Another key factor is that, in tropical rainforests, most species are locally rare throughout all or much of their geographic range ( Hubbell & Foster 1986; Pittman et al. 1999). The acidic, nutrient-poor soils prevalent in much of Amazonia ( Brown 1987 ) appear to promote animal rarity by limiting fruit and flower production and reducing the nutrient content of foliage (reviewed by Laurance 2001. As a result, many invertebrates ( Vasconcelos 1988; Becker et al. 1991) and vertebrates ( Emmons 1984; Rylands & Keuroghlian 1988; Stouffer & Bierregaaard 1995a; Kalko 1998; Spironello 2001 are considerably less abundant in forests overlaying nutrient-poor Amazonian soils than they are in more-productive areas of the Neotropics. Intrinsic rarity is a critical feature, as demonstrated by studies of Amazonian trees. Even if a species is present when a fragment is initially isolated, its population may be so small that it has little chance of persisting in the long term ( Laurance et al. 1998a).
Figure 2. Species-area relationships for nine species of terrestrial insectivorous birds (mean ± SE) in the Biological Dynamics of Forest Fragments Project study area. Regression lines are fitted separately for fragments ( R2 = 94.3%) and control sites ( R2 = 99.4%) (after Stratford & Stouffer 1999.
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In contrast, a few taxa have remained stable or even increased in species richness after fragment isolation. Frog richness increased because of an apparent resilience of most rainforest frogs to area and edge effects and an influx of nonrainforest species from the surrounding matrix (Gascon 1993; Tocher et al. 1997 ). Butterfly richness also rose after fragment isolation, largely from an invasion of generalist matrix species at the expense of forest-interior butterflies ( Brown & Hutchings 1997 ). Small-mammal richness has not declined in the BDFFP fragments, because most species readily use edge and regrowth habitats ( Malcolm 1997 ). Collectively, BDFFP results reveal that the responses of different species and taxonomic groups to fragmentation are highly individualistic and suggest that species with small area needs which tolerate matrix and edge habitats are the least vulnerable (e.g., Offerman et al. 1995; Stouffer & Bierregaard 1995b; Didham et al. 1998a; Gascon et al. 1999.
The BDFFP has helped reveal the remarkable diversity of edge effects in fragmented rainforests, effects that alter physical gradients, species distributions, and many ecological and ecosystem processes ( Fig. 3). Microclimatic changes near edges, such as reduced humidity, increased light, and greater temperature variability, penetrate up to 60 m into fragment interiors ( Kapos 1989) and can negatively affect species adapted for humid, dark forest interiors ( Lovejoy et al. 1986; Benitez-Malvido 1998). Leaf litter accumulates near edges (Carvalho & Vasconcelos 1999; Didham & Lawton 1999) because drought-stressed trees shed leaves and possibly because drier edge conditions slow litter decomposition ( Kapos et al. 1993; Didham 1998). Accumulating litter may negatively affect seed germination ( Bruna 1999) and seedling survival (Scariot 2001) and makes forest edges vulnerable to surface fires during droughts ( Cochrane et al. 1999).
Figure 3. Penetration distances of different edge effects into the forest remnants of the Biological Dynamics of Forest Fragments Project (data sources: 1, Lewis 1998; 2, Laurance et al. 1998b, 2000; 3, Lovejoy et al. 1986; 4, Carvalho & Vasconcelos 1999; 5, Didham 1997b; 6, Didham 1997a; 7, Camargo & Kapos 1995; 8, Laurance et al. 1998c; 9, Camargo 1993; 10, Malcolm 1994; 11, Kapos et al. 1993; 12, Kapos 1989; 13, Sizer & Tanner 1999; 14, Bierregaard et al. 1992; 15, R. K. Didham, unpublished data).
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One of the most striking edge effects is a sharp increase in rates of tree mortality and damage ( Ferreira & Laurance 1997; Laurance et al. 1998b). When an edge is created, some trees simply drop their leaves and die standing ( Lovejoy et al. 1986), apparently because abrupt changes in light, temperature, or moisture exceed their physiological tolerances. Other trees are snapped or felled by winds, which accelerate over cleared land and then strike forest edges, creating strong turbulence ( Laurance 1997 ). Finally, lianas (woody vines)—important structural parasites that reduce tree growth, survival, and reproduction—increase markedly near edges and may further elevate tree mortality ( Laurance et al. 2001b).
The abrupt rise in tree mortality fundamentally alters canopy-gap dynamics ( Ferreira & Laurance 1997; Laurance et al. 1998b), which can influence forest structure, composition, and diversity ( Brokaw 1985; Hubbell & Foster 1986; Denslow 1987 ). Smaller fragments often become hyperdisturbed, leading to progressive changes in floristic composition. New trees regenerating within 100 m of forest edges are significantly biased toward disturbance-loving pioneer and secondary species and against old-growth, forest-interior species ( Laurance et al. 1998c). The pioneer tree Cecropia sciadophylla, for example, has increased 33-fold in density since the BDFFP fragments were isolated ( Laurance et al. 2001b).
