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

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Herpetologica, 70(3), 2014, 298–308� 2014 by The Herpetologists’ League, Inc.

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

RAFAEL PONTES1, 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 species of glass frog (Vitreorana) from Fazenda Novo Pau Brasil, in theAtlantic Forest habitat of northeastern Brazil. Previous to this work, Vitreorana baliomma sp. nov. wasmisidentified as V. eurygnatha, from which it can be distinguished by the iris pattern flecked with star-shapemelanophores; 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 peritoneatranslucent; 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: Centroleninae; Cochranellini; Eye coloration; Nuptial excrescences; Peritoneum; Vitreoranabaliomma sp. nov.

FOR DECADES, members of the Neotropicalfamily Centrolenidae (Taylor, 1951), com-monly known as glass frogs, have attractedthe attention of scientists because of theirconspicuous biological and morphologicalfeatures (Cisneros Heredia and McDiarmid,2007). This clade comprises about 150 spe-cies, most of which inhabit the vegetationalong streams in forested areas (Guayasaminet al., 2009; Frost, 2013). The family is foundthroughout Central America, tropical Andes,Guiana Shield, and the Amazon basin, and adisjoint group occurs in the Atlantic Forest,from southeastern Brazil to Argentina (Heyer,1985; Guayasamin et al., 2009; Castroviejo-Fisher et al., 2011).

Recently, the phylogenetic relationships andsystematics of glass frogs have been the focusof various studies, culminating in severaltaxonomic changes (e.g., Cisneros-Herediaand McDiarmid, 2007; Guayasamin et al.,2008, 2009). Although recent studies (e.g.,Castroviejo-Fisher et al., 2011; Hutter andGuayasamin, 2012) have resolved some taxo-nomic problems, several issues need to beclarified at the alpha taxonomic level (Cis-neros-Heredia and McDiarmid, 2007; Castro-viejo-Fisher et al., 2011).

Of these issues, the three species ofVitreorana known to occur in the Atlantic

Forest—Vitreorana parvula (Boulenger,1895), Vitreorana uranoscopa (Muller, 1924),and Vitreorana eurygnatha (Lutz, 1925)—persist obscured. This group remains unclar-ified because of the scarcity of recenttaxonomic studies and lack of refined analysisof morphological characters (Cisneros-Hered-ia and McDiarmid, 2007). These species havebeen placed in the genus Vitreorana, amonophyletic clade informed from molecularevidence, which accommodates species fromthe Cordillera de la Costa in Venezuela, thePrecambrian Shields of South America, theAmazon basin, and the Atlantic Forest domain(Guayasamin et al., 2009). Vitreorana ischaracterized by the following phenotypiccharacters: (1) white peritoneum covering,totally or partially, the liver; (2) whitegastrointestinal peritoneum; (3) green bonesin life; (4) a lavender dorsal coloration inpreservative; and (5) eggs deposited on theupper or under side of leaves (Guayasamin etal., 2009). Using only morphology, however,this genus cannot be diagnosed from othercentrolenid genera, as Chimerella.

Studies addressing taxonomic questions onglass frogs from the Atlantic Forest biomewere generally based on few specimensavailable from limited localities from thesoutheastern and southern portions of thatregion (Taylor and Cochran, 1953; Heyer,1978, 1985). Recently, field collections pro-duced range extensions for glass frogs, report-ing occurrence for northeastern fragments of

1 CORRESPONDENCE: email, rafaelcunhapontes@hotmail.com

298

this biome (Freitas et al., 2004; Carvalho et al.,2005; Freitas et al., 2007; Gouveia et al.,2012); however, because of the lack ofmorphological information, the taxonomicstatus of these populations remains unclear(Gouveia et al., 2012).

Herein, we examine aforementioned col-lected specimens from the northern portion ofthe Atlantic Forest and describe a new speciesof Vitreorana, previously assigned to V.eurygnatha. In addition, we provide a briefdiscussion on the morphological affinitieswithin Vitreorana and standardizations onnuptial excrescences in Centrolenidae.

