Journal of Herpetology, Vol. 48, No. 3, 434–438, 2014 Copyright 2014 Society for the Study of and Reptiles

The Tadpole of azarai (Gallardo, 1965) with Comments on Larval Morphology in the Group (Anura: Bufonidae)

1,2 1 3 BORIS L. BLOTTO, MARTI´N O. PEREYRA, AND DIEGO BALDO

1Divisio´n Herpetologı´a, Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’– CONICET, A´ ngel Gallardo 470, C1405DJR, Ciudad Auto´noma de Buenos Aires, Argentina 3Laboratorio de Gene´tica Evolutiva, Instituto de Biologı´a Subtropical (CONICET-UNaM), Facultad de Ciencias Exactas, Universidad Nacional de Misiones; Fe´lix de Azara 1552, CPA N3300LQF, Posadas, Misiones, Argentina

ABSTRACT.—We describe the larval morphology of Rhinella azarai, a medium-sized species of the Rhinella granulosa group. None of the morphological characters allow the larvae of R. azarai to be distinguished unequivocally from those of other species in the group. However, the tadpoles show a distinctive set of character states shared with some species of the group, which may represent putative synapomorphies of the R. granulosa group or internal clades.

Rhinella is a diverse genus of composed of 86 species Biologı´a Subtropical (CONICET-UNaM), Posadas, Misiones, (Frost, 2013). Species groups have been defined on the basis of Argentina (LGE 2438, LGE 2440). A third series (LGE 2439) external morphology and osteological characters (Martin, 1972; was raised in the laboratory from an egg clutch obtained from Duellman and Schulte, 1992). The Rhinella granulosa group is an amplectant pair from the same locality. All specimens and composed of 13 species of medium-sized toads distributed in egg clutches were fixed in 10% formalin. The tadpole series LGE southern Panama´ and South America (Narvaes and Rodrigues, 2438 and LGE 2440 were assigned to R. azarai by comparison to 2009). Ecologically, the species are characterized by inhabiting the one raised in captivity. Tadpoles in these series differ lowlands, displaying explosive reproductive aggregations dur- remarkably in some characters and are significantly smaller ing rains, and sheltering in holes they dig using their legs from other bufonids species found in the study area (Rhinella (Narvaes and Rodrigues, 2009). schneideri and , see Table 1). Clutches (LGE 3736 Rhinella azarai (Gallardo, 1965) is known from eastern Para- and LGE 3737) were obtained from two additional amplectic guay, Mato Grosso do Sul (), and northeastern Argentina pairs, which were taken to the laboratory where they laid eggs. (Gallardo, 1957; Narvaes and Rodrigues, 2009; Ingaramo et al., Individual eggs and egg strings were measured to the nearest 2012). Knowledge about its reproductive biology is limited to 0.1 mm using an ocular micrometer in a Nikon SMZ–10 descriptions of reproductive sites (Narvaes and Rodrigues, stereoscopic microscope. Morphological terminology follows 2009). Altig and McDiarmid (1999a). Tadpoles were staged according Information on larval morphology of the R. granulosa group is to Gosner (1960), and oral discs were stained with a 1% solution limited to seven species: (Borteiro et al., 2006 of methylene blue to enhance visualization of marginal papillae. [as Chaunus dorbignyi]), (Ferna´ndez, 1927 [as Measurements were taken from digital photographs (taken with Bufo dorbignyi]; Lavilla et al., 2000 [as Bufo fernandezae]; Borteiro a digital camera Micrometrics 391CU 3.2 M CCD) of 10 et al., 2006 [as Chaunus fernandezae]), R. granulosa (Merceˆs et al., individuals to the nearest 0.01 mm (Gosner stage 35; LGE 2009), (Kenny, 1969 [as Bufo granulosus beebei]; 2440), using a stereoscopic microscope fitted with a 