Global economic trade-offs between wild nature and tropical agriculture.

Global demands for agricultural and forestry products provide economic incentives for deforestation across the tropics. Much of this deforestation occurs with a lack of information on the spatial distribution of benefits and costs of deforestation. To inform global sustainable land-use policies, we combine geographic information systems (GIS) with a meta-analysis of ecosystem services (ES) studies to perform a spatially explicit analysis of the trade-offs between agricultural benefits, carbon emissions, and losses of multiple ecosystem services because of tropical deforestation from 2000 to 2012. Even though the value of ecosystem services presents large inherent uncertainties, we find a pattern supporting the argument that the externalities of destroying tropical forests are greater than the current direct economic benefits derived from agriculture in all cases bar one: when yield and rent potentials of high-value crops could be realized in the future. Our analysis identifies the Atlantic Forest, areas around the Gulf of Guinea, and Thailand as areas where agricultural conversion appears economically efficient, indicating a major impediment to the long-term financial sustainability of Reducing Emissions from Deforestation and forest Degradation (REDD+) schemes in those countries. By contrast, Latin America, insular Southeast Asia, and Madagascar present areas with low agricultural rents (ARs) and high values in carbon stocks and ES, suggesting that they are economically viable conservation targets. Our study helps identify optimal areas for conservation and agriculture together with their associated uncertainties, which could enhance the efficiency and sustainability of pantropical land-use policies and help direct future research efforts.

Primary forests are irreplaceable for sustaining tropical biodiversity.

Human-driven land-use changes increasingly threaten biodiversity, particularly in tropical forests where both species diversity and human pressures on natural environments are high. The rapid conversion of tropical forests for agriculture, timber production and other uses has generated vast, human-dominated landscapes with potentially dire consequences for tropical biodiversity. Today, few truly undisturbed tropical forests exist, whereas those degraded by repeated logging and fires, as well as secondary and plantation forests, are rapidly expanding. Here we provide a global assessment of the impact of disturbance and land conversion on biodiversity in tropical forests using a meta-analysis of 138 studies. We analysed 2,220 pairwise comparisons of biodiversity values in primary forests (with little or no human disturbance) and disturbed forests. We found that biodiversity values were substantially lower in degraded forests, but that this varied considerably by geographic region, taxonomic group, ecological metric and disturbance type. Even after partly accounting for confounding colonization and succession effects due to the composition of surrounding habitats, isolation and time since disturbance, we find that most forms of forest degradation have an overwhelmingly detrimental effect on tropical biodiversity. Our results clearly indicate that when it comes to maintaining tropical biodiversity, there is no substitute for primary forests.

Increasing arboreality with altitude: a novel biogeographic dimension.

Biodiversity is spatially organized by climatic gradients across elevation and latitude. But do other gradients exist that might drive biogeographic patterns? Here, we show that rainforest's vertical strata provide climatic gradients much steeper than those offered by elevation and latitude, and biodiversity of arboreal species is organized along this gradient. In Philippine and Singaporean rainforests, we demonstrate that rainforest frogs tend to shift up in the rainforest strata as altitude increases. Moreover, a Philippine-wide dataset of frog distributions shows that frog assemblages become increasingly arboreal at higher elevations. Thus, increased arboreality with elevation at broad biogeographic scales mirrors patterns we observed at local scales. Our proposed 'arboreality hypothesis' suggests that the ability to exploit arboreal habitats confers the potential for larger geographical distributions because species can shift their location in the rainforest strata to compensate for shifts in temperature associated with elevation and latitude. This novel finding may help explain patterns of species richness and abundance wherever vegetation produces a vertical microclimatic gradient. Our results further suggest that global warming will 'flatten' the biodiversity in rainforests by pushing arboreal species towards the cooler and wetter ground. This 'flattening' could potentially have serious impacts on forest functioning and species survival.

Reservoirs of richness: least disturbed tropical forests are centres of undescribed species diversity.

