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Two new species of brachycephalus (anura: brachycephalidae) from the atlantic forest in parana- state, southern brazil Premium gy cris221D anpenR 24, 2012 | Al pagos Herpetologica, 62(2), 2006, 221-233 Ó 2006 by The Herpetologists’ League, Inc. TWO NEW SPECIES OF BRACHYCEPHALUS (ANURA BRACHYCEPHALIDAE) FROM THE ATLANTIC FOREST ‘ IN PARANA STATE, SOUTHERN BRAZIL ANA C. R. ALVESI, LUIZ F. CELIO F. B. HADDADI, AND to view nut*ge SÉRGIO F. DOS REIS5,6 Ancias, Universidade Estadual Paulista, Departamento de Zoologia, Instituto de Biocie Caixa Postal Igg, 13506-900, Rio Claro, SP, Brazi12 Universidade Tuiuti do Parana Rua Marcelino

Champagnat, 505, 80710-250, Curitiba, PR, grazil 3 Mater Natura, Instituto de Estudos Ambientais, Rua Desembargador Westphalen, 15-168 andar, 80010-110, Curitiba, PR, Brazil 4 ‘s-Graduaca em Gene ‘tica e Biologia Molecular, Instituto de Biologia, Programa de Po -o Universidade Estadual de campinas, caixa postal 6109, 13083-970, campinas, sp, Brazil 5 Departamento de Parasitologia, Instituto de Biologia, new species from Pico Marumbi is characterized by male SVL 5 1 1. 6-12. 5 and female SVL 5 13. -14. 5 mm; and general color orange with dorsal reddish-brown irregular markings, lateral urfaces with small dark brown spots, and belly with brownish spots and small dots. The new species trom Pico da Igreja is characterized by male SVI_ 5 12. 6-13. 9 and female SVI_ 5 14. 6 15. 3 mm; and general color orange, lateral surfaces with small dark brown spots, and belly with brownish coalescent spots and small dots. Comparisons with other brachycephalid species and osteological data are provided.

Key words: Amphibia; Anura; Atlantic Forest; Brachycephalidae; Brachycephalus; New species; Osteology; Southern Brazil THE FAMILY Brachycephalidae is monotypic (Frost, 2004). The species of the genus Brachycephalus have snout-vent length . 8 cm, phalangeal loss, and reduced number of toes and are believed to have evolved by miniaturization (Yeh, 2002). These small frogs inhabit leaf litter and are endemic to the Atlantic rainforest of southeastern and southern grazil (Giaretta and Sawaya, 1998; Izecksohn, 1971; Miranda-Ribeiro, 1920; Pombal, 2001; Pombal et ala, 1998).

Until recently, the known diversity of Brachycephalus included species occurring in the States of Rio de – Janeiro, Sao Paulo, and Parana, namely, Brachycephalus didactylus (Izecksohn, 1971), Brachycephalus ephippium (Spix, 1824), Brachycephalus hermogenesi (Giaretta and Sawaya, 998), grachycephalus nodoterga Miranda-Ribeiro, 1920, Brachycephalus pernix Pombal, Wistuba and Bornschein, 1998, and Brachycephalus vertebralis Pombal, 2001. 6 CORRESP PAGF 31 Pombal, Wistuba and Bornschein, 1998, and Brachycephalus vertebralis Pombal, 2001. CORRESPONDENCE: e-mail, sfreis@unicarnp. r 221 As a result of recent herpetological surveys in the mountain slopes of the Serra do Mar, we discovered two undescribed species from the – State of Sao Paulo and four undescribed species from the State of Parana. These findings double the known diversity of Brachycephalus. We have already described wo of the four new species from the State of ‘ , Parana namely, Brachycephalus brunneus Ribeiro, Alves, Haddad, and Reis, 2005 and Brachycephalus izecksohni Ribeiro, Alves, Haddad, and Reis, 2005, and here we described the other two species.

