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Done but not dusted: Reflections on the first global reptile assessment and priorities for the second

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Abstract

The IUCN recently coordinated the first assessment of extinction risk of the world's reptile species. This monumental undertaking allows, for the first time, an examination of threats and prioritization of conservation effort, not just for reptiles, but for land vertebrates as a whole. Reptiles are now the largest class of land vertebrates in terms of species numbers. The dynamic nature of reptile taxonomy, the 18 years it took for the Global Reptile Assessment to be completed, the poor state of knowledge for many species – especially of squamates – and the evolving nature of threats, however, all highlight the need for continued monitoring of reptile species and threats. Here we review the status of reptile conservation assessments, and identify the challenges facing the next reptile assessments. We then recommend potential avenues that could facilitate efficient, accurate and timely future assessments.

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Accurate taxonomy is central to the study of biological diversity, as it provides the needed evolutionary framework for taxon sampling and interpreting results. While the number of recognized species in the class Mammalia has increased through time, tabulation of those increases has relied on the sporadic release of revisionary compendia like the Mammal Species of the World (MSW) series. Here, we present the Mammal Diversity Database (MDD), a digital, publically accessible, and updateable list of all mammalian species, now available online: https://mammaldiversity.org. The MDD will continue to be updated as manuscripts describing new species and higher taxonomic changes are released. Starting from the baseline of the 3rd edition of MSW (MSW3), we performed a review of taxonomic changes published since 2004 and digitally linked species names to their original descriptions and subsequent revisionary articles in an interactive, hierarchical database. We found 6,495 species of currently recognized mammals (96 recently extinct, 6,399 extant), compared to 5,416 in MSW3 (75 extinct, 5,341 extant)—an increase of 1,079 species in about 13 years, including 11 species newly described as having gone extinct in the last 500 years. We tabulate 1,251 new species recognitions, at least 172 unions, and multiple major, higher-level changes, including an additional 88 genera (1,314 now, compared to 1,226 in MSW3) and 14 newly recognized families (167 compared to 153). Analyses of the description of new species through time and across biogeographic regions show a long-term global rate of ~25 species recognized per year, with the Neotropics as the overall most species-dense biogeographic region for mammals, followed closely by the Afrotropics. The MDD provides the mammalogical community with an updateable online database of taxonomic changes, joining digital efforts already established for amphibians (AmphibiaWeb, AMNH’s Amphibian Species of the World), birds (e.g., Avibase, IOC World Bird List, HBW Alive), non-avian reptiles (The Reptile Database), and sh (e.g., FishBase, Catalog of Fishes).
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Aim: Small geographic ranges make species especially prone to extinction from anthropogenic disturbances or natural stochastic events. We assemble and analyse a comprehensive dataset of all the world's lizard species and identify the species with the smallest ranges—those known only from their type localities. We compare them to wide-ranging species to infer whether specific geographic regions or biological traits predispose species to have small ranges. Location: Global. Methods: We extensively surveyed museum collections, the primary literature and our own field records to identify all the species of lizards with a maximum linear geographic extent of <10 km. We compared their biogeography, key biological traits and threat status to those of all other lizards. Results: One in seven lizards (927 of the 6,568 currently recognized species) are known only from their type localities. These include 213 species known only from a single specimen. Compared to more wide-ranging taxa, they mostly inhabit relatively inaccessible regions at lower, mostly tropical, latitudes. Surprisingly, we found that burrowing lifestyle is a relatively unimportant driver of small range size. Geckos are especially prone to having tiny ranges, and skinks dominate lists of such species not seen for over 50 years, as well as of species known only from their holotype. Two-thirds of these species have no IUCN assessments, and at least 20 are extinct. Main conclusions: Fourteen per cent of lizard diversity is restricted to a single location, often in inaccessible regions. These species are elusive, usually poorly known and little studied. Many face severe extinction risk, but current knowledge is inadequate to properly assess this for all of them. We recommend that such species become the focus of taxonomic, ecological and survey efforts.
