David Bickford

Measuring the Meltdown: Drivers of Global Amphibian Extinction and Decline

Habitat loss, climate change, over-exploitation, disease and other factors have been hypothesised in the global decline of amphibian biodiversity. However, the relative importance of and synergies among different drivers are still poorly understood. We present the largest global analysis of roughly 45% of known amphibians (2,583 species) to quantify the influences of life history, climate, human density and habitat loss on declines and extinction risk. Multi-model Bayesian inference reveals that large amphibian species with small geographic range and pronounced seasonality in temperature and precipitation are most likely to be Red-Listed by IUCN. Elevated habitat loss and human densities are also correlated with high threat risk. Range size, habitat loss and more extreme seasonality in precipitation contributed to decline risk in the 2,454 species that declined between 1980 and 2004, compared to species that were stable (n = 1,545) or had increased (n = 28). These empirical results show that amphibian species with restricted ranges should be urgently targeted for conservation.

The state and conservation of Southeast Asian biodiversity.

Southeast Asia is a region of conservation concern due to heavy losses of its native habitats. In this overview, we highlight the conservation importance of Southeast Asia by comparing its degree of species endemism and endangerment, and its rate of deforestation with other tropical regions (i.e., Meso-America, South America, and Sub-Saharan Africa). Southeast Asia contains the highest mean proportion of country-endemic bird (9%) and mammal species (11%). This region also has the highest proportion of threatened vascular plant, reptile, bird, and mammal species. Furthermore, not only is Southeast Asia’s annual deforestation rate the highest in the tropics, but it has also increased between the periods 1990–2000 and 2000–2005. This could result in projected losses of 13–85% of biodiversity in the region by 2100. Secondary habitat restoration, at least in certain countries, would allow for some amelioration of biodiversity loss and thus potentially lower the currently predicted extinction rates. Nonetheless, urgent conservation actions are needed. Conservation initiatives should include public education, sustaining livelihoods, and ways to enhance the sustainability of agriculture and increase the capacity of conservation institutions. Furthermore, these actions should be country-specific and not ignore areas heavily populated by humans, as they can also harbour high numbers of threatened species. We urge that cooperative conservation initiatives be undertaken and support (e.g., capacity-building) be given by more developed countries in the region and beyond.

Near-Complete Extinction of Native Small Mammal Fauna 25 Years After Forest Fragmentation

Futile Forest Fragments Most of the planets terrestrial biodiversity is found in tropical forests, but much of this critical habitat now persists as fragmented patches surrounded by agriculture. Smaller forest patches sustain fewer species than larger patches or contiguous forest. However, the numbers of species that will disappear from a forest fragment—and the rate of species loss—remain poorly understood. Gibson et al. (p. 1508) surveyed islands in a reservoir in Thailand to measure the rate of loss of small mammals from small forest fragments. Collapse of the entire native community (up to 12 species) from 16 forest fragments was observed after 25 years of isolation. Thus, small forest fragments hold little value for mammalian biodiversity, and conservation efforts should instead focus on the preservation of large forest expanses. The rapid loss of native mammals from isolated Thai forests suggests that forest fragments cannot maintain biodiversity. Tropical forests continue to be felled and fragmented around the world. A key question is how rapidly species disappear from forest fragments and how quickly humans must restore forest connectivity to minimize extinctions. We surveyed small mammals on forest islands in Chiew Larn Reservoir in Thailand 5 to 7 and 25 to 26 years after isolation and observed the near-total loss of native small mammals within 5 years from <10-hectare (ha) fragments and within 25 years from 10- to 56-ha fragments. Based on our results, we developed an island biogeographic model and estimated mean extinction half-life (50% of resident species disappearing) to be 13.9 years. These catastrophic extinctions were probably partly driven by an invasive rat species; such biotic invasions are becoming increasingly common in human-modified landscapes. Our results are thus particularly relevant to other fragmented forest landscapes and suggest that small fragments are potentially even more vulnerable to biodiversity loss than previously thought.

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.

Eating frogs to extinction.

IAN G. WARKENTIN,∗ DAVID BICKFORD,† NAVJOT S. SODHI,†‡ AND COREY J. A. BRADSHAW§∗∗ ∗Environmental Science—Biology, Memorial University of Newfoundland, Corner Brook, Newfoundland and Labrador A2H 6P9, Canada, email iwarkent@swgc.mun.ca †Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore ‡Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, U.S.A. §Research Institute for Climate Change and Sustainability, School of Earth and Environmental Sciences, University of Adelaide, South Australia 5005, Australia ∗∗South Australian Research and Development Institute, P.O. Box 120, Henley Beach, South Australia 5022, Australia

An Ancient Origin for the Enigmatic Flat-Headed Frogs (Bombinatoridae: Barbourula) from the Islands of Southeast Asia