0.8· and Lynch, 2006 [as B. granulosus]), Rhinella major (Lavilla et al., 2000 equipped with a Micrometricst SE Premium 4 software. The [as B. granulosus major]), Rhinella merianae (Hero, 1990 [as B. same morphological measurements described by Kolenc et al. granulosus]), and Rhinella pygmaea (de Carvalho e Silva and de (2009) were taken, with the addition of the ventral gap length Carvalho e Silva, 1994 [as Bufo pygmaeus]). The only available (VG, distance of the lower lip free of papillation). The other two data for comes from Yanosky et al. (1993), who tadpole series (LGE 2438 and LGE 2439) were considered for presented an illustration of the tadpole (as Bufo pygmaeus). comparison of coloration and morphology. Values are reported However, these data must be taken cautiously because R. as mean 6 SD, min–max. For comparisons with other Rhinella fernandezae and R. major are present in the area, and it is not species, published descriptions of larvae were compiled from stated how the material was identified. Here, we provide a the literature (see Table 1). Observations of reproductive biology detailed description of the tadpole of R. azarai, compare it with were taken ad libitum between 1999 and 2012. the other known tadpoles of the R. granulosa group, and discuss putative synapomorphies for both the species group and internal clades. RESULTS Reproductive Biology.—Reproduction occurs after heavy rains, MATERIALS AND METHODS during the spring and summer (September to February). This Two series of tadpoles were collected in a pond located in the species, as other taxa of the R. granulosa group, is a typical Campus of Universidad Nacional de Misiones (UNaM), Villa explosive breeder (sensu Wells, 1977). During the breeding Lanu´s, Departamento Capital, Misiones (2782601300 S, season the males aggregate in choruses in temporary and 5585303900 W; 99 m a.s.l.), and deposited in the herpetological semitemporary shallow pools. The amplexus is axillary, and the collection of the Laboratorio de Gene´tica Evolutiva, Instituto de eggs are laid in long coiled strings arranged linearly and attached to submerged vegetation. The two amplectant pairs laid 3,770 2Corresponding Author. E-mail: [email protected] (LGE 3736) and 7,548 eggs (LGE 3737) in the laboratory. The eggs DOI: 10.1670/12-121 in preservative have a mean diameter of 1.19 mm to level of TABLE 1. Selected characteristics of the larvae of Rhinella. LTRF: Labial tooth row formula.

Flap-bearing P3 Color pattern of dorsal Species Species group LTRF labial teeth row Submarginal papillae region of caudal musculature Source R. azarai granulosa 2(2)/2 — Absent Banded This study R. dorbignyi granulosa 2(2)/2 — Absent Banded Borteiro et al., 2006 R. fernandezae granulosa 2(2)/2[1] — Absent/present Banded Lavilla et al., 2000; Borteiro et al., 2006 R. granulosa granulosa 2(2)/3 Present Absent Banded Merceˆs et al., 2009 R. humboldti granulosa 2(2)/3 Present Absent Uniformly pigmented/banded Kenny, 1969; Lynch, 2006 R. major granulosa 2(2)/3 Absenta Absent/present Uniformly pigmented Lavilla et al., 2000 R. merianae granulosa 2(2)/3 ? Absenta Uniformly pigmented Hero, 1990 R. pygmaea granulosa 2(2)/2 — Absenta Banded de Carvalho e Silva and de Carvalho e Silva, 1994 R. abei crucifer 2(2)/3 Absent Present Uniformly pigmented Fehlberg et al., 2012 R. crucifer crucifer 2(2)/3 Absent Present Uniformly pigmented Ruas et al., 2012 R. ornata crucifer 2(2)/3 Absent Present Uniformly pigmented Heyer et al., 1990 OF TADPOLE R. pombali crucifer 2(2)/3 Absent Present Uniformly pigmented Lourenc¸o et al., 2010 R. arenarum marina 2(2)/3[1] Absent Present Uniformly pigmented Ferna´ndez, 1927; Cei, 1980; Fabrezi and Vera, 1997; Vera Candioti, 2007 R. cerradensis marina 2(2)/3(1) Absent ? Uniformly pigmented Maciel et al., 2007 R. icterica marina 2(2)/3[1] Absent Present Uniformly pigmented Heyer et al., 1990 R. jimi marina 2(2)/3[1] Absent Present Uniformly pigmented Merceˆs et al., 2009; Tolledo and Toledo, 2010

