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

Marianna isabella rosa rodrigues de oliveira1,3, luiz norberto Weber1, and

Joice ruggeri2

1 universidade federal da bahia, instituto de Ciências ambientais e Desenvolvimento sustentável. rua Professor José seabra, s/n,Centro. CeP 47805‑100. barreiras, ba, brasil. e‑mail: oliveira.rmi@gmail.com

2 universidade federal da bahia, Departamento de Zoologia, instituto de biologia, Campus universitário de ondina, rua barão de Jeremoabo, s/n, ondina, CeP 40170‑115, salvador, ba, brasil.

3 Corresponding author.

abstract. The tadpoles of Physalaemus albifrons used in this description were obtained from a pair collected in a permanent pond in Brotas de Macaúbas, 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 cur-rently composed of 42 species distributed form north-ern to central argentina, eastern Bolivia, paraguay, uruguay, Brazil, the Guianas, lowlands of southern Venezuela, southeastern Colombia, and western ec-uador (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 taxo-nomic review, P. albifrons species group comprises of four species: P. albifrons Spix, 1824, P. biligonigerus Cope, 1861, P. marmoratus (reinhardt and lütken, 1862) (= P. fuscomaculatus, see nascimento et al., 2006), and P. santafecinus Bario, 1965, all occur-ring 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 spe-cies group have been described, including external and internal oral morphologies (perotti and Céspe-dez, 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 (12°0024’24.65”S, 42°37’35.72”W) in the municipal-ity of Brotas de Macaúbas, Chapada diamantina, Bahia state, Brazil. The Chapada diamantina is covered main-ly by open formations of the Caatinga domain, with dry semi-arid to humid climate, mean temperature 20.6°C and mean altitude 814 m. rainy season comprises the months from november to March (CnM, 2010).

Tadpoles were fixed in 8% formalin and the stag-es of development were defined according to Gos-ner (1960). The description of the external morphol-ogy 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 mi-crometer 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.

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

Body height is 57% of body length, and body width is 65% of body length. Snout rounded in dorsal and lat-eral 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 dorsolater-ally positioned, and with a diameter corresponding to 14% of body length. Spiracle sinistral, narrow, short, located at the middle third of the body, directed up-ward, centripetal wall fused to the body wall, open-ing 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 muscu-lature 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 ex-tensive 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).

250 The tadpole of Physalaemus albifrons

gaps in the lower lip. Jaw sheaths dark, finely serrat-ed. 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 trans-lucid, 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 col-ored, 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 descend-ing sequence of blotches over the region of of the tail insertion, which extends dorsally along the tail mus-culature (fig. 1a). lateral region of body with many dark and brown spots, from the eyes to the lateral-ly-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 transpar-ent 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 discern-ible 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

apices, closer to the posterior pair of infralabial pa-pillae 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, round-shaped 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 ir-regular 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 post-narial 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

table 1. range, mean and standard deviation (Sd) of mea-surements (mm) of Physalaemus albifrons tadpoles (n = 20 stage 36-39), municipality of Brotas de Macaúbas, Bahia, Bra-zil. 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 dis-tance; SSd = Snout-Spiracle distance; odW = oral disc Width.

range Mean SdTl 18.2 – 20.5 19.4 0.6Bl 6.5 – 7.1 6.9 0.2BW 3.9 – 5.3 4.5 0.3Bh 3.4 – 4.3 3.9 0.2

Tail l 11.8 – 13.3 12.5 0.6Th 3.7 – 4.5 4.0 0.3

hTM 1.4 – 2.0 1.7 0.2dfh 1.2 – 1.7 1.5 0.1Vfh 0.6 – 0.9 0.8 0.1ind 0.6 – 0.9 0.7 0.1iod 1.1 – 0.7 0.9 0.1ed 0.7 – 1.2 1.0 0.1nd 0.3 0.3 0

nSd 0.6 – 1.2 1.0 0.2eSd 1.6 – 1.9 1.6 0.1SSd 4.5 – 5.9 5.5 0.3

odW 1.5 – 1.9 1.6 0.1

251oliveira, M. i. r. r. et al.

the side of the major papilla of the postnarial are-na. 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. pres-ence of small irregularities in the margin of the medi-an ridge and four pustulations on the surface. Buccal roof arena (Bra) with three or four finger-like papil-lae 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 differ-entiated. 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 Cés-pedez, 1999; nomura et al., 2003; Borteiro and Ko-lenc, 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 Céspedez, 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 ros-tral 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, ventro-lateral 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 for-mula 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 spe-cies 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 (Baêta 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).

252 The tadpole of Physalaemus albifrons

P. biligonigerus and P. albifrons, the dextral configu-ration is only related to its opening, it originates me-dially 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 Céspedez, 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 Cés-pedez, 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 re-gion of the buccal floor (perotti and Céspedez, 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 Cés-pedez, 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 Céspedez, 1999; nomura et al., 2003).

The position and shape of the internal nares are similar in all four species of the P. albifrons spe-cies group. The presence of four prenarial papillae is shared by P. albifrons, P. marmoratus and P. santaf‑ecinus (perotti and Céspedez, 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 Céspedez, 1999; nomura et al., 2003; Borteiro and Kolenc, 2007). The number of pa-pillae 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 Céspedez, 1999).

To conclude, the following features can distin-guish 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 descrição foram obtidos de um casal coletado em uma lagoa permanente em Brotas de Macaúbas, estado da Bahia, Brasil. as características da morfologia externa são semelhantes aos demais membros do grupo de espécies de P. albifrons, diferindo quanto a presença de interrupções na fileira de papilas marginais do lábio inferior. fórmula dentária 2(2)/3(1, 2). a morfologia oral interna difere dos girinos de P. marmoratus, P. santafecinus e P. biligonigerus pela presença de três papilas linguais, como ocorre no grupo de espécies 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 Científico e Tecnológico (Cnpq) and fundação 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 renováveis – iBaMa.

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Submitted 29 July 2010 accepted 17 november 2010

254 The tadpole of Physalaemus albifrons