InTech uses cookies to offer you the best online experience. By continuing to use our site, you agree to our Privacy Policy.

Environmental Sciences » "Tropical Forests", book edited by Padmini Sudarshana, Madhugiri Nageswara-Rao and Jaya R. Soneji, ISBN 978-953-51-0255-7, Published: March 14, 2012 under CC BY 3.0 license. © The Author(s).

Chapter 10

Human-Altered Mesoherbivore Densities and Cascading Effects on Plant and Animal Communities in Fragmented Tropical Forests

By Nicole L. Michel and Thomas W. Sherry
DOI: 10.5772/30166

Article top


Diagrammatic representation of the potential cascading consequences of apex predator loss via mesopredator and mesoherbivore release.
Figure 1. Diagrammatic representation of the potential cascading consequences of apex predator loss via mesopredator and mesoherbivore release.
Collared peccary (Pecari tajacu; top left), Central American Agouti (Dasyprocta punctata; bottom left), and a carpet of undispersed Attalea butyraceae fruits at a heavily hunted site in Parque Nacional Camino de Cruces, Panama (all photos by Nicole L. Michel).
Figure 2. Collared peccary (Pecari tajacu; top left), Central American Agouti (Dasyprocta punctata; bottom left), and a carpet of undispersed Attalea butyraceae fruits at a heavily hunted site in Parque Nacional Camino de Cruces, Panama (all photos by Nicole L. Michel).
Understory vegetation density at La Selva Biological Station, Costa Rica, is lower in areas exposed to collared peccaries (left) than within experimental peccary exclosures (right; photos by Nicole L. Michel).
Figure 3. Understory vegetation density at La Selva Biological Station, Costa Rica, is lower in areas exposed to collared peccaries (left) than within experimental peccary exclosures (right; photos by Nicole L. Michel).

Human-Altered Mesoherbivore Densities and Cascading Effects on Plant and Animal Communities in Fragmented Tropical Forests

Nicole L. Michel1 and Thomas W. Sherry

1. Introduction

Rainforest loss and fragmentation are proceeding at an alarming rate, and having demonstrable consequences for the relevant plant and animal communities. Between 1984 and 1990 6.5 million hectares of humid tropical rainforest were lost annually worldwide (Hansen & DeFries, 2004). This rate increased to 7.3 million hectares annually between 1990-1997, due largely to accelerating deforestation rates in Asia. Though the pantropical deforestation rate slowed to 5.5 million hectares annually between 2000-2005 due to slowing in much of Asia and Latin America, deforestation continues to increase in Brazil (Hansen et al., 2008). As of 2005, half to two-thirds of humid tropical regions have <50% tree cover, with an additional 20% undergoing selective logging between 2000 and 2005 (Asner et al., 2009; Table 1).

Much of the remaining original forest persists as small, isolated fragments. The highest rates of forest fragmentation are found in North and South America, respectively (Riitters et al., 2000). In the Amazon, the amount of forest in fragments or within 1km of forest edge exceeded the extant forest area by 150% (Skole & Tucker, 1993), and between 1999 and 2002 over 30,000 km of new forest edge was created there annually (Broadbent et al., 2008). Asia and Africa currently have the lowest levels of tropical rainforest fragmentation, although with the rapidly accelerating Southeast Asian deforestation rates this is likely to change (Sodhi et al., 2010a).

Such loss and fragmentation of tropical forest, coupled with other global change phenomena, have profound and diverse effects on the remaining forest fragments. The very complexity of these synergistic effects is only beginning to be documented and comprehended. Recent studies show that tropical forest fragmentation disproportionately affects the largest vertebrates (Henle et al., 2004; Stork et al., 2009; Wilkie et al., 2011). Large predators experience the strongest fragmentation effects, with cascading consequences for the small- and intermediate-sized herbivores regulated by vertebrate predators (Duffy, 2003; Purvis et al., 2000; Redford, 1992). Altered populations of these herbivores, which we term “mesoherbivores” (after Soulé et al.’s (1988) term “mesopredator” referring to small- and intermediate-sized predators), in turn cascade down to affect plant growth and recruitment via altered seed predation and dispersal (Duffy, 2003; Redford, 1992).

Annual deforestation rate
(x106 hectares)
Selective logging3 (%)
1984-19901 1990-19971 2000-20052 2000s
Latin America4.314.283.3117.2%
Tropical Asia1.812.571.8819.2%
Tropical Africa0.430.370.3027.2%
1 Data from Hansen & DeFries, 20042 Data from Hansen et al., 20083 Percent of regional forest area experiencing selective logging. Data from Asner et al., 2009

Table 1.

Annual deforestation rate and selective logging extent in humid tropical forests.

Herein, we review both the direct and indirect effects of fragmentation on tropical forest communities. We review the literature on vertebrate herbivores both because few reviews are available for tropical forests and the pervasiveness and diversity of their ecological effects remain largely undocumented. We begin by reviewing the substantial tropical literature on human overhunting of mesoherbivores and the consequences this has for tropical forest plant communities, in an effort to understand the magnitude of the effects of human-perturbed mesoherbivore populations on tropical forest plant communities.

Ultimately, however, we are particularly interested in the poorly-studied phenomenon wherein loss of vertebrate predators without compensatory human hunting may result in dramatic increases in mesoherbivore populations, which we call “mesoherbivore release.” This phenomenon has been observed in multiple temperate systems, as well as tropical savanna and grassland systems (see review in Salo et al., 2010), yet it is poorly studied in tropical forests. This section of the review will synthesize for the first time the sparse and scattered literature involving putative tropical examples of mesoherbivore release, making the case that the cascading consequences of increased mesoherbivore abundance can be as widespread and ecologically destructive as those resulting from mesoherbivore decline. Finally, we address the most pressing conservation and management implications of the research on perturbed mesoherbivore populations, both decline and release. We also identify topics in need of further investigation, in terms of both ecology and conservation.

2. Direct effects of fragmentation

Predictably, rainforest loss and fragmentation are dramatically altering tropical forests, both directly and indirectly. Loss of forest area and, to a lesser degree fragmentation, directly drive population decline and extinction of myriad plant, invertebrate, and vertebrate species pan-tropically (Beier et al., 2002; Fahrig, 1997, 2002, 2003; Laurance, 1999; Laurance et al., 2011; Michalski & Peres, 2007; Newmark, 1991; Sodhi et al., 2008, 2010b; Yaacobi et al., 2007). Pervasive edge effects further alter the microclimate and vegetation structure of remnant fragments, affecting still more species (Fletcher et al., 2007; Laurance, 2000; Laurance et al., 2002, 2011; Lindell et al., 2007; Manu et al., 2007; Norris et al., 2008; Pardini, 2004; Tabarelli et al., 2008). Synergistic interactions between fragmentation and other global change drivers, notably climate change with its concomitant increased drought and fire frequency, and exploitation of wildlife, further exacerbate loss and degradation of remnant tropical rainforest and their plant and animal communities (Brooks et al., 2008; Ewers & Didham, 2006; Laurance & Useche, 2009; Laurance & Williamson, 2001; Tabarelli et al., 2008). Roads and other infrastructure also contribute to accelerating declines of mammals, birds, and other organisms in both fragments and intact forests (Benítez-López et al., 2010), e.g., by increasing hunting pressure (Peres, 2001).

Even if a species persists temporarily in fragmented forest, it is likely to experience reduced genetic diversity, inbreeding depression, reduced adaptive potential, and accumulation of deleterious mutations (Keyghobadi, 2007). Inbreeding depression and reduced genetic diversity combine with dispersal limitation, competitive disadvantages, fragment area and isolation effects, and other species- and fragment-level traits to create an “extinction debt,” wherein extinctions proceed for decades post-fragmentation (Brooks et al., 1999; Ewers & Didham, 2006; Ferraz et al., 2003; Laurance et al., 2008; Metzger et al., 2009; Tilman et al., 1994), if not at the rate once thought (He & Hubbell, 2011). These high short- and long-term extinction rates, combined with the rapid and accelerating loss and fragmentation of remnant tropical forest, have led many scientists to warn of a tropical biodiversity crisis resulting in a potential mass wave of extinctions rivaling historical extinction events, resulting in an era of novel secondary tropical forests (Bradshaw et al., 2009; Brooks et al., 2008; Dirzo & Raven, 2003; Gardner et al., 2007; Laurance, 1999, 2006; Lugo, 2009; but see Wright & Muller-Landau, 2006a,b).

Species declines following rainforest loss and fragmentation are highly non-random. Fragmentation-sensitive species typically share a common suite of traits, including small population size/rarity, large body size, and specializations (see Table 2). Many of these traits (e.g., “slow” life-histories, dietary and habitat specialization) are unique to, or relatively prevalent in tropical species, thus rendering many paradigms (e.g., edge effects) and conservation strategies developed for temperate and boreal forests largely irrelevant when developing conservation plans for tropical forests (Stratford & Robinson, 2005).

Common traits of fragmentation-sensitive species
Small population size / rarityHigh sociality
Large body sizeDisturbance- and competition- sensitivity
High trophic positionSpecialized diet (e.g., insectivorous and
large frugivorous birds)
Fluctuating population dynamicsSpecialized habitat use (especially forest
“Slow” life-histories (low
fecundity, high annual survival)
Location near edge of altitudinal or
biogeographical range
Low dispersal capabilityInvolved in mutualistic interaction

Tropical forests also tend to harbor diverse, pervasive mutualistic interactions, notably plant-animal interactions (Terborgh & Feeley, 2010). Between 70 and 90% of tropical trees rely on animals for seed dispersal (Muller-Landau & Hardesty, 2005), and >95% of lowland tropical trees are animal-pollinated (Bawa et al., 1985). Thus, habitat loss and fragmentation also alter many important plant-animal interactions, including pollination, seed dispersal, seed predation, and herbivory (Herrera et al., 2011; Laurance, 2005). Some of these altered interactions result from direct effects of habitat loss and fragmentation on plants and animals involved in mutualisms, e.g., extirpations of forest-interior butterflies following loss of their host plants (Brown & Hutchings, 1997; Koh et al., 2004). However, in many cases plant-animal interactions change in response to indirect effects of other animals declining higher in the food chain, in what is known as trophic cascades.

3. Indirect effects of fragmentation: Trophic cascades

Fragmentation effects are particularly strong on large predators, due to their high trophic position, “slow” life-histories that preclude rapid population response to disturbances, large home ranges, and other traits characteristic of fragmentation-sensitive species. Apex predators such as jaguars, pumas, tigers, leopards, large raptors, and large snakes are amongst the first species to disappear from tropical rainforest fragments (Duffy, 2003; Pimm et al., 1988; Purvis et al., 2000; Ray et al., 2005; Redford, 1992; Terborgh, 1992). Moreover, the cascading consequences resulting from apex predator loss can dramatically affect ecosystem structure and function in ways we are just beginning to understand, and thus far exceed the effects of loss of species from lower trophic levels (Dobson et al., 2006; Duffy, 2003; Estes et al., 2011; Schmitz et al., 2010; Terborgh et al., 1999).

