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Article

ZOOTAXA
ISSN 1175-5334 (online edition)

urn:lsid:zoobank.org:pub:BC6CB247-BCCA-49FD-A014-E3A5FDB366DC

A new dwarf species of Proceratophrys Miranda-Ribeiro, 1920 (Anura, Cycloramphidae) from the highlands of Chapada Diamantina, Bahia, Brazil
MAURO TEIXEIRA JUNIOR1,2, RENATA CECLIA AMARO1, RENATO SOUSA RECODER1, FRANCISCO DAL VECHIO1 & MIGUEL TREFAUT RODRIGUES1
1

Laboratrio de Herpetologia, Departamento de Zoologia, Instituto de Biocincias, Rua do Mato, no 101, CEP 05508-090, Universidade de So Paulo, So Paulo, Brazil 2 Corresponding author. E-mail: tropidurus@gmail.com

Abstract
A new species of Proceratophrys is described from the highlands of northeastern Brazil. Molecular and morphological data suggests that Proceratophrys redacta sp. nov. is sister to P. minuta, and related to P. schirchi and P. cristiceps. The new species is diagnosed by its small size, absence of rostral and palpebral appendages, sagittal ridges interrupted, absence of postocular swellings, snout vertical in profile and dorsal coloration lacking distinct ocelli. The new species represents another example of endemism for the genus Proceratophrys in Chapada Diamantina region, and of another appendageless small-sized species associated with highlands. The phylogenetic results indicate that current morphological groupings in Proceratophrys may not represent natural groups. Key words: Proceratophrys redacta sp. nov., mountain endemism, frog diversity

Introduction
After his travel through the Brazilian coast, the German naturalist Alexander Phillip Maximilian, Prinz zu WiedNeuwied (see Myers et al. 2011), described the horned frog, Ceratophrys boiei (Wied 1824), which underwent taxonomic rearrangement (Gravenhorst (1825; 1829), ending up to be the first described species in the currently recognized genus Proceratophrys. After that several species were described (Peters 1872; Gnther 1873; Mller 1883; Miranda-Ribeiro 1920; 1926; 1937; Jim & Caramaschi 1980; Izecksohn & Peixoto 1981; Weygoldt & Peixoto 1985; Giaretta & Sazima 1993; Mercadal de Barrio & Barrio 1993; Eterovick & Sazima, 1998; Izecsohn et al. 1999; Giaretta et al. 2000; Kwet & Faivovich 2001; Cruz et al. 2005; Prado & Pombal 2008; Cruz & Napoli 2010; Frost 2011; Martins & Giaretta 2011; Napoli et al. 2011; Cruz et al. 2012) and its taxonomy rearranged (Lynch 1971; Prado & Pombal 2008; Amaro et al. 2009). Currently the genus comprises 27 species of small to medium/large-sized frogs, occurring in forests, savannas, grasslands and shrubby lands of eastern, central and southern South America, in Brazil, Argentina and Paraguay (Prado & Pombal 2008; Frost 2011; Martins & Giaretta 2011; Napoli et al. 2011). However, its present richness is likely underestimated, as indicated by the constant discovery of new species (Prado & Pombal 2008; vila et al. 2011; Martins & Giaretta 2011; Napoli et al. 2011; Cruz et al. 2012). Furthermore, preliminary molecular phylogenies are showing that species formerly attributed to Odontophrynus, are indeed members of Proceratophrys (Amaro et al. 2009). Recently, a dwarf species of Proceratophrys (P. minuta Napoli, Cruz, Abreu & Del Grande 2011) was described from the highlands of Chapada Diamantina, at the northern portion of Espinhao range in state of Bahia (Napoli et al. 2011). This small-sized highland species seems to be restricted to the cloud forest patches of high elevations (above 800 m a.s.l., being very common at about 1170 m a.s.l.). Based on similarities in external morphology this new species was supposed to be allied to P. schirchi, (Napoli et al. 2011). Both P. schirchi and P. minuta are not currently assigned to any species group, as well as P. rondonae, however the remaining species have been informally assigned to three or four species groups, based on overall
Accepted by M. Vences: 10 Oct. 2012; published: 16 Nov. 2012

