Richard T. Corlett

Fig-eating by vertebrate frugivores: a global review

The consumption of figs (the fruit of Ficus spp.; Moraceae) by vertebrates is reviewed using data from the literature, unpublished accounts and new field data from Borneo and Hong Kong. Records of frugivory from over 75 countries are presented for 260 Ficus species (approximately 30% of described species). Explanations are presented for geographical and taxonomic gaps in the otherwise extensive literature. In addition to a small number of reptiles and fishes, 1274 bird and mammal species in 523 genera and 92 families are known to eat figs. In terms of the number of species and genera of fig‐eaters and the number of fig species eaten we identify the avian families interacting most with Ficus to be Columbidae, Psittacidae, Pycnonotidae, Bucerotidae, Sturnidae and Lybiidae. Among mammals, the major fig‐eating families are Pteropodidae, Cercopithecidae, Sciuridae, Phyllostomidae and Cebidae. We assess the role these and other frugivores play in Ficus seed dispersal and identify fig‐specialists. In most, but not all, cases fig specialists provide effective seed dispersal services to the Ficus species on which they feed. The diversity of fig‐eaters is explained with respect to fig design and nutrient content, phenology of fig ripening and the diversity of fig presentation. Whilst at a gross level there exists considerable overlap between birds, arboreal mammals and fruit bats with regard to the fig species they consume, closer analysis, based on evidence from across the tropics, suggests that discrete guilds of Ficus species differentially attract subsets of sympatric frugivore communities. This dispersal guild structure is determined by interspecific differences in fig design and presentation. Throughout our examination of the fig‐frugivore interaction we consider phylogenetic factors and make comparisons between large‐scale biogeographical regions. Our dataset supports previous claims that Ficus is the most important plant genus for tropical frugivores. We explore the concept of figs as keystone resources and suggest criteria for future investigations of their dietary importance. Finally, fully referenced lists of frugivores recorded at each Ficus species and of Ficus species in the diet of each frugivore are presented as online appendices. In situations where ecological information is incomplete or its retrieval is impractical, this valuable resource will assist conservationists in evaluating the role of figs or their frugivores in tropical forest sites.

Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region

Current knowledge of frugivory and seed dispersal by vertebrates in the Oriental Region is summarized. Some degree of frugivory has been reported for many fish and reptile species, almost half the genera of non‐marine mammals and more than 40% of bird genera in the region. Highly frugivorous species, for which fruit dominates the diet for at least part of the year, occur in at least two families of reptiles, 12 families of mammals and 17 families of birds. Predation on seeds in fleshy fruits is much less widespread taxonomically: the major seed predators are colobine monkeys and rodents among the mammals, and parrots, some pigeons, and finches among the birds. Most seeds in the Oriental Region, except near its northern margins, are dispersed by vertebrate families which are endemic to the region or to the Old World. Small fruits and large, soft fruits with many small seeds are consumed by a wide range of potential seed dispersal agents, including species which thrive in small forest fragments and degraded landscapes. Larger, bigger‐seeded fruits are consumed by progressively fewer dispersers, and the largest depend on a few species of mammals and birds which are highly vulnerable to hunting, fragmentation and habitat loss.

Impacts of warming on tropical lowland rainforests

Before the end of this century, tropical rainforests will be subject to climatic conditions that have not existed anywhere on Earth for millions of years. These forests are the most species-rich ecosystems in the world and play a crucial role in regulating carbon and water feedbacks in the global climate system; therefore, it is important that the probable impacts of anthropogenic climate change are understood. However, the recent literature shows a striking range of views on the vulnerability of tropical rainforests, from least to most concern among major ecosystems. This review, which focuses on the impact of rising temperatures, examines the evidence for and against high vulnerability, identifies key research needs for resolving current differences and suggests ways of mitigating or adapting to potential impacts.

A global synthesis of plant extinction rates in urban areas

Plant extinctions from urban areas are a growing threat to biodiversity worldwide. To minimize this threat, it is critical to understand what factors are influencing plant extinction rates. We compiled plant extinction rate data for 22 cities around the world. Two-thirds of the variation in plant extinction rates was explained by a combination of the citys historical development and the current proportion of native vegetation, with the former explaining the greatest variability. As a single variable, the amount of native vegetation remaining also influenced extinction rates, particularly in cities > 200 years old. Our study demonstrates that the legacies of landscape transformations by agrarian and urban development last for hundreds of years, and modern cities potentially carry a large extinction debt. This finding highlights the importance of preserving native vegetation in urban areas and the need for mitigation to minimize potential plant extinctions in the future.

