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

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1 Journal of Herpetology, Vol. 48, No. 3, , 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) BORIS L. BLOTTO, 1,2 MARTÍN O. PEREYRA, 1 AND DIEGO BALDO 3 1 División Herpetología, Museo Argentino de Ciencias Naturales Bernardino Rivadavia CONICET, Angel Gallardo 470, C1405DJR, Ciudad Autónoma de Buenos Aires, Argentina 3 Laboratorio de Genética Evolutiva, Instituto de Biología Subtropical (CONICET-UNaM), Facultad de Ciencias Exactas, Universidad Nacional de Misiones; Félix 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 (Frost, 2013). Species groups have been defined on the basis of external morphology and osteological characters (Martin, 1972; Duellman and Schulte, 1992). The Rhinella granulosa group is composed of 13 species of medium-sized toads distributed in southern Panamá and South America (Narvaes and Rodrigues, 2009). Ecologically, the species are characterized by inhabiting lowlands, displaying explosive reproductive aggregations during rains, and sheltering in holes they dig using their legs (Narvaes and Rodrigues, 2009). Rhinella azarai (Gallardo, 1965) is known from eastern Paraguay, Mato Grosso do Sul (Brazil), and northeastern Argentina (Gallardo, 1957; Narvaes and Rodrigues, 2009; Ingaramo et al., 2012). Knowledge about its reproductive biology is limited to descriptions of reproductive sites (Narvaes and Rodrigues, 2009). Information on larval morphology of the R. granulosa group is limited to seven species: Rhinella dorbignyi (Borteiro et al., 2006 [as Chaunus dorbignyi]), Rhinella fernandezae (Fernández, 1927 [as Bufo dorbignyi]; Lavilla et al., 2000 [as Bufo fernandezae]; Borteiro et al., 2006 [as Chaunus fernandezae]), R. granulosa (Merces ˆ et al., 2009), Rhinella humboldti (Kenny, 1969 [as Bufo granulosus beebei]; Lynch, 2006 [as B. granulosus]), Rhinella major (Lavilla et al., 2000 [as B. granulosus major]), Rhinella merianae (Hero, 1990 [as B. granulosus]), and Rhinella pygmaea (de Carvalho e Silva and de Carvalho e Silva, 1994 [as Bufo pygmaeus]). The only available data for Rhinella bergi comes from Yanosky et al. (1993), who presented an illustration of the tadpole (as Bufo pygmaeus). However, these data must be taken cautiously because R. fernandezae and R. major are present in the area, and it is not stated how the material was identified. Here, we provide a detailed description of the tadpole of R. azarai, compare it with the other known tadpoles of the R. granulosa group, and discuss putative synapomorphies for both the species group and internal clades. MATERIALS AND METHODS Two series of tadpoles were collected in a pond located in the Campus of Universidad Nacional de Misiones (UNaM), Villa Lan us, Departamento Capital, Misiones ( S, W; 99 m a.s.l.), and deposited in the herpetological collection of the Laboratorio de Genética Evolutiva, Instituto de 2 Corresponding Author. boris@macn.gov.ar DOI: / Biología Subtropical (CONICET-UNaM), Posadas, Misiones, Argentina (LGE 2438, LGE 2440). A third series (LGE 2439) was raised in the laboratory from an egg clutch obtained from an amplectant pair from the same locality. All specimens and egg clutches were fixed in 10% formalin. The tadpole series LGE 2438 and LGE 2440 were assigned to R. azarai by comparison to the one raised in captivity. Tadpoles in these series differ remarkably in some characters and are significantly smaller from other bufonids species found in the study area (Rhinella schneideri and Rhinella icterica, see Table 1). Clutches (LGE 3736 and LGE 3737) were obtained from two additional amplectic pairs, which were taken to the laboratory where they laid eggs. Individual eggs and egg strings were measured to the nearest 0.1 mm using an ocular micrometer in a Nikon SMZ 10 stereoscopic microscope. Morphological terminology follows Altig and McDiarmid (1999a). Tadpoles were staged according to Gosner (1960), and oral discs were stained with a 1% solution of methylene blue to enhance visualization of marginal papillae. Measurements were taken from digital photographs (taken with a digital camera Micrometrics 391CU 3.2 M CCD) of 10 individuals to the nearest 0.01 mm (Gosner stage 35; LGE 2440), using a stereoscopic microscope fitted with a 0.8 and equipped with a Micrometricst SE Premium 4 software. The same morphological measurements described by Kolenc et al. (2009) were taken, with the addition of the ventral gap length (VG, distance of the lower lip free of papillation). The other two tadpole series (LGE 2438 and LGE 2439) were considered for comparison of coloration and morphology. Values are reported as mean 6 SD, min max. For comparisons with other Rhinella species, published descriptions of larvae were compiled from the literature (see Table 1). Observations of reproductive biology were taken ad libitum between 1999 and RESULTS Reproductive Biology. Reproduction occurs after heavy rains, during the spring and summer (September to February). This species, as other taxa of the R. granulosa group, is a typical explosive breeder (sensu Wells, 1977). During the breeding season the males aggregate in choruses in temporary and semitemporary shallow pools. The amplexus is axillary, and the eggs are laid in long coiled strings arranged linearly and attached to submerged vegetation. The two amplectant pairs laid 3,770 (LGE 3736) and 7,548 eggs (LGE 3737) in the laboratory. The eggs in preservative have a mean diameter of 1.19 mm to level of

