A Remarkable New Glass (Centrolenidae: ) from the Northeast Atlantic Forest, Brazil Author(s): Rafael Pontes, Ulisses Caramaschi, and José P. Pombal, Jr. Source: Herpetologica, 70(3):298-308. 2014. Published By: The Herpetologists' League DOI: http://dx.doi.org/10.1655/HERPETOLOGICA-D-13-00024 URL: http://www.bioone.org/doi/full/10.1655/HERPETOLOGICA-D-13-00024

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A REMARKABLE NEW (CENTROLENIDAE: VITREORANA) FROM THE NORTHEAST ATLANTIC FOREST, BRAZIL

1 RAFAEL PONTES ,ULISSES CARAMASCHI, AND JOSE´ P. POMBAL,JR. Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Vertebrados, Quinta da Boa Vista, 20940-040 Rio de Janeiro, Brasil

ABSTRACT: We describe a new of glass frog (Vitreorana) from Fazenda Novo Pau Brasil, in the Atlantic Forest of northeastern Brazil. Previous to this work, Vitreorana baliomma sp. nov. was misidentified as V. eurygnatha, from which it can be distinguished by the iris pattern flecked with star-shape melanophores; rudimentary nuptial excrescences formed by glands on the dorsomedial surface of Finger I, with some accessorial glands along its periphery; parietal, urinary bladder, kidneys, and testes peritonea translucent; visceral peritoneum with iridophores covering the pericardium, liver, and gastrointestinal tract. We also provide a brief discussion on its morphological similarities with other Vitreorana species. Key words: ; Cochranellini; Eye coloration; Nuptial excrescences; Peritoneum; Vitreorana baliomma sp. nov.

FOR DECADES, members of the Neotropical Forest—Vitreorana parvula (Boulenger, family Centrolenidae (Taylor, 1951), com- 1895), (Muller, ¨ 1924), monly known as glass , have attracted and (Lutz, 1925)— the attention of scientists because of their persist obscured. This group remains unclar- conspicuous biological and morphological ified because of the scarcity of recent features (Cisneros Heredia and McDiarmid, taxonomic studies and lack of refined analysis 2007). This clade comprises about 150 spe- of morphological characters (Cisneros-Hered- cies, most of which inhabit the vegetation ia and McDiarmid, 2007). These species have along streams in forested areas (Guayasamin been placed in the genus Vitreorana,a et al., 2009; Frost, 2013). The family is found monophyletic clade informed from molecular throughout Central America, tropical Andes, evidence, which accommodates species from Guiana Shield, and the Amazon basin, and a the Cordillera de la Costa in Venezuela, the disjoint group occurs in the Atlantic Forest, Precambrian Shields of South America, the from southeastern Brazil to Argentina (Heyer, Amazon basin, and the Atlantic Forest domain 1985; Guayasamin et al., 2009; Castroviejo- (Guayasamin et al., 2009). Vitreorana is Fisher et al., 2011). characterized by the following phenotypic Recently, the phylogenetic relationships and characters: (1) white peritoneum covering, systematics of glass frogs have been the focus totally or partially, the liver; (2) white of various studies, culminating in several gastrointestinal peritoneum; (3) green bones taxonomic changes (e.g., Cisneros-Heredia in life; (4) a lavender dorsal coloration in preservative; and (5) eggs deposited on the and McDiarmid, 2007; Guayasamin et al., upper or under side of leaves (Guayasamin et 2008, 2009). Although recent studies (e.g., al., 2009). Using only morphology, however, Castroviejo-Fisher et al., 2011; Hutter and this genus cannot be diagnosed from other Guayasamin, 2012) have resolved some taxo- centrolenid genera, as Chimerella. nomic problems, several issues need to be Studies addressing taxonomic questions on clarified at the alpha taxonomic level (Cis- glass frogs from the Atlantic Forest biome neros-Heredia and McDiarmid, 2007; Castro- were generally based on few specimens viejo-Fisher et al., 2011). available from limited localities from the Of these issues, the three species of southeastern and southern portions of that Vitreorana known to occur in the Atlantic region (Taylor and Cochran, 1953; Heyer, 1978, 1985). Recently, field collections pro- 1 CORRESPONDENCE: email, rafaelcunhapontes@hotmail. duced range extensions for glass frogs, report- com ing occurrence for northeastern fragments of

