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      Morphological and biochemical characterization of the cutaneous poison glands in toads ( Rhinella marina group) from different environments

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          Abstract

          Background

          Amphibian defence against predators and microorganisms is directly related to cutaneous glands that produce a huge number of different toxins. These glands are distributed throughout the body but can form accumulations in specific regions. When grouped in low numbers, poison glands form structures similar to warts, quite common in the dorsal skin of bufonids (toads). When accumulated in large numbers, the glands constitute protuberant structures known as macroglands, among which the parotoids are the most common ones. This work aimed at the morphological and biochemical characterization of the poison glands composing different glandular accumulations in four species of toads belonging to group Rhinella marina ( R. icterica, R. marina, R. schneideri and R. jimi). These species constitute a good model since they possess other glandular accumulations together with the dorsal warts and the parotoids and inhabit environments with different degrees of water availability.

          Results

          We have observed that the toads skin has three types of poison glands that can be differentiated from each other through the morphology and the chemical content of their secretion product. The distribution of these different glands throughout the body is peculiar to each toad species, except for the parotoids and the other macroglands, which are composed of an exclusive gland type that is usually different from that composing the dorsal warts. Each type of poison gland presents histochemical and biochemical peculiarities, mainly regarding protein components.

          Conclusions

          The distribution, morphology and chemical composition of the different types of poison glands, indicate that they may have different defensive functions in each toad species.

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          Most cited references42

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          Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates.

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            Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds.

            A diverse array of biologically active, lipid-soluble alkaloids have been discovered in amphibian skin. Such alkaloids include the following: the steroidal samandarines from salamanders, the batrachotoxins, histrionicotoxins, gephyrotoxins, and epibatidine from neotropical poison frogs (Dendrobatidae), the pumiliotoxins, allopumiliotoxins, homopumiliotoxins, and decahydroquinolines from certain genera of anurans from four families (Dendrobatidae, Mantellidae, Bufonidae, and Myobatrachidae), a variety of izidines (pyrrolizidines, indolizidines, quinolizidines, lehmizidines), pyrrolidines, piperidines, various tricyclics (related in structures to the coccinellines), and spiropyrrolizidines from the first three of these four families, the pseudophrynamines from one genus of Australian frogs, and a variety of unclassified alkaloids as yet of undetermined structure. With the exception of the samandarines and the pseudophrynamines, all alkaloids appear to be derived from dietary sources. Although only a few of the over 800 amphibian skin alkaloids have been detected in arthropods, putative arthropod sources for the batrachotoxins and coccinelline-like tricyclics (beetles), the pumiliotoxins (ants, mites), the decahydroquinolines, izidines, pyrrolidines, and piperidines (ants), and the spiropyrrolizidines (millipedes) have been discovered. Ants are likely sources for histrionicotoxins, lehmizidines, and tricyclic gephyrotoxins. Epibatidines represent an important alkaloid class without a putative dietary source. The structures for many of these alkaloids have been rigorously established, while the structures of others represent tentative proposals, based only on mass spectral and FTIR spectral data, along with analogies to structures of well-defined alkaloids.
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              Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads.

              Recent studies have identified range expansion as a potential driver of speciation. Yet it remains poorly understood how, under identical extrinsic settings, differential tendencies for geographic movement of taxa originate and subsequently affect diversification. We identified multiple traits that predict large distributional ranges in extant species of toads (Bufonidae) and used statistical methods to define and phylogenetically reconstruct an optimal range-expansion phenotype. Our results indicate that lineage-specific range-shifting abilities increased through an accumulation of adaptive traits that culminated in such a phenotype. This initiated the episode of global colonization and triggered the major radiation of toads. Evolution toward a range-expansion phenotype might be crucial to understanding both ancient widespread radiations and the evolutionary background of contemporary invasive species such as the cane toad.
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                Author and article information

                Contributors
                mailho.fontana@gmail.com
                marta.antoniazzi@butantan.gov.br
                juliana.sciani@usf.edu.br
                dcpimenta@butantan.gov.br
                katia.barbaro@butantan.gov.br
                carlos.jared@butantan.gov.br
                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                23 November 2018
                23 November 2018
                2018
                : 15
                : 46
                Affiliations
                [1 ]ISNI 0000 0001 1702 8585, GRID grid.418514.d, Laboratory of Cell Biology, , Instituto Butantan, ; Av. Vital Brasil 1500, São Paulo, 05503-000 Brazil
                [2 ]ISNI 0000 0001 1702 8585, GRID grid.418514.d, Laboratory of Biochemistry and Biophysics, , Instituto Butantan, ; São Paulo, Brazil
                [3 ]ISNI 0000 0001 1702 8585, GRID grid.418514.d, Laboratory of Immunopathology, , Instituto Butantan, ; São Paulo, Brazil
                Author information
                http://orcid.org/0000-0002-9117-6276
                Article
                294
                10.1186/s12983-018-0294-5
                6251109
                9430004a-3228-481c-8f4b-f5087e085115
                © The Author(s). 2018

                Open AccessThis 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
                : 2 July 2018
                : 8 November 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 308178/2014-9
                Award ID: 309589/2017-7
                Award ID: 461457/2014-8
                Award ID: 303792/2016-7
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2014/15334-4
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Animal science & Zoology
                amphibia,bufonidae,rhinella,granular glands,macroglands
                Animal science & Zoology
                amphibia, bufonidae, rhinella, granular glands, macroglands

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