Two Major Extinction Events in the Evolutionary History of Turtles: One Caused by an Asteroid, the Other by Hominins.

AbstractWe live in a time of accelerated biological extinctions that has the potential to mirror past mass extinction events. However, the rarity of mass extinctions and the restructuring of diversity they cause complicate direct comparisons between the current extinction crisis and earlier events. Among animals, turtles (Testudinata) are one of few groups that have both a rich fossil record and sufficiently stable ecological and functional roles to enable meaningful comparisons between the end-Cretaceous mass extinction (∼66 Ma) and the ongoing wave of extinctions. Here we analyze the fossil record of the entire turtle clade and identify two peaks in extinction rates over their evolutionary history. The first coincides with the Cretaceous-Paleogene transition, reflecting patterns previously reported for other taxa. The second major extinction event started in the Pliocene and continues until now. This peak is detectable only for terrestrial turtles and started much earlier in Africa and Eurasia than elsewhere. On the basis of the timing, geography, and functional group of this extinction event, we postulate a link to co-occurring hominins rather than climate change as the cause. These results lend further support to the view that negative biodiversity impacts were already incurred by our ancestors and related lineages and demonstrate the severity of this continued impact through human activities.

The importance of migratory drop-off for island colonization in birds.

Seasonal migration is an underappreciated driver of animal diversification. Changes in migratory behaviour may favour the establishment of sedentary founder populations and promote speciation if there is sufficient reproductive isolation between sedentary and migratory populations. From a systematic literature review, we here quantify the role of migratory drop-off-the loss of migratory behaviour-in promoting speciation in birds on islands. We identify at least 157 independent colonization events likely initiated by migratory species that led to speciation, including 44 cases among recently extinct species. By comparing, for all islands, the proportion of island endemic species that derived from migratory drop-off with the proportion of migratory species among potential colonizers, we showed that seasonal migration has a larger effect on island endemic richness than direct dispersal. We also found that the role of migration in island colonization increases with the geographic isolation of islands. Furthermore, the success of speciation events depends in part on species biogeographic and ecological factors, here positively associated with greater range size and larger flock sizes. These results highlight the importance of shifts in migratory behaviour in the speciation process and calls for greater consideration of migratory drop-off in the biogeographic distribution of birds.

Undiscovered bird extinctions obscure the true magnitude of human-driven extinction waves.

Birds are among the best-studied animal groups, but their prehistoric diversity is poorly known due to low fossilization potential. Hence, while many human-driven bird extinctions (i.e., extinctions caused directly by human activities such as hunting, as well as indirectly through human-associated impacts such as land use change, fire, and the introduction of invasive species) have been recorded, the true number is likely much larger. Here, by combining recorded extinctions with model estimates based on the completeness of the fossil record, we suggest that at least ~1300-1500 bird species (~12% of the total) have gone extinct since the Late Pleistocene, with 55% of these extinctions undiscovered (not yet discovered or left no trace). We estimate that the Pacific accounts for 61% of total bird extinctions. Bird extinction rate varied through time with an intense episode ~1300 CE, which likely represents the largest human-driven vertebrate extinction wave ever, and a rate 80 (60-95) times the background extinction rate. Thus, humans have already driven more than one in nine bird species to extinction, with likely severe, and potentially irreversible, ecological and evolutionary consequences.

Rediscovery of the lost skink Proscelotes aenea and implications for conservation.