The diagnoses of the two new species are based on the color, external morphology, and ostelogy of adults. Additionally, we used continuous metric traits to characterize these two new species morphometrically and discriminate them from B. brunneus, g. pernix, and B. izecksohni, all of which are restricted in distribution to the Serra ‘ do Mar mountain range in the State of Parana. We also provide morphological compansons among species in the genus Brachycephalus. 222 HERPETOLOGICA [vol. 62, NO. 2 MATERIALS AND METHODS specmens were anaesthetized and killed in 30% ethyl alcohol, fixed in 10% formalin, and preserved in 70% ethyl alcohol.

The terminology used for the external morphology and texture of the skin followed Lynch and Duellman (1997). The color codes used in color descriptions were those of smithe (1975). The bon es were cleared and bones and cartilages were cleared and doublestained with alizarin red and alcian blue according to Taylor and Van Dyke (1985). Specimens of B. runneus (n 5 2), B. ephippium (n 5 1), B. hermogenesi (n 5 1), B. izecksohni (n 5 2), and B. pernix (n 5 1) were used for osteological comparisons. Drawings were made using a Zeiss stereomicroscope fitted with a drawing tube.

Ten metric traits were measured with a micrometric ocular fitted to the stereomicroscope. The abbreviations used were: SVL (snout- vent length); HL (head length; from tip of snout to angle of jaw); HW (head width; greatest width of head located between angles of jaw); ND (nostril diameter); IND (internostril distance; between inner margins of nostrils); ED (eye diameter); IOD (interorbital istance; between anterior corners of the eyes); END (eye—nostril distance; from anterior corner of the eye to posterior margin of nostril); THI_ (thigh length); TBL (tibia length)_ All measurements were in millimeters.

Canonical variate analysis (CVA) was used to describe variation in metric traits within and among the five species of Brachycephalus from ‘ the State of Parana. As noted by Rohlf et al. (1996:347), assumptions of multivariate normality and homogeneity of within-group covariance matrices underlie the construction of canonical axes and impose restrictions on inferential approaches to CVA (Krzanowski, 1989; Krzanowski nd Radley, 1989).

In the present analysis, we constructed confidence regions around sample centroids for canonical axes using parametric bootstrap theory developed for CVA by Ringrose (1996). The parametric bootstrap proced 31 parametric bootstrap theory developed for CVA by Ringrose (1996). The parametric bootstrap procedure is based on the N( i, () distribution, where xi is the vector ofx means for the i-th population group and ( is the unbiased estimate of the pooled withingroup covariance matrix.

The Cholesky factoriA zation was applied to ( in the simulation of 1 000 replicate data matrices (Von Zuben et al. 1998). For each replicate matrix, bootstrap analogs were obtained for the sample group vector means and for the within- and betweengroup sum of squares and product matrices. Canonical variate analysis was done to yield bootstrap eigenvalues and eigenvectors. The vanances and covariances of sample centroids on canonical axes were estimated over all replicates and the x2 distribution was used to construct 95% confidence regions by applying formulas provided by Krzanowski (1989).

Computations for the parametric bootstrap were numerically formulated and computationally implemented in MATLAB as described in Von Zuben et al. (1998). Vector correlations between original metric traits and canonical variate scores were calculated and were graphically displayed to portray the principal directions of variatlon of each metric tralt in the reduced canonical variate space (Garavello et al. , 1992).

Sample sizes used for the morphometric analyses were as follows: B. brunneus (n 5 24), B. ferrugnus (n 5 13), 3. izec«ohni (n 5 15), B. pernix (n 5 12), and g. pombali (n 5 8). The specimens used in the description or examined for comparisons are in AL-MN (Adolpho Lutz collection, deposited in the Museu Nacional, s 1 omparisons are in AL-MN (Adolpho Lutz collection, deposited in the Museu Nacional, Rio de Janeiro, Rio de ‘ Janeiro, Brazil), CFBH (Celio F. B.