298 September 2014] HERPETOLOGICA 299 this biome (Freitas et al., 2004; Carvalho et al., Heredia and McDiarmid (2007). We obtained 2005; Freitas et al., 2007; Gouveia et al., nine measurements using digital calipers 2012); however, because of the lack of (60.1 mm): (1) snout–vent length (SVL), (2) morphological information, the taxonomic head length (HL), (3) head width (HW), (4) status of these populations remains unclear radio–ulna length (RL), (5) hand length (Gouveia et al., 2012). (HaL), (6) femur length (FL), (7) tibia length Herein, we examine aforementioned col- (TL), (8) tarsal length (TaL), and (9) foot lected specimens from the northern portion of length (FL). With the use of a stereoscopic the Atlantic Forest and describe a new species microscope, we obtained seven additional of Vitreorana, previously assigned to V. morphometric variables (60.05 mm): (10) eurygnatha. In addition, we provide a brief snout–nostril distance (SND), (11) internarial discussion on the morphological affinities distance (ID), (12) eye–nostril distance (EN), within Vitreorana and standardizations on (14) eye diameter (ED), (15) interorbital nuptial excrescences in Centrolenidae. distance (IOD), and (16) width of disc of third finger (3WD). All morphometric data MATERIALS AND METHODS from preserved specimens were measured by Nomenclature and Conventions RPandreportedasminimum–maximum Museum acronyms follow those established (mean 6 standard deviation). by the ASIH (http://www.asih.org/codons. pdf); in addition, the following collections SPECIES DESCRIPTION were examined: Cole¸ca˜oCelio´ F.B. Haddad, Departamento de Zoologia, I.B., Universidade Vitreorana baliomma sp. nov. Estadual Paulista, Rio Claro, Brazil (CFBH); (Figs. 1A–C; 2D,G) Cole¸ca˜o Adolpho Lutz, housed at the Museu sp. (cf. eurygnathum).— Nacional, Rio de Janeiro, Brazil (AL-MN); Carvalho et al. (2005: 51). Cole¸ca˜o da Universidade Federal de Sergipe, Aracaju, Brazil (UFSE). We also examined Hyalinobatrachium eurygnathum.—Freitas et photos of the holotype of Vitreorana urano- al. (2004: 281). scopa (ZSM 81/1921) and the lectotype of V. Vitreorana aff. eurygnatha.—Gouveia et al. parvula (BMNH 88.2.7.32). Specimens of the (2012: 16). new species were fixed in 10% formalin Holotype.—MNRJ 46857, adult male col- solution and preserved in 70% alcohol (Ap- lected at Mata de Cabruca, Fazenda Novo pendix). Sex and maturity were determined by 0 0 Pau Brasil (16859 22"S; 39834 58"W; 98 m secondary sexual characteristics (nuptial ex- above sea level (a.s.l.); datum ¼ WGS84), crescences, vocal sacs, and slits) and the Municipality of Itamaraju, State of Bahia, observation of convoluted oviducts through Brazil, by C. Canedo and F. Falca˜o, on 2 the transparent ventral skin. February 2007. Morphology Paratypes.—MNRJ 37904 and 37905 Characters followed the descriptions of (cleared and stained), two adult males collect- ed at Parque Nacional Serra de Itabaiana Lynch and Duellman (1973), Ruiz-Carranza 0 0 and Lynch (1991), Cisneros-Heredia and (10845 S; 37820 W), Municipality of Areia McDiarmid (2007), Guayasamin et al. Branca, State of Sergipe, Brazil, by C.M. (2009), Castroviejo-Fisher et al. (2011), Hut- Carvalho, on 30 April 1997; MNRJ 35557, ter and Guayasamin (2012), and citations adult male collected at Fazenda Palmeiras, therein. We followed the terminology devel- Municipality of Itapebi, State of Bahia, Brazil, oped by Lynch and Ruiz-Carranza (1996) and by M.A. Freitas, on 5 September 2002. Glaw and Vences (1997) when describing Referred specimens.—Ten males (UFSE nuptial excrescences and eye coloration, 623–628, UFSE 630, and UFSE 632–634) respectively. and two females (UFSE 629 and UFSE 631) Morphometric characters followed Heyer et collected at Parque Nacional Serra de Itabai- al. (1990), Duellman (2001), and Cisneros- ana (108450S; 378200W), Municipality of Areia 300 HERPETOLOGICA [Vol. 70, No. 3

FIG. 1.—(A) Dorsal and (B) ventral views of the holotype of Vitreorana baliomma sp. nov. (MNRJ 46857; SVL ¼ 17.9 mm). (C) Lateral view of head of V. baliomma sp. nov. (MNRJ 46857, holotype; scale bar ¼ 4 mm). (D) Ventral (left) and dorsal (right) views of internal organs of the paratype of V. baliomma sp. nov. (MNRJ 37905).

