south american Journal of herpetology, 5(3), 2010, 249-254 2010 Brazilian Society of herpetology

The Tadpole of Physalaemus albifrons (Spix, 1824) (anura, leiuperidae)

Marianna isabella rosa rodrigues de oliveira1,3, luiz norberto Weber1, and Joice ruggeri2
universidade federal da bahia, instituto de Cincias ambientais e Desenvolvimento sustentvel. rua Professor Jos seabra, s/n, Centro. CeP 47805100. barreiras, ba, brasil. email: oliveira.rmi@gmail.com 2 universidade federal da bahia, Departamento de Zoologia, instituto de biologia, Campus universitrio de ondina, rua baro de Jeremoabo, s/n, ondina, CeP 40170115, salvador, ba, brasil. 3 Corresponding author.
1

abstract. The tadpoles of Physalaemus albifrons used in this description were obtained from a pair collected in a permanent pond in Brotas de Macabas, state of Bahia, Brazil. The external morphological features are similar to those of other members of the P. albifrons species group, differing by the presence of interruptions in the row of the marginal papillae of the lower lip. labial tooth row formula is 2(2)/3(1, 2). The internal oral morphology of P. albifrons differed from those of P. marmoratus, P. santafecinus and P. biligonigerus by the presence of three lingual papillae. KeyWords. Taxonomy, internal oral morphology, description.

introduction The genus Physalaemus fitzinger, 1826, is currently composed of 42 species distributed form northern to central argentina, eastern Bolivia, paraguay, uruguay, Brazil, the Guianas, lowlands of southern Venezuela, southeastern Colombia, and western ecuador (frost, 2010). recently, nascimento et al. (2005) revised the genus and proposed seven species groups: Physalae mus albifrons sp. gr., P. cuvieri sp. gr., P. deimaticus sp. gr., P. gracilis sp. gr., P. henselii sp. gr., P. olfersii sp. gr. and P. signifer sp. gr. according to this taxonomic review, P. albifrons species group comprises of four species: P. albifrons Spix, 1824, P. biligonigerus Cope, 1861, P. marmoratus (reinhardt and ltken, 1862) (= P. fuscomaculatus, see nascimento et al., 2006), and P. santafecinus Bario, 1965, all occurring in South america, from argentina, uruguay, and paraguay, to central, southeastern, and northeastern Brazil, associated with open formations of the Chaco, Cerrado, and Caatinga domains (frost, 2010; iuCn, 2010). except for the Physalaemus albifrons tadpole, the larvae of all other members of the P. albiforns species group have been described, including external and internal oral morphologies (perotti and Cspedez, 1999; nomura et al., 2003). herein, we describe the external and internal oral features of the tadpole of P. albifrons and we compare them with the larval traits described for tadpoles belonging to this species group.

Materials and Methods eggs were obtained from a pair of Physalaemus al bifrons collected in January 2010, in a permanent pond (12002424.65S, 423735.72W) in the municipality of Brotas de Macabas, Chapada diamantina, Bahia state, Brazil. The Chapada diamantina is covered mainly by open formations of the Caatinga domain, with dry semi-arid to humid climate, mean temperature 20.6C and mean altitude 814 m. rainy season comprises the months from november to March (CnM, 2010). Tadpoles were fixed in 8% formalin and the stages of development were defined according to Gosner (1960). The description of the external morphology was based on twenty specimens at stages 36-39 and terminology and measurements follow altig and Mcdiarmid (1999). Teeth row formula follows altig (1970). The external and internal oral morphology was based on five specimens at stages 36-38, stained with 3% Methylene Blue solution and terminology follows Wassersug (1976). Measurements and observation of morphological features were made using an ocular micrometer under a stereoscopic microscope (olympus SZ40). drawings are based on specimens at stage 38. The tadpoles are deposited at the Museu de Zoologia da universidade federal da Bahia (MZufBa 010375). results Description of tadpole (figs. 1a, B, C): Body oval in ventral and dorsal views, and elliptic in lateral view.

