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Zootaxa 1680: 25–53 (2008) www.mapress.com/ zootaxa/

ISSN 1175-5326 (print edition)

Copyright © 2008 · Magnolia Press

ISSN 1175-5334 (online edition)

ZOOTAXA

Glassfrogs (Anura: Centrolenidae) of Kaieteur National Park, Guyana, with notes on the distribution and taxonomy of some species of the family in the Guiana Shield PHILIPPE J. R. KOK1 & SANTIAGO CASTROVIEJO-FISHER2 1

Department of Vertebrates, Royal Belgian Institute of Natural Sciences, 29 rue Vautier, B-1000 Brussels, Belgium. E-mail: [email protected] 2 Department of Evolution genomics and systematics, Evolutionary Biology Centre (EBC), Uppsala University, Norbyvägen 18D, SE75236 Uppsala, Sweden. E-mail: [email protected]

Abstract We provide new distribution records and discuss the taxonomy of three species of Glassfrogs from the Guiana Shield: Centrolene gorzulai, Cochranella helenae, and Hyalinobatrachium taylori. These three species were collected in Kaieteur National Park in west-central Guyana. Taxonomic changes were based on morphological, bioacoustic and genetic (a fragment of the mitochondrial ribosomal gene 16S) comparisons. We consider Centrolene papillahallicum to be a junior synonym of C. gorzulai. We assign the Venezuelan population of Cochranella oyampiensis to Co. helenae and describe the phenotypic variation of this taxon. We refine the description of Cochranella oyampiensis and transfer it to the Co. spinosa species group. We propose the new name Cochranella helenae Group for those species of Cochranella assigned to the former Co. oyampiensis Group. We report the first record of Cochranella midas for French Guiana, and the first record of Hyalinobatrachium nouraguense, new emendation, for Suriname. Key words: Centrolenid frogs, Centrolene gorzulai, Centrolene papillahallicum, Cochranella ametarsia, Cochranella helenae, Cochranella midas, Cochranella oyampiensis, French Guiana, Hyalinobatrachium mondolfii, Hyalinobatrachium nouraguense, Hyalinobatrachium taylori, mitochondrial DNA, Suriname

Resumen Presentamos nuevos datos de distribución y discutimos la taxonomía de tres especies de Ranas de Cristal del Escudo Guayanés: Centrolene gorzulai, Cochranella helenae, e Hyalinobatrachium taylori. Las tres especies fueron colectadas en el Parque Nacional Kaieteur, situado en el centro-oeste de Guyana. Los cambios taxonómicos propuestos están basados en comparaciones morfológicas, bioacústicas, y genéticas de un fragmento del gen ribosómico mitocondrial 16S. Consideramos C. papillahallicum como un sinónimo de C. gorzulai. Asignamos las poblaciones venezolanas de Co. oyampiensis a Co. helenae y describimos la variación fenotípica de este taxón. Refinamos la descripción de Cochranella oyampiensis, que transferimos al grupo de especies Co. spinosa. Proponemos el nuevo nombre “grupo de especies Cochranella helenae” para las restantes especies pertenecientes al antiguo grupo de especies Co. oyampiensis. Aportamos el primer registro de Cochranella midas para la Guayana Francesa, y de Hyalinobatrachium nouraguense, nueva enmendación, para Surinam. Palabras Clave: Ranas, Centrolénidos, Centrolene gorzulai, Centrolene papillahallicum, Cochranella ametarsia, Cochranella helenae, Cochranella midas, Cochranella oyampiensis, Hyalinobatrachium mondolfii, Hyalinobatrachium nouraguense, Hyalinobatrachium taylori, Guyana Francesa, ADN mitocondrial, Surinam

Résumé Nous présentons de nouvelles données de distribution et discutons la taxonomie de trois espèces de “grenouilles de Accepted by M. Vences: 16 Nov. 2007; published: 14 Jan. 2008

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verres”: Centrolene gorzulai, Cochranella helenae, et Hyalinobatrachium taylori. Ces trois espèces ont été récoltées dans le Parc National de Kaieteur situé au centre ouest du Guyana. Nos modifications taxonomiques sont basées sur la comparaison de caractères morphologiques, bioacoustiques, et génétiques (un fragment du gène mitochondrial ribosomal 16S). Nous considérons Centrolene papillahallicum comme étant un synonyme junior de C. gorzulai. Nous rattachons la population de Cochranella oyampiensis du Venezuela à Co. helenae et décrivons la variation phénotypique de ce taxon. Nous affinons la description de Cochranella oyampiensis et transférons cette espèce dans le groupe phénotypique d’espèces Co. spinosa. Nous proposons le nouveau groupe Cochranella helenae pour les espèces préalablement assignées au groupe phénotypique d’espèces Co. oyampiensis. Nous mentionnons pour la première fois la présence de Cochranella midas en Guyane Française, ainsi que la présence de Hyalinobatrachium nouraguense, nouvelle émendation, au Surinam. Mots-clés: Grenouilles, Centrolenidés, Centrolene gorzulai, Centrolene papillahallicum, Cochranella ametarsia, Cochranella helenae, Cochranella midas, Cochranella oyampiensis, Hyalinobatrachium mondolfii, Hyalinobatrachium nouraguense, Hyalinobatrachium taylori, Guyane Française, Surinam, ADN mitochondrial

Introduction Glassfrogs (family Centrolenidae) constitute a monophyletic group (see Guayasamin & Trueb 2007 and citations therein) distributed throughout the Neotropics, from Mexico to Bolivia, and a vicariant group of species in southeastern Brazil and northeastern Argentina (Frost 2007). Currently, there are 147 recognized species (updated from AmphibiaWeb 2006) but the alpha diversity of these frogs is far from stable and several new species are described each year (Kubicki 2007). Ruiz-Carranza and Lynch (1991a) identified three genera of Glassfrogs. Species of the genera Centrolene and Cochranella are organized into four phenetic species groups each, those of Hyalinobatrachium in three [see Guayasamin et al. (2006a) for phenotypic characteristics and composition of the species groups]. Cisneros-Heredia and McDiarmid (2006a), following Noonan and Harvey (2000), included the Centrolene peristictum Group within the diversity of the Centrolene prosoblepon Group. Later, Cisneros-Heredia and McDiarmid (2007) created the genus Nymphargus to accommodate all but two species of the Cochranella ocellata Group (Ruiz-Carranza & Lynch 1991a, 1995a). Additionally, CisnerosHeredia and McDiarmid (2007) considered “ … inappropriate to continue to recognize or expand species groups in the Centrolenidae when their utility is very limited and their recognition uninformative”. We consider this statement as controversial and we keep using diagnosable specie groups (see below for argumentation). Representatives of the three genera occur in the Guiana Shield (GS), sensu Señaris and MacCulloch (2005: Fig. 2). Centrolene is represented by three species of the C. gorzulai Group: C. gorzulai (Ayarzagüena, 1992) and C. lema Duellman and Señaris, 2003 both from Venezuela, and C. papillahallicum Noonan and Harvey, 2000 in Guyana (Señaris & MacCulloch 2005). The genus Cochranella is represented by Co. duidaeana (Ayarzagüena, 1992), Co. helenae (Ayarzagüena, 1992) and Co. riveroi (Ayarzagüena, 1992) in Venezuela; Co. geijskesi (Goin, 1966) in Suriname; and Co. oyampiensis (Lescure, 1975) in French Guiana, Suriname, Venezuela and northern Brazil (Señaris & MacCulloch 2005). Lastly, the genus Hyalinobatrachium is represented by H. crurifasciatum Myers and Donnelly, 1997, H. eccentricum Myers and Donnelly, 2001, H. iaspidiense (Ayarzagüena, 1992) and H. mondolfii Señaris and Ayarzagüena, 2001 in Venezuela; H. ignioculus Noonan and Bonett, 2003 in Guyana; H. fleischmanni (Boettger, 1893) in Guyana and Suriname (records dubious, probably due to confusion with other species, see Noonan & Harvey 2000; Señaris “1999” [2001]; Cisneros-Heredia & McDiarmid 2007; Frost 2007; not listed in Señaris & MacCulloch 2005); H. nouraguensis Lescure and Marty, “2000” (2001) in Guyana, French Guiana and Brazil (Cordeiro-Duarte et al. 2002; Ernst et al. 2005; Señaris & MacCulloch 2005); and H. taylori (Goin, 1968) in Venezuela, Guyana, Suriname and French Guiana (Lescure 1975; Ayarzagüena 1992; Lescure & Marty “2000” [2001]; Señaris & Ayarzagüena 2005; Señaris & MacCulloch 2005). All of these, except H. taylori, are in the Hyalinobatrachium fleis-

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KOK & CASTROVIEJO-FISHER

chmanni Group (Señaris & Ayarzagüena 2005). An additional, unidentified species of Hyalinobatrachium was reported by Ernst et al. (2005) from the Mabura Hill Forest Reserve in central Guyana. The same authors pointed out the possible synonymy of H. ignioculus with H. crurifasciatum, and of H. nouraguensis with H. iaspidiense (see also Cisneros-Heredia & McDiarmid 2007). The taxonomic status of the species of the genus Hyalinobatrachium from the Guiana Shield will be addressed elsewhere (Castroviejo-Fisher et al. submitted). During recent herpetological surveys in Kaieteur National Park, Guyana, three centrolenid species were collected: Centrolene gorzulai, Cochranella helenae and Hyalinobatrachium taylori. We present herein the implications of these discoveries to the distribution and taxonomy of anurans of the family Centrolenidae plus a key to the centrolenid species of Guyana.