Branca, State of Sergipe, Brazil, by S. Gouveia tympanum to the shoulder; (4) dorsal skin and R. Faria from May through August 2006. texture smooth; (5) cloacal ornamentation Diagnosis.—Vitreorana baliomma sp. nov. comprised of a flap above the cloacal opening can be distinguished from all other related and a patch of small tubercles around it, all and similar species by the following combina- similar in size, white pigmentation scarce and tion of characters: (1) vomerine teeth absent; only visible under magnification; (6) parietal (2) snout truncate in dorsal view, rounded in peritoneum translucent (P0 condition), irido- profile; (3) tympanum rounded, nonpigment- phores covering pericardium, hepatic perito- ed, outline barely visible, supratympanic fold neum, gall bladder, and gastrointestinal tract poorly developed around the upper portion of (V5condition;Fig.1D),peritoneumof September 2014] HERPETOLOGICA 301 urinary bladder, kidneys, and testes translu- TABLE 1.—Measurements (mm) of morphometric cent; (7) bulbous liver (H2 condition); (8) variables obtained from 16 specimens of Vitreorana baliomma sp. nov.a adult males lacking humeral spine; (9) web- þ bing formula of fingers III (1 –3 ) (1–3) IV; Standard a (10) webbing formula of toes I (1–2) (1–2–)II Variable Mean deviation Range – – (0–2 ) (1–2 ) III (1–2 ) (2–3 ) IV (2–3 )(1– SVL 19.1 1.5 16.4–21.2 2) V; (11) outer tarsal and ulnar folds slightly HL 6.7 0.5 6–7.6 visible and outlined by white pigment, visible HW 7.3 0.5 6.5–8.3 RL 3.7 0.4 3.2–4.4 only under magnification; (12) rudimentary HaL 6.2 0.4 5.6–6.8 nuptial excrescences formed by aggregation of FL 11.3 0.5 10.5–12.2 glands on dorsomedial surface of Finger I, TL 10.9 0.6 9.9–11.6 forming a poorly defined pad, with some TaL 6 0.4 5.5–6.9 FL 8.8 0.6 7.7–9.5 accessorial glands on its periphery reaching SND 1.2 0.2 0.8–1.8 the ventral surface of digit (similar to rudi- ID 2.2 0.2 1.8–2.7 mentary Type I), concealed prepollex; (13) EN 2.6 0.4 2.2–3.2 first finger longer than second; (14) eye ED 4.4 0.4 3.8–5 IOD 5.2 0.7 4.2–6.5 diameter larger than width of disc on Finger 3WD 1.5 0.3 0.9–1.9 III; (15) in life, leaf green dorsum with minute a SVL ¼ snout–vent length, HL ¼ head length, HW ¼ head width, RL ¼ white punctuations; (16) in preservative, radio–ulna length, HaL ¼ hand length, FL ¼ femur length, TL ¼ tibia length, TaL ¼ tarsal length, FL ¼ foot length, SND ¼ snout–nostril distance, ID ¼ background coloration cream, small and star- internarial distance, EN ¼ eye–nostril distance, ED ¼ eye diameter, IOD ¼ shape lavender melanophores uniformly dis- interorbital distance, and 3WD ¼ width of disc of third finger. tributed on dorsal surface; (17) in life, tunic around the eye white, iris periphery tan, iris dorsomedial surface of the first phalange in area flecked of golden melanophores, pupil the thumb—Fig. 2E,F); kidneys, urinary peripheral area tan, and horizontal halter-like bladder, and testes lacking iridophores layer dark pupil; in preservative, tunic around the (in V. eurygnatha, V. uranoscopa, and V. eye cream, iris periphery cream, iris area parvula, kidneys, urinary bladder, and testes flecked of lavender starred melanophores, white); and iris pattern flecked by lavender pupil periphery white, black and horizontal star-shape melanophores (Fig. 2G; in V. halter-like pupil; (18) hands and feet yellowish eurygnatha, V. uranoscopa, and V. parvula, green, melanophores usually absent from iris pattern is encircling black or lavender fingers and toes, when present, restricted to reticulations; Fig. 2H,I). dorsal portion of Finger IV and toes IV and V; Vitreorana baliomma sp. nov. differs from (19) small male size (Table 1). Below, we Vitreorana helenae by the absence of irido- compare the diagnostic characters of the new phores on the parietal peritoneum (in V. species against all species members of Vitre- helenae, parietal peritoneum with iridophores orana, in addition to the similar species covering anterior third); in life, dorsum Chimerella mariaelenae. uniformly leaf green with minute white Vitreorana baliomma sp. nov. is diagnosed punctuations (in V. helenae, in life, dorsum from Vitreorana species from Atlantic Forest pale lime spotted by groups of dark purple (V. eurygnatha, V. uranoscopa, and V. parvu- melanophores); bulbous liver (in V. helenae, la) by