Trophic cascades, wherein perturbations of apex predator populations cascade down to affect lower consumer (e.g., herbivore) and producer (i.e., plant) levels (Paine, 1980), were once thought not to occur in tropical forests as a result of their high species diversity and high intraguild predation, leading to functional redundancy and weak links between individual predator and prey species (Polis & Holt, 1992; Polis & Strong, 1996; Shurin et al., 2002; Strong, 1992; Van Bael et al., 2003; Vance-Chalcraft et al., 2007). Terborgh (1992) first presented evidence suggesting a carnivore (jaguar, Panthera onca; puma, Puma concolor) – large seed predator (peccary, Pecari spp.; paca, Cuniculus spp.; agouti, Dasyprocta spp.) – large-seeded tree (Dipteryx, Protium) trophic cascade at Barro Colorado Island, Panama. Three years later, Dial and Roughgarden (1995) published one of the first experimental studies of trophic cascades in tropical rainforest, showing that insectivorous Anolis lizards limit herbivorous insects and in turn, herbivory on canopy trees. Shortly thereafter, Letourneau and Dyer (1998) were the first to experimentally show a four-level (beetle – ant – herbivore – plant) trophic cascade in tropical rainforest understory. Within the next few years, a flurry of exclosure experiments demonstrated that insectivorous birds and bats limit arthropod herbivores and herbivory in rain forest canopy and understory (review by Van Bael et al., 2008; Kalka et al., 2008; Michel et al., in review; Williams-Guillén et al., 2008).

Additionally, a number of experimental and observational studies have shown effects of mesopredator release (reviews by Brashares et al., 2010; Prugh et al., 2009). Mesopredator release is a phenomenon wherein small to mid-sized predators increase in abundance following declines of their own predators, resulting in declines in their prey, which are typically small herbivores and insectivores, especially birds and small rodents (Fig. 1; Soulé et al. 1988, Crooks and Soulé 1999). Though first documented in fragmented temperate habitats, Laurance (1994) noted increases in rodents - including one species, Uromys, known


Figure 1.

Diagrammatic representation of the potential cascading consequences of apex predator loss via mesopredator and mesoherbivore release.

to depredate bird nests and consume small vertebrates - in Australian rainforest fragments missing large predators. Increases in other small, generalist predators (e.g., barn owls, red-bellied blacksnakes, and white-tailed rats) were also observed in fragments without large, specialist predators (Laurance, 1997). Elsewhere in Australia, declines and extirpations of dingoes, an apex predator, resulted in continent-wide collapse of native marsupials due to release of invasive house cats and red foxes from predation (Johnson et al., 2007). On Barro Colorado Island, Panama, high avian nest predation has been attributed in part to increased small mammalian nest predators such as white-nosed coatimundi (Nasua narica), white-faced capuchin monkeys (Cebus capucinus), and opossums following isolation from the mainland, and subsequent loss of large carnivores, when the Panama Canal was built (Loiselle & Hoppes, 1983; Sieving, 1992; Wright et al., 1994). On the Lago Guri islands in Venezuela, former hilltops isolated from nearby mainland by a hydro-electric reservoir, anomalously low bird densities were associated with abundant olive capuchin monkeys (Cebus olivaceus), which depredated all artificial nests (Terborgh et al., 1997). Olive baboons (Papio anubis) also dramatically increased in Ghana following steep declines in lions (Pantera leo) and leopards (Pantera pardus), negatively impacting smaller ungulates, primates, rodents, and birds, as well as human livestock, pets, and crops (Brashares et al., 2010).

In summary, strong trophic cascades, resulting in increases in arthropod herbivores and mesopredators, have been repeatedly demonstrated to occur in tropical rainforest despite the functional redundancy and potentially weak links between predators and prey (Terborgh & Feeley, 2010). However, very few experimental studies have focused on the potential cascading consequences of loss of large terrestrial predators on vertebrate herbivores (i.e., of mesoherbivore release), and subsequent plant community effects, despite the fact that large predators have been shown to effectively limit vertebrate herbivores in a variety of habitats worldwide (Estes et al., 2011; Salo et al., 2010). This is likely due, in large part, to logistical, methodological, and financial constraints, including the large scale of impacts and the long generation times of vertebrate herbivores and the trees they frequently impact; responses may not be apparent for years or even decades following perturbations to predator and herbivore populations (Terborgh & Estes, 2010). Furthermore, in many cases, apex predator populations were decimated decades or centuries prior to the development of the theory of trophic cascades (Estes et al., 2011). Moreover, across much of the tropics, the lost ecological services attributable to prey regulation (Dobson et al., 2006, Schmitz et al., 2010) once provided by predators such as jaguars, leopards, and tigers have been compensated - and often overcompensated - for by a new apex predator: human hunters.

4. Humans, herbivores, and tropical tree germination and recruitment

By far the majority of studies documenting cascading effects of altered vertebrate herbivore densities on rainforest plant communities have focused on consequences of extirpated or greatly reduced herbivore populations. Herbivores, especially larger herbivores, often experience declines due to simple area effects of habitat loss and fragmentation (MacArthur & Wilson, 1967; e.g., Dalecky et al., 2002; Laurance et al., 2011), as well as edge effects (Norris et al., 2008; Restrepo et al., 1999), altered vegetation structure, local climate (e.g., droughts), and/or microclimate within fragments (Chiarello, 1999; Fleury & Galetti, 2006; Laurance, 1994; Laurance et al., 2008; Laurance & Williamson, 2001). But tropical forests are rarely impacted by habitat loss and fragmentation alone. Many anthropogenic factors, including logging, fires, introduction of invasive species or disease, and hunting, interact synergistically to exacerbate fragmentation effects on tropical forest residents (Brooks et al., 2008; Laurance, 2005, 2008; Laurance & Useche, 2009; Wright 2005, 2010).

Synergistic effects of fragmentation and hunting are particularly strong, as fragmentation - also commonly associated with increased road-building - both a) allows hunters easier access to prey species and to markets, and b) subdivides remnant forest into patches below the minimum area requirement to support sustainable hunting (Peres, 2001). As a result, hunting is having dramatic effects on vertebrates, including herbivores and the plants dependent upon them for pollination and dispersal, resulting in what has come to be known as the “bush meat crisis” (Milner-Gulland et al., 2003; Wright et al., 2007a). Humans have been implicated in extinctions of large vertebrates as far back as 46,000 years ago, when extinctions of Australia’s megafauna coincided with human arrival (Roberts et al., 2001). Similarly, humans are partially, if not predominantly, responsible for the North American megafauna extinction, including loss of herbivorous mammoths and mastodons, over 12,000 years ago (Alroy, 2001; Johnson, 2002). The impact of human hunters on large herbivores have only increased as the human population grew exponentially over the last 2,000-3,000 years, and also as it developed modern hunting techniques and weapons, including firearms and traps (Corlett, 2007). Their relative abundance (compared to cats and other apex predators) often makes vertebrate herbivores a prime target for human hunting.

Today human hunting is decimating herbivore populations pan-tropically in intact as well as fragmented forest. In the Congo, 60% of mammals are unsustainably harvested, including 93% of herbivorous ungulates, suggesting catastrophic losses of herbivores and their dependent plants in the near future (Fa et al., 2002). While Fa et al. (2002) estimated that only 20% of Amazonian mammals are unsustainably hunted, Peres and Palacios (2007), using slightly different methods, found that 22 of 30 large mammals, birds, and reptiles significantly declined under high hunting pressure, at rates of up to 74.8%. Large-bodied vertebrates and seed dispersers experienced greater declines than seed predators and browsers. As a result, hunted Amazonian forests will likely experience altered plant communities as large-seeded trees and lianas are no longer able to escape and recruit away from the parent tree (Peres & Palacios, 2007). Indeed, tree species richness is already 55% lower, and density of large-seeded, primate-dispersed trees is 60% lower, in hunted sites near Manu National Park, Peru, where large primates were exterminated and midsize primate populations reduced 80% by hunters (Nuñez-Iturri & Howe, 2007). Another study from the same hunted site found 50-60% lower sapling densities, and declines amongst 72% of tree species, particularly among large-seeded species (Terborgh et al., 2008). Within the Biological Dynamics of Forest Fragments Project (BDFFP) reserves, the large-seeded, mammal-dispersed Duckeodendron cestroides experienced a 300% reduction in seed dispersal, 500% reduction in maximum dispersal distance, and 5000% reduction in the number of seeds dispersed 10m beyond the crown in hunted fragments relative to continuous forest (Cramer et al., 2007). Overall, up to one third of Amazonian plants may suffer failed dispersal due to losses of vertebrate seed dispersers (da Silva & Tabarelli, 2000).

Similarly, in the Atlantic coastal forest of Brazil, large-seeded Astrocaryum aculeatissimum palms in fragments with low agouti density faced a collapse in seed dispersal, as agoutis disperse more seeds than they predate, and smaller rodents are unable to compensate for the agouti’s absence (Donatti et al., 2009). In southern Mexico, fragments <30ha lack most to all large frugivores, and as a result dispersal and recruitment of large-seeded species declined ~50% (Melo et al., 2010). Large frugivorous seed dispersers have also declined in Australian rainforest fragments, affecting 12% of all plant species, particularly large-seeded species (Moran et al., 2009). In Asia, commercial hunting threatens mass extinctions of mammals greater than 1-2 kg, particularly the major seed dispersers – elephants, tapirs, deer, primates, and large birds and bats, all of which face greater hunting pressure than seed predators. As a result, future Asian forests are likely to be dominated by small-fruited and –seeded, fast-growing trees at the expense of large-seeded species (Corlett, 2007).

