Comparative histology of the vocal sac in three species of hylid frogs with comments on its functional correlates

Authors

  • Natalia Ferreira Bueno Universidade Federal de São Carlos. Departamento de Hidrobiologia
  • Agustín J. Elias-Costa Museum für Naturkunde Berlin. Leibnitz Institute for Evolution and Biodiversity Science
  • Délio Baêta Universidade Estadual Paulista. Departamento de Biodiversidade e Centro de Aquicultura
  • Evelise N. Fragoso-Moura Universidade Federal de São Carlos. Departamento de Hidrobiologia

DOI:

https://doi.org/10.11606/issn.2316-9079.v22i2p147-158

Keywords:

Animal histology, Anura, Elastic fibers, Morphology, Vocal slits, Vocalization

Abstract

The vocal sacs of frogs are elastic structures responsible for the circulation of air during vocalization, amplifying the sounds produced by these animals during multimodal communication. Vocal sacs present a wide array of morphologies among species and may be single, paired, or absent in adult males. Most studies on vocal sacs in Anura deal with their external morphology, and not with their internal structure, which has been explored in only a handful of species. The aim of this study was to assess vocal sac structure in three hylid species, Dendropsophus haddadi, D. elegans, and Scinax fuscovarius, using histological techniques. These species differ greatly in the degree of development and histological properties of the gular skin and submandibular musculature. In particular, elastic fibers are abundant in the thick m. interhyoideus and the relatively tight gular skin of S. fuscovarius. In contrast, in both species of Dendropsophus (although more evident in D. elegans), the m. interhyoideus is extremely thin and expanded, with a negligible number of elastic fibers that appear as a loose, pleated sheet when deflated. We analyzed videos of calling males of the three species and their close relatives, which show two different patterns of inflation/deflation. These patterns are strongly correlated with the histological properties of the vocal sac wall. The three species have different vocal sac shapes and rely differently on elasticity for vocal sac function.

Downloads

Download data is not yet available.

References

Araujo-Vieira, K., A. C. C. Lourenço, J. V. A. Lacerda, M. L. Lyra, B. L. Blotto, S. R. Ron, D. Baldo, M. O. Pereyra, Á. M. Suárez Mayorga, D. Baêta, R. B. Ferreira, C. L. Barrio-Amorós, C. Borteiro, R. A. Brandão, C. A. Brasileiro, M. A. Donnelly, M. J. M. Dubeux, J. Köhler, F. Kolenc, F. S. F. Leite, N. M. Maciel, I. Nunes, V. G. D. Orrico, P. L. V. Peloso, T. L. Pezzuti, S. Reichle, F. J. M. Rojas-Runjaic, H. R. Silva, M. J. Sturaro, J. A. Langone, P. C. A. Garcia, M. T. Rodrigues, D. R. Frost, W. C. Wheeler, T. Grant, J. P. Pombal Jr., C. F. B. Haddad, and J. Faivovich. 2023. Treefrog diversity in the Neotropics: phylogenetic relationships of Scinaxini (Anura: Hylidae: Hylinae). South American Journal of Herpetology 27 (Special Issue): 1–143.

Bancroft, J. D. and M. Gamble (eds.). 2008. Theory and Practice of Histological Techniques. 5th Edition. Philadelphia. Churchill Livingstone, Elsevier Ltd. 725 pp.

Boulenger, G. A. 1882. Catalogue of the Batrachia Salientia s. Ecaudata in the Collection of the British Museum. 2nd Edition. London. Taylor and Francis. 528 pp.

Burton, T. C. 1998. Variation in the hand and superfcial throat musculature of neotropical leptodactylid frogs. Herpetologica 54: 53–72.

Butcher, T. L., M. J. Ryan, and G. A. Bartholomew. 1982.

Oxygen consumption during resting, calling, and nest building in the frog Physalaemus pustulosus. Physiological Zoology 55: 10–22.

Drewes, R. C. 1984. A phylogenetic analysis of the Hyperoliidae (Anura): Treefrogs of Africa, Madagascar and the Seychelles Islands. Occasional Papers of the California Academy of Sciences 139: 1–70.

Dudley, R. and A. S. Rand. 1991. Sound production and vocal sac infation in the túngara frog, Physalaemus pustulosus (Leptodactylidae). Copeia 1991: 460–470.

Duellman, W. E. 1956. The frogs of the hylid genus Phrynohyas Fitzinger, 1843. Miscellaneous Publications of the Museum of Zoology, University of Michigan 96: 1–60.

Duellman, W. E. 2001. Hylid Frogs of Middle America. 2nd Edition. Ithaca. Society for the Study of Amphibians and Reptiles, Natural History Museum of the University of Kansas. 1158 pp.

Elias-Costa, A. J. and J. Faivovich. 2019. Convergence to the tiniest detail: vocal sac structure in torrent-dwelling frogs. Biological Journal of the Linnean Society 128: 390–402.

Elias-Costa, A. J., K. Araujo-Vieira, and J. Faivovich. 2021.

Evolution of the strikingly diverse submandibular muscles in Anura. Cladistics 37: 489–517.

Elias-Costa, A. J., R. Montesinos, T. Grant, and J. Faivovich. 2017. The vocal sac of Hylodidae (Amphibia, Anura): Phylogenetic and functional implications of a unique morphology. Journal of Morphology 278: 1506–1516.

Faivovich, J. 2002. A cladistic analysis of Scinax (Anura: Hylidae). Cladistics 18: 367–393.