Material and methods Nomenclature and terminology. For the infrageneric classification we follow that presented by Guayasamin et al. (2006a) with the addition of Centrolene mariaelenae Cisneros-Heredia and McDiarmid, 2006a to the Centrolene gorzulai species group and the new combinations Centrolene balionotum (Duellman, 1981) and Cochranella puyoensis (Flores & McDiarmid, 1989) (Cisneros-Heredia & McDiarmid 2006a–b). To avoid confusion between abbreviations, Centrolene and Cochranella are respectively mentioned along the text as C. and Co. Frost et al. (2006) suggested ranking Allophryne ruthveni Gaige, 1926 in the subfamily Allophryninae of the family Centrolenidae, placing “Glassfrogs” or centrolenids in the subfamily Centroleninae. The taxonomic status of A. ruthveni has a long history of controversy (e.g. Caldwell & Hoogmoed 1998; Guayasamin & Trueb 2007) and, for the same reasons exposed by Guayasamin and Trueb (2007), we did not include A. ruthveni in the family Centrolenidae. Abbreviations for museum collections are those of Frost (2007), with the following additions: JCC = Juan Carlos Chaparro field numbers [specimens housed at the Museo de Historia Natural, Universidad Nacional de San Antonio Abad del Cusco, Peru (MHNC), but not yet catalogued]; MAD = Maureen A. Donnelly field numbers; MB = Michel Blanc field numbers (not yet catalogued); MSH = Marinus S. Hoogmoed field numbers [specimens housed at the RMNH, but not yet catalogued]. Study site. Collections were made in Kaieteur National Park (5°10’N, 59°29’W), located at the eastern edge of the Pakaraima Mountains, approximately 200 km SW of Georgetown, capital city of Guyana. The park encompasses an area of 62,680 hectares (Kelloff 2003). Elevations within the park range approximately from 100–900 m. The only permanent settlement near Kaieteur National Park is the Amerindian village of Chenapou, located along the Potaro river (which runs through the park), about 54 km SW of Kaieteur Falls. The park harbors a mixture of the upland and lowland flora found on the Guiana Shield (Kelloff & Funk 2004) and supports a mosaic of habitats like the “Guiana type” savannah; a submontane forest of the Pakaraima uplands on white sand (ter Steege 2001); and patches of cloud forest - notably a large one at the top of Kaieteur Falls created by the mist rising up the Kaieteur gorge (Kelloff 2003). For a detailed description of Kaieteur National Park see Kelloff (2003) and Kelloff and Funk (2004). Taxon sampling and morphology. All the specimens from Kaieteur National Park were collected during the periods 19 June-1 July 2004, 30 November-16 December 2005, 12 March-2 April 2006, and 17-30 January 2007 at elevations between 400–530 m (Fig. 1). They were collected according to approved animal use and care protocols (Heyer et al. 1994), and euthanized in Xylocaïne solution prior to fixation in 10% formalin. After 24 hours in formalin, specimens were transferred to 70% ethanol for permanent storage. Muscle or liver samples were removed immediately after euthanization and preserved in 95% ethanol. Liver was sometimes left untouched to allow accurate examination of hepatic, parietal and visceral peritonea, which are important diagnostic characters in the family Centrolenidae. Both specimens and tissue samples are housed at IRSNB.

GLASSFROGS OF KAIETEUR NATIONAL PARK

Zootaxa 1680 © 2008 Magnolia Press ·

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Other specimens and tissues used in the study are listed in Table 1 and Appendix.

FIGURE 1. Map of Kaieteur National Park with main sampling localities (numbered dots) and local distributions of Centrolene gorzulai (blue), Cochranella helenae (green), and Hyalinobatrachium taylori (red). (1) Kaieteur Falls; (2) Menzies Landing trail; (3) Kaieteur airstrip; (4) Muri Muri trail; (5) Right bank Potaro River, opposite Menzies Landing; (6) Tukeit trail; (7) Tukeit Landing; (8) Elinkwa River mouth; (9) Elinkwa River; (10) Elinkwa camp #1; (11) Elinkwa camp #2; (12) Amakwa River mouth; (13) Amamuri River mouth. Insert map indicates the location of Kaieteur National Park in Guyana. Map after the Natural Resources Management Project, Topographic Map of Kaieteur National Park, Guyana.

Coordinates were acquired using a hand-held Garmin 12 Map GPS unit and were referenced to map datum WGS84. Specimens were compared to original published descriptions and museum material (see Appendix). Diagnoses follow Guayasamin et al. (2006a), with the addition of ventral skin condition, male calling site and advertisement call. Terminology for webbing formula follows Savage and Heyer (1967), with modifications proposed by Myers and Duellman (1982) and Savage and Heyer (1997). Use of the term “enameled” fol-



lows Noonan and Bonett (2003) and refers to the presence of a hard, white substance. Description of nuptial excrescences (= nuptial pads, glandular clumps or nuptial glands) and prepollical spines follow Flores (1985) with additions of Cisneros-Heredia and McDiarmid (2007). TABLE 1. Specimens included in the genetic analysis. See Appendix for localities, and Material and methods for abbreviations. Taxa and collection number

Locality

GenBank number

Allophryne ruthveni MAD 1512

Guyana

AY843564

Centrolene gorzulai MHNLS 17325

Venezuela

EU266750

Centrolene lema MHNLS 17142

Venezuela

EU266749

Centrolene gorzulai IRSNB 13976

Guyana

EU266751

Cochranella helenae IRSNB 13979

Guyana

EU266752

Cochranella helenae MHNLS 17127

Venezuela

EU266753

Cochranella helenae* MHNLS 17136

Venezuela

EU266754

Cochranella oyampiensis MB 165

French Guiana

EU266755

* Specimens from this population were previously identified as Cochranella oyampiensis.

It is necessary to point out that fringes and folds on hand, foot, ulna, and tarsus are of diagnostic importance in Centrolenidae (Fig. 2). Fringes and folds sometimes disappear in preservative, hence it is important to examine these characters on living or freshly euthanized specimens to provide an accurate description. Sex was confirmed by dissection and examination of gonads. Measurements were made on preserved specimens to the nearest 0.01 mm with electronic digital calipers, and, following Hayek et al. (2001), rounded to 0.1 mm. Abbreviations are as follows: snout-vent length (SVL); head length (from rictus to tip of snout, HL); head width (at the level of rictus, HW); interorbital distance (IOD); eye length (horizontal, EL); anterior corner of eye to snout tip distance (ES); width of the terminal disc of the third finger (FIII); femur length (from cloaca to the joint between femur and tibia, FEL); tibia length (from the joint between femur and tibia to the joint between tibia and astragalus-calcaneus, TL). Color characteristics were obtained from field notes, color slides and color digital photographs and compared to descriptions and photographs in the literature (Goin 1968; Lynch & Duellman 1973; Lescure 1975; Duellman 1978; Ayarzagüena 1992; Señaris & Ayarzagüena 1993, 2005; Noonan & Harvey 2000; Lescure & Marty “2000” [2001]; Cisneros-Heredia & McDiarmid 2005). Coloration of peritonea was determined by dissection. Bioacoustics. We recorded frog vocalizations in the field. Sound recording equipment consisted of a Sony DAT TCD-D100 recorder with a Sony ECM-MS907 microphone and a Sony WM D6C tape recorder with a Sennheiser Me 80 directional microphone. Recordings were processed on an Apple Macintosh computer. The sounds were digitized and edited at a sampling frequency of 44.1 KHz and 16 bit resolution with a Delta 66 digitizing board and Peak 3.2 software. We also analyzed the recordings of track 11 included in Marty and Gaucher (1999), assigned by the authors to Co. oyampiensis, and Co. midas (Lynch & Duellman, 1973) in Read (2000). All calls were edited with Audacity 1.2.6 for MacOS X (Free Software Foundation Inc. 1991). Praat 4.5.02 for MacOS X (Boersma & Weenick 2006) software was used to obtain numerical information and to generate audiospectrograms and oscillograms. Frequency information was obtained through Fast Fourier Transformations (FFT) (width, 1024 points). Air temperature was measured immediately after sound recording. Recordings were deposited in the Fonoteca Zoológica of the MNCN and at IRSNB. Genetics. We used DNA sequences to test reciprocal monophyly of species as recovered by phylogenetic inference, and to compare genetic distances between species and populations. Elucidation of the phylogenetic relationships between centrolenids is beyond the scope of this work and will be addressed elsewhere (GuaGLASSFROGS OF KAIETEUR NATIONAL PARK


29

yasamin et al. submitted). Sequences from eight individuals were included in the molecular analysis (Table 1).

FIGURE 2. Names and locations of fringes and folds that are of diagnostic importance in Centrolenidae. Left: HAND ULNA (1) fringe on postaxial edge of Finger IV; (2) metacarpal fold; (3) ulnar fold. Right: FOOT - TARSUS (4) fringe on postaxial edge of Toe V; (5) metatarsal fold; (6) tarsal fold; (7) tarsal fringe.