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morphological similarity. The P. boiei species complex, characterized by a single and long uni-cuspidate palpebral appendage and lack of a triangular rostral appendage, is thought to include P. boiei (Wied, 1824); P. paviotii Cruz, Prado and Izecksohn, 2005; and P. renalis (Miranda-Ribeiro, 1920). The P. appendiculata species complex, sometimes referred to as a subset of P. boiei group, also with a single and long uni-cuspidate palpebral appendage, additionally characterized by the presence of a triangular rostral appendage: P. appendiculata (Gnther, 1873); P. laticeps Izecksohn and Peixoto, 1981; P. melanopogon (Miranda- Ribeiro, 1926), P. moehringi Weygoldt and Peixoto, 1985; P. phyllostomus Izecksohn, Cruz and Peixoto, 1998; P. sanctaritae Cruz and Napoli, 2010; P. subguttata Izecksohn, Cruz and Peixoto,1998; and P. tupinamba Prado and Pombal, 2008. Four species have been associated to the P. bigibbosa group, characterized by the presence of postocular swellings (Kwet & Faivovich 2001): P. avelinoi Mercadal de Barrio & Barrio, 1993; P. bigibbosa (Peters, 1872); P. brauni Kwet & Faivovich, 2001; and P. palustris Giaretta & Sazima, 1993. Finally, eight species have been associated with the P. cristiceps group, which gathers species lacking both prominent supraocular appendages and postocular swellings, but does not have any recognized shared derived characters (Giaretta et al. 2000): P. aridus Cruz, Nunes and Junca, 2012; P. caramaschi Cruz, Nunes and Junca, 2012: P. cristiceps (Mller, 1883); P. concavitympanum Giaretta, Bernarde & Kokubum, 2000; P. cururu Eterovick & Sazima, 1998; P. goyana (Miranda-Ribeiro, 1937); P. moratoi (Jim and Caramaschi, 1980); P. strussmannae vila, Kawashita-Ribeiro & Morais, 2011; and P. vielliardi Martins & Giaretta, 2011. Herein, based on a series of specimens recently collected at the highlands of northern Chapada Diamantina, at Morro do Chapu municipality, we describe a new dwarf species of Proceratophrys providing data on its natural history, its phylogenetic placement, as well as those for P. minuta, discussing the evolution of body shape and the validity of the recognized species groups within Proceratophrys.

Material and methods

Field sampling. Fieldwork was carried out during the rainy season, from 22nd December 2011 to 2nd January 2012, at Morro do Chapu municipality. Ten pitfall traps with drift fences were installed at a plain sandy Caatinga, and 25 others at a montane forest at the slopes of Morro do Chapu hill. Unquantified active search was also performed at the surrounding areas and at Ferro Doido waterfall. Collected specimens were killed with lethal doses of anesthesics, fixed in 10% formalin, preserved in 70% alcohol and housed at the herpetological collection of Museu de Zoologia da Universidade de So Paulo, So Paulo, Brazil. Morphological assessment. Morphological comparisons were based on voucher specimens housed at the herpetological collection of the Museu de Zoologia da Universidade de So Paulo (MZUSP) and specimens collected by the Laboratrio de Herpetologia, Instituto de Biocincias da Universidade de So Paulo (MTR) (Appendix I), and data available in the literature (Giaretta & Sazima 1993; Mercadal de Barrio & Barrio 1993; Eterovick & Sazima 1998; Giaretta et al. 2000; Kwet & Faivovich 2001; Cruz et al. 2005; Prado & Pombal 2008; Cruz & Napoli 2010; Santana et al. 2010; vila et al. 2011; Martins & Giaretta 2011; Napoli et al. 2011; Cruz et al. 2012). Diagnostic features and morphological descriptions follow Prado and Pombal (2008) and Napoli et al. (2011). Measurements were taken using a digital caliper to the nearest 0.01 mm and rounded to the first decimal unit to avoid pseudoprecision (Hayek et al. 2001). Twelve morphometric measurements were taken following Heyer et al. (1990) and Prado and Pombal (2008): snout-vent length (SVL); head length (HL); head width (HW); eye diameter (ED); eye to nostril distance (END); upper eyelid width (UEW); interorbital distance (IOD); internostril distance (IND); thigh length (THL); tibia length (TL); foot plus tarsus length (FTL); and hand length (HAL). All individuals were measured, as all were consider adults: males with vocal slits and females with vitelogenic eggs visible though skin. Moreover individuals were found in amplexus, attesting for their maturity. Geographical distribution. The geographical distribution of Proceratophrys was assessed, to present the distribution of the new species in the genus context and to add some data to the discussion on validity of some species. For this purpose records were compiled, mostly from literature (Miranda-Ribeiro 1955; Jim & Caramaschi 1980; Giaretta & Sazima 1993; Mercadal de Barrio & Barrio 1993; Rossa-Feres & Jim 1996; Caramaschi & Velosa 1997; Eterovick & Sazima 1998; Machado et al. 1999; Giaretta et al. 2000; Brando & Araujo 2001; Giasson et al. 2001; Kwet & Faivovich 2001; Boquimpani-Freitas et al. 2002; de S & Langone 2002; Lavilla et al. 2002; Kwet & Baldo 2003; Silvano & Pimenta 2003; Hiert & Moura 2004; Pimenta & Carvalho-e-Silva 2004; Cruz et al. 2005;