Biodiversity loss is recognized as a grand challenge of the twenty-first century but ascertaining when a species is "lost" can be incredibly difficult-since the absence of evidence is not evidence of absence. This may be a relatively easy task for large and conspicuous animals, but extremely difficult for those living hidden lives or at low population sizes. We showcase this challenge by focusing on Africa's montane skink, Proscelotes aenea (Barbour & Loveridge 1928). In this study, we embarked on a year-long intensive survey to find this fossorial species in Lumbo, Northern Mozambique, the only remaining location where it may still occur but was recorded for the last time over 100 years ago. We located the species already after 20 days of intensive and targeted searching by five members of our team. The finding allowed us to describe, for the first time, details on the biology and ecology of the species, alongside photos and videos of live specimens (including a pregnant female), and to sequence DNA from the species, which we used to infer the phylogenetic placement. Our combined 12S and 16S phylogenetic analysis weakly suggest that the genus Proscelotes may not be monophyletic and therefore requires further phylogenetic work and potentially taxonomic revision. We also gathered evidence of a possible decrease in population abundance and, based on the species' ecology, we identified urbanization as a potential key threat, which could lead to the local or global extirpation of the species. We call for urgent conservation actions that help protect the future of the montane skink, and additional surveys to map its full distribution. As countries now work towards implementing the goals and targets of the Kunming-Montreal Global Biodiversity Framework, our study demonstrates the need for proper investments in biodiversity inventories and monitoring in order to halt species extinctions by 2030.

Madagascar's extraordinary biodiversity: Evolution, distribution, and use.

Madagascar's biota is hyperdiverse and includes exceptional levels of endemicity. We review the current state of knowledge on Madagascar's past and current terrestrial and freshwater biodiversity by compiling and presenting comprehensive data on species diversity, endemism, and rates of species description and human uses, in addition to presenting an updated and simplified map of vegetation types. We report a substantial increase of records and species new to science in recent years; however, the diversity and evolution of many groups remain practically unknown (e.g., fungi and most invertebrates). Digitization efforts are increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge and identifying gaps in our understanding, particularly as species richness corresponds closely to collection effort. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. We highlight humid forests as centers of diversity and endemism because of their role as refugia and centers of recent and rapid radiations. However, the distinct endemism of other areas, such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest, is also biologically important despite lower species richness. The documented uses of Malagasy biodiversity are manifold, with much potential for the uncovering of new useful traits for food, medicine, and climate mitigation. The data presented here showcase Madagascar as a unique "living laboratory" for our understanding of evolution and the complex interactions between people and nature. The gathering and analysis of biodiversity data must continue and accelerate if we are to fully understand and safeguard this unique subset of Earth's biodiversity.

Madagascar's extraordinary biodiversity: Threats and opportunities.

Madagascar's unique biota is heavily affected by human activity and is under intense threat. Here, we review the current state of knowledge on the conservation status of Madagascar's terrestrial and freshwater biodiversity by presenting data and analyses on documented and predicted species-level conservation statuses, the most prevalent and relevant threats, ex situ collections and programs, and the coverage and comprehensiveness of protected areas. The existing terrestrial protected area network in Madagascar covers 10.4% of its land area and includes at least part of the range of the majority of described native species of vertebrates with known distributions (97.1% of freshwater fishes, amphibians, reptiles, birds, and mammals combined) and plants (67.7%). The overall figures are higher for threatened species (97.7% of threatened vertebrates and 79.6% of threatened plants occurring within at least one protected area). International Union for Conservation of Nature (IUCN) Red List assessments and Bayesian neural network analyses for plants identify overexploitation of biological resources and unsustainable agriculture as the most prominent threats to biodiversity. We highlight five opportunities for action at multiple levels to ensure that conservation and ecological restoration objectives, programs, and activities take account of complex underlying and interacting factors and produce tangible benefits for the biodiversity and people of Madagascar.

Snakebite incidence in rural sub-Saharan Africa might be severely underestimated.