Some animals respond positively to edges. Certain termites, leafhoppers, scale insects, aphids, aphid-tending ants ( Fowler et al. 1993), and light-loving butterflies ( Brown & Hutchings 1997 ) increase near edges. Birds that forage in treefall gaps, such as some arboreal insectivores, hummingbirds, and habitat generalists, often become abundant near edges ( Bierregaard & Lovejoy 1989; Bierregaard 1990; Stouffer & Bierregaard 1995a, 1995b). Frugivorous bats increase in number near edges, probably because such areas have higher fruit abundance than forest interiors ( Kalko 1998). The insectivorous marsupial Metachirus nudicaudatus apparently increases in fragments because dead trees and ground cover, which provide favored foraging microhabitats, increase near edges ( Malcolm 1991).
Many other animal species respond negatively to edges and thus are likely to be vulnerable to fragmentation. Numerous flies, bees, wasps ( Fowler et al. 1993), beetles ( Didham et al. 1998a, 1998b), ants (Carvalho & Vasconcelos 1999), and butterflies ( Brown & Hutchings 1997 ) decline in abundance near edges. A number of insectivorous understory birds avoid edges (Quintela 1985), particularly solitary species, obligatory ant followers, and those that forage in mixed-species flocks (S. G. Laurance 2000). Some frog species use breeding habitat independent of its proximity to edges (Gascon 1993), whereas others may be edge avoiders (e.g., Pearman 1997 .
Figure 4. Changes in the composition of leaf-litter beetle assemblages as a function of distance from forest edge. For each sample, the mean percentage similarity (± SE ) to forest-interior samples (approximately 5000 m from edge) is shown. Dotted line shows the average background level of similarity among different forest-interior samples. The regression was highly significant ( R2 = 23.2%, p = 0.005) (after Didham 1997b.
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Another important finding is that rapid changes in the physical permeability of edges occur in the initial years after fragmentation. Newly created edges are structurally open and thereby permeable to lateral light penetration and hot, dry winds from adjoining cattle pastures. After a few years, these microclimatic alterations decline in intensity as edges are partially sealed by a profusion of second growth ( Kapos 1989; Camargo & Kapos 1995; Kapos et al. 1997 ). Desiccation-related plant mortality may also decline over time because of an increase in drought-tolerant species or physiological acclimation of plants near edges. Unlike microclimatic changes, however, wind damage to forests is unlikely to lessen as fragment edges become older and less permeable, because downwind turbulence usually increases as edge permeability is reduced (Savill 1983). In terms of edge permeability, three phases of edge evolution can be identified: initial isolation, edge-closure, and post-closure.
In the initial isolation phase (<1 year after edge formation), the gradient between the forest interior and edge is steepest, with hot, dry conditions and increased light and wind penetrating into the fragment. There is a dramatic pulse in tree mortality; many trees die standing ( Laurance et al. 1998b). Leaf-litter accumulates as drought-stressed trees shed leaves to conserve water, or replace shade-adapted leaves with sun-adapted leaves ( Didham 1998). Abundances of many animals fluctuate sharply. The most sensitive species decline almost immediately.
During the edge-closure phase (1–5 years after edge formation), a proliferation of secondary vegetation and lateral branching by edge trees progressively seals the edge. Edge gradients in microclimate become more complex but do not disappear entirely ( Kapos et al. 1997 ). Plants near the edge die or become physiologically acclimated to edge conditions. Treefall gaps proliferate within the first 100–300 m of edges, partly as a result of increased windthrow. Additional animal species disappear from fragments. Edge-favoring plants and animals sometimes increase dramatically in abundance ( Laurance & Bierregaard 1997 ).
In the post-closure phase ( >5 years after edge formation), edge-related changes are largely stabilized, although external land-use changes (such as fires or the development of adjoining regrowth) can disrupt this equilibrium (Gascon et al. 2000). Windthrow remains elevated near edges, despite the fact that the edge is partially sealed by secondary growth. Proliferating lianas near edges probably contribute to increased tree mortality. Turnover rates of trees increase near edges because of elevated tree mortality and recruitment and increasing numbers of short-lived pioneer species. Pioneer plants replace leaves rapidly, contributing to the accumulation of leaf litter near edges. Although edge closure occurs relatively quickly in tropical rainforests because of rapid plant growth, edges are still more dynamic and vulnerable to climatic vicissitudes than are forest interiors ( Laurance et al. 2002).