In the last few decades, there has been a remarkable discovery of new species of plants, invertebrates and vertebrates, in what have been called the new age of discovery. However, owing to anthropogenic impacts such as habitat conversion, many of the still unknown species may go extinct before being scientifically documented (i.e. 'crypto-extinctions'). Here, by applying a mathematical model of species descriptions which accounts for taxonomic effort, we show that even after 250 years of taxonomic classification, about 3050 amphibians and at least 160 land mammal species remain to be discovered and described. These values represent, respectively, 33 and 3 per cent of the current species total for amphibians and land mammals. We found that tropical moist forests of the Neotropics, Afrotropics and Indomalaya probably harbour the greatest numbers of undescribed species. Tropical forests with minimal anthropogenic disturbance are predicted to have larger proportions of undescribed species. However, the protected area coverage is low in many of these key biomes. Moreover, undescribed species are likely to be at a greater risk of extinction compared with known species because of small geographical ranges among other factors. By highlighting the key areas of undescribed species diversity, our study provides a starting template to rapidly document these species and protect them through better habitat management.

Endemic predators, invasive prey and native diversity.

Interactions between native diversity and invasive species can be more complex than is currently understood. Invasive ant species often substantially reduce diversity in the native ants diversity that act as natural control agents for pest insects. In Indonesia (on the island of Sulawesi), the third largest cacao producer worldwide, we show that a predatory endemic toad (Ingerophrynus celebensis) controls invasive ant (Anoplolepis gracilipes) abundance, and positively affects native ant diversity. We call this the invasive-naivety effect (an opposite of enemy release), whereby alien species may not harbour anti-predatory defences against a novel native predator. A positive effect of the toads on native ants may facilitate their predation on insect vectors of cacao diseases. Hence, toads may increase crop yield, but further research is needed on this aspect. Ironically, amphibians are globally the most threatened vertebrate class and are strongly impacted by the conversion of rainforest to cacao plantations in Sulawesi. It is, therefore, crucial to manage cacao plantations to maintain these endemic toads, as they may provide critical ecosystem services, such as invasion resistance and preservation of native insect diversity.

Conservation biology: predicting birds' responses to forest fragmentation.

Understanding species' ecological responses to habitat fragmentation is critical for biodiversity conservation, especially in tropical forests. A detailed recent study has shown that changes in the abundances of bird species following fragmentation may be dramatic and unpredictable.

Mechanisms driving change: altered species interactions and ecosystem function through global warming.

1. We review the mechanisms behind ecosystem functions, the processes that facilitate energy transfer along food webs, and the major processes that allow the cycling of carbon, oxygen and nitrogen, and use case studies to show how these have already been, and will continue to be, altered by global warming. 2. Increased temperatures will affect the interactions between heterotrophs and autotrophs (e.g. pollination and seed dispersal), and between heterotrophs (e.g. predators-prey, parasites/pathogens-hosts), with generally negative ramifications for important ecosystem services (functions that provide direct benefit to human society such as pollination) and potential for heightened species co-extinction rates. 3. Mitigation of likely impacts of warming will require, in particular, the maintenance of species diversity as insurance for the provision of basic ecosystem services. Key to this will be long-term monitoring and focused research that seek to maintain ecosystem resilience in the face of global warming. 4. We provide guidelines for pursuing research that quantifies the nexus between ecosystem function and global warming. These include documentation of key functional species groups within systems, and understanding the principal outcomes arising from direct and indirect effects of a rapidly warming environment. Localized and targeted research and monitoring, complemented with laboratory work, will determine outcomes for resilience and guide adaptive conservation responses and long-term planning.

Effects of land-use change on community composition of tropical amphibians and reptiles in Sulawesi, Indonesia.