having a thin layer of iridophores trilobate liver); snout rounded in profile (in V. covering the stomach and intestines (in V. helenae, snout sloping in profile); and cloacal eurygnatha, V. uranoscopa, and V. parvula, ornamentation comprised of a patch of small iridophores are absent from stomach and tubercles, all similar in size, white pigmenta- intestines); in males, rudimentary nuptial tion scarce and visible under magnification (in excrescences formed by glands on the dorso- V. helenae, cloacal ornamentation comprised medial surface of Finger I, with some of paired, enlarged round tubercles ventral to accessorial glands along its periphery (Fig. cloacal opening). 2D; in V. eurygnatha, V. uranoscopa, and V. Thenewspeciesisdistinguishedfrom parvula, a large aggregation of glands forming Vitreorana gorzulae by the absence of irido- a defined pad covering approximately the phores on the parietal peritoneum (in V. 302 HERPETOLOGICA [Vol. 70, No. 3

FIG. 2.—Comparative images of Vitreorana species from the Atlantic Forest: (A) living amplectant pair of Vitreorana baliomma sp. nov. from Serra de Itabaiana, State of Sergipe (UFSE 630–631; photo: Sidney Gouveia); (B) nuptial pad and (C) iris detail (MNRJ 46857, holotype). (D) Male V. eurygnatha from State of Sa˜o Paulo (noncollected specimen; photo: Renato Gaiga); (E) nuptial pad and (F) iris detail (MZUSP 105231). (G) Male V. uranoscopa from Floresta da Tijuca, State of Rio de Janeiro (MNRJ 77352; photo: RP); (H) nuptial pad and (I) iris detail (MNRJ 79412). gorzulae, anterior third of parietal peritoneum cent parietal peritoneum (in V. castroviejoi, covered by iridophores); in adult males, anterior third of parietal peritoneum white); prepollex and prepollical spines absent (in by the absence of prominent prepollical adult males of V. gorzulae, prepollex enlarged bulges or projected spines (in V. castroviejoi, and prepollical spine projecting medially but prominent prepollical bulges and prepollical not exposed); first finger longer than second spines medially projected); in life, dorsum (in V. gorzulae, first finger shorter than uniformly leaf green with minute white second); absence of noticeable humeral crest punctuations (in V. castroviejoi, dorsal surfac- or spine in adult males (adult males of V. es yellow spotted); and bulbous liver (in V. gorzulae have humeral crests and nonproject- castroviejoi, lobed liver). ing spines on the humerus); and bulbous liver Vitreorana baliomma sp. nov. differs from (in V. gorzulae, trilobate liver). V. oyampiensis by the absence of iridophores Compared to Vitreorana castroviejoi, V. on the parietal peritoneum (in V. oyampiensis, baliomma sp. nov. differs in having a translu- anterior third of parietal peritoneum covered September 2014] HERPETOLOGICA 303 by iridophores); hepatic peritoneum com- Description of holotype.—Adult male, SVL pletely covered by iridophores (in V. oyam- 17.9 mm. Body moderately slender; head piensis, translucent hepatic peritoneum or length smaller than head width; HL 36.9% iridophores covering only anterior part of and HW 38% of SVL; snout truncate in dorsal liver); in adult males, absence of distinct view, rounded in profile; canthus rostralis prepollex (in V. oyampiensis, distinct prepol- indistinct, loreal region slightly concave; lex on the base of thumb); bulbous liver (in V. nostrils not protuberant, closer to the tip of oyampiensis, lobed liver); and in preservative, snout than to eye; eyes large, directed dorsum uniformly lavender or with minute anterolaterally at an angle of 458; ED 63.2% white punctuations (in V. oyampiensis, dor- of HW; supratympanic fold present, barely sum lavender with black or dark purple spots). visible around the upper portion of tympanum Vitreorana baliomma sp. nov. is distin- to the shoulder; tympanum rounded, outline guished from Vitreorana antisthenesi by slightly visible; vomerine teeth absent; pre- having, in life, uniformly leaf green dorsum maxillary and maxillary teeth present; choanae with minute white punctuations (in V. anti- large, elliptical; tongue elongated, free later- sthenesi, dorsum spotted by yellow maculae); ally and posteriorly; vocal slits short, extending males slightly smaller, SVL 16.4–21.2 mm (in laterally from the edge of tongue to the V. antisthenesi, larger males SVL 21.4–27 articulation