Haddad collection, deposited in the Departamento de Zoologia, universidade Estadual paulista, – Campus de Rio Claro, Sao Paulo, Brazil), ” MHNCI (Museu de Historia Natural do – Capao da Imbuia, Curitiba, Parana Brazil), MNRJ (Museu Nacional, Rio de Janeiro, Rio de Janeiro, Brazil), MZUSP (Museu de – – Zoologia da Universidade de Sao Paulo, Sao Paulo, grazil), and ZUEC (Museu de Historia Natural, Universidade Estadual de Campinas, – Campinas, Sao Paulo, grazil). The specimens examined in the comparisons are listed in Appendix I. RESULTS Brachycephalus ferruginus sp. ov Holotype. —CFBH 8024, adult male, one of a series collected at Pico Marumbi (258 259 S; 488 559 W), municipality of Morretes, Parana State, southern Brazil, altitude 1200 m, on 17 December 2002 by F. Ribeiro (Fig. IA,B). paratopotypes. —CFBH 8037, one male and, CFBH 8036, one female collected on 27 June 2006] 223 FIG. 1 . —Brachycephalus ferruginus, CFBH 8024 (h010type), adult male from Pico Marumbi (258 269 S; 488 59 W), municipality of Morretes, Parana State, southern Brazil. (A) Dorsal view, (B) entral view. SVL 5 12. 0 mm. March 2001 by L.

F. Ribeiro; CFBH 8039, 8040, two males collected on 19 April 2001 by L. F. Ribeiro; CFBH 8041 (cleared and stained), one male collected on 18 January 2002 by L F. Ribeiro; CFBH 8025-27, three males and, CFBH 8038, one female collected with the h010type on 17 Decernber 2002 by L F. Ribeiro; CF3H 8030, 8031, 8033, one female collected with the holotype on 17 December 2002 by L. F. Ribeiro; CFBH 8030, 8031, 8033, 8034, four males, CFBH 8029 (cleared and stained), 8035, two females and CFBH 8028, 8032, two juveniles collected on 24 April 2003 by L.

F. Ribeiro. Diagnosis. ??(l) SVL in males 11. 6-12. 5 and SVL in fernales 13. 0- 14. 5 mm; (2) body bufoniform, (3) skin on top of the head and central part of the back body smooth and without dermal co- ossification; (4) general color orange with dorsal reddish-brown irregular markings, lateral surfaces with small dark brown spots, and belly with brownish spots and small dots. Like other species of the genus Brachycephalus, B. erruginus is miniaturized (sensu Yeh, 2002) with loss of phalanges in the manus and pes; and has a completely ossified pectoral glrdle WIth epicoracoids closely juxtaposed and articulating throughout their lengths, mosternum present, and sternum absent. The dorsal color pattern of B. ferruginus resembles B. pernix but is readily distinguished from the latter by the presence of dorsal reddish- brown irregular markings, and by the form and brownish color of the dorso-lateral spots. The relative larger size and the dorsal color pattern also distinguish B. erruginus from B. izecksohni, which is smaller and without dorsal or lateral marks or spots. The general orange color and the rounded snout shape in dorsal view distinguish B. ferruginus from B. brunneus, which has a general brown color and a mucronate snout shape in dorsal iew. Brachycephalus ferruginus has smooth skin texture with no dermal co-ossification on top of the head and central part of PAGF 7 31 ferruginus has smooth skin texture with no dermal co-ossification on top of the head and central part of the back body, whereas B. phippium, B. nodoterga, and B. vertebralis have dermal co- ossificatlon on top of the head and central part of the back body. Brachycephalus ferruginus differs from 3. didactylus and B. hermogenesi in having a bufoniform body shape, a rounded snout shape in dorsal view, and a general orange color; whereas B. didactylus and g. ermogenesi have a leptodactyliform body shape, a short and pointed with a rounded tip snout shape in dorsal view, and general brownish color. Description of holotype. —Body robust, bufoniform (Figs. IA, 2A).

Head as wide as long, slightly narrower than body; head length 36% of snout-vent length; snout short with length almost equal to eye diameter, rounded in lateral and dorsal views (Fig. 2A,B); nostrils protuberant, directed anterolaterally; canthus rostralis not distinct; loreal region weakly concave; lips nearly sigmoid; eye slightly 224 [VOI. 62, NO. 2 TABLE 1. —Measurements in millimeters of the type series Brachycephalus ferruginus ( S mean; SD 5 x standard deviation). Character abbreviations are listed in the Material and Methods.