While all the studies cited above found declines in large-seeded tree species in hunted fragments due to loss of seed dispersers, a number of studies have found the opposite: large-seeded species increase in abundance and diversity due to the loss of hunted vertebrate seed predators. In Panama, hunters favor large-seeded tree species by removing seed predators (e.g., Central American agoutis, Dasyprocta punctata, and collared peccaries, Pecari tajacu), and thereby increasing seedling survival (Wright et al., 2007b), resulting in 300-500% higher seedling density of two large-seeded palms at heavily hunted sites (Wright et al., 2000). Lianas also benefit from hunting, as most liana seeds are wind-dispersed, then escape competition from small-seeded species that have lost their seed dispersers (Wright et al., 2007b). This effect is particularly pronounced in Los Tuxtlas, Mexico, where thick monospecific carpets of large-seeded seedlings result from heavy rodent predation of small-seeds (Dirzo et al., 2007). In northeastern Costa Rica, large-seeded Dipteryx panamensis escaped predation in fragments due to heavy hunting of squirrels (Sciurus spp.), agoutis, and peccaries, resulting in higher seedling densities (Hanson & Brunsfeld, 2006). However, even where seed and seedling survival is increased due to the loss of seed predators, the concurrent loss of seed dispersers often results in monospecific seed and seedling carpets clustered underneath conspecific parent trees, eventually resulting in lower tree species diversity (Figure 2; Wright et al., 2000; Wright & Duber, 2001).


Figure 2.

Collared peccary (Pecari tajacu; top left), Central American Agouti (Dasyprocta punctata; bottom left), and a carpet of undispersed Attalea butyraceae fruits at a heavily hunted site in Parque Nacional Camino de Cruces, Panama (all photos by Nicole L. Michel).

Relative seed dispersal and predation rates between hunted fragments and protected forest tend to be highly plant species-specific (Guariguata et al., 2000, 2002; Wright et al., 2000). Regardless of which species are impacted or favored by increased hunting pressure on seed dispersers and predators, it is clear that the loss of large herbivores and frugivores is having dramatic effects on density and diversity of the remnant plant communities (Wright, 2010; Wright et al., 2007a). There is some hope, however, that negative density dependence may allow once declining plant species to rebound as the forest is protected, and once seed disperser and predator populations to return to their historical levels (Muller-Landau, 2007).

5. Mesoherbivore release

The previous section focused on the consequences of excessive human predation on midsize and large herbivores and frugivores, the so-called mesoherbivores. However, large non-human predators also effectively limit vertebrate herbivores in diverse natural systems (Fig. 1; Estes et al. 2011; Salo et al., 2010). What happens when large non-human predators are removed in the absence of human hunting? Terborgh (1992) first suggested that the loss of large carnivores (jaguars, pumas) from Barro Colorado Island, Panama could explain the seemingly higher densities of mesoherbivores such as peccaries, pacas, and agoutis relative to Cocha Cashu, Peru. Yet, very few studies have since followed up with experimental or observational studies documenting increased mesoherbivore abundance in tropical forests following losses of large predators. The few studies that do exist, however, suggest that mesoherbivore release may have consequences just as catastrophic as their decline.

The best-known and most clear-cut cases of mesoherbivore release occur at temperate latitudes. In North America, white-tailed (Odocoileus virginianus) and mule deer (O. hemionus) populations have exploded following the disappearance of wolves and mountain lions, with catastrophic effects on plant cover and diversity, nutrient and carbon cycling, and forest successional rates, with rebounding effects on insects, birds, and other mammals (see reviews by Côté et al., 2004; McShea et al., 1997). In Yellowstone National Park, in the western United States, elk (Cervus canadensis) populations increased and altered their foraging behavior when wolves (Canis lupus) were extirpated, causing collapses in aspen and cottonwood (Populus spp.) recruitment that did not recover until wolves were reintroduced (Beschta, 2005; Halofsky & Ripple, 2008a,b; Ripple & Larsen, 2000). Less well-known in the literature is the eradication of dholes (wild dogs; Cuon alpinus) in Bhutan that allowed wild pig (Sus scrofa) densities to increase thirty-fold, resulting in extensive crop losses and even direct attacks on humans and livestock (Wang et al., 2006; Wangchuk, 2004).

In tropical forests, mesoherbivore release was first suggested at Barro Colorado Island (BCI), Panama. Terborgh (1992) compared mesoherbivore densities at BCI, with ocelots persisting but not jaguars and pumas, versus Cocha Cashu (CC), Peru, with all large cats. He reported mesoherbivore densities 8 to 20 times greater on BCI than CC, and predicted that this could have a detrimental impact on large-seeded tree species via increased seed predation. However, this result is controversial, as Wright et al. (1994) pointed out multiple problems with both the data and its proposed implications. Mesoherbivore densities at BCI may have been overestimated due to human habituation, and densities at CC may be anomalously low due to seasonal flooding; indeed other Neotropical sites with large predators have mesoherbivore densities similar to BCI. Further, predation on and recruitment of the large-seeded Dipteryx panamensis, commonly predated by agoutis, was similar at BCI and CC despite an order of magnitude difference in agouti abundance between the sites (Terborgh & Wright, 1994). Seed survival of three large-seeded species was also similar at BCI and the nearby mainland after poaching was greatly reduced, and seedling herbivory was lower on BCI (Asquith et al., 1997). Additionally, calculations of total herbivore consumption rates by predators indicates that Manu’s jaguars, pumas, and ocelets do not eat sufficient herbivore biomass to effectively limit their populations (Leigh 1999). This led Wright et al. (1994) to conclude that, in comparison to the effects of hunting-driven meso-herbivore loss, “There is, however, no evidence to support the hypothesis that the relatively subtle increases in abundances that may follow the extirpation of large felids are of similar importance.”

However, release of tropical mesoherbivores from predation does not always result in “relatively subtle increases in abundance,” especially when combined with other factors (e.g., increased food availability) that may amplify mesoherbivore population growth. At Pasoh Forest Reserve, an aseasonal tropical forest in Malaysia have, native wild pig (S. scrofa) densities exploded to an estimated 47/km2 in 1996, due to a combination of lost natural predators (tigers, leopards) and increased food supply provided by nearby oil palm plantations (Ickes, 2001). These densities are one or two orders of magnitude greater than the observed wild pig densities of 0.1 – 4.2/km2 in tropical forest with predators present, and are similar to densities found on Peucang Island, coastal dipterocarp forest with no natural predators (27-32/km2; Ickes, 2001). The hyperabundant pigs had dramatic effects on the natural forest vegetation structure and diversity. Within experimental pig exclosures, the number of seedling recruits increased 3 times, stem density increased by 56%, liana density increased 18%, plant species richness increased by 10%, and height growth increased 52.5% for trees 1-7m tall, though mortality was not affected (Ickes et al., 2001). Female pigs damage an estimated 170,000 saplings/km2 annually by snapping the stems to build woody nests (Ickes et al., 2003). Pigs build 6 nests/ha annually, causing an estimated 29% of observed tree mortality and 43% of sapling mortality and damage (Ickes et al., 2005). Pigs preferentially select saplings of the dominant and ecologically important Dipterocarpaceae for nest building (Ickes et al., 2005). Yet, tree species have differential ability to regenerate following snapping; the dominant dipterocarps have particularly poor regrowth rates (Ickes et al., 2003). The wild pigs are also implicated in Pasoh’s recent invasion by Clidemia hirta (Melastomataceae), an invasive shrub colonizing recent treefall gaps and pig-disturbed soil (Peters, 2001). Thus, the ecological release of feral pigs in Pasoh, due to a combination of artificial food inputs (i.e., oil palm) and lost native predators (Ickes, 2001; Ickes & Williamson, 2000), is having and will continue to have dramatic cascading effects on forest structure and tree community composition.

In Gunung Palung National Park in Borneo, recruitment of the dominant dipterocarp canopy trees collapsed during the 1990s, purportedly due, in part, to release of vertebrate seed predators (Curran et al., 1999). Dipterocarps exhibit mast fruiting during El Niño-Southern Oscillation events, and the large extent and synchronous production allow some seeds to escape predation. However, forest fragmentation due to logging and human-induced wildfires has reduced the extent and intensity of the mast fruiting events; and masting events at Pasoh Forest Reserve in Malaysia also have been highly variable in recent years, for unknown reasons (S.J. Wright, pers. comm.). Nonetheless, vertebrate seed predators (including bearded pigs, Sus barbatus; primates, rodents, and birds) and seed predation increased dramatically in 1998, particularly in logged and degraded land (Curran et al., 1999; Curran & Leighton, 2000). The combination of high predation, logging, and wildfires contributed to a complete collapse in dipterocarp reproduction: not a single seedling was found following the 1998 masting event, compared to 150,000 seedlings/ha following the previous masting event (Curran et al., 1999).

At Lago Guri in Venezuela, herbivorous howler monkeys (Alouatta seniculus), common iguanas (Iguana iguana), and leaf-cutter ants (Acromyrmex spp. and Atta spp.) occur at densities 10-100 times greater than nearby mainland sites (reviewed by Terborgh & Feeley, 2010). As a result, seedling and sapling densities have dramatically decreased due to high mortality and low recruitment, creating “ecological meltdown” (Terborgh et al., 2001, 2006). Mortality and recruitment of both small and large saplings on these islands exceeded comparable rates on the mainland by a factor of 2, primarily due to leaf-cutter ant herbivory (Lopez & Terborgh 2007; Terborgh et al., 2006). Though leaf-cutter ants are clearly not mesoherbivores, this example demonstrates the magnitude of the effects herbivores can have on tropical forest plant communities. Furthermore, hyperabundant mesoherbivores also had species-specific effects on nutrient cycling: iguanas and howler monkeys increased the carbon/nitrogen ratio and, in turn, tree growth, while leaf-cutter ants had the opposite effect (Feeley & Terborgh, 2005). This altered nutrient regime drove a ricocheting bottom-up effect, in which the positive indirect effects of howler monkey density (and concomitant increased nutrient availability) on bird species richness exceeded the negative, direct effects of island area on bird species richness (Feeley & Terborgh, 2008). Indeed, birds maintained territories 3 to 5 times smaller on islands with abundant howler monkeys than on the adjacent mainland (Terborgh et al., 1997). While the herbivore hyperdensities are commonly attributed to the absence of all large and mid-sized predators from the islands (Terborgh et al., 2001, 2006), the very small size of the islands, extensive edge effects, and refuge effect during reservoir inundation also likely contributed (S.J. Wright, pers. comm.).

In each of the previous examples, hyperabundant mesoherbivores were shown to have dramatic, cascading consequences on the rainforest plant communities, yet release from predation may have accounted only in part for the altered herbivore densities. On the contrary, La Selva Biological Station in Costa Rica presents a more clear-cut case of mesoherbivore release. Collared peccaries (Pecari tajacu) have increased from a density of ~0/km2 of trail in the 1970s (T.W. Sherry, pers. obs.) to 14/km2 in 1993 (Torrealba-Suárez & Rau, 1994), and likely higher today (Romero et al., unpubl. data). While some herds forage in neighboring croplands (Torrealba-Suárez & Rau, 1994), peccaries had similar effect sizes (i.e., no block effects) on vegetation density at 5 paired mammal exclosures located far from any station boundary. This suggests that peccary densities are consistent across the station and thus not dependent on food inputs or experiencing a refuge effect, leaving release from predation a likely driver of the current high peccary densities (Michel et al., unpubl. data).

