Zootaxa 1397: 1724 (2007) www.mapress.

com/ zootaxa/ Copyright 2007 Magnolia Press

ISSN 1175-5326 (print edition)

ZOOTAXA
ISSN 1175-5334 (online edition)

Description of the tadpoles of Proceratophrys cristiceps (Anura: Cycloramphidae, Odontophrynini)

WASHINGTON LUIZ DA SILVA VIEIRA, KLEBER DA SILVA VIEIRA & GINDOMAR GOMES SANTANA
Programa de Ps-graduao em Cincias Biolgicas (rea de concentrao em zoologia) e Coleo Herpetolgica do Departamento de Sistemtica e Ecologia, Universidade Federal da Paraba, Campus I, Joo Pessoa, PB, Brasil 58059-900. E-mail: wlsvieira@yahoo.com.br; ksvieira04@yahoo.com.br; gindomar@yahoo.com.br

Abstract
The tadpoles of Proceratophrys cristiceps (Mller, 1884) are described based on specimens collected in a temporary pool at the Estao Experimental de So Joo do Cariri, in the municipality of So Joo do Cariri, Paraba State, in NE Brazil. Tadpoles in stage 39 had a total length of 30.31 mm, a body length of 12.45 mm (corresponding to 41.07% of their total length), were ovoid shaped in dorsal view, slightly depressed in lateral view, and with a dental formula 2(2)/3(1). The morphological characteristics of the tadpole P. cristiceps were compared with other tadpoles of four species belonging to the Proceratophrys bigibbosa group. Key words. Anura, Cycloramphidae, Proceratophrys cristiceps, tadpole, northeastern Brazil

Introduction The genus Proceratophrys Miranda-Ribeiro, 1920, is currently represented by 18 species distributed throughout a number of morphoclimatic domains, with some species almost exclusively terrestrial and demonstrating mimetic behavior (Sazima 1978). These species usually inhabit the leaf-litter, which makes them difficult to see (Izecksohn & Peixoto 1996), and is one of the factors that has limited studies on these animals (Boquimpani-Freitas 2002). Our knowledge of the biology of many of the species of the genus Proceratophrys is very limited, being restricted to information concerning the feeding and behavioral habits of Proceratophrys boiei Wied-Neuwied, 1825 (Giaretta et al. 1998; Bertoluci 1998), Proceratophrys cururu Eterovick & Sazima, 1998 (Eterovick & Sazima 2000), and Proceratophrys appendiculata Gnther, 1873 (Sazima 1978; Boquimpani-Freitas 2002). The genera Proceratophrys and Odontophrynus Reinhardt & Letken, 1862 are closely related and of uncertain identification (Peixoto & Cruz 1980; Barrio & Barrio 1993). These two taxa were placed in the tribe Odontophrynini by Lynch (1971), but later removed from the family Leptodactylidae Werner, 1896, and placed in Cycloramphidae Bonaparte, 1850 (Frost et al. 2006). Not only do the adult forms of Odontophrynus and Proceratophrys demonstrate many common features, but their tadpoles also share characteristics related to mouth structure, as well as the form of the snout and the body (Peixoto & Cruz 1980; Brando & Batista 2000). The species Proceratophrys cristiceps (Mller, 1884), the focus of the present work, was originally described as Ceratophrys cristiceps Mller, 1884. They were diagnosed by the author of that description according to their color pattern and the distribution of nodules and tuberculos, as verified by Mller (1884).
Accepted by M. Vences: 19 Dec. 2006; published: 25 Jan. 2007

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There is little current information concerning this species and its larval stage is unknown, resulting in its imprecise generic placement (Reig & Limeses 1963; Lynch 1971; Barrio & Barrio 1993). A description of the tadpole of P. cristiceps is presented here, including characteristics of the internal oral anatomy and other new information based on specimens obtained at So Joo do Cariri (Paraba State, Brazil).