Genomic DNA was isolated using a standard phenol-chloroform extraction protocol (Sambrook et al. 1989). A fragment of approximately 850 bp from the mitochondrial gene 16S was amplified using previously described primers (16SC-5’ and 16Sbr) and PCR conditions (Hillis et al. 1996). This fragment performs better than COI for amphibian species identification through DNA barcodes (Vences et al. 2005a–b) and has been broadly used in amphibian phylogenies (e.g. Darst & Cannatella 2004; Frost et al. 2006). PCR products were purified and sequenced in an ABI 3730xl Genetic Analyzer (Applied Biosciences) following manufacturer protocols. Sequence alignments were performed using the program CLUSTAL_X (Thompson et al. 1997) under default parameters. We used PAUP* 4.0b10 (Swofford 1998) to calculate uncorrected pair-wise distances. The same program was used to construct a Neighbor Joining phylogenetic tree (using uncorrected p–distance) and for an exhaustive search of the most parsimonious tree. The support of the internal nodes in the trees was



assessed using 5000 and 1000 non-parametric bootstrap pseudoreplicates respectively. We placed Allophryne ruthveni as outgroup following recent studies based on molecular and/or morphological data (Austin et al. 2002; Burton 2004; Faivovich et al. 2005; Wiens et al. 2005; Grant et al. 2006;).

Results Morphology and bioacoustics. Detailed morphological descriptions are provided under each species. Morphometric data for Centrolene gorzulai are summarized in Table 2. Spectrograms and oscillograms of the advertisement calls analyzed are presented in Figure 3. TABLE 2. Measurements of Centrolene gorzulai. See Appendix for localities, and Material and methods for abbreviations. Measurements of the type material Centrolene gorzulai and its synonym C. auyantepuiana are from Señaris and Ayarzagüena (2005). Museum Number

Sex

SVL

HL

HW

IOD

EL

ES

FIII

FEL

TL

EBD 28824 (paratype of C. auyantepuiana)

F

21.6

7.8

8.7

2.6

3.2

2.7

1.1

12.3

12.5

EBD 28825 (paratype of C. auyantepuiana)

F

21.2

7.6

8.7

2.3

3.1

2.7

1.1

12.6

13.3

IRSNB 13974

F

22.0

7.3

11.0

2.6

3.9

2.7

1.3

11.2

12.3

IRSNB 13975

M

22.5

6.2

8.8

2.6

3.4

2.8

1.2

12.5

13.3

IRSNB 13976

M

19.7

6.0

7.6

2.7

3.2

2.5

1.0

11.4

11.5

IRSNB 13977

M

20.6

6.2

7.8

2.7

3.2

2.6

1.1

11.0

12.2

IRSNB 13978

M

19.9

6.4

7.6

2.8

3.0

2.6

1.2

10.5

12.4

MHNLS 11221 (holotype)

M

20.5

7.4

8.5

2.9

3.4

2.9

1.0

12.9

12.7

MHNLS 12482 (holotype of C. auyantepuiana)

M

20.7

7.3

8.1

2.4

3.1

2.9

1.0

11.6

11.9

MHNLS 17325

M

21.5

7.0

8.0

2.3

3.8

2.6

1.1

11.8

12.2

MHNLS 17326

M

22.5

7.1

8.4

2.2

3.7

2.8

1.2

10.1

11.8

UTA 52243 (paratype of C. papillahal- M licum)

19.2

6.1

7.7

2.5

3.2

2.9

1.3

11.7

11.9

UTA 52233 (paratype of C. papillahallicum)

19.2

6.0

7.5

2.4

3.2

2.8

1.2

12.3

11.7

M

Genetics The NJ phylogenetic tree (Fig. 4) shows that the three sequences of the specimens of the Centrolene gorzulai Group here included are almost identical and that they form a monophyletic group with a high bootstrap value (100). The estimated genetic distances between the three sequences is < 0.5%. The sequence of the specimen of Cochranella from Salto Karuay, Venezuela (MHNLS 17136) is almost identical to the ones of Co. helenae from the type locality (MHNLS 17127) and from the specimen from Kaieteur National Park, Guyana (IRSNB 13979), while the sequence from the specimen of Co. oyampiensis from French Guiana (MB 165) is outside this clade. The genetic distance between the Venezuelan and Guyanan specimens of Co. helenae is < 0.5 %;



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however the genetic distance between Co. oyampiensis MB 165 and the three other specimens is 5%. The MP analyses yield a single most parsimonious tree (not shown) with a similar topology and support to the NJ tree, which confirm the results.

FIGURE 3. Audiospectrograms and oscillograms (top and down respectively) of the advertisement calls of (A) Cochranella midas from Ecuador (Read 2000), T° unknown; (B) Cochranella midas from French Guiana (Marty & Gaucher 1999), T° unknown; (C) Hyalinobatrachium mondolfii from Venezuela, MHNLS 17120, T° 23°C; (D) Hyalinobatrachium sp. from Guyana, specimen not collected, T° 26°C.



FIGURE 4. Gene tree representing Neighbor Joining phylogenetic relationships of some frogs of the family Centrolenidae from the Guiana Region inferred from a 850 bp of the 16S gene (mtDNA). Numbers indicate support for nodes (non-parametric bootstrap). Maximum Parsimony analysis of the same sequences retrieved a similar topology with same bootstrap values. Each specimen is followed by its collection number to clearly associate the individual with the corresponding sequence of Table 1; see Appendix for details about the localities. * Specimens from this locality were previously assigned to Cochranella oyampiensis.



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Species accounts CENTROLENE GORZULAI (Ayarzagüena 1992) Figs. 5a–b, 6 Centrolenella gorzulae Ayarzagüena 1992: 19 Centrolene gorzulai Duellman 1993: 35 Centrolenella auyantepuiana Señaris and Ayarzagüena 1993: 122 Centrolene gorzulae Ruiz-Carranza and Lynch 1995b: 2 Hyalinobatrachium auyantepuianum Ayarzagüena and Señaris “1996” 1997: 13 Cochranella auyantepuianum Myers and Donnelly 1997: 16 Cochranella auyantepuiana Duellman 1999: 300 Centrolene papillahallicum Noonan and Harvey 2000: 295, new synonym

Holotype and type locality. MHNLS 11221 (adult male), Venezuela, Estado Bolívar: Central sector of Auyan-tepui (05°56’ N, 62°34’ W; 1850 m). Material from Kaieteur National Park. IRSNB 13974–8 (4 males, 1 female). Diagnosis. Centrolene gorzulai differs from other species in the family by the following combination of characters: (1) dentigerous process on vomer and vomerine teeth absent; (2) bones green in life; (3) in preservative, dorsum lavender entirely covered with melanophores (minute punctuations); parietal peritoneum mostly transparent, a small anterior portion white (the “bib-like white patch” of Duellman & Señaris 2003), only appreciable in dissected specimens; pericardial peritoneum white; hepatic and visceral peritonea white, except for the urinary bladder that is transparent; (4) in life, dorsum dark green with scattered paler flecks; (5) finger webbing II 2-–3 III 2+–(2-–2) IV; (6) toe webbing I (1–1½)–(2–2+) II 1–2+ III 1–(2–2+) IV (2–2+)–1 V; (7) snout subtruncate in dorsal view, truncate to slightly sloping in lateral profile; (8) dorsal skin finely shagreened, ventral skin strongly granular; (9) fringe on postaxial edge of Finger IV present, enameled, metacarpal fold present, weakly enameled, ulnar fold absent; fringe on postaxial edge of Toe V present, enameled, metatarsal fold present, weakly enameled, tarsal fold usually absent or very weak; (10) humeral spine in adult males present; (11) tympanum distinct, oriented dorsolaterally with a slight posterior inclination; (12) SVL in males 19.7–22.5 mm (mean = 20.9, n = 4), 22.0 mm in one female; (13) prepollex slightly enlarged; prepollical spine projecting (spine not exposed); nuptial excrescences finely granular, white, comprised of a dense group of glands and situated in the medial, dorsolateral internal side of Finger I (Type-V); (14) anal ornamentation consisting of small enameled tubercles posterior to vent and enlarged paired or unpaired round tubercles below vent; (15) when appressed, Finger II = Finger I; (16) liver trilobate; (17) diameter of eye about 2X width of disc on Finger III; (18) males call from the upper side of leaves; (19) advertisement call a single note, pulsed. Centrolene gorzulai can be differentiated from species of the genus Hyalinobatrachium by having a trilobate liver and a humeral spine in adult males. Males of Cochranella lack the humeral spine. Other species of the Centrolene gorzulai Group are C. lema, which has transparent visceral peritonea (Duellman & Señaris 2003), and C. mariaelenae, characterized by having a bulbous liver and completely transparent parietal peritoneum (Cisneros-Heredia & McDiarmid 2006a). Centrolene gorzulai is easily distinguished from other centrolenids in Kaieteur National Park by the presence of a humeral spine in males, dark green dorsum and white upper lip. Hand and foot of the species are illustrated in Figure 6. Color in life. Specimens from Kaieteur have a dark green dorsum with minute paler flecks that are less visible at night (Fig. 5a). Upper lip enameled, hands and feet bluish green to green, tips of fingers and toes yellowish green. Postaxial edges of Finger IV and Toe V with enameled fringes; metacarpal and metatarsal folds weakly enameled. Nuptial excrescences white, comprised of a dense group of glands and situated in the medial, dorsolateral internal side of Finger I (Type-V). Bones green. Iris metallic copper with dark brown reticulations; an incomplete pale yellow ring around pupil. Skin of flanks and venter translucent, throat trans-



