Herpetology Notes, volume 12: 537-542 (2019) (published online on 27 May 2019)

Oral cavity of the tadpoles of Boana bandeirantes (Caramaschi and Cruz, 2013) and B. polytaenia (Cope, 1870), with a new state record for B. bandeirantes (Amphibia, Anura, )

Cyro de Luna-Dias1,*, Joice Ruggeri2, and Sergio P. de Carvalho-e-Silva1

Abstract. The clade of Boana polytaenia is composed of 12 , including B. bandeirantes, and B. polytaenia, two morphologically similar species. We describe the oral cavity morphology of the tadpoles of B. bandeirantes and B. polytaenia. Their morphologies are very similar to the oral cavity morphology of B. leptolineata, the only species of the B. polytaenia clade to have had this feature described to date. The two species can be distinguished based on two combined characters: (1) number of papillae forming the ridge in the prenarial arena and (2) number of lateral papillae at each side of the median ridge. The geographic distribution of B. bandeirantes is extended to southern state of Minas Gerais, Brazil, representing the first record of the species in this state.

Keywords. Boana pulchella group, buccopharyngeal morphology, Cophomantini, larvae, mouthparts,

Introduction (Caramaschi and Cruz, 2000); B. polytaenia (Cope, 1870); and B. stenocephala (Caramaschi and Cruz, The clade of Boana polytaenia belongs to the Boana 1999). Of these, the tadpoles of B. bandeirantes, B. pulchella species group, and its geographical distribution cipoensis, B. goiana, B. leptolineata, and B. polytaenia encompasses the central-western, south-eastern and have been described (Heyer et al., 1990; Eterovick et al., southern regions of Brazil. The clade of B. polytaenia 2002; Both et al., 2007; Orrico et al., 2007; Pinheiro et is comprised of 12 species of tree recognized by al., 2012), but only the oral cavity morphology for the a striped dorsal pattern (Caramaschi and Cruz, 2013): tadpole of B. leptolineata has been described (Both et Boana bandeirantes (Caramaschi and Cruz, 2013); B. al., 2007). beckeri (Caramaschi and Cruz, 2004); B. botumirim Boana bandeirantes is a small tree described (Caramaschi et al., 2009); B. buriti (Caramaschi and from Itapecerica da Serra, São Paulo State, and is Cruz, 1999); B. cipoensis (Lutz, 1968); B. goiana (Lutz, known to occur from north-eastern São Paulo through 1968); B. jaguariaivensis (Caramaschi, Cruz and Segalla, to southern Rio de Janeiro State (Caramaschi and Cruz, 2010); B. latistriata (Caramaschi and Cruz, 2004); B. 2013; Silva et al., 2017; Lourenço-de-Moraes et al., leptolineata (Braun and Braun, 1977); B. phaeopleura 2018; Polettini Neto and Bertoluci, 2018). Heyer et al. (1990) described the advertisement call and the tadpole of the population from Estação Ecológica da Boracéia, São Paulo (identified at the time as “ polytaenia”), but only presented measurements for the total length 1 Laboratório de Anfíbios e Répteis, Departamento de Zoologia, and a few proportions of the illustrated specimen. Instituto de Biologia, Universidade Federal do Rio de Later, Pinheiro et al. (2012) provided more information Janeiro, Av. Brigadeiro Trompowski s/nº, CCS, Cidade on the advertisement call of the same population (as Universitária, Caixa Postal 68044, Rio de Janeiro, Rio de “Hypsiboas aff. polytaenius”). Boana polytaenia is Janeiro 21944-970, Brazil. known to occur in the states of Rio de Janeiro, Minas 2 Laboratório de História Natural de Anfíbios Brasileiros, Gerais and Espírito Santo (Cruz and Caramaschi, 1998; Departamento de Biologia , Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, Ferreira and Vrcibradic, 2005), but the exact type locality Campinas, São Paulo 13083-863, Brazil. for this species is unknown (see Cruz and Caramaschi, * Corresponding author. E-mail: [email protected] 1998). Pinheiro et al. (2012) described the tadpoles 538 Cyro de Luna-Dias et al. and the advertisement calls from populations of B. Results polytaenia from the Quadrilátero Ferrífero highlands, in Boana bandeirantes.