Successional changes in the BDFFP landscape reveal that surrounding matrix habitats strongly influence fragment ecology. For example, fragments surrounded by regrowth forest 5–10 m tall experienced less-intensive changes in microclimate ( Didham & Lawton 1999) and had lower edge-related tree mortality ( Mesquita et al. 1999) than did similar fragments adjoined by cattle pastures. Edge avoidance by mixed-species bird flocks was also reduced when fragments were surrounded by regrowth rather than cattle pastures (Stouffer & Bierregaard 1995b).
Figure 5. Changes in capture rates (mean ± SE captures/1000 mist-net hours) over time for two guilds of rainforest birds in 10-ha forest fragments that gradually became surrounded by Vismia-dominated and Cecropia-dominated regrowth (after Stouffer & Bierregaard 1995b.
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Some matrix habitats are more suitable for rainforest fauna than others. Regrowth dominated by Cecropia trees, which tends to be tall and floristically diverse with a relatively closed canopy ( Williamson et al. 1998), is used by more rainforest bird, frog, and ant species than is more open Vismia-dominated regrowth (Stouffer & Bierregaard 1995b; Tocher 1998; Borges & Stouffer 1999; Vasconcelos 1999; Stouffer & Borges 2001). Virtually any kind of regrowth is better than cattle pastures; for example, forest-dependent dung and carrion beetles are far more likely to cross a matrix of regrowth than one that has been clearcut ( Klein 1989). In general, the more closely the matrix approximates the structure and microclimate of primary forest, the more likely that fragmentation-sensitive species can use it.
The matrix can have both positive and negative effects on fragmented populations. Because game in farmland mosaics is often intensively hunted ( Robinson & Redford 1991; Rabinowitz 2000), the matrix can become a population sink for exploited species ( Woodroffe & Ginsberg 1998). The matrix can also be a source of fruits, flowers, and other resources that help maintain fragment populations ( Bierregaard et al. 1992; Brown & Hutchings 1997 ). Finally, the matrix supports many nonforest species; for example, from 8% to 25% of all frog, bird, small mammal, and ant species in the BDFFP study area are associated exclusively with the matrix (Gascon et al. 1999).
A key finding of the BDFFP is that even small clearings are barriers for many rainforest organisms. Many terrestrial insectivorous birds have disappeared from the BDFFP fragments and failed to recolonize even those isolated by only 80 m, despite a proliferation of regrowth around many fragments (Stratford & Stouffer 1999). Clearings of just 15–100 m are insurmountable barriers for certain dung and carrion beetles ( Klein 1989), euglossine bees ( Powell & Powell 1987 ), and arboreal mammals ( Malcolm 1991; Gilbert & Setz 2001). Peccaries (Offerman et al. 1995) and many insect-gleaning bats ( Kalko 1998) are also highly reluctant to enter clearings. Even an unpaved road only 30–40 m wide dramatically alters the community structure of understory birds and inhibits the movements of many species (S. G. Laurance 2000).
Some species will cross small clearings but are inhibited by larger expanses of degraded land. Woodcreepers ( Dendrocolaptidae) were induced by translocation to move between the BDFFP fragments and nearby areas (80–150 m) of mainland forest ( Harper 1989), but they have disappeared from slightly more isolated areas such as Barro Colorado Island in Panama ( Robinson 1999). Large predators such as jaguars (Panthera onca) and pumas (Puma concolor) traverse pastures and regrowth in the BDFFP study area but would likely avoid these areas if hunters were present or human density was higher ( Rabinowitz 2000). Some ant-following birds (Pithys albifrons, Gymnopithys rufigula, Dendrocincla merula) translocated into forest fragments where army ants are absent will cross clearings of 100–320 m to return to primary forest ( Lovejoy et al. 1986; Harper 1989), although clearings of only 100 m preclude such movement under normal circumstances ( Bierregaard & Lovejoy 1989; Stouffer & Bierregaard 1995b).
Amazonian animals avoid clearings for many reasons. Most understory species have had little reason to traverse clearings in their evolutionary history, so the avoidance of such areas is probably an innate response (Greenberg 1989). Other species are constrained by morphology or physiology; strictly arboreal species, for instance, will find even a small pasture an impenetrable barrier. Specialized habitat needs probably limit yet others; for example, rainforest birds that flip over dead leaves in order to find insects, such as the antbird Myrmornis torquata, probably cannot manipulate the large leaves of Cecropia trees, and therefore avoid Cecropia-dominated regrowth (Stratford & Stouffer 1999). A final limit on interfragment movements, at least in Amazonian birds, is that few species are migratory. In temperate forests, even truly isolated fragments can be colonized in the breeding season by migratory species (e.g., Blake & Karr 1987 , but Amazonian birds appear less likely to do so.