Little is known about the effects of anthropogenic land-use change on the amphibians and reptiles of the biodiverse tropical forests of Southeast Asia. We studied a land-use modification gradient stretching from primary forest, secondary forest, natural-shade cacao agroforest, planted-shade cacao agroforest to open areas in central Sulawesi, Indonesia. We determined species richness, abundance, turnover, and community composition in all habitat types and related these to environmental correlates, such as canopy heterogeneity and thickness of leaf litter. Amphibian species richness decreased systematically along the land-use modification gradient, but reptile richness and abundance peaked in natural-shade cacao agroforests. Species richness and abundance patterns across the disturbance gradient were best explained by canopy cover and leaf-litter thickness in amphibians and by canopy heterogeneity and cover in reptiles. Amphibians were more severely affected by forest disturbance in Sulawesi than reptiles. Heterogeneous canopy cover and thick leaf litter should be maintained in cacao plantations to facilitate the conservation value for both groups. For long-term and sustainable use of plantations, pruned shade trees should be permanently kept to allow rejuvenation of cacao and, thus, to prevent repeated forest encroachment.

Deforestation and avian extinction on tropical landbridge islands.

There are few empirical data, particularly collected simultaneously from multiple sites, on extinctions resulting from human-driven land-use change. Southeast Asia has the highest deforestation rate in the world, but the resulting losses of biological diversity remain poorly documented. Between November 2006 and March 2008, we conducted bird surveys on six landbridge islands in Malaysia and Indonesia. These islands were surveyed previously for birds in the early 1900 s, when they were extensively forested. Our bird inventories of the islands were nearly complete, as indicated by sampling saturation curves and nonparametric true richness estimators. From zero (Pulau Malawali and Pulau Mantanani) to 15 (Pulau Bintan) diurnal resident landbird species were apparently extirpated since the early 1900 s. Adding comparable but published extinction data from Singapore to our regression analyses, we found there were proportionally fewer forest bird extinctions in areas with greater remaining forest cover. Nevertheless, the statistical evidence to support this relationship was weak, owing to our unavoidably small sample size. Bird species that are restricted to the Indomalayan region, lay few eggs, are heavier, and occupy a narrower habitat breadth, were most vulnerable to extinction on Pulau Bintan. This was the only island where sufficient data existed to analyze the correlates of extinction. Forest preservation and restoration are needed on these islands to conserve the remaining forest avifauna. Our study of landbridge islands indicates that deforestation may increasingly threaten Southeast Asian biodiversity.

Catastrophic extinctions follow deforestation in Singapore.

The looming mass extinction of biodiversity in the humid tropics is a major concern for the future, yet most reports of extinctions in these regions are anecdotal or conjectural, with a scarcity of robust, broad-based empirical data. Here we report on local extinctions among a wide range of terrestrial and freshwater taxa from Singapore (540 km2) in relation to habitat loss exceeding 95% over 183 years. Substantial rates of documented and inferred extinctions were found, especially for forest specialists, with the greatest proportion of extinct taxa (34-87%) in butterflies, fish, birds and mammals. Observed extinctions were generally fewer, but inferred losses often higher, in vascular plants, phasmids, decapods, amphibians and reptiles (5-80%). Forest reserves comprising only 0.25% of Singapore's area now harbour over 50% of the residual native biodiversity. Extrapolations of the observed and inferred local extinction data, using a calibrated species-area model, imply that the current unprecedented rate of habitat destruction in Southeast Asia will result in the loss of 13-42% of regional populations over the next century, at least half of which will represent global species extinctions.

Prospects for tropical forest biodiversity in a human-modified world.

The future of tropical forest biodiversity depends more than ever on the effective management of human-modified landscapes, presenting a daunting challenge to conservation practitioners and land use managers. We provide a critical synthesis of the scientific insights that guide our understanding of patterns and processes underpinning forest biodiversity in the human-modified tropics, and present a conceptual framework that integrates a broad range of social and ecological factors that define and contextualize the possible future of tropical forest species. A growing body of research demonstrates that spatial and temporal patterns of biodiversity are the dynamic product of interacting historical and contemporary human and ecological processes. These processes vary radically in their relative importance within and among regions, and have effects that may take years to become fully manifest. Interpreting biodiversity research findings is frequently made difficult by constrained study designs, low congruence in species responses to disturbance, shifting baselines and an over-dependence on comparative inferences from a small number of well studied localities. Spatial and temporal heterogeneity in the potential prospects for biodiversity conservation can be explained by regional differences in biotic vulnerability and anthropogenic legacies, an ever-tighter coupling of human-ecological systems and the influence of global environmental change. These differences provide both challenges and opportunities for biodiversity conservation. Building upon our synthesis we outline a simple adaptive-landscape planning framework that can help guide a new research agenda to enhance biodiversity conservation prospects in the human-modified tropics.

