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      A return-on-investment approach for prioritization of rigorous taxonomic research needed to inform responses to the biodiversity crisis

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          Abstract

          Global biodiversity loss is a profound consequence of human activity. Disturbingly, biodiversity loss is greater than realized because of the unknown number of undocumented species. Conservation fundamentally relies on taxonomic recognition of species, but only a fraction of biodiversity is described. Here, we provide a new quantitative approach for prioritizing rigorous taxonomic research for conservation. We implement this approach in a highly diverse vertebrate group—Australian lizards and snakes. Of 870 species assessed, we identified 282 (32.4%) with taxonomic uncertainty, of which 17.6% likely comprise undescribed species of conservation concern. We identify 24 species in need of immediate taxonomic attention to facilitate conservation. Using a broadly applicable return-on-investment framework, we demonstrate the importance of prioritizing the fundamental work of identifying species before they are lost.

          Abstract

          In order to inform conservation effort, there is urgent need for rigorous taxonomic research to describe species under threat of extinction. Implementation of a new prioritization method identified 282 Australian reptile species needing taxonomic research, of which 17.6% represent undescribed species of conservation concern; this approach could be readily implemented across many faunal groups.

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          The integrative future of taxonomy

          Background Taxonomy is the biological discipline that identifies, describes, classifies and names extant and extinct species and other taxa. Nowadays, species taxonomy is confronted with the challenge to fully incorporate new theory, methods and data from disciplines that study the origin, limits and evolution of species. Results Integrative taxonomy has been proposed as a framework to bring together these conceptual and methodological developments. Here we review perspectives for an integrative taxonomy that directly bear on what species are, how they can be discovered, and how much diversity is on Earth. Conclusions We conclude that taxonomy needs to be pluralistic to improve species discovery and description, and to develop novel protocols to produce the much-needed inventory of life in a reasonable time. To cope with the large number of candidate species revealed by molecular studies of eukaryotes, we propose a classification scheme for those units that will facilitate the subsequent assembly of data sets for the formal description of new species under the Linnaean system, and will ultimately integrate the activities of taxonomists and molecular biologists.
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            The biodiversity of species and their rates of extinction, distribution, and protection.

            Recent studies clarify where the most vulnerable species live, where and how humanity changes the planet, and how this drives extinctions. We assess key statistics about species, their distribution, and their status. Most are undescribed. Those we know best have large geographical ranges and are often common within them. Most known species have small ranges. The numbers of small-ranged species are increasing quickly, even in well-known taxa. They are geographically concentrated and are disproportionately likely to be threatened or already extinct. Current rates of extinction are about 1000 times the likely background rate of extinction. Future rates depend on many factors and are poised to increase. Although there has been rapid progress in developing protected areas, such efforts are not ecologically representative, nor do they optimally protect biodiversity. Copyright © 2014, American Association for the Advancement of Science.
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              How Many Species of Insects and Other Terrestrial Arthropods Are There on Earth?

