The vocal sac of Hylodidae (Amphibia, Anura): Phylogenetic and functional implications of a unique morphology

Abstract

Anuran vocal sacs are elastic chambers that recycle exhaled air during vocalizations and are present in males of most species of frogs. Most knowledge of the diversity of vocal sacs relates to external morphology; detailed information on internal anatomy is available for few groups of frogs. Frogs of the family Hylodidae, which is endemic to the Atlantic Forest of Brazil and adjacent Argentina and Paraguay, have three patterns of vocal sac morphology-that is, single, subgular; paired, lateral; and absent. The submandibular musculature and structure of the vocal sac mucosa (the internal wall of the vocal sac) of exemplar species of this family and relatives were studied. In contrast to previous accounts, we found that all species of Crossodactylus and Hylodes possess paired, lateral vocal sacs, with the internal mucosa of each sac being separate from the contralateral one. Unlike all other frogs for which data are available, the mucosa of the vocal sacs in these genera is not supported externally by the mm. intermandibularis and interhyoideus. Rather, the vocal sac mucosa projects through the musculature and is free in the submandibular lymphatic sac. The presence of paired, lateral vocal sacs, the internal separation of the sac mucosae, and their projection through the m. interhyoideus are synapomorphies of the family. Furthermore, the specific configuration of the m. interhyoideus allows asymmetric inflation of paired vocal sacs, a feature only reported in species of these diurnal, stream-dwelling frogs.

Multimodal signaling in Boana albopunctata (Anura: Hylidae): reading visual and acoustic cues

“…Behavioral studies of diurnal anuran species of the genera Hylodes and Micrixalus have demonstrated that individuals direct their visual signals toward their conspecific receivers (Preininger et al 2013, de Sá et al 2016. Male Hylodes japi, for example, perform visual signals by using their double vocal sacs independently, inflating either the right or left vocal sac depending on the location of the target conspecific (de Sá et al 2016, Elias-Costa et al 2017. Similarly, male Micrixalus saxicola (Jerdon, 1853) coordinate the use of their forelimbs toward the position of a conspecific (Preininger et al 2013).…”

Evolution of the strikingly diverse submandibular muscles in Anura

“…These include unique types of lateral vocal sacs in Trachycephalus (Hylidae) and Pelophylax (Ranidae), paired subgular lobes in Hylodidae, Nannophryne + Euphlyctis + Hoplophryne (Dicroglossidae), and Gephyromantis (Mantellidae), and bilobate expansions in Triprion + Smilisca (Hylidae) and Spea (Scaphiopodidae), among others (see full list of synapomorphies in Appendix S6). Nevertheless, the other two components that make up the vocal sac (the internal mucosa and the gular skin) also are highly diverse, and their variation, which was not studied here, must necessarily be evaluated to properly assess the evolution of vocal sacs (Elias-Costa et al, 2017).…”

“…They consist of a thin elastic chamber derived from the buccal mucosa, enveloped externally by the IM and the IH, and the gular skin (Tyler, 1971a). The great morphological diversity of vocal sacs among anuran species is, in part, related to the disparity of the submandibular muscles that form its ventral wall (Liu, 1935;Tyler, 1971aTyler, , 1972Elias-Costa et al, 2017;Targino et al, 2019).…”

“…Recent studies have included characters of submandibular muscles in phylogenetic analyses in diverse taxa, including Cycloramphidae (Verdade, 2005), Dendrobatoidea (Grant et al, 2006(Grant et al, , 2017, Hemiphractidae (Mendelson et al, 2000), Scinax (Hylidae, Faivovich, 2002), and Sphaenorhynchini (Hylidae, Araujo-Vieira et al, 2019), whereas others focused specifically on this character system, for instance in Ascaphidae + Leiopelmatidae (Johnston, 2011), Brachycephaloidea (Taboada et al, 2013), Ceratophryidae (Fabrezi and Lobo, 2009), Phyllomedusinae (Hylidae, Faivovich et al, 2011), a number of genera formerly included in "Leptodactylidae" (Burton, 1998), Rhinoderma (Manzano and Lavilla, 1995), and a sample of amphibian species (Kordylewski, 1977). Additionally, other authors referred to this system in the context of the study of the vocal sac structure in specific groups: Anaxyrus boreas (Bufonidae; Pauly, 2008), Dryaderces and Osteocephalus (Hylidae; Trueb and Duellman, 1971), Osteopilus (Hylidae; Trueb and Tyler, 1974), Trachycephalus typhonius (Hylidae; Duellman, 1956), Pseudis minuta (Hylidae; Goldberg et al, 2016), Hylodidae (Elias-Costa et al, 2017), part of Natatanura (Elias-Costa and Faivovich, 2019), Lithobates, (Ranidae; Hayes and Krempels, 1986), and Rhacophorus and Zhangixalus (Harvey et al, 2002). Despite the number of studies dedicated to exploring this character system in specific groups, its morphology in many species is still unknown and its diversity and evolution has not been studied in a large-scale phylogenetic context.…”

The Specific Molecular Composition and Structural Arrangement of Eleutherodactylus Coqui Gular Skin Tissue Provide Its High Mechanical Compliance

“…Most families in the order anuran have inflatable gular skin, such as Hylidae , Eleutherodactylidae , and Leptopelis; however, the size, shape, and color can vary significantly between species [ 6 , 7 , 8 ]. Commonly associated with frogs is the single inflated gular skin located under the floor of the gular; however, some species can have two external vocal sacs or no external vocal sac at all [ 5 ].…”