Background The complex history of Southeast Asian islands has long been of interest to biogeographers. Dispersal and vicariance events in the Pleistocene have received the most attention, though recent studies suggest a potentially more ancient history to components of the terrestrial fauna. Among this fauna is the enigmatic archaeobatrachian frog genus Barbourula, which only occurs on the islands of Borneo and Palawan. We utilize this lineage to gain unique insight into the temporal history of lineage diversification in Southeast Asian islands. Methodology/Principal Findings Using mitochondrial and nuclear genetic data, multiple fossil calibration points, and likelihood and Bayesian methods, we estimate phylogenetic relationships and divergence times for Barbourula. We determine the sensitivity of focal divergence times to specific calibration points by jackknife approach in which each calibration point is excluded from analysis. We find that relevant divergence time estimates are robust to the exclusion of specific calibration points. Barbourula is recovered as a monophyletic lineage nested within a monophyletic Costata. Barbourula diverged from its sister taxon Bombina in the Paleogene and the two species of Barbourula diverged in the Late Miocene. Conclusions/Significance The divergences within Barbourula and between it and Bombina are surprisingly old and represent the oldest estimates for a cladogenetic event resulting in living taxa endemic to Southeast Asian islands. Moreover, these divergence time estimates are consistent with a new biogeographic scenario: the Palawan Ark Hypothesis. We suggest that components of Palawans terrestrial fauna might have “rafted” on emergent portions of the North Palawan Block during its migration from the Asian mainland to its present-day position near Borneo. Further, dispersal from Palawan to Borneo (rather than Borneo to Palawan) may explain the current day disjunct distribution of this ancient lineage.

Conservation. Boosting CITES.

To protect biodiversity, more, improved biological and trade data and analyses are needed. International wildlife trade remains a leading threat to biodiversity conservation (1) and is a common vector for infectious diseases (2, 3) and invasive species (4) that also affect agriculture, livestock, and public health. With 175 member countries, the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) is the most important global initiative to monitor and regulate international trade of plants and animals (5). CITES regulates trade of nearly 34,000 species and has reduced threats associated with overharvest of imperiled species for international trade.

Phylogeography and historical demography of Polypedates leucomystax in the islands of Indonesia and the Philippines: evidence for recent human-mediated range expansion?

Southeast Asias widespread species offer unique opportunities to explore the effects of geographical barriers to dispersal on patterns of vertebrate lineage diversification. We analyzed mitochondrial gene sequences (16S rDNA) from a geographically widespread sample of 266 Southeast Asian tree frogs, including 244 individuals of Polypedates leucomystax and its close relatives. Our expectation was that lineages on island archipelagos would exhibit more substantial geographic structure, corresponding to the geological history of terrestrial connectivity in this region, compared to the Asian mainland. Contrary to predictions, we found evidence of numerous highly divergent lineages from a limited area on the Asian mainland, but fewer lineages with shallower divergences throughout oceanic islands of the Philippines and Indonesia. Surprisingly and in numerous instances, lineages in the archipelagos span distinct biogeographical provinces. Phylogeographic analyses identified four major haplotype clades; summary statistics, mismatch distributions, and Bayesian coalescent inference of demography provide support for recent range expansion, population growth, and/or admixture in the Philippine and some Sulawesi populations. We speculate that the current range of P. leucomystax in Southeast Asia is much larger now than in the recent past. Conversion of forested areas to monoculture agriculture and transportation of agricultural products between islands may have facilitated unprecedented population and range expansion in P. leucomystax throughout thousands of islands in the Philippine and Indonesian archipelagos.

Differential parental care behaviors of arboreal and terrestrial microhylid frogs from Papua New Guinea

I studied the ecology of parental care behaviors displayed by two closely related sympatric species of microhylid frogs in Papua New Guinea that occupy different microhabitats. Adult removal experiments on the terrestrial frog Hylophorbus rufescens and the undescribed arboreal frog Oreophryne sp. “A” demonstrate a significant positive effect of parental attendance on offspring survivorship and differential causes of egg mortality between microhabitats. Desiccation was the primary cause of egg mortality for the arboreal frog, whereas predation was the main source of mortality for the terrestrial frog. These selection pressures (desiccation and predation) are comparable to two of Wilson’s “prime movers” of the evolution of parental care (harsh environment and predation) and may have driven and/or are maintaining the evolution of parental care behaviors in these Papuan microhylid frogs. These results highlight microhabitat-specific selection pressures in the evolution and maintenance of parental care behaviors.

Quantifying the role of online news in linking conservation research to Facebook and Twitter

Conservation science needs to engage the general public to ensure successful conservation interventions. Although online technologies such as Twitter and Facebook offer new opportunities to accelerate communication between conservation scientists and the online public, factors influencing the spread of conservation news in online media are not well understood. We explored transmission of conservation research through online news articles with generalized linear mixed-effects models and an information theoretic approach. In particular, we assessed differences in the frequency conservation research is featured on online news sites and the impact of online conservation news content and delivery on Facebook likes and shares and Twitter tweets. Five percent of articles in conservation journals are reported in online news, and the probability of reporting depended on the journal. There was weak evidence that articles on climate change and mammals were more likely to be featured. Online news articles about charismatic mammals with illustrations were more likely to be shared or liked on Facebook and Twitter, but the effect of news sites was much larger. These results suggest journals have the greatest impact on which conservation research is featured and that news site has the greatest impact on how popular an online article will be on Facebook and Twitter.