Snakebites in sub-Saharan Africa account for 20,000 to 32,000 annual deaths. But since most data is retrieved from hospital or incomplete central databases, and many victims do not seek hospital treatment or prefer traditional remedies, the current numbers are likely underestimated. In order to reduce snakebite incidence by 50% by 2030 as targeted by World Health Organization, it is crucial to accurately quantify and understand the current rates of snakebite incidence, which can only be reliably measured through household surveys. In this study, we interviewed 1037 households in nine communities in Cabo Delgado, northern Mozambique. Our aim was to quantify true snakebite incidence and under-reporting, by comparing the total number of snakebites reported to our team during household surveys with the subset of reports that reached health centers. We additionally quantified snakebite incidence in terms of species, location of the attack, type of treatment, season, and gender of the victims. These data allow us to propose conservative extrapolations of snakebite incidence and mortality for the province of Cabo Delgado and for Mozambique. Of all snakebites reported in the surveys (N = 296), most incidents were treated exclusively by traditional doctors (N = 174; 59%) and 25% were not seen by any doctor. Most bites occurred on farms and during the rainy season. Using a conservative estimation where we assume our results to be extrapolatable for the whole of rural Mozambique, but considering snakebites in urban areas to be inexistent, we propose that in Cabo Delgado, every year at least 6124 people are victims of snakebites, of which at least 791 result in deaths. In Mozambique, we extrapolated that every year at least 69,261 people are victims of snakebite, of which at least 8950 result in death (one in eight snakebites is fatal). Our estimates are the first for Mozambique based on data retrieved in the country, and despite being an underestimation they increase snakebite incidence levels ten-fold and the number of deaths by 30-fold. Urgent and widespread surveys are needed to further assess the full extent of snakebites in sub-Saharan Africa, explore regional patterns and develop mitigation plans.

Phylogenetic and functional clustering illustrate the roles of adaptive radiation and dispersal filtering in jointly shaping late-Quaternary mammal assemblages on oceanic islands.

Islands frequently harbour unique assemblages of species, yet their ecological roles and differences are largely ignored in island biogeography studies. Here, we examine eco-evolutionary processes structuring mammal assemblages on oceanic islands worldwide, including all extant and extinct late-Quaternary mammal species. We find island mammal assemblages tend to be phylogenetically clustered (share more recent evolutionary histories), with clustering increasing with island area and isolation. We also observe that mammal assemblages often tend to be functionally clustered (share similar traits), but the strength of clustering is weak and generally independent from island area or isolation. These findings indicate the important roles of in situ speciation and dispersal filtering in shaping island mammal assemblages under pre-anthropogenic conditions, notably through adaptive radiation of a few clades (e.g. bats, with generally high dispersal abilities). Our study demonstrates that considering the functional and phylogenetic axes of diversity can better reveal the eco-evolutionary processes of island community assembly.

Species perceived to be dangerous are more likely to have distinctive local names.

BACKGROUND: Species with direct uses, such as sources of food, shelter, building material and medicine tend to have more specific local names. But could the same apply for species that people fear? METHODS: To address this question, here we explore the behavior and perception of species diversity and dangerousness through a survey of 1037 households in nine villages in Cabo Delgado, northern Mozambique. We compare people's knowledge of snakes with that of lizards and amphibians. RESULTS: We find that northern Mozambicans know four to five times more local names for snakes than for lizards and frogs, despite the local species richness of snakes being comparable to the diversity of lizards and frogs. We further find that local knowledge was on par with the academic literature regarding snakebite symptoms. CONCLUSIONS: Our results suggest that fear can increase the level of specificity in naming species among indigenous communities, which could lead to biases in the mapping and protection of species that include data from citizen reports.

Loss of functional diversity through anthropogenic extinctions of island birds is not offset by biotic invasions.

Human impacts reshape ecological communities through the extinction and introduction of species. The combined impact of these factors depends on whether non-native species fill the functional roles of extinct species, thus buffering the loss of functional diversity. This question has been difficult to address, because comprehensive information about past extinctions and their traits is generally lacking. We combine detailed information about extinct, extant, and established alien birds to quantify historical changes in functional diversity across nine oceanic archipelagos. We found that alien species often equal or exceed the number of anthropogenic extinctions yet apparently perform a narrower set of functional roles as current island assemblages have undergone a substantial and ubiquitous net loss in functional diversity and increased functional similarity among assemblages. Our results reveal that the introduction of alien species has not prevented anthropogenic extinctions from reducing and homogenizing the functional diversity of native bird assemblages on oceanic archipelagos.

Mapping Africa's Biodiversity: More of the Same Is Just Not Good Enough.