lucent green. Parietal peritoneum mostly transparent, a small anterior portion white that is only noticeable after dissection, pericardial peritoneum white, hepatic and visceral peritonea white (visible through the ventral skin, see Fig. 5b). Color in preservative. Dorsum lavender, entirely covered with minute punctuations and with some small white (on body) to bright light blue (on eyelids) warts; both melanophores and warts are only visible under magnification (small bright light blue warts are particularly numerous and visible on eyelids). Upper lip enameled. Eyelids and eyes dark lavender. Dorsal ground color of arms and legs cream, covered with punctuations (punctuations slightly less numerous on thighs). Fringes on postaxial edges of Finger IV and Toe V, metacarpal and metatarsal folds weakly enameled. Distribution of melanophores on digits is variable, but they are always more numerous on Fingers III–IV than I and II; Toes IV–V with many melanophores, rarely present on Toes I–III, if present they are very few and restricted to the two distal phalanges. Flanks, shoulder and ventral surfaces cream. Bones white (green pigments are lost in preservative). Nuptial excrescences form a white patch on dorsal surface of Finger I. Coloration of internal organs (after dissection): parietal peritoneum mostly transparent, a small anterior portion white, pericardial, hepatic and visceral peritonea white, except for the urinary bladder that is transparent. Taxonomic comments. Centrolene papillahallicum was described from 20 male specimens collected on Peters Mountain, ca. 900 m elevation about 4 km north of Imbaimadai in west-central Guyana (Noonan & Harvey 2000). However, our comparisons based on morphometrics (Table 2), morphology, coloration (Figs. 5a–b, 7) and molecular data (Fig. 4) do not support the hypothesis of C. papillahallicum as distinct from C. gorzulai. We discuss here the diagnostic characters given by Noonan and Harvey (2000: 297) to distinguish C. papillahallicum from C. gorzulai (characters of the latter in parentheses) and argue how our new observations justify the consideration of C. papillahallicum as a junior synonym of C. gorzulai. (1) Notch in lower lip present (absent). This character seems to be variable, probably depending of age of the specimen, and could be prone to post-mortem and preservation artifacts. MHNLS 17326, collected near the type locality of C. gorzulai, has a notch, while it is absent in MHNLS 17325 collected at the same location. Examination of two paratypes of C. papillahallicum (UTA 52233 and UTA 52243) reveals that this character is either absent or barely noticeable; (2) Dorsal skin shagreened (smooth). At first glance, the dorsal skin of the holotype of C. gorzulai is smooth, but magnification reveals a finely shagreened skin (Ayarzagüena 1992, SCF personal observation). Other specimens of C. gorzulai collected at Auyan-tepui have finely shagreened skin on the dorsum in life (Fig. 7). We note that this character is also highly subject to post-mortem and preservation artifacts; (3) Pericardium white (transparent). This is an error in the original description (J. Ayarzagüena pers. comm.), who meant “white” but wrote “clear”; the same applies to the visceral and hepatic peritonea; (4) Prepollical spine not exposed externally (exposed). The spine is exposed in the holotype of C. gorzulai, but not in any other topotype that we have examined. We argue that exposure of the spine in the holotype of C. gorzulai is because of its partially dried condition that caused the skin to shrink, exposing the prepollical spine. Indeed, Señaris and Ayarzagüena (2005) pointed out that the prepollical spine could be covered by skin or not; (5) Fringe on postaxial edge of Toe V (fringe absent). Living specimens of C. gorzulai from the type locality show evident enameled fringes on the postaxial edge of Toe V (followed by a weakly enameled contiguous lower metatarsal fold, rarely extending along tarsus) and also on the postaxial edge of Finger IV (followed by a coextensive lower metacarpal fold, not extending along ulna). These fringes are barely distinguishable on the holotype of C. gorzulai. After preservation the fringes and folds become difficult to distinguish or even completely disappear in some specimens, especially if the specimen is desiccated. Centrolenids have very fragile skin, fringes and folds are easily altered by preservation; (6) Metatarsal tubercle present (absent). Although Ayarzagüena (1992) stated that the metatarsal tubercle is not noticeable in the holotype of C. gorzulai (which is actually different from absent), our examination of the holotype and topotypes reveals that this tubercle is present (see also Señaris & Ayarzagüena 2005: Figure 42c, in which the metatarsal tubercle is



35

clearly visible); (7) Noonan and Harvey (2000) emphasized the presence of a pointed tip on Toe I in C. papillahallicum (hence the name). This character is also present in C. gorzulai (although it may be barely distinguishable in some preserved specimens). As aforementioned, the original description of C. gorzulai contains several inaccuracies. Internal and external morphologies of specimens from Kaieteur National Park match very well with those of specimensfrom the type locality and those of C. papillahallicum from Peters Mountain. In addition to the small enameled tubercles posterior to vent, we noted the presence of enlarged tubercles below vent (see Fig. 5b), which are mentioned as absent in C. papillahallicum by Noonan and Harvey (2000). Closer examination of two paratypes of C. papillahallicum reveals that these enlarged subcloacal tubercles are well visible in UTA 52233, but undistinguishable in UTA 52243. These tubercles possibly disappeared in several of their specimens due to an artifact of preservation (as observed in some of our material). Enlarged subcloacal tubercles are mentioned in the original description of C. gorzulai (Ayarzagüena 1992) and in that of Señaris and Ayarzagüena (2005). Cisneros-Heredia and McDiarmid (2006a: Table 2), who did not examine type specimens of C. papillahallicum, do not mention the enlarged tubercles below vent in C. papillahallicum. As mentioned by Señaris and Ayarzagüena (2005), a small fraction of the anterior part of the parietal peritoneum (above heart) is covered with white pigment in C. gorzulai; the same white pigment was observed in specimens from Kaieteur National Park. Our molecular data support our hypothesis that the two species here mentioned are merely different populations of C. gorzulai. The genetic distances are close to zero and the phylogenetic tree (Fig. 4) shows that the two specimens are very closely related to each other. Therefore we formally consider Centrolene papillahallicum as a junior synonym of C. gorzulai. Our molecular data also indicate that Centrolene lema shows virtually no differences from C. gorzulai in mtDNA 16S (2 bp). Furthermore, preliminary morphological studies of new topotype specimens of C. lema (previously known only from one specimen) indicate that these two species are more similar that previously stated (Duellman & Señaris 2003). This matter will be addressed elsewhere (Castroviejo-Fisher in preparation). Distribution and ecology. Centrolene gorzulai has been reported from its type locality and neighboring areas in Bolívar, Venezuela (Señaris & Ayarzagüena 2005). Specimens from Kaieteur National Park, as well as specimens from Peters Mountain, 3.6 km N of Imbaimadai in the Pakaraima Mountains (the type locality of C. papillahallicum), extend the known distribution by about 360 km SEE (see Fig. 8). All individuals were collected by night between 1.0–1.5 m above the ground, on leaves, above or along small streams (max 3.0 m wide) in primary forest, at elevations between 430 and 530 m. Several males were calling from the upper surfaces of leaves in March and June 2006. The call was not recorded but, to the ear, it is similar to the one described by Noonan and Harvey (2000) for C. papillahallicum and by Señaris and Ayarzagüena (2005).



FIGURE 5. Dorsolateral (left) and ventral (right) views of the Glassfrogs of Kaieteur National Park in life. (A, B) Centrolene gorzulai (IRSNB 13977); (C, D) Cochranella helenae (IRSNB 13980); and (E, F) Hyalinobatrachium taylori (IRSNB 13982). Black arrows indicate enlarged tubercles below vent. Photographs Philippe J. R. Kok.



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FIGURE 6. Hand (left) and foot (right) of Centrolene gorzulai (IRSNB 13976) from Kaieteur National Park, Guyana. Scale bars = 2 mm. Photographs Philippe J. R. Kok.

FIGURE 7. Left: Centrolene gorzulai, male from Auyan-tepui (MHNLS 17325). Right: habitat of C. gorzulai near the type locality (Auyan-tepui: Campamento Oso, top of Auyan-tepui, 1700 m elevation). Photographs Santiago Castroviejo-Fisher.



FIGURE 8. Distribution maps of (A) Centrolene gorzulai; (B) Cochranella helenae; and (C) Hyalinobatrachium taylori in Guyana. Red dot = Kaieteur National Park.