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Brusquetti & Lavilla 2006; Leite et al. 2006; Cacciali et al. 2007; Vieira et al. 2007; de Lima 2007; Zanella & Busin 2007; Brasileiro et al. 2008; Gonsales 2008; Lucas & Foster 2008; Prado & Pombal 2008; Vieira et al. 2008; Amaro et al. 2009; Cintra et al. 2009; Oda et al. 2009; Santos et al. 2009; Caldart et al. 2010; Carosini et al. 2010; Carvalho et al. 2010; Cruz & Napoli 2010; Fatorelli et al. 2010; Rolim et al. 2010; Santana et al. 2010; vila et al. 2011; Barros et al. 2011; Maffei et al. 2011; Martins & Giaretta 2011; Napoli et al. 2011; Valdujo et al. 2011; Bernardo et al. 2012; Brando et al. 2012; Cruz et al. 2012; Mangia et al. 2012), and from examined specimens (Appendix I). Molecular data. Partial sequences of two mitochondrial (16S and cyt b) and one nuclear (Rag-1) genes of two individuals from the new species, and two individuals of Proceratophrys minuta were obtained (Appendix II) and added in a matrix including Proceratophrys appendiculata, P. avelinoi, P. bigibbosa, P. boiei, P. concavitympanum, P. cristiceps, P. cururu, P. goyana, P. laticeps, P. melanopogon, P. moratoi, P. renalis, P. schirchi, Odontophrynus americanus, O. carvalhoi, O. cultripes, Macrogenioglottus alipioi, Cycloramphus acangatan and Thoropa taophora from Amaro et al. (2009). Total genomic DNA was extracted from liver and muscle according to Fetzner (1999) and amplification was carried using standard PCR protocols with primers 16SAR and 16SBR (Palumbi 1996) for amplification of 16S, primers CB1 and CB3 for cyt b (Palumbi 1996) and primers R1GFF and R1GFR (Faivovich et al. 2005) for Rag-1. The PCR cycle protocol consisted of one initial cycle of 94 C for 5 min followed by 35 cycles of 94 C for 40 sec, 48 C for 40 sec, 72 C for 40 sec and the products were directly purified with Exonuclease I and Shrimp Alkaline Phosphatase (USB or Fermentas). Automated sequencing was carried out using BigDye Terminator v3.1 Cycle Sequencing kit (Applied Biosystems), followed by analysis on ABI Prism 310, 3700 or 3170 Genetic Analyzer Sequencers (Applied Biosystems) according to the manufacturers instructions. Sequences were edited and initially aligned in CodonCode Aligner (CodonCode Corporation). The three data sets were combined in a matrix of 1558 bp (536 bp form 16S, 594 bp from cyt b and 428 bp from Rag-1) and different modes of inference were used in phylogenetic analyses: Bayesian analysis (BA) implemented in MrBayes 3.0b4 (Ronquist & Huelsenbeck 2003) and Maximum Likelihood (ML) in Treefinder (Jobb 2008). Some heterozygous sites were found for Rag-1 and were treated as ambiguities. Two independent Bayesian analyses were performed for each partition, with a random starting tree, four incrementally heated Markov chains, and 10,000,000 generations, with trees sampled every 1000 generations to estimate likelihood and sequence evolution parameters. For Bayesian analyses, the best-fit model of nucleotide substitution for each data partition was selected using the Akaike information criterion (AIC) and we used a separate model for each gene (GTR+I+G for 16S; HKY+I+G for cyt b ; HKY+G for Rag-1). Stationarity for each run was detected by plotting the likelihood scores of the trees against generation time, and the topology, posterior probability values, and branch lengths inferences were estimated after discarding 25% of the initial trees of each run as burn-in samples. Nodes with posterior probability 95% on a 50% majority rule consensus tree from both runs were considered significant support for a given clade. Maximum likelihood (ML) bootstrapping (1000 replicates) was performed in Treefinder (Jobb 2008) using default settings and models GTR + G for cyt b and 16S and HKY + G for RAG-1 (models were also estimated in Treefinder). The majority 50% consensus trees saved with posterior probabilities and bootstrap values on the nodes were visualized using FigTree 1.3.1 (http://tree.bio.ed.ac.uk/). Uncorrected genetic distances (p distances) were calculated using PAUP* 4.0b10 (Swofford 2003).

Results Proceratophrys redacta sp. nov. (Figs. 13)

Holotype. MZUSP 150266, an adult male, field number MTR 22579, collected at Morro do Chapu hill, Morro do Chapu municipality, Bahia, Brazil (1135'26.02"S, 4112'32.87"W, 1254 m a.s.l. datum WGS-84), by M. Teixeira Jr, F. Dal Vechio, I. Prates, R. P. Damasceno and M. T. Rodrigues, on 30th December 2011. Paratopotypes. MZUSP 150263, 150264, 150265, 150268, 150269, adult males, field numbers MTR 22474, 22554, 22564, 22582, 22583; MZUSP 150267, adult female, field number MTR 22580. Collected between 27th and 30th December 2011.

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Paratypes. MZUSP 150272, an adult male, field number MTR 22628; MZUSP 150270, 150271, 150273 adult females, field numbers MTR 22623, MTR 22626, MTR 22629. All from an old road (1133'58.3"S, 4107'32.3"W, 929 m a.s.l., datum SAD69), at Morro do Chapu municipality, close to city town. Collected between 31st December 2011 and 2nd January 2012.