of jaws; vocal sac single, subgular. mm); iris flecked by star-shape melanophores Arms slender, with few minute melanophores (in V. antisthenesi, iris pattern consisting of on the dorsal portion; forearm thicker than purple or lavender reticulations); in preserva- arm, with abundant melanophores on dorsal tive, upper lip nonpigmented (in V. antisthe- surface; humeral spine or crests not visible nesi, upper lip evident and highlighted by externally; ulnar ridges present, low, not white pigment); rudimentary nuptial excres- forming folds; white pigment scarce, visible cences formed by glands on the dorsomedial under magnification; relative finger lengths II surface of Finger I, with some accessorial , I , IV , III; adhesive discs expanded, glands on its periphery (in V. antisthenesi,a almost rounded, discs of Finger I and II large aggregation of glands forming a defined smaller than others, 3DW equals 8.4% of pad covering approximately the dorsomedial SVL; membrane formula on hand I vestigial II surface of the first phalange of the thumb); 2–vestigial III 2þ–1 IV. Palmar tubercle and snout rounded in profile (in V. antisthe- rounded, evident; thenar tubercle absent; nesi, snout truncate in profile). subarticular tubercles simple, rounded; super- Vitreorana baliomma sp. nov. is diagnosed numerary tubercles on the palmar surface from Chimerella mariaelenae by the absence barely noticeable; nuptial excrescences consist of humeral spine in males (in males of C. of a small aggregation of nonkeratinized mariaelenae, humeral spine prominent); in glands on dorsomedial surface of Finger I, life, dorsum uniform green or with small white pale or cream colored, forming an underde- punctuations (in C. mariaelenae, dorsum pale veloped pad, with some accessorial glands on green with dark macules); in males, rudimen- its periphery reaching the ventrolateral sur- tary nuptial excrescences formed by glands on face of the digit (similar to rudimentary Type the dorsomedial surface of Finger I, with I); prepollex concealed. Legs slender, long; some accessorial glands along its periphery (in FL 59.2% of SVL and TL 56.4% of SVL; outer males of C. mariaelenae, nuptial pad com- tarsal and foot ridges present, not forming prised of a large cluster of glands on folds, white pigment slightly visible under dorsomedial surface of Finger I), and cloacal magnification; relative toe lengths I . II . III ornamentation comprised of a flap above the ‹ V . IV; adhesive discs of toes rounded, Toe cloacal opening and a patch of small tubercles I smallest, Toe II small, the others medium- around it, all similar in size, white pigmenta- sized; webbing formula I 2–2 II 1þ–2 III 11/3– tion scarce and only visible under magnifica- 2þ IV 2þ–1 V; outer tarsal tubercle absent; tion (in C. mariaelenae, cloacal ornamentation inner metatarsal tubercle elongated, weakly comprised of a pair of large, round, flat developed, equivalent to one sixth of Toe I; tubercles on ventral surfaces of thighs). subarticular tubercles simple, small, rounded; 304 HERPETOLOGICA [Vol. 70, No. 3 supernumerary tubercles absent. Cloacal or- metric variation is summarized in Table 1. namentation composed of a dorsal flap, and a Gouveia et al. (2012) observed that females patch of small tubercles around the cloacal (SVL ¼ 20.55 6 0.8 mm; n ¼ 6) are larger than opening, all similar in size; white pigmentation males (SVL ¼ 18.18 6 0.6 mm; n ¼ 6). scarce, visible under magnification. Dorsal Etymology.—The specific epithet baliomma surfaces smooth; gular region and ventral is a feminine adjective derived from the Greek portion of upper limbs smooth; venter and nouns Balios meaning ‘‘spotted’’ and Omma ventral surface of hind limbs slightly granular meaning ‘‘eye.’’ The name of this new species with small rounded granules, all of similar refers to the distinctive punctuated pattern on size. the iris, unique among the Vitreorana species Measurements of holotype (in mm).—SVL described from the Atlantic Forest. 17.9; HL 6.6; HW 6.8; RL 3.2; HL 6.8; FL Distribution.—Vitreorana baliomma is 10.6; TL 10.1; TaL 5.5; FL 8.9; SND 1.4; ID known from the northern portion of the 2.7; EN 2.3; ED 4.3; IOD 6.0; 3WD 1.5. Atlantic Forest biome, in ombrophilous for- Color of holotype in preservative.