MATERIALS AND METHODS

Nomenclature and Conventions

Museum acronyms follow those establishedby the ASIH (http://www.asih.org/codons.pdf); in addition, the following collectionswere examined: Colecao Celio F.B. Haddad,Departamento de Zoologia, I.B., UniversidadeEstadual Paulista, Rio Claro, Brazil (CFBH);Colecao Adolpho Lutz, housed at the MuseuNacional, Rio de Janeiro, Brazil (AL-MN);Colecao da Universidade Federal de Sergipe,Aracaju, Brazil (UFSE). We also examinedphotos of the holotype of Vitreorana urano-scopa (ZSM 81/1921) and the lectotype of V.parvula (BMNH 88.2.7.32). Specimens of thenew species were fixed in 10% formalinsolution and preserved in 70% alcohol (Ap-pendix). Sex and maturity were determined bysecondary sexual characteristics (nuptial ex-crescences, vocal sacs, and slits) and theobservation of convoluted oviducts throughthe transparent ventral skin.

Morphology

Characters followed the descriptions ofLynch and Duellman (1973), Ruiz-Carranzaand Lynch (1991), Cisneros-Heredia andMcDiarmid (2007), Guayasamin et al.(2009), Castroviejo-Fisher et al. (2011), Hut-ter and Guayasamin (2012), and citationstherein. We followed the terminology devel-oped by Lynch and Ruiz-Carranza (1996) andGlaw and Vences (1997) when describingnuptial excrescences and eye coloration,respectively.

Morphometric characters followed Heyer etal. (1990), Duellman (2001), and Cisneros-

Heredia and McDiarmid (2007). We obtainednine measurements using digital calipers(60.1 mm): (1) snout–vent length (SVL), (2)head length (HL), (3) head width (HW), (4)radio–ulna length (RL), (5) hand length(HaL), (6) femur length (FL), (7) tibia length(TL), (8) tarsal length (TaL), and (9) footlength (FL). With the use of a stereoscopicmicroscope, we obtained seven additionalmorphometric variables (60.05 mm): (10)snout–nostril distance (SND), (11) internarialdistance (ID), (12) eye–nostril distance (EN),(14) eye diameter (ED), (15) interorbitaldistance (IOD), and (16) width of disc ofthird finger (3WD). All morphometric datafrom preserved specimens were measured byRP and reported as minimum–maximum(mean 6 standard deviation).

SPECIES DESCRIPTION

Vitreorana baliomma sp. nov.(Figs. 1A–C; 2D,G)

Hyalinobatrachium sp. (cf. eurygnathum).—Carvalho et al. (2005: 51).

Hyalinobatrachium eurygnathum.—Freitas etal. (2004: 281).

Vitreorana aff. eurygnatha.—Gouveia et al.(2012: 16).

Holotype.—MNRJ 46857, adult male col-lected at Mata de Cabruca, Fazenda NovoPau Brasil (16859022"S; 39834058"W; 98 mabove sea level (a.s.l.); datum ¼ WGS84),Municipality of Itamaraju, State of Bahia,Brazil, by C. Canedo and F. Falcao, on 2February 2007.

Paratypes.—MNRJ 37904 and 37905(cleared and stained), two adult males collect-ed at Parque Nacional Serra de Itabaiana(10845 0S; 37820 0W), Municipality of AreiaBranca, State of Sergipe, Brazil, by C.M.Carvalho, on 30 April 1997; MNRJ 35557,adult male collected at Fazenda Palmeiras,Municipality of Itapebi, State of Bahia, Brazil,by M.A. Freitas, on 5 September 2002.

Referred specimens.—Ten males (UFSE623–628, UFSE 630, and UFSE 632–634)and two females (UFSE 629 and UFSE 631)collected at Parque Nacional Serra de Itabai-ana (108450S; 378200W), Municipality of Areia

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Branca, State of Sergipe, Brazil, by S. Gouveiaand R. Faria from May through August 2006.

Diagnosis.—Vitreorana baliomma sp. nov.can be distinguished from all other relatedand similar species by the following combina-tion of characters: (1) vomerine teeth absent;(2) snout truncate in dorsal view, rounded inprofile; (3) tympanum rounded, nonpigment-ed, outline barely visible, supratympanic foldpoorly developed around the upper portion of

tympanum to the shoulder; (4) dorsal skintexture smooth; (5) cloacal ornamentationcomprised of a flap above the cloacal openingand a patch of small tubercles around it, allsimilar in size, white pigmentation scarce andonly visible under magnification; (6) parietalperitoneum translucent (P0 condition), irido-phores covering pericardium, hepatic perito-neum, gall bladder, and gastrointestinal tract(V5 condition; Fig. 1D), peritoneum of

FIG. 1.—(A) Dorsal and (B) ventral views of the holotype of Vitreorana baliomma sp. nov. (MNRJ 46857; SVL¼ 17.9mm). (C) Lateral view of head of V. baliomma sp. nov. (MNRJ 46857, holotype; scale bar¼4 mm). (D) Ventral (left) anddorsal (right) views of internal organs of the paratype of V. baliomma sp. nov. (MNRJ 37905).