COCHRANELLA HELENAE (Ayarzagüena, 1992) Figs 5c–d, 9 Centrolenella helenae Ayarzagüena 1992: 21 Cochranella helenae Duellman 1993: 45 Hyalinobatrachium helenae La Marca 1995: 60 Cochranella helenae Señaris & Ayarzagüena 2005: 113 Cochranella oyampiensis Señaris & Ayarzagüena 2005: 118

Holotype and type locality. MHNLS 9431 (adult male), Venezuela, Estado Bolívar: San Ignacio de Yuraní: Quebrada de Jaspe (04°55’ N, 61°05’ W; 800–1000 m). Material from Kaieteur National Park. IRSNB 13979–80 (2 males). Diagnosis. Cochranella helenae differs from other species in the family by the following combination of characters: (1) dentigerous process on vomer and vomerine teeth absent or present; (2) bones pale green in life; (3) in preservative, dorsum light lavender covered with melanophores (punctuations) and a few larger dark purple flecks; anterior third of parietal peritoneum white, covering anterior part of the abdomen (heart not visible); pericardial peritoneum white; hepatic (but see below) and visceral peritonea white, except for the transparent urinary bladder; (4) in life, dorsum pale lime green to greenish yellow heavily speckled with minute dark green punctuations and a few larger dark brown flecks; (5) finger webbing II 2+–3 III (1½–2-)–2IV; (6) toe webbing I 1–2 II 1–2- III 1–2+ IV 2-–1 V; (7) snout round in dorsal view, sloping in lateral profile; (8) dorsal skin shagreened, ventral skin granular; (9) fringe on postaxial edge of Finger IV present, metacarpal fold absent, ulnar fold absent; fringe on postaxial edge of Toe V present on first phalange only, metatarsal fold absent or very low, tarsal fold absent; (10) humeral spine in adult males absent; (11) tympanum distinct, oriented posterodorsally with a slight lateral inclination; (12) SVL in males 19.6–20.2 mm (mean = 19.9, n = 2); (13) prepollical spine concealed in radial side of base of Finger I; nuptial excrescences finely granular, unpigmented, elliptical, on dorsolateral surface of Finger I (Type-I); (14) anal ornamentation consisting of small tubercles posterior to vent, and paired enlarged round tubercles below vent; (15) when appressed, Finger II GLASSFROGS OF KAIETEUR NATIONAL PARK


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almost equal in length to Finger I; (16) liver trilobate; (17) diameter of eye about 3X width of disc on Finger III; (18) males call from the upper side of leaves; (19) advertisement calls of two or three short pulsed notes. Comparisons. Cochranella helenae differs from all the species of the genus Hyalinobatrachium by having at least 1/3 of the parietal peritoneum white anteriorly and a trilobate liver. All species of the genus Centrolene have humeral spines in adult males and transparent hepatic peritonea, except C. gorzulai and C. mariaelenae. Centrolene mariaelenae can be differentiated from Co. helenae by its completely transparent parietal peritoneum, and C. gorzulai by having the white coloration restricted to the most anterior part of the parietal peritoneum and not extending down to at least 1/3 of the parietal peritoneum as in Co. helenae. All other species of Cochranella have transparent hepatic peritonea except Co. castroviejoi Señaris and Ayarzagüena, 1996, but that species has a truncate snout in profile and dorsal yellow spots in life (white in preservative). In Kaieteur National Park, Cochranella helenae is the only Glassfrog species with a white parietal peritoneum and a yellow iris. Hand and foot of the species are illustrated in Figure 9. Color in life. Dorsal surfaces light lime green to greenish yellow and heavily speckled with minute dark green punctuations, except on upper lip and upper arms, the skin of the latter being transparent white (Fig. 5c). Speckling slightly less on snout, limbs and cloacal region. Eyelids greenish yellow. Fingers and toes transparent bluish green, no speckling on Fingers I–III and Toes I–III. Numerous (24–27) large dark brown flecks on dorsum of head and body. Bones green. Iris yellow, heavily speckled with minute dark brown punctuations; a thin, incomplete white ring encircles the pupil. Upper flanks greenish yellow. Skin on lower flanks and venter transparent, parietal peritoneum white, covering anterior part of abdomen (heart not visible). Internal organs visible through the skin, white (Fig. 5d). Color in preservative. Dorsum of head and body pale lavender, thin cream line on upper lip. Dorsum of head and body heavily speckled with minute pale purple chromatophores (punctuations), speckling less on snout, limbs and cloacal region, absent on upper arms. As observed in Centrolene gorzulai, some small white (on body) to bright light blue (on eyelids) “warts” are visible under magnification. Dorsally Fingers I–III and Toes I–III unpigmented. Eyelids and eyes dark lavender. Twenty-four to 27 larger dark purple flecks on dorsum of head and body. Venter cream, semitransparent. Bones white (green pigments are lost in preservative). Cream nuptial pad on Finger I. Parietal peritoneum white, covering one-third of the anterior part of the abdomen (heart not visible, unless parietal peritoneum removed), pericardial, hepatic and visceral peritonea white, except for the transparent urinary bladder. Note that the hepatic peritoneum is transparent in the posterior corner of the posterior lobe (Fig. 10b), which was already observed by Señaris and Ayarzagüena (2005: 113). Taxonomic comments. Specimens from Kaieteur National Park are very similar to specimens from the type locality. It should be noted that both the original description (Ayarzagüena 1992) and subsequent description by Señaris and Ayarzagüena (2005) do not mention the presence of enlarged subcloacal tubercles. Señaris and Ayarzagüena (2005) even explicitly mentioned “sin tubérculos infracloacales” (without infra-cloacal tubercles), although these tubercles are found in specimens from Kaieteur [IRSNB 13979–80] and in two specimens from the type locality [MHNLS 17129–30]. Nevertheless, Señaris and Ayarzagüena (2005: 121) mentioned these tubercles for Co. oyampiensis from Venezuela. As stated above, this character is easily overlooked and prone to change after preservation. The original description (Ayarzagüena 1992) of Co. helenae contains several inaccuracies in addition to those aforementioned. Ayarzagüena (1992) pointed out the lack of post-cephalic constriction - a very poor diagnostic character probably prone to post-mortem modification or to change after preservation - but some preserved specimens we examined have a strong post-cephalic constriction, while others have none at all. Living specimens also may have or not have a more or less distinct postcephalic constriction. The same author describes ventral and dorsal skin as smooth, while it is actually shagreened on dorsum and granular on venter (as confirmed by examination of specimens from the type locality and as also stated by Señaris & Ayarzagüena 2005). Ayarzagüena (1992) also mentioned quadrangular choanae (another unreliable diagnostic character), although they are rounded (as confirmed by examination of specimens from the type locality and as also stated by Señaris & Ayarzagüena 2005).



FIGURE 9. Hand (left) and foot (right) of Cochranella helenae (IRSNB 13980) from Kaieteur National Park, Guyana. Scale bars = 2 mm. Photographs Philippe J. R. Kok.

FIGURE 10. (A) Internal organs of Cochranella oyampiensis (MSH 2776, Tafelberg, Suriname) showing condition of peritonea: blue arrow indicates parietal peritoneum with anterior third white (posterior two-thirds transparent), black arrow indicates only a few white pigments on the anterior part of the transparent hepatic peritoneum; (B) internal organs of Cochranella helenae (IRSNB 13980, Kaieteur National Park, Guyana) showing condition of peritonea: blue arrow indicates parietal peritoneum with anterior third white (posterior two-thirds transparent), black arrow indicates hepatic peritoneum mostly covered with white pigments (a small portion of the posterior lobe is transparent). Photograph Philippe J. R. Kok.



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Cochranella helenae was assigned to the Cochranella oyampiensis species group, created by Señaris and Ayarzagüena (2005) to accommodate species of Cochranella having a white hepatic peritoneum. They named the group according to the oldest species described; however they did not determine whether the type of Co. oyampiensis possesses a white hepatic peritoneum. Instead they identified three specimens collected in Venezuela (Salto Karuay, Estado Bolívar) as Co. oyampiensis based on the presence of vomerine teeth (reported as absent in Co. helenae) and an advertisement call of two notes (three in Co. helenae). We examined five specimens of Co. oyampiensis (including the only paratype), photographs of living Co. oyampiensis from French Guiana, the holotype and five topotypes of Co. helenae and four specimens of Co. oyampiensis sensu Señaris and Ayarzagüena (2005) from the same locality as their material. The results show that Co. oyampiensis (Figs. 10a, 11a–b) is a species with transparent hepatic peritoneum that has been reported from French Guiana, Suriname and Brazil (Lescure 1975; Frost 1985; Zimmerman & Rodrigues 1990; Lescure & Marty “2000” [2001]). Examination of three dissected specimens from Suriname confirmed this observation, even though we observed a few white pigments visible on the anterior part of the liver and around its periphery (Figs. 11a– b). The specimens from French Guiana, including the paratype, are in bad state of preservation and were left undissected. We also found that some of the material identified as Co. oyampiensis by Lescure and Marty (“2000” [2001]) is indeed Co. midas (Fig. 3c–d), a species previously unknown from French Guiana. Furthermore, the advertisement call described in Lescure and Marty (“2000” [2001]) corresponds to that of Co. midas (Fig. 11a–b); therefore the call of Co. oyampiensis apparently remains undescribed. Conversely, the specimens identified by Señaris and Ayarzagüena (2005) as Co. oyampiensis are indeed Co. helenae. We found that one topotype of Co. helenae has vomerine teeth (MHNLS 17127) and that one specimen from Salto Karuay lacks them (MHNLS 17137). Thus, it seems that there is inter- and intrapopulation variability in this character. Similarly, Señaris and Ayarzagüena (2005) indicated that 17% of the calls of Co. helenae from the type locality have three notes, a fact that we also noted in some specimens from Salto Karuay. We observed that a same specimen might emit calls with two or three notes. The molecular data support our results. Genetic distances between the specimens from the three localities are minimal and all sequences cluster together in a highly supported clade that indicates no significant differentiation between its terminals (Fig. 4). Distribution and ecology. Prior to this work Cochranella helenae was known only from its type locality in Venezuela (Ayarzagüena 1992; Señaris & Ayarzagüena 2005). The specimens from Kaieteur National Park extend the species’ range eastward by about 180 km (Fig. 8) and those from Salto Karuay in Venezuela, Estado Bolívar (previously identified as Co. oyampiensis by Señaris & Ayarzagüena 2005), see above] by about 100 km towards the northwest. The first specimen from Kaieteur National Park was located by call, at night, and was on a leaf, about 1.8 m above ground, along a small cascading stream (Fig. 12). The collecting site is in a small clearing (open canopy, full sunlight and high temperature during the day), close to a Brocchinia micrantha field. Another male was heard but escaped. The call consisted of three fast, short notes (not recorded) and, to the ear, is identical to the one described in Señaris and Ayarzagüena (2005). No more specimens were heard or seen at that locality on following nights. The second specimen was also located by call (call identical to that of previous specimen) at night, along the Potaro River, about 8.0 m above ground in a tree overhanging the water. Several specimens were calling at the same site but we failed to collect more than one specimen due to the difficulty of reaching the frogs. The species was also heard calling farther upstream on the Potaro River, near the Amakwa River mouth (Fig. 1). Apparently Co. helenae prefers the vicinity of large rivers (Fig. 13), where it is often syntopic with Hyalinobatrachium taylori, but it may also be encountered along small cascading streams in open areas. Both specimens were collected at about 440 m elevation.