—Dorsal mations (sensu Veloso et al., 1991). In background cream; a few minute, lavender, addition to type-locality, the new species has star-shaped melanophores concentrated on been collected in Municipality of Itapebi, orbital region and uniformly distributed on State of Bahia, and in Parque Nacional da other dorsal surfaces of head, dorsum, and Serra de Itabaiana, Municipality of Areia limbs. Tunic around the eye cream, iris Branca, State of Sergipe (Fig. 3). The new periphery cream, iris area flecked of lavender species is allopatric from other members of starred melanophores, pupil periphery white, Vitreorana, except V. eurygnatha, with which black and horizontal halter-like pupil; ventral it is sympatric in southern Bahia. However, surfaces cream, immaculate. Internal organs our data do not allow us to infer syntopic pigmented white and visible through trans- localities between these species. parent skin (heart, liver, and gastrointestinal Natural history.—The type-locality is a tract). forested fragment with strong anthropogenic Color in life.—Our description is based on a influence. Much of the original vegetation has photo of amplectant pair (UFSE 630–631; Fig. 2A) from Serra de Itabaiana, State of been selectively removed for cacao cultivation. Sergipe. Dorsal surfaces leaf green punctuat- In cacao plantations, sporadic emergent trees ed by sparse white dots; flanks, hands, and are preserved to shade the understory cacao ‘‘ ’’ feet light green with yellowish shades. Upper plants (a pattern locally known as cabruca ; lip, outer tarsal and ulnar ridges outlined by Canedo et al., 2004). Males of V. baliomma sp. white pigment; tunic around the eye white, nov. were observed vocalizing perched on iris periphery tan, iris area flecked of golden vegetation along a permanent creek at cab- melanophores, pupil peripheral area tan, and rucas. On one occasion, 5–6 males were horizontal halter-like black pupil. Ventral observed vocalizing at heights from 1 to 1.8 surfaces light green, allowing the visualization m above the water, on upper surfaces of leaves of internal organs (pericardium, liver, and (C. Canedo, personal communication). gastrointestinal tract) pigmented in white by Gouveia et al. (2012) provided ecological an iridophore layer visible through skin. data for the population of Serra de Itabaiana Variation.—Two analyzed specimens from (referred to as Vitreorana aff. eurygnatha). Serra de Itabaiana show the iris and dorsal According to those authors, V. baliomma sp. coloration of melanophores gray instead of nov. occurs in clumped distributions along lavender. Also, the ventral region is more streams, forming groups of 2–4 individuals. translucent than the other specimens exam- Perched males call from dorsal surfaces of ined. We attributed these differences to leaves of riverine understory from 0.3 to 4 m excessive light exposure. Furthermore, three in height. Amplectant pairs deposited egg well-preserved specimens from Serra de clutches (10–25 eggs) preferentially on upper Itabaiana show white dots distributed along surfaces of leaves; however, egg masses were dorsum visible under magnification. Morpho- also observed on lower surfaces. September 2014] HERPETOLOGICA 305

FIG. 3.—Geographic distribution of Vitreorana baliomma sp. nov. in Brazil (shaded area of inset). Star ¼ type-locality; shaded squares ¼ additional localities of occurrence of V. baliomma sp. nov.

Remarks.—We tentatively assign the new thus corroborating the placement of V. species to the genus Vitreorana because it baliomma sp. nov. in this genus. exhibits most of diagnostic traits for the genus, as semisolid iridophores layer on liver and DISCUSSION gastrointestinal tract visible by transparency, Prior to this study, all species of glass frogs green bones in life, lavender coloration in from the Atlantic Forest shared a condition of preservative (see Guayasamin et al., 2009). an iridophore layer that covers the pericardi- Currently, this genus is defined by ambiguous um, liver, urinary bladder, kidneys, and testes; morphological synapomorphies and lacks a and is absent from the stomach and intestines. more detailed morphologic definition within As described here, however, V. baliomma Centrolenidae, making the assignment of the presents a different pattern, where irido- genus without molecular evidence difficult. phores cover the pericardium, liver, stomach, The