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      Species- and sex-specific chemical composition from an internal gland-like tissue of an African frog family

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          Abstract

          Intraspecific chemical communication in frogs is understudied and the few published cases are limited to externally visible and male-specific breeding glands. Frogs of the family Odontobatrachidae, a West African endemic complex of five morphologically cryptic species, have large, fatty gland-like strands along their lower mandible. We investigated the general anatomy of this gland-like strand and analysed its chemical composition. We found the strand to be present in males and females of all species. The strand varies in markedness, with well-developed strands usually found in reproductively active individuals. The strands are situated under particularly thin skin sections, the vocal sac in male frogs and a respective area in females. Gas-chromatography/mass spectrometry and multivariate analysis revealed that the strands contain sex- and species-specific chemical profiles, which are consistent across geographically distant populations. The profiles varied between reproductive and non-reproductive individuals. These results indicate that the mandibular strands in the Odontobatrachidae comprise a so far overlooked structure (potentially a gland) that most likely plays a role in the mating and/or breeding behaviour of the five Odontobatrachus species. Our results highlight the relevance of multimodal signalling in anurans, and indicate that chemical communication in frogs may not be restricted to sexually dimorphic, apparent skin glands.

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          Building Predictive Models inRUsing thecaretPackage

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            Insect pheromones--an overview of biosynthesis and endocrine regulation.

            This overview describes, compares, and attempts to unify major themes related to the biosynthetic pathways and endocrine regulation of insect pheromone production. Rather than developing and dedicating an entirely unique set of enzymes for pheromone biosynthesis, insects appear to have evolved to add one or a few tissue-specific auxiliary or modified enzymes that transform the products of "normal" metabolism to pheromone compounds of high stereochemical and quantitative specificity. This general understanding is derived from research on model species from one exopterygote insect order (Blattodea) and three endopterygote insect orders (Coleoptera, Diptera, and Lepidoptera). For instance, the ketone hydrocarbon contact sex pheromone of the female German cockroach, Blattella germanica, derives its origins from fatty acid biosynthesis, arising from elongation of a methyl-branched fatty acyl-CoA moiety followed by decarboxylation, hydroxylation, and oxidation. Coleopteran sex and aggregation pheromones also arise from modifications of fatty acid biosynthesis or other biosynthetic pathways, such as the isoprenoid pathway (e.g. Cucujidae, Curculionidae, and Scolytidae), or from simple transformations of amino acids or other highly elaborated host precursors (e.g. Scarabaeidae and Scolytidae). Like the sex pheromone of B. germanica, female-produced dipteran (e.g. Drosophilidae and Muscidae) sex pheromone components originate from elongation of fatty acyl-CoA moieties followed by loss of the carbonyl carbon and the formation of the corresponding hydrocarbon. Female-produced lepidopteran sex pheromones are also derived from fatty acids, but many moths utilize a species-specific combination of desaturation and chain-shortening reactions followed by reductive modification of the carbonyl carbon. Carbon skeletons derived from amino acids can also be used as chain initiating units and elongated to lepidopteran pheromones by this pathway (e.g. Arctiidae and Noctuidae). Insects utilize at least three hormonal messengers to regulate pheromone biosynthesis. Blattodean and coleopteran pheromone production is induced by juvenile hormone III (JH III). In the female common house fly, Musca domestica, and possibly other species of Diptera, it appears that during hydrocarbon sex pheromone biosynthesis, ovarian-produced ecdysteroids regulate synthesis by affecting the activities of one or more fatty acyl-CoA elongation enzyme(s) (elongases). Lepidopteran sex pheromone biosynthesis is often mediated by a 33 or 34 amino acid pheromone biosynthesis activating neuropeptide (PBAN) through alteration of enzyme activities at one or more steps prior to or during fatty acid synthesis or during modification of the carbonyl group. Although a molecular level understanding of the regulation of insect pheromone biosynthesis is in its infancy, in the male California fivespined ips, Ips paraconfusus (Coleoptera: Scolytidae), JH III acts at the transcriptional level by increasing the abundance of mRNA for 3-hydroxy-3-methylglutaryl-CoA reductase, a key enzyme in de novo isoprenoid aggregation pheromone biosynthesis.
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              Ultrasonic communication in frogs.

              Among vertebrates, only microchiropteran bats, cetaceans and some rodents are known to produce and detect ultrasounds (frequencies greater than 20 kHz) for the purpose of communication and/or echolocation, suggesting that this capacity might be restricted to mammals. Amphibians, reptiles and most birds generally have limited hearing capacity, with the ability to detect and produce sounds below approximately 12 kHz. Here we report evidence of ultrasonic communication in an amphibian, the concave-eared torrent frog (Amolops tormotus) from Huangshan Hot Springs, China. Males of A. tormotus produce diverse bird-like melodic calls with pronounced frequency modulations that often contain spectral energy in the ultrasonic range. To determine whether A. tormotus communicates using ultrasound to avoid masking by the wideband background noise of local fast-flowing streams, or whether the ultrasound is simply a by-product of the sound-production mechanism, we conducted acoustic playback experiments in the frogs' natural habitat. We found that the audible as well as the ultrasonic components of an A. tormotus call can evoke male vocal responses. Electrophysiological recordings from the auditory midbrain confirmed the ultrasonic hearing capacity of these frogs and that of a sympatric species facing similar environmental constraints. This extraordinary upward extension into the ultrasonic range of both the harmonic content of the advertisement calls and the frog's hearing sensitivity is likely to have co-evolved in response to the intense, predominantly low-frequency ambient noise from local streams. Because amphibians are a distinct evolutionary lineage from microchiropterans and cetaceans (which have evolved ultrasonic hearing to minimize congestion in the frequency bands used for sound communication and to increase hunting efficacy in darkness), ultrasonic perception in these animals represents a new example of independent evolution.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Investigation
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: Formal analysisRole: Investigation
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Journal
                Proc Biol Sci
                Proc Biol Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                January 10, 2024
                January 2024
                January 10, 2024
                : 291
                : 2014
                : 20231693
                Affiliations
                [ 1 ] Museum für Naturkunde – Leibniz Institute for Evolution and Biodiversity Science, , Invalidenstraße 43, 10115 Berlin, Germany
                [ 2 ] Zoology III Department of Animal Ecology and Tropical Biology, University of Würzburg, , Am Hubland, 97074 Würzburg, Germany
                [ 3 ] ONG EnviSud Guinée, Quartier Kipé T2 commune de Ratoma, , 530 BP 558 Conakry, Guinea
                Author notes

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.6978835.

                Author information
                http://orcid.org/0000-0001-7141-9544
                http://orcid.org/0000-0002-6719-8635
                http://orcid.org/0000-0002-1666-195X
                Article
                rspb20231693
                10.1098/rspb.2023.1693
                10777154
                38196358
                24cbf68e-36b6-4de8-85bb-52fa835835de
                © 2024 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : August 4, 2023
                : November 27, 2023
                Funding
                Funded by: SMFG;
                Award ID: logistic support and staging during fieldwork at M
                Funded by: PROMOS;
                Award ID: Travel grant to D. Sydow
                Funded by: Evangelisches Studienwerk Villigst, http://dx.doi.org/10.13039/501100003088;
                Award ID: Doctoral stipend to M. Schäfer
                Categories
                1001
                60
                Ecology
                Research Articles

                Life sciences
                anuran,breeding gland,chemical communication,fat tissue,multimodal communication,odontobatrachidae

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