FIGURE 11. (A) Ventral view of Cochranella oyampiensis in life; (B) dorsal view of the same specimen in life (MB292, Aya/Trinité, French Guiana); (C) ventral view of Cochranella midas in life (MB299, Aya/Trinité, French Guiana); (D) dorsolateral view of Cochranella midas in life (MB204, Crique Grand Leblond, French Guiana). Photographs courtesy of Michel Blanc.

FIGURE 12. Vegetation along a small cascading stream in open situation, occasional habitat of Cochranella helenae in Kaieteur National Park, Guyana. Photograph Philippe J. R. Kok.



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HYALINOBATRACHIUM TAYLORI (Goin, 1968) Figs. 5e–f, 14 Centrolenella taylori Goin 1968: 115 Hyalinobatrachium taylori Ruiz-Carranza & Lynch 1991a: 25

Holotype and type locality. BMNH 1939.1.1.65 (adult male), Guyana: Along New River (ca. 228 m). Material from Kaieteur National Park. IRSNB 13981–7 (7 males). Diagnosis. Hyalinobatrachium taylori differs from other species in the family by the following combination of characters: (1) dentigerous process on vomer and vomerine teeth absent; (2) bones translucent green in life; (3) in preservative, dorsum lavender with numerous small white dots; parietal peritoneum transparent; pericardial peritoneum partially transparent, most areas covered with white pigment; hepatic and visceral peritonea white, except for the transparent urinary bladder; (4) in life, dorsum dark green with pale green spots usually bearing a white fleck in the center of each spot; (5) finger webbing III (1–2) IV (1–2-); (6) toe webbing I 1–(2-–2+) II 1–(2-–2) III 1–(2–2+) IV (2-–2+)–1 V; (7) snout rounded in dorsal view, truncate to slightly obtuse in lateral profile; (8) dorsal skin smooth to finely shagreened, venter granular; (9) fringe on postaxial edge of Finger IV present, enameled, metacarpal fold present, enameled, ulnar fold present, enameled; fringe on postaxial edge of Toe V present, enameled, metatarsal fold present, enameled, tarsal fold present, enameled; (10) humeral spine in adult males absent; (11) tympanum barely visible in life; (12) SVL in males 18.8– 20.5 mm (mean = 19.3, n = 7); (13) prepollex not enlarged, no prepollical spine, nuptial excrescences granular, orange-colored, comprised of a dense group of glands and situated in the medial, dorsolateral internal side of Finger I and extending externally to the base of the disc; glands are also present on webs and fringes of Fingers II, III and IV (Type-V); (14) anal ornamentation consisting of enameled tubercles posterior to vent, no enlarged round subcloacal tubercles; (15) when appressed, Finger II much shorter than Finger I; (16) liver bulbous; (17) diameter of eye about 2X width of disc on Finger III; (18) males call from the upper side of leaves; (19) advertisement call 5–8 short notes. Comparisons. Hyalinobatrachium taylori can be distinguished from all members of the genus Centrolene by the absence of humeral spine in males; species in the genus Cochranella have a non bulbous liver (tri- or tetralobate); species in the Hyalinobatrachium fleischmanni Group have white bones in life, those of the Hyalinobatrachium parvulum Group have a white peritoneum covering the urinary bladder and species of the Hyalinobatrachium pulveratum Group have vomerine teeth. In Kaieteur National Park, H. taylori is easily distinguished from other centrolenid frogs by its translucent green bones, green dorsal coloration with pale dots and white flecks, pericardium only partially transparent, absence of humeral spine in males, and Finger I much longer than Finger II (Fig. 14). Color in life. Dorsum dark green with pale green spots usually bearing a white fleck in the center of each spot; white flecks are sometimes outside the pale spots (Fig. 5e). Several bronze flecks and/or lines may be present on dorsal surfaces (some congruent with scar tissue). Elbow and tibio-tarsal articulations usually bronze, sometimes pale green. Forearms and hind limbs slightly paler than dorsum, heavily speckled with minute dark green punctuations and paler flecks; skin of upper arms translucent, without chromatophores. All fingers and Toes I–III transparent; distal phalanges and fringes of digits orange; dark green chromatophores often visible on Toes IV–V, which may be transparent or with similar coloration to hind limbs. Nuptial excrescences orange. White spotting usually more extensive on hind limbs, less on forelimbs and head. Bones translucent green. Iris metallic lavender with dark brown reticulations and a few bronze punctuations; an incomplete pale yellow ring around pupil. Upper flanks translucent green to greenish bronze with scattered dark green punctuations. Skin on lower flanks and venter transparent, parietal peritoneum transparent, heart partly visible, pericardial peritoneum mostly white with some transparent areas. Internal organs visible through the skin, white (Fig. 5f).



FIGURE 13. Riparian vegetation along a large river (here the Potaro River), typical habitat of Cochranella helenae, Hyalinobatrachium taylori and Hyalinobatrachium sp in Kaieteur National Park, Guyana. Photograph Philippe J. R. Kok.

FIGURE 14. Hand (left) and foot (right) of Hyalinobatrachium taylori (IRSNB 13984) from Kaieteur National Park, Guyana. Scale bars = 2 mm. Photographs Philippe J. R. Kok.



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Color in preservative. Dorsal surfaces of head, body, forearms, part of legs (on thighs, restricted to a narrow band on the dorsal surface) and outer fingers lavender in the oldest specimen (about three years in 70% alcohol), light green in recently collected specimens (after three months in 70% alcohol); thin cream line on upper lip. Dorsal surfaces that are lavender/light green are covered with melanophores and numerous small rounded white spots. Eyes dark lavender, a dark lavender spot on eyelids present in most specimens. Fringes and folds on hand, ulna, foot and tarsus covered with a white-pigmented line. Dorsally fingers and Toes I–III unpigmented, except on the proximal part of Finger IV, which bears a few melanophores; Toes IV–V usually covered with melanophores. All other surfaces cream, venter semitransparent. Bones white (green pigments are lost in preservative). Whitish nuptial pad on Finger I. Parietal peritoneum transparent; pericardial peritoneum partly transparent, mostly covered with white pigment (heart partly visible), in specimens that have been preserved for long periods (more than a year) the pericardium looks completely white and the transparent areas can be observed only after dissection; hepatic and visceral peritonea white, except for the transparent urinary bladder. Taxonomic comments. Our specimens conform to the original description (Goin 1968), the description in Señaris and Ayarzagüena (2005) and the type specimens. As pointed out by Señaris and Ayarzagüena (2005), it is evident that Lescure (1975), Hoogmoed and Avila-Pires (1991) and Lescure and Marty (“2000” [2001]) confused at least two distinct species under the name Hyalinobatrachium taylori. Noonan and Bonett (2003) introduced some additional confusion by indicating that tarsal folds are absent (instead of present) and that pericardial peritoneum is white (in part only) in H. taylori. The taxonomy of the Hyalinobatrachium taylori species complex will be addressed elsewhere (Castroviejo-Fisher et al. submitted), meanwhile we use the name H. taylori in a sensu lato fashion, that is, to accommodate specimens of at least two species. Hyalinobatrachium taylori was not assigned to any species group by Señaris and Ayarzagüena (2005), and we cannot confidently assign this species to a group. Distribution and ecology. Hyalinobatrachium taylori is known across the Guiana Shield: from French Guiana (see comments by Señaris & Ayarzagüena 2005), through Suriname and Guyana to Bolívar and Amazonas, Venezuela between 30–1850 m (Señaris & Ayarzagüena 2005). In Guyana the species was known only from the type locality: New River (Fig. 8) (see comments about the type locality in Noonan & Bonett 2003). All individuals were collected calling by night, between 1.0–10.0 m above the ground, on leaves above or along large rivers (Fig. 13) at elevation ca. 440 m. The call was recorded and is similar to the one described by Señaris and Ayarzagüena (2005). Discussion The presence of well-developed membranes between Fingers III–IV, combined with a mostly transparent hepatic peritoneum lead us to place Cochranella oyampiensis in the Co. spinosa Group. This action leaves only two species in the former oyampiensis species group (according to criteria in Señaris & Ayarzagüena 2005): Co. castroviejoi and Co. helenae. Hence, we rename this group the Cochranella helenae Group, diagnosed by the following characters: anterior third of parietal peritoneum white, white peritoneum covering liver, viscera and heart, eye diameter > transverse diameter of disc of Finger III, dentigerous process on vomer and vomerine teeth present or absent, bones green. These changes do not necessarily imply any phylogenetic affinity and we just use the name helenae Group to stress the similarity between its species, which we believe facilitates species comparisons, identification and description. Phylogenetic studies including several species of Centrolenidae (Darst & Cannatella 2004; Faivovich et al. 2005; Wiens et al. 2005; Frost et al. 2006; Grant et al. 2006; Guayasamin et al. 2006a) indicate that Centrolene, Cochranella and Hyalinobatrachium (sensu Ruiz-Carranza & Lynch 1991a–b, 1995a, 1998) are nonmonophyletic groups; although there are some contradictory results concerning Hyalinobatrachium, which is supported as monophyletic by phenotypic data (Guayasamin et al. 2006a) but as non-monophyletic by molec-