interpretations of these ambiguous traits and intestines, and are absent from the could support the insertion of this new species urinary bladder, kidneys, and testes (similar in the genus Teratohyla or Chimerella. Based to the pattern described for V. gorzulae). To on biogeographical affinities, however, we date, general external and internal morpho- prefer to keep this new species in the genus logical features suggest that V. baliomma Vitreorana until new studies emerge assessing resembles congeneric species from the Cor- the molecular data set of V. baliomma sp. dillera de la Costa in Venezuela, Guiana nov., or improve the morphological charac- Shield, and the Amazonian basin, and prob- terization of higher taxa of Centrolenidae, ably is sister to V. gorzulae. We encourage 306 HERPETOLOGICA [Vol. 70, No. 3 future researchers to investigate the phyloge- presence of this species in other forest netic relationships of glass frogs in order to fragments. clarify the position of the new species within Since the works of Taylor and Cochran Vitreorana and Centrolenidae. (1953) and Heyer (1978, 1985), Atlantic Glass frogs exhibit a wide diversity of Forest glass frogs have not been the main nuptial excrescences that have been studied focus of any published study dealing with by many researchers (Flores, 1985; Lynch and Centrolenidae. In view of newly collected Ruiz-Carranza, 1996; Cisneros-Heredia and specimens, the description of V. baliomma sp. McDiarmid, 2007). Most Brazilian glass frogs nov. highlights the need for more studies were neglected in these studies, however, and assessing the systematics of Vitreorana from few descriptions are available for their nuptial Atlantic Forest in Brazil and Argenti- excrescences, as well as any ontogenetic shifts, na in order to clarify the taxonomic status of or intra- and interspecific variation, in this populations, the species relationships within trait. Flores (1985) and Lynch and Ruiz- the genus, and to provide an improved Carranza (1996) referred to a reduced or morphological characterization of currently rudimentary type of nuptial pad for Atlantic recognized species. Forest glass frogs underlying Type I and Type Acknowledgments.—We thank M. Rada and S. Cas- II, informally named as rudimentary or troviejo-Fisher for their suggested improvements to an reduced Type I, which we attribute to V. earlier version of this manuscript; C. Hutter for his baliomma, despite the presence of some feedback and linguistic revision; G. Bittencourt and F. Glaw for photographs of the lectotype of V. parvula and of accessorial glands along ventrolateral base of the holotype of V. uranoscopa, respectively; S. Gouveia thumb (see Fig. 2D). Notwithstanding, all and R. Gaiga for their photos of live V. baliomma and V. examined specimens of V. uranoscopa and V. eurygnatha, respectively; and C.F.B. Haddad, C. Mello, eurygnatha show different nuptial excrescenc- H. Zaher, and R. Faria for loan or permission to examine specimens under their care. RP thanks the Coordena¸ca˜o es (Fig. 2E,H), forming a densely packed pad de Aperfei¸coamento de Pessoal de Nıvel´ Superior which covers almost the entire surface of the (CAPES) for scholarship grants; UC and JPPJ acknowl- first phalange in the thumb; thus fitting in the edge the Conselho Nacional de Desenvolvimento typical Type I nuptial excrescence, following Cientıfico´ e Tecnologico´ (CNPq) and Funda¸ca˜o Carlos Flores (1985) and Lynch and Ruiz-Carranza Chagas Filho de Amparo a` Pesquisa do Estado do Rio de Janeiro (FAPERJ) for financial support. (1996). Still, most of classifications proposed for nuptial excrescences of Centrolenidae lack a comprehensive survey of all taxa within the LITERATURE CITED clade (Flores, 1985; Lynch and Ruiz-Carran- Boulenger, G.A. 1895. Third report on additions to the batrachians collections in the Natural History Museum. za, 1996; Cisneros-Heredia and McDiarmid, Proceedings of the Zoological Society of London 4:640– 2007). Further studies should consider the 646. external morphology of nuptial excrescences Canedo, C., M. Dixo, and J.P. Pombal, Jr. 2004. A new in Centrolenidae, in addition to using other species of Chiasmocleis Mehely,´ 1904 (Anura, Micro- hylidae) from the Atlantic Rainforest of Bahia, Brazil. approaches, such as micro-ornamentation, Herpetologica 60:495–501. histological, and glandular surveys. These Carvalho, C.M., J.C. Vilar, and F.F. Oliveira. 