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The distributions of amphibians, birds and mammals have underpinned global and local conservation priorities, and have been fundamental to our understanding of the determinants of global biodiversity. In contrast, the global distributions of reptiles, representing a third of terrestrial vertebrate diversity, have been unavailable. This prevented the incorporation of reptiles into conservation planning and biased our understanding of the underlying processes governing global vertebrate biodiversity. Here, we present and analyse the global distribution of 10,064 reptile species (99% of extant terrestrial species). We show that richness patterns of the other three tetrapod classes are good spatial surrogates for species richness of all reptiles combined and of snakes, but characterize diversity patterns of lizards and turtles poorly. Hotspots of total and endemic lizard richness overlap very little with those of other taxa. Moreover, existing protected areas, sites of biodiversity significance and global conservation schemes represent birds and mammals better than reptiles. We show that additional conservation actions are needed to effectively protect reptiles, particularly lizards and turtles. Adding reptile knowledge to a global complementarity conservation priority scheme identifies many locations that consequently become important. Notably, investing resources in some of the world’s arid, grassland and savannah habitats might be necessary to represent all terrestrial vertebrates efficiently.
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Responding to purported taxonomic anarchy, in an article published in the widely read journal Nature, Garnett & Christidis (2017) [hereafter GC] opined on the need for “standardized global species lists”, at the behest of conservationists, and proposed the construction of a judicial committee to “restrict … freedom of taxonomic action” and promote taxonomic stability. Here we reflect on this perspective and contest that the view of GC conflicts with some basic and indisputable principles underpinning the philosophy of science, most notably: it must be free. They appear to believe that taxonomic revisions should be based on political, economic and conservation concerns, and they treat species as fixed real entities, instead of refutable scientific hypotheses. In addition to such theoretical misconceptions, GC did not consider important practical aspects of what they term taxonomic anarchy, most significantly the participation of conservationists as authors of taxonomic works, and the importance of alternative management units, a well-established discussion in conservation biology.
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This is our 8th edition of an annotated checklist of all recognized and named taxa of the world’s modern chelonian fauna, documenting recent changes and controversies in nomenclature through early 2017, and including all primary synonyms, updated from 7 previous checklists (Turtle Taxonomy Working Group 2007b, 2009, 2010, 2011, 2012, 2014; Rhodin et al. 2008). We provide an updated comprehensive listing of taxonomy, names, and conservation status of all turtles and tortoises of the world, including detailed distribution maps. We strive to record the most recent justified taxonomic assignment of taxa in a hierarchical framework, providing annotations, including alternative possible arrangements, for some proposed changes. We provide common English names and detailed distributional data for all taxa, listing occurrence by countries and many smaller political or geographic subunits (states or regions), including indications of native, extirpated, and introduced (modern or prehistoric) populations. We include current published and draft IUCN Red List status assessments for all turtles, as well as CITES listings. The diversity of turtles and tortoises in the world that has existed in modern times (since 1500 AD) and currently generally recognized as distinct and included in this checklist, now consists of 356 species. Of these, 60 are polytypic, representing 122 additional recognized subspecies, or 478 total taxa of modern turtles and tortoises. Of these, 7 species and 3 subspecies, or 10 taxa (2.1%), have gone extinct. As of the current IUCN 2017 Red List, 148 turtle species (60.4% of 245 species listed, 41.6% of all 356 recognized modern species) are officially regarded as globally Threatened (Critically Endangered [CR], Endangered [EN], or Vulnerable [VU]). We record additional draft Red List assessments by the IUCN Tortoise and Freshwater Turtle Specialist Group (TFTSG) of previously “unevaluated” species, and updated draft re-assessments of previously listed species, allowing us to evaluate the overall current threat levels for all turtles and tortoises. Of the 356 total species of turtles and tortoises, 114 (32.0%) are CR or EN, 179 (50.3%) are Threatened (CR, EN, or VU), and 186 (52.2%) are Threatened or Extinct. If we provisionally adjust for predicted threat rates of Data Deficient and Not Evaluated species, then ca. 59% of all extant turtles are Threatened. These numbers and percentages of Threatened species have increased since our last checklist. Turtles are among the most threatened of the major groups of vertebrates, in general more than birds, mammals, cartilaginous or bony fishes, or amphibians.