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urinary bladder, kidneys, and testes translu-cent; (7) bulbous liver (H2 condition); (8)adult males lacking humeral spine; (9) web-bing formula of fingers III (1þ–3�) (1–3) IV;(10) webbing formula of toes I (1–2�) (1–2–) II(0–2�) (1–2–) III (1–2�) (2–3�) IV (2–3�) (1––2�) V; (11) outer tarsal and ulnar folds slightlyvisible and outlined by white pigment, visibleonly under magnification; (12) rudimentarynuptial excrescences formed by aggregation ofglands on dorsomedial surface of Finger I,forming a poorly defined pad, with someaccessorial glands on its periphery reachingthe ventral surface of digit (similar to rudi-mentary Type I), concealed prepollex; (13)first finger longer than second; (14) eyediameter larger than width of disc on FingerIII; (15) in life, leaf green dorsum with minutewhite punctuations; (16) in preservative,background coloration cream, small and star-shape lavender melanophores uniformly dis-tributed on dorsal surface; (17) in life, tunicaround the eye white, iris periphery tan, irisarea flecked of golden melanophores, pupilperipheral area tan, and horizontal halter-likedark pupil; in preservative, tunic around theeye cream, iris periphery cream, iris areaflecked of lavender starred melanophores,pupil periphery white, black and horizontalhalter-like pupil; (18) hands and feet yellowishgreen, melanophores usually absent fromfingers and toes, when present, restricted todorsal portion of Finger IV and toes IV and V;(19) small male size (Table 1). Below, wecompare the diagnostic characters of the newspecies against all species members of Vitre-orana, in addition to the similar speciesChimerella mariaelenae.

Vitreorana baliomma sp. nov. is diagnosedfrom Vitreorana species from Atlantic Forest(V. eurygnatha, V. uranoscopa, and V. parvu-la) by having a thin layer of iridophorescovering the stomach and intestines (in V.eurygnatha, V. uranoscopa, and V. parvula,iridophores are absent from stomach andintestines); in males, rudimentary nuptialexcrescences formed by glands on the dorso-medial surface of Finger I, with someaccessorial glands along its periphery (Fig.2D; in V. eurygnatha, V. uranoscopa, and V.parvula, a large aggregation of glands forminga defined pad covering approximately the

dorsomedial surface of the first phalange inthe thumb—Fig. 2E,F); kidneys, urinarybladder, and testes lacking iridophores layer(in V. eurygnatha, V. uranoscopa, and V.parvula, kidneys, urinary bladder, and testeswhite); and iris pattern flecked by lavenderstar-shape melanophores (Fig. 2G; in V.eurygnatha, V. uranoscopa, and V. parvula,iris pattern is encircling black or lavenderreticulations; Fig. 2H,I).

Vitreorana baliomma sp. nov. differs fromVitreorana helenae by the absence of irido-phores on the parietal peritoneum (in V.helenae, parietal peritoneum with iridophorescovering anterior third); in life, dorsumuniformly leaf green with minute whitepunctuations (in V. helenae, in life, dorsumpale lime spotted by groups of dark purplemelanophores); bulbous liver (in V. helenae,trilobate liver); snout rounded in profile (in V.helenae, snout sloping in profile); and cloacalornamentation comprised of a patch of smalltubercles, all similar in size, white pigmenta-tion scarce and visible under magnification (inV. helenae, cloacal ornamentation comprisedof paired, enlarged round tubercles ventral tocloacal opening).

The new species is distinguished fromVitreorana gorzulae by the absence of irido-phores on the parietal peritoneum (in V.