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Body height is 57% of body length, and body width is 65% of body length. Snout rounded in dorsal and lateral views. nostrils large, ovoid with a small rounded fleshy projection in inernalmargin, dorsally oriented, closer to the eyes than to the tip of snout. inter-nostril distance about 15% of body width. eyes dorsolaterally positioned, and with a diameter corresponding to 14% of body length. Spiracle sinistral, narrow, short, located at the middle third of the body, directed upward, centripetal wall fused to the body wall, opening laterally directed, with opening diameter smaller than the diameter of the spiracle tube. Spiracle-snout distance about 80% of body length. Vent tube short,

large, medial, attached to ventral fin with dextral opening. Tail length is 64% of total length. origin of dorsal fin at the posterior third of the body. dorsal fin higher than ventral fin, 38% of total tail height, and ventral fin about 20% of total tail height. Tail musculature well developed with height representing 44% of body height and 45% of total tail height (Table 1). oral Disc Ventral, about 35% of body width. Tooth row formula 2(2)/3(1, 2), with p-3 about half length of p-2. Single row of marginal papillae, with an extensive gap in the median upper lip and a short gap in the median lower lip. presence of two ventrolateral

Figure 1. The tadpole of Physalaemus albifrons, stage 38 of Gosner (1960): (a) dorsal view; (B) ventral view; (C) lateral view (scale = 2 mm); (d) oral disc (scale = 1 mm).

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gaps in the lower lip. Jaw sheaths dark, finely serrated. upper jaw sheath convex, arch-shaped, and lower jaw sheath V-shaped (fig. 1d). Coloration in vivo The tadpole has a golden iris, translucid body walls with light brown coloration; in dorsal view it has dispersed dark blotches and dots, with a concentration of golden dots in the midline; two black blotches between the nostrils, the eyes, and posterior to the eyes. in lateral view it has dark and gilded spots concentrated below the eye and near to the mouth, gold spots concentrated above the eye, and black spots concentrated between the eye and mouth that extend to the ventrolateral portion; spiracle translucid, with some golden spots located near to the opening; lateroposterior region of body dark brown with dispersed golden spots. Vent transparent, golden on the intestine. There is a descending sequence of blotches over the region of the tail insertion, which extends dorsally along the tail musculature (fig. 1a). dorsal and ventral fins translucid, with dispersed black points, also present on the tail musculature. Coloration in formalin Translucid body, grey colored, with black spots along the dorsal part of the body. Two black blotches between the nostrils, the eyes, and posterior to the eyes. There is a descending sequence of blotches over the region of of the tail insertion, which extends dorsally along the tail musculature (fig. 1a). lateral region of body with many dark and brown spots, from the eyes to the laterally-posterior portion of the body. Ventral region grey translucid. Some white dots extending laterally from the ventral part of the body to the oral disc region, together with many dark dots. Tail grey with transparent dorsal and ventral fins, with few dark dots along them, also present on the tail musculature. internal oral features buccal floor (fig. 2a): Trapezoidal, as long as wide. presence of two pairs of infralabial papillae, the anterior pair much smaller than the posterior, with smooth surface and irregular apices. The posterior pair showing discrete branches, much larger than the first, with smooth surface and irregular margins and apices. The posterior pair of papillae is easily discernible from the first. presence of three lingual papillae on the same transverse plane; the median papillae is slightly larger than the lateral ones, which are tapered, have equivalent sizes, smooth surfaces and rounded

table 1. range, mean and standard deviation (Sd) of measurements (mm) of Physalaemus albifrons tadpoles (n = 20 stage 36-39), municipality of Brotas de Macabas, Bahia, Brazil. Tl = Total length; Bl = Body length; BW = Body Width; Bh = Body height; Tail l = Tail length; Th = Tail height; hTM = height of the Tail Musculature; dfh = dorsal fin height; Vfh = Ventral fin height; ind = internostril distance; iod = interorbital distance; ed = eye diameter; nd = nostril diameter; nSd = nostril-Snout distance; eSd = eye-Snout distance; SSd = Snout-Spiracle distance; odW = oral disc Width. Tl Bl BW Bh Tail l Th hTM dfh Vfh ind iod ed nd nSd eSd SSd odW range 18.2 20.5 6.5 7.1 3.9 5.3 3.4 4.3 11.8 13.3 3.7 4.5 1.4 2.0 1.2 1.7 0.6 0.9 0.6 0.9 1.1 0.7 0.7 1.2 0.3 0.6 1.2 1.6 1.9 4.5 5.9 1.5 1.9 Mean 19.4 6.9 4.5 3.9 12.5 4.0 1.7 1.5 0.8 0.7 0.9 1.0 0.3 1.0 1.6 5.5 1.6 Sd 0.6 0.2 0.3 0.2 0.6 0.3 0.2 0.1 0.1 0.1 0.1 0.1 0 0.2 0.1 0.3 0.1

