. (1995) Linearstrips dispersal corridors for rain forest insects, Conseru. Biol. 9, 1559-1566 34 Robbins, C.S. et al. (1992) Comparison of neotropical migrant land bird populations wintering in tropical forest, isolated forest fragments, and agricultural habitats, in Ecology and Conservation of Neotropical MigrantLandbirds (Hagan, J.M. and Johnston, D.W.,eds), pp. 207-220, Smithsonian Institution Press 35 Bennet, E.L. and Caldecott, J.O. (1981) Unexpected abundance: the trees and wildlife of the Lima Belas Estate Forest Reserve, near Slim River, Perak, Planter 57,516-519 36 Duff,A.B., Hall, R.A.and Marsh, C.W. (1984) A survey of wildlife in and around a commercial tree plantation in Sabah, Malays. Forest. 47, 197-213 37 Turner, I.M.et al. (1994) A study of plant species extinction in Singapore: lessons for the conservation of tropical biodiversity, Conseru. Biol. 8, 705-712 38 Lugo, A.E., Parrotta, J.A. and Brown, S. (1993) Loss in species caused by tropical deforestation and their recovery through management, Ambio 22,106-109 39 Finegan, B. (1996) Pattern and process in neotropical secondary rain forests: the first 100 years of succession, Trends Ecol. Euol. 11, 119-124 40 Blake, J.G. (1991) Nested subsets and the distribution of birds on isolated woodlots, Conseru. Biol. 5,58-66 41 Chin, S.C. et al., eds (1995) Rain Forest in ihe City; Bukif Timah Nature Reserue Singapore (Gardens’ Bulletin, Supplement No. 3), National Parks Board 42 Corlett, R.T. (1990) Flora and reproductive phenology of the rain forest at Bukit Timah, Singapore, J. Trop. Ecol. 6,55-63 43 Turner, I.M.(1994)The taxonomy and ecology of the vascular plant flora of Singapore: a statistical analysis, Bat J. Linn. Sot. 114, 215-227 44 Corlett, R.T. (1990) The ecological transformation of Singapore, 1819-1990,J. Biogeog. 19,411-420