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      Follow-up ecological studies for cryptic species discoveries: Decrypting the leopard frogs of the eastern U.S.

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          Abstract

          Cryptic species are a challenge for systematics, but their elucidation also may leave critical information gaps about the distribution, conservation status, and behavior of affected species. We use the leopard frogs of the eastern U.S. as a case study of this issue. We refined the known range of the recently described Rana kauffeldi, the Atlantic Coast Leopard Frog, relative to the region’s two other leopard frog species, conducted assessments of conservation status, and improved methods for separating the three species using morphological field characters. We conducted over 2,000 call and visual surveys and took photographs of and tissue samples from hundreds of frogs. Genetic analysis supported a three-species taxonomy and provided determinations for 220 individual photographed frogs. Rana kauffeldi was confirmed in eight U.S. states, from North Carolina to southern Connecticut, hewing closely to the Atlantic Coastal Plain. It can be reliably differentiated in life from R. pipiens, and from R. sphenocephala 90% of the time, based on such characters as the femoral reticulum patterning, dorsal spot size and number, and presence of a snout spot. However, the only diagnostic character separating R. kauffeldi from R. sphenocephala remains the breeding call described in 2014. Based on our field study, museum specimens, and prior survey data, we suggest that R. kauffeldi has declined substantially in the northern part of its range, but is more secure in the core of its range. We also report, for the first time, apparent extirpations of R. pipiens from the southeastern portion of its range, previously overlooked because of confusion with R. kauffeldi. We conclude with a generalized ecological research agenda for cryptic species. For R. kauffeldi, needs include descriptions of earlier life stages, studies of niche partitioning with sympatric congeners and the potential for hybridization, and identification of conservation actions to prevent further declines.

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          Cryptic species as a window on diversity and conservation.

          The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
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            A synthesis of two decades of research documenting the effects of noise on wildlife

            Global increases in environmental noise levels - arising from expansion of human populations, transportation networks, and resource extraction - have catalysed a recent surge of research into the effects of noise on wildlife. Synthesising a coherent understanding of the biological consequences of noise from this literature is challenging. Taxonomic groups vary in auditory capabilities. A wide range of noise sources and exposure levels occur, and many kinds of biological responses have been observed, ranging from individual behaviours to changes in ecological communities. Also, noise is one of several environmental effects generated by human activities, so researchers must contend with potentially confounding explanations for biological responses. Nonetheless, it is clear that noise presents diverse threats to species and ecosystems and salient patterns are emerging to help inform future natural resource-management decisions. We conducted a systematic and standardised review of the scientific literature published from 1990 to 2013 on the effects of anthropogenic noise on wildlife, including both terrestrial and aquatic studies. Research to date has concentrated predominantly on European and North American species that rely on vocal communication, with approximately two-thirds of the data set focussing on songbirds and marine mammals. The majority of studies documented effects from noise, including altered vocal behaviour to mitigate masking, reduced abundance in noisy habitats, changes in vigilance and foraging behaviour, and impacts on individual fitness and the structure of ecological communities. This literature survey shows that terrestrial wildlife responses begin at noise levels of approximately 40 dBA, and 20% of papers documented impacts below 50 dBA. Our analysis highlights the utility of existing scientific information concerning the effects of anthropogenic noise on wildlife for predicting potential outcomes of noise exposure and implementing meaningful mitigation measures. Future research directions that would support more comprehensive predictions regarding the magnitude and severity of noise impacts include: broadening taxonomic and geographical scope, exploring interacting stressors, conducting larger-scale studies, testing mitigation approaches, standardising reporting of acoustic metrics, and assessing the biological response to noise-source removal or mitigation. The broad volume of existing information concerning the effects of anthropogenic noise on wildlife offers a valuable resource to assist scientists, industry, and natural-resource managers in predicting potential outcomes of noise exposure.
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              Back to the future: museum specimens in population genetics.