The question of whether collared peccaries at La Selva are over- or hyperabundant is under debate, and accurate current density estimates are greatly needed. However, the most recent available estimate (14/km2 in 1993) is itself over double the mean 6.6/km2 density estimated at 26 unhunted Amazonian sites (Peres & Palacios, 2007), despite some hunting occurring at La Selva (N.L. Michel, pers. obs.). It also exceeds reported densities of 9.6/km2 at BCI, Panama, despite similar area, hunting pressure, and soil nutrient levels to La Selva (Powers et al., 2005; Wright et al., 2000). Known peccary densities elsewhere in Central America are all lower (3-7.5/km2; Michel et al., unpubl. data). Furthermore, effect sizes of mammal (primarily collared peccary) exclosure on vegetation metrics at La Selva exceed effect sizes from exclosures at BCI and Gigante Peninsula, Panama by 200-400%, despite sturdier exclosures in Panama that exclude more terrestrial mammals (Michel et al., unpubl. data). Thus all evidence suggests that La Selva’s collared peccaries occur at unusually high densities that could be considered overabundant (McShea et al., 1997).

High-density peccaries at La Selva consume 98.6% of Mucuna holtonii (liana) seeds on the forest floor (Kuprewicz and García-Robledo, 2010), and reduce seedling densities at La Selva vs. nearby sites with greater hunting pressure (Chazdon et al., in press; Hanson et al., 2006). Peccaries consume stilt roots of Socratea exorrhiza, causing high mortality in these once-abundant trees, effects rarely observed at other Central American sites (Lieberman & Lieberman, 1994; N.L. Michel, pers. obs.). Seedling abundances of 30 focal species in exclosures versus controls were significantly different, presumably due to differences in seed predation pressures and herbivory rates (A. Wendt et al., unpubl. data). Peccaries have also reduced woody and herbaceous stem density, canopy cover, and vine and liana density and cover at La Selva (based on mammal exclosures, Fig. 3). Moreover, six sites from Costa Rica-Panama show liana tangle frequency varies inversely with peccary density, and liana tangles are 133% more abundant within mammal exclosures than paired controls at La Selva. This research suggests that the hyperabundant collared peccaries at La Selva are having dramatic effects on understory, and even canopy, vegetation. This is particularly troubling, given that vines and lianas provide important foraging and nesting substrate for many organisms, including understory insectivorous birds, a guild that has experienced significant declines at both La Selva and BCI over the past 40 years (Sigel et al., 2006, 2010).


Figure 3.

Understory vegetation density at La Selva Biological Station, Costa Rica, is lower in areas exposed to collared peccaries (left) than within experimental peccary exclosures (right; photos by Nicole L. Michel).

6. Conclusion

6.1. Conservation and management implications

It is clear from this review that fragmentation-induced trophic cascades are having catastrophic impacts on tropical forests worldwide. Regardless of whether mesoherbivores are increasing due to the loss of large predators, over-protection in some ecological reserves (e.g., La Selva), and/or food inputs, or decreasing due to human hunting pressure, it is clear that the cascading effects of perturbations in mesoherbivore populations on tropical forest plant communities and the animals reliant on them are catastrophic, diverse, and pervasive. Indeed, trophic cascades and increased mesoherbivore abundances are considered to be as serious threats to tropical biodiversity as climate change (Terborgh & Feeley 2010).

The solution to the problem is clear: large extents of continuous, or at least connected, forest must be protected and carefully managed to keep populations of both apex predators and mesoherbivores within natural ranges (Soulé, 2010). However clear the solution, its implementation is far from simple for many reasons:

  • Large predators have large home ranges and are highly edge-sensitive. In Central America, female jaguars have home range sizes of 10-18.8 km2, whereas male jaguars roam over 28-40km2 (Rabinowitz & Nottingham, 1986; Woodruffe & Ginsberg, 1998). As a result, jaguars require a minimum “critical reserve size” of 69 km2, or 6,900 hectares, to maintain a 50% probability of population persistence (Woodruffe & Ginsberg, 1998). This far exceeds the size of most Central American forest reserves. Tigers, with a female home range size of 16.9 km2, require even more space: 135 km2 is the minimum required to maintain a 50% probability of population persistence (Woodruffe & Ginsberg, 1998). Where mesoherbivores are also hunted by humans and prey is thus scarce, predators are likely to need even more space (Cramshaw & Quigley, 1991).

  • Human phobias associated with large predators and their impacts on domesticated animal herds contribute to resisting reintroduction of predators to areas from which they have been extirpated, and heavily persecuting predators even beyond reserve borders (Soulé, 2010). Conflict with humans along reserve borders is one of the major causes of predator mortality within protected reserves (Woodruffe & Ginsberg, 1998).

  • Many tropical forests are found in countries with limited funds to protect and effectively manage forest reserves (Bruner et al., 2004). The corruption endemic to many national governments in tropical regions further complicates matters (Wright et al., 2007c). Even in Costa Rica and Panama, two of the wealthiest (International Monetary Fund, 2010) and least corrupt (Transparency International, 2010) countries in Central America, poaching is endemic. In Panama, poachers are altering seed dispersal, predation, and recruitment via limitation of mesoherbivores (Wright & Duber, 2001; Wright et al., 2000, 2007b). In Costa Rica, poaching continues to affect vertebrates such as white-lipped peccaries even in the relatively well-protected Corcovado National Park (Carrillo et al., 2000, 2002), and the 260 km2 Tortuguero National Park was often patrolled by fewer than five forest guards as recently as 2005 (N. Michel, pers. obs.).

  • Many people in tropical countries rely upon hunting for either their own subsistence or to trade for food and other necessities (Corlett, 2007). If patrolling forest reserves effectively limits hunting, many neighboring people would need other means of support. This could result in increased slash-and-burn agriculture with its concomitant negative effects on tropical biodiversity (Naughton-Treves et al., 2003).

Many scientists and conservationists argue that simply setting aside land in forest reserves is sufficient to preserve biodiversity, regardless of connectivity or management (e.g., Fahrig, 1997). Yet, others argue that connectivity, i.e., developing biological corridors to connect nearby reserves, is sufficient to preserve biodiversity (e.g., Soulé, 2010). However, if proposed reserves do not already have apex predators, or have degraded habitat unable to support apex predators, or if heavy hunting pressure is limiting mesoherbivore and/or predator populations, the reserve will function in reality as an “Empty Forest” (Redford, 1992; Wilkie et al., 2011). This is a serious problem, as much of the land remaining in tropical regions is either degraded, or in suboptimal habitat, and/or heavily impacted by hunting, and – as discussed above – government funding of reserve protection is often insufficient to control poaching. In order for conservation to succeed, it is imperative that reserves of sufficient size and/or connectivity not only be set aside, but these reserves must also contain sustainable populations of both apex predators (whether extant or reintroduced) and mesoherbivores, i.e., balanced populations to which the natural vegetation and other organisms are adapted. Furthermore, adequate protection needs to be instituted and continued monitoring of predator and herbivore populations, perhaps using a Footprint index (de Thoisy et al., 2010), is crucial in order to prevent destructive trophic cascades and the subsequent loss of tropical biodiversity.

6.2. Future research needs

In terms of future research, we need intensive study of not only what are “normal” and sustainable abundances of mesoherbivores, but also how to maintain these abundances through a combination of vegetation, predator, and/or hunting management. We need better information on all the consequences, both long- and short-term, of human-altered mesoherbivore abundances on native tropical forest communities. There is an urgent need for better information and models on how altered trophic dynamics, especially mesoherbivore abundances, will be affected by other global phenomena, especially climate destabilization. Finally, it is essential to determine the effectiveness of various conservation actions, in order to determine which techniques can best prevent a mass extinction of tropical biodiversity (Brooks et al., 2009).

7. Acknowledgements

The authors thank S. Joseph Wright and Padmini Sudarshana for their helpful reviews of the original manuscript. We thank Walter P. Carson, David and Deborah Clark, Deedra McClearn, Robert Timm, and other La Selva researchers for constructive comments and advice, and thank W.P. Carson as well for access to experimental mammal exclosures on BCI and La Selva. The Explorers Club, National Science Foundation, Organization for Tropical Studies, Smithsonian Tropical Research Institute, and Tulane University all generously supported this research.


