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      Comparative and functional analysis of the digital mucus glands and secretions of tree frogs

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          Abstract

          Background

          Mucus and mucus glands are important features of the amphibian cutis. In tree frogs, the mucus glands and their secretions are crucial components of the adhesive digital pads of these animals. Despite a variety of hypothesised functions of these components in tree frog attachment, the functional morphology of the digital mucus glands and the chemistry of the digital mucus are barely known. Here, we use an interdisciplinary comparative approach to analyse these components, and discuss their roles in tree frog attachment.

          Results

          Using synchrotron micro-computer-tomography, we discovered in the arboreal frog Hyla cinerea that the ventral digital mucus glands differ in their morphology from regular anuran mucus glands and form a subdermal gland cluster. We show the presence of this gland cluster also in several other—not exclusively arboreal—anuran families. Using cryo-histochemistry as well as infrared and sum frequency generation spectroscopy on the mucus of two arboreal ( H. cinerea and Osteopilus septentrionalis) and of two terrestrial, non-climbing frog species ( Pyxicephalus adspersus and Ceratophrys cranwelli), we find neutral and acidic polysaccharides, and indications for proteinaceous and lipid-like mucus components. The mucus chemistry varies only little between dorsal and ventral digital mucus in H. cinerea, ventral digital and abdominal mucus in H. cinerea and O. septentrionalis, and between the ventral abdominal mucus of all four studied species.

          Conclusions

          The presence of a digital mucus gland cluster in various anuran families, as well as the absence of differences in the mucus chemistry between arboreal and non-arboreal frog species indicate an adaptation towards generic functional requirements as well as to attachment-related requirements. Overall, this study contributes to the understanding of the role of glands and their secretions in tree frog attachment and in bioadhesion in general, as well as the evolution of anurans.

          Electronic supplementary material

          The online version of this article (10.1186/s12983-019-0315-z) contains supplementary material, which is available to authorized users.

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          Most cited references88

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          Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host.

          Batrachochytrium dendrobatidis (Bd) is a chytrid fungus that causes chytridiomycosis in amphibians. Only named in 1999, Bd is a proximate driver of declines in global amphibian biodiversity. The pathogen infects over 350 species of amphibians and is found on all continents except Antarctica. However, the processes that have led to the global distribution of Bd and the occurrence of chytridiomycosis remain unclear. This review explores the molecular, epidemiological, and ecological evidence that Bd evolved from an endemic ancestral lineage to achieve global prominence via anthropogenically mediated spread. We then consider the major host and pathogen factors that have led to the occurrence of chytridiomycosis in amphibian species, populations, and communities.
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            The natural history of amphibian skin secretions, their normal functioning and potential medical applications.

            Amphibians occupy a wide range of habitat types from arid deserts to deep freshwater lakes; they may spend most of their life underground or high in cloud forest canopy. Some are found north of the Arctic Circle and can tolerate freezing conditions, while others have evolved a range of adaptations to avoid desiccation in some of the hotter areas of the world. The skin plays key roles in the everyday survival of amphibians and their ability to exploit a wide range of habitats and ecological conditions. The normal functions of the skin are surveyed and Eisner's biorational approach to chemical prospecting--seeking clues from an animal's behaviour and its interactions with its environment to reveal the presence of chemical compounds with potential medical or veterinary applications--is applied to amphibians. The biology and natural history of amphibian skin, its glands and their secretions are briefly reviewed. Four categories of compounds are found in the granular or poison glands, these are: biogenic amines, bufodienolides (bufogenins), alkaloids and steroids, peptides and proteins. Toads, particularly members of the genus Bufo, are identified as a particularly convenient and useful source of granular gland secretions. The potential medical-pharmaceutical significance of products derived from amphibian skin secretions is discussed. The need for a humane approach to this work is noted.
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              Cutaneous granular glands and amphibian venoms

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                Author and article information

                Contributors
                julian.langowski@wur.nl
                ss321@zips.uakron.edu
                an48@zips.uakron.edu
                henk.schipper@wur.nl
                frank.vandenberg@wur.nl
                sk201@zips.uakron.edu
                hastley@uakron.edu
                sander.gussekloo@wur.nl
                ali4@uakron.edu
                johan.vanleeuwen@wur.nl
                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                13 June 2019
                13 June 2019
                2019
                : 16
                : 19
                Affiliations
                [1 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Experimental Zoology Group, Department of Animal Sciences, Wageningen University & Research, ; De Elst 1, Wageningen, 6708 WD The Netherlands
                [2 ]ISNI 0000 0001 2186 8990, GRID grid.265881.0, Department of Polymer Science, The University of Akron, ; 170 University Ave, Akron, Ohio 44325-3909 USA
                [3 ]ISNI 0000 0001 2186 8990, GRID grid.265881.0, Biomimicry Research & Innovation Center, Departments of Biology and Polymer Science, The University of Akron, ; 235 Carroll St., Akron, Ohio 44325-3908 USA
                Author information
                http://orcid.org/0000-0001-8791-3061
                Article
                315
                10.1186/s12983-019-0315-z
                6563374
                31210775
                51d490b9-2066-4838-91bc-f2ff6c578cbe
                © The Author(s) 2019

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 13 March 2019
                : 6 May 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003958, Stichting voor de Technische Wetenschappen;
                Award ID: 13353
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DMR 1610483
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IOS 1656645
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Animal science & Zoology
                hyla cinerea,macrogland,mucosubstance,lubrication,wet adhesion,cryo-histochemistry,infrared spectroscopy,sum frequency generation spectroscopy,synchrotron micro-computer-tomography

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