R. marina marina 2(2)/3 Absent Absent/present Uniformly pigmented Savage, 1960; Kenny, 1969; Ford and Scott, 1996; AZARAI RHINELLA Duellman, 2005 R. rubescens marina 2(2)/3(1) Absent Presenta Uniformly pigmented Eterovick and Sazima, 1999 R. schneideri marina 2(2)/3[1] Absent Present Uniformly pigmented Rossa-Feres and Nomura, 2006; Cei, 1980; Fabrezi and Vera, 1997 R. arequipensis spinulosa 2(2)/3 Absent Present Uniformly pigmented Aguilar and Gamarra, 2004 R. atacamensis spinulosa 2(2)/3 Absenta Presenta Uniformly pigmented Cei, 1962 R. chilensis spinulosa 2(2)/3 Absenta ? Uniformly pigmented Mu¨ ller and Hellmich, 1932; Cei, 1962 R. limensis spinulosa 2(2)/3[1] Absent Present Uniformly pigmented Angulo and Aguilar, 2003; Aguilar and Gamarra, 2004; Aguilar et al., 2007 R. rubropunctata spinulosa 2(2)/3b Absent ? Uniformly pigmented Formas and Pugin, 1978 R. spinulosa spinulosa 2(2)/3 Absent Present Uniformly pigmented Ferna´ndez, 1927; Donoso-Barros, 1975; Aguilar et al., 2007; Vera Candioti, 2007 R. chrysophora veraguensis 2/3 Absent ? Banded McCranie et al., 1989; Pramuk and Lehr, 2005 R. quechua veraguensis 2/3 Absent Present Uniformly pigmented Aguayo et al., 2009 R. veraguensis veraguensis 2/3 Absent Present Banded Cadle and Altig, 1991; Pramuk and Lehr, 2005 R. castaneotica margaritifera 2(2)/3 Absent Absent Uniformly pigmented Caldwell, 1991 R. hoogmoedi margaritifera 2(2)/3 Absent Absenta Uniformly pigmented Merceˆs et al., 2009 R. magnussoni margaritifera 2(2)/3 Absent Absent Only the proximal third pigmented Lima et al., 2007 R. margaritifera margaritifera 2(2)/3 Absent Present Uniformly pigmented Duellman, 1978, 2005; Caldwell, 1991 R. proboscidea margaritifera 2(2)/3 Absent Absent Uniformly pigmented Menin et al., 2006 R. scitula margaritifera 2(2)/3 Absent Absenta Uniformly pigmented Caramaschi and Niemeyer, 2003 aInformation inferred from the pictures from the original articles. b2/3 in the text, but the figure clearly shows a 2(2)/3 formulae. 435 436 B. L. BLOTTO ET AL. vitelinic capsule (range = 1.06–1.33; N = 42) and have a darkly pigmented pole and a beige vegetal pole; they are staggered in a unilayered outer jelly string approximately 3 mm wide (type I sensu Altig and McDiarmid, 2007). Tadpole Morphology.—Ten tadpoles (Gosner [1960] stage 35) were measured (Table 2). The larvae in stage 35 (Fig. 1 A, B, C) have the body depressed (BMH/BMW = 0.74 6 0.06), ovoid in dorsal view. Body length less than half of the total length (BL/TL = 0.41 6 0.02). Body maximum width located at the level of the spiracle opening. Snout rounded in lateral view, and rounded to slightly truncate in dorsal view. Nostrils oval with a small medial projection, resulting in a subreniform opening; dorsally located (EN/BWE = 0.36 6 0.03), closer to the eye than to the snout (FN/END = 1.26 6 0.24, N = 8) or equidistant (N = 2). Eyes large (E/BWE = 0.24 6 0.024) and dorsal (IOD/BWE = 0.69 6 0.04). Pineal end organ visible as a small, unpigmented protuberance between the eyes. Spiracle single, sinistral, lateral, directed posterodorsally, with the inner wall fused to the body. Spiracle opening oval, with smaller diameter than the tube width, and located at the level of the posterior third of the body (RSD/ BL = 0.65 6 0.06); it is visible both dorsally and ventrally. Intestinal