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The Submandibular Musculature of Phyllomedusinae (Anura: Hylidae): a Reappraisal

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The Submandibular Musculature of Phyllomedusinae (Anura: Hylidae): a Reappraisal JOURNAL OF MORPHOLOGY 272:354–362 (2011) The Submandibular Musculature of Phyllomedusinae (Anura: Hylidae): A Reappraisal J. Faivovich,1* D. Baeˆ ta,2 F. Vera Candioti,3 C.F.B. Haddad,4 and M.J. Tyler5 1Divisio´n Herpetologı´a, Museo Argentino de Ciencias Naturales-CONICET, Buenos Aires, Argentina 2Setor de Herpetologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil 3CONICET—Instituto de Herpetologı´a, Fundacio´n Miguel Lillo, Tucuma´n, Argentina 4Departamento de Zoologia, I.B., Universidade Estadual Paulista, Rio Claro, Sa˜o Paulo, Brazil 5Department of Ecology and Evolutionary Biology, School of Earth and Environmental Sciences, University of Adelaide, South Australia, Australia ABSTRACT The submandibular musculature of 37 era Hyla and Nyctimystes) have supplementary ap- species of the five currently recognized genera of the ical elements of the m. intermandibularis; these subfamily Phyllomedusinae (Anura: Hylidae) is arise from the lingual surface of the mandible on described; observations are made on the variation and each side of the m. submentalis and extend poster- ontogeny of these muscles. Supplementary apical ele- omedially to attach to the median raphe of the ments of the m. intermandibularis occur in all phyllome- dusines studied, in addition to the supplementary pos- principal element of the m. intermandibularis. Sec- terolateral elements previously reported. Our observa- ond, phyllomedusines have supplementary postero- tions are discussed in the context of 1) the proposed lateral elements of the m. intermandibularis; these homology between supplementary apical and posterolat- arise from the ventral surface of the mandible, eral elements; 2) the homology with the apical elements near the pars articularis, and extend anterome- reported for Pelodryadinae (sister taxon of Phyllomedu- dially to attach on the ventral surface of the prin- sinae); and 3) the implications for our understanding of cipal element of the m. intermandibularis. Tyler the relationships between Phyllomedusinae and Pelo- (1971) also noted that all Australopapuan hylids dryadinae. Anatomical differences between the apical possess an m. intermandibularis with a median and posterolateral elements and their co-occurrence in raphe, whereas phyllomedusines have a broad me- phyllomedusines indicate that these supplementary ele- ments are not homologous. Despite differences between dian aponeurosis. phyllomedusines and pelodryadines in the adhesion of On the basis of the presence of supplementary supplementary fibers to the principal element of the m. apical elements of the m. intermandibularis, Tyler intermandibularis and the occurrence of a broad aponeu- (1971) resurrected the genus Litoria to accommo- rosis or a medial raphe, the extensive morphological and date all Australopapuan species previously placed developmental resemblances of the apical elements indi- in Hyla. On the basis of the same evidence, Savage cate that these structures are homologous, and that the (1973) suggested that the Australopapuan hylids presence of apical elements is a synapomorphy of Phyllo- medusinae 1 Pelodryadinae. J. Morphol. 272:354–362, Additional Supporting Information may be found in the online 2011. Ó 2011 Wiley-Liss, Inc. version of this article. KEY WORDS: Phyllomedusinae; Pelodryadinae; sub- Contract grant sponsor: ANPCyT PICT; Contract grant numbers: mandibular musculature; anatomy; systematics; 2006-223, 2007-2202, 2007-01485; Contract grant sponsor: Consejo supplementary elements Nacional de Investigaciones Cientı´ficas y Te´cnicas (CONICET); Con- tract grant number: PIP 1112008010 2422; Contract grant sponsor: UNT CIUNT; Contract grant number: G430; Contract grant spon- INTRODUCTION sors: CAPES; FAPERJ; Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq).; Contract grant sponsor: FAPESP; The presence of supplementary elements of the Contract grant numbers: 05/56756-0, 06/52088-5, 01/13341-3, 08/ intermandibularis muscle in hylid frogs was first 50928-1. noted by Trewavas (1933) in two species of Aus- tralopapuan hylids. In a major review, Tyler (1971) *Correspondence to: J. Faivovich, Divisio´n Herpetologı´a, Museo Argentino de Ciencias Naturales-CONICET, A´ ngel Gallardo 470, described morphological variation of submandibu- C1405DJR, Buenos Aires, Argentina. E-mail: [email protected] lar musculature in hylid frogs and studied its taxo- nomic distribution. His observations in great part Received 4 June 2010; Revised 19 August 2010; shaped ideas on higher level relationships of hylids Accepted 2 October 2010 for the next 35 years. The two most historically Published online 18 January 2011 in important