The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia, with Notes on their Ecology and Comments on the Morphology of Atelopus Larvae

Abstract

We describe for the first time the tadpole of two endemic harlequin frogs of the Sierra Nevada de Santa Marta, north of Colombia:
Atelopus nahumae and A. laetissimus. In addition, we provide further morphological data for a third species, A. carrikeri. We also discuss some external morphological features for the tadpoles of these species and compare them with data currently available in the literature for the genus and with other larvae deposited in the amphibian collection of the Instituto de Ciencias Naturales of the National University of Colombia. The examined characters comprise eight morphometric variables and many traits of external morphology related with the oral apparatus, abdominal disc, fins, and dorsal color pattern. The tadpoles of A. nahumae and A. laetissimus are gastromyzophorous and morphologically similar, sharing a
great number of features with their congeners. The tadpoles of A. nahumae, A. laetissimus, and A. carrikeri contrast morphometrically; total length and tail width are the morphometric traits that are useful to differentiate among them. They are also differentiated by the size of the abdominal sucker and spiracle. In A. carrikeri, the abdominal sucker is large relative to that of A. nahumae and A. laetissimus; the spiracle of A. laetissimus and A. carrikeri is not visible in ventral and dorsal view, whereas it is large and conspicuous in A. nahumae. The tadpoles of the species from Sierra Nevada de Santa Marta differ from most of their congeners found in the Cordillera Oriental and Central of Colombia by lacking a dark band on the fins and caudal musculature. We recorded abiotic factors of the microhabitat where tadpoles of A. nahumae were observed (temperature, dissolved oxygen, and water depth). Our results indicate that the probability of finding A. nahumae tadpoles depends on the depth of the stream.

Full text

The Tadpoles of Two Atelopus Species (Anura:
Bufonidae) from the Sierra Nevada de Santa Marta,
Colombia, with Notes on their Ecology and Comments
on the Morphology of Atelopus Larvae
Authors: Pérez-Gonzalez, José Luis, Rada, Marco, Vargas-Salinas,
Fernando, and Rueda-Solano, Luis Alberto
Source: South American Journal of Herpetology, 15(1) : 47-62
Published By: Brazilian Society of Herpetology
URL: https://doi.org/10.2994/SAJH-D-17-00093.1
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The Tadpoles of Two Atelopus Species
(Anura:Bufonidae) from the Sierra Nevada de
SantaMarta, Colombia, with Notes on their Ecology
and Comments on the Morphology of Atelopus Larvae
José Luis Pérez-Gonzalez¹,², Marco Rada³, Fernando Vargas-Salinas⁴, Luis Alberto Rueda-Solano¹,⁵,*
¹ Grupo de Investigación en Biodiversidad y Ecología Aplicada, Facultad de Ciencias Básicas, Universidad del Magdalena, Santa Marta, Colombia.
² Fundación Atelopus, Santa Marta, Colombia.
³ Departamento de Zoologia, Instituto de Biociências; Universidade de São Paulo,
Rua do Matão, trav. 14, 321, Cidade Universitaria, CEP05508–090. São Paulo, Brazil.
⁴ Grupo de investigación en Evolución, Ecología y Conservación, Programa de Biología, Facultad de Ciencias Básicas y Tecnologías,
Universidad del Quindío, Armenia, Colombia.
⁵ Grupo Biomics, Departmento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia.
* Corresponding author. Email: biologoluisrueda@gmail.com
Abstract. We describe for the first time the tadpole of two endemic harlequin frogs of the Sierra Nevada de Santa Marta, north of Colombia:
Atelopus nahumae and A.laetissimus. In addition, we provide further morphological data for a third species, A.carrikeri. We also discuss some
external morphological features for the tadpoles of these species and compare them with data currently available in the literature for the genus
and with other larvae deposited in the amphibian collection of the Instituto de Ciencias Naturales of the National University of Colombia. The
examined characters comprise eight morphometric variables and many traits of external morpholog y related with the oral apparatus, abdominal
disc, fins, and dorsal color pattern. The tadpoles of A.nahumae and A.laetissimus are gastromyzophorous and morphologically similar, sharing a
great number of features with their congeners. The tadpoles of A.nahumae, A.laetissimus, and A.carrikeri contrast morphometrically; total length
and tail width are the morphometric traits that are useful to differentiate among them. They are also differentiated by the size of the abdominal
sucker and spiracle. In A.carrikeri, the abdominal sucker is large relative to that of A.nahumae and A.laetissimus; the spiracle of A.laetissimus and
A.carrikeri is not visible in ventral and dorsal view, whereas it is large and conspicuous in A.nahumae. The tadpoles of the species from Sierra
Nevada de Santa Marta differ from most of their congeners found in the Cordillera Oriental and Central of Colombia by lacking a dark band on
the fins and caudal musculature. We recorded abiotic factors of the microhabitat where tadpoles of A.nahumae were observed (temperature,
dissolved oxygen, and water depth). Our results indicate that the probability of finding A.nahumae tadpoles depends on the depth of the stream.
Keywords. Atelopus carrikeri; A.laetissimus; A.nahumae; Gastromyzophorous; Larval features; Microhabitats; Ontogeny.
Resumen. Describimos por primera vez el renacuajo de dos especies de sapitos Harlequines de la Sierra Nevada de Santa Marta, Colombia:
Atelopus nahumae y A. laetissimus. Adicionalmente, proveemos información morfológica adicional del renacuajo de una tercera especie,
A.carrikeri. Discutimos algunas características de la morfología externa de las larvas de estas especies y las comparamos con la evidencia
reportada en la literatura para otros renacuajos del género y con larvas depositadas en la colección de anfibios del Instituto de Ciencias
Naturales de la Universidad Nacional de Colombia. Los caracteres examinados incluyen ocho variables morfométricas y un amplio número
de caracteres de la anatomía externa relacionados con el aparato oral, el disco abdominal, las aletas y el patrón de color dorsal. Los renacuajos
de A.nahumae y A.laetissimus son considerados de tipo gastromizóforo y similares morfológicamente, compartiendo un gran número de
caracteres con sus congéneres. Las larvas de A.nahumae, A.laetissimus y A.carrikeri contrastan morfológicamente, siendo la longitud total y
el ancho de la cola las variables morfométricas que permiten diferenciar las