assa (‘‘point de rebroussement’’; sensu Hourdry and FIG. 1. Tadpole of Rhinella azarai, stage 35, LGE 2440. (A) Dorsal Beaumont, 1985) located approximately at the center of the view. (B) Lateral view. (C) Ventral view. (D) Oral disc. Scale bars = 1mm abdominal ventral surface. Vent tube always starting medially (A, B), and = 0.25 mm (C). PEO = pineal end organ. but opening medially (N = 4) or dextrally (N = 6). Tail medium- sized (TAL/TL = 0.58 6 0.04), with its maximum height slightly where we did not find any clear diagnostic feature to lower than the body (MTH/BMH = 0.90 6 0.10). Tail axis distinguish the tadpole of R. azarai from the other species in straight. Dorsal fin originating at the body-tail junction, with a the group. In addition to morphology that overlaps other uniformly convex free margin. Ventral fin fused to the vent tube; Rhinella tadpoles, those of the R. granulosa group have a free margin somewhat parallel to the tail axis. Tail tip rounded, distinctive combination of characters. The pattern of white without caudal musculature. Oral disc (Fig. 1 D) anteroventral, unpigmented bands on the dorsum of the caudal musculature medium sized (OD/BMW = 0.30 6 0.02), emarginated with a in the tadpole of R. azarai has also been reported for most single row of marginal papillae laterally located. Dorsal gap wide tadpoles of the R. granulosa group (with the exception of R. (DG/OD = 0.84 6 0.06) and ventral gap medium sized (VG/OD major, and R. merianae, and polymorphic in R. humboldti), as = 6 0.66 0.07). Marginal papillae simple, longer than wide, and opposed to the uniform pigmentation in the remainder species with rounded tip. Submarginal papillae absent. Jaw sheaths of Rhinella (the only exception is Rhinella chrysophora, with fewer distally pigmented, with marginal serrations. Upper jaw sheath and greatly expanded bands, and extended through most or all wider than long, with free margin U-shaped; lower jaw sheath V- the lateral region of the caudal musculature; McCranie et al., shaped. Labial tooth row formula (LTRF) 2(2)/2. Labial teeth 1989: fig. 2). The pattern of white bands is a putative curved, with an oblong, relatively short head with four to six synapomorphy of the R. granulosa group or an internal clade. cusps. Another typical character state of this group is the absence of Coloration in Preservative.—Dorsally and laterally brownish, submarginal papillae in the oral disc, which are present only in perinarial region darker, ventral region with scattered melano- some individuals of R. fernandezae and R. major. This type of cytes, being the intestine visible by transparency. Spiracle with papillae is also absent from five of the six known species of the scattered spots on its base and vent tube unpigmented. Jaw R. margaritifera species group (present only in R. margaritifera), sheaths dark brown. Ventral fin transparent and unpigmented. whereas they are present in all the described tadpoles of Rhinella Dorsal fin mostly transparent with melanocytes covering crucifer, Rhinella marina (polymorphic in R. marina), Rhinella irregularly some blood vessel, giving a thin brownish reticulated spinulosa, and Rhinella veraguensis species groups. Although not pattern. Caudal musculature brownish, less pigmented toward all the species have been examined for the character (Table 1), the ventral region, being totally unpigmented in the ventral the absence of submarginal papillae could be considered a quarter of it. Dorsal region of the caudal musculature with seven putative synapomorphy of R. granulosa species group. This to eight irregular whitish stripes (attributable to the absence