Global conservation status of the jawed vertebrate Tree of Life.

Human-driven extinction threatens entire lineages across the Tree of Life. Here we assess the conservation status of jawed vertebrate evolutionary history, using three policy-relevant approaches. First, we calculate an index of threat to overall evolutionary history, showing that we expect to lose 86-150 billion years (11-19%) of jawed vertebrate evolutionary history over the next 50-500 years. Second, we rank jawed vertebrate species by their EDGE scores to identify the highest priorities for species-focused conservation of evolutionary history, finding that chondrichthyans, ray-finned fish and testudines rank highest of all jawed vertebrates. Third, we assess the conservation status of jawed vertebrate families. We found that species within monotypic families are more likely to be threatened and more likely to be in decline than other species. We provide a baseline for the status of families at risk of extinction to catalyse conservation action. This work continues a trend of highlighting neglected groups-such as testudines, crocodylians, amphibians and chondrichthyans-as conservation priorities from a phylogenetic perspective.

Phylogenetic Biodiversity Metrics Should Account for Both Accumulation and Attrition of Evolutionary Heritage.

Phylogenetic metrics are essential tools used in the study of ecology, evolution and conservation. Phylogenetic diversity (PD) in particular is one of the most prominent measures of biodiversity, and is based on the idea that biological features accumulate along the edges of phylogenetic trees that are summed. We argue that PD and many other phylogenetic biodiversity metrics fail to capture an essential process that we term attrition. Attrition is the gradual loss of features through causes other than extinction. Here we introduce 'EvoHeritage', a generalisation of PD that is founded on the joint processes of accumulation and attrition of features. We argue that whilst PD measures evolutionary history, EvoHeritage is required to capture a more pertinent subset of evolutionary history including only components that have survived attrition. We show that EvoHeritage is not the same as PD on a tree with scaled edges; instead, accumulation and attrition interact in a more complex non-monophyletic way that cannot be captured by edge lengths alone. This leads us to speculate that the one dimensional edge lengths of classic trees may be insufficiently flexible to capture the nuances of evolutionary processes. We derive a measure of EvoHeritage and show that it elegantly reproduces species richness and PD at opposite ends of a continuum based on the intensity of attrition. We demonstrate the utility of EvoHeritage in ecology as a predictor of community productivity compared with species richness and PD. We also show how EvoHeritage can quantify living fossils and resolve their associated controversy. We suggest how the existing calculus of PD-based metrics and other phylogenetic biodiversity metrics can and should be recast in terms of EvoHeritage accumulation and attrition.

Quantifying the behavioural consequences of shark ecotourism.

Shark populations globally are facing catastrophic declines. Ecotourism has been posited as a potential solution to many of the issues facing shark conservation, yet increasingly studies suggest that such activity may negatively influence aspects of shark ecology and so further pressure declining populations. Here we combine UAV videography with deep learning algorithms, multivariate statistics and hidden Markov models (HMM) to quantitatively investigate the behavioural consequences of ecotourism in the whale shark (Rhincodon typus). We find that ecotourism increases the probability of sharks being in a disturbed behavioural state, likely increasing energetic expenditure and potentially leading to downstream ecological effects. These results are only recovered when fitting models that account for individual variation in behavioural responses and past behavioural history. Our results demonstrate that behavioural responses to ecotourism are context dependent, as the initial behavioural state is important in determining responses to human activity. We argue that models incorporating individuality and context-dependence should, wherever possible, be incorporated into future studies investigating the ecological impacts of shark ecotourism, which are only likely to increase in importance given the expansion of the industry and the dire conservation status of many shark species.

Genomic screening of 16 UK native bat species through conservationist networks uncovers coronaviruses with zoonotic potential.

There has been limited characterisation of bat-borne coronaviruses in Europe. Here, we screened for coronaviruses in 48 faecal samples from 16 of the 17 bat species breeding in the UK, collected through a bat rehabilitation and conservationist network. We recovered nine complete genomes, including two novel coronavirus species, across six bat species: four alphacoronaviruses, a MERS-related betacoronavirus, and four closely related sarbecoviruses. We demonstrate that at least one of these sarbecoviruses can bind and use the human ACE2 receptor for infecting human cells, albeit suboptimally. Additionally, the spike proteins of these sarbecoviruses possess an R-A-K-Q motif, which lies only one nucleotide mutation away from a furin cleavage site (FCS) that enhances infectivity in other coronaviruses, including SARS-CoV-2. However, mutating this motif to an FCS does not enable spike cleavage. Overall, while UK sarbecoviruses would require further molecular adaptations to infect humans, their zoonotic risk warrants closer surveillance.

