BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions,research libraries, and research funders in the common goal of maximizing access to critical research.

The Tadpole of Nymphargus Grandisonae (Anura, Centrolenidae) from ValleDel Cauca, ColombiaAuthor(s) :Jhon Jairo Ospina-Sarria, Wilmar Bolíívar-G., Javier Mendez-Narvaez, Carlos Burbano-YandiSource: South American Journal of Herpetology, 6(2):79-86. 2011.Published By: Brazilian Society of HerpetologyDOI: 10.2994/057.006.0206URL: http://www.bioone.org/doi/full/10.2994/057.006.0206

BioOne (www.bioone.org) is a a nonprofit, online aggregation of core research in the biological, ecological,and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and bookspublished by nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance ofBioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercialinquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

THE TADPOLE OF NYMPHARGUS GRANDISONAE (ANURA, CENTROLENIDAE)FROM VALLE DEL CAUCA, COLOMBIA

JHON JAIRO OSPINA-SARRIA1,4, WILMAR BOLÍVAR-G.2, JAVIER MENDEZ-NARVAEZ3, CARLOS BURBANO-YANDI2

1 Instituto de Ciencias Naturales, Laboratorio de Anfibios, Universidad Nacional de Colombia, Bogotá, Colombia.2 Universidad del Valle, Departamento de Biología, Grupo de investigación en Ecología Animal. A.A. 25360, Cali, Colombia.

3 Departamento de Ciencias Biológicas, Grupo de Ecofisiología, Comportamiento y Herpetología,Universidad de los Andes, A.A. 4976, Bogotá, Colombia.

4 Corresponding author: sarriajhon@gmail.com

ABSTRACT. The tadpole of Nymphargus grandisonae is described from Serranía de los Paraguas, Valle del Cauca-Colombia. Characteristics of clutches (i.e., position, coloration, number of ova) and ontogenetic variation, as well as some aspects of natural history of adult males, are provided. The tadpole of N. grandisonae differs from other centrolenid tadpoles in characteristics such as M-shaped upper jaw sheath, small gap in row A-2, and by having a non-emarginate oral disc. Although it has been proposed that the lack of morphological differences in glassfrog tadpoles is due to ecomorphological convergence, the number of tadpole descriptions based on feeding specimens is limited, as is the number of comparative studies of larval anatomy. Additional standardized studies of larval characters and subsequent phylogenetic analysis are required to test this hypothesis.

KEYWORDS. Amphibia; Larva; Glassfrog; Morphology.

INTRODUCTION

Glassfrogs breed out of the water and females lay their eggs on leaves, branches, and mosses overhang-ing water or on stones next to streams and waterfalls (Ruiz-Carranza and Lynch, 1991). After hatching, tadpoles fall into the water and seek refuge within leaf litter and sand where they feed and grow un-til completing development (Wassersug and Hoff, 1979). These characteristics, in addition to certain morphological features (i.e., elongate body, dorsal eyes, and sinistral spiracle), define a unique type of tadpole hypothesized to be shared by all species of the family (Cisneros-Heredia and McDiarmid, 2007).

A way to discriminate modes of development in frogs employs the source of energy that larvae use for growth. Endotrophic tadpoles obtain developmental nutrients exclusively from parentally derived sources, which, in most cases, means that they are entirely lec-ithotrophic. In contrast, exotrophic tadpoles must ob-tain nutrients from the external environment to com-plete their development (Altig and Johnston, 1989). Exotrophic tadpoles are also lecithotrophic prior to hatching, with lecithotrophy usually presumed to cease at the beginning of the free-living larval phase. However, energy reserves can persist for some time after initiating free life, and most descriptions of the oral disc in centrolenids are based on specimens in lecithotrophic stages. Because tadpoles in lecithotro-phic stages have not initiated functional feeding rela-tionships with the external environment, they tend to present little variation in the morphology of the oral disc (Altig and Johnston, 1989).

Herein we describe the tadpole of Nymphargus grandisonae (Cochran and Goin, 1970) based on feeding larvae and provide novel data on some as-pects of its natural history, including descriptions of adult male behavior, position of egg masses, larval ontogeny, and embryonic pigmentation.