TABLE 1.—Measurements (mm) of morphometricvariables obtained from 16 specimens of Vitreoranabaliomma sp. nov.a

Variablea MeanStandarddeviation Range

SVL 19.1 1.5 16.4–21.2HL 6.7 0.5 6–7.6HW 7.3 0.5 6.5–8.3RL 3.7 0.4 3.2–4.4HaL 6.2 0.4 5.6–6.8FL 11.3 0.5 10.5–12.2TL 10.9 0.6 9.9–11.6TaL 6 0.4 5.5–6.9FL 8.8 0.6 7.7–9.5SND 1.2 0.2 0.8–1.8ID 2.2 0.2 1.8–2.7EN 2.6 0.4 2.2–3.2ED 4.4 0.4 3.8–5IOD 5.2 0.7 4.2–6.53WD 1.5 0.3 0.9–1.9

a SVL ¼ snout–vent length, HL ¼ head length, HW ¼ head width, RL ¼radio–ulna length, HaL¼ hand length, FL¼ femur length, TL¼ tibia length,TaL ¼ tarsal length, FL ¼ foot length, SND ¼ snout–nostril distance, ID ¼internarial distance, EN ¼ eye–nostril distance, ED ¼ eye diameter, IOD ¼interorbital distance, and 3WD ¼ width of disc of third finger.

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gorzulae, anterior third of parietal peritoneumcovered by iridophores); in adult males,prepollex and prepollical spines absent (inadult males of V. gorzulae, prepollex enlargedand prepollical spine projecting medially butnot exposed); first finger longer than second(in V. gorzulae, first finger shorter thansecond); absence of noticeable humeral crestor spine in adult males (adult males of V.gorzulae have humeral crests and nonproject-ing spines on the humerus); and bulbous liver(in V. gorzulae, trilobate liver).

Compared to Vitreorana castroviejoi, V.baliomma sp. nov. differs in having a translu-

cent parietal peritoneum (in V. castroviejoi,anterior third of parietal peritoneum white);by the absence of prominent prepollicalbulges or projected spines (in V. castroviejoi,prominent prepollical bulges and prepollicalspines medially projected); in life, dorsumuniformly leaf green with minute whitepunctuations (in V. castroviejoi, dorsal surfac-es yellow spotted); and bulbous liver (in V.castroviejoi, lobed liver).

Vitreorana baliomma sp. nov. differs fromV. oyampiensis by the absence of iridophoreson the parietal peritoneum (in V. oyampiensis,anterior third of parietal peritoneum covered

FIG. 2.—Comparative images of Vitreorana species from the Atlantic Forest: (A) living amplectant pair of Vitreoranabaliomma sp. nov. from Serra de Itabaiana, State of Sergipe (UFSE 630–631; photo: Sidney Gouveia); (B) nuptial padand (C) iris detail (MNRJ 46857, holotype). (D) Male V. eurygnatha from State of Sao Paulo (noncollected specimen;photo: Renato Gaiga); (E) nuptial pad and (F) iris detail (MZUSP 105231). (G) Male V. uranoscopa from Floresta daTijuca, State of Rio de Janeiro (MNRJ 77352; photo: RP); (H) nuptial pad and (I) iris detail (MNRJ 79412).

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by iridophores); hepatic peritoneum com-pletely covered by iridophores (in V. oyam-piensis, translucent hepatic peritoneum oriridophores covering only anterior part ofliver); in adult males, absence of distinctprepollex (in V. oyampiensis, distinct prepol-lex on the base of thumb); bulbous liver (in V.oyampiensis, lobed liver); and in preservative,dorsum uniformly lavender or with minutewhite punctuations (in V. oyampiensis, dor-sum lavender with black or dark purple spots).

Vitreorana baliomma sp. nov. is distin-guished from Vitreorana antisthenesi byhaving, in life, uniformly leaf green dorsumwith minute white punctuations (in V. anti-sthenesi, dorsum spotted by yellow maculae);males slightly smaller, SVL 16.4–21.2 mm (inV. antisthenesi, larger males SVL 21.4–27mm); iris flecked by star-shape melanophores(in V. antisthenesi, iris pattern consisting ofpurple or lavender reticulations); in preserva-tive, upper lip nonpigmented (in V. antisthe-nesi, upper lip evident and highlighted bywhite pigment); rudimentary nuptial excres-cences formed by glands on the dorsomedialsurface of Finger I, with some accessorialglands on its periphery (in V. antisthenesi, alarge aggregation of glands forming a definedpad covering approximately the dorsomedialsurface of the first phalange of the thumb);and snout rounded in profile (in V. antisthe-nesi, snout truncate in profile).