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The classification of complex organisms is in chaos. Stephen T. Garnett and Les Christidis propose a solution.
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Aim A major Late Quaternary vertebrate extinction event affected mostly large-bodied 'megafauna'. This is well documented in both mammals and birds, but evidence of a similar trend in reptiles is scant. We assess the relationship between body size and Late Quaternary extinction in reptiles at the global level. Location Global. Methods We compile a body size database for all 82 reptile species that are known to have gone extinct during the last 50,000 years and compare them with the sizes of 10,090 extant reptile species (97% of known extant diversity). We assess the body size distributions in the major reptile groups: crocodiles, lizards, snakes and turtles, while testing and correcting for a size bias in the fossil record. We examine geographical biases in extinction by contrasting mainland and insular reptile assemblages, and testing for biases within regions and then globally by using geographically weighted models. Results Extinct reptiles were larger than extant ones, but there was considerable variation in extinction size biases among groups. Extinct lizards and turtles were large, extinct crocodiles were small and there was no trend in snakes. Lizard lineages vary in the way their extinction is related to size. Extinctions were particularly prevalent on islands, with 73 of the 82 extinct species being island endemics. Four others occurred in Australia. The fossil record is biased towards large-bodied reptiles, but extinct lizards were larger than extant ones even after we account for this. Main conclusions Body size played a complex role in the extinction of Late Quaternary reptiles. Larger lizard and turtle species were clearly more affected by extinction mechanisms such as over exploitation and invasive species, resulting in a prevalence of large-bodied species among extinct taxa. Insularity was by far the strongest correlate of recent reptile extinctions, suggesting that size-biased extinction mechanisms are amplified in insular environments.
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While greater research on threatened species alone cannot ensure their protection, understanding taxonomic bias may be helpful to address knowledge gaps in order to identify research directions and inform policy. Using data for over 10 000 animal species listed on the International Union for Conservation of Nature Red List, we investigated taxonomic and geographic biodiversity conservation research trends worldwide. We found extreme bias in conservation research effort on threatened vertebrates compared with lesser-studied invertebrates in both terrestrial and aquatic habitats at a global scale. Based on an analysis of common threats affecting vertebrates and invertebrates, we suggest a path forward for narrowing the research gap between threatened vertebrates and invertebrates.
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The mechanisms that underpin ecological speciation, morphological convergence and the evolution of ecological morphotypes (ecomorphs) in squamates have allowed for a better appreciation of the speciation process in chameleons. In particular, attention has been drawn to several populations of chameleons (Sauria, Chamaeleonidae, Bradypodion) from the Cape Fold Mountains, South Africa. Previous work suggested that these populations are genetically divergent, but with strong similarities in phenotype. Using an integrative taxonomic approach that accounts for genetic diversity, habitat and morphology, three of these populations are described as species. One population is from an isolated forest patch and is genetically different at the species level, but morphologically similar to Bradypodion damaranum (Boulenger, 1887) from forested areas in the Knysna region. Although not sister species, the two are in the same clade and probably diverged through vicariance of the forest. Two other populations are from fynbos habitat in adjacent mountain ranges (Tsitsikamma/Langkloof/Kouga mountains and Baviaanskloof Mountains) and are also morphologically similar, but genetically divergent at the species level. These two species are not sister taxa and are not in the same clade yet have a virtually identical phenotype presumably as the result of convergent evolution for the fynbos habitat. Within the context of morphological taxonomy, these populations have been difficult to evaluate. However, when viewed in the context of ecological speciation, convergence and morphological conservatism, the species boundaries are apparent, allowing for them to be described as new taxa.