The sixth mass coextinction: are most endangered species parasites and mutualists?

The effects of species declines and extinction on biotic interactions remain poorly understood. The loss of a species is expected to result in the loss of other species that depend on it (coextinction), leading to cascading effects across trophic levels. Such effects are likely to be most severe in mutualistic and parasitic interactions. Indeed, models suggest that coextinction may be the most common form of biodiversity loss. Paradoxically, few historical or contemporary coextinction events have actually been recorded. We review the current knowledge of coextinction by: (i) considering plausible explanations for the discrepancy between predicted and observed coextinction rates; (ii) exploring the potential consequences of coextinctions; (iii) discussing the interactions and synergies between coextinction and other drivers of species loss, particularly climate change; and (iv) suggesting the way forward for understanding the phenomenon of coextinction, which may well be the most insidious threat to global biodiversity.

Landscape constraints on functional diversity of birds and insects in tropical agroecosystems.

In this paper, we analyze databases [corrected] on birds and insects to assess patterns of functional diversity in human-dominated landscapes in the tropics. A perspective from developed landscapes is essential for understanding remnant natural ecosystems, because most species experience their surroundings at spatial scales beyond the plot level, and spillover between natural and managed ecosystems is common. Agricultural bird species have greater habitat and diet breadth than forest species. Based on a global data base, bird assemblages in tropical agroforest ecosystems were composed of disproportionately more frugivorous and nectarivorous, but fewer insectivorous bird species compared with forest. Similarly, insect predators of plant-feeding arthropods were more diverse in Ecuadorian agroforest and forest compared with rice and pasture, while, in Indonesia, bee diversity was also higher in forested habitats. Hence, diversity of insectivorous birds and insect predators as well as bee pollinators declined with agricultural transformation. In contrast, with increasing agricultural intensification, avian pollinators and seed dispersers initially increase then decrease in proportion. It is well established that the proximity of agricultural habitats to forests has a strong influence on the functional diversity of agroecosystems. Community similarity is higher among agricultural systems than in natural habitats and higher in simple than in complex landscapes for both birds and insects, so natural communities, low-intensity agriculture, and heterogeneous landscapes appear to be critical in the preservation of beta diversity. We require a better understanding of the relative role of landscape composition and the spatial configuration of landscape elements in affecting spillover of functionally important species across managed and natural habitats. This is important for data-based management of tropical human-dominated landscapes sustaining the capacity of communities to reorganize after disturbance and to ensure ecological functioning.

The importance of protected areas for the forest and endemic avifauna of Sulawesi (Indonesia).

Protected areas are critical for the conservation of residual tropical forest biodiversity, yet many of these are being deforested by humans both within and outside of their administrative boundaries. Therefore, it is critical to document the significance of protected areas for conserving tropical biodiversity, particularly in mega-diverse Southeast Asia. We evaluated the importance of protected areas (national parks [NP], nature reserves [NR], and wildlife reserves [WR]) in preserving avifaunal diversity, particularly the endemic and forest species, on the island of Sulawesi. This island has one of the highest numbers of endemic avifauna genera (12) globally and is also experiencing heavy deforestation. Rarefaction analyses and species estimators showed that parks and reserves consistently recorded higher number of forest, endemic, and endemic forest bird species, in addition to larger population densities, than in their surrounding human-modified areas across eight protected areas (Gunung Manembo-nembo WR, Tangkoko-Batu Angus and Dua Saudara NR, Gunung Ambang NR, Bogani Nani Wartabone NP, Gunung Tinombala NR, Gunung Sojol NR, Lore Lindu NP, and Rawa Aopa Watumohai NP). This implies that protecting natural forests must remain as one of the fundamental conservation strategies in Sulawesi. Two small reserves (Gunung Manembo-nembo WR and Tangkoko-Batu Angus and Dua Saudara NR), however, had high number of forest and endemic bird species both within and outside their boundaries, suggesting the importance of buffer areas for augmenting small reserves so as to improve their conservation value. Ordination analyses revealed the differential response of bird species to different environmental factors (e.g., native tree cover), highlighting the significance of forested habitats with dense native vegetation cover for effective conservation of forest dependent and endemic avifauna. In addition, the distinctiveness in bird species composition among protected areas highlights the importance of establishing a reserve network across major altitudinal zones so as to achieve maximum complementarity for the conservation of Sulawesi's unique avifauna.