Faivovich, J., D. Baêta, F. Vera Candioti, C. F. B. Haddad, and M. J. Tyler. 2011. The submandibular musculature of Phyllomedusinae (Anura: Hylidae): a reappraisal. Journal of Morphology 272: 354–62.

Frost, D. R. 2023. Amphibian Species of the World: an Online Reference. Version 6.2. Electronic Database accessible at https://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA. Captured on 01 November 2023.

Gans, C. 1973. Sound production in the Salientia: mechanism and evolution of the emitter. American Zoologist 13: 1179–1194.

Humason, G. L. 1972. Animal Tissue Techniques. 3rd Edition. New York. W. H. Freeman and Company. 641 pp.

Inger, R. F. 1956. Morphology and development of the vocal sac apparatus in the African frog Rana (Ptychadena) porosissima Steindachner. Journal of Morphology 99: 57–72.

Inger, R. F. and B. Greenberg. 1956. Morphology and seasonal development of sex characters in two sympatric African toads. Journal of Morphology 99: 549–574.

Jaramillo, C., A. S. Rand, R. Ibañezz, and R. Dudley. 1997. Elastic structuresin the vocalization apparatus of the tungara frog Physalaemus pustulosus (Leptodactylidae). Journal of Morphology 233: 287–295.

Liem, S. S. 1970. The morphology, systematics, and evolution of the Old World treefrogs (Rhacophoridae and Hyperoliidae). Fieldiana, Zoology 57: 1–145.

Liu, C. 1935. Types of vocal sac in the Salientia. Proceedings of the Boston Society of Natural History 41: 19–40.

Köhler, J., M. Jansen, A. Rodriguez, P. J. R. Kok, L. F. Toledo, M. Emmrich, F. Glaw, C. F. B. Haddad, M.-O.

Rödel, and M. Vences. 2017. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251: 1–124.

Moura, M. R. and W. Jetz. 2021. Shortfalls and opportunities in terrestrial vertebrate species discovery. Nature Ecology and Evolution 5: 631–639.

Noble, G. K. 1931. The Biology of the Amphibia. New York and London. McGraw-Hill. 577 pp.

Prestwich, K. 1994. The energetics of acoustic signaling in anurans and insects. American Zoologist 34: 625–643.

Ryan, M. J. 1985. The Túngara Frog. A Study in Sexual Selection and Communication. Chicago. University of Chicago Press. 230 pp.

Sabaj, M. H. 2022. Codes for Natural History collections in Ichthyology and Herpetology (online supplement). Version 9.0 (2022). Electronical Database accessible at https://asih.org, American Society of Ichthyologists and Herpetologists, Washington, DC.

Savitzky, A. H., A. S. Rand, and B. A. Savitzky. 2002. Organization of the elastic fbers in the vocal sac musculature of neotropical frogs. Abstracts of Papers Presented at the Joint 18th Annual Meeting of the American Elasmobranch Society, 80th Annual Meeting of the American Society of Ichthyologists and Herpetologists, 50th Annual Meeting of the Herpetologists’ League, and 45th Annual Meeting of the Society for the Study of Amphibians and Reptiles: 266.

Savitzky, A. H., K. A. Roberts, and A. S. Rand. 2000. Organization of elastic fbers in the vocal sac of frogs. Abstracts of Papers Presented at the Society for Integrative and Comparative Biology.

Starnberger, I., D. Preininger, and W. Hödl. 2014. The anuran vocal sac: a tool for multimodal signalling. Animal Behaviour 97: 281–288.

Taigen, T. L. and K. D. Wells. 1985. Energetics of vocalization by an anuran amphibian (Hyla versicolor). Journal of Comparative Physiology B 155: 163–170.

Targino, M., A. J. Elias-Costa, C. Taboada, and J. Faivovich. 2019. Novel morphological structures in frogs: vocal sac diversity and evolution in Microhylidae (Amphibia: Anura). Zoological Journal of the Linnean Society 187: 479–493.

Trueb, L. 1971. Phylogenetic relationships of certain neotropical toads with the description of a new genus (Anura:Bufonidae). Contributions in Science, Los Angeles County Museum 216: 1–40.

Trueb, L. and H. J. Tyler. 1974. Systematics and evolution of the Greater Antillean hylid frogs. Occasional Papers, Museum of Natural History, University of Kansas 24:1–60.

Tyler, M. J. 1971. Observations on anuran myo-integumental attachments associated with the vocal sac apparatus. Journal of Natural History 5: 225–231.

Tyler, M. J. 1972. Superfcial mandibular musculature, vocal sacs and the phylogeny of Australo-Papuan leptodactylid frogs. Records of South Australian Museum 16: 1–20.

Tyler, M. J. 1974. Superfcial mandibular musculature and vocal sac structure in the Anura. Ms. Thesis. Department of Anatomy and Histology, University of Adelaide.

Tyler, M. J. and W. E. Duellman. 1995. Superfcial mandibular musculature and vocal sac structure in hemiphractine hylid frogs. Journal of Morphology 224: 65–71.

Wells, K. D. 2007. The Ecology and Behavior of Amphibians. Chicago and London. University of Chicago Press. 1400 pp.

Downloads

Published

2023-12-15

Issue

Section

Articles

How to Cite

Bueno, N. F., Elias-Costa, A. J., Baêta, D., & Fragoso-Moura, E. N. (2023). Comparative histology of the vocal sac in three species of hylid frogs with comments on its functional correlates. Phyllomedusa: Journal of Herpetology, 22(2), 147-158. https://doi.org/10.11606/issn.2316-9079.v22i2p147-158