2 TADPOLE OF RHINELLA AZARAI 435 TABLE 1. Selected characteristics of the larvae of Rhinella. LTRF: Labial tooth row formula. Species Species group LTRF Flap-bearing P3 labial teeth row Submarginal papillae Color pattern of dorsal 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 Mercês et al., 2009 R. humboldti granulosa 2(2)/3 Present Absent Uniformly pigmented/banded Kenny, 1969; Lynch, 2006 R. major granulosa 2(2)/3 Absent a Absent/present Uniformly pigmented Lavilla et al., 2000 R. merianae granulosa 2(2)/3? Absent a Uniformly pigmented Hero, 1990 R. pygmaea granulosa 2(2)/2 Absent a 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 R. pombali crucifer 2(2)/3 Absent Present Uniformly pigmented Louren co et al., 2010 R. arenarum marina 2(2)/3[1] Absent Present Uniformly pigmented Fernández, 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 Mercês 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; Duellman, 2005 R. rubescens marina 2(2)/3(1) Absent Present a 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 Absent a Present a Uniformly pigmented Cei, 1962 R. chilensis spinulosa 2(2)/3 Absent a? Uniformly pigmented Müller 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)/3 b Absent? Uniformly pigmented Formas and Pugin, 1978 R. spinulosa spinulosa 2(2)/3 Absent Present Uniformly pigmented Fernández, 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 Absent a Uniformly pigmented Mercês 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 Absent a Uniformly pigmented Caramaschi and Niemeyer, 2003 a Information inferred from the pictures from the original articles. b 2/3 in the text, but the figure clearly shows a 2(2)/3 formulae.

3 436 B. L. BLOTTO ET AL. vitelinic capsule (range = ; 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). 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 = ), ovoid in dorsal view. Body length less than half of the total length (BL/TL = ). 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 = ), closer to the eye than to the snout (FN/END = , N = 8) or equidistant (N = 2). Eyes large (E/BWE = ) and dorsal (IOD/BWE = ). 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 = ); it is visible both dorsally and ventrally. Intestinal assa ( point de rebroussement ; sensu Hourdry and Beaumont, 1985) located approximately at the center of the abdominal ventral surface. Vent tube always starting medially but opening medially (N = 4) or dextrally (N = 6). Tail mediumsized (TAL/TL = ), with its maximum height slightly lower than the body (MTH/BMH = ). Tail axis straight. Dorsal fin originating at the body-tail junction, with a uniformly convex free margin. Ventral fin fused to the vent tube; free margin somewhat parallel to the tail axis. Tail tip rounded, without caudal musculature. Oral disc (Fig. 1 D) anteroventral, medium sized (OD/BMW = ), emarginated with a single row of marginal papillae laterally located. Dorsal gap wide (DG/OD = ) and ventral gap medium sized (VG/OD = ). Marginal papillae simple, longer than wide, and with rounded tip. Submarginal papillae absent. Jaw sheaths distally pigmented, with marginal serrations. Upper jaw sheath wider than long, with free margin U-shaped; lower jaw sheath V- shaped. Labial tooth row formula (LTRF) 2(2)/2. Labial teeth curved, with an oblong, relatively short head with four to six cusps. Coloration in Preservative. Dorsally and laterally brownish, perinarial region darker, ventral region with scattered melanocytes, being the intestine visible by transparency. Spiracle with scattered spots on its base and vent tube unpigmented. Jaw sheaths dark brown. Ventral fin transparent and unpigmented. Dorsal fin mostly transparent with melanocytes covering irregularly some blood vessel, giving a thin brownish reticulated pattern. Caudal musculature brownish, less pigmented toward the ventral region, being totally unpigmented in the ventral quarter of it. Dorsal region of the caudal musculature with seven to eight irregular whitish stripes (attributable to the absence of melanocytes), which are more evident in dorsal view. DISCUSSION Tadpoles of R. azarai are similar to those of most Rhinella species (and those of most bufonid larvae), having a small, globose and dark body, with a medium-sized tail (Altig and McDiarmid, 1999b). Additionally, morphological similarities within Rhinella margaritifera (Menin et al., 2006) and R. marina (Tolledo and Toledo, 2010) species groups have been identified previously. It is also the case for the R. granulosa species group, FIG. 1. Tadpole of Rhinella azarai, stage 35, LGE (A) Dorsal view. (B) Lateral view. (C) Ventral view. (D) Oral disc. Scale bars = 1mm (A, B), and = 0.25 mm (C). PEO = pineal end organ. where we did not find any clear diagnostic feature to distinguish the tadpole of R. azarai from the other species in the group. In addition to morphology that overlaps other Rhinella tadpoles, those of the R. granulosa group have a distinctive combination of characters. The pattern of white unpigmented bands on the dorsum of the caudal musculature in the tadpole of R. azarai has also been reported for most tadpoles of the R. granulosa group (with the exception of R. major, and R. merianae, and polymorphic in R. humboldti), as opposed to the uniform pigmentation in the remainder species of Rhinella (the only exception is Rhinella chrysophora, with fewer and greatly expanded