Species distribution data are fundamental to the understanding of biodiversity patterns and processes. Yet, such data are strongly affected by sampling biases, mostly related to site accessibility. The understanding of these biases is therefore crucial in systematics, biogeography, and conservation. Here we present a novel approach for quantifying sampling effort and its impact on biodiversity knowledge, focusing on Africa. In contrast to previous studies assessing sampling completeness (percentage of species recorded in relation to predicted), we investigate whether the lack of knowledge of a site attracts scientists to visit these areas and collect samples of species. We then estimate the time required to sample 90% of the continent under a Weibull distributed biodiversity sampling rate and the number of sampling events required to record $ \ge $50% of the species. Using linear and spatial regression models, we show that previous sampling has been strongly influencing the resampling of areas, attracting repeated visits. This bias has existed for over two centuries, has increased in recent decades, and is most pronounced among mammals. It may take between 172 and 274 years, depending on the group, to achieve at least one sampling event per grid cell in the entire continent. Just one visit will, however, not be enough: in order to record $ \ge $50% of the current diversity, it will require at least 12 sampling events for amphibians, 13 for mammals, and 27 for birds. Our results demonstrate the importance of sampling areas that lack primary biodiversity data and the urgency with which this needs to be done. Current practice is insufficient to adequately classify and map African biodiversity; it can lead to incorrect conclusions being drawn from biogeographic analyses and can result in misleading and self-reinforcing conservation priorities. [Amphibians; birds; mammals; sampling bias; sampling gaps; Wallacean shortfall.].

Taxonomic revision of the genus Xenopholis Peters, 1869 (Serpentes: Dipsadidae): Integrating morphology with ecological niche.

A reliable identification and delimitation of species is an essential pre-requisite for many fields of science and conservation. The Neotropical herpetofauna is the world's most diverse, including many taxa of uncertain or debated taxonomy. Here we tackle one such species complex, by evaluating the taxonomic status of species currently allocated in the snake genus Xenopholis (X. scalaris, X. undulatus, and X. werdingorum). We base our conclusions on concordance between quantitative (meristic and morphometric) and qualitative (color pattern, hemipenes and skull features) analyses of morphological characters, in combination with ecological niche modeling. We recognize all three taxa as valid species and improve their respective diagnosis, including new data on color in life, pholidosis, bony morphology, and male genitalia. We find low overlap among the niches of each species, corroborating the independent source of phenotypic evidence. Even though all three species occur in the leaf litter of distinct forested habitats, Xenopholis undulatus is found in the elevated areas of the Brazilian Shield (Caatinga, Cerrado and Chaco), whereas X. scalaris occurs in the Amazon and Atlantic rainforests, and X. werdingorum in the Chiquitanos forest and Pantanal wetlands. We discuss the disjunct distribution between Amazonian and Atlantic Forest snake species in the light of available natural history and ecological aspects. This study shows the advantages of combining multiple data sources for reliable identification and circumscription of ecologically similar species.

Disproportionate extinction of South American mammals drove the asymmetry of the Great American Biotic Interchange.

The interchange between the previously disconnected faunas of North and South America was a massive experiment in biological invasion. A major gap in our understanding of this invasion is why there was a drastic increase in the proportion of mammals of North American origin found in South America. Four nonmutually exclusive mechanisms may explain this asymmetry: 1) Higher dispersal rate of North American mammals toward the south, 2) higher origination of North American immigrants in South America, 3) higher extinction of mammals with South American origin, and 4) similar dispersal rate but a larger pool of native taxa in North versus South America. We test among these mechanisms by analyzing ∼20,000 fossil occurrences with Bayesian methods to infer dispersal and diversification rates and taxonomic selectivity of immigrants. We find no differences in the dispersal and origination rates of immigrants. In contrast, native South American mammals show higher extinction. We also find that two clades with North American origin (Carnivora and Artiodactyla) had significantly more immigrants in South America than other clades. Altogether, the asymmetry of the interchange was not due to higher origination of immigrants in South America as previously suggested, but resulted from higher extinction of native taxa in southern South America. These results from one of the greatest biological invasions highlight how biogeographic processes and biotic interactions can shape continental diversity.