Materials and Methods Tadpoles of Proceratophrys cristiceps where captured with a dipnet in a temporary pool (7o2245S and 36o3150W) located in an area of caatinga dry land vegetation at an Estao Experimental de So Joo do Cariri, in the municipality of So Joo do Cariri (72934S and 364153W), Paraba State, NE Brazil, in March of 2006. Analyses of the external morphological characteristics and the illustrations presented here are based on tadpoles in stage 39 (Gosner 1960), employing the dental formula proposed by Altig (1970). All individuals were fixed in 4% formalin and deposited at the Museu Nacional do Rio de Janeiro (MNRJ 41840) and in the Coleo Herpetolgica do Departamento de Sistemtica e Ecologia of the Universidade Federal da Paraba (UFPB 4315). Measurements were taken of 20 individuals using a stereoscopic microscope fitted with a 0.8x micrometric lens, except for the measurements of total length and body length, which were made using precision calipers (0.05 mm). Morphological characteristics follow Altig and Johnston (1986, 1989) and Altig and McDiarmid (1999). In order to observe the marginal papillae, the oral disk was stained with a 2% solution of methylene blue, and the mouth parts (containing the labial teeth) were mounted on temporary slides and observed under a light microscope fitted with a 100x micrometric lens. Additionally, four stage 39 tadpoles were dissected and stained with a 2% solution of methylene blue in order to observe their internal oral structures. The buccopharyngeal terminology follows Wassersug (1976).

Description of the tadpoles of Proceratophrys cristiceps (Mller, 1884) Stage 39 tadpoles (Gosner 1960) demonstrated a globular body form that is slightly depressed in lateral view (Fig. 1A), ovoid in both the dorsal (Fig. 1B) and the ventral view (Fig. 1C), and were wider than they were high (Table I). Body length is approximately 41.1% of the total length; the snout is short and rounded in both the lateral and their dorsal view, large eyes, dorsal, with diameters equal to 15.2% of the body length, interorbital distance is 26.7% of body width; eye-snout distance is 15,5 % of body length, and eye-nostril distance is 7.9% of body length. Nostrils small, rounded, with inter-nasal distance 15.2% of the body width, and positioned dorsally midway between the eyes and the snout. Spiracle short, sinistral, fused to the body and positioned laterally on the medium third of the body, with circular opening directed dorsally. Short vent tube fused to tail with dextral-directed opening (Fig. 1C). Tail with visible muscles, wide base, edge rounded, length equal to 64.1% of total length. Dorsal fin placed at rear third of body, higher than the ventral fin, with its greatest height at the middle of the tail; ventral fin thin and slightly arched. Oral disk emarginate, positioned ventrally (Fig.1C), with width equivalent to 36.1% of body width, surrounded by a single row of marginal papillae, widely interrupted at the anterior section. Some submarginal papillae present, placed more internally in a disperse pattern (Fig. 2A). Papillae long, conical, simple and rounded, with convex extremities. Dental formula 2(2)/3(1); rows A1 and A2 are of similar length; A2 widely interrupted medially; P1 slightly interrupted, and P3 shorter than the others (Fig. 2A). Labial teeth dark, slightly curved towards oral opening, with 22 to 26 cusps (Fig. 2B and 2C). Upper and lower jaw sheaths intensely pigmented and slightly serrated, upper sheath U-shaped and the lower slightly convex.

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FIGURE 1. Proceratophrys cristiceps tadpole at stage 39 (Gosner, 1960), (A) Lateral view, (B) Dorsal view, (C) ventral view (scale = 8,75 mm).

FIGURE 2. Proceratophrys cristiceps tadpole (A) Oral disc (scale = 1,85 mm), (B) Ventral view of apical region of a tooth, (C) Lateral view of a tooth of the A1 row (scale = 0,40 mm).

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The dorsal portion of live tadpoles olive-colored, with scattered dark brown blotches, flanks same color as dorsal portion; spiracle transparent; anterior third of belly whitened and posterior portion pigmented, internal organs visible. Dorsal and ventral fins slightly pigmented, with some blotches of the same color as those seen in the dorsal area, muscular section of the tail more pigmented in the dorsal area than ventral portion. When preserved in formalin, the dorsal area of the tadpoles is dark-brown, with irregularly scattered black blotches, flanks the same color as dorsal area, belly transparent. The ventral and dorsal fins are transparent, with few dark patches; muscular section of the tail slightly pigmented, with small blotches of color as seen on dorsal area. Tadpole measurements are listed in Table I.