MATERIALS AND METHODS

Field observations of adult behavior were oppor-tunistic and are presented as descriptive data. Oneegg clutch (Figure 1) of Nymphargus grandisonaewas collected from the Serranía de los Paraguas (Bo-querón; 04°44.2’N, 76°18.3’W, 2000 m.a.s.l.) mu-nicipality of El Cairo, Valle del Cauca department, Colombia (Figure 2), on 16 April 2009 by Jhon Jairo Ospina-Sarria, Wilmar Bolívar-G., and Javier Men-dez. The egg mass was collected with the leaf on which it was found and transported in a plastic bag to an aquarium at the Universidad del Valle, Cali-Colombia (03°27’N, 76°31’W, 990 m.a.s.l.). Larvaewere fed each third day with fish food (2-4 g). The aquarium was maintained at ambient temperature (22-28°C). We carried out continuous observations of size and morphology of larvae during growth (Table 1).

Vouchers were preserved in buffered formalin (formaldehyde 10%) and deposited in the Zoologi-cal collection of the Universidad del Valle (UV-CD).Some tadpoles were maintained until metamorphosis to confirm species identity. Tadpole staging follows Gosner (1960). A tadpole in stage 36 was used for

South American Journal of Herpetology, 6(2), 2011, 79-86© 2011 Brazilian Society of Herpetology

the general description of the species because in this stage the final number of tooth rows was obtained and key traits are relatively stable. Ontogenetic variation in morphology was documented from 29 tadpoles in different stages. Measurements were taken to 0.1 mmwith Mitutoyo digital calipers. Descriptive terminol-ogy and morphometric variables follow Altig (1970), Mijares-Urrutia (1998), and McDiarmid and Altig(1999). We measured 12 morphometric variables related to ontogenetic variation: (TL) total length = distance from tip of snout to tip of tail; (BL) body length = distance from tip of snout to join of the cau-dal axis with body; (BW) body width = width of body at the level of spiracle; (BH) body height = height of the body behind the eyes; (TAL) tail length = dis-tance from body-tail junction to tip of tail; (TMH) tail muscle height = height of caudal musculature at the proximal end of tail; (MTH) maximum tail height = height of tail, including the fins, where tail reaches its maximum height; (NED) nostril-eye distance = distance between center of nostril aperture to anterior edge of eye; (SSD) spiracle-snout distance = distance between the tip of snout and posterior border of spir-acle; (IND) internarial distance = distance between centers of narial apertures; (ODW) oral disc width = transverse diameter of oral disc; (VTL) vent tube length = distance between beginning of vent tube and

its aperture. The oral apparatus of some specimens was stained with methylene blue to facilitate visu-alization of structures. The taxonomy of glassfrogs follows Guayasamin et al. (2009). Comparisons of the tadpole of N. grandisonae with other species are based on published descriptions (Table 1)

RESULTS

Morphology (UV-CD 1912, Stage 36, Figure 3A, Table 2)

Total Length: 31.6 mm, body length: 10.8 mm. Body elongate and depressed in lateral view, wider than high (19.2%). Snout round in dorsal and lateral views. Eyes dorsal, separated by a distance slightly greater than the eye diameter. Nasal apertures small, dorsal, located midway from the tip of the snout to the eyes. Spiracle long, sinistral, located in the posterolateral region of the body. Vent tube short (12.3% of the body length) positioned along the ven-tral midline and connected dorsally to the tail. Tail long, length approximately twice of body length, robust with tip roundly pointed. Dorsal and ventral fins originate at the junction of the body and the tail, increasing continuously in height along almost

FIGURE 1. Egg masses of Nymphargus grandisonae from Serranía de los Paraguas, Valle del Cauca-Colombia. Left: Egg mass collected for the tadpole description. Right: Four egg masses observed near a calling male. (Photos: Wilmar Bolivar-G).

80 Tadpole of Nymphargus grandisonae

2/3 of tail. Caudal musculature strong. Oral disc ventral, not emarginate (Figure 4), surrounded by large, conical, marginal papillae. Upper jaw sheath fully keratinized, M-shaped with finely serrated margin. Lower jaw sheath completely keratinized, U-shaped, serrate. Labial tooth row formula 2/3, row

A1 complete, row A2 short and discontinuous. Rows P-1, P-2, and P-3 complete and well developed. The estimated duration of the lecithotrophic phase for Nymphargus grandisonae is at least eight days after hatching, during which time growth was evident de-spite lack of feeding.

FIGURE 2. Distribution map of Nymphargus grandisonae in Colombia, highlighting the collection locality of the studied egg clutch (tri-angle) and the type locality of the species (square).