ular data (Faivovich et al. 2005). Nevertheless, none of the studies mentioned above proposed taxonomic changes due to the low number of species included in the molecular analyses or the lack of resolution and limited number of morphological characters (Frost et al. 2006; Guayasamin et al. 2006a). Cisneros-Heredia and McDiarmid (2007) contradicted this conservative approach and created the genus Nymphargus. CisnerosHeredia and McDiarmid (2007: 35) stated that: “Although present evidence is insufficient to allow an exhaustive phylogenetic hypothesis to solve this problem, the recognition of Nymphargus as a monophyletic group is the first step, and concerns about future improvements in our knowledge should not prevent present progress”. However, Cisneros-Heredia and McDiarmid (2007) did not include any phylogenetic analysis, their study was based on phenetic similarities and suggested just a single putative synapomorphy: reduced or absent webbing between fingers, which is actually present in other species of Centrolenidae [e.g. C. balionotum, Co. vozmedianoi Ayarzagüena & Señaris, “1996” (1997), C. buckleyi (Boulenger, 1882)]. Furthermore, the genus Nymphargus includes all the species of the Cochranella ocellata Group except two [Co. ocellata (Boulenger, 1918) and Co. vozmedianoi] and none of the cladistic analyses including this species group support its monophyly (Ruiz-Carranza & Lynch 1991a, 1995a; Guayasamin et al. 2006a); hence, the validity of Nymphargus as a clade remains unsolved. Species groups in Centrolenidae cluster phenetically similar species to help in their identification and description (Ruiz-Carranza & Lynch 1991a; Cisneros-Heredia & McDiarmid 2007). They are based on a set of diagnostic phenotypic characters. Some species groups are not diagnosable and show no utility. For instance, Centrolene geckoideum and Centrolene peristictum Groups are not diagnosable from the Centrolene prosoblepon Group, and the Hyalinobatrachium chirripoi subgroup is not diagnosable from the remaining species of the Hyalinobatrachium fleischmanni Group (Noonan & Harvey 2000; Guayasamin et al. 2006a; Cisneros-Heredia & McDiarmid 2006a, 2007). However, we argue that in the context of the generic classification of Ruiz-Carranza and Lynch (1991a–b, 1995a, 1998) – where Centrolene includes those species in which adult males exhibit humeral spine, Hyalinobatrachium those species with transparent parietal peritoneum and bulbous liver covered with white hepatic peritoneum, and Cochranella those species without humeral spine in adult males and lobed livers – the phenetic species groups gorzulai and prosoblepon in Centrolene; granulosa, helenae, ocellata and spinosa in Cochranella; fleischmanni, parvulum and pulveratum in Hyalinobatrachium are diagnosable and helpful for species comparisons. We clearly need a phylogenetic analysis of centrolenid frogs based on molecular data to properly evaluate their taxonomy. However, and until such a study is available, we recommend caution about making taxonomic changes because there is a high risk of promoting name instability without guarantees of implementing a monophyletic taxonomy. Cochranella ametarsia Flores, 1987 was distinguished from Co. oyampiensis by a set of characters that we consider erroneous. Flores (1987) stated that Co. ametarsia has: (i) a transparent parietal peritoneum (white in Co. oyampiensis), but in both species the anterior third is white and the posterior two-thirds transparent (Fig. 10a; described as white by Guayasamin et al. 2006b); (ii) white visceral peritonea (transparent in Co. oyampiensis), but the Co. oyampiensis examined have white visceral peritonea; (iii) lower two-thirds of tympanum exposed (concealed in Co. oyampiensis), but in the Co. oyampiensis examined at least the lower twothirds of the tympanum is exposed; (iv) a distinct prepollex (concealed in Co. oyampiensis), but the Co. oyampiensis examined have distinct prepollex. These observations indicate that both species are similar in their morphology and that Co. ametarsia could be a junior synonym of Co. oyampiensis. However, this hypothesis needs further studies (see Cisneros-Heredia & McDiarmid 2007). We report Cochranella midas for the first time from the Guiana Shield; specimens of this species from French Guiana were identified as Co. oyampiensis by Lescure and Marty (“2000” [2001]). The characteristic yellow spots of Co. midas were treated as a variable character of Co. oyampiensis. The discovery of Co. midas in French Guiana highlights the species’ extensive distribution, from Ecuador to southern Peru and western Brazil (Lynch & Duellman 1973; Cisneros-Heredia & McDiarmid 2005, 2006a). The distributional gap



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between western Brazil and French Guiana may be an artifact of sampling effort and misidentifications with Co. oyampiensis; however, the possibility that Co. midas consists of several cryptic species must also be considered. We report the first records of Hyalinobatrachium nouraguense from Suriname (Sipaliwini District), based on identification of uncatalogued specimens that PJRK examined with Marinus S. Hoogmoed (MPEG) during a visit to RMNH (but see comments on this species by Ernst et al. 2005). The specific epithet refers to the type locality, Réserve des Nouragues; because Hyalinobatrachium is neuter in gender, the correct combination is nouraguense. The records from Suriname extend the range ca. 500 km to the west. During fieldwork in Kaieteur National Park an unidentified and uncollected species of Hyalinobatrachium was detected by its advertisement call. We compared the audiospectogram and oscillogram of this call (Fig. 3d) to those described in the literature and to our own recordings for species of Hyalinobatrachium from the GS, and conclude that the call resembles the one described for H. mondolfii (Señaris & Ayarzagüena 2001, 2005) (Fig. 3c). Therefore, we consider the presence of H. mondolfii in Guyana as likely; this species is presently known from ca. 420 km NW of Kaieteur National Park. Furthermore, photographs of H. ignioculus and H. crurifasciatum (treated as H. taylori sensu Lescure & Marty [“2000” (2001): 79], see remark above) were recognized by indigenous people as being present in Kaieteur. Ernst et al. (2005) found H. aff. ignioculus in Mabura Hill Forest Reserve, Guyana (5°13’N, 58°48’W; ca. 76 km NE of Kaieteur). This evidence supports the presence of H. crurifasciatum in Kaieteur National Park. However voucher material (i.e. pictures, specimens) is needed to confirm the identity of the species, especially if we take into account the confusing taxonomy of H. crurifasciatum and allies (H. eccentricum and H. ignioculus). A detailed review of the frogs of the family Centrolenidae in the Guiana Shield is beyond the scope of this paper. However, during our study of the Glassfrogs from the area we came across several taxonomic problems, and it became clear that there is much confusion surrounding the identity of several Guiana Shield centrolenid species. Some were described on the basis of relatively poor diagnostic characters and older descriptions were often overlooked. Deficient descriptions, and the difficulty of obtaining type specimens for comparison have exacerbated the situation. As mentioned above, centrolenids have fragile skin that is easily subject to damage during handling and modification after preservation. Extensive field notes (and if possible photographs of the animal in life) are therefore important because some characters may disappear after a few days in preservative. Many of these characters are of diagnostic importance and may thus lead to misidentifications. We noticed that some preservation techniques and heat (including sunlight) could destroy the white pigments on peritonea and thus lead to mistakes in description of specimens. Some authors used diagnostic characters that are best avoided (i.e. postcephalic constriction). We recommend comparing putative new species with type series of similar species because some original descriptions are inaccurate or deficient. In the light of recent discoveries, it appears that species that were thought to occur at high elevation only and/or having restricted distribution may be much more widespread than expected. It is therefore important to compare material not only with species that occur nearby, but also with all the species phenotypically similar. Several taxonomic problems concerning the validity of some species of Glassfrogs from the Guiana Shield await resolution: (1) Hyalinobatrachium ignioculus and H. eccentricum are candidates to be synonyms of H. crurifasciatum; (2) Hyalinobatrachium nouraguense is a putative synonym of H. iaspidiense; (3) Centrolene lema is likely conspecific with C. gorzulai; (4) the name Hyalinobatrachium taylori is used to designate at least two different species; (5) the presence of Hyalinobatrachium fleischmanni in the Guiana Shield is dubious and the name cappellei is available for that species (Noonan & Harvey 2000; Noonan & Bonett 2003; Señaris & Ayarzagüena 2005; Cisneros-Heredia & McDiarmid 2007; Castroviejo-Fisher unpublished data). Additionally, molecular evidences (Castroviejo-Fisher unpublished data) indicate the presence of potential morphologically cryptic species. A detailed taxonomic review of the Glassfrogs from the Guiana Shield is highly recommendable and seriously needed.