results of that article are as follows. Wiley Online Library (wileyonlinelibrary.com) First, all Australopapuan hylids (then in the gen- DOI: 10.1002/jmor.10919 Ó 2011 WILEY-LISS, INC. SUBMANDIBULAR MUSCLES OF PHYLLOMEDUSINAE 355 were unrelated to Hylidae and recognized them MATERIALS AND METHODS as Pelodryadidae, a group that Duellman (1977) We examined 95 adults representing 37 species of all five gen- considered to be a hylid subfamily. Cyclorana,a era of Phyllomedusinae. For Pelodryadinae, we relied on Tyler’s fossorial group of anurans with supplementary (1971, 1972) observations. We also studied metamorphic series apical elements (Tyler, 1971, 1972), was included of Phyllomedusa azurea and P. boliviana to understand details in Pelodryadinae by Tyler (1978). The differences of the origin of the supplementary elements of the m. interman- dibularis. We staged larvae according to Gosner’s (1960) devel- in the supplementary elements in Phyllomedusi- opmental table. We performed dissections with the use of a nae and Pelodryadinae were one of the lines of evi- stereomicroscope and visualized muscles by applying an iodum/ dence used by Tyler and Davies (1978) to justify potassium iodide solution topically (Bock and Shear, 1972). We the monophyly of Pelodryadinae with respect to follow the submandibular muscle terminology of Tyler (1971) and the mandibular muscle terminology of Haas (2001). We Phyllomedusinae. Subsequently, the presence and stained larvae following the protocol of Wassersug (1976). To nature of the supplementary elements of the visualize the musculature, we applied an iodine/potassium m. intermandibularis in these two subfamilies were iodide solution to specimens to improve the contrast between or- reported in the context of taxonomic descriptions ange muscles and blue cartilages. Institutional codes follow (Cannatella, 1980) and revisions (Cruz, 1990), Leviton et al. (1985) with the exception of CFBH: Colec¸a˜oCe´lio F. B. Haddad, Departamento de Zoologia, Universidade Estad- briefly discussed in reviews (Faivovich et al., 2005; ual Paulista, Rio Claro, Sa˜o Paulo, Brazil. All material exam- Frost et al., 2006; Burton and Tyler, 2007), and ined is listed as Supporting Information. included in phylogenetic analyses (da Silva, 1998; Mendelson et al., 2000; Duellman, 2001; Haas, 2003; Wiens et al., 2005; Frost et al., 2006). Herein, RESULTS the submandibular musculature of species included All Phyllomedusinae species examined have in the five recognized genera of Phyllomedusinae similarly organized submandibular musculature (Faivovich et al., 2010; Fig. 1) is surveyed and (Figs. 2 and 3). The m. submentalis (SM) is small our findings discussed in the context of previous and araphic and completely visible in ventral studies. aspect; it lacks any muscular attachment to the m. intermandibularis (IM). The principal element of the m. intermandibularis is a thin sheath of mus- cle with a broad, median aponeurosis (AP) through which, by transparency, the mm. geniohyoidei are visible. The m. intermandibularis is differentiated to produce two pairs of supplementary elements— one apical (AE) and one posterolateral (PLE). Each apical element arises from the lingual surface of the maxilla; the fibers are oriented posteromedially and insert widely on the fibers of the principal element and along the margin of the large aponeu- rosis. The posterolateral elements originate from ligaments that arise from fasciae at the level of the mm. levatores mandibulae (LMEP, LMES, and LML; Fig. 4). The fibers are oriented anteromedially and insert on the surface of the principal element and on the margin of the aponeurosis (described below). The vocal sac seems to lie above the posterior part of the principal element of the m. intermandibu- laris, and the m. interhyoideus, which is a thin mus- cle possessing a raphe and lacking folds. Observed Variation Contact between the m. submentalis and the apical elements of the m. intermandibularis. There is a clear gap between the apical elements and the posterior margin of the m. submentalis through which the mm. geniohioydei are visible in Agalychnis aspera, A. callidryas, A. granulosa, A. lemur (Fig. 2D), Phasmahyla cochranae, P. cruzi, P. exilis, P. guttata, P. jandaia, P. spectabilis, Fig. 1. Phylogenetic relationships among Phyllomedusinae. P. timbo (Fig. 2F), Phyllomedusa ayeaye, P. camba, Redrawn from Faivovich et al. (2010: Fig. 6). and P. vaillanti. The gap is present but is noticeably Journal of Morphology Fig. 2. Submandibular musculature in phyllomedusines. The white frames in figures on the left indicate the area detailed in the figures on the right. (A) Cruziohyla calcarifer (AMNH 107248), submandibular area, with detail (B) of the supplementary api- cal elements of the m. intermandibularis. Notice the thin gap between the m. submentalis and the
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