              Museums and other natural history collections (NHC) worldwide house millions of specimens. With the advent of molecular genetic approaches these collections have become the source of many fascinating population studies in conservation genetics that contrast historical with present-day genetic diversity. Recent developments in molecular genetics and genomics and the associated statistical tools have opened up the further possibility of studying evolutionary change directly. As we discuss here, we believe that NHC specimens provide a largely underutilized resource for such investigations. However, because DNA extracted from NHC samples is degraded, analyses of such samples are technically demanding and many potential pitfalls exist. Thus, we propose a set of guidelines that outline the steps necessary to begin genetic investigations using specimens from NHC.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Formal analysisRole: Investigation
                Role: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 November 2018
                2018
                : 13
                : 11
                : e0205805
                Affiliations
                [1 ] New York Natural Heritage Program, State University of New York College of Environmental Science and Forestry, Albany, New York, United States of America
                [2 ] Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, New Jersey, United States of America
                [3 ] Smithsonian Institution, National Museum of National History and Conservation Biology Institute, Washington, DC, United States of America
                [4 ] Department of Entomology & Wildlife Ecology, University of Delaware, Newark, Delaware, United States of America
                [5 ] Virginia Department of Game and Inland Fisheries, Charles City, Virginia, United States of America
                [6 ] North Carolina Museum of Natural Sciences, Raleigh, North Carolina, United States of America
                [7 ] New Jersey Pinelands Commission, New Lisbon, New Jersey, United States of America
                [8 ] Division of Life Sciences, Rutgers University, Piscataway, New Jersey, United States of America
                [9 ] North Carolina Division of Parks and Recreation, Raleigh, North Carolina, United States of America
                [10 ] Natural Diversity Section, Pennsylvania Fish and Boat Commission, Bellefonte, Pennsylvania, United States of America
                [11 ] New York State Office of Parks, Recreation, and Historic Preservation, Staatsburg, New York, United States of America
                [12 ] Hudsonia, Ltd., Annandale, New York, United States of America
                [13 ] Natural Heritage & Endangered Species Program, Massachusetts Division of Fisheries & Wildlife, Westborough, Massachusetts, United States of America
                [14 ] CTHerpConsultant, LLC, Southington, Connecticut, United States of America
                [15 ] Division of Fish and Wildlife, Rhode Island Department of Environmental Management, Providence, Rhode Island, United States of America
                [16 ] Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, California, United States of America
                [17 ] Endangered and Nongame Species Program, New Jersey Division of Fish and Wildlife, Clinton, New Jersey, United States of America
                [18 ] UCLA La Kretz Center for California Conservation Science, Institute of the Environment and Sustainability University of California, Los Angeles, Los Angeles, California, United States of America
                University of South Dakota, UNITED STATES
                Author notes

                Competing Interests: EK and DPQ are affiliated with Hudsonia, Ltd. and CTHerpConsultant, LLC, respectively. The commercial affiliations of these two authors did not play any role in the study. There are no patents or products in development to declare. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

                [¤a]

                Current address: Wildlife Species Conservation & Research Program, Delaware Division of Fish and Wildlife, Dover, Delaware, United States of America

                [¤b]

                Current address: Department of Biology, California State University, Northridge, Northridge, California, United States of America

                Author information
                http://orcid.org/0000-0003-1058-3572
                Article
                PONE-D-17-44420
                10.1371/journal.pone.0205805
                6226167
                30412587
                f4f77541-1b6d-4016-83af-56377eb3491d
                © 2018 Schlesinger 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
                : 20 December 2017
                : 2 October 2018
                Page count
                Figures: 7, Tables: 3, Pages: 28
                Funding
                This study was funded by the Northeast Association of Fish and Wildlife Agencies as Regional Conservation Needs grant 2013-03, administered by the Wildlife Management Institute, with matching funds and in-kind from the authors' institutions. J. Feinberg, J. Burger, and E. Kiviat were also supported by grants from the Hudson River Foundation, and B. Shaffer and S. Wenner by the NSF (DEB 1239961). The funders provided support in the form of salaries for authors [MDS, JAF, NHN, JB, EK, SMW, HBS], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. EK and DPQ are affiliated with Hudsonia, Ltd. and CTHerpConsultant, LLC, respectively. The commercial affiliations of these two authors did not play any role in the study.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amphibians
                Frogs
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Cryptic Speciation
                Ecology and Environmental Sciences
                Conservation Science
                Research and Analysis Methods
                Research Facilities
                Museum Collections
                Biology and Life Sciences
                Genetics
                Animal Genetics
                Amphibian Genetics
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Wetlands
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Wetlands
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Wetlands
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Species Delimitation
                Biology and Life Sciences
                Psychology
                Behavior
                Animal Behavior
                Social Sciences
                Psychology
                Behavior
                Animal Behavior
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Custom metadata
                Data on leopard frog calling surveys, visual surveys, and other localities, as well as characteristics derived from photographs of live frogs, are archived at Zenodo: DOI 10.5281/zenodo.1464256. Location data in decimal degrees have been rounded to the tenths place, and in some cases removed entirely, to ensure the protection of at-risk species. Sources and details of environmental layer data used to generate the distribution model, which are not owned by the authors, may be requested from Tim Howard, New York Natural Heritage Program ( tghoward@ 123456esf.edu ).

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