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Book
This is our 9th edition of an annotated checklist and atlas of all recognized taxa of the world’s modern turtle and tortoise fauna, documenting recent changes and controversies through mid-2021, and including all primary synonyms, updated from eight previous checklists. We provide an updated comprehensive listing of taxonomy and nomenclature, including type localities, type specimens, detailed distribution maps, as well as calculated presumed historic indigenous ranges, conservation status, and maximum known sex-based carapace lengths for all taxa. We strive to record the most recent justified taxonomic assignment of taxa in a hierarchical framework, providing detailed annotations, including alternative arrangements for a few taxa. We include current published and provisional IUCN Red List status assessments for all species, as well as current listings on CITES appendices. The diversity of turtles and tortoises in the world that has existed in modern times (since 1500 CE) and currently generally recognized as distinct and included in this checklist, now consists of 357 species. Of these, 58 are polytypic, representing 129 additional recognized subspecies (one unnamed), or 486 total taxa of modern chelonians, increased from 478 taxa in our previous checklist. Of these, 5 species and 5 subspecies (one unnamed), or 10 taxa (2.1%), are extinct. We also include a supplementary checklist of 17 taxa of terrestrial chelonians that went extinct during the Holocene from ca. 10,000 BCE to 1500 CE. As of the current IUCN 2021 Red List, 171 turtle species (62.4% of the 274 species red-listed, 47.9% of all 357 recognized modern species) are officially regarded as globally Threatened (Critically Endangered [CR], Endangered [EN], or Vulnerable [VU]). We record additional provisional Red List assessments by the IUCN Tortoise and Freshwater Turtle Specialist Group, allowing us to evaluate the overall current threat levels for all 357 species of turtles and tortoises. Of these, 183 (51.3%) are Threatened (CR, EN, or VU); if we provisionally adjust for predicted threat rates of Data Deficient (DD) species, then ca. 55.9% of all extant turtles are Threatened. These numbers and percentages of Threatened species have increased since our last checklist, although our reclassification of 12 Threatened Galápagos tortoises as subspecies rather than species has moderated the results; the number and percentage of Threatened species increases to 193 (52.3% of 369) if they are considered full species. Turtles and tortoises are among the most threatened of the major groups of vertebrates.
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Our knowledge of the conservation status of reptiles, the most diverse class of terrestrial vertebrates, has improved dramatically over the past decade, but still lags behind that of the other tetrapod groups. Here, we conduct the first comprehensive evaluation (~92% of the world's ~1714 described species) of the conservation 1 Joint senior authors. D.G. Chapple et al. Biological Conservation 257 (2021) 109101 3 Lizard Protected areas Reptile Skink Taxonomic bias status of skinks (Scincidae), a speciose reptile family with a worldwide distribution. Using International Union for Conservation of Nature (IUCN) criteria, we report that ~20% of species are threatened with extinction, and nine species are Extinct or Extinct in the Wild. The highest levels of threat are evident in Madagascar and the Neotropics, and in the subfamilies Mabuyinae, Eugongylinae and Scincinae. The vast majority of threatened skink species were listed based primarily on their small geographic ranges (Criterion B, 83%; Criterion D2, 13%). Although the population trend of 42% of species was stable, 14% have declining populations. The key threats to skinks are habitat loss due to agriculture, invasive species, and biological resource use (e.g., hunting, timber harvesting). The distributions of 61% of species do not overlap with protected areas. Despite our improved knowledge of the conservation status of the world's skinks, 8% of species remain to be assessed, and 14% are listed as Data Deficient. The conservation status of almost a quarter of the world's skink species thus remains unknown. We use our updated knowledge of the conservation status of the group to develop and outline the priorities for the conservation assessment and management of the world's skink species.
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The complexity and transnational nature of environmental issues our societies are facing, and the need to build scientific capacity building in many regions of the world, require the establishment of global collaborative research networks that include a diverse representation of scientists from multiple geographical, cultural and socio-economical backgrounds. This topic is currently gaining relevance in the field of soil ecology, as awareness is increasing that recognizing, addressing, and predicting the changes that soils are facing requires global collaboration. However, the setup, management and operation of research networks imply multiple tasks and challenges that need to be carefully considered. While major issues related to the setup of such networks in ecology have already been described in the literature, here we focus on aspects that are important to make them truly global and inclusive. For doing so, we introduce a series of recommendations to successfully develop research networks that: i) explore ecological questions requiring data with a global coverage and ii) foster the participation of scientists who have been traditionally underrepresented in international research collaborations. These recommendations, which are based on our own experience, also provide practical advice to anyone aiming to initiate (or join) a global collaborative research network to the mutual benefit of all contributors.