The EDGE2 protocol: Advancing the prioritisation of Evolutionarily Distinct and Globally Endangered species for practical conservation action.

The conservation of evolutionary history has been linked to increased benefits for humanity and can be captured by phylogenetic diversity (PD). The Evolutionarily Distinct and Globally Endangered (EDGE) metric has, since 2007, been used to prioritise threatened species for practical conservation that embody large amounts of evolutionary history. While there have been important research advances since 2007, they have not been adopted in practice because of a lack of consensus in the conservation community. Here, building from an interdisciplinary workshop to update the existing EDGE approach, we present an "EDGE2" protocol that draws on a decade of research and innovation to develop an improved, consistent methodology for prioritising species conservation efforts. Key advances include methods for dealing with uncertainty and accounting for the extinction risk of closely related species. We describe EDGE2 in terms of distinct components to facilitate future revisions to its constituent parts without needing to reconsider the whole. We illustrate EDGE2 by applying it to the world's mammals. As we approach a crossroads for global biodiversity policy, this Consensus View shows how collaboration between academic and applied conservation biologists can guide effective and practical priority-setting to conserve biodiversity.

Signatures of increasing environmental stress in bumblebee wings over the past century: Insights from museum specimens.

Determining when animal populations have experienced stress in the past is fundamental to understanding how risk factors drive contemporary and future species' responses to environmental change. For insects, quantifying stress and associating it with environmental factors has been challenging due to a paucity of time-series data and because detectable population-level responses can show varying lag effects. One solution is to leverage historic entomological specimens to detect morphological proxies of stress experienced at the time stressors emerged, allowing us to more accurately determine population responses. Here we studied specimens of four bumblebee species, an invaluable group of insect pollinators, from five museums collected across Britain over the 20th century. We calculated the degree of fluctuating asymmetry (FA; random deviations from bilateral symmetry) between the right and left forewings as a potential proxy of developmental stress. We: (a) investigated whether baseline FA levels vary between species, and how this compares between the first and second half of the century; (b) determined the extent of FA change over the century in the four bumblebee species, and whether this followed a linear or nonlinear trend; (c) tested which annual climatic conditions correlated with increased FA in bumblebees. Species differed in their baseline FA, with FA being higher in the two species that have recently expanded their ranges in Britain. Overall, FA significantly increased over the century but followed a nonlinear trend, with the increase starting c. 1925. We found relatively warm and wet years were associated with higher FA. Collectively our findings show that FA in bumblebees increased over the 20th century and under weather conditions that will likely increase in frequency with climate change. By plotting FA trends and quantifying the contribution of annual climate conditions on past populations, we provide an important step towards improving our understanding of how environmental factors could impact future populations of wild beneficial insects.

Disorder or a new order: How climate change affects phenological variability.

Advancing spring phenology is a well documented consequence of anthropogenic climate change, but it is not well understood how climate change will affect the variability of phenology year to year. Species' phenological timings reflect the adaptation to a broad suite of abiotic needs (e.g., thermal energy) and biotic interactions (e.g., predation and pollination), and changes in patterns of variability may disrupt those adaptations and interactions. Here, we present a geographically and taxonomically broad analysis of phenological shifts, temperature sensitivity, and changes in interannual variability encompassing nearly 10,000 long-term phenology time series representing more than 1000 species across much of the Northern Hemisphere. We show that the timings of leaf-out, flowering, insect first-occurrence, and bird arrival were the most sensitive to temperature variation and have advanced at the fastest pace for early-season species in colder and less seasonal regions. We did not find evidence for changing variability in warmer years in any phenophase groups, although leaf-out and flower phenology have become moderately but significantly less variable over time. Our findings suggest that climate change has not to this point fundamentally altered the patterns of interannual phenological variability.

AREAdata: A worldwide climate dataset averaged across spatial units at different scales through time.

In an era of increasingly cross-discipline collaborative science, it is imperative to produce data resources which can be quickly and easily utilised by non-specialists. In particular, climate data often require heavy processing before they can be used for analyses. Here we describe AREAdata, a continually updated, free-to-use online global climate dataset, pre-processed to provide the averages of various climate variables across different administrative units (e.g., countries, states). These are daily estimates, based on the Copernicus Climate Data Store's ERA-5 data, regularly updated to the near-present and provided as direct downloads from our website (https://pearselab.github.io/areadata/). The daily climate estimates from AREAdata are consistent with other openly available data, but at much finer-grained spatial and temporal scales than available elsewhere. AREAdata complements the existing suite of climate resources by providing these data in a form more readily usable by researchers unfamiliar with GIS data-processing methods, and we anticipate these resources being of particular use to environmental and epidemiological researchers.