1 - J. Alroy, 2001 A Multispecies Overkill Simulation of the End-Pleistocene Megafaunal Mass Extinction. Science, 282 5523 (June 2001), 1893 1896 , 0036-8075
2 - G. P. Asner, T. K. Rudel, T. M. Aide, R. Defries, R. Emerson, 2009 A Contemporary Assessment of Change in Humid Tropical Forests. Conservation Biology, 23 6 (December 2009), 1386 1395 , 0888-8892
3 - K. S. Bawa, S. H. Bullock, D. R. Perry, R. E. Coville, M. H. Grayum, 1985 Reproductive Biology of Tropical Lowland Rain Forest Trees. II. Pollination Systems. American Journal of Botany, 72 3 (March 1985), 346 356 , 0002-9122
4 - P. Beier, M. Van Drielen, B. O. Kankam, 2002 Avifaunal Collapse in West African Forest Fragments. Conservation Biology, 16 4 (August 2002), 1097 1111 , 0888-8892
5 - A. Benítez-López, R. Alkemade, P. A. Verweij, 2010 The Impacts of Roads and Other Infrastructure on Mammal and Bird Populations: A Meta-Analysis. Biological Conservation, 143 6 (June 2010), 1307 1316 , 0006-3207
6 - R. L. Beschta, 2005 Reduced Cottonwood Recruitment Following Extirpation of Wolves in Yellowstone’s Northern Range. Ecology, 86 2 February 2005), 391 403 , 0012-9658
7 - C. J. Bradshaw, N. S. Sodhi, B. W. Brooks, 2009 Tropical Turmoil: A Biodiversity Tragedy in Progress. Frontiers in Ecology and the Environment, 7 2 (March 2009), 79 87 , 1540-9295
8 - J. S. Brashares, L. R. Prugh, C. J. Stoner, C. W. Epps, 2010 Ecological and Conservation Implications of Mesopredator Release, In: Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature, Terborgh, J., & J.A. Estes, (Eds.), 221 240 , Island Press, 978-1-59726-487-7 Washington, DC.
9 - E. Broadbent, G. P. Asner, M. Keller, D. Knapp, P. Oliveira, J. Silva, 2008 Forest Fragmentation and Edge Effects from Deforestation and Selective Logging in the Brazilian Amazon. Biological Conservation, 141 7 (July 2008), 1745 1757 , 0006-3207
10 - B. W. Brooks, N. S. Sodhi, C. J. A. Bradshaw, 2008 Synergisms Among Extinction Drivers Under Global Change. Trends in Ecology and Evolution, 23 8 (August 2008), 453 460 , 0169-5347
11 - T. M. Brooks, S. L. Pimm, J. O. Oyugi, 1999 Time Lag between Deforestation and Bird Extinction in Tropical Forest Fragments. Conservation Biology, 13 5 (October 1999), 1140 1150 , 0888-8892
12 - T. M. Brooks, S. J. Wright, D. Sheil, 2009 Evaluating the Success of Conservation Actions in Safeguarding Tropical Forest Biodiversity. Conservation Biology, 23 6 December 2009), 1448 1457 , 0888-8892
13 - K. S. Jr Brown, R. W. Hutchings, 1997 Disturbance, Fragmentation, and the Dynamics of Diversity in Amazonian Forest Butterflies, In: Tropical Forest Remnants: Ecology, Management, and Conservation of Fragmented Communities, Laurance, W.F., & Bierregaard, R.O., (Eds.), 91 110 , University of Chicago Press, 978-0-22646-899-0 pp. 91-110, Chicago, IL.
14 - A. G. Bruner, R. E. Gullison, A. Balmford, 2004 Financial Costs and Shortfalls of Managing and Expanding Protected-Area Systems in Developing Countries. BioScience, 54 12 (December 2004), 1119 1126 , 0006-3568
15 - E. Carrillo, G. Wong, A. Cuarón, 2000 Monitoring Mammal Populations in Costa Rican Protected Areas under Different Hunting Restrictions. Conservation Biology, 14 6 (December 2000), 1580 1591 , 0888-8892
16 - E. Carrillo, J. C. Saenz, T. K. Fuller, 2002 Movements and Activities of White-lipped Peccaries in Corcovado National Park, Costa Rica. Biological Conservation, 108 3 (December 2002), 317 324 , 0006-3207
17 - R. L. Chazdon, Alvarado. B. Vilchez, S. Letcher, A. Wendt, U. . Sezen, press. In, Effects of Human Activities on Successional Pathways: Case Studies from Lowland Set Forests of Northeastern Costa Rica, In: The Social Life of Forests, Hecht, S., Morrison, K., & Padoch, C., (Eds.), pp. xxx-xxx, University of Chicago Press, Chicago, IL.
18 - A. G. Chiarello, 1999 Effects of Fragmentation of the Atlantic Forest on Mammal Communities in South-Eastern Brazil. Biological Conservation, 89 1 July 1999), 71 82 , 0006-3207
19 - R. T. Corlett, 2007 The Impact of Hunting on the Mammalian Fauna of Tropical Asian Forests. Biotropica, 39 3 (May 2007), 292 303 , 0006-3606
20 - S. D. Côté, T. P. Rooney, J. Tremblay, P. , C. Dussault, D. M. Waller, 2004 Ecological Impacts of Deer Overabundance. Annual Review of Ecology, Evolution, and Systematics, 35 1 December 2004), 113 147 , 0066-4162
21 - J. M. Cramer, R. Mesquita, T. Bentos, B. Moser, G. B. Williamson, 2007 Forest fragmentation reduces seed dispersal of Duckeodendron cestroides, a Central Amazon endemic. Biotropica, 39 6 (November 2007), 709 718 , 0006-3606
22 - P. G. Cramshaw, H. B. Quigley, 1991 Jaguar Spacing, Activity and Habitat Use in a Seasonally Flooded Environment in Brazil. Journal of Zoology, 223 3 357 370 , 0952-8369
23 - K. R. Crooks, M. E. Soulé, 1999 Mesopredator Release and Avifaunal Extinctions in a Fragmented System. Nature, 400 6744 August 1999), 563 566 , 0028-0836
24 - L. M. Curran, I. Caniago, G. D. Paoli, D. Astianti, M. Kusneti, M. Leighton, C. E. Nirarita, H. Haeruman, 1999 Impact of El Niño and Logging on Canopy Tree Recruitment in Borneo. Science, 286 5447 (December 1999), 2184 2188 , 0036-8075
25 - L. M. Curran, M. Leighton, 2000 Vertebrate Responses to Spatiotemporal Variation in Seed Production of Mast-Fruiting Dipterocarpaceae. Ecological Monographs, 70 1 (February 2000), 0012-9615
26 - A. Dalecky, S. Chauvet, S. Ringuet, O. Claessens, J. Judas, M. Larue, J. F. Cosson, 2002 Large Mammals on Small Islands: Short Term Effects of Forest Fragmentation on the Large Mammal Fauna in French Guiana. Revue d’Ecologie Terra et la Vie, 54 1 March 2002), 0249-7395
27 - Silva. J. M. C. da, M. Tabarelli, 2000 Tree Species Impoverishment and the Future Flora of the Atlantic Forest of Northeast Brazil. Nature, 404 6773 (March 2000), 72 74 , 0028-0836
28 - B. de Thoisy, C. Richard-Hansen, B. Goguillon, P. Joubert, J. Obstancias, P. Winterton, S. Brosse, 2010 Rapid Evaluation of Threats to Biodiversity: Human Footprint Score and Large Vertebrate Species Responses in French Guiana. Biodiversity and Conservation, 19 6 (June 2010), 1567 1584 , 0960-3115
29 - R. Dial, J. Roughgarden, 1995 Experimental Removal of Insectivores from Rain Forest Canopy: Direct and Indirect Effects. Ecology, 76 6 (September 1995), 1821 1834 , 0012-9658
30 - R. Dirzo, P. H. Raven, 2003 Global State of Biodiversity and Loss. Annual Review of Environment and Resources, 28 1 (November 2003), 137 167 , 1543-5938
31 - R. Dirzo, E. Mendoza, P. Ortíz, 2007 Size-Related Differential Seed Predation in a Heavily Defaunated Neotropical Rain Forest. Biotropica, 39 3 (May 2007), 355 362 , 0006-3606
32 - A. Dobson, D. Lodge, J. Alder, G. S. Cumming, J. Keymer, J. Mc Glade, H. Mooney, J. A. Rusak, O. Sala, V. Wolters, D. Wall, R. Winfree, M. A. Xenopoulos, 2006 Hatitat Loss, Trophic Collapse, and the Decline of Ecosystem Services. Ecology, 87 8 (August 2006), 1915 1924 , 0012-9658
33 - C. I. Donatti, P. R. Guimarães, Jr , M. Galetti, 2009 Seed Dispersal and Predation in the Endemic Atlantic Rainforest Palm Astrocaryum aculeatissimum across a Gradient of Seed Disperser Abundance. Ecological Research, 24 6 (November 2009), 1187 1195 , 0912-3814
34 - J. E. Duffy, 2003 Biodiversity Loss, Trophic Skew, and Ecosystem Functioning. Ecology Letters, 6 8 (August 2003), 680 687 , 1461-0248
35 - J. A. Estes, J. Terborgh, J. S. Brashares, M. E. Power, J. Berger, W. J. Bond, S. C. Carpenter, T. E. Essington, R. D. Holt, J. B. C. Jackson, R. J. Marquis, L. Oksanen, T. Oksanen, R. T. Paine, E. K. Pikitch, W. J. Ripple, S. A. Sandin, M. Scheffer, T. W. Shcoener, J. B. Shurin, A. R. E. Sinclair, M. E. Soulé, R. Virtanen, D. A. Wardle, 2011 Trophic Downgrading of Planet Earth. Science, 333 6040 (July 2011), 301 306 , 0036-8075
36 - R. M. Ewers, R. K. Didham, 2006 Confounding Factors in the Detection of Species Responses to Habitat Fragmentation. Biological Reviews, 81 2 (May 2006), 117 142 , 1464-7931
37 - J. E. Fa, C. A. Peres, J. Meeuwig, 2002 Bushmeat Exploitation in Tropical Forests: An Intercontinental Comparison. Conservation Biology, 16 1 (February 2002), 232 237 , 0888-8892
38 - L. Fahrig, 1997 Relative Effects of Habitat Loss and Fragmentation on Population Extinction. The Journal of Wildlife Management, 61 3 (July 1997), 603 610 , 1937-2817
39 - L. Fahrig, 2002 Effect of Habitat Fragmentation on the Extinction Threshold: A Synthesis. Ecological Applications, 12 2 (April 2002), 346 353 , 1051-0761
40 - L. Fahrig, 2003 Effects of Habitat Fragmentation on Biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34 1 (December 2003), 487 515 , 0066-4162
41 - K. J. Feeley, J. W. Terborgh, 2005 The Effects of Herbivore Density on Soil Nutrients and Tree Growth in Tropical Forest Fragments. Ecology, 86 1 (January 2005), 116 124 , 0012-9658