—Dorsal aspects: buccal Minas Gerais. roof (Fig. 1A) triangular shaped, longer than wide. Larval morphology can be useful for taxonomic and Three pustulations in the prenarial arena, connected evolutionary studies in (Larson and de Sá, forming a ridge (Fig. 1C). Choanae large, oriented 45° 1998; Faivovich, 2002; Provete et al., 2013; Dias, 2018), from transverse plane, with rounded vacuities in the especially under total evidence, an important approach anteromedial margins. Posterior margins of the choanae in the study of amphibians (e.g., Grant et al., 2006; forming the narial valves. Postnarial arena with about ten Castroviejo-Fisher et al., 2015). However, information small papillae arranged in a row, parallel to the median about the buccopharyngeal morphology of tadpoles is ridge (Fig. 1D). Median ridge with many irregularities scarce (Larson et al., 2003; Provete et al., 2017). Herein, along its anterior margin. One pair of large, hand-like we describe the oral cavity morphology of the tadpoles lateral ridge papilla, and another two small, finger-like of Boana bandeirantes and B. polytaenia to provide papillae under the lateral ridge papilla on each side (Fig. important traits that might help elucidate taxonomic 1E). Buccal roof arena (BRA) with about 30 pustulations problems in the clade. Additionally, a brief discussion and about eight papillae on each side, varying in size and on the taxonomy of the clade is presented, and the shape. Glandular zone distinguished. Dorsal velum with geographic distribution of B. bandeirantes is extended. a few short projections in its posterior margin. Ventral aspects: buccal floor (Fig. 1B) triangular, as long as Material and Methods wide. Very short papillae anteriorly to the infralabial Tadpoles of Boana bandeirantes were collected at papillae. Two pairs of infralabial papillae; one large pair Estação Lambedor (22.2086º S, 45.4769º W, 1,200 m and one thin and tapered pair, located ventrally to the of altitude), a small dam surrounded by forest, which first pair. Tongue anlage, with two thin lingual papillae. provides water for part of the city of Pedralva, Minas Buccal floor arena (BFA) with less than 10 pustulations Gerais. The dam is located in Serra da Pedra Branca, and 12 small, thin papillae on each side; most papillae 220 km away from the type locality of B. bandeirantes. are finger-like; medial ones are bifid. Buccal pocket Other species of Boana found at the site are B. faber horizontally oriented. About five small finger-like (Wied-Neuwied, 1821) and B. albopunctata (Spix, lateral floor papillae. Distinguished glandular zone. 1824). Tadpoles of B. polytaenia were collected at Lago Ventral velum round shaped, with few projections along Jaci (22.4483º S, 42.9911º W, 1,020 m of altitude) a its margin. small artificial pond in the urban area of Teresópolis, Boana polytaenia.—Dorsal aspects: buccal roof (Fig. on the vicinity of the Serra dos Órgãos National Park. 2A) triangular shaped, longer than wide. Five pustulations Other species of the genus found at the site are B. faber in the prenarial arena, connected forming a ridge (Fig. and B. pardalis (Spix, 1824). 2C). Choanae large, oriented 45º from transverse plane, Tadpoles were collected between 2007 and 2010 with rounded vacuities in the anteromedial margins. with a dip net or a funnel trap made from plastic Posterior margins forming the narial valves. Postnarial bottles. Tadpoles were fixed in 5% formalin and arena with eight to ten small and papillae arranged in subsequently staged following Gosner´s table (1960). a row, parallel to the median ridge (Fig. 2D). Median One tadpole of each species was reared in captivity ridge with many irregularities along its anterior margin. until metamorphosis for species confirmation. All One pair of large, hand-like lateral ridge papilla, and specimens are deposited in the Collection of two small, finger-like papillae under the lateral ridge the Departamento de Zoologia of Universidade Federal papilla on each side (Fig. 2E). Buccal roof arena (BRA) do Rio de Janeiro (ZUFRJ). Descriptions of oral cavities with about 30 pustulations and about nine papillae on are based on five specimens of Boana bandeirantes each side, varying in size and shape. Distinguished and three of B. polytaenia (Appendix 1)� �������������� glandular zone. Dorsal velum with short projections in tadpoles were dissected under a stereomicroscope its posterior margin. Ventral aspects: buccal floor (Fig. and the oral morphological features were stained with 2B) triangular, as long as wide. Short papillae, which 3% Methylene Blue solution. Dissections followed may be single, bifid or trifid, anteriorly to the infralabial the procedure described by Wassersug (1976) and papillae. Two pairs of infralabial papillae; one large pair Spirandeli-Cruz (1991), and terminology follows and one thin and tapered pair, located ventrally to the Wassersug (1976). first pair; this second pair was absent in one individual. Oral cavity of the tadpoles of Boana bandeirantes and B. polytaenia 539