The past and future human impact on mammalian diversity.

To understand the current biodiversity crisis, it is crucial to determine how humans have affected biodiversity in the past. However, the extent of human involvement in species extinctions from the Late Pleistocene onward remains contentious. Here, we apply Bayesian models to the fossil record to estimate how mammalian extinction rates have changed over the past 126,000 years, inferring specific times of rate increases. We specifically test the hypothesis of human-caused extinctions by using posterior predictive methods. We find that human population size is able to predict past extinctions with 96% accuracy. Predictors based on past climate, in contrast, perform no better than expected by chance, suggesting that climate had a negligible impact on global mammal extinctions. Based on current trends, we predict for the near future a rate escalation of unprecedented magnitude. Our results provide a comprehensive assessment of the human impact on past and predicted future extinctions of mammals.

Frugivore-fruit size relationships between palms and mammals reveal past and future defaunation impacts.

Mammalian frugivores are critical seed dispersers, but many are under threat of extinction. Futhermore, the impact of past and future defaunation on plant assemblages has yet to be quantified at the global scale. Here, we integrate palm and mammalian frugivore trait and occurrence data and reveal a global positive relationship between fruit size and frugivore body size. Global variation in fruit size is better explained by present-day frugivore assemblages than by Late Pleistocene assemblages, suggesting ecological and evolutionary reorganization after end-Pleistocene extinctions, except in the Neotropics, where some large-fruited palm species may have outlived their main seed dispersers by thousands of years. Our simulations of frugivore extinction over the next 100 years suggest that the impact of defaunation will be highest in the Old World tropics, and an up to 4% assemblage-level decrease in fruit size would be required to maintain the global body size-fruit size relationship. Overall, our results suggest that while some palm species may be able to keep pace with future defaunation through evolutionary changes in fruit size, large-fruited species may be especially vulnerable to continued defaunation.

Endemism patterns are scale dependent.

Areas of endemism are important in biogeography because they capture facets of biodiversity not represented elsewhere. However, the scales at which they are relevant to research and conservation are poorly analysed. Here, we calculate weighted endemism (WE) and phylogenetic endemism (PE) separately for all birds and amphibians across the globe. We show that scale dependence is widespread for both indices and manifests across grain sizes, spatial extents and taxonomic treatments. Variations in taxonomic opinions-whether species are treated by systematic 'lumping' or 'splitting'-can profoundly affect the allocation of WE hotspots. Global patterns of PE can provide insights into complex evolutionary processes but this congruence is lost at the continental to country extents. These findings are explained by environmental heterogeneity at coarser grains, and to a far lesser extent at finer resolutions. Regardless of scale, we find widespread deficits of protection for endemism hotspots. Our study presents a framework for assessing areas for conservation that are robust to assumptions on taxonomy, spatial grain and extent.

Rethinking megafauna.

Concern for megafauna is increasing among scientists and non-scientists. Many studies have emphasized that megafauna play prominent ecological roles and provide important ecosystem services to humanity. But, what precisely are 'megafauna'? Here, we critically assess the concept of megafauna and propose a goal-oriented framework for megafaunal research. First, we review definitions of megafauna and analyse associated terminology in the scientific literature. Second, we conduct a survey among ecologists and palaeontologists to assess the species traits used to identify and define megafauna. Our review indicates that definitions are highly dependent on the study ecosystem and research question, and primarily rely on ad hoc size-related criteria. Our survey suggests that body size is crucial, but not necessarily sufficient, for addressing the different applications of the term megafauna. Thus, after discussing the pros and cons of existing definitions, we propose an additional approach by defining two function-oriented megafaunal concepts: 'keystone megafauna' and 'functional megafauna', with its variant 'apex megafauna'. Assessing megafauna from a functional perspective could challenge the perception that there may not be a unifying definition of megafauna that can be applied to all eco-evolutionary narratives. In addition, using functional definitions of megafauna could be especially conducive to cross-disciplinary understanding and cooperation, improvement of conservation policy and practice, and strengthening of public perception. As megafaunal research advances, we encourage scientists to unambiguously define how they use the term 'megafauna' and to present the logic underpinning their definition.