42 - K. J. Feeley, J. W. Terborgh, 2008 Direct Versus Indirect Effects of Habitat Reduction on the Loss of Avian Species from Tropical Forest Fragments. Animal Conservation, 11 5 (October 2008), 353 360 , 1469-1795
43 - G. Ferraz, G. J. Russell, P. C. Stouffer, R. O. Bierregaard, S. L. Pimm, T. E. Lovejoy, 2003 Rates of Species Loss from Amazonian Forest Fragments. Proceedings of the National Academy of the Sciences of the USA, 100 24 (November 2003), 14069 14073 , 1091-6490
44 - R. J. Fletcher, Jr , L. Ries, J. Battin, A. D. Chalfoun, 2007 The Role of Habitat Area and Edge in Fragmented Landscapes: Definitely Distinct or Inevitably Intertwined? Canadian Journal of Zoology, 85 10 (October 2007), 1017 1030 , 0008-4301
45 - M. Fleury, M. Galetti, 2006 Forest Fragment Size and Microhabitat Effects on Palm Seed Predation. Biological Conservation, 131 1 (July 2006), 1 13 , 0006-3207
46 - T. A. Gardner, J. Barlow, L. W. Parry, C. A. Peres, 2007 Predicting the Uncertain Future of Tropical Forest Species in a Data Vacuum. Biotropica, 39 1 (January 2007), 25 30 , 0006-3606
47 - M. R. Guariguata, Claire. H. Arias Le, G. Jones, 2002 Tree Seed Fate in a Logged and Fragmented Forest Landscape, Northeastern Costa Rica. Biotropica, 34 3 (September 2002), 405 415 , 0006-3606
48 - M. R. Guariguata, Adame. J. J. Rosales, B. Finegan, 2000 Seed Removal and Fate in Two Selectively Logged Lowland Forests with Contrasting Protection Levels. Conservation Biology, 14 4 (August 2000), 1046 1054 , 0888-8892
49 - J. S. Halofsky, W. J. Ripple, 2008a Fine-Scale Predation Risk on Elk After Wolf Reintroduction in Yellowstone National Park, USA. Oecologia, 155 4 (April 2008), 869 877 , 0029-8549
50 - J. S. Halofsky, W. J. Ripple, 2008b Linkages Between Wolf Presence and Aspen Recruitment in the Gallatin Elk Winter Range of Southwestern Montana, USA. Forestry, 81 2 (April 2008), 195 207 , 0001-5752X.
51 - M. C. Hansen, R. S. De Fries, 2004 Detecting Long-Term Global Forest Change Using Continuous Fields of Tree-Cover Maps From 8-km Advanced Very High Resolution Radiometer (AVHRR) Data for the Years 1982-99. Ecosystems, 7 7 (November 2004), 695 716 , 1432-9840
52 - M. C. Hansen, S. V. Stehman, P. V. Potapov, T. R. Loveland, J. R. G. Townshend, R. S. De Fries, K. W. Pittman, B. Arunarwati, F. Stolle, M. K. Steininger, M. Carroll, C. Di Miceli, 2008 Humid Tropical Forest Clearing from 2000 to 2005 Quantified by Using Multitemporal and Multiresolution Remotely Sensed Data. Proceedings of the National Academy of the Sciences of the USA, 105 27 (July 2008), 9439 9444 , 1091-6490
53 - T. Hanson, S. Brunsfeld, B. Finegan, 2006 Variation in Seedling Density and Seed Predation Indicators for the Emergent Tree Dipteryx panamensis in Continuous and Fragmented Rain Forest. Biotropica, 38 6 (November 2006), 770 774 , 0006-3606
54 - F. He, S. P. Hubbell, 2011 Species-Area Relationships Always Overestimate Extinction Rates from Habitat Loss. Nature, 473 7347 (May 2011), 368 371 , 0028-0836
55 - K. Henle, K. F. Davies, M. Kleyer, C. Margules, J. Settele, 2004 Predictors of Species Sensitivity to Fragmentation. Biodiversity and Conservation, 13 1 (January 2004), 207 251 , 0960-3115
56 - J. M. Herrera, D. García, D. Martínez, A. Valdés, 2011 Regional vs Local Effects of Habitat Loss and Fragmentation on Two Plant-Animal Interactions. Ecography, 34 4 (August 2011), 606 615 , 0906-7590
57 - K. Ickes, 2001 Hyper-Abundance of Native Wild Pigs (Sus scrofa) in a Lowland Dipterocarp Rain Forest of Peninsular Malaysia. Biotropica, 33 4 (December 2001), 682 690 , 0006-3606
58 - K. Ickes, S. J. Dewalt, S. Appanah, 2001 Effects of Native Pigs (Sus scrofa) on Woody Understorey Vegetation in a Malaysian Lowland Rain Forest. Journal of Tropical Ecology, 17 2 (March 2001), 191 206 , 0266-4674
59 - K. Ickes, S. J. De Walt, S. C. Thomas, 2003 Resprouting of Woody Saplings Following Stem Snap by Wild Pigs in a Malaysian Rain Forest. Journal of Ecology, 91 2 (April 2003), 222 233 , 1365-2745
60 - K. Ickes, C. J. Paciorek, S. C. Thomas, 2005 Impacts of Nest Construction by Native Pigs (Sus scrofa) on Lowland Malaysian Rain Forest Saplings. Ecology, 86 6 (June 2005), 1540 1547 , 0012-9658
61 - K. Ickes, G. B. Williamson, 2000 Edge Effects and Ecological Processes- Are they on the Same Scale? Trends in Ecology and Evolution, 15 9 (September 2000), 373 0169-5347
62 - International Monetary Fund. 2010 World Economic Outlook Database, In: World Economic and Financial Surveys, 01.08.2011, Available from: < pubs/ft/weo/2011/01/weodata/index.aspx>.
63 - C. N. Johnson, 2002 Determinants of Loss of Mammal Species During the Late Quaternary ‘Megafauna’ Extinctions: Life History and Ecology, but Not Body Size. Proceedings of the Royal Society B: Biological Sciences, 269 1506 November 2002), 2221 2227 , 1471-2954
64 - C. N. Johnson, J. L. Isaac, D. O. Fisher, 2007 Rarity of a Top Predator Triggers Continent-Wide Collapse of Mammal Prey: Dingoes and Marsupials in Australia. Proceedings of the Royal Society B: Biological Sciences, 274 1608 (February 2007), 341 346 , 1471-2954
65 - M. B. Kalka, A. R. Smith, E. K. V. Kalko, 2008 Bats Limit Arthropods and Herbivory in a Tropical Forest. Science, 320 5872 (April 2008), 71 0036-8075
66 - G. H. Kattan, H. Alvarez-Lopez, M. Giraldo, 1994 Forest Fragmentation and Bird Extinctions: San Antonio Eighty Years Later. Conservation Biology, 8 1 March 1994), 138 146 , 0888-8892
67 - N. Keyghobadi, 2007 The Genetic Implications of Habitat Fragmentation for Animals. Canadian Journal of Zoology, 85 10 (October 2007), 1049 1064 , 0008-4301
68 - L. P. Koh, R. R. Dunn, N. S. Sodhi, R. K. Colwell, H. C. Proctor, V. S. Smith, 2004 Species Coextinctions and the Biodiversity Crisis. Science, 305 5690 (September 2004), 1632 1634 , 0036-8075
69 - E. K. Kuprewicz, C. García-Robledo, 2010 Mammal and Insect Predation of Chemically and Structurally Defended Mucuna holtonii (Fabaceae) Seeds in a Costa Rican Rain Forest. Journal of Tropical Ecology, 26 3 (May 2010), 263 269 , 0266-4674
70 - W. F. Laurance, 1991 Ecological Correlates of Extinction Proneness in Australian Tropical Rain Forest Mammals. Conservation Biology, 5 1 (March 1991), 79 89 , 0888-8892
71 - W. F. Laurance, 1994 Rainforest Fragmentation and the Structure of Small Mammal Communities in Tropical Queensland. Biological Conservation, 69 1 (January 1994), 23 32 , 0006-3207
72 - W. F. Laurance, 1997 Responses of Mammals to Rainforest Fragmentation in Tropical Queensland: A Review and Synthesis. Wildlife Research, 24 5 (October 1997), 603 612 , 1035-3712
73 - W. F. Laurance, 1999 Introduction and Synthesis. Biological Conservation, 91 2-3 , (December 1999), 101 107 , 0006-3207
74 - W. F. Laurance, 2000 Do Edge Effects Occur Over Large Spatial Scales? Trends in Ecology and Evolution, 15 4 (April 2000), 134 135 , 0169-5347
75 - W. F. Laurance, 2005 The Alteration of Biotic Interactions in Fragmented Tropical Forests, In: Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity, Burslem, D.F.R.P., Pinard, M.A., & S.E. Hartley, (Eds.), 441 458 , Cambridge University Press, 978-0-52160-985-2 Cambridge, UK.
76 - W. F. Laurance, 2006 Have we Overstated the Tropical Biodiversity Crisis? Trends in Ecology and Evolution, 22 2 February 2006), 65 70 , 0169-5347
77 - W. F. Laurance, 2008 Theory Meets Reality: How Habitat Fragmentation Research has Transcended Island Biogeographic Theory. Biological Conservation, 141 7 (July 2008), 1731 1744 , 0006-3207
78 - W. F. Laurance, D. C. Useche, 2009 Environmental Synergisms and Extinctions of Tropical Species. Conservation Biology, 23 6 (December 2009), 1427 1437 , 0888-8892
79 - W. F. Laurance, G. B. Williamson, 2001 Positive Feedbacks among Forest Fragmentation, Drought, and Climate Change in the Amazon. Conservation Biology, 15 6 (December 2001), 1529 1535 , 8888-8892
80 - W. F. Laurance, J. L. C. Camargo, R. C. C. Luizão, S. G. Laurance, S. L. Pimm, E. M. Bruna, P. C. Stouffer, G. B. Williamson, J. Benítez-Malvido, H. L. Vasconcelos, K. S. Van Houtan, C. E. Zartman, S. A. Boyle, R. K. Didham, A. Andrade, T. E. Lovejoy, 2011 The Fate of Amazonian Forest Fragments: A 32-Year Investigation. Biological Conservation, 144 1 (January 2011), 56 67 , 0006-3207
81 - W. F. Laurance, T. E. Lovejoy, H. L. Vasconcelos, E. M. Bruna, R. K. Didham, P. C. Stouffer, C. Gascon, R. O. Bierregaard, S. G. Laurance, E. Sampaio, 2002 Ecosystem Decay of Amazonian Forest Fragments: a 22-Year Investigation. Conservation Biology, 16 3 (June 2002), 605 618 , 0888-8892
82 - W. F. Laurance, S. G. Laurance, D. W. Hilbert, 2008 Long-Term Dynamics of a Fragmented Rainforest Mammal Assemblage. Conservation Biology, 22 5 (October 2008), 1154 1164 , 0888-8892
83 - A. C. Lees, C. A. Peres, 2008 Conservation Value of Remnant Riparian Forest Corridors of Varying Quality for Amazonian Birds and Mammals. Conservation Biology, 22 2 (April 2008), 439 449 , 0888-8892
