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Taxonomic Review of Allobates (Anura, Aromobatidae) from the Atlantic Forest, Brazil

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Taxonomic Review of Allobates (Anura, Aromobatidae) from the Atlantic Forest, Brazil Journal of Herpetology, Vol. 41, No. 4, pp. 566–580, 2007 Copyright 2007 Society for the Study of Amphibians and Reptiles Taxonomic Review of Allobates (Anura, Aromobatidae) from the Atlantic Forest, Brazil 1 VANESSA K. VERDADE AND MIGUEL T. RODRIGUES Departamento de Zoologia, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Caixa Postal 11461, CEP 05422–970, Sa˜o Paulo, Brazil ABSTRACT.—We present the results of a taxonomic review of the four species of Allobates endemic to the Atlantic Forest Domain in Brazil. A total of 880 preserved specimens from 29 localities covering their range in Atlantic Forest were studied based on external attributes. Characters formerly described as diagnostic in original descriptions and others cited for dendrobatids in the literature were studied along the total geographic range of the populations of these species, including the type localities. We found no discrete characters, qualitative or quantitative, capable of differentiating the species. Most local and geographic variation was limited to snout-vent length and color pattern. Considering the lack of evidence otherwise, we use the results of our morphological analysis to allocate all Atlantic Forest species of Allobates to synonymy with Allobates olfersioides. Dendrobatids are a monophyletic group of Allobates olfersioides was described as Eupem- frogs that are mostly known for their bright phix olfersioides Lutz, 1925 from the coastal color and poisonous skin. Nevertheless, about region of the state of Rio de Janeiro (RJ). half of the species are cryptically and dull Cochran (1955) considered it a synonym of colored, presumably nontoxic and until recently Phyllobates brunneus Cope, 1887. Bokermann (Grant et al., 2006) placed in the genus Colos- (1966) restricted the type locality of A. olfer- tethus sensu lato. There had been about a hun- sioides to Angra dos Reis (RJ) and, in 1967, dred recognized species in the genus ranging described the other three Atlantic Forest species: from Nicaragua to southeastern Brazil (Frost, Phyllobates alagoanus from Usina Sinimbu, Man- 2006). The systematics of the family has recently gabeiras, state of Alagoas; Phyllobates capixaba gone through significant changes (Grant et al., from Lagoa do Macuco, Refu´gio Sooretama, 2006) supported by a molecular and morpho- Linhares, state of Espı´rito Santo; and Phyllobates logical based phylogeny. The family Dendroba- carioca from Represa Rio Grande, Jacarepagua´, tidae, as previously known, corresponds now to Rio de Janeiro, state of Rio de Janeiro. Boker- Dendrobatoidea, which includes the families mann (1967) also considered P. olfersioides re- Aromobatidae and Dendrobatidae. The four lated to P. alagoanus, P. capixaba and P. carioca. species of Colostethus from Atlantic Forest, Edwards (1974) placed these four species in now allocated to the genus Allobates, are placed Colostethus, as did Silverstone (1975). Grant et al. in the family Aromobatidae. (2006) based on an extensive sampling and The Brazilian species of Allobates are leaf litter molecular plus morphological based phylogeny inhabitants of forests and can be found through- allocated them to the genus Allobates. out the Amazon Basin, Brazilian Savannas, and The four species are very similar in external Atlantic Forest. Most of the 17 currently attributes and were described based on small recognized species are Amazonian and de- and geographically remote samples. The char- scribed recently, probably as a consequence of acters used by Bokermann (1967) to separate a vast and poorly sampled territory along with these species were basically color pattern, increased knowledge of the natural history of length of limbs and fingers, size of carpal and these frogs (e.g., Morales, 2000; Lima and tarsal tubercles, shape of head, and snout-vent Caldwell, 2001; Caldwell and Lima, 2003). There length. All of these characters are presumably are four species in eastern Brazil, endemic to the subject to geographical variation, a possibility that could not be tested at that time. Atlantic Forest Domain (Ab’Saber, 1977): Allo- bates alagoanus (Bokermann, 1967), Allobates Bokermann (1967) also presented information on call variation, pointing out that the calls of A. capixaba (Bokermann, 1967), Allobates carioca capixaba and A. carioca were distinct from that of (Bokermann, 1967), and Allobates olfersioides A. olfersioides, but, except for saying that the call (Lutz, 1925). of A. capixaba was more spaced than those of A. olfersioides, no further description was given. 