Vitreorana baliomma sp. nov. is diagnosedfrom Chimerella mariaelenae by the absenceof humeral spine in males (in males of C.mariaelenae, humeral spine prominent); inlife, dorsum uniform green or with small whitepunctuations (in C. mariaelenae, dorsum palegreen with dark macules); in males, rudimen-tary nuptial excrescences formed by glands onthe dorsomedial surface of Finger I, withsome accessorial glands along its periphery (inmales of C. mariaelenae, nuptial pad com-prised of a large cluster of glands ondorsomedial surface of Finger I), and cloacalornamentation comprised of a flap above thecloacal opening and a patch of small tuberclesaround it, all similar in size, white pigmenta-tion scarce and only visible under magnifica-tion (in C. mariaelenae, cloacal ornamentationcomprised of a pair of large, round, flattubercles on ventral surfaces of thighs).

Description of holotype.—Adult male, SVL17.9 mm. Body moderately slender; headlength smaller than head width; HL 36.9%and HW 38% of SVL; snout truncate in dorsalview, rounded in profile; canthus rostralisindistinct, loreal region slightly concave;nostrils not protuberant, closer to the tip ofsnout than to eye; eyes large, directedanterolaterally at an angle of 458; ED 63.2%of HW; supratympanic fold present, barelyvisible around the upper portion of tympanumto the shoulder; tympanum rounded, outlineslightly visible; vomerine teeth absent; pre-maxillary and maxillary teeth present; choanaelarge, elliptical; tongue elongated, free later-ally and posteriorly; vocal slits short, extendinglaterally from the edge of tongue to thearticulation of jaws; vocal sac single, subgular.Arms slender, with few minute melanophoreson the dorsal portion; forearm thicker thanarm, with abundant melanophores on dorsalsurface; humeral spine or crests not visibleexternally; ulnar ridges present, low, notforming folds; white pigment scarce, visibleunder magnification; relative finger lengths II, I , IV , III; adhesive discs expanded,almost rounded, discs of Finger I and IIsmaller than others, 3DW equals 8.4% ofSVL; membrane formula on hand I vestigial II2–vestigial III 2þ–1� IV. Palmar tuberclerounded, evident; thenar tubercle absent;subarticular tubercles simple, rounded; super-numerary tubercles on the palmar surfacebarely noticeable; nuptial excrescences consistof a small aggregation of nonkeratinizedglands on dorsomedial surface of Finger I,pale or cream colored, forming an underde-veloped pad, with some accessorial glands onits periphery reaching the ventrolateral sur-face of the digit (similar to rudimentary TypeI); prepollex concealed. Legs slender, long;FL 59.2% of SVL and TL 56.4% of SVL; outertarsal and foot ridges present, not formingfolds, white pigment slightly visible undermagnification; relative toe lengths I . II . III‹ V . IV; adhesive discs of toes rounded, ToeI smallest, Toe II small, the others medium-sized; webbing formula I 2–2� II 1þ–2 III 11/3–2þ IV 2þ–1 V; outer tarsal tubercle absent;inner metatarsal tubercle elongated, weaklydeveloped, equivalent to one sixth of Toe I;subarticular tubercles simple, small, rounded;

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supernumerary tubercles absent. Cloacal or-namentation composed of a dorsal flap, and apatch of small tubercles around the cloacalopening, all similar in size; white pigmentationscarce, visible under magnification. Dorsalsurfaces smooth; gular region and ventralportion of upper limbs smooth; venter andventral surface of hind limbs slightly granularwith small rounded granules, all of similarsize.

Measurements of holotype (in mm).—SVL17.9; HL 6.6; HW 6.8; RL 3.2; HL 6.8; FL10.6; TL 10.1; TaL 5.5; FL 8.9; SND 1.4; ID2.7; EN 2.3; ED 4.3; IOD 6.0; 3WD 1.5.

Color of holotype in preservative.—Dorsalbackground cream; a few minute, lavender,star-shaped melanophores concentrated onorbital region and uniformly distributed onother dorsal surfaces of head, dorsum, andlimbs. Tunic around the eye cream, irisperiphery cream, iris area flecked of lavenderstarred melanophores, pupil periphery white,black and horizontal halter-like pupil; ventralsurfaces cream, immaculate. Internal organspigmented white and visible through trans-parent skin (heart, liver, and gastrointestinaltract).

