Zootaxa, Redescription of tadpole of the hylodid frog

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Jun 29, 2010 - Tadpoles were manually collected with a fish-net on July 2006 in a torrent stream in Reserva Rio das Pedras (ReRP;. 22°59'29”S, 44°06'01”W) ...
Zootaxa 2521: 65–68 (2010) www.mapress.com / zootaxa/

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ZOOTAXA ISSN 1175-5334 (online edition)

Redescription of tadpole of the hylodid frog Hylodes asper (Müller, 1924) PAULO NOGUEIRA COSTA1,5, THIAGO SILVA-SOARES2, LUIZ NORBERTO WEBER3, & ANA MARIA PAULINO TELLES DE CARVALHO-E-SILVA4 1

Universidade do Estado do Rio de Janeiro, Depto. Ecologia, R. São Francisco Xavier 524, 20550-013, Rio de Janeiro, RJ, Brazil Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia. Ilha do Fundão, 21944-270, Rio de Janeiro, RJ, Brazil 3 Universidade Federal da Bahia, Instituto de Ciências Ambientais e Desenvolvimento Sustentável. Rua Professor José Seabra s/n, Centro, 47805-100, Barreiras, BA, Brazil 4 Universidade Federal do Estado do Rio de Janeiro Departamento de Zoologia , Avenida Paster 458, Urca, 22290-240, Rio de Janeiro, RJ, Brazil 5 Corresponding author. E-mail: [email protected] 2

The genus Hylodes Fitzinger, 1826 currently comprises 24 species of diurnal frogs (Frost 2010), most of them restricted to mountainous rheophilic habitats of the Brazilian Atlantic Forest Biome ((Nascimento et al. 2001), with exception for Hylodes otavioi, inhabitant of the rocky fields from the riparian forests at the Serra do Cipó (Sazima & Bokermann 1982). Of the 24 species of the genus Hylodes, only 11 have their larvae described (Costa et al. 2009). Costa et al. (2009) stated the need for redescription of the tadpole of H. asper because a single tadpole of the species (WCAB 13290) was used for description without any information about its development stage (Bokermann, 1963). Larval characters have proven to be important for phylogenetic and taxonomic studies and, considering the need for characters that could serve to define morphological synapomorphies for anurans, herein we redescribe the tadpole of H. asper and its oral internal features. The species is known from the states of Rio de Janeiro, São Paulo and Paraná, in southeastern Brazil (Frost 2010). Tadpoles were manually collected with a fish-net on July 2006 in a torrent stream in Reserva Rio das Pedras (ReRP; 22°59’29”S, 44°06’01”W), municipality of Mangaratiba, Rio de Janeiro state, southeastern Brazil. Twelve tadpoles (UNIRIO 3600) were anesthetized with 0.10% cloretona and then fixed and preserved in 5% formalin. Four tadpoles were reared to froglets in order to allow specific identification. In the study area, there are two species of Hylodes: H. asper and H. phyllodes. Hylodes asper belong to the Hylodes nasus species group that is characterized by large size, robust body, distinctly granular dorsolateral surfaces, absence of light dorsolateral stripes and moderate-sized fringe on the outer margin of toe V. While Hylodes phyllodes belong to the Hylodes lateristrigatus species group that contains small to moderate-sized species with slender bodies, smooth dorsum, and light dorsolateral stripes (Heyer 1982). The differences observed between the Hylodes lateristrigatus species group and the Hylodes nasus species group can be used the differentiated H. asper of H. phyllodes. Some of these differences, like the smooth or granular dorsal surface and presence or absence of ligth dorsolateral stripes, can be observed in the juvenile. Adults of Hylodes asper can be easily observed in the same stream that the tadpoles were collected. The analyzed material is housed at the amphibian collection of the Laboratório de Biossistemática de Anfíbios in the Universidade Federal do Estado do Rio de Janeiro (UNIRIO). For the description of oral internal features, five specimens of tadpoles in the stages 27, 28, 30, 33 and 36 (MNRJ 35039) were collected in Barreiras (22°29′ S, 43°00′ W), Municipality of Guapimirim, Rio de Janeiro, Brazil. In the laboratory, the tadpoles were dissected and stained with a 1% methylene blue solution for description the oral internal features. Those tadpoles are housed at the amphibian collection of the Museu Nacional, Rio de Janeiro. The terminology for the oral internal features follows Wassersug (1976). Descriptions and measurements are based on tadpoles at stages 25–36 (Gosner 1960). Nomenclature and measurements follow Altig & McDiarmid (1999). Measurements (in millimeters) were taken using a caliper to the nearest 0.1 mm. Description of tadpole (stages 25–36). Body robust and elongated, elliptical in dorsal and lateral views (Figs. 1B, C). Body length is 33.5 % of the total length and body height is 74.5% of tail height. The snout is rounded in dorsal view and truncate in lateral view. Eyes are located dorsally and their diameter is 10% of body length; distance between the eye and nostril represents 44.4% of the distance between the eye and snout. The nostrils are rounded, closer to the eyes than the snout; internostril distance is 93.5% of interorbital distance; the distance between the nostril and snout is 17.4% of body length. The spiracle is sinistral, short, tubular-shaped, and with the inner wall free. It is posterolaterally oriented and its opening located approximately in the middle of the body. Distance between spiracle and snout is 55.4% of the Accepted by M. Vences: 22 May 2010; published: 29 Jun. 2010