81Ospina-Sarria, J. J. et al.

Color in life (Stage 36, Figure 3A)

Background color cream on dorsolateral surfaces. Hyobranchial apparatus and heart pinkish, as ob-served externally, vocal cavity cream and intestine translucent. Caudal musculature cream with reddish pigmentation. Caudal and ventral fins almost trans-lucent with small dark spots on distal region of the tail.

Color in preservative (Stage 36, Figure 3C)

The tadpole has a uniform cream color (UV-CD1912) with the cephalic region possessing dark pig-mentation. In ventral view tadpoles have iridophores covering at least ¾ of the posterior region of body. One tadpole (stage 39, UV-CD 1915) presented just dark pigmentation between eyes, while in ventral view the iridophores covered the posterior half of the body. Iridophores were also observed in lateral view body.

Ontogenetic variation

Tadpoles prior to stage 25 are darker with chro-matophores distributed along the body and tail (Fig-ure 1). However, it appears that tadpoles from more advanced stage are almost totally translucent (Fig-ure 3). Between stages 25-28 tadpoles are reddish,

FIGURE 3. Tadpoles of Nymphargus grandisonae. A: Live specimen, stage 36 (UV-CD 1912), scale = 3 mm. B: Live specimen, stage 28 (UV-CD 1913), scale = 6 mm. C: Preserved specimen, stage 36 (UV-CD 1912), scale = 3 mm.

FIGURE 4. Oral disc of the tadpole of Nymphargus grandisonae(UV-CD 1912). Scale = 2 mm.

82 Tadpole of Nymphargus grandisonae

with intense coloration on the hyobranchial apparatus. Myotomes are distinguishable in the tail, in lateral and dorsal views, and have dark pigmentation (Figure 3). Eyes are visible as an aggrupation of dark pigments. The oral disc is not totally formed and papillae are large with round tip. Upper and lower jaw sheaths are keratinized but tooth rows A-1, A-2, and P-1 are in-complete, while P-2 and P-3 are fully developed. Iri-dophores are present on the lateral side of the body. Distal tip of tail variably between pointed and rounded.

In stages 32-36 the toes have round terminations and the dark pigments observed in some tadpoles around the eyes disappear; advanced tadpoles have greenish yellow spots on the dorsal side of the body (red juveniles and adults; Figure 5).

Natural history

Egg clutches and males were observed on the upper side of leaves. Males called with the snout directed toward the tip of the leaf. Clutches were deposited above small lotic streams (N = 7); there were 30 and 53 embryos in two clutches, respective-ly. Embryos were light brown in recently laid egg clutches and brownish-red coloration in advanced clutches. Males were in reproductive activity near clutches but not in direct contact with them. The number of clutches associated with a given male was variable; we observed three males close to two egg masses and one close to four clutches (Figure 1, right).

TABLE 1. Available descriptions of larvae of 35 species of glassfrogs. Descriptions based on feeding larvae in stages later than Gosner (1960) stage 30 in bold.

Species SourceCelsiella vozmedianoi Señaris and Ayarzagüena, 2005Centrolene altitudinale Señaris and Ayarzagüena, 2005Centrolene daidaleum Rada et al., 2007Centrolene geckoideum Rueda-Almonacid, 1994Centrolene hesperium Cadle and McDiarmid, 1990Cochranella euknemos Hoffmann, 2010Cochranella granulosa Starrett, 1960; Savage, 2002; Hoffman, 2010Cochranella resplendens Terán et al., 2009Espadarana andina Mijares-Urrutia, 1990Espadarana prosoblepon Starrett, 1960; Savage, 2002; Hoffmann, 2010Hyalinobatrachium aureoguttatum Terán et al., 2009Hyalinobatrachium chirripoi Hoffmann, 2010Hyalinobatrachium colymbiphyllum Jaramillo et al., 1997; Savage 2002; Hoffmann 2010Hyalinobatrachium crurifasciatum Señaris and Ayarzagüena, 2005Hyalinobatrachium duranti Señaris and Ayarzagüena, 2005Hyalinobatrachium fleischmanni Starrett, 1960; Savage, 2002; Hoffmann, 2010Hyalinobatrachium ibama Rada et al., 2007Hyalinobatrachium ignioculus Noonan and Bonett, 2003Hyalinobatrachium munozorum Duellman, 1978Hyalinobatrachium orientale Señaris and Ayarzagüena, 2005Hyalinobatrachium talamancae Hoffmann, 2010Hyalinobatrachium taylori Señaris and Ayarzagüena, 2005Hyalinobatrachium valerioi Savage, 2002; Hoffmann, 2010Hyalinobatrachium vireovittatum Hoffmann, 2010Ikakogi tayrona Cochran and Goin, 1970Sachatamia albomaculata Hoffmann, 2010Sachatamia ilex Hoffmann, 2010Teratohyla midas Duellmam, 1978Teratohyla spinosa Starret, 1960; Savage, 2002; Hoffmann, 2010Teratohyla pulverata Hoffmann, 2004, 2010Vitreorana castroviejoi Señaris and Ayarzagüena, 2005Vitreorana eurygnatha Heyer, 1985Vitreorana helenae Señaris and Ayarzagüena, 2005Vitreorana oyampiensis Menin et al., 2009Vitreorana uranoscopa Heyer, 1985