84 - E. G. Leigh, Jr , 1999 Tropical Forest Ecology: A View From Barro Colorado Island (1st edition), Oxford University Press, 978-0-19509-603-3 New York, NY, USA.
85 - D. K. Letourneau, L. A. Dyer, 1998 Experimental Tests in Lowland Tropical Forest Shows Top-Down Effects Through Four Trophic Levels. Ecology, 79 5 (July 1998), 1678 1687 , 0012-9658
86 - M. Lieberman, D. Lieberman, 1994 Patterns of Density and Dispersion of Forest Trees, In: La Selva: Ecology and Natural History of a Neotropical Rainforest, McDade, L.A., Bawa, K.S., Hespenheide, H.A., & Hartshorn, G.S., (Eds.), 106 119 , University of Chicago Press, 978-0-22603-950-3 Chicago, IL.
87 - C. A. Lindell, S. K. Riffell, S. A. Kaiser, A. L. Battin, M. L. Smith, T. D. Sisk, 2007 Edge Responses of Tropical and Temperate Birds. Wilson Journal of Ornithology, 119 2 (June 2007), 205 220 , 1559-4491
88 - B. A. Loiselle, W. G. Hoppes, 1983 Nest Predation in Insular and Mainland Lowland Rainforest in Panama. Condor, 85 1 (February 1983), 93 95 , 0010-5422
89 - L. Lopez, J. Terborgh, 2007 Seed Predation and Seedling Herbivory as Factors in Tree Recruitment Failure on Predator-Free Forested Islands. Journal of Tropical Ecology, 23 2 (March 2007), 129 137 , 0266-4674
90 - A. E. Lugo, 2009 The Emerging Era of Novel Tropical Forests. Biotropica, 41 5 (September 2009), 589 591 , 0006-3606
91 - Arthur. R. H. Mac, E. O. Wilson, 1967 The Theory of Island Biogeography, Princeton University Press, 978-0-69108-836-5 Princeton, NJ.
92 - S. Manu, W. Peach, W. Cresswell, 2007 The Effects of Edge, Fragment Size and Degree of Isolation on Avian Species Richness in Highly Fragmented Forest in West Africa. Ibis, 149 2 (April 2007), 287 297 , 0147-4919X.
93 - W. J. Mc Shea, H. B. Underwood, J. H. Rappole, 1997 (Eds.). The Science of Overabundance: Deer Ecology and Population Management. Smithsonian Books, 978-1-56098-681-2 Washington, D.C.
94 - F. P. L. Melo, E. Martínez-Salas, J. Benítez-Malvido, G. Ceballos, 2010 Forest Fragmentation Reduces Recruitment of Large-Seeded Tree Species in a Semi-Deciduous Tropical Forest of Southern Mexico. Journal of Tropical Ecology, 26 1 (January 2010), 35 43 , 0266-4674
95 - J. P. Metzger, A. C. Martensen, M. Dixo, L. C. Bernacci, M. C. Ribeiro, Texeira. A. M. Godoy, R. Pardini, 2009 Time-Lag in Biological Responses to Landscape Changes in a Highly Dynamic Atlantic Forest Region. Biological Conservation, 142 6 (June 2009), 1166 1177 , 0006-3207
96 - F. Michalski, C. A. Peres, 2007 Disturbance-Mediated Mammal Persistence and Abundance-Area Relationships in Amazonian Forest Fragments. Conservation Biology, 21 6 (December 2007), 1626 1640 , 0888-8892
97 - N. L. Michel, T. W. Sherry, W. P. Carson, (In Review, Oecologia). Non-Trophic Effects of Large Vertebrates Reverse Trophic Cascades in Wet-Tropical Forest Understory.
98 - E. J. Milner-Gulland, E. L. Bennett, for. Society, Biology. Conservation, 2002 Annual Meeting Wild Meat Group. (2003). Wild Meat: the Bigger Picture. Trends in Ecology and Evolution, 18 7 (July 2003), 351 357 , 0169-5347
99 - C. Moran, C. P. Catterall, J. Kanowski, 2009 Reduced Dispersal of Native Plant Species as a Consequence of the Reduced Abundance of Frugivore Species in Fragmented Rainforest. Biological Conservation, 142 3 (March 2009), 541 552 , 0006-3207
100 - H. C. Muller-Landau, 2007 Predicting the Long-Term Effects of Hunting on Plant Species Composition and Diversity in Tropical Forests. Biotropica, 39 3 (May 2007), 372 384 , 0006-3606
101 - H. C. Muller-Landau, B. D. Hardesty, 2005 Seed Dispersal of Woody Plants in Tropical Forests: Concepts, Examples, and Future Directions, In: Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity, Burslem, D.F.R.P., Pinard, M.A., & S.E. Hartley, (Eds.), 267 309 , Cambridge University Press, 978-0-52160-985-2 Cambridge, UK.
102 - L. Naughton-Treves, J. L. Mena, A. Treves, N. Alvarez, V. C. Radeloff, 2003 Wildlife Survival Beyond Park Boundaries: the Impact of Slash-and-Burn Agriculture and Hunting on Mammals in Tambopatu, Peru. Conservation Biology, 17 4 (August 2003), 1106 1117 , 0888-8892
103 - W. D. Newmark, 1991 Tropical Forest Fragmentation and the Local Extinction of Understory Birds in the Eastern Usambara Mountains, Tanzania. Conservation Biology, 5 1 (March 1991), 67 78 , 0888-8892
104 - D. Norris, C. A. Peres, F. Michalski, K. Hinchsliffe, 2008 Terrestrial Mammal Responses to Edges in Amazonian Forest Patches: A Study based on Track Stations. Mammalia, 72 1 (March 2008), 15 23 , 0025-1461
105 - G. Nuñez-Iturri, H. F. Howe, 2007 Bushmeat and the Fate of Trees with Seeds Dispersed by Large Primates in a Lowland Rain Forest in Western Amazonia. Biotropica, 39 3 (May 2007), 348 357 , 0006-3606
106 - R. T. Paine, 1980 Food Webs: Linkage, Interaction Strength, and Community Infrastructure. Journal of Animal Ecology, 49 667 685 , 1365-2656
107 - R. Pardini, 2004 Effects of Forest Fragmentation on Small Mammals in an Atlantic Forest Landscape. Biodiversity and Conservation, 13 13 (December 2004), 2567 2586 , 0960-3115
108 - C. A. Peres, 2001 Synergistic Effects of Subsistence Hunting and Habitat Fragmentation on Amazonian Forest Vertebrates. Conservation Biology, 15 6 (December 2001), 1490 1505 , 0888-8892
109 - C. A. Peres, E. Palacios, 2007 Basin-Wide Effects of Game Harvest on Vertebrate Population Densities in Amazonian Forests: Implications for Animal-Mediated Seed Dispersal. Biotropica, 39 3 (May 2007), 304 315 , 0006-3606
110 - H. A. Peters, 2001 Clidemia hirta Invasion at the Pasoh Forest Reserve: An Unexpected Plant Invasion in an Undisturbed Tropical Forest. Biotropica, 33 1 (March 2001), 60 68 , 0006-3606
111 - S. L. Pimm, H. L. Jones, J. Diamond, 1988 On the Risk Of Extinction. American Naturalist, 132 6 (December 1988), 757 785 , 0003-0147
112 - G. A. Polis, R. D. Holt, 1992 Intraguild Predation: the Dynamics of Complex Trophic Interactions. Trends in Ecology & Evolution, 7 3 (March 1992), 151 154 , 0169-5347
113 - G. A. Polis, D. R. Strong, 1996 Food Web Complexity and Community Dynamics. American Naturalist, 147 5 (May 1996), 813 846 , 0003-0147
114 - J. S. Powers, K. K. Treseder, M. T. Lerdau, 2005 Fine Roots, Arbuscular Mycorrhizal Hyphae and Soil Nutrients in Four Neotropical Rain Forests: Patterns Across Large Geographic Distances. New Phytologist, 165 3 March 2005), 913 921 , 1469-8137
115 - L. R. Prugh, C. J. Stoner, C. W. Epps, W. T. Bean, W. J. Ripple, A. S. Laliberte, J. S. Brashares, 2009 The Rise of the Mesopredator. BioScience, 59 9 (October 2009), 779 791 , 0006-3568
116 - A. Purvis, J. L. Gittleman, G. Cowlishaw, G. M. Mace, 2000 Predicting Extinction Risk in Declining Species. Proceedings of the Royal Society B: Biological Sciences, 267 1451 (July 2000), 1947 1952 , 1471-2954
117 - A. R. Rabinowitz, B. G. Nottingham, Jr , 1986 Ecology and Behaviour of the Jaguar (Panthera onca) in Belize, Central America. Journal of Zoology, 210 1 (September 1986), 149 159 , 0952-8369
118 - J. Ray, K. H. Redford, R. Steneck, J. . Berger, Eds., 2005 Large Carnivores and the Conservation of Biodiversity. Island Press, 978-1-55963-080-1 Washington, DC.
119 - K. Redford, 1992 The Empty Forest. BioScience, 42 6 (June 1992), 412 422 , 0006-3568
120 - C. Restrepo, N. Gomez, S. Heredia, 1999 Anthropogenic Edges, Treefall Gaps, and Fruit-Frugivore Interactions in a Neotropical Montane Forest. Ecology, 80 2 (March 1999), 668 685 , 0012-9658
121 - K. Riitters, J. Wickham, R. O’Neill, B. Jones, E. Smith, 2000 Global-Scale Patterns of Forest Fragmentation. Conservation Ecology, 4 2 (September 2000), art. 3. Available from: <>.
122 - W. J. Ripple, E. J. Larsen, 2000 Historic Aspen Recruitment, Elk, and Wolves in Northern Yellowstone National Park, USA. Biological Conservation, 95 3 (October 2000), 361 370 , 0006-3207
123 - E. G. Roberts, T. F. Flannery, L. K. Ayliffe, G. H. Yoshida, J. M. Olley, G. J. Prideaux, G. M. Laslett, A. Baynes, M. A. Smith, R. Jones, B. L. Smith, 2001 New Ages for the Last Australian Megafauna: Continent-Wide Extinction About 46,000 Years Ago. Science, 292 5523 (June 2001), 1888 1892 , 0036-8075
124 - P. Salo, P. B. Banks, C. R. Dickman, E. Korpimäki, 2010 Predator Manipulation Experiments: Impacts on Populations of Terrestrial Vertebrate Prey. Ecological Monographs, 80 4 (November 2010), 531 546 , 0012-9615
125 - O. J. Schmitz, D. Hawlena, G. C. Trussell, 2010 Predator Control of Ecosystem Nutrient Dynamics. Ecology Letters, 13 10 (October 2010), 1199 1209 , 1461-0248
126 - J. B. Shurin, E. T. Borer, E. W. Seabloom, K. Anderson, C. A. Blanchette, B. Broitman, S. D. Cooper, B. S. Halpern, 2002 A Cross-Ecosystem Comparison of the Strength of Trophic Cascades. Ecology Letters, 5 6 (November 2002), 785 791 , 1461-0248
127 - K. E. Sieving, 1992 Nest Predation and Differential Insular Extinction Among Selected Forest Birds of Panama. Ecology, 73 6 (December 1992), 2310 2328 , 0012-9658