FIGURE 1. Proceratophrys redacta sp. nov. holotype (MZUSP 150266) in dorsal (left) and ventral (right) views (21.9 mm in SVL, male)

Diagnosis. A Proceratophrys species (nuptial pads absent, enlarged glands absent, fingers webbing absent, supernumerary tubercles on hands and feet present, dorsal surfaces of fingers and toes wrinkled, and dorsum with sinuous longitudinal ridges outlining a spear-shaped ornamentation) characterized by: (1) small size (26.929.7 mm of SVL in males; 33.634.9 mm of SVL in females); (2) no rostral appendage; (3) no palpebral appendage; (4) snout rounded from above and vertical in profile; (5) rostral ridge sharp, slightly curved; (6) presence of interrupted sagittal ridges of warts from eyelids to sacral region; (7) absence of postocular swellings; (8) tympanic region indistinct; (9) dorsal coloration lacking distinct dark ocelli. Comparisons with other species (data for the species in comparison are given in parenthesis). Proceratophrys redacta sp. nov. can be promptly distinguished from all species of Proceratophrys, with the exception of P. avelinoi, P. minuta, P. moratoi and P. palustris, by its smaller body size, SVL ranging from 26.929.7 mm in males, and 33.634.9 mm in females (P. appendiculata: 40.459.9 males, 33.563.2 females; P. aridus: 32.542.8 males, 43.246.3 females; P. bigibbosa: 35.543.8 males, 51.253.4 females; P. boiei: 39.861.9 males, 4074.3 females; P. brauni: 3034.6 males, 38.939.8 females; P. caramaschii: 42.756.3 males, 53.865 females; P. concavitympanum: 39.657.1 males, 53.660.3 females; P. cristiceps: 39.550.2 males, 4353.8 females; P. cururu: 36.543.1 males, 4753.9 females; P. goyana: 39.653.5 males, 54.660.0 females; P. laticeps: 59.578 males, 50.382.7 females; P. melanopogon: 34.949.9 males, 40.762.1 females; P. moehringi: 59.262.6 males, 63.6 the only female known; P. paviotti: 41.953.2 males, 50.951.8 females; P. phyllostomus: 55.4 the only male known, 40.976.6 females; P. renalis: 36.853 males, 38.571.9 females; P. rondonae: 62.9 the only male knwon; P. sanctaritae: 38.445.5 males, 60.8 female; P. schirchi: 31.640.4 males; P. strussmanae: 41.147.3 males, 52.659.8 females; P. subguttata: 36.741.8 males, 36.658.9 females; P. tupinamba. 52.663.4 males, 37.772.8 females; P. vielliardi: 39.141.9 males, 45.5 the only female known; P. redacta sp. nov. can be distinguished from P. minuta by its larger size, SVL ranging from 26.929.7 mm in males, and 33.634.9 mm in females, by having an incomplete sagittal ridge of warts extending from eyelid to sacral region, and having a row of small, rounded tubercles in the eyelid (SVL 19.225.2 mm males, 25.931.9 mm females; presence of a

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complete sagittal ridge of warts from eyelids to urostile; a row of enlarged, pointed tubercles in the eyelid is present); from P. avelinoi, P. palustris, P. brauni and P. bigibbosa, it can be distinguished by lacking postocular swellings (present) a additionally from P. avelinoi and also P. schirchi by having a row of small, rounded tubercles in the eyelid (a row of enlarged, pointed tubercles in the eyelid is present); from P. moratoi, P. palustris and P. vielliardi it can be distinguished by having the dorsal and lateral surfaces of body covered with small granules with a few scattered larger tubercles, incomplete sagittal ridge of tubercles extending from eyelid to sacral region, and dorsal coloration variable, but never with dark irregular ocelli (dorsal surfaces with many large tubercles, no sagittal ridge of tubercles and dorsal coloration with irregular ocelli). Additionally P. redacta sp. nov. can also be distinguished from P. appendiculata, P. boiei, P. laticeps, P. melanopogon, P. moehringi, P. paviotti, P. phyllostomus, P. renalis, P. rondonae, P. sanctaritae, P. subguttata, and P. tupinamba by lacking a single long horn-like palpebral appendage (present); from P. appendiculata, P. melanopogon, P. laticeps, P. phyllostomus, P. subguttata and P. tupinamba by lacking a rostral appendage (present); and from P. concavitympanum and P. strussmannae by having an indistinct tympanic region (tympanic region defined by a concave depression on the skin).

FIGURE 2. Details of the head in dorsal view (A), and profile (B), and ventral views of right hand (C) and foot (D) of the holotype (MZUSP 150266) of Proceratophrys redacta sp. nov. Scale bars correspond to 5 mm.