83Ospina-Sarria, J. J. et al.

DISCUSSION

Nymphargus grandisonae is the first species of the genus for which the tadpole is described; there-fore, it is not possible to compare it with congeneric species. In comparison with species of other genera, the upper jaw sheath of N. grandisonae is M-shaped,

of Centrolene daidaleum, Cochranella resplendens, C. euknemos, Espadarana prosoblepon, Hyalino-batrachium ibama, H. ignioculus, H. fleischmanni,H. chirripoi, H. colymbiphyllum, H. talamancae,Ikakogi tayrona, Sachatamia ilex, S. albomaculata,Teratohyla pulverata, T. spinosa, and Vitreorana

FIGURE 5. Nymphargus grandisonae from Serranía de los Paraguas, Valle del Cauca, Colombia. Left: Adult male with distended vocal sac. Right: Metamorphosing froglet (UV-CD 1914).

TABLE 2. Dimensions in mm of Nymphargus grandisonae tadpoles, Gosner (1960) stages 23-39. Mean and standard deviation are shown when n>1. Abbreviations: Body length (BL), Body width (BW), Body height (BH), Tail length (TAL), Tail muscle height (TMH), Tail height (TH), Total length (TL), Eye-snout distance (ESD), Snout-spiracle distance (SSD), Internarial distance (IND), Oral disc width (ODW), Vent tube length (VTL).

Stage Date N BL BW BH TAL TMH TH TL ESD SSD IND ODW VTL Tooth RowFormula

23 29 April2009

4 3.3 ± 0.1

1.6 ± 0.2

1.6 ± 0.2

9.6 ± 0.6

1.9 ± 0.2

1.3 ± 0.1

12.8 ± 0.7

0.8 ± 0.1

2.2 ± 0.1

0.7 ± 0.1

0.8 ± 0.2

0.3 (0/0)-(0/2)

24 15 May2009

5 6.5 ± 0.5

3.5 ± 0.4

3.5 14.4 ± 1.5

2.7 ± 0.5

5.36 ± 1.5

20.8 ± 1.7

1.8 ± 0.2

4.6 ± 0.5

1.1 ± 0.4

2.1 ± 0.5

— (0/0)

24 28 May2009

3 7.5 ± 0.5

4.5 ± 0.6

2.4 ± 0.3

15.1 ± 1.8

2.9 ± 0.7

1.7 ± 0.4

22.6 ± 2.2

2 ± 0.5 5.1 ± 0.3

1.4 ± 0.1

2.2 ± 0.3

0.6 ± 0.1

(2/2)-(2/3)

25 02 June 2009

4 8.3 ± 0.7

4.7 ± 0.5

3.2 ± 0.6

16.1 ± 2.5

3.5 ± 0.6

2.1 ± 0.4

24.4 ± 3.3

2.2 ± 0.2

5.5 ± 0.7

1.4 ± 0.2

2.1 ± 0.6

0.8 ± 0.1

(2/2)

25 10 June 2009

4 8.4 ± 1.6

4.7 ± 0.8

3.3 ± 0.4

15.1 ± 1.2

2.8 ± 1.3

2 ± 0.4 23.6 ± 3.5

2.3 ± 0.3

5 ± 0.6 1.2 ± 0.2

1.5 ± 0.4

0.6 ± 0.2

(2/2)