              In the last decade, new methods of estimating global species richness have been developed and existing ones improved through the use of more appropriate statistical tools and new data. Taking the mean of most of these new estimates indicates that globally there are approximately 1.5 million, 5.5 million, and 7 million species of beetles, insects, and terrestrial arthropods, respectively. Previous estimates of 30 million species or more based on the host specificity of insects to plants now seem extremely unlikely. With 1 million insect species named, this suggests that 80% remain to be discovered and that a greater focus should be placed on less-studied taxa such as many families of Coleoptera, Diptera, and Hymenoptera and on poorly sampled parts of the world. DNA tools have revealed many new species in taxonomically intractable groups, but unbiased studies of previously well-researched insect faunas indicate that 1-2% of species may be truly cryptic.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                1 June 2021
                June 2021
                1 June 2021
                : 19
                : 6
                : e3001210
                Affiliations
                [1 ] Department of Sciences, Museums Victoria, Melbourne, Australia
                [2 ] Department of Biology, Washington University, St. Louis, MI, United States of America
                [3 ] School of Biological Sciences, Monash University, Clayton, Australia
                [4 ] Division of Ecology & Evolution, Research School of Biology, Australian National University, Canberra, Australia
                [5 ] Biodiversity & Geosciences Program, Queensland Museum, Brisbane, Australia
                [6 ] Snake & Lizard Red List Authority, CI-IUCN Biodiversity Assessment Unit, IUCN North America Office, Washington, DC, United States of America
                [7 ] South Australian Museum, North Terrace, Adelaide, Australia
                [8 ] Collections & Research, Western Australian Museum, Welshpool, Australia
                [9 ] Department of Life & Environmental Sciences, University of California, Merced, Merced, CA, United States of America
                [10 ] Biologic Environmental Survey, East Perth, Australia
                [11 ] College of Science & Engineering, Flinders University, Adelaide, Australia
                [12 ] Institute for Applied Ecology, University of Canberra, Canberra, Australia
                [13 ] College of Science & Engineering, James Cook University, Townsville, Australia
                [14 ] School of Biological Sciences, University of Adelaide, Adelaide, Australia
                [15 ] Environmental Futures Research Institute, Griffith University, Australia
                [16 ] Museum of Zoology & Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, United States of America
                [17 ] School of Veterinary Science, University of Sydney, Sydney, Australia
                [18 ] Australian Museum Research Institute, The Australian Museum, Sydney, Australia
                [19 ] Department of Biology, California State University, Dominguez Hills, Carson, CA, United States of America
                Princeton University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-9994-6423
                https://orcid.org/0000-0002-1373-6186
                https://orcid.org/0000-0002-0498-6642
                https://orcid.org/0000-0002-6366-2875
                https://orcid.org/0000-0002-7808-3892
                https://orcid.org/0000-0002-4416-5224
                https://orcid.org/0000-0002-0439-6757
                https://orcid.org/0000-0002-1165-4427
                https://orcid.org/0000-0002-9272-8204
                https://orcid.org/0000-0002-7430-3886
                https://orcid.org/0000-0003-2910-1983
                https://orcid.org/0000-0003-0521-7383
                https://orcid.org/0000-0003-4291-257X
                https://orcid.org/0000-0001-7484-7026
                https://orcid.org/0000-0002-7499-8251
                https://orcid.org/0000-0002-4362-4054
                Article
                PBIOLOGY-D-20-03622
                10.1371/journal.pbio.3001210
                8168848
                34061821
                d4b876a9-20f0-4061-87d8-43aa0801dffc
                © 2021 Melville et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 December 2020
                : 29 March 2021
                Page count
                Figures: 4, Tables: 0, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001058, Australian-American Fulbright Commission;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000153, Division of Biological Infrastructure;
                Award ID: DBI-1519732
                Award Recipient :
                JM undertook this work supported by an Australian Fulbright Commission scholarship; S.S. received funding support to undertake research that allowed assessment in the current study from the NSF (DBI-1519732). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Meta-Research Article
                Biology and Life Sciences
                Taxonomy
                Computer and Information Sciences
                Data Management
                Taxonomy
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Ecology and Environmental Sciences
                Conservation Science
                Biology and Life Sciences
                Conservation Biology
                Endangered Species
                Ecology and Environmental Sciences
                Conservation Science
                Conservation Biology
                Endangered Species
                Biology and Life Sciences
                Conservation Biology
                Ecology and Environmental Sciences
                Conservation Science
                Conservation Biology
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Species Delimitation
                Earth Sciences
                Geography
                Cartography
                Custom metadata
                The list of recognized Australian reptile species used in this study was compiled and provided by the Australian Society of Herpetologists ( http://www.australiansocietyofherpetologists.org/). Distributional data used for mapping was collated by Tingley et al. (19) and is publically available from the IUCN website ( https://www.iucnredlist.org/). Some fine-scale mapping data are not publicly available due to conservation concerns regarding locality information for threatened species.

                Life sciences
                Life sciences

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