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Description of holotype. Body small, stout, nearly ovoid (Fig. 1); 28.3 mm in SVL. Head wider than long; head length 87% of head width. Snout rounded in dorsal view, vertical to slightly oblique in profile (Fig. 2). Upper eyelids without appendages, covered with a row of small rounded tubercles. Canthal crests distinct, loreal region slightly concave. Interocular crests absent. Interorbital distance 88% of upper eyelid width, 23.9% of head width. No oblique rows of warts on head sides. Three prominent and yellowish postrictal tubercles posteriorly to mouth commissure. Pre-ocular crests present, short and vertical. Eyes large, eye diameter 34% of head length, and 1.52 times the eye to nostril distance. Tympanum hidden. Nares prominent, nostrils elliptical, nearly horizontal in profile, diverging posteriorly in dorsal view. Tongue cordiform, free posteriorly. Vomerine teeth in two short rows between choannae. Choannae large, rounded, separated by a distance of about 2.5 times its diameter. Vocal sac single, subgular; vocal slits present, lateral to tongue on the floor of mouth. Arms short and robust; finger length IV<II<I<III. Finger tips rounded, not expanded. Fingers not webbed, bordered laterally by distinct ridges of tubercles. Nuptial pads absent in males. Inner carpal tubercle elliptical. Outer carpal tubercle bifid, ovoid with a ventral invagination inwards. Subarticular tubercles large, rectangular with rounded corners; supernumerary tubercles well defined, rounded. Outer margin of forearms with enlarged tubercles, but not forming well defined rows. Legs short and moderately robust, leg length (THL+TL) 75% of SVL, foot plus tarsus 91% of SVL. Toe lengths I<II<V<III<IV. Toe tips rounded, smooth, without expansions, bordered laterally by distinct ridges. Toes basally webbed, web formula I 01- II 12- III 1-3+ IV 3-1- V. Inner metatarsal tubercle large, globular, and semicircular. Outer metatarsal tubercle small, rounded. Subarticular tubercles large, rectangular with rounded corners; supernumerary tubercles present. Tarsal tubercles in a ventrolateral row, forming a lateral ridge on foot. Dorsal surfaces granulate with larger granules irregularly distributed in the dorsum, especially within dorsal ridges. Symmetrical sinuous longitudinal ridges of tubercles on dorsum, from posterior border of eyelids and scapulae, converging at middle of the body, and fading posteriorly, not reaching the urostile. Ventral surfaces shagreened. A pair of enlarged light tubercles below the anal region. Color in preservative. Dorsal background color light brown. Dark brown interorbital bar projecting posteriorly. Dark brown triangular areas irregularly delimited along the outer margins of the dorsal sagittal crests projecting posteriorly over scapulae, curving inwards, reaching sacrum region. A small chevron medially located at the dorsum. Irregular dark brown markings distributed over the dorsum and along flanks. Limbs with transverse dark brown bars. Ventrally, ground color yellowish-brown; darker brown on palms, soles, anal region and throat. Three oblique dark brown stripes on sides of head, accompanying ridges of tubercles, and two less defined on snout to lips. Upper lip cream. Measurements of holotype (in mm). SVL 28.3; HL 11.0; HW 12.6; ED 3.8; END 2.5; UEW 3.4; IOD 3.0; IND 2.1; THL 11.4; TL 9.9; FTL 15.9; HAL 12.4. Variation. We found great variation on color pattern among specimens, the more common individuals have a similar pattern to that described for the holotype (Fig. 3A and C) as well as a more melanic-marbled pattern (Fig. 3B). Although less common, a pattern with a yellowish brown inner to the borders of the sagittal crests is also found (Fig. 3D). Although males and females share the same dorsal color variation, the throat in males present a dark brown color, and females a whitish coloration. Measurements for P. redacta sp. nov. and P. minuta are presented in Table 1. Etymology. The name of the new species is derived from the Latin adjective redactus that means reduced, in allusion to the small size of the new species. Natural history and distribution. Proceratophrys redacta sp. nov. is known only from the surroundings of type locality, at the montane region of Morro do Chapu municipality, close to where P. minuta occurs (about 100 km away) (Fig. 4). The region is dominated by the Mesoproterozoic sandstones of Morro do Chapu formation (Battilani et al. 1996), reaching up to 1300 m a.s.l., the climate is a sub-warm semi-humid with annual mean temperatures under 22oC, (4oC was already recorded), and precipitation is regular with a short dry season (Nimer 1972). Landscape in the area consists of an extensive and relatively flat plateau situated around 1200 m from which the hill of Morro do Chapu (hat hill) emerges. At the plain sandy depositional areas grows an open shrubby vegetation, however at the richer soil areas a semi-deciduous forest is found; the bare rock at the mountain tops and eroded areas are covered by a typical rocky meadows vegetation, where Cactaceae, Bromeliaceae, and Velloziaceae are abundant. Steeper areas are covered by a lower open forest, the ground is sandy and covered with a deep layer of leaves and a few scattered small ponds are present, surrounded with mosses.

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FIGURE 3. Individuals of Proceratophrys redacta sp. nov. in life. Adult male (A); melanic-marbled male individual (B); an adult female (C) and a couple in amplexus (D).

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FIGURE 4. Distributional map Proceratophrys redacta sp. nov. (red stars) and P. minuta (blue circles) at the northeastern portion of Chapada Diamantina, Bahia, Brazil. White dots represent cities.