26 17 June 2009

4 8.8 ± 0.7

4.5 ± 0.4

2.8 ± 0.5

18.3 ± 3.2

3.4 ± 0.2

2.2 ± 0.2

27.1 ± 3.9

2.4 ± 0.2

5 ± 0.4 1.4 ± 0.3

2 ± 0.5 0.8 ± 0.1

(2/2)

27 24 June 2009

4 10.1 ± 0.4

5.2 ± 0.5

2.6 ± 0.4

19.1 ± 1.3

3.5 ± 0.2

2.3 ± 0.2

29.2 ± 0.9

3.3 ± 0.7

6.1 ± 0.6

1.1 ± 0.3

2.2 ± 0.5

0.7 ± 0.1

(2/2)

28 10 July 2009

4 10 ± 1 5.3 ± 0.8

3.2 ± 0.4

20.2 ± 1.8

3.6 ± 0.5

2.5 ± 0.2

30.3 ± 2.6

3.2 ± 1.6

5.5 ± 2.1

1.1 2.4 ± 0.2

0.7 ± 0.2

(2/2)-(2/3)

29 16 July 2009

4 10.2 ± 1.2

5.6 ± 0.8

3.8 ± 1.2

18.4 ± 1.8

3.6 ± 0.6

2.5 ± 0.4

28.6 ± 2.7

2.5 ± 0.5

6.3 ± 0.9

1.3 ± 0.2

2.4 ± 0.2

0.7 ± 0.1

(2/2)-(2/3)

32 01 August2009

4 11.5 ± 0.3

7.3 ± 0.3

4.9 ± 0.7

21.0 ± 0.8

5.3 ± 0.7

3.4 ± 0.3

32.6 ± 0.9

3.2 ± 0.5

7.4 ± 0.7

2.3 ± 0.7

3.3 ± 0.5

0.5 ± 0.2

(2/3)

36 07 August2009

4 12.3 ± 0.2

6.9 ± 0.6

5.2 ± 0.6

22.8 ± 1.6

5.2 ± 0.8

3.3 ± 0.3

35.1 ± 1.8

3.2 ± 0.2

7.3 ± 0.8

1.8 ± 0.5

3.7 ± 0.5

1.2 ± 0.3

(2/3)

38 20 August2009

4 12.4 ± 0.1

7.3 ± 0.4

5.3 ± 0.4

23.9± 1

5.4 ± 0.4

3.6 ± 0.5

36.3 ± 0.9

3.1 ± 0.4

7.9 ± 0.3

1.8 ± 0.4

3.5 ± 0.4

1.3 ± 0.3

(2/2)-(1/2)

39 27 August2009

4 12.9 ± 0.5

7.5 ± 0.8

5.3 ± 0.4

24.1 ± 0.6

5.4 ± 0.2

3.5 ± 0.5

37.0 ± 1.0

2.8 ± 0.4

7.8 ± 0.4

1.9 ± 0.3

3.4 ± 0.3

0.9 ± 0.2

(1/2)

84 Tadpole of Nymphargus grandisonae

oyampiensis. Nymphargus grandisonae shares the M-shaped upper jaw with Hyalinobatrachium au-reoguttatum, H. valerioi, and Cochranella granulosa;however, H. aureoguttatum and H. valerioi present an emarginate oral disc (not emarginate in N. gran-disonae). Larvae of Cochranella granulosa have a rounded and pronounced snout (Hoffmann, 2010: fig. 20-21), in N. grandisonae the snout is short and rounded (Figure 3). Additionally, Cochranella gran-ulosa possesses a medial gap in A-2 as wide as the length of the upper jaw sheath (Hoffmann, 2010: fig. 23), whereas in N. grandisonae this gap is nar-rower than the upper jaw sheath (Figure 4).

As has been shown in descriptions of other glass-frog tadpoles (Rada et al., 2007; Menin et al., 2009; Terán et al., 2009), we observed oral disc shape to be constant during development. However, we found ontogenetic variation in tooth rows, body coloration, and number and shape of marginal papillae. We also observed variation in tadpole sizes within the same stage, despite being from the same egg clutch (Table 2).

McDiamird and Altig (1999) proposed a larval categorization for the genera Hyalinobatrachium,Cochranella, and Centrolene (sensu Ruiz-Carranzaand Lynch, 1991). However, such differentiation is not evident, which could be attributed to the limited number of larvae descriptions available at the time. The illustrations of the oral disc of Hyalinobatrachi-um aureoguttatum (Terán et al., 2009), H. igniocu-lus (Noonan and Bonett, 2003) and H. ibama (Radaet al., 2007) show the absence of a morphological pattern of this structure associated with the genus Hy-alinobatrachium (i.e., emarginate or not, shape upper jaw sheath).