TABLE I. Average ( x ), standard deviation (dp), and amplitude (minimum-maximum) of the averages (mm) for tadpoles of Proceratophris cristiceps (n = 20, stage 39).

Measurements
Total length Body length Maximum body height Maximum body width Tail length Maximum tail muscle height Maximum dorsal fin height Maximum ventral fin height Eye diameter Internasal distance Interorbital distance Eye-snout distance Eye-nare distance Oral disk width

x
30.31 12.45 5.51 7.15 19.44 2.54 2.04 1.52 1.89 1.09 1.91 1.94 0.99 2.58

Standard Deviation
1.59 0.78 0.56 0.39 1.21 0.15 0.17 0.15 0.08 0.11 0.14 0.13 0.33 0.14

Amplitude
26.0 33.0 11.0 14.0 5.0 6.9 6.5 8.0 16.5 21.45 2.25 2.87 1.75 2.37 1.25 1.87 1.75 2.0 0.87 1.25 1.75 2.25 1.62 2.12 0.75 2.25 2.37 2.75

Internal oral anatomy buccal floor circular and wide (Fig. 3A). Mouth opening equivalent to 11.8 % of width of buccal floor. Presence of four simple infralabial papillae, conical, with apices rhomboid and margins pustulose, anterior pair long and median pair short. Three long and bifurcate lingual papillae with sharp apices are present on buccal floor. Four short and conical prepocket papillae, three with rounded apices, only one is bifurcate with sharp apex. Buccal floor arena triangular, with eight long papillae and 14-17 smaller papillae on each side, majority of these are conical with sharp tips. Internal section of Buccal floor arena with long pustulations, homogeneously spread, with 30 to 40 small papillae among those pustulations. Buccal pocket longer than wide, oriented transversally over the mid region of the buccal floor. Velar surface free, long, with posterior margin continuous and lightly dentate. Glottis distinct, with opening slightly exposed. Buccal roof slightly triangular, thin in prenarinal arena and wide behind (Fig. 3B). Presence of curved transversal ridge in prenarinal arena, directly in front of internal nares. Internal nares longer than wide, oriented horizontally, positioned approximately 30.9% of the distance between the oral disk and the esophagus. Anterior section of each nare with pustulations, posterior section with convex narial valve, only slightly or not at all raised.

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FIGURE 3. Proceratophrys cristiceps tadpole (A) Floor and (B) roof of buccopharyngeal cavity (scale = 2,33 mm). bfa = buccal floor arena; bfap = buccal floor arena papillae; bp = buccal pocket; bra = buccal roof arena; brap = buccal roof arena papillae; dv = dordal velum; fr = filter row; g = glottis; gz = glandular zone; in = internal nares; ip = infralabial papillae; ir = infrarostrodont; lp = lingual papillae; lrp = lateral ridge papillae; mr = median ridge; p = pustulation; pa = prenarinal arena; pp = prepocket papillae; ptp = postnarial papillae; sr = suprarostrodont; vv = ventral velum. TADPOLES OF PROCERATOPHRYS CRISTICEPS

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Postnarinal arena narrow with four papillae, anteromedial pair short and conical, posterolateral pair long, equally conical. Among the postnarial papillae are five to eight pustulations. Median ridge wide and semi-circular, with four to five long papillae with sharp tips on free surface. Lateral ridge papillae elaborate, oriented transversally on each side of the median ridge and with four to five short papillae on anterior margin. Two long papillae are projected medially over the median ridge. Buccal roof arena narrow, with four papillae located posterior to median ridge, with semi-circular format, surrounded by five long papillae and four to five smaller papillae, all conical with sharp apices. Small pustulations homogeneously distributed within the Buccal roof arena, with 20-30 small papillae among the pustulations. Glandular zone conspicuous, with small pustulations and 35-40 small papillae. Dorsal velum long, gradually curving, interrupted medially and with free margin pustulate.