The ecological transformation of Singapore, 1819-1990

In 1819 the island of Singapore was almost en- tirely covered in rain forest, with a flora similar to the adja- cent Malay Peninsula but a relatively depauperate vertebrate fauna. The cultivation of cash crops resulted in rapid deforestation which was largely completed by the end of the nineteenth century. The cultivated area reached a maximum in 1935 and declined thereafter. Today, more than half the island is urbanized and less than 100 ha of primary rain forest survives. A further 1600 ha is covered in tall secondary forest. Floristic extinctions are impossible to quantify reliably but at least 100 bird species, twenty fresh- water fish species and several species of mammal have been lost. Man-made, open habitats are dominated by exotics but few have penetrated the forest. The naturalized biota in- cludes at least 138 vascular plant species, eighteen bird species, five mammal species, twenty fish species, several species of reptiles and amphibia, and an unknown number of invertebrates. Over much of inland Singapore there are probably none of the plant or animal species that occurred there 170 years ago. Despite this, in all the major taxonomic groups for which I have information the majority of known native species can still be found in Singapore today.

Potential Impacts of Climate Change on Tropical Asian Forests Through an Influence on Phenology

Changes in plant phenology will be one of the earliest responses to rapid global climate change and could potentially have serious consequences both for plants and for animals that depend on periodically available plant resources. Phenological patterns are most diverse and least understood in the tropics. In those parts of tropical Asia where low temperature or drought impose a seasonal rest period, regular annual cycles of growth and reproduction predominate at the individual, population, and community level. In aseasonal areas, individuals and populations show a range of sub- to supra-annual periodicities, with an overall supra-annual reproductive periodicity at the community level. There is no evidence for photoperiod control of phenology in the Asian tropics, and seasonal changes in temperature are a likely factor only near the northern margins. An opportunistic response to water availability is the simplest explanation for most observed patterns where water is seasonally limiting, while the great diversity of phenological patterns in the aseasonal tropics suggests an equal diversity of controls. The robustness of current phenological patterns to high interannual and spatial variability suggests that most plant species will not be seriously affected by the phenological consequences alone of climate change. However, some individual plant species may suffer, and the consequences of changes in plant phenology for flower- and fruit-dependent animals in fragmented forests could be serious.