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total length. The anal tube is longer than wide, dextral, and attached to the ventral fin. Tail length is 67.3% of the total length; tail is higher than the body and ends in a pointed tip. The dorsal fin originates at the same height as the caudal musculature; it is arched and slightly wider than the ventral fin, which is relatively straight. Oral disc is ventral (Fig. 1A), its width 65.8% of the body width, not emarginated, surrounded by a biseriate row of papillae except in the anterior labium. The labial tooth row formula is 2(2)/3(1). Submarginal papillae are absent. Jaw sheaths are developed and completely serrated, the upper one being V–shaped and lower one U–shaped.

FIGURE 1. Tadpoles of Hylodes asper, stage 26 of Gosner (1960), from Reserva Rio das Pedras, municipality of Mangaratiba, Rio de Janeiro, Brazil: (A) Tadpoles of Hylodes asper in life; (B) oral disc (scale 1 mm), (C) lateral and (D) dorsal views (scale 10 mm); Buccal floor (E) and roof (F). Scale = 1 mm. Measurements (in mm; ranges and standard deviation are show in parentheses). Twelve tadpoles (stages 25–36), mean values: Total length56.6 (49.3–60.6; 3.2) ; Body length19.0 (16.9–21.1; 1.3); Body width 9.8 (7.5– 10.9; 1.0); Body height 8.2 (7.5–10.2; 0.7); Tail length 38.1 (32.1– 41.3; 2.9); Tail height 11.0 (9.3M. Vences13.0; 1.0); Dorsal fin

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height 3.3 (2.5–4.1; 0.5); Ventral fin height 2.6 (1.8–3.3; 0.4); Internostril distance 4.3 (3.5–5.0; 0.4); Interorbital distance 4.6 (4.0–6.3; 0.7); Eye diameter 1.9 (1.2–2.7; 0.5); Nostril diameter 0.6 (0.4–0.8; 0.1); Eye-nostril distance 2.4 (1.8–2.8; 0.3); Nostril-snout distance 3.3 (2.5–4.2; 0.6); Eye-snout distance 5.4 (4.8–6.6; 0.6); Snout-spiracle distance 10.2 (9.0–11.3 ;0.7); Oral disc width 5.4 (4.5–6.3; 0.6). Tadpole color. In life, the tadpoles are light brown with dark brown spots on the flanks and dorsum. In lateral view, the flanks are lighter than the dorsum. Dorsally, the anterior region of tail is adorned with a conspicuous light beige stripe with a dark brown rim, which extends from the base to about the proximal one-third of the tail. Laterally, the muscles are light brown with a horizontal dark brown band extending from the origin to the middle of the tail. Dorsal and ventral tail fins are beige translucent as well as the spiracle, the oral disc and the anal tube. Iris is gold. In preservative, the color pattern is the same, but becomes slightly opaque. Internal oral features. Ventral aspect: Buccal floor triangular, wider than long; two pairs of infralabial papillae presents, apart from one another; the outer pair has a complex structure and is longer than wide, with four to six fingershaped projections of irregular margin that touch each other; long papilla base; the posterior pair approximately equivalent to half the length of the lingual papilla, and it is small, tapered and with irregular surface bearing small projections; two filiform lingual papillae present, placed side by side, tapered, with apex slightly irregular and with length equivalent to the width of the largest infralabial papilla; lingual papillae closer to the first papilla of the buccal floor arena than to the infralabial papilla; there are about 28 papillae on each side, enclosing the buccal floor arena and extending from the region near the tongue rudiments to near the ventral velum; papillae directed to the arena center, finger-shaped and curved; arena papillae arranged similar to a V or U; the bigger papilla of the floor arena is bifurcate and chela-shaped, located in the middle portion of the arena; some arena papillae show irregular margin; about four prepocket papillae, small to medium-sized, similar to those from the buccal floor arena; large number of pustules present on the arena surface, more concentrated in its medial-posterior portion; ventral velum with median notch not pronounced, with undulated margin and four to six finger-shaped projections of average size above the glottis. Dorsal aspect: Buccal roof triangular, somewhat shaped as the floor; prenarial arena with low crest and shaped as a reversed V, low distinctive in some specimens; reniform choanae separated and oriented at an angle of 45° in relation to the transverse plane; distance between choanae is equivalent to the width of the median crest; diminutive and conical prechoanal papillae, about four per choana; postnarial arena with eight to 14 papillae, arranged on each side in a separate row; papillae with varied sizes and shapes; smaller papillae located anteriorly, with no sharp apex provided with weak irregularity; largest papillae located in the most internal row and postero-located, finger-shaped, with sharp apex, irregular antero-margin and directed to the center; these resemble the projections of the lateral-ridge papillae; cluster of papillae in postnarial arena forming an inverted V; a conical and small papilla, ahead of the median-ridge; complex lateral-ridge papillae , hand-shaped with four to five ramifications of anterior margin finely serrated and directed to the center; the median ridge triangular-shaped with irregular margin; buccal roof arena bordered by 18 to 21 papillae of varied size on each side, finger-shaped, tapered and with anterior margin aliasing, directed to the arena center; papillae of similar size in antero-median portion; smaller papillae at the arena base; absence of bifurcate chela-shaped papilla in the arena; arena papillae forming an approximate V design; pustules are present and evenly distributed in the arena surface; distinct row with about nine lateral papillae on the roof arena; distinct glandular area; dorsal velum medially interrupted, having about six uniform projections of small to medium size. The tadpole of H. asper has some differences with respect to other known tadpoles of the genus. The tadpole of H. heyeri (Costa et al. 2009) has only one row of oral papillae. The eye of the H. asper tadpole is bigger than the eye of Hylodes uai (Nascimento et al. 2001), Hylodes amnicola ( Pombal et al. 2002) and H. phyllodes (Heyer et al. 1990) tadpoles. The tadpoles of H. asper can be distinguished from all species of Hylodes genus with described tadpoles for its conspicuous coloration of the tail with dorsal light beige stripes with a thin dark brown rim. Wassersug and Heyer (1988) described the internal oral anatomy of species of the family Leptodactylidae (which has since been partitioned into several families, including Hylodidae; Frost 2010). In that work, internal oral anatomy of only one species of Hylodes, identified as Hylodes cf. asperus (sic), from a stream in the Rio de Janeiro municipality. However, there is a problem of misidentification because the only species of the Hylodes genus that occurs in the region is Hylodes nasus (which belongs to the same species group as H. asper), and thus the description given should apply to that species and not to H. asper.