Males (n 5 9) x SD Range x Females (n 54) SD Range SVL HL HW ED ND IOD IND END TAL TBL 12. 2 4. 5 4. 8 1. 2 0. 2 2. 4 1. 2 0. 6 4. 4 4. 0 0. 3 0. 1 0. 3 0. 1 0. 0 0. 1 0. 0 0. 0 0. 1 0. 1 1 1. 6-12. 5 4. 3-4. 6 4. 0-5. 0 2. 2-2. 6 1. 1-1. 3 0. 5-0. 7 0. 7 4. 8 4. 4 0. 6 0. 1 0. 1 0. 1 0. 0 0. 0 0. 1 0. 1 0. 3 0. 1 13. 0-14. 5 5. 1-5. 3 su-5. 8 1 . 2-1 . 4 0. 2-0. 2 2. 6-2. 7 1. 3-1. 5 0. 6-0. 8 4. 5-5. 3 4. 3-4. 6 FIG. 2. —Brachycephalus ferruginus, CFBH 8024 (holotype). A) Dorsal view of body, (3) lateral view of head, (C) Ieft hand, and (D) left foot. rotruding in dorsal and lateral views, eye diameter 26% of head length; tympanum absent; vocal sac not expanded externally; vocal slits present; tongue longer than wide, posterior 1/2 not adherent to floor of mouth; choanae relatively small and round; vomerine odontophores absent. Upper arm and forearm relatively slender, upper arm approximately as long as forearm; fingers 1-111 robust, short and distinct; finger IV very reduced; tip of fingers and II slightly rounded, tip offinger III pointed; relative engths offingers IV , I , II , III; subarticular tubercles and inner and outer metacarpal tubercles absent (Fig. C). Legs relatively short, thigh robust; thigh length 35% of SVI- tibia length 90% of thigh length; toe II very reduced, toe III short and relatively distinct, toe IV robust and distinct, toes and V externally absent; relative lengths of toes II , III , IV; subarticular tubercles and inner metatarsal tubercles absent; outer metatarsal tubercle distinct, large, and ovoid (Fig. 2D). Skin on top of the head and central part of the back body smooth and with no dermal coossification (Figs. IA.

A); skin on dorso-lateral surfaces of body, flanks, and dorsal surface of thighs granular; skin on venter and ventral surfaces of the legs smooth; skin on ventrolat- eral surfaces of body and area around the cloa surfaces of the legs smooth; skin on ventrolat- eral surfaces of body and area around the cloacal opening granular. Coloratlon of holotype In life. —Dorsum bright orange (orange yellow, #18); central area of body and head with reddish- brown (maroon, #31) irregular markings; light areas pale brigh Yellow (su fur yellow, #157) with very small Olive gray (#42) dots near or around the reddish-brown markings.

Lateral areas of body, flanks, and thighs with small dark brown (sepia, #21 9) spots. Arms orange (spectrum orange, #1 7) and legs bright orange (orange yellow, #18). hroat and belly orange (spectrum orange, #17) with small greenish (Olive gray, #42) dots. Belly with glandular aspect and with brownish Craw umber, #23) spots and small dots. Coloration of holotype in preservative. — General color pale cream (cream calor, #54); central area of body and head with markings orange-brown (amber, #36), lateral spots almost black (dusky brown, #19); small dots on belly pale greyish (smoke gray, #44).

Measurements of holotype. —SVL 12. 0; HL 4. 4; HW 4. 8; IND 1. 1; ED 1. 1; IOD 2. 2; END 0. 6; THL 4. 3; TBL 3. 8. Variation in the type series. —Measurements and proportions of nine males and four females are given in Tables 1 and 2. Color in life varying among specmens in the extension of reddish-brown markings on the central area of body and head (Fig. 3). Distribution. — Brachycephalus ferruginus is known only from Pico Marumbi (258 269 S; ‘ 488 559 W), municipality of Morretes, parana state, southern Brazil. 225 . roportions (%) of the type series of Brachycephalus f TABLE 2 —P