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TABLE 1. Morphometric data for Proceratophrys redacta sp. nov. and P. minuta. Measurements abbreviations are explained in the text. Average values are given (in mm), followed by range, in parenthesis. Proceratoprys redacta sp.n. Males (N=6) SVL HL HW ED END UEW IOD IND THL TL FTL HAL 28.4 (26.929.7) 11.6 (10.812.4) 13 (12.213.8) 4.1 (3.74.4) 2.5 (2.42.6) 3.4 (3.33.7) 3 (2.43.4) 1.9 (1.72.2) 12.1 (11.312.8) 10.2 (9.810.5) 17.2 (15.918.4) 13.3 (12.314.2) Females (N=4) 34.4 (33.534.9) 13.3 (12.714.1) 15.7 (15.216.2) 4.6 (4.54.7) 2.9 (2.73.1) 4 (3.84.2) 3.4 (3.13.8) 2.1 (22.5) 13.9 (13.114.5) 12 (11.912.2) 20.1 (19.720.4) 23.9 (15.946.4) Proceratophrys minuta Males (N=10) 20.9 (19.222.6) 9.1 (8.69.5) 10.0 (9.210.8) 2.6 (2.42.9) 2.1 (1.82.3) 3.1 (2.83.4) 2.5 (2.33.0) 1.8 (1.61.9) 9.5 (8.610.4) 8.5 (8.19.1) 13.1 (11.914.1) 11.1 (10.412.2) Females (N=11) 28.9 (25.931.6) 11.2 (10.512.2) 13.2 (12.214.1) 3.2 (2.93.6) 2.6 (2.43.2) 3.8 (3.44.3) 3.2 (3.13.4) 2.2 (2.12.3) 11.9 (11.312.4) 10.9 (10.511.3) 17.2 (15.817.8) 14.5 (14.114.8)

P. redacta sp. nov. was found active on the ground at night, within the montane forest and the adjacent open vegetation (Fig. 5). It was also captured in pitfall traps, along the Morro do Chapu hill, about 1250 m a.s.l. and in the dense vegetation at the shores of streams running over bare rock outcrops, as those of Ferro Doido waterfall at about 890 m a.s.l. No individual was heard calling. Also none was found at the dry sandy scrublands, the most abundant vegetation at this area, indicating a restriction to this open mesic areas. Molecular phylogeny. Our analyses recovered Proceratophrys as monophyletic, and consisting of two main clades. The first is composed by P. cristiceps, P schirchi, P. minuta and P. redacta sp. nov. All analyses recovered Proceratophrys redacta sp. nov. as sister to P. minuta, both being sister of a clade assembling P. cristiceps and P. schirchi (Fig. 6). The second clade is composed by the remaining species of Proceratophrys, however the intrageneric relationships are poorly resolved. Three different lineages were recovered in this clade: 1) P. appendiculata and P. melanopogon as sister species; 2) P. avelinoi and P. bigibbosa as sister species; and 3) a clade containing P. boiei, P. goyana, P. concavitympanum, P. moratoi, P. cururu, P. renalis, and P. laticeps. In the latter Proceratophrys moratoi is sister to P. concavitympanum and both sister to P. boiei and P. goyana. This latter clade is sister to a clade where Proceratophrys laticeps is basal to P.cururu and P. renalis, which are recovered as sister species. Uncorrected p-distances ranged from 12 to 21% for cyt b, 3 to 11% for 16S and 1 to 5% for Rag-1 among Proceratophrys species (Table 2). Genetic distances between P. minuta and P. redacta sp. nov. were 12-13% for cyt b, 4% for 16S and 2% for Rag-1 and are compatible with interspecific distances found among Proceratophrys species (Table 2). It is important to note that none of the differences found on Rag-1 between P. minuta and P. redacta sp nov. were related to heterozygous sites.

Discussion
Among the Proceratophrys species, the ones lacking eyelid appendages such as those included in the P. cristiceps group, are difficult to identify confidently. The species here described as well as P. minuta, are good examples; they are morphologically very similar to P. cristiceps, but as they are much smaller, the size helps to diagnose them. However, among the species with similar sizes the distinction is not so clear. Such problematic diagnoses might result in possible misidentifications as those visualized on our map (Fig. 7). Individuals identified as P. cristiceps (Cintra et al. 2009; Oda et al. 2009), thought to be a Caatinga dweller, are reported deep into the Cerrado biome, where P. goyana is widespread and thought to be endemic. Similarly individuals occurring deep in to the Caatinga biome, were identified as P. goyana (vila et al. 2011). Highlighting this confusion Cruz et al. (2012) redescribed P. cristiceps, and two additional related new species, restricting the distribution of P. cristiceps to the coastal

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lowland and suggesting that individuals from Espinhao range should be considered P. cururu, while those west from it, at the Cerrado, should be considered P. goyana. Unfortunately the authors did not examined specimens from those localities, and other areas at the Caatinga, thus leaving Caatinga specimens without a specific name. Thus these dubious identifications from some localities mentioned above, and the recent results on Proceratophrys taxonomy (Prado & Pombal 2008; vila et al. 2011; Martins & Giaretta 2011; Napoli et al. 2011; Cruz et al. 2012) strongly indicate that a rich cryptic diversity is still uncovered, highlighting the urgently need for a taxonomic revision of several species, especially on the widespread appendageless ones.