Figure 1. Oral cavity of the tadpole of Boana bandeirantes at stage 35. (A) Buccal roof (ZUFRJ 12285 35-2). (B) Buccal floor (ZUFRJ 12285 35-2). (C) Structures detailed in the red circles are ridge in the prenarial arena. (D) Papillae in the postnarial arena (ZUFRJ 12285 35-1). (E) Papillae under the lateral ridge papilla (laterally inclined view) (ZUFRJ 12285 35-1). Individuals on C–E were stained with 3% Methylene Blue solution. Drawings by Rebeca Khouri.

Tongue anlage with two lingual papillae varying in size. also for the B. pulchella group. Kolenc et al. (2008) Buccal floor arena (BFA) with more than 20 pustulations reported the species in the B. pulchella group as and a variable number (11–30) of papillae on each side, having 8–40 long papillae in the BRA, distributed in finger-like and long in its majority (some bifid). Buccal a V, except for three species in which BRA papillae pocket horizontally oriented. Presence of two to five are absent – B. caingua, B. cordobae and B. joaquini. small finger-like lateral floor papillae. Glandular zone This feature is seen in the B. polytaenia clade, with very distinguished. Ventral velum with projections eight papillae on either side in B. bandeirantes, about along its margin. nine papillae on each side in B. polytaenia and about We detected a variation on LTRF of Boana six papillae on each side for B. leptolineata (Both et bandeirantes when comparing to the description al., 2007; present study). These long papillae, despite presented by Heyer et al. (1990): 2(2)/3(1) on the present being present in some species of Aplastodiscus Lutz, study and 2(2)/3(1,2) in Heyer et al. (1990). 1950 and Bokermannohyla Faivovich, Haddad, Garcia, Frost, Campbell and Wheeler, 2005 (all members of Discussion Cophomantini), are absent in other groups of Boana, The oral cavity morphology seems to be taxonomically being a putative synapomorphy for the B. pulchella valuable not only for the Boana polytaenia clade, but group, with homoplasies in those two genera �������� 540 Cyro de Luna-Dias et al.

Figure 2. Oral cavity of the tadpole of Boana polytaenia. (A) Buccal roof of tadpole at stage 35 (ZUFRJ 13406 35-1). (B) Buccal floor of tadpole at stage 33 (ZUFRJ 13406 33-3). (C) Structures detailed in the red circles are ridge in the prenarial arena of tadpole at stage 35 (ZUFRJ 13406 35-1). (D) Papillae in the postnarial arena of tadpole at stage 35 (ZUFRJ 13406 35-1). (E) Papillae under the lateral ridge papilla (laterally inclined view) of tadpole at stage 33 (ZUFRJ 13406 33-3). Individuals on C–E were stained with 3% Methylene Blue solution. Drawings by Rebeca Khouri.

et al., 2008). Boana polytaenia clade is the presence of pustulations Kolenc et al. (2008) also cite the absence of papillae on forming a flat ridge in the prenarial arena. In B. the region anteriorly to the infralabial papillae (referred bandeirantes, there are three connected pustulations. In as “infralabial papillae laying on the infrarostral B. polytaenia there are five, but these are not always cartilages within the orobranchial chamber”) as being connected. Both et al. (2007) noted the presence of characteristic of all species in the Boana pulchella the ridge in B. leptolineata, but did not describe its clade, except B. leptolineata. These infralabial papillae formation. However, in the figure presented by them, are also present in the species within the B. faber (Wied- it is possible to see irregularities along the margin of Neuwied, 1821) and B. pellucens (Werner, 1901) groups, the ridge, suggesting its formation is through connected and in other related genera, such as Aplastodiscus and pustulations as with the other two species. Kolenc et al. Bokermannohyla (D’Heursel and Haddad, 2007). In (2008) also reported the presence of pustulations for the Boana polytaenia clade, although B. leptolineata, other species of Boana (e.g., B. andina, B. cordobae, B. B. bandeirantes and B. polytaenia also present this faber, B. geographica, B. lundii, B. prasina, B. punctata feature (Both et al., 2007; present study), the papillae and B. semilineata). are apparently reduced in comparison to those found The taxonomy of the Boana polytaenia clade is in other species. This feature, as well as its taxonomic complex (Cruz and Caramaschi, 1998; Martins et distribution, deserves additional studies to clarify its al., 2016). However, descriptions of the oral cavity significance. morphology facilitate the comparison and identification Another shared characteristic of the species of the of tadpoles (Provete et al., 2012). Therefore, the tadpoles Oral cavity of the tadpoles of Boana bandeirantes and B. polytaenia 541