2005. approaches have been useful for other anuran Repteis´ e anfıbios.´ Pp. 39–61 In C.M. Carvalho and groups (e.g., Luna et al., 2012). J.C. Vilar (Eds.), Parque Nacional da Serra de Itabaiana—Levantamento da Biota. IBAMA Biologia Several studies assessing vertebrate diversi- Geral e Experimental—UFS, Brazil. ty of the Atlantic Forest biome indicate an Castroviejo-Fisher, S., C. Vila´, J. Ayarzaguena, ¨ M. Blanc, intricate pattern of endemism, which can be and R. Ernst. 2011. Species diversity of Hyalinoba- separated latitudinally and longitudinally trachium glassfrog (Amphibia: Centrolenidae) from the Guiana Shield, with description of two new species. along climatic conditions, vegetation, and Zootaxa 3132:1–55. geographical formations (Costa, 2003; Santos Cisneros-Heredia, D.F., and R.W. McDiarmid. 2007. et al., 2007; Silva et al., 2012). Therefore, V. Revision of the characters of Centrolenidae (Amphibia: baliomma might have a geographic distribu- Anura: Athesphatanura), with comments on its taxon- omy and the description of new taxa of glassfrogs. tion that is constrained to the northern portion Zootaxa 1572:1–82. of the Atlantic Forest. Increased sampling Costa, L.P. 2003. 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Guayasamin. 2012. A new cryptic Bonito, PARNA Serra da Bocaina, Municipality of Sa˜o species of glassfrog (Centrolenidae: Nymphargus) from Jose´ do Barreiro; MZUSP 105224–105231 Campo de Reserva Las Gralarias, Ecuador. Zootaxa 3257:1–21. Fruticultura, Municipality of Sa˜o Jose´ do Barreiro; MNRJ Luna, M.C., C. Taboada, D. Baeta,ˆ and J. Faivovich. 2012. 17649, CFBH 269, 362, 1854 Fazendinha Sa˜oLuıs,´ Structural diversity of nuptial pads in Phyllomedusinae Municipality of Ribeira˜o Branco; MNRJ 34758 Esta¸ca˜o (Amphibia: Anura: Hylidae). Journal of Morphology ´ ´ 273:712–714. Biologica de Paranapiacaba, Municipality of Santo Andre; Lutz, A. 1925. Batraciens du Bresil.´ Comptes Rendus des MZUSP 53052–53059 Fazenda do Veado, Municipality of Sceances´ de la Societe´ de Biologie et de Ses Filiales, Bananal; MZUSP 15153–15180 Cidade Azul, Municipality Paris 93:137–139. of Joanopolis;´ MZUSP 104856–104867, 105399–105402 308 HERPETOLOGICA [Vol. 70, No. 3

Fazenda Lagoinha da Serra, Municipality of Campos do 30606–30607 Serrinha, Municipality of Mariana; MNRJ Jorda˜o. Rio de Janeiro: MNRJ 2178, 73107, 73162, 23125 Mata da Mutuca, Municipality of Nova Lima; MZUSP 53350–53357 Municipality of Teresopolis;´ MNRJ MNRJ 24688 Esta¸ca˜oBiologica´ Mata do Sossego, 32872 Represa do Guinle, Municipality of Teresopolis;´ Municipality of Simonesia.´ Rio de Janeiro: MNRJ MNRJ 52690–52692, 73166, PARNA Serra dos Orga´ ˜os, 78040–78043 Lıdice,´ Municipality of Rio Claro; CFBH Municipality of Teresopolis;´ MNRJ 78575 Municipality of 19256, 19279 PARNA Serra da Bocaina; MNRJ 73012 Petropolis;´ MNRJ 73163–73165, 73422 Municipality of Parque Natural Municipal da Taquara, Municipality of Itatiaia; MNRJ 51575 Macieiras, PARNA Itatiaia, Munic- Duque de Caxias; MNRJ 32873, 72450, 75389–75390, ipality of Itatiaia; MNRJ 51801–51810, 52699–52701, PARNA Itatiaia, Municipality of Itatiaia; MNRJ Represa 73128–73134 Tijuca, Municipality of Rio de Janeiro. do Guinle, Municipality of Teresopolis;´ MNRJ 46680, Vitreorana uranoscopa.—Brazil: Santa Catarina: 64815–64816, 77352–77362, PARNA Tijuca, Municipality MZUSP 35429–35436 Municipality of Novo Horizonte; of Rio de Janeiro. Sa˜o Paulo: MZUSP 104892–104895, CFBH 5280–5282, 5284 Bairro Len¸col, Municipality of CFBH 869, 1528, Paranapiacaba, Municipality of Santo Sa˜o Bento do Sul. Minas Gerais: CFBH 16534 Pousada Andre;´ MZUSP 136535–136537 Parque Estadual Carlos Floresta, Municipality of Itamonte; MZUSP 135659, Botelho, Municipality of Sa˜o Miguel Arcanjo; MNRJ 133838, PARNA Caparao,´ Municipality of Vale Verde; 63951–63954 Rubia˜oJunior,´ Municipality of Botucatu; MZUSP 145472 Municipality of Concei¸ca˜o do Mato MNRJ 32510–32511 Estrada de Botucatu, Municipality of Dentro; MNRJ 56300, 77778–77780 Ponte para o Botucatu; CFBH 2252 Picinguaba, Municipality of Belchior, Reserva Particular do Patrimonioˆ Natural da Ubatuba; CFBH 6208 Nucleo´ Santa Virgınia,´ PESM, Serra do Cara¸ca, Municipality of Catas Altas; MNRJ Municipality of Sa˜oLuıs´ do Paraitinga.