Acknowledgements We thank the Universidade Federal do Estado do Rio de Janeiro (UNIRIO) for logistic support and Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis (IBAMA) provided collection permits (IBAMA N° 2022.003111/9614). We are grateful to Igor Miahyraby provide photography of the tadpole.

REDESCRIPTION OF HYLODES ASPER TADPOLE

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References Altig, R. & McDiarmid, R.W. (1999) Body plan: development and morphology. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago, Illinois, USA, pp. 24−51. Bokermann, W.C.A. (1963) Girinos de anfíbios brasileiros - 2 (Amphibia, Salientia). Revista Brasileira de Biologia, 23, 349−353. Costa T.R.N, Lingnau R. & Toledo L.F. (2009) The tadpoles of the Brazilian torrent frog Hylodes heyeri (Anura, Hylodidae). Zootaxa, 2222, 66−68. Frost, D.R. (2010) Amphibian Species of the World: an Online Reference. Version 5.0. Electronic database accessible at http://research.amnh.org/herpetology/ amphibia/index.php. American Museum of Natural History, New York, USA. (accessed 11 March 2010). Gosner, K.L. (1960) A simplified table for staging anuran embryo and larvae with notes on identification. Herpetologica, 16, 183−190. Heyer, W.R. (1982) Two new species of the frog genus Hylodes from Caparaó , Minas Gerais, Brasil (Amphibia: Leptodactylidae). Proceedings of Biological Society of Washington, 95, 377–385. Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C E. (1990) Frogs of Boracéia. Arquivos de Zooogia, 31, 4, 231–410. Nascimento, L.B., Pombal Jr., J.P. & Haddad, C.F.B. (2001) A new frog of the genus Hylodes (Amphibia: Leptodactylidae) from Minas Gerais, Brazil. Journal of Zoology, London, 254, 421–428. Pombal Jr., J.P., Feio, R.N. & Haddad, C.F.B. (2002) A new species of torrent frog genus Hylodes (Anura: Leptodactylidae) from southeastern Brazil. Herpetologica, 58, 462–471. Sazima, I. & Bokermann, W.C.A. (1982) Anfíbios da Serra do Cipó, Minas Gerais, Brasil. 5: Hylodes otavioi sp. n. (Anura, Leptodactylidae). Revista Brasileira de Biologia, 42, 767–771. Wassersug, R.J. (1976) Oral morphology of anuran larvae: terminology and general description. Occasional Papers of the Museum of Natural History University of Kansas, 48, 1–23. Wassersug, R. & Heyer, W.R. (1988) A Survey of Internal Oral Features of Leptodactyloid Larvae (Amphibia: Anura). Smithsonian Contributions to Zoology, 457, 1–99.

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