Brett R. Scheffers

What we know and don't know about Earth's missing biodiversity.

Estimates of non-microbial diversity on Earth range from 2 million to over 50 million species, with great uncertainties in numbers of insects, fungi, nematodes, and deep-sea organisms. We summarize estimates for major taxa, the methods used to obtain them, and prospects for further discoveries. Major challenges include frequent synonymy, the difficulty of discriminating certain species by morphology alone, and the fact that many undiscovered species are small, difficult to find, or have small geographic ranges. Cryptic species could be numerous in some taxa. Novel techniques, such as DNA barcoding, new databases, and crowd-sourcing, could greatly accelerate the rate of species discovery. Such advances are timely. Most missing species probably live in biodiversity hotspots, where habitat destruction is rife, and so current estimates of extinction rates from known species are too low.

Biodiversity redistribution under climate change : Impacts on ecosystems and human well-being

Consequences of shifting species distributions Climate change is causing geographical redistribution of plant and animal species globally. These distributional shifts are leading to new ecosystems and ecological communities, changes that will affect human society. Pecl et al. review these current and future impacts and assess their implications for sustainable development goals. Science, this issue p. eaai9214 BACKGROUND The success of human societies depends intimately on the living components of natural and managed systems. Although the geographical range limits of species are dynamic and fluctuate over time, climate change is impelling a universal redistribution of life on Earth. For marine, freshwater, and terrestrial species alike, the first response to changing climate is often a shift in location, to stay within preferred environmental conditions. At the cooler extremes of their distributions, species are moving poleward, whereas range limits are contracting at the warmer range edge, where temperatures are no longer tolerable. On land, species are also moving to cooler, higher elevations; in the ocean, they are moving to colder water at greater depths. Because different species respond at different rates and to varying degrees, key interactions among species are often disrupted, and new interactions develop. These idiosyncrasies can result in novel biotic communities and rapid changes in ecosystem functioning, with pervasive and sometimes unexpected consequences that propagate through and affect both biological and human communities. ADVANCES At a time when the world is anticipating unprecedented increases in human population growth and demands, the ability of natural ecosystems to deliver ecosystem services is being challenged by the largest climate-driven global redistribution of species since the Last Glacial Maximum. We demonstrate the serious consequences of this species redistribution for economic development, livelihoods, food security, human health, and culture, and we document feedbacks on climate itself. As with other impacts of climate change, species range shifts will leave “winners” and “losers” in their wake, radically reshaping the pattern of human well-being between regions and different sectors and potentially leading to substantial conflict. The pervasive impacts of changes in species distribution transcend single systems or dimensions, with feedbacks and linkages between multiple interacting scales and through whole ecosystems, inclusive of humans. We argue that the negative effects of climate change cannot be adequately anticipated or prepared for unless species responses are explicitly included in decision-making and global strategic frameworks. OUTLOOK Despite mounting evidence for the pervasive and substantial impacts of a climate-driven redistribution of Earth’s species, current global goals, policies, and international agreements fail to account for these effects. With the predicted intensification of species movements and their diverse societal and environmental impacts, awareness of species “on the move” should be incorporated into local, regional, and global assessments as standard practice. This will raise hope that future targets—whether they be global sustainability goals, plans for regional biodiversity maintenance, or local fishing or forestry harvest strategies—can be achievable and that society is prepared for a world of universal ecological change. Human society has yet to appreciate the implications of unprecedented species redistribution for life on Earth, including for human lives. Even if greenhouse gas emissions stopped today, the responses required in human systems to adapt to the most serious effects of climate-driven species redistribution would be massive. Meeting these challenges requires governance that can anticipate and adapt to changing conditions, as well as minimize negative consequences. As the global climate changes, human well-being, ecosystem function, and even climate itself are increasingly affected by the shifting geography of life. Climate-driven changes in species distributions, or range shifts, affect human well-being both directly (for example, through emerging diseases and changes in food supply) and indirectly (by degrading ecosystem health). Some range shifts even create feedbacks (positive or negative) on the climate system, altering the pace of climate change. Distributions of Earth’s species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation’s Sustainable Development Goals.

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.

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.

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 rainforests 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.

The world's rediscovered species: Back from the brink?

Each year, numerous species thought to have disappeared are rediscovered. Yet, do these rediscoveries represent the return of viable populations or the delayed extinction of doomed species? We document the number, distribution and conservation status of rediscovered amphibian, bird, and mammal species globally. Over the past 122 years, at least 351 species have been rediscovered, most occurring in the tropics. These species, on average, were missing for 61 years before being rediscovered (range of 3–331 years). The number of rediscoveries per year increased over time and the majority of these rediscoveries represent first documentations since their original description. Most rediscovered species have restricted ranges and small populations, and 92% of amphibians, 86% of birds, and 86% of mammals are highly threatened, independent of how long they were missing or when they were rediscovered. Under the current trends of widespread habitat loss, particularly in the tropics, most rediscovered species remain on the brink of extinction.

