The Tadpole of Nymphargus Grandisonae (Anura, Centrolenidae) from Valle

Del Cauca, Colombia

Author(s) :Jhon Jairo Ospina-Sarria, Wilmar Bolíívar-G., Javier Mendez-Narvaez, Carlos Burbano-
Yandi
Source: South American Journal of Herpetology, 6(2):79-86. 2011.
Published By: Brazilian Society of Herpetology
DOI: 10.2994/057.006.0206
URL: http://www.bioone.org/doi/full/10.2994/057.006.0206

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

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 Herein we describe the tadpole of Nymphargus

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).
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. One
egg clutch (Figure 1) of Nymphargus grandisonae
was 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.). Larvae
were 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
80 Tadpole of Nymphargus grandisonae
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 mm
with 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
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).
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
 Ospina-Sarria, J. J. et al. 81

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).
82 Tadpole of Nymphargus grandisonae

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.

Color in life (Stage 36, Figure 3A) Ontogenetic variation

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.
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,

Color in preservative (Stage 36, Figure 3C)

The tadpole has a uniform cream color (UV-CD

1912) 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 FIGURE 4. Oral disc of the tadpole of Nymphargus grandisonae
body. (UV-CD 1912). Scale = 2 mm.
 Ospina-Sarria, J. J. et al. 83

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

with intense coloration on the hyobranchial apparatus. Natural history

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).
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).
84 Tadpole of Nymphargus grandisonae

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).

Tooth Row
Stage Date N BL BW BH TAL TMH TH TL ESD SSD IND ODW VTL
Formula
23 29 April 4 3.3 ± 1.6 ± 1.6 ± 9.6 ± 1.9 ± 1.3 ± 12.8 ± 0.8 ± 2.2 ± 0.7 ± 0.8 ± 0.3 (0/0)-(0/2)
2009 0.1 0.2 0.2 0.6 0.2 0.1 0.7 0.1 0.1 0.1 0.2
24 15 May 5 6.5 ± 3.5 ± 3.5 14.4 ± 2.7 ± 5.36 ± 20.8 ± 1.8 ± 4.6 ± 1.1 ± 2.1 ± — (0/0)
2009 0.5 0.4 1.5 0.5 1.5 1.7 0.2 0.5 0.4 0.5
24 28 May 3 7.5 ± 4.5 ± 2.4 ± 15.1 ± 2.9 ± 1.7 ± 22.6 ± 2 ± 0.5 5.1 ± 1.4 ± 2.2 ± 0.6 ± (2/2)-(2/3)
2009 0.5 0.6 0.3 1.8 0.7 0.4 2.2 0.3 0.1 0.3 0.1
25 02 June 4 8.3 ± 4.7 ± 3.2 ± 16.1 ± 3.5 ± 2.1 ± 24.4 ± 2.2 ± 5.5 ± 1.4 ± 2.1 ± 0.8 ± (2/2)
2009 0.7 0.5 0.6 2.5 0.6 0.4 3.3 0.2 0.7 0.2 0.6 0.1
25 10 June 4 8.4 ± 4.7 ± 3.3 ± 15.1 ± 2.8 ± 2 ± 0.4 23.6 ± 2.3 ± 5 ± 0.6 1.2 ± 1.5 ± 0.6 ± (2/2)
2009 1.6 0.8 0.4 1.2 1.3 3.5 0.3 0.2 0.4 0.2
26 17 June 4 8.8 ± 4.5 ± 2.8 ± 18.3 ± 3.4 ± 2.2 ± 27.1 ± 2.4 ± 5 ± 0.4 1.4 ± 2 ± 0.5 0.8 ± (2/2)
2009 0.7 0.4 0.5 3.2 0.2 0.2 3.9 0.2 0.3 0.1
27 24 June 4 10.1 ± 5.2 ± 2.6 ± 19.1 ± 3.5 ± 2.3 ± 29.2 ± 3.3 ± 6.1 ± 1.1 ± 2.2 ± 0.7 ± (2/2)
2009 0.4 0.5 0.4 1.3 0.2 0.2 0.9 0.7 0.6 0.3 0.5 0.1
28 10 July 4 10 ± 1 5.3 ± 3.2 ± 20.2 ± 3.6 ± 2.5 ± 30.3 ± 3.2 ± 5.5 ± 1.1 2.4 ± 0.7 ± (2/2)-(2/3)
2009 0.8 0.4 1.8 0.5 0.2 2.6 1.6 2.1 0.2 0.2
29 16 July 4 10.2 ± 5.6 ± 3.8 ± 18.4 ± 3.6 ± 2.5 ± 28.6 ± 2.5 ± 6.3 ± 1.3 ± 2.4 ± 0.7 ± (2/2)-(2/3)
2009 1.2 0.8 1.2 1.8 0.6 0.4 2.7 0.5 0.9 0.2 0.2 0.1
32 01 August 4 11.5 ± 7.3 ± 4.9 ± 21.0 ± 5.3 ± 3.4 ± 32.6 ± 3.2 ± 7.4 ± 2.3 ± 3.3 ± 0.5 ± (2/3)
2009 0.3 0.3 0.7 0.8 0.7 0.3 0.9 0.5 0.7 0.7 0.5 0.2
36 07 August 4 12.3 ± 6.9 ± 5.2 ± 22.8 ± 5.2 ± 3.3 ± 35.1 ± 3.2 ± 7.3 ± 1.8 ± 3.7 ± 1.2 ± (2/3)
2009 0.2 0.6 0.6 1.6 0.8 0.3 1.8 0.2 0.8 0.5 0.5 0.3
38 20 August 4 12.4 ± 7.3 ± 5.3 ± 23.9 5.4 ± 3.6 ± 36.3 ± 3.1 ± 7.9 ± 1.8 ± 3.5 ± 1.3 ± (2/2)-(1/2)
2009 0.1 0.4 0.4 ±1 0.4 0.5 0.9 0.4 0.3 0.4 0.4 0.3
39 27 August 4 12.9 ± 7.5 ± 5.3 ± 24.1 ± 5.4 ± 3.5 ± 37.0 ± 2.8 ± 7.8 ± 1.9 ± 3.4 ± 0.9 ± (1/2)
2009 0.5 0.8 0.4 0.6 0.2 0.5 1.0 0.4 0.4 0.3 0.3 0.2

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,
LQFRQWUDVWWRWKHVPRRWKŀVKDSHGXSSHUMDZVKHDWK
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).
 Ospina-Sarria, J. J. et al.
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-Carranza
and 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 (Rada
et 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-1
and 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
85
based on feeding specimens is limited, as is the num-
ber of comparative studies of larval anatomy. Addi-
tional standardized studies of larval characters (Rada
et 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. Aunque
se 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. Es
necesario 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 Manuel
Guayasamin and anonymous reviewer for detailed comments that
significantly improved this manuscript. We are thankful to Marco
Rada, John D. Lynch, Santiago Castroviejo-Fisher, Nathalie
Baena, Maria Lucia Prado, and Marvin Anganoy for suggestions
that improved the manuscript. Finally, we thank the Academic
Program of Biology of the Universidad del Valle, Cali-Colombia.
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Submitted 08 February 2011
Accepted 21 August 2011