Predicting catchment suitability for biodiversity at national scales.

Biomonitoring of water quality and catchment management are often disconnected, due to mismatching scales. Considerable effort and money are spent each year on routine reach-scale surveying across many sites, particularly in countries like the UK, where nationwide sampling has been conducted using standardised techniques for many decades. Most of these traditional freshwater biomonitoring schemes focus on pre-defined indicators of organic pollution to compare observed vs expected subsets of common macroinvertebrate indicator species. Other taxa, including many threatened species, are often ignored due to their rarity, as are many invasive species, which are seen as undesirable despite becoming increasingly common and widespread in freshwaters, especially in urban ecosystems. Both these types of taxa are often monitored separately for reasons related to biodiversity concerns rather than for gauging water quality. Repurposing such data could therefore provide important new biomonitoring tools that can help catchment managers to directly link the water quality they aim to control with the biodiversity they are trying to protect. Here we used extensive data held in the England Non-Native and Rare/Protected species records that track these two groups of species as a proof-of-concept for linking catchment scale management of freshwater ecosystems and biodiversity to a range of potential drivers across England. We used national land use (Centre for Ecology and Hydrology land cover map) and water quality indicator (Environment Agency water quality data archive) datasets to predict, at the catchment scale, the presence or absence of 48 focal threatened or invasive species of concern routinely sampled by the English Environment Agency, with a median accuracy of 0.81 area under the receiver operating characteristic curve. A variety of water quality indicators and land-use types were useful in predictions, highlighting that future biomonitoring schemes could use such complementary measures to capture a wider spectrum of drivers and responses. In particular, the percentage of a catchment covered by freshwater was the single most important metric, reinforcing the need for space/habitat to support biodiversity, but we were also able to resolve a range of key environmental drivers for particular focal species. We show how our method could inform new catchment management approaches, by highlighting how key relationships can be identified and how to understand, visualise and prioritise catchments that are most suitable for restoration or water quality interventions. The scale of this work, in terms of number of species, drivers and locations, represents a significant step towards forging a new approach to catchment management that enables managers to link drivers they can control (water quality and land use) to the biota they are trying to protect (biodiversity).

Macrophenology: insights into the broad-scale patterns, drivers, and consequences of phenology.

Plant phenology research has surged in recent decades, in part due to interest in phenological sensitivity to climate change and the vital role phenology plays in ecology. Many local-scale studies have generated important findings regarding the physiology, responses, and risks associated with shifts in plant phenology. By comparison, our understanding of regional- and global-scale phenology has been largely limited to remote sensing of green-up without the ability to differentiate among plant species. However, a new generation of analytical tools and data sources-including enhanced remote sensing products, digitized herbarium specimen data, and public participation in science-now permits investigating patterns and drivers of phenology across extensive taxonomic, temporal, and spatial scales, in an emerging field that we call macrophenology. Recent studies have highlighted how phenology affects dynamics at broad scales, including species interactions and ranges, carbon fluxes, and climate. At the cusp of this developing field of study, we review the theoretical and practical advances in four primary areas of plant macrophenology: (1) global patterns and shifts in plant phenology, (2) within-species changes in phenology as they mediate species' range limits and invasions at the regional scale, (3) broad-scale variation in phenology among species leading to ecological mismatches, and (4) interactions between phenology and global ecosystem processes. To stimulate future research, we describe opportunities for macrophenology to address grand challenges in each of these research areas, as well as recently available data sources that enhance and enable macrophenology research.

Temperature and population density influence SARS-CoV-2 transmission in the absence of nonpharmaceutical interventions.