The broad footprint of climate change from genes to biomes to people

Accumulating impacts Anthropogenic climate change is now in full swing, our global average temperature already having increased by 1°C from preindustrial levels. Many studies have documented individual impacts of the changing climate that are particular to species or regions, but individual impacts are accumulating and being amplified more broadly. Scheffers et al. review the set of impacts that have been observed across genes, species, and ecosystems to reveal a world already undergoing substantial change. Understanding the causes, consequences, and potential mitigation of these changes will be essential as we move forward into a warming world. Science, this issue p. 10.1126/science.aaf7671 BACKGROUND Climate change impacts have now been documented across every ecosystem on Earth, despite an average warming of only ~1°C so far. Here, we describe the full range and scale of climate change effects on global biodiversity that have been observed in natural systems. To do this, we identify a set of core ecological processes (32 in terrestrial and 31 each in marine and freshwater ecosystems) that underpin ecosystem functioning and support services to people. Of the 94 processes considered, 82% show evidence of impact from climate change in the peer-reviewed literature. Examples of observed impacts from meta-analyses and case studies go beyond well-established shifts in species ranges and changes to phenology and population dynamics to include disruptions that scale from the gene to the ecosystem. ADVANCES Species are undergoing evolutionary adaptation to temperature extremes, and climate change has substantial impacts on species physiology that include changes in tolerances to high temperatures, shifts in sex ratios in species with temperature-dependent sex determination, and increased metabolic costs of living in a warmer world. These physiological adjustments have observable impacts on morphology, with many species in both aquatic and terrestrial systems shrinking in body size because large surface-to-volume ratios are generally favored under warmer conditions. Other morphological changes include reductions in melanism to improve thermoregulation, and altered wing and bill length in birds. Broader-scale responses to climate change include changes in the phenology, abundance, and distribution of species. Temperate plants are budding and flowering earlier in spring and later in autumn. Comparable adjustments have been observed in marine and freshwater fish spawning events and in the timing of seasonal migrations of animals worldwide. Changes in the abundance and age structure of populations have also been observed, with widespread evidence of range expansion in warm-adapted species and range contraction in cold-adapted species. As a by-product of species redistributions, novel community interactions have emerged. Tropical and boreal species are increasingly incorporated into temperate and polar communities, respectively, and when possible, lowland species are increasingly assimilating into mountain communities. Multiplicative impacts from gene to community levels scale up to produce ecological regime shifts, in which one ecosystem state shifts to an alternative state. OUTLOOK The many observed impacts of climate change at different levels of biological organization point toward an increasingly unpredictable future for humans. Reduced genetic diversity in crops, inconsistent crop yields, decreased productivity in fisheries from reduced body size, and decreased fruit yields from fewer winter chill events threaten food security. Changes in the distribution of disease vectors alongside the emergence of novel pathogens and pests are a direct threat to human health as well as to crops, timber, and livestock resources. Humanity depends on intact, functioning ecosystems for a range of goods and services. Enhanced understanding of the observed impacts of climate change on core ecological processes is an essential first step to adapting to them and mitigating their influence on biodiversity and ecosystem service provision. Climate change impacts on ecological processes in marine, freshwater, and terrestrial ecosystems. Impacts can be measured on multiple processes at different levels of biological organization within ecosystems. In total, 82% of 94 ecological processes show evidence of being affected by climate change. Within levels of organization, the percentage of processes impacted varies from 60% for genetics to 100% for species distribution. Most ecological processes now show responses to anthropogenic climate change. In terrestrial, freshwater, and marine ecosystems, species are changing genetically, physiologically, morphologically, and phenologically and are shifting their distributions, which affects food webs and results in new interactions. Disruptions scale from the gene to the ecosystem and have documented consequences for people, including unpredictable fisheries and crop yields, loss of genetic diversity in wild crop varieties, and increasing impacts of pests and diseases. In addition to the more easily observed changes, such as shifts in flowering phenology, we argue that many hidden dynamics, such as genetic changes, are also taking place. Understanding shifts in ecological processes can guide human adaptation strategies. In addition to reducing greenhouse gases, climate action and policy must therefore focus equally on strategies that safeguard biodiversity and ecosystems.

Biodiversity and Conservation of Tropical Peat Swamp Forests

Tropical peat swamp forest is a unique ecosystem that is most extensive in Southeast Asia, where it is under enormous threat from logging, fire, and land conversion. Recent research has shown this ecosystems significance as a global carbon store, but its value for biodiversity remains poorly understood. We review the current status and biological knowledge of tropical peat swamp forests, as well as the impacts of human disturbances. We demonstrate that these forests have distinct floral compositions, provide habitat for a considerable proportion of the regions fauna, and are important for the conservation of threatened taxa, particularly specialized freshwater fishes. However, we estimate that only 36% of the historical peat swamp forest area remains, with only 9% currently in designated protected areas. Given that peat swamp forests are more vulnerable to synergies between human disturbances than other forest ecosystems, their protection and restoration are conservation priorities that require urgent action.

Characteristics of vertebrate-dispersed fruits in Hong Kong

Hong Kong has a native angiosperm flora of approximately 1800 species, of which 27% (482 spp.) bear fleshy, presumably vertebrate-dispersed fruits, including 76% of the 337 tree and shrub species and 70% of the 103 climber species. Morphological characteristics were determined for 255 species and nutritional characteristics of the fruit pulp for 153 species. Most fruit species were black (45.1%) or red (24.3%) and 85.9% had a mean diameter

Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis)

SummaryThe seeds in fruits consumed by primates may be chewed and digested, swallowed and defecated intact, or separated from the flesh and spat out. We show by a combination of close field observations and experiments with caged animals, that long-tailed macaques (Macaca fascicularis) have a remarkably low threshold of 3–4 mm for swallowing seeds and also that wild macaques rarely break them. The seeds of 69% of the ripe fruit species eaten are spat out intact or cleaned outside the mouth and dropped. Seed-spitting significantly reduces the swallowed food bulk and may lessen the risk of releasing seed toxins during mastication. However, it requires that even small fruits are processed in the mouth one or a few at a time. We suggest that fruit storage in the cheek pouches of cercopithecine monkeys allows them to spit seeds individually without excessively slowing fruit intake while feeding on patchily distributed fruit. In contrast, Apes and New World monkeys apparently swallow and defecate most ripe seeds in their diet and colobine monkeys break and digest them, detoxifying seed defenses by bacterial fermentation.