Figure 3. Geographic distribution of Boana bandeirantes. Red circle: new record in Serra da Pedra Branca. Black circle: type locality in Itapecerica da Serra. White circles: other records by Caramaschi and Cruz (2013), Silva et al. (2017), Lourenço-de- Moraes et al. (2018), and Polettini Neto and Bertoluci (2018).

of Boana bandeirantes, B. polytaenia and B. leptolineata (Grant n. 312606/2017-6 and Grant n. 311156/2013-4), Fundação can be easily distinguished based on the combination of de Amparo à Pesquisa do Estado de São Paulo (Grant n. two characters: the number of pustulations forming the 2017/01917-6), and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (Grant n. E-26/112.137/2008). CLD received ridge in the prenarial arena (three in B. bandeirantes, a fellowship from Coordenação de Aperfeiçoamento de Pessoal five in B. polytaenia, not reported in B. leptolineata) de Nível Superior. ����� ���������������������������������� and number of lateral ridge papillae (one large pair and funded by FAPERJ (Grant n. E-26/111.638/2012). The Instituto one small pair in B. leptolineata and one large pair and Chico Mendes de Conservação da Biodiversidade/Sistema de two small pairs in the other two species). Information Autorização e Informação em Biodiversidade (Process n. 12164) about the oral cavity morphology of other species of the kindly provided a collecting permit. Boana polytaenia clade will be helpful when comparing and identifying its tadpoles, elucidating taxonomic References problems and clarifying its phylogenetic relationships. Both, C., Kwet, A., Solé, M. (2007): The tadpole of Hypsiboas With the present work, the geographical distribution leptolineatus (Braun and Braun, 1977), a species in the of Boana bandeirantes is extended to Serra da Pedra Hypsiboas polytaenius clade (Anura; Hylidae). Brazilian Journal Branca, with this being the first record of the species in of Biology 67: 309–312. Minas Gerais. This locality is approximately 100 km NW Caramaschi, U., Cruz, C.A.G. (2013): A new species of the Hypsiboas polytaenius clade from southeastern Brazil (Anura: from the nearest record locality in São José do Barreiro Hylidae). South American Journal of Herpetology 8: 121–126. Municipality, and approximately 225 km NE from the Castroviejo-Fisher, S., Padial Jr, J.M., De la Riva, I., Pombal Jr, type locality on Itapecerica da Serra Municipality, both J.P., Da Silva, H.R., Rojas-Runjaic, F.J., Medina-Méndez, E., in São Paulo (Fig. 3). Frost, D.R. (2015): Phylogenetic systematics of egg-brooding frogs (Anura: Hemiphractidae) and the evolution of direct Acknowledgments. We thank Pedro H. S. Dias for carefully development. ������� 4004: 1–75. reviewing this manuscript, and Chris Sergeant for reviewing the Cruz, C.A.G., Caramaschi, U. (1998): Definição, composição e English. We would also like to thank the two reviewers and editor distribuição geográfica do grupo de Hyla polytaenia Cope, 1870 for their comments and improvements. ���� ������������������� (Amphibia, Anura, Hylidae). �������������������������������� Conselho Nacional de Desenvolvimento Científico e Tecnológico Série, Zoologia 392: 1–19. 542 Cyro de Luna-Dias et al.

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(2007): 42.9911ºW, 1,020 m a.s.l). ������������������������ The tadpole of Hypsiboas latistriatus (Caramashi & Cruz, 2004) and 35-1). a species of the Hypsiboas polytaenius (Cope, 1870) clade (Amphibia, Anura, Hylidae). Zootaxa 1531: 25–37. Accepted by Fabrício Oda Pinheiro, P.D.P., Pezzuti, T.L, Garcia, P.C.A. (2012): The tadpole and vocalizations of Hypsiboas polytaenius (Cope, 1870)(Anura,