As COVID-19 continues to spread across the world, it is increasingly important to understand the factors that influence its transmission. Seasonal variation driven by responses to changing environment has been shown to affect the transmission intensity of several coronaviruses. However, the impact of the environment on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) remains largely unknown, and thus seasonal variation remains a source of uncertainty in forecasts of SARS-CoV-2 transmission. Here we address this issue by assessing the association of temperature, humidity, ultraviolet radiation, and population density with estimates of transmission rate (R). Using data from the United States, we explore correlates of transmission across US states using comparative regression and integrative epidemiological modeling. We find that policy intervention ("lockdown") and reductions in individuals' mobility are the major predictors of SARS-CoV-2 transmission rates, but, in their absence, lower temperatures and higher population densities are correlated with increased SARS-CoV-2 transmission. Our results show that summer weather cannot be considered a substitute for mitigation policies, but that lower autumn and winter temperatures may lead to an increase in transmission intensity in the absence of policy interventions or behavioral changes. We outline how this information may improve the forecasting of COVID-19, reveal its future seasonal dynamics, and inform intervention policies.

Herbivores at the highest risk of extinction among mammals, birds, and reptiles.

As a result of their extensive home ranges and slow population growth rates, predators have often been perceived to suffer higher risks of extinction than other trophic groups. Our study challenges this extinction-risk paradigm by quantitatively comparing patterns of extinction risk across different trophic groups of mammals, birds, and reptiles. We found that trophic level and body size were significant factors that influenced extinction risk in all taxa. At multiple spatial and temporal scales, herbivores, especially herbivorous reptiles and large-bodied herbivores, consistently have the highest proportions of threatened species. This observed elevated extinction risk for herbivores is ecologically consequential, given the important roles that herbivores are known to play in controlling ecosystem function.

Cryptic diversity in the model fern genus Ceratopteris (Pteridaceae).

Cryptic species are present throughout the tree of life. They are especially prevalent in ferns, because of processes such hybridization, polyploidy, and reticulate evolution. In addition, the simple morphology of ferns limits phenotypic variation and makes it difficult to detect cryptic species. The model fern genus Ceratopteris has long been suspected to harbor cryptic diversity, in particular within the highly polymorphic C. thalictroides. Yet no studies have included samples from throughout its pan-tropical range or utilized genomic sequencing, making it difficult to assess the full extent of cryptic variation within this genus. Here, we present the first multilocus phylogeny of the genus using reduced representation genomic sequencing (RADseq) and examine population structure, phylogenetic relationships, and ploidy level variation. We recover similar species relationships found in previous studies, find support for the cryptic species C. gaudichaudii as genetically distinct, and identify novel genomic variation within two of the mostly broadly distributed species in the genus, C. thalictroides and C. cornuta. Finally, we detail the utility of our approach for working on cryptic, reticulate groups of ferns. Specifically, it does not require a reference genome, of which there are very few available for ferns. RADseq is a cost-effective way to work with study groups lacking genomic resources, and to obtain the thousands of nuclear markers needed to untangle species complexes.

Bee phenology is predicted by climatic variation and functional traits.

Climate change is shifting the environmental cues that determine the phenology of interacting species. Plant-pollinator systems may be susceptible to temporal mismatch if bees and flowering plants differ in their phenological responses to warming temperatures. While the cues that trigger flowering are well-understood, little is known about what determines bee phenology. Using generalised additive models, we analyzed time-series data representing 67 bee species collected over 9 years in the Colorado Rocky Mountains to perform the first community-wide quantification of the drivers of bee phenology. Bee emergence was sensitive to climatic variation, advancing with earlier snowmelt timing, whereas later phenophases were best explained by functional traits including overwintering stage and nest location. Comparison of these findings to a long-term flower study showed that bee phenology is less sensitive than flower phenology to climatic variation, indicating potential for reduced synchrony of flowers and pollinators under climate change.

SoilTemp: A global database of near-surface temperature.

Current analyses and predictions of spatially explicit patterns and processes in ecology most often rely on climate data interpolated from standardized weather stations. This interpolated climate data represents long-term average thermal conditions at coarse spatial resolutions only. Hence, many climate-forcing factors that operate at fine spatiotemporal resolutions are overlooked. This is particularly important in relation to effects of observation height (e.g. vegetation, snow and soil characteristics) and in habitats varying in their exposure to radiation, moisture and wind (e.g. topography, radiative forcing or cold-air pooling). Since organisms living close to the ground relate more strongly to these microclimatic conditions than to free-air temperatures, microclimatic ground and near-surface data are needed to provide realistic forecasts of the fate of such organisms under anthropogenic climate change, as well as of the functioning of the ecosystems they live in. To fill this critical gap, we highlight a call for temperature time series submissions to SoilTemp, a geospatial database initiative compiling soil and near-surface temperature data from all over the world. Currently, this database contains time series from 7,538 temperature sensors from 51 countries across all key biomes. The database will pave the way toward an improved global understanding of microclimate and bridge the gap between the available climate data and the climate at fine spatiotemporal resolutions relevant to most organisms and ecosystem processes.

