Taxonomic Revision of Rhinella Granulosa Species Group (Amphibia, Anura, Bufonidae), with a Description of a New Species
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Volume 40(1):1‑73, 2009 Taxonomic revision of RHINELLA GRANULOSA species group (Amphibia, Anura, Bufonidae), with a description of a new species Patrícia Narvaes1,2 Miguel Trefaut Rodrigues1,3 AbstRACT An extensive review of Rhinella granulosa species group was conducted based on external morphological and morphometrical characteristics. Data set included 8700 specimens deposited in 35 collections, representing 865 localities, from South and Central America. Twelve species were recognized for the group, one described as new; they are: Rhinella granulosa (Northeastern Brazil), R. pygmaea (Rio de Janeiro State, Brazil), R. bergi (Paraguay, Northwestern Argentina, and Mato Grosso State, Brazil), R. major (Argentina, Bolivia, Paraguay, and North and Western Brazil), R. mirandaribeiroi (Central Brazil and Bolivia), R. azarai (Provincia de Misiones, Argentina, Paraguay, and Mato Grosso do Sul State, Brazil), R. nattereri (Venezuela, Guiana, Roraima State, Brazil), R. fernandezae (Argentina, Uruguay, Paraguay, and Rio Grande do Sul State, Brazil), R. dorbignyi (Provincia de Buenos Aires, Argentina, Uruguay, and Rio Grande do Sul State, Brazil), R. merianae (Venezuela, Surinam, Guiana, and Brazilian States of Amazonas and Roraima), R. humboldti (Colombia, Venezuela, Surinam, Guiana, Trinidad), R. centralis sp. n. (Panama). External morphological characters, such as head and snout shape, type of cephalic crests, size of tympanum, size and shape of parotoid gland, and skin granulation, are some of the traits used to identify the species. For each species, comparative diagnosis, description, and summaries of distribution are provided. An artificial key to species is also presented. The geographic distributions of species of Rhinella are largely associated with the open habitats of South America and Panama. Keywords: Bufonidae; Rhinella granulosa group; Taxonomic revision; Geographic distribution; South and Central America. INTRODUCTION terized by having a small parotoid gland, wart skin, and well-developed and keratinized cranial crests. Rhinella granulosa group assembles common, The first two species of the group were described moderate-sized, and wide-ranging South American in the 19th century: Rhinella granulosa (Spix, 1824) toads, occurring also in Panama. Species are charac- from Bahia, Brazil, and Rhinella dorbignyi (Duméril & 1. Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, 05422-970, São Paulo, SP, Brasil. 2. E-mail: [email protected] 3. E-mail: [email protected] 2 Narvaes, P. & Rodrigues, M.T.: Taxonomic revision of RHINELLA GRANULOSA species group Bibron, 1841), from Montevideo, Uruguay. In subse- distributions are provided for all recognized taxa, in- quent years, these names were randomly used on the cluding a description of a new species. The geographic attempt to identify specimens found between the type distribution of the species is discussed hereinafter. localities of the two species (Gallardo, 1957). In 1936, Müller & Hellmich described a subspecies for Rhinella granulosa (Rhinella granulosa major) from San José de MATERIAL AND METHODS Chiquitos, Bolivia. Rhinella pygmaea was described by Myers & Carvalho in 1952, from Rio de Janeiro, Brazil, External morphology and another subspecies (Rhinella granulosa fernandezae) was described by Gallardo in 1957 from Argentina. Up to 8700 specimens deposited in 35 collec- Distribution and taxonomy of the forms of tions were studied representing 865 localities in South the group were first assigned by Gallardo (1965), and Central America. Specimens examined are in Ap- who recognized 14 subspecies of Rhinella granu- pendix 1. The following external morphological char- losa (R. g. major, R. g. fernandezae, R. g. dorbignyi, acters were examined. R. g. granulosa, R. g. pygmaea, R. g. azarai, R. g. beebei, R. g. humboldti, R. g. merianae, R. g. mirandaribeiroi, R. g. mini, R. g. lutzi, R. g. goeldii, and R. g. barbouri). Head shape The author presented a hypothesis to explain the dis- tribution of the subspecies based on their fidelity to Three categories of head shape were recognized the South American hydrographic systems. After his in dorsal view: rounded (Fig. 1A), elongated (Fig. 1B) work, two other forms were described for the group: or subtriangular (Fig. 1C). The rounded head is semi- Rhinella granulosa nattereri (Bokermann, 1967), and circular with a short snout (tip of snout not surpass- Rhinella bergi (Cespedez, 2002). A few of the subspe- ing anterior margin of maxilla in ventral and dorsal cies (Rhinella fernandezae, Rhinella dorbignyi, Rhinella views (Figs. 2A and 2C), or with a slightly protruding pygmaea) were elevated to specific rank by Cei (1968, snout. The head shape exhibited in Fig. 2D occur in 1972), a decision followed by other authors (Acha- only one species of the group and it is also considered val & Olmos, 1997; Carvalho e Silva & Carvalho e in the rounded category; although it is not perfectly Silva, 1994; Duellman, 1999; Langone, 1999; Lavilla rounded in profile due to the presence of a long snout; et al., 1992; Maneyro et al., 1995). In 1986, Rivero nevertheless, the circumference of the head is consid- et al. considered Rhinella beebei a valid species based erably perceptible. The subtriangular head is wide on information available in the literature and on in- with a long snout (Fig. 2F). The elongated head is dications of sympatry among the subspecies described narrow with a long snout (Fig. 2E). by Gallardo. Besides the absence of a thoroughly revi- sion, this decision was followed by Frost (2008), who recognized six species for the group (Rhinella granu- Snout shape losa, Rhinella dorbignyi, Rhinella fernandezae, Rhinella pygmaea, Rhinella bergi, and Rhinella beebei). In dorsal view, the snout can be rounded or Nevertheless, the diagnosis and descriptions squared (Fig. 2D); in lateral view, it can be rounded made available by Gallardo and subsequent authors (Figs. 3A and 3C) or straight (Figs. 3D and 3F). In were inadequate to recognize taxonomic variation in lateral and dorsal view, the snout can be short (tip the group, and Rhinella granulosa remain as a conve- of snout not surpassing anterior margin of maxilla nience name for this complex. The amount of mate- or surpassing it only slightly); or long (tip of snout rial accumulated in collections over the past 40 years highly surpassing anterior margin of maxilla). provides a new perspective in this scenario, allowing an extensive taxonomic revision of the group, stated as needed by several authors (Klappenbach & Langone, Dorsal body granulation 1992; Langone, 1994; Prigioni & Achaval, 1992). The purpose of this study is to provide, based on Dorsal granulation can vary in intensity but museum specimens, an analysis of geographic variation tubercles are always keratinized, partially or totally. of the forms of Rhinella granulosa species group in South Tubercles can be conical, rounded or elongated; flat- and Central America and to determine their taxonomic tened or fleshy. Pungent conical tubercles can be al- status. Detailed diagnoses and descriptions, an artifi- most entirely keratinized or have one to several kera- cial key to identification, and a summary of the known tinized spicules. Arquivos de Zoologia, 40(1), 2009 Head granulation Cephalic crests Skin is always smooth; when present, keratin- All species of R. granulosa group present cephal- ized granules, spicules or flecks are always spaced out, ic crests with keratinized borders. Regarding height, leaving portions of smooth skin visible between them. crests can be high or low. In high crests, borders are A few species present a more intense granulation on usually continuous (Figs. 2A and 2C); in low crests, top of head (Fig. 2D) than others, where granulation they are usually discontinuous, granulose (Figs. 2D is more spaced (Figs. 2C and 2F). Keratinization cov- and 2F). In some cases, crests with continuous borders ering tubercles, granules, and crests may fade after may present gaps (Fig. 2B); and crests with granulose long periods of storage and manipulation. borders may present a few united granules (Fig. 2E). Cephalic crests may be bulky (Fig. 2C). The following categories of cephalic crests were Color pattern recognized: Dorsal colors vary from dark-brown to light ol- Supraorbital crest ive-green, with dark spots. In dark-brown patterns, spots are nonexistent or not conspicuous. A labial Supraorbital crest is situated dorsally to eye, stripe, lightly colored or spotted, may be present be- between canthal and supratympanic crests. It can be tween upper maxilla and infraorbital crest, visible or straight, forming a continuous straight line with can- not in dorsal view. thal and supra tympanic crests (Fig. 2C) or, as in most cases, rounded (Fig. 2E). Compared to other cephalic crests, supraorbital crest presents the highest varia- Longitudinal dorsal stripe tion related to height (high or low), thickness (thin or bulky), and type of keratinization (continuous or A mid-dorsal longitudinal stripe, white, yellow granular). When high and continuous, it can be later- or lighter than the dorsal color pattern, extending ally and posteriorly wrinkled, and gapped or serrate from nostril or eye level to end of body, can be pres- at the top (Fig. 2B). When granular, the granules can ent (Figs. 2B, 2C and 2E) or absent. When present, it be well individualized or partially united. Interorbital is better visualized if observed through the glass of a portion of supraorbital crest can be strongly