Key to the identification of species of Centrolenidae from Guyana 1. Anterior third of parietal peritoneum white, dorsum light lime green with a few small black flecks........... ......................................................................................................................................Cochranella helenae Parietal peritoneum transparent (from external view and without dissection) ............................................ 2 2. Prepollex distinct, humeral spine present in adult males, dorsum dark green ............... Centrolene gorzulai Prepollex concealed, humeral spine absent in adult males.......................................................................... 3 3. Snout sloping in profile, bones translucent green, dorsum green with small whitish spots .......................... ............................................................................................................................ Hyalinobatrachium taylori Snout truncate in profile, bones white and dorsum not as above ................................................................ 4 4. Yellow round spots on dorsum (cream in preservative) ............................... Hyalinobatrachium ignioculus Irregular lime green areas on dorsum (white in preservative) and black dots............................................... .................................................................................................................. Hyalinobatrachium nouraguense

Acknowledgements Thanks are due to Indarjit Ramdass, Ramesh Lilwah and Annie Pitamber (Environmental Protection Agency, Guyana), Michelle Kalamandeen, Kristine Erskine, Kaslyn Holder and Calvin Bernard (University of Guyana) for help in obtaining export permits for the specimens; to the Nyron Rahaman family for logistic help at Menzies Landing; to Deokie Arjoon, Paul Benjamin, Michelle Kalamandeen, Indranee Roopsind, Hemchandranauth Sambhu, Solomon “Jack” Garcia (who has uncommon tree climbing skills), Rafael Antelo, José Ayarzagüena, Daniel González, Jose María Castroviejo and Jose Ruíz for field assistance and companionship; to Jackie Van Goethem, Anne Franklin and Yves Samyn (Belgian Focal Point to the Global Taxonomy Initiative, IRSNB) for support of PJRK capacity building activities; to Georges Lenglet (IRSNB) for his support and collaboration in the Global Taxonomy Initiative project; to Ross MacCulloch (ROM) and Celsa Señaris (MHNLS) for kindly supplying some literature; to Michel Blanc for photographs of Cochranella midas and Co. oyampiensis and for tissue samples of Co. oyampiensis; to Rafael Márquez (MNCN), Morley Read, Christian Marty and Philippe Gaucher for access to the recordings; to Juan Manuel Guayasamin (QCAZ) and Diego Cisneros-Heredia (Universidad San Francisco de Quito, Ecuador) for comments on the morphology of Co. ametarsia; and to Marinus Hoogmoed (MPEG) for interesting and constructive discussions and for helpfully providing accommodation to PJRK during a visit to RMNH. For the loan or exchange of specimens under their care we thank Annemarie Ohler and Laure Pierre (MNHNP), Celsa Señaris and Gilson Rivas (MHNLS), J. van Egmond (RMNH), and Jon Campbell and Carl Franklin (UTA). Collection and genetic permits from Venezuela were negotiated by the MHNLS, this study is included in the “Contrato Marco de Acceso a Recursos Genéticos N° 0001, 11 Enero 2007” subscribed between Fundación La Salle de Ciencias Naturales and the Ministerio del Ambiente, Venezuela, to which we are thankful for its help. The financial support of the Belgian Directorate-General of Development Cooperation (to PJRK) and the enthusiast help and support of the Prime Minister of Guyana, Honorable Samuel Hinds are gratefully acknowledged. This work was additionally supported by grants (to SCF) from the Estación Biológica El Frío, Asociación Amigos de Doñana and its director Javier Castroviejo Bolíbar, Stiftelsen Sven och Lilly Lawskis, Helge Ax:son Johnsons Stiftelse Foundation and the Swedish Research Council (SCF granted to Carles Vilà). Permission to conduct this study in Kaieteur National Park was granted by Shyam Nokta and Inge Nathoo of the Guyana National Parks Commission, with research and collection permits issued by the Guyana EPA (research permits 180604BR011, 030605BR006, 160107BR068; export permits 100804SP010, 191205SP011, 040406SP014, 010207SP001). Finally we are indebted to Ross MacCulloch and an anonymous reviewer for providing helpful comments that improved the manuscript.



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Appendix: Additional specimens examined Centrolene gorzulai: VENEZUELA: Estado Bolívar: Central sector of Auyan-tepui (05°56’ N, 62°34’ W; 1850 m): MHNLS 11221 (holotype); West-central sector of Auyan-tepui (05°54’ N, 62°38’ W; 1850 m): MHNLS 12482 (holotype of C. auyantepuiana) EBD 2824–5 (paratypes of C. auyantepuiana); Auyan-tepui, Campamento Uayaraca (05°41’06’’ N, 62°31’32’’ W; 1005 m): MHNLS 17325–6. GUYANA: Potaro-Siparuni district: Peters Mountain, 3.6 km N Imbaimadai: UTA 52233, 52243 (paratypes of Centrolene papillahallicum). Centrolene lema: VENEZUELA: Estado Bolívar: Kilometer 127 on the El Dorado-Santa Elena de Uairén road (860 m), MHNLS 17267, 17142 (topotypes). Cochranella castroviejoi: VENEZUELA: Estado Sucre: Cerro El Humo, Quebrada las Melenas (10°42’ N, 62°37’ W; 750 m): MHNLS 17289–91, 17293, 17300, 17303–4, 17306, 17308–11, RMNH 28421, RMNH 28423 (all topotypes). Cochranella helenae: VENEZUELA: Estado Bolívar: Gran Sabana, Quebrada Jaspe (04°55’ N, 61°05’ W; 800–1000 m): MHNLS 9431 (holotype), 17127–30, IRSNB 13988 (ex MHNLS 17988); Salto Karuay, Karuay river (05°41’27’’ N, 61°51’40’’ W; 900 m): MHNLS 17136–40. Cochranella midas: FRENCH GUIANA: Petit Saut: MNHNP 1997.2200 (previously identified as Cochranella oyampiensis). PERU: Departamento Cusco: JCC 3457. Cochranella oyampiensis: FRENCH GUIANA: Grigel (Rivière Ouaqui): MNHNP 1973.1674 (paratype); Saut Eleupoucing: MNHNP 2003.1598; SURINAME: Sipaliwini district: Tafelberg: MSH 2538, 2750, 2776. Hyalinobatrachium iaspidiense: VENEZUELA: Estado Bolívar: Gran Sabana, Quebrada Jaspe (04°55’ N, 61°05’W; 800-1000 m): EBD 28803 (holotype), 28804 (paratype), MHNLS 17126 (topotype); Estado Delta Amacuro: First stream of Caño Acoima, tributary of río Grande, slopes of Serranía de Imatáca (08°22’ N, 61°32’ W; 15 m): MHNLS 17118. Hyalinobatrachium ignioculus: GUYANA: Potaro-Siparuni district: Peters Mountain, ca. 3.4 km N Imbaimadai: UTA 51658, 51661–2 (paratypes). Hyalinobatrachium nouraguense: FRENCH GUIANA: Saut Arataye, Bassin de l’Approuague: MNHNP 1999.8604, 1999.8605 (holotype and paratype respectively); Pic Matécho: MNHNP 2000.5172; Saut Ipouang: MNHNP 2003.1620. SURINAME: Sipaliwini district: Vreedzaamkreek, 14 km N Lucie rivier: MSH 504 (2 specimens); 10 km N Lucie rivier: MSH 570 (3 specimens); Kabalebo, eerste boetoe: MSH 1127; Loekreek, kamp Hofwijks: MSH 1551 (all previously unidentified). GUYANA: Mabura Hill Forest Reserve, Maiko creek (N 05°09' 19.30" N, 58° 41' 58.96" W; 60 m): SMNS 12247. Hyalinobatrachium taylori: FRENCH GUIANA: Petite Montagne Tortue near Régina: MNHNP 1995.1782; Camp de Saint Eugène: MNHNP 1997.2199; Montagne St Marcel: MNHNP 2003.1640. SURINAME: Sipaliwini district: Marowijne River: RMNH 11472 (paratype); Nassaugebergte: RMNH 11473 (paratype); Langa Soela on the Paleomeu River at the base of Grensgebergte: RMNH 11474 (paratype); Tafelberg: MHS 2490; Amotopo: MSH 3280, 3395. VENEZUELA: Estado Bolívar: RMNH 26988; Salto Karuay, Karuay river (05°41’27’’ N, 61°51’40’’ W; 900 m): MHNLS 17141; Gran Sabana, Quebrada Jaspe (04°55’ N, 61°05’ W; 800–1000 m): MHNLS 17279, 17281–2.



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