apices, closer to the posterior pair of infralabial papillae than to the first arena papillae. There are four papillae on each side delimiting the arena floor, the most anterior papillae smaller than the others, roundshaped and with an irregular surface. The other arena papillae have similar sizes and shapes, tapered, with smooth surface, and a tapered apex oriented to the center of the arena. pustules distributed irregularly on the buccal floor arena (Bfa). Ventral velum with irregular margin and presence of small projections of equivalent sizes. buccal roof (fig. 2B): prenarial arena with three small papillae arranged in semicircle on the transverse plane. elliptical choanae, separated and oriented on the transverse plane, with a slight tilt to the sides and anterior margin with small irregularities. distance between the choanae about three times smaller than the width of the median ridge. postnarial arena with dispersed pustulations; presence of two pairs of postnarial papillae, one pair much larger, curved and more discernible, with minor irregularities and directed to the center of the arena, somehow touching each other. The second pair is smaller, tapered and arranged on

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the side of the major papilla of the postnarial arena. lateral ridge papillae bifid, with tapered apex, smooth, anterior margin with slight irregularities and directed upwards. Median ridge slightly wider than long, forming a semicircle in most specimens. presence of small irregularities in the margin of the median ridge and four pustulations on the surface. Buccal roof arena (Bra) with three or four finger-like papillae on each side, curved to the center, with similar sizes, tapered apices and smooth surfaces. presence of pustules dispersed in small amounts distributed on the surface of the Bra. Glandular zone little differentiated. dorsal velum with wavy margin, with two small median projections of equivalent sizes. discussion external morphology The tadpole of Physalaemus albifrons presents features that are similar to those of other members of the P. albifrons species group, like total body length, ovoid body in dorsal and ventral views, eyes dorsolaterally positioned, spiracle single, sinistral and fused to the body wall (perotti and Cspedez, 1999; nomura et al., 2003; Borteiro and Kolenc, 2007). it differs from P. marmoratus because it has rounded nostrils (nomura et al., 2003) and from P. santafecinus because of the spiracle opening,

which is located in the posterior portion of the tube (perotti and Cspedez, 1999). regarding the oral disc, the tadpole of P. albi frons is similar to the tadpoles of P. biligonigerus, P. marmoratus and P. santafecinus, by the presence of a single row of marginal papillae with a large rostral gap, but differs from P. biligonigerus and P. san tafecinus, getting close to P. marmoratus (nomura et al., 2003) by the presence of ventrolateral gaps in the lower lip. Physalaemus albonotatus, like P. cuqui and P. cuvieri, presents a median ventral gap, ventrolateral gaps and p3 is usually shorter than the other rows. Physalaemus fernandezae and P. henselii share the referred features as well (Kolenc et al., 2006). The tadpole of P. albifrons presents labial tooth row formula 2(2)/3(1, 2), like P. rupestris (nascimento et al., 2001). Physalaemus albifrons, P. marmoratus and P. santafecinus have a V-shaped lower jaw sheath, differing from P. biligonigerus, P. cicada and P. cuvi eri, which present a u-shaped one (Cei, 1980; heyer et al., 1990; Borteiro and Kolenc, 2007; Vieira and arzabe, 2008). in all tadpoles of the Physalaemus albifrons species group, the vent tube configuration is dextral, a feature shared with other species in the genus, like P. cuqui and P. cuvieri (heyer et al., 1990; perotti, 1997), P. erythros (Bata et al., 2007) and P. jordanen sis (Gomes et al., 2010). although in P. marmoratus,

Figure 2. The tadpole of Physalaemus albifrons, stage 38 of Gosner (1960): (a) buccal floor and (B) buccal roof (scale = 1 mm).