The effects of urbanization on North American amphibian species: Identifying new directions for urban conservation

Urbanization is a pervasive and growing threat to amphibian populations globally. Although the number of studies is increasing, many aspects of basic amphibian biology have not been investigated in urban settings. We reviewed 32 urban studies from North America and quantified the number of species studied and their response to urbanization. We examined existing research on breeding habitats, life-history stages, movement patterns, and habitat use relative to urbanization. We found amphibians as a whole respond negatively to urbanization (69 reported responses were negative, 6 were positive and 35 showed no effect). We caution, however, that many North American species still lack or are associated with conflicting information regarding species-specific responses (e.g., 89 potential responses were unknown). Approximately 40% of all anuran and 14% of caudate species in North America were investigated in the literature; however, the most diverse genera (e.g., Plethodon and Eurycea) were the most understudied likely due to their cryptic terrestrial lifestyles and biases in sampling protocols that assess wetland habitats via call surveys. Research on movement and small scale habitat use was deficient. Adult, juvenile, tadpole, and egg mass life-history stages commonly served as direct measures of species presence and abundance; however, such data do not accurately reflect recruitment into subsequent age classes and population persistence. The lack of data on many North American species may be contributing to poor management of urban amphibian populations and their habitats.

Impacts of hunting on tropical forests in Southeast Asia

Although deforestation and forest degradation have long been considered the most significant threats to tropical biodiversity, across Southeast Asia (Northeast India, Indochina, Sundaland, Philippines) substantial areas of natural habitat have few wild animals (>1 kg), bar a few hunting-tolerant species. To document hunting impacts on vertebrate populations regionally, we conducted an extensive literature review, including papers in local journals and reports of governmental and nongovernmental agencies. Evidence from multiple sites indicated animal populations declined precipitously across the region since approximately 1980, and many species are now extirpated from substantial portions of their former ranges. Hunting is by far the greatest immediate threat to the survival of most of the regions endangered vertebrates. Causes of recent overhunting include improved access to forests and markets, improved hunting technology, and escalating demand for wild meat, wildlife-derived medicinal products, and wild animals as pets. Although hunters often take common species, such as pigs or rats, for their own consumption, they take rarer species opportunistically and sell surplus meat and commercially valuable products. There is also widespread targeted hunting of high-value species. Consequently, as currently practiced, hunting cannot be considered sustainable anywhere in the region, and in most places enforcement of protected-area and protected-species legislation is weak. The international communitys focus on cross-border trade fails to address overexploitation of wildlife because hunting and the sale of wild meat is largely a local issue and most of the harvest is consumed in villages, rural towns, and nearby cities. In addition to improved enforcement, efforts to engage hunters and manage wildlife populations through sustainable hunting practices are urgently needed. Unless there is a step change in efforts to reduce wildlife exploitation to sustainable levels, the region will likely lose most of its iconic species, and many others besides, within the next few years.

Local Demand Drives a Bushmeat Industry in a Philippine Forest Preserve

Unregulated hunting can severely affect wildlife populations, particularly in the tropics. From May to October, 2011, we documented target species, hunting techniques, and demand and sale of bushmeat from a local community located at the base of a forested National Park on an isolated mountain (over 10,000 ha) in southern Luzon, the Philippines. The prey taken by hunters (i.e., poachers) included 22 invertebrate and vertebrate species. The main prey items were fruit-eating birds, bats, civets and wild pigs, but the most sought-after prey were flying foxes. Money was the major driver of bushmeat hunting in our study area. Bushmeat was sold and consumed almost entirely by residents of the local community and nearby towns, as hunters stated that they do not have demand from regional urban markets. Localized consumption suggests that focused conservation efforts may be effective in reducing the documented hunting pressures. Fines for hunting endangered species, according to hunters, were a deterrent. Because of limited law enforcement in our study area, however, conservation efforts such as teaching local hunters to avoid endangered species or encouraging them to monitor local animal populations may be the best bottom-up approach to minimize the negative effects of hunting.

Managing consequences of climate-driven species redistribution requires integration of ecology, conservation and social science

Climate change is driving a pervasive global redistribution of the planets species. Species redistribution poses new questions for the study of ecosystems, conservation science and human societies that require a coordinated and integrated approach. Here we review recent progress, key gaps and strategic directions in this nascent research area, emphasising emerging themes in species redistribution biology, the importance of understanding underlying drivers and the need to anticipate novel outcomes of changes in species ranges. We highlight that species redistribution has manifest implications across multiple temporal and spatial scales and from genes to ecosystems. Understanding range shifts from ecological, physiological, genetic and biogeographical perspectives is essential for informing changing paradigms in conservation science and for designing conservation strategies that incorporate changing population connectivity and advance adaptation to climate change. Species redistributions present challenges for human well‐being, environmental management and sustainable development. By synthesising recent approaches, theories and tools, our review establishes an interdisciplinary foundation for the development of future research on species redistribution. Specifically, we demonstrate how ecological, conservation and social research on species redistribution can best be achieved by working across disciplinary boundaries to develop and implement solutions to climate change challenges. Future studies should therefore integrate existing and complementary scientific frameworks while incorporating social science and human‐centred approaches. Finally, we emphasise that the best science will not be useful unless more scientists engage with managers, policy makers and the public to develop responsible and socially acceptable options for the global challenges arising from species redistributions.