Little is known about the sequence of develop-ment of labial tooth rows in centrolenid larva. We have shown that in Nymphargus grandisonae the de-velopment of labial tooth rows begins with rows P-1and P-2, followed by A-1 and A-2, and finally P-3.Although some larvae in stage 28 presented complete development of the dental rows (2/3), other individu-als presented only four rows (2/2). However, between stages 32 and 36, all examined larvae presented com-plete development of labial tooth rows (2/3). Thus, we recommend describing oral discs in these stages.

The current incongruence in some larval charac-ters (i.e., disc oral emarginate or not and shape up-per jaw sheath), with the phylogeny of centrolenids (Guayasamin et al., 2009) might be due to ecomor-phological convergence in tadpoles (Hoffmann, 2010). However, the number of tadpole descriptions

based on feeding specimens is limited, as is the num-ber of comparative studies of larval anatomy. Addi-tional standardized studies of larval characters (Radaet al., 2007; Terán et al., 2009) and subsequent phy-logenetic analysis are required to test this hypothesis.

RESUMEN

Se describe el renacuajo y la variación ontogénica de Nymphargus grandisonae de la Serranía de los Paraguas, Valle del Cauca-Colombia. También, las características de la postura (posición, coloración, número de renacuajos) y algunos aspectos de la historia natural de machos adultos. El renacuajo de Nymphargus grandisonae difiere de otros renacuajos de la familia por presentar un supraqueratostoma en forma de “M”, un pequeño espacio en la hilera dental A-2 y un disco oral no emarginado. Aunquese ha propuesto que la ausencia de diferencias morfológicas en ranas de cristal se debe a una convergencia ecomorfológica, se debe reconocer que es limitado el número de descripciones basadas en renacuajos exotróficos, como también los reducidos estudios comparativos sobre su anatomía larval. Esnecesario realizar estudios con caracteres larvales y posteriormente analizarlos en contexto filogenético para probar estas hipótesis.

ACKNOWLEDGMENTS

We are grateful to the staff of Corporación Serraniagua, specially Yohany Andrés Gaviria and Johnnier Andres Arango-Bermúdez for field support. Thanks to Marcelo Menin who provide us with valuable literature. To Taran Grant, Juan ManuelGuayasamin and anonymous reviewer for detailed comments that significantly improved this manuscript. We are thankful to MarcoRada, John D. Lynch, Santiago Castroviejo-Fisher, NathalieBaena, Maria Lucia Prado, and Marvin Anganoy for suggestions that improved the manuscript. Finally, we thank the AcademicProgram of Biology of the Universidad del Valle, Cali-Colombia.

LITERATURE CITED

ALTIG, R. 1970. A key to the tadpole of the Continental UnitedStates and Canada. Herpetologica, 26(2):180-207.

ALTIG, R. AND G. F. JOHNSTON. 1989. Guilds of anuran larvae: Relationships among developmental modes, morphologies, and habitats. Herpetological Monographs, 3:81-109.

CADLE, J. E. AND R. W. MCDIARMID. 1990. Two new species of Centrolenella (Anura: Centrolenidae) from NorthwesternPeru. Proceedings of the Biological Society of Washington,10:746-768.

85Ospina-Sarria, J. J. et al.

CISNEROS-HEREDIA, D. F. AND R. W. MCDIARMID. 2007. Revisionof the characters of Centrolenidae (Amphibia: Anura:Athesphatanura), with comments on its taxonomy and the description of new taxa of glassfrogs. Zootaxa, 1572:1-82.

COCHRAN, D. M. AND C. J. GOIN. 1970. Frogs of Colombia. UnitedStates National Museum Bulletin, Smithsonian InstitutionPress, 655 pp.

DUELLMAN, W. E. 1978. The biology of an Equatorial herpetofauna in Amazonian Ecuador. University of Kansas Museum of Natural History Miscellaneous Publication, 65:1-352.

GUAYASAMIN, J. M., S. CASTROVIEJO-FISHER, L. TRUEB, J. AYARZAGÜENA, M. RADA, AND C. VILÀ. 2009. Phylogeneticsystematic of glassfrogs (Amphibia: Centrolenidae) and their sister taxon Allophryne ruthveni. Zootaxa, 2100:1-97.