Color in life.—Our description is based on aphoto of amplectant pair (UFSE 630–631;Fig. 2A) from Serra de Itabaiana, State ofSergipe. Dorsal surfaces leaf green punctuat-ed by sparse white dots; flanks, hands, andfeet light green with yellowish shades. Upperlip, outer tarsal and ulnar ridges outlined bywhite pigment; tunic around the eye white,iris periphery tan, iris area flecked of goldenmelanophores, pupil peripheral area tan, andhorizontal halter-like black pupil. Ventralsurfaces light green, allowing the visualizationof internal organs (pericardium, liver, andgastrointestinal tract) pigmented in white byan iridophore layer visible through skin.

Variation.—Two analyzed specimens fromSerra de Itabaiana show the iris and dorsalcoloration of melanophores gray instead oflavender. Also, the ventral region is moretranslucent than the other specimens exam-ined. We attributed these differences toexcessive light exposure. Furthermore, threewell-preserved specimens from Serra deItabaiana show white dots distributed alongdorsum visible under magnification. Morpho-

metric variation is summarized in Table 1.Gouveia et al. (2012) observed that females(SVL¼20.55 6 0.8 mm; n¼ 6) are larger thanmales (SVL ¼ 18.18 6 0.6 mm; n ¼ 6).

Etymology.—The specific epithet baliommais a feminine adjective derived from the Greeknouns Balios meaning ‘‘spotted’’ and Ommameaning ‘‘eye.’’ The name of this new speciesrefers to the distinctive punctuated pattern onthe iris, unique among the Vitreorana speciesdescribed from the Atlantic Forest.

Distribution.—Vitreorana baliomma isknown from the northern portion of theAtlantic Forest biome, in ombrophilous for-mations (sensu Veloso et al., 1991). Inaddition to type-locality, the new species hasbeen collected in Municipality of Itapebi,State of Bahia, and in Parque Nacional daSerra de Itabaiana, Municipality of AreiaBranca, State of Sergipe (Fig. 3). The newspecies is allopatric from other members ofVitreorana, except V. eurygnatha, with whichit is sympatric in southern Bahia. However,our data do not allow us to infer syntopiclocalities between these species.

Natural history.—The type-locality is aforested fragment with strong anthropogenicinfluence. Much of the original vegetation hasbeen selectively removed for cacao cultivation.In cacao plantations, sporadic emergent treesare preserved to shade the understory cacaoplants (a pattern locally known as ‘‘cabruca’’;Canedo et al., 2004). Males of V. baliomma sp.nov. were observed vocalizing perched onvegetation along a permanent creek at cab-rucas. On one occasion, 5–6 males wereobserved vocalizing at heights from 1 to 1.8m above the water, on upper surfaces of leaves(C. Canedo, personal communication).

Gouveia et al. (2012) provided ecologicaldata for the population of Serra de Itabaiana(referred to as Vitreorana aff. eurygnatha).According to those authors, V. baliomma sp.nov. occurs in clumped distributions alongstreams, forming groups of 2–4 individuals.Perched males call from dorsal surfaces ofleaves of riverine understory from 0.3 to 4 min height. Amplectant pairs deposited eggclutches (10–25 eggs) preferentially on uppersurfaces of leaves; however, egg masses werealso observed on lower surfaces.

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Remarks.—We tentatively assign the newspecies to the genus Vitreorana because itexhibits most of diagnostic traits for the genus,as semisolid iridophores layer on liver andgastrointestinal tract visible by transparency,green bones in life, lavender coloration inpreservative (see Guayasamin et al., 2009).Currently, this genus is defined by ambiguousmorphological synapomorphies and lacks amore detailed morphologic definition withinCentrolenidae, making the assignment of thegenus without molecular evidence difficult.The interpretations of these ambiguous traitscould support the insertion of this new speciesin the genus Teratohyla or Chimerella. Basedon biogeographical affinities, however, weprefer to keep this new species in the genusVitreorana until new studies emerge assessingthe molecular data set of V. baliomma sp.nov., or improve the morphological charac-terization of higher taxa of Centrolenidae,

thus corroborating the placement of V.baliomma sp. nov. in this genus.