FIGURE 5. Habitat in which Proceratophrys redacta sp. nov. was found. (A) general view of Morro do Chapu hill, which reaches 1300 m a.s.l., showing the shrubby vegetation at the lower lands and the montane forest at the slopes close to the top; (B) General view of Ferro Doido waterfall; (C) detailed view of the shrubby vegetation over bare rock at Ferro Doido waterfall; (D) and detailed view from the inside of the forest at the top of Morro do Chapu hill.

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FIGURE 6. Bayesian tree topology obtained from the combined molecular data set (16S, cyt b and Rag-1); figure shows the 50% majority-rule consensus phylogram. Posterior probability and ML bootstrap values are shown above the branches.

Despite the taxonomic clarity, the geographical distributions of Proceratophrys morphotypes bring some insights on the evolution of body shape. Although intermediate forms can also be found, two patterns can be visualized: (i) large-bodied species with median to long palpebral and rostral appendages are generally found at the warm/ wet forests, and (ii) small-bodied species with very short or no appendages are generally found in open and/ or dryer habitats, at high altitude and/or latitude. This switch in body shape could be the result of a process such as Allens rule, in which reducing body surfaces (e.g. by reducing appendages) (Alho et al. 2011) would be adaptive for maximize heat gain and minimize water loss at cold and/or dry areas, as the open environments are generally dryer and/or cooler than the forest ones. However physiological analyzes, together with further morphological and phylogenetic data are needed to attest this suggestion. The dwarf species P. redacta sp. nov. and P. minuta are currently known only from a few highland areas at Espinhao range, and seems to be sister to either a Caatinga dweller (P. cristiceps) or a Atlantic Forest one (P. schirchi). Nonetheless they are found in broad sympatry with P. cristiceps, however not syntopically. The environmental climatic conditions as well as microhabitat availability at both above and below 800 m a.s.l. at the Espinhao range may be representing an eco-physiological barrier (Lomolino et al. 2006) for those species, where P. cristiceps do not climb up, and P. redacta sp. nov. and P. minuta do not go down, been therefore restricted to the highland habitats.

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FIGURE 7. Distributional records of all current recognized Proceratophrys species, including the new species described here: P. redacta sp. nov.

Considering this montane restriction, the disjunct distribution of P. minuta at Miguel Calmon and Palmeiras, having P. redacta sp. nov. in its middle (Fig. 4), deserves further investigation as these areas are presently separated by lowlands covered with Caatinga vegetation. It will be important in the future to analyze population variation through both molecular and morphological approaches to verify their specific identity. As in the former results (Amaro et al. 2009; Pyron & Wiens 2011), in our phylogenetic analysis the traditional morphological groups are not recovered as monophyletic. Nonetheless the phylogenies published to date (Amaro et al. 2009; Pyron & Wiens 2011) are likely to change considerably in the future as the new recently described Proceratophrys species (Cruz et al. 2005; Prado & Pombal 2008; Cruz & Napoli 2010; vila et al. 2011; Martins & Giaretta 2011; Napoli et al. 2011; Cruz et al. 2012) are to be included, what would confirm that the diversity within the genus is clearly underestimated.

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Acknowledgements
We are grateful to Ivan Prates, Roberta Pacheco Damasceno, Caroline Garcia, Milena Ferreira dos Santos and Eric Cazetta for assistance in the field work and to Sabrina Baroni for technical assistance, Hussam Zaher and Carolina Castro Mello for access to specimens, and Instituto Chico Mendes de Conservao da Biodiversidade (ICMBio) for collection authorization (permit number 19754-1). We would also like to thank Miguel Vences, Paula Valdujo and an anonymous reviewer for valuable comments, corrections and suggestions on early versions of this manuscript. We thank Fundao de Apoio Pesquisa do Estado de So Paulo (FAPESP), Conselho Nacional de Desenvolvimento Cientfico e Tecnolgico (CNPq), and National Science Foundation (NSF) for support.

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Vieira, W.L.S, Vieira, K.S. & Santana, G.G. (2007) Description of the tadpoles of Proceratophrys cristiceps (Anura : Cycloramphidae, Odontophrynini). Zootaxa, 1724. Vieira, K.S., Arzabe, C., Hernandez, M.I.M. & Vieira, W.L.S. (2008) An Examination of Morphometric Variations in a Neotropical Toad Population (Proceratophrys cristiceps, Amphibia, Anura, Cycloramphidae). Plos One, 3, Weygoldt, P. & Peixoto, O.L. (1985) A new species of horned toad (Proceratophrys) from Espirito Santo, Brazil (Amphibia: Salientia: Leptodactylidae). Senckenbergiana Biologica, 66, 18. Wied, M.P.N. (1824) Verzeichnis der Amphibien welche in zweiten Bande der Naturgeschichte Brasiliens von Prinz Max von Neuwied werden beschreiben Werden. Isis von Oken, 14, 661673. Zanella, N. & Busin, C.S. (2007) Amphibia, Anura, Cycloramphidae, Proceratophrys bigibbosa: distribution extension for Rio Grande do Sul, Brazil. Check List, 3, 6566.