128 - B. J. Sigel, W. D. Robinson, T. W. Sherry, 2010 Comparing Bird Community Responses to Forest Fragmentation in Two Lowland Central American Reserves. Biological Conservation, 143 2 (February 2010), 340 350 , 0006-3207
129 - B. J. Sigel, T. W. Sherry, B. E. Young, 2006 Avian Community Response to Lowland Tropical Rainforest Isolation: 40 Years of Change at La Selva Biological Station, Costa Rica. Biotropica, 20 1 (January 2006), 111 121, 0006-3606
130 - D. S. Skole, C. J. Tucker, 1993 Tropical Deforestation and Habitat Fragmentation in the Amazon: Satellite Data from 1978 to 1988. Science, 260 5116 (June 1993), 1905 1910 , 0036-8075
131 - N. S. Sodhi, M. R. C. Posa, T. M. Lee, I. G. Warkentin, 2008 Effects of Disturbance or Loss of Tropical Rainforest on Birds. Auk, 125 3 (July 2008), 511 519 , 0004-8038
132 - N. S. Sodhi, L. P. Koh, R. Clements, T. C. Wanger, J. K. Hill, K. C. Hamer, Y. Clough, T. Tscharntke, M. R. C. Posa, T. M. Lee, 2010b Conserving Southeast Asian Forest Biodiversity in Human-Modified Landscapes. Biological Conservation, 143 10 (October 2010), 2375 2384 , 0006-3207
133 - N. S. Sodhi, M. R. C. Posa, T. M. Lee, D. Bickford, L. P. Koh, B. W. Brook, 2010a The State and Conservation of Southeast Asian Biodiversity. Biodiversity and Conservation, 19 2 (February 2010), 317 328 , 0960-3115
134 - M. E. Soulé, 2010 Conservation Relevance of Ecological Cascades, In: Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature, Terborgh, J., & J.A. Estes, (Eds.), 337 352 , Island Press, 978-1-59726-487-7 Washington, DC.
135 - M. E. Soulé, D. T. Bolger, A. C. Alberts, J. Wright, S. Sorice, S. Hill, 1988 Reconstructing Dynamics of Rapid Extinctions of Chaparral-Requiring Birds in Urban Habitat Islands. Conservation Biology, 2 1 (March 1988), 75 92 , 0888-8892
136 - N. E. Stork, J. A. Coddington, R. K. Colwell, R. L. Chazdon, C. W. Dick, C. A. Peres, S. Sloan, K. Wills, 2009 Vulnerability and Resilience of Tropical Forest Species to Land-Use Change. Conservation Biology, 23 6 (December 2009), 1438 1447 , 0888-8892
137 - J. A. Stratford, W. D. Robinson, 2005 Gulliver Travels to the Fragmented Tropics: Geographic Variation in Mechanisms of Avian Extinction. Frontiers in Ecology and the Environment, 3 2 (March 2005), 91 98 , 1540-9295
138 - D. R. Strong, 1992 Are Trophic Cascades All Wet? Differentiation and Donor-Control in Speciose Ecosystems. Ecology, 73 3 (June 1992), 747 754 , 0012-9658
139 - M. Tabarelli, A. V. Lopes, C. A. Peres, 2008 Edge-Effects Drive Tropical Forest Fragments Towards an Early-Successional System. Biotropica, 40 6 November 2008), 657 661 , 0006-3606
140 - J. Terborgh, 1992 Maintenance of diversity in tropical forests. Biotropica, 24 2 June 1992), 283 292 , 0006-3606
141 - J. Terborgh, J. A. Estes, 2010 Preface, In: Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature, Terborgh, J., & J.A. Estes, (Eds.), pp. xiii-xx, Island Press, 978-1-59726-487-7 Washington, DC.
142 - J. Terborgh, J. A. Estes, P. Paquet, K. Ralls, D. Boyd-Heigher, B. J. Miller, R. F. Noss, 1999 The Role of Top Carnivores in Regulating Terrestrial Ecosystems, In: Continental Conservation: Scientific Foundations of Regional Reserve Networks, Soulé, M., & J. Terborgh, (Eds.), 39 54 , Island Press, 978-1-55963-698-8 Washington, DC.
143 - J. Terborgh, K. Feeley, 2010 Propagation of Trophic Cascades via Multiple Pathways in Tropical Forests, In: Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature, Terborgh, J., & J.A. Estes, (Eds.), 125 140 , Island Press, 978-1-59726-487-7 Washington, DC.
144 - J. Terborgh, K. Feeley, M. Silman, P. Nuñez, B. Balukjan, 2006 Vegetation Dynamics on Predator-Free Land-Bridge Islands. Journal of Ecology, 94 2 (March 2006), 253 263 , 1365-2745
145 - J. Terborgh, L. Lopez, P. Nuñez, M. Rao, B. Shahabuddin, G. Orihuela, M. Riveros, R. Ascanio, G. H. Adler, T. D. Lambert, L. Balbas, 2001 Ecological Meltdown in Predator-Free Forest Fragments. Science, 294 5548 (November 2001), 1923 1926 , 0036-8075
146 - J. Terborgh, L. Lopez, J. Tello, 1997 Bird Communities in Transition: The Lago Guri Islands. Ecology, 78 5 (July 1997), 1494 1501 , 0012-9658
147 - J. Terborgh, G. Nuñez-Ituri, N. Pitman, F. Cornejo, P. Alvarez, B. Pringle, V. Swamy, T. Paine, 2008 Tree Recruitment in an “Empty” Forest. Ecology, 89 6 (June 2008), 1757 1768 , 0012-9658
148 - J. Terborgh, S. J. Wright, 1994 Effects of Mammalian Herbivores on Plant Recruitment in Two Neotropical Forests. Ecology, 75 6 (September 1994), 1829 1833 , 0012-9658
149 - D. Tilman, R. M. May, C. L. Lehman, M. A. Nowak, 1994 Habitat Destruction and the Extinction Debt. Nature, 371 1 (September 1994), 65 66 , 0028-0836
150 - I. M. Torrealba-Suárez, J. M. Rau, 1994 Biology of collared peccary groups Tayassu tajacu and their damage provocated in crops neighboring La Selva Biological Station, Costa Rica: Final report 1993. (Unpubl.) Universidad Nacional de Costa Rica, Programa Regional Manejo de Vida Silvestre.
151 - Transparency International. 2010 Corruption Perceptions Index 2010, 01.08.2011, Available from:<>
152 - S. A. Van Bael, J. D. Brawn, S. K. Robinson, 2003 Birds Defend Trees from Herbivores in a Neotropical Forest Canopy. Proceedings of the National Academy of the Sciences of the USA, 100 14 (July 2008), 8304 8307 , 1091-6490
153 - S. A. Van Bael, S. M. Philpott, R. Greenberg, P. Bichier, N. A. Barber, K. A. Mooney, D. S. Gruner, 2008 Birds as Predators in Tropical Agroforestry Systems. Ecology, 89 4 (April 2008), 928 934 , 0012-9658
154 - H. D. Vance-Chalcraft, J. A. Rosenheim, J. R. Vonesh, C. W. Osenberg, A. Sih, 2007 The Influence of Intraguild Predation on Prey Suppression and Prey Release: A Meta-Analysis. Ecology, 88 11 (November 2007), 2689 2696 , 0012-9658
155 - S. Wang, P. D. Curtis, J. P. Lassoie, 2006 Farmer Perceptions of Crop Damage by Wildlife in Jigme Singye Wangchuck National Park, Bhutan. Wildlife Society Bulletin, 34 2 (June 2006), 369 365 , 0091-7648
156 - T. Wangchuk, 2004 Predator-Prey Dynamics: The Role of Predators in the Control of Problem Species. Journal of Bhutan Studies, 10 1 (Summer 2004), 68 89 , 0160-8411X.
157 - D. S. Wilkie, E. L. Bennett, C. A. Peres, A. A. Cunningham, 2011 The Empty Forest Revisited. Annals of the New York Academy of Sciences, The Year in Ecology and Conservation Biology, 1223 1 (March 2011), 120 128 , 0077-8923
158 - K. Williams-Guillén, I. Perfecto, J. Vandermeer, 2008 Bats Limit Insects in a Neotropical Agroforestry System. Science, 320 5872 (April 2008), 70 0036-8075
159 - R. Woodroffe, J. R. Ginsberg, 1998 Edge Effects and Extinction of Populations Inside Protected Areas. Science, 280 5372 (June 1998), 2126 2128 , 0036-8075
160 - S. J. Wright, 2005 Tropical Forests in a Changing Environment. Trends in Ecology and Evolution, 20 10 (October 2005), 553 560 , 0169-5347
161 - S. J. Wright, 2010 The Future of Tropical Forests. Annals of the New York Academy of Sciences, The Year in Ecology and Conservation Biology, 1195 1 (March 2010), 1 27 , 0077-8923
162 - S. J. Wright, H. C. Duber, 2001 Poachers and Forest Fragmentation Alter Seed Dispersal, Seed Survival, and Seedling Recruitment in the Palm Attalea butyraceae, with Implications for Tropical Tree Diversity. Biotropica, 33 4 (December 2001), 583 595 , 0006-3606
163 - S. J. Wright, M. E. Gompper, B. De Leon, 1994 Are Large Predators Keystone Species in Neotropical Forests? The Evidence from Barro Colorado Island. Oikos, 71 2 (November 1994), 279 294 , 0030-1299
164 - S. J. Wright, A. Hernandez, R. Condit, 2007b The Bush Meat Harvest Alters Seedling Banks by Favoring Lianas, Large Seeds, and Seeds Dispersed by Bats, Birds, and Wind. Biotropica, 39 3 (May 2007), 363 371 , 0006-3606
165 - S. J. Wright, H. C. Muller-Landau, 2006a The Future of Tropical Forest Species. Biotropica, 38 3 (May 2006), 287 301 , 0006-3606
166 - S. J. Wright, H. C. Muller-Landau, 2006b The Uncertain Future of Tropical Forest Species. Biotropica, 38 4 (July 2006), 443 445 , 0006-3606
167 - S. J. Wright, G. A. Sanchez-Azofeifa, C. Portillo-Quintero, D. Davies, 2007c Poverty and Corruption Compromise Tropical Forest Reserves. Ecological Applications, 17 5 1259 1266 , 1051-0761
168 - S. J. Wright, K. E. Stoner, N. Beckman, R. T. Corlett, R. Dirzo, H. C. Muller-Landau, G. Nuñez-Iturri, C. A. Peres, B. C. Wang, 2007a The Plight of Large Animals in Tropical Forests and the Consequences for Plant Regeneration. Biotropica, 39 3 (May 2007), 289 291 , 0006-3606
169 - S. J. Wright, H. Zeballos, I. Domínguez, M. M. Gallardo, M. C. Moreno, R. Ibáñez, 2000 Poachers Alter Mammal Abundance, Seed Dispersal and Seed Predation in a Neotropical Forest. Conservation Biology, 14 1 (February 2000), 227 239 , 0888-8892
170 - G. Yaacobi, Y. Ziv, M. L. Rosenzweig, 2007 Habitat Fragmentation May Not Matter to Diversity. Proceedings of the Royal Society B: Biological Sciences, 274 1624 October 2007), 2409 2412 , 1471-2954