DISCUSSION

Prior to this study, all species of glass frogsfrom the Atlantic Forest shared a condition ofan iridophore layer that covers the pericardi-um, liver, urinary bladder, kidneys, and testes;and is absent from the stomach and intestines.As described here, however, V. baliommapresents a different pattern, where irido-phores cover the pericardium, liver, stomach,and intestines, and are absent from theurinary bladder, kidneys, and testes (similarto the pattern described for V. gorzulae). Todate, general external and internal morpho-logical features suggest that V. baliommaresembles congeneric species from the Cor-dillera de la Costa in Venezuela, GuianaShield, and the Amazonian basin, and prob-ably is sister to V. gorzulae. We encourage

FIG. 3.—Geographic distribution of Vitreorana baliomma sp. nov. in Brazil (shaded area of inset). Star¼ type-locality;shaded squares¼ additional localities of occurrence of V. baliomma sp. nov.

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future researchers to investigate the phyloge-netic relationships of glass frogs in order toclarify the position of the new species withinVitreorana and Centrolenidae.

Glass frogs exhibit a wide diversity ofnuptial excrescences that have been studiedby many researchers (Flores, 1985; Lynch andRuiz-Carranza, 1996; Cisneros-Heredia andMcDiarmid, 2007). Most Brazilian glass frogswere neglected in these studies, however, andfew descriptions are available for their nuptialexcrescences, as well as any ontogenetic shifts,or intra- and interspecific variation, in thistrait. Flores (1985) and Lynch and Ruiz-Carranza (1996) referred to a reduced orrudimentary type of nuptial pad for AtlanticForest glass frogs underlying Type I and TypeII, informally named as rudimentary orreduced Type I, which we attribute to V.baliomma, despite the presence of someaccessorial glands along ventrolateral base ofthumb (see Fig. 2D). Notwithstanding, allexamined specimens of V. uranoscopa and V.eurygnatha show different nuptial excrescenc-es (Fig. 2E,H), forming a densely packed padwhich covers almost the entire surface of thefirst phalange in the thumb; thus fitting in thetypical Type I nuptial excrescence, followingFlores (1985) and Lynch and Ruiz-Carranza(1996). Still, most of classifications proposedfor nuptial excrescences of Centrolenidae lacka comprehensive survey of all taxa within theclade (Flores, 1985; Lynch and Ruiz-Carran-za, 1996; Cisneros-Heredia and McDiarmid,2007). Further studies should consider theexternal morphology of nuptial excrescencesin Centrolenidae, in addition to using otherapproaches, such as micro-ornamentation,histological, and glandular surveys. Theseapproaches have been useful for other anurangroups (e.g., Luna et al., 2012).

Several studies assessing vertebrate diversi-ty of the Atlantic Forest biome indicate anintricate pattern of endemism, which can beseparated latitudinally and longitudinallyalong climatic conditions, vegetation, andgeographical formations (Costa, 2003; Santoset al., 2007; Silva et al., 2012). Therefore, V.baliomma might have a geographic distribu-tion that is constrained to the northern portionof the Atlantic Forest. Increased samplingefforts in these areas might reveal the

presence of this species in other forestfragments.

Since the works of Taylor and Cochran(1953) and Heyer (1978, 1985), AtlanticForest glass frogs have not been the mainfocus of any published study dealing withCentrolenidae. In view of newly collectedspecimens, the description of V. baliomma sp.nov. highlights the need for more studiesassessing the systematics of Vitreorana fromAtlantic Forest habitats in Brazil and Argenti-na in order to clarify the taxonomic status ofpopulations, the species relationships withinthe genus, and to provide an improvedmorphological characterization of currentlyrecognized species.

Acknowledgments.—We thank M. Rada and S. Cas-troviejo-Fisher for their suggested improvements to anearlier version of this manuscript; C. Hutter for hisfeedback and linguistic revision; G. Bittencourt and F.Glaw for photographs of the lectotype of V. parvula and ofthe holotype of V. uranoscopa, respectively; S. Gouveiaand R. Gaiga for their photos of live V. baliomma and V.eurygnatha, respectively; and C.F.B. Haddad, C. Mello,H. Zaher, and R. Faria for loan or permission to examinespecimens under their care. RP thanks the Coordenacaode Aperfeicoamento de Pessoal de Nıvel Superior(CAPES) for scholarship grants; UC and JPPJ acknowl-edge the Conselho Nacional de DesenvolvimentoCientıfico e Tecnologico (CNPq) and Fundacao CarlosChagas Filho de Amparo a Pesquisa do Estado do Rio deJaneiro (FAPERJ) for financial support.