Publisher Correction: Open Science principles for accelerating trait-based science across the Tree of Life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Open Science principles for accelerating trait-based science across the Tree of Life.

Synthesizing trait observations and knowledge across the Tree of Life remains a grand challenge for biodiversity science. Species traits are widely used in ecological and evolutionary science, and new data and methods have proliferated rapidly. Yet accessing and integrating disparate data sources remains a considerable challenge, slowing progress toward a global synthesis to integrate trait data across organisms. Trait science needs a vision for achieving global integration across all organisms. Here, we outline how the adoption of key Open Science principles-open data, open source and open methods-is transforming trait science, increasing transparency, democratizing access and accelerating global synthesis. To enhance widespread adoption of these principles, we introduce the Open Traits Network (OTN), a global, decentralized community welcoming all researchers and institutions pursuing the collaborative goal of standardizing and integrating trait data across organisms. We demonstrate how adherence to Open Science principles is key to the OTN community and outline five activities that can accelerate the synthesis of trait data across the Tree of Life, thereby facilitating rapid advances to address scientific inquiries and environmental issues. Lessons learned along the path to a global synthesis of trait data will provide a framework for addressing similarly complex data science and informatics challenges.

Horticultural availability and homeowner preferences drive plant diversity and composition in urban yards.

Understanding the factors that influence biodiversity in urban areas is important for informing management efforts aimed at enhancing the ecosystem services in urban settings and curbing the spread of invasive introduced species. We determined the ecological and socioeconomic factors that influence patterns of plant richness, phylogenetic diversity, and composition in 133 private household yards in the Minneapolis-Saint Paul Metropolitan area, Minnesota, USA. We compared the composition of spontaneously occurring plant species and those planted by homeowners with composition in natural areas (at the Cedar Creek Ecosystem Science Reserve) and in the horticulture pool of species available from commercial growers. Yard area and fertilizer frequency influenced species richness of the spontaneous species but expressed homeowner values did not. In contrast, the criteria that homeowners articulated as important in their management decisions, including aesthetics, wildlife, neatness and food provision, significantly predicted cultivated species richness. Strikingly, the composition of plant species that people cultivated in their yards resembled the taxonomic and phylogenetic composition of species available commercially. In contrast, the taxonomic and phylogenetic composition of spontaneous species showed high similarity to natural areas. The large fraction of introduced species that homeowners planted was a likely consequence of what was available for them to purchase. The study links the composition and diversity of yard flora to their natural and anthropogenic sources and sheds light on the human factors and values that influence the plant diversity in residential areas of a major urban system. Enhanced understanding of the influences of the sources of plants, both native and introduced, that enter urban systems and the human factors and values that influence their diversity is critical to identifying the levers to manage urban biodiversity and ecosystem services.

Global imprint of mycorrhizal fungi on whole-plant nutrient economics.

Mycorrhizal fungi are critical members of the plant microbiome, forming a symbiosis with the roots of most plants on Earth. Most plant species partner with either arbuscular or ectomycorrhizal fungi, and these symbioses are thought to represent plant adaptations to fast and slow soil nutrient cycling rates. This generates a second hypothesis, that arbuscular and ectomycorrhizal plant species traits complement and reinforce these fungal strategies, resulting in nutrient acquisitive vs. conservative plant trait profiles. Here we analyzed 17,764 species level trait observations from 2,940 woody plant species to show that mycorrhizal plants differ systematically in nitrogen and phosphorus economic traits. Differences were clearest in temperate latitudes, where ectomycorrhizal plant species are more nitrogen use- and phosphorus use-conservative than arbuscular mycorrhizal species. This difference is reflected in both aboveground and belowground plant traits and is robust to controlling for evolutionary history, nitrogen fixation ability, deciduousness, latitude, and species climate niche. Furthermore, mycorrhizal effects are large and frequently similar to or greater in magnitude than the influence of plant nitrogen fixation ability or deciduous vs. evergreen leaf habit. Ectomycorrhizal plants are also more nitrogen conservative than arbuscular plants in boreal and tropical ecosystems, although differences in phosphorus use are less apparent outside temperate latitudes. Our findings bolster current theories of ecosystems rooted in mycorrhizal ecology and support the hypothesis that plant mycorrhizal association is linked to the evolution of plant nutrient economic strategies.