The Global Museum: natural history collections and the future of evolutionary science and public education.

Natural history museums are unique spaces for interdisciplinary research and educational innovation. Through extensive exhibits and public programming and by hosting rich communities of amateurs, students, and researchers at all stages of their careers, they can provide a place-based window to focus on integration of science and discovery, as well as a locus for community engagement. At the same time, like a synthesis radio telescope, when joined together through emerging digital resources, the global community of museums (the 'Global Museum') is more than the sum of its parts, allowing insights and answers to diverse biological, environmental, and societal questions at the global scale, across eons of time, and spanning vast diversity across the Tree of Life. We argue that, whereas natural history collections and museums began with a focus on describing the diversity and peculiarities of species on Earth, they are now increasingly leveraged in new ways that significantly expand their impact and relevance. These new directions include the possibility to ask new, often interdisciplinary questions in basic and applied science, such as in biomimetic design, and by contributing to solutions to climate change, global health and food security challenges. As institutions, they have long been incubators for cutting-edge research in biology while simultaneously providing core infrastructure for research on present and future societal needs. Here we explore how the intersection between pressing issues in environmental and human health and rapid technological innovation have reinforced the relevance of museum collections. We do this by providing examples as food for thought for both the broader academic community and museum scientists on the evolving role of museums. We also identify challenges to the realization of the full potential of natural history collections and the Global Museum to science and society and discuss the critical need to grow these collections. We then focus on mapping and modelling of museum data (including place-based approaches and discovery), and explore the main projects, platforms and databases enabling this growth. Finally, we aim to improve relevant protocols for the long-term storage of specimens and tissues, ensuring proper connection with tomorrow's technologies and hence further increasing the relevance of natural history museums.

Trophic rewilding presents regionally specific opportunities for mitigating climate change.

Large-bodied mammalian herbivores can influence processes that exacerbate or mitigate climate change. Herbivore impacts are, in turn, influenced by predators that place top-down forcing on prey species within a given body size range. Here, we explore how the functional composition of terrestrial large-herbivore and -carnivore guilds varies between three mammal distribution scenarios: Present-Natural, Current-Day and Extant-Native Trophic (ENT) Rewilding. Considering the effects of herbivore species weakly influenced by top-down forcing, we quantify the relative influence keystone large-herbivore guilds have on methane emissions, woody vegetation expansion, fire dynamics, large-seed dispersal, and nitrogen and phosphorus transport potential. We find strong regional differences in the number of herbivores under weak top-down regulation between our three scenarios, with important implications for how they will influence climate change relevant processes. Under the Present-Natural non-ruminant, megaherbivore, browsers were a particularly important guild across much of the world. Megaherbivore extinction and range contraction and the arrival of livestock mean large, ruminant, grazers have become more dominant. ENT Rewilding can restore the Afrotropics and the Indo-Malay realm to the Present-Natural benchmark, but causes top-down forcing of the largest herbivores to become commonplace elsewhere. ENT Rewilding will reduce methane emissions, but does not maximize natural climate solution potential. This article is part of the theme issue 'Climate change and ecosystems: threats, opportunities and solutions'.

Brain expansion in early hominins predicts carnivore extinctions in East Africa.

While the anthropogenic impact on ecosystems today is evident, it remains unclear if the detrimental effect of hominins on co-occurring biodiversity is a recent phenomenon or has also been the pattern for earlier hominin species. We test this using the East African carnivore fossil record. We analyse the diversity of carnivores over the last four million years and investigate whether any decline is related to an increase in hominin cognitive capacity, vegetation changes or climatic changes. We find that extinction rates in large carnivores correlate with increased hominin brain size and with vegetation changes, but not with precipitation or temperature changes. While temporal analyses cannot distinguish between the effects of vegetation changes and hominins, we show through spatial analyses of contemporary carnivores in Africa that only hominin causation is plausible. Our results suggest that substantial anthropogenic influence on biodiversity started millions of years earlier than currently assumed.