The Tadpole of Rhinella Azarai (Gallardo, 1965) with Comments on Larval Morphology in the Rhinella Granulosa Species Group (Anura: Bufonidae)

Journal of Herpetology, Vol. 48, No. 3, 434–438, 2014 Copyright 2014 Society for the Study of Amphibians and Reptiles The Tadpole of Rhinella azarai (Gallardo, 1965) with Comments on Larval Morphology in the Rhinella granulosa Species Group (Anura: Bufonidae) 1,2 1 3 BORIS L. BLOTTO, MARTIŃ O. PEREYRA, AND DIEGO BALDO 1Divisioń Herpetologıá, Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’– CONICET, A´ ngel Gallardo 470, C1405DJR, Ciudad Autońoma de Buenos Aires, Argentina 3Laboratorio de Gene´tica Evolutiva, Instituto de Biologıá 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 toads composed of 86 species Biologıá 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 Rhinella icterica, 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 (Brazil), 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: Rhinella dorbignyi (Borteiro et al., 2006 of methylene blue to enhance visualization of marginal papillae. [as Chaunus dorbignyi]), Rhinella fernandezae (Fernańdez, 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), Rhinella humboldti (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 Rhinella bergi 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 TADPOLE OF R. pombali crucifer 2(2)/3 Absent Present Uniformly pigmented Lourenço et al., 2010 R. arenarum marina 2(2)/3[1] Absent Present Uniformly pigmented Fernańdez, 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; RHINELLA AZARAI 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 Fernańdez, 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 animal 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).

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