Heavy Extinctions of Forest Avifauna in Singapore: Lessons for Biodiversity Conservation in Southeast Asia.

The consequences of rapid rainforest clearance on native avifauna are poorly understood. In Southeast Asia, Singapore, a newly developing country, has had 95% of its native lowland rainforest cleared. Most of the rainforest was lost in the mid- to late-nineteenth century. We compared avifauna checklists from 1923, 1949, and 1998 to determine the extent of extinctions between 1923 and 1998 in Singapore. Of 203 diurnal bird species, 65 were extirpated in Singapore in the past 75 years. Four of these species were nonforest- dependent species, whereas 61 (94%) were forest bird species dependent on the primary or old secondary forest to survive. Twenty-six forest bird species became extinct between 1923 and 1949, whereas 35 forest species disappeared after 1949. We compared the body lengths, feeding guilds, and vertical feeding zones between extinct and extant forest bird species to determine whether extinction patterns were dependent on these characteristics. Larger forest bird species went extinct between 1923 and 1949. Body sizes, however, did not affect the loss of forest bird species between 1949 and 1998. We observed high losses of insectivorous birds; the insectivore-carnivore and insectivore-granivore guilds lost> 80% of the species present in 1923. The highest losses were among birds that fed in the canopy. None of the forest bird species are currently common (>100 individuals/species) within Singapore. Our study shows that more than half the forest avifauna became locally extinct after extensive deforestation. Based on this fact, the countries within Southeast Asia should reconsider their heavy deforestation practices.

RESUMEN: Las consecuencias de la tala rápida del bosque lluvioso sobre la avifauna nativa son poco conocidas. En Asia sudoriental, Singapur, un país en desarrollo, un 95% de su bosque nativo de tierras bajas ha sido talado. La mayoríia del bosque se perdió entre mediados y finales del siglo diecinueve. En este trabajo comparamos las listas de avifauna de 1923, 1949 y 1998 para determinar la extensión de las extinciones en Singapur entre 1923 y 1998. Sesenta y cinco de las 203 especies diurnas de aves fueron extirpadas de Singapur en los últimos 75 años. Cuatro de estas especies fueron especies no dependientes del bosque, mientras que 61 (94%) fueron especies de aves del bosque (especies que dependen del bosque primario o secundario viejo para sobrevivir). Veintiséis de las especies de aves del bosque se extinguieron entre 1923 y 1949, mientras que 35 especies del bosque desaparecieron después de 1949. Comparamos las longitudes del cuerpo, los gremios de alimentación y las zonas de alimentación vertical entre especies de aves de bosque extintas y existentes para determinar si los patrones de extinción fueron dependientes de estas características. Las especies de aves grandes del bosque se extinguieron entre 1923 y 1949. Sin embargo, el tamaño del cuerpo no afectó la pérdida de especies del bosque entre 1949 y 1998. Observamos altas pérdidas de aves insectívoras; los gremios de insectívoros-carnívoros e insectívoros-granívoros perdieron> 80% de las especies que estaban presentes en 1923. Los números más altos de pérdidas fueron de aves que se alimentan en el dosel. Ninguna de las especies de aves del bosque es común en la actualidad (>100 individuos/especie) dentro de Singapur. Nuestro estudio muestra que más de la mitad de la avifauna del bosque se ha extinguido localmente después de una deforestación extensiva. Con base en este hecho, los países dentro de Asia Sudoriental deberían reconsiderar sus prácticas de intensa deforestación.