bands, and extended through most or all the lateral region of the caudal musculature; McCranie et al., 1989: fig. 2). The pattern of white bands is a putative synapomorphy of the R. granulosa group or an internal clade. Another typical character state of this group is the absence of submarginal papillae in the oral disc, which are present only in some individuals of R. fernandezae and R. major. This type of papillae is also absent from five of the six known species of the R. margaritifera species group (present only in R. margaritifera), whereas they are present in all the described tadpoles of Rhinella crucifer, Rhinella marina (polymorphic in R. marina), Rhinella spinulosa, and Rhinella veraguensis species groups. Although not all the species have been examined for the character (Table 1), the absence of submarginal papillae could be considered a putative synapomorphy of R. granulosa species group. This hypothesis could be tested in the future when data for the remaining species became available. The absence of this type of papillae occurs also in five of the six known tadpoles species of the R. margaritifera group. A comment must be made with respect to the presence of submarginal papillae in R. margaritifera and Rhinella scitula. Duellman (1978) is not clear about the presence of submarginal papillae in R. margaritifera, and no figure of the oral disc is presented in that paper. Caldwell (1991) describes the submarginal papillae as present in R. margaritifera, as did Duellman (2005). Subsequently, Menin et al. (2006) considered submarginal papillae absent in R. margaritifera

4 TADPOLE OF RHINELLA AZARAI 437 TABLE 2. Mean measurements, standard deviations, and range (in millimeters) of 10 Rhinella azarai tadpoles in Stages 35 of Gosner (1960), LGE Characteristic Mean 6 SD Range Total length (TL) Body length (BL) Body maximum width (BMW) Body width at nostrils (BWN) Body width at eye level (BWE) Body maximum height (BMH) Tail length (TAL) Maximum tail height (MTH) Dorsal fin height (DFH) Ventral fin height (VFH) Tail muscle height (TMH) Internarial distance (IND) Extra nasal distance (EN) Interorbital distance (IOD) Intraocular distance (IO) Eye diameter (E) Nostril major axis (N) Eye nostril distance (END) Fronto nasal distance (FN) Rostro spiracular distance (RSD) Oral disc width (OD) Dorsal gap length (DG) Ventral gap length (VG) following Duellman (1978, 2005). However, Duellman (2005) clearly states that submarginal papillae are present, and we interpret the condition reported by Menin et al. (2006) as a misinterpretation of these works. On these grounds, we consider the submarginal papillae as present in R. margaritifera. Menin et al. (2006), following Caramaschi and Niemeyer (2003), report that the submarginal papillae are present in R. scitula. However, Caramaschi and Niemeyer (2003) describe only biserial labial papillae on lateral side of oral disc, and one series on the posterior region of it, with no reference to submarginal, intramarginal or internal papillae. Although their illustration is not detailed enough to unequivocally diagnose this character, the submarginal papillae are apparently absent. Thus, we consider this kind of papillae to be tentatively absent in R. scitula, although pending confirmation. When the taxonomic distribution of the absence/presence of submarginal papillae are optimized in current phylogenetic hypotheses of Rhinella (Pramuk, 2006; van Bocxlaer et al., 2010), the absence of submarginal papillae is a putative synapomorphy of the R. margaritifera species group or a subgroup of it. The LTRF is variable among species of the R. granulosa group: R. merianae, R. major, R. granulosa, and R. humboldti have the most common formula of Rhinella (i.e., 2[2]/3), whereas R. azarai, R. dorbignyi, R. fernandezae, and R. pygmaea have only two posterior rows, 2(2)/2. In R. granulosa and R. humboldti a medial flap bearing the P3 were reported, although it has been described poorly (Kenny, 1969; Mercês et al., 2009). This structure was not reported in other bufonids, and a detailed characterization of this medial flap is necessary to properly compare it with similar modifications in the last keratodonts row present in others anurans (e.g., labial arm of some Scinax; McDiarmid and Altig, 1990). The absence of P3 and the presence of a medial flap are both putative synapomorphies that may indicate a closer phylogenetic relationship between the species having these character states. Even though the larval morphology of the species of R. granulosa group does not present characters that permit unequivocal differentiation between species, it shows interesting variability at a supraspecific level. As a phylogenetic hypothesis for the group becomes available, it would be possible to better interpret the patterns of morphological diversity reported here. In the same way, oral morphology of tadpoles of the genus Rhinella shows interesting variation that may prove to be synapomorphies of some groups, and the inclusion of this source of evidence in future phylogenetic analyses would improve our understanding of the evolution of these features. Acknowledgments. We are grateful to M. F. Vera Candioti who kindly prepared the illustrations. We thank J. Faivovich and M. F. Vera Candioti for critical comments on the manuscript; and E. Krauczuk, J. Ver on, M. D Oria, M. Baleani, and P. Quiroga for field assistance. 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