Discussion Only eight tadpoles of the eighteen known species of Proceratophrys have been described until the present moment (S & Langone 2002; Cruz et al. 2005), although the characteristics of the caudal fins, the dental formula and body form of the larvae of P. goyana and P. schirchi were described by Rossa-Feres and Jim (1996), and Brando and Batista (2000). There is currently no information available concerning tadpoles of the species in the group of P. bigibbosa (Peters 1872), such as P. brauni (Kwet & Faivovich 2001), P. cristiceps, P. fryi (Gnther 1873), P. melanopogon (Miranda-Ribeiro 1926), P. phyllostomus Izecksohn (Cruz & Peixoto 1999), and P. subguttata (Izecksohn, Cruz, & Peixoto 1999). The characteristics observed in the tadpoles of the species P. cristiceps, such as ovoid body slightly depressed, dorsal fin higher than the ventral fin, oral disk in ventral position, left-spiraled, vent tube with dextral opening, oral disk surrounded by marginal papillae, and dental formula 2(2)/3(1), all characteristics shared with all representatives of the genus Proceratophrys (S & Langone 2002). When tadpoles of P. cristiceps are compared to the species P. avelinoi Barrio & Barrio, 1993, P. cururu Eterovick & Sazima, 1998, P. concavitympanum Giaretta, Bernarde & Kokubum, 2000, and P. palustris Giaretta & Sazima, 1993, species whose adult forms are intimately related to P. cristiceps (Lynch 1971; Eterovick & Sazima 1998; Giaretta et al. 2000), it can be seen that the species P. concavitympanum shares with P. cristiceps the presence of a short vent tube and submarginal papillae on the lower lip. The existence of submarginal papillae also group these species with P. cururu and P. avelinoi, according to the descriptions of Eterovick and Sazima (1998), and S and Langone (2002). P. cururu also has a P3 row shorter than the P1 and P2, a characteristic also seen in P. cristiceps, but different from that encountered in P. palustris, P. avelinoi, which have a vestigial P3, and P. concavitympanum, which has a V-shaped P3 the same length as P1 and P2. Among the characteristics observed, the presence of submarginal papillae in tadpoles of P. cristiceps demonstrates a unique condition of submarginal papillae on both the superior and inferior lips. Among the species examined, this places P. cristiceps closest to P. avelinoi, which has submarginal papillae on the upper lip, and P. concavitympanum, which has sub-marginal papillae on the lower lip. The lack of sufficient information concerning these characteristics for P. cururu prevents comparisons with this species at this time (see Eterovick & Sazima 1998). According to S and Langone (2002), information concerning the internal oral anatomy of tadpoles of Proceratophrys is still very limited, and is available only for the species P. appendiculata (Gnther 1873), P. boiei (Wied-Newied 1825), and P. avelinoi. A comparison of the internal oral anatomy of P. cristiceps with that of P. avelinoi reveals many similarities between them, with the major differences being observed within the buccal roof. Tadpoles of P. cristiceps differ from P. avelinoi basically by having horizontally oriented nares, four postnarial papillae, with the anteromedial pair short and conical and the posterolateral pair being long but equally

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conical, five to eight pustulations between the postnarial papillae, medial ridge wide and in the form of semicircle, with four to five long papillae. The glandular zone is conspicuous, with small pustulations, buccal floor is approximately circular, the infralabial papillae are of different sizes, with the anterior pair being long, and the median pair short. The lingual papillae are long and bifurcated, and the buccal floor arena triangular. Of the species that were examined, the tadpoles of P. palustris shared with P. cristiceps only those characteristics common to all representatives of that genus; the convex form of the posterior portion of the lower lip is one of the characteristics that differentiates these tadpoles from P. avelinoi, P. cururu, and P. concavitympanum. In P. palustris, slight concavities in the lateral portion of the oral disk were observed, these giving rise to lateral folds of the lower lip, a characteristic not observed in tadpoles of P. cristiceps. The tadpole this latter species is more similar to species in the genus Odontophrynus (see Savage & Cei 1965 and Brando & Batista 2000).

Acknowledgements The authors would like to thank the Programa de Ps-graduao em Cincias Biolgicas, the Conselho Nacional de Desenvolvimento Cientfico e Tecnolgico (CNPq), and the Programa de Pesquisas Ecolgicas de Longa Durao (PELD) for their financial support, as well as the So Joo do Cariri Meteorological Station for logistic support and their cooperation with the field work.

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