1 Corresponding Author. E–mail: [email protected] Besides, the putative call differences between TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST 567 species were reported by the collector (F. M. Oliveira) and not based on the authors’ field experiences or knowledge. The main character- istics of the advertisement call of Allobates (a trill or an acute buzz) can vary in fundamental frequency, number of pulses and spacing, according to environmental conditions and sometimes, as a function of population density (Coloma, 1995; Junca´, 1998; Grant and Rodri- guez, 2001; Caldwell et al., 2002a). Considering the subjective call differences reported and their variation, we think that the evidence alone is weak to keep the Atlantic Forest species of Allobates separated. Moreover, the observations on vocalization pointed out in the species description refer only to the surroundings of the type locality, and geographical variation of call should be considered. Unfortunately, we were unable to find available calling records in collections, either institutional or personal, and our attempts to get new ones failed. Because this problem will probably persist in the future, FIG. 1. Geographic distribution of Atlantic Forest because the Atlantic Forest species of Allobates Allobates. Open circles represent the type localities of are showing declines (Weygoldt, 1989; Izeck- the four currently admitted species. Numbers are the sohn and Carvalho-e-Silva, 2001), specimens localities sampled (see Appendix 2). The OTUs gathered in collections will be the main source studied are indicated by OTU1, 2, 3, and 4. for studying species limits of this complex in the Atlantic Forest. Indeed, the samples collected (TIL) from the outer edge of the flexed knee to during the last 40 years are a source of new data the heel; foot length (FOL) from the heel to the on morphological variation that could clarify tip of toe IV; head width (HW) between the the similarities and differences among the four angle of jaws; head length (HL) perpendicular species of Allobates from Atlantic Forest. to the imaginary line linking the angle of jaws to We present, herein, a detailed study of the the tip of the snout; internarial distance (IND) morphological variation of these populations between the inner edge of the nares; eye-nostril along a latitudinal gradient that includes the distance (END) from the anterior corner of the type localities of the presently recognized eye to the outer edge of the nostril; eye diameter species. We assume that external morphology (ED) from posterior to anterior corners; tympa- is the strongest available source of data sustain- num diameter (TD) from posterior to anterior ing the Atlantic Forest species of Allobates, and, edges; interorbital distance (IOD) between the if we found no discrete differences in morpho- inner edges of the eyelids; hand length (HAL) logical characters among populations, they dorsally from the junction of radio-ulna and should be considered synonyms until new carpal to the tip of the finger III; thumb length sources of data can be explored. (TBL); second, third, and fourth fingers length (FL2, FL3, FL4) dorsally from the base to the tip of the finger; third finger diameter (TFD) MATERIALS AND METHODS dorsally at the distal edge of the second finger To cover their total range, 880 preserved tubercle; greatest length of the inner and outer specimens of Allobates from 29 localities were carpal tubercles (ICT, OCT); and greatest length studied (Fig. 1, Appendices 1 and 2). All speci- of the inner and outer metatarsal tubercles mens were observed regarding external mor- (IMT, OMT). phology. We measured and classified 396 All measurements were taken on the left side individuals to be used in the statistical analysis. of the specimens. The measurements were This number comprises all individuals from obtained with a stereomicroscope except for localities with N below 100 and 100 randomly SVL, taken by a dial caliper, to the nearest of picked up individuals from localities with N 0.01 mm. The axis of the greatest length at ICT, above 100. Twenty-two measurements were OCT, IMT, and OMT variables was the same for obtained for the specimens included in the all specimens. analysis: snout-vent length (SVL); thigh length Qualitative characters studied were: shape of (THL) from the middle of the cloacal opening to the snout (dorsal, ventral, and lateral views); the outer edge of the flexed knee; tibia length pattern of the lateral dark stripe between the 568 V. K. VERDADE AND M. T. RODRIGUES Estadual de Sa˜o Paulo, UNESP); MNRJ (Museu Nacional do Rio de Janeiro); MUFAL (Museu da Universidade Federal de Alagoas); MZUSP (Museu de Zoologia da Universidade de Sa˜o Paulo, currently including the Werner Boker- mann collection, WCAB); UEFS (Universidade Estadual de Feira de Santana); UFPB (Universi- dade Federal da Paraı´ba); UFRJ (Universidade Federal do Rio de Janeiro); USNM (United States National Museum); ZUEC (Museu de Histo´ria Natural, Universidade de
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