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Accepted: 6 February 2014Associate Editor: Bryan Stuart

APPENDIX

Specimens ExaminedVitreorana oyampiensis.—Brazil: Para: MNRJ 48270

Porto Trombetas, FLONA Sacara-Taquera, Municipalityof Oriximina; MNRJ 47899 Porto Trombetas, Sacara-Monte Branco; MNRJ 52867–52869 Plato Sacara, FLO-NA Sacara-Taquera, Porto Trombetas, Municipality ofOriximina. Amazonas: MNRJ 4557 Igarape Acara, ReservaDucke, Municipality of Manaus; MZUSP 105136–105138Reserva Ducke, Municipality of Manaus; MZUSP 60166–60168 Reserva INPA WWF, Municipality of Gaviao.

Vitreorana eurygnatha.—Brazil: Sao Paulo: AL-MN973–975 syntypes; MNRJ 73167–73185 Fazenda doBonito, PARNA Serra da Bocaina, Municipality of SaoJose do Barreiro; MZUSP 105224–105231 Campo deFruticultura, Municipality of Sao Jose do Barreiro; MNRJ17649, CFBH 269, 362, 1854 Fazendinha Sao Luıs,Municipality of Ribeirao Branco; MNRJ 34758 EstacaoBiologica de Paranapiacaba, Municipality of Santo Andre;MZUSP 53052–53059 Fazenda do Veado, Municipality ofBananal; MZUSP 15153–15180 Cidade Azul, Municipalityof Joanopolis; MZUSP 104856–104867, 105399–105402

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Fazenda Lagoinha da Serra, Municipality of Campos doJordao. Rio de Janeiro: MNRJ 2178, 73107, 73162,MZUSP 53350–53357 Municipality of Teresopolis; MNRJ32872 Represa do Guinle, Municipality of Teresopolis;MNRJ 52690–52692, 73166, PARNA Serra dos Orgaos,Municipality of Teresopolis; MNRJ 78575 Municipality ofPetropolis; MNRJ 73163–73165, 73422 Municipality ofItatiaia; MNRJ 51575 Macieiras, PARNA Itatiaia, Munic-ipality of Itatiaia; MNRJ 51801–51810, 52699–52701,73128–73134 Tijuca, Municipality of Rio de Janeiro.

Vitreorana uranoscopa.—Brazil: Santa Catarina:MZUSP 35429–35436 Municipality of Novo Horizonte;CFBH 5280–5282, 5284 Bairro Lencol, Municipality ofSao Bento do Sul. Minas Gerais: CFBH 16534 PousadaFloresta, Municipality of Itamonte; MZUSP 135659,133838, PARNA Caparao, Municipality of Vale Verde;MZUSP 145472 Municipality of Conceicao do MatoDentro; MNRJ 56300, 77778–77780 Ponte para oBelchior, Reserva Particular do Patrimonio Natural daSerra do Caraca, Municipality of Catas Altas; MNRJ

30606–30607 Serrinha, Municipality of Mariana; MNRJ23125 Mata da Mutuca, Municipality of Nova Lima;MNRJ 24688 Estacao Biologica Mata do Sossego,Municipality of Simonesia. Rio de Janeiro: MNRJ78040–78043 Lıdice, Municipality of Rio Claro; CFBH19256, 19279 PARNA Serra da Bocaina; MNRJ 73012Parque Natural Municipal da Taquara, Municipality ofDuque de Caxias; MNRJ 32873, 72450, 75389–75390,PARNA Itatiaia, Municipality of Itatiaia; MNRJ Represado Guinle, Municipality of Teresopolis; MNRJ 46680,64815–64816, 77352–77362, PARNA Tijuca, Municipalityof Rio de Janeiro. Sao Paulo: MZUSP 104892–104895,CFBH 869, 1528, Paranapiacaba, Municipality of SantoAndre; MZUSP 136535–136537 Parque Estadual CarlosBotelho, Municipality of Sao Miguel Arcanjo; MNRJ63951–63954 Rubiao Junior, Municipality of Botucatu;MNRJ 32510–32511 Estrada de Botucatu, Municipality ofBotucatu; CFBH 2252 Picinguaba, Municipality ofUbatuba; CFBH 6208 Nucleo Santa Virgınia, PESM,Municipality of Sao Luıs do Paraitinga.

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