of hypothesis could be tested in the future when data for the melanocytes), which are more evident in dorsal view. remaining species became available. The absence of this type of papillae occurs also in five of the six known tadpoles species of DISCUSSION the R. margaritifera group. A comment must be made with Tadpoles of R. azarai are similar to those of most Rhinella respect to the presence of submarginal papillae in R. margar- species (and those of most bufonid larvae), having a small, itifera and Rhinella scitula. Duellman (1978) is not clear about the globose and dark body, with a medium-sized tail (Altig and presence of submarginal papillae in R. margaritifera, and no McDiarmid, 1999b). Additionally, morphological similarities figure of the oral disc is presented in that paper. Caldwell (1991) within Rhinella margaritifera (Menin et al., 2006) and R. marina describes the submarginal papillae as present in R. margaritifera, (Tolledo and Toledo, 2010) species groups have been identified as did Duellman (2005). Subsequently, Menin et al. (2006) previously. It is also the case for the R. granulosa species group, considered submarginal papillae absent in R. margaritifera TADPOLE OF RHINELLA AZARAI 437

TABLE 2. Mean measurements, standard deviations, and range (in characters that permit unequivocal differentiation between millimeters) of 10 Rhinella azarai tadpoles in Stages 35 of Gosner (1960), species, it shows interesting variability at a supraspecific level. LGE 2440. As a phylogenetic hypothesis for the group becomes available, it would be possible to better interpret the patterns of morpho- Characteristic Mean 6 SD Range logical diversity reported here. In the same way, oral morphol- Total length (TL) 13.98 6 0.36 13.36–14.58 ogy of tadpoles of the genus Rhinella shows interesting variation Body length (BL) 5.78 6 0.18 5.38–6.04 that may prove to be synapomorphies of some groups, and the 6 Body maximum width (BMW) 4.14 0.12 3.96–4.32 inclusion of this source of evidence in future phylogenetic Body width at nostrils (BWN) 1.86 6 0.13 1.58–2.02 Body width at eye level (BWE) 2.90 6 0.10 2.68–2.99 analyses would improve our understanding of the evolution of Body maximum height (BMH) 3.08 6 0.14 2.89–3.30 these features. Tail length (TAL) 8.13 6 0.33 7.6–8.52 6 Maximum tail height (MTH) 2.77 0.17 2.62–3.2 Acknowledgments.—We are grateful to M. F. Vera Candioti Dorsal fin height (DFH) 1.22 6 0.10 1.13–1.49 Ventral fin height (VFH) 0.91 6 0.08 0.81–1.06 who kindly prepared the illustrations. We thank J. Faivovich Tail muscle height (TMH) 1.18 6 0.04 1.09–1.22 and M. F. Vera Candioti for critical comments on the Internarial distance (IND) 0.62 6 0.03 0.58–0.66 manuscript; and E. Krauczuk, J. Vero´n, M. D’Oria, M. Baleani, 6 Extra nasal distance (EN) 1.04 0.06 0.95–1.16 and P. Quiroga for field assistance. We thanks to ANPCyT PICT- Interorbital distance (IOD) 2.00 6 0.04 1.93–2.06 Intraocular distance (IO) 0.86 6 0.04 0.8–0.93 2007-2202 and 2011-1895, and Consejo Nacional de Investiga- Eye diameter (E) 0.70 6 0.05 0.61–0.76 ciones Cientı´ficas y Te´cnicas (CONICET) for financial support. Nostril major axis (N) 0.24 6 0.04 0.18–0.27 DLB thanks Instituto de Herpetologı´a (FML), CONICET PIP Eye–nostril distance (END) 0.39 6 0.03 0.35–0.45 1112008010 2422, and ANPCyT PICT-O 37035. Fronto–nasal distance (FN) 0.48 6 0.07 0.36–0.59 Rostro–spiracular distance (RSD) 3.73 6 0.24 3.4–4.25 Oral disc width (OD) 1.24 6 0.04 1.19–1.33 Dorsal gap length (DG) 1.04 6 0.04 0.99–1.11 Ventral gap length (VG) 0.82 6 0.06 0.72–0.90 LITERATURE CITED AGUAYO, R., E. O. 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