APPENDIX I. Material examined. Proceratophrys concavitympanumBrazil: Tocantins: Palmas, MRT 68266827. Proceratophrys cristicepsBrazil: Pernambuco, So Jos dos Cordeiros, MRT 99869995; Cear: Macuripe, MZUSP 8842788434; Rio Grande do Norte: Angicos, MZUSP 8842788434. Proceratophrys cururuBrazil: Minas Gerais: Santana do Riacho, Parque Nacional da Serra do Cip, MTR 19628; MTR19629; MTR 19639. Itabira, Serra dos Alves, MTR 21764, MTR 21853. Proceratophrys minutaBrazil: Bahia: Miguel Calmon, Parque Estadual de Sete Passagens, MZUSP 146197146536. Proceratophrys goyanaBrazil: Gois: UHE Serra da Mesa, MZUSP 8910489113. Proceratophrys schirchiBrazil: Bahia: Amargosa, MZUSP 14272114724; Minas Gerais: Jequitinhonha: Reserva Biolgica da Mata Escura, MTR 1732017321; MTR 17351.

A NEW DWARF PROCERATOPHRYS SPECIES

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APPENDIX II. Species, voucher id and localities of molecular sampled in this study. Voucher abbreviations are AF (Laboratrio de Citogentica de Vertebrados, Instituto de Biocincias, Universidade de So Paulo, Brazil), JC (field number of Jos Cassimiro, Universidade de So Paulo, Brazil), FSFL (Field number of Felipe S Fortes Leite, Pontifcia Universidade Catlica de Minas Gerais, Brazil), CH (Clio F.B. Haddad, tissue collection , Universidade Estadual Paulista, Rio Claro, So Paulo, Brazil), DB (Diego Baldo, Universidad Nacional de Misiones, Argentina), MZUSP (Museu de Zoologia, Universidade de So Paulo, Brazil) ZUFRJ (Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Brazil).

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Voucher Id Caucaia do Alto, Cotia, SP Serra do Teimoso, Jussari, BA Caucaia do Alto, Cotia, SP Poos de Caldas, MG Mucug, BA Varginha, MG Itirapina, SP Santos, SP Misiones, Argentina Serra da Cantareira, So Paulo, SP Misiones, Argentina Usina Hidreltrica de Lajeado, Palmas, TO Parque Nacional da Serra das Confuses, PI Cardeal Mota, MG Petrolina de Gois, GO Reserva Natural da Vale do Rio Doce, Linhares, ES Maring, Itatiaia, RJ Miguel Calmon, BA Miguel Calmon, BA Morro do Chapu, BA Morro do Chapu, BA Brejo Madre de Deus, PE So Loureno, Santa Teresa, ES Santos, SP Locality GenBank accession number cyt b 16S Rag-1 FJ685663 FJ685683 FJ685703 FJ685664 FJ685684 FJ685704 FJ685665 FJ685685 FJ685705 FJ685666 FJ685686 FJ685706 FJ685667 FJ685687 FJ685707 FJ685668 FJ685688 FJ685708 FJ685669 FJ685689 FJ685709 JX987065 JX987066 JX987067 FJ685671 FJ685691 FJ685711 FJ685672 FJ685692 FJ685712 FJ685673 FJ685693 FJ685713 FJ685674 FJ685694 FJ685714 FJ685675 FJ685695 FJ685715 FJ685676 FJ685696 FJ685716 FJ685677 FJ685697 FJ685717 FJ685678 FJ685698 FJ685718 FJ685679 FJ685699 FJ685719 JX982961 JX982965 JX982969 JX982962 JX982966 JX982970 JX982963 JX982967 JX982971 JX982964 JX982968 JX982972 FJ685680 FJ685700 FJ685720 FJ685681 FJ685701 FJ685721 FJ685662 FJ685682 FJ685702

Species

Cycloramphus acangatan Macrogenioglottus alipioi Macrogenioglottus alipioi Odontophrynus americanus O. carvalhoi O. cultripes O. moratoi Proceratophrys appendiculata P. avelinoi P. boiei P. bigibbosa P. concavitympanum P. cristiceps P. cururu P. goyana P. laticeps P. melanopogon P. minuta P. minuta P. redacta sp. nov. P. redacta sp. nov. P. renalis P. schirchi Thoropa taophora

AF 1605 AF 919 AF 1607 AF 665 JC 1224 FSFL 875 CH 511 AF1446 DB 1246 AF 1587 DB 2313 AF 1094 AF 887 FSFL 580 AF 1188 AF 1900 CH 362 AF2008 AF2009 MTR22579 MTR22582 ZUFRJ 8682 CH 371 AF 1434

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