HEYER, W. R. 1985. Taxonomic and natural history notes of frogs of the genus Centrolenella (Amphibia: Centrolenidae) from southeastern Brasil and adjacent Argentina. Papéis Avulsosde Zoologia. Museu de Zoologia da Universidade de SãoPaulo, 36 (1):1-21.

HOFFMANN, H. 2004. Description if the previously unknown tadpole of Hyalinobatrachium pulveratum (Anura:Centrolenidae). Revista Biología Tropical, 52(1):219-228.

HOFFMANN, H. 2010. The glass frog tadpoles of Costa Rica (Anura:Centrolenidae): A study of morphology. Abhandlungen der Senckenberg Gesellschaft für Naturforschung, 567:1-78.

IBÁÑEZ-D. R., F. E. JARAMILLO-A., AND C. A. JARAMILLO-A.1999. Ampliación del ámbito de distribución y descripción del renacuajo de la rana de cristal Hyalinobatrachiumaureoguttatum (Anura: Centrolenidae). Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, Suplemento especial, 23:293-298.

JARAMILLO, F. E., C. A. JARAMILLO, AND D. R. IBÁÑEZ-D.1997. Renacuajo de la rana cristal Hyalinobatrachiumcolymbiphyllum (Anura: Centrolenidae). Revista de Biología Tropical, 45(2):867-870.

MCDIARMID, R. W. AND R. ALTIG. 1999. Tadpoles – the biology of anuran larvae. Chicago and London. The University of Chicago Press. 633 pp.

MENIN, M., A. P. LIMA, AND D. J. RODRIGUEZ. 2009. The tadpole of Vitreorana oyampiensis (Anura, Centrolenidae) in Central Amazonia, Brazil. Zootaxa, 2203:65-68.

MIJARES-URRUTIA, A. 1990. The tadpole of Centrolenella andina (Anura: Centrolenidae). Journal of Herpetology,24(4):410-412.

MIJARES-URRUTIA, A. 1998. Los renacuajos de los anuros (Amphibia) altoandinos de Venezuela: Morfología externa y claves. Revista de Biología Tropical, 46(1):119-143.

NOONAN, B. AND R. BONETT. 2003. A new species of Hyalinobatrachium (Anura: Centrolenidae) from the highlands of Guyana. Journal of Herpetology, 37(1):91-97.

RADA, M., J. V. RUEDAD-ALMONACID., A. A. VELÁSQUEZ-ÁLVAREZ,AND S. J. SÁNCHEZ-PACHECO. 2007. Descripción de las larvas de dos Centrolénidos (Anura: Centrolenidae) del noroccidente de la cordillera oriental, Colombia. PapéisAvulsos de Zoologia. Museu de Zoologia da Universidade de São Paulo, 47(21):259-272.

RUEDA-ALMONACID, J. V. 1994. Estudio anatómico y relaciones sistemáticas de Centrolene geckoideum (Salienta: Anura:Centrolenidae). Trianea, 5:133-187.

SAVAGE, J. M. 2002. The Amphibians and Reptiles of Costa Rica.A Herpetofauna Between Two Continents, and Two Seas. University of Chicago, Chicago, USA. 934 pp.

SEÑARIS, J. C. AND J. AYARZAGÜENA. 2005. Revisión taxonómica de la familia Centrolenidae (Amphibia: Anura) de Venezuela. Publicaciones del Comité Español del Programa Hombrey Biosfera – Red IberoMab de la UNESCO n. 07, Sevilla, España. 337 pp.

STARRETT, P. 1960. Descriptions of tadpoles of middle AmericanFrogs. Museum of Zoology, University of Michigan, 11-17.

TERÁN-VALDEZ, A., J. M. GUAYASAMIN, AND L. A. COLOMA. 2009.Description of the tadpole of Cochranella resplendensand redescription of the tadpole of Hyalinobatrachiumaureoguttatum (Anura, Centrolenidae). Phyllomedusa,8(2):105-124.

WASSERSUG, R. J. AND K. HOFF. 1979. A Comparative study of the buccal pumping mechanism of tadpoles. Biological Journal of the Linnean Society, 12:225-259.

Submitted 08 February 2011Accepted 21 August 2011

86 Tadpole of Nymphargus grandisonae