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Freshwater ecosystems are among the most diverse and dynamic ecosystems on Earth. At the same time, they are among the most threatened ecosystems but remain underrepresented in biodiversity research and conservation efforts. The rate of decline of vertebrate populations is much higher in freshwaters than in terrestrial or marine realms. Freshwater megafauna (i.e., freshwater animals that can reach a body mass ≥30 kg) are intrinsically prone to extinction due to their large body size, complex habitat requirements and slow life‐history strategies such as long life span and late maturity. However, population trends and distribution changes of freshwater megafauna, at continental or global scales, remain unclear. In the present study, we compiled population data of 126 freshwater megafauna species globally from the Living Planet Database and available literature, and distribution data of 44 species inhabiting Europe and the United States from literature and databases of the International Union for Conservation of Nature and NatureServe. We quantified changes in population abundance and distribution range of freshwater megafauna species. Globally, freshwater megafauna populations declined by 88% from 1970 to 2012, with the highest declines in the Indomalaya and Palearctic realms (−99% and −97%, respectively). Among taxonomic groups, mega‐fishes exhibited the greatest global decline (−94%). In addition, freshwater megafauna experienced major range contractions. For example, distribution ranges of 42% of all freshwater megafauna species in Europe contracted by more than 40% of historical areas. We highlight the various sources of uncertainty in tracking changes in populations and distributions of freshwater megafauna, such as the lack of monitoring data and taxonomic and spatial biases. The detected trends emphasize the critical plight of freshwater megafauna globally and highlight the broader need for concerted, targeted and timely conservation of freshwater biodiversity.
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Addressing global environmental problems requires collaborative international arrangements that incorporate the strengths of multiple partners with cultural, infrastructural, educational, and economic differences to produce more robust research and improved environmental outcomes. This can be especially important for research in the tropics given the ecological importance and economic and social constraints. However, significant economic, social and institutional barriers exist towards establishing effective collaborative networks, especially between North–South partners. In this paper, we integrate best practices from the collaboration and social networking literatures to examine a teaching and research partnership between American and Costa Rican institutions. This case demonstrates the potential for research stations to serve as central nodes in establishing collaborative networks involving researchers, government, and community organizations.
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Climate warming may lower environmental resource levels, growth, and fitness of many ectotherms. In a classic experiment, Brett and colleagues documented that growth rates of salmon depended strikingly on both temperature and food levels. Here we develop a simple bioenergetic model that explores how fixed temperatures and food jointly alter the thermal sensitivity of net energy gain. The model incorporates differing thermal sensitivities of energy intake and metabolism. In qualitative agreement with Brett's results, it predicts that decreased food intake reduces growth rates, lowers optimal temperatures for growth, and lowers the highest temperatures sustaining growth (upper thermal limit). Consequently, ectotherms facing reduced food intake in warm environments should restrict activity to times when low body temperatures are biophysically feasible, but-in a warming world-that will force ectotherms to shorten activity times and thus further reduce food intake. This "metabolic meltdown" is a consequence of declining energy intake coupled with accelerating metabolic costs at high temperatures and with warming-imposed restrictions on activity. Next, we extend the model to explore how increasing mean environmental temperatures alter the thermal sensitivity of growth: when food intake is reduced, optimal temperatures and upper thermal limits for growth are lowered. We discuss our model's key assumptions and caveats as well as its relationship to a recent model for phytoplankton. Both models illustrate that the deleterious impacts of climate warming on ectotherms will be amplified if food intake is also reduced, either because warming reduces standing food resources or because it restricts foraging time.