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P. biligonigerus and P. albifrons, the dextral configuration is only related to its opening, it originates medially and is partially fused to the ventral fin (nomura et al., 2003; Borteiro and Kolenc, 2007). internal oral features The tadpole of Physalaemus albifrons is similar to P. marmoratus and P. santaf ecinus, regarding the number of infralabial papillae (nomura et al., 2003; perotti and Cspedez, 1999). This feature is shared with some species in the P. cu vieri group, such as P. albonotatus, P. centralis and P. cuvieri (Miranda and ferreira, 2009), differing from P. albifrons, P. santafecinus and P. marmoratus by the length of those papillae, which are bigger in species from the P. albifrons group (perotti and Cspedez, 1999; nomura et al., 2003). Physalaemus al bifrons, on the other hand, presents three independent lingual papillae, similar to some species of the P. cu vieri species group (Miranda and ferreira, 2009). Physalaemus albifrons, P. santafecinus and P. marmoratus present pustulations in the anterior region of the buccal floor (perotti and Cspedez, 1999, nomura et al., 2003), which are more dispersed and fewer in number in P. albifrons. The Bfa in P. albi frons and in P. santafecinus are similar in number, location and shape of the papillae (perotti and Cspedez, 1999), but differ in number of pustulations in the region. Three small papillae that occur in the prenarial area in P. albifrons can be misinterpreted as pustulations; they are oriented in a semicircle on the transverse plane of the area. Physalaemus mar moratus and P. santafecinus do not present papillae in this area, but they do present pustulations oriented in a semicircle (perotti and Cspedez, 1999; nomura et al., 2003). The position and shape of the internal nares are similar in all four species of the P. albifrons species group. The presence of four prenarial papillae is shared by P. albifrons, P. marmoratus and P. santaf ecinus (perotti and Cspedez, 1999; nomura et al., 2003). The lateral ridge papilla is bifurcated in P. al bifrons and in P. marmoratus (nomura et al., 2003) and the median ridge presents pustulations in the upper margin in P. albifrons, P. marmoratus, P. san tafecinus and P. biligonigerus, differing in its shape, which is a semicircle in all species except P. biligo nigerus (perotti and Cspedez, 1999; nomura et al., 2003; Borteiro and Kolenc, 2007). The number of papillae in the roof arena may vary from three to four in P. albifrons and P. marmoratus (nomura et al., 2003) and from five to six in P. santafecinus (perotti and Cspedez, 1999).

To conclude, the following features can distinguish Physalaemus albifrons from other tadpoles of Physalaemus: single row of marginal papillae with a large rostral gap, two short gaps in the lower lip in the infra angular region and one gap in the median region; labial tooth row formula 2(2)/3(1, 2); median vent tube, partially fused to the tip of ventral fin, and with dextral opening; three lingual papillae oriented in the transverse plane from the floor arena of the oral cavity. resuMo os girinos de Physalaemus albifrons utilizados nesta descrio foram obtidos de um casal coletado em uma lagoa permanente em Brotas de Macabas, estado da Bahia, Brasil. as caractersticas da morfologia externa so semelhantes aos demais membros do grupo de espcies de P. albifrons, diferindo quanto a presena de interrupes na fileira de papilas marginais do lbio inferior. frmula dentria 2(2)/3(1, 2). a morfologia oral interna difere dos girinos de P. marmoratus, P. santafecinus e P. biligonigerus pela presena de trs papilas linguais, como ocorre no grupo de espcies de P. cuvieri. acKnoWledgeMents
We thank Tiago Silva-Soares (universidade federal do rio de Janeiro ufrJ) for reading and reviewing the manuscript and ana Carolina Guedes (universidade federal da Bahia ufBa) for producing the illustrations; Conselho nacional de desenvolvimento Cientfico e Tecnolgico (Cnpq) and fundao de amparo a pesquisa do estado da Bahia (fapeSB) for financial support. Specimens were collected using the license number 17014-1, issued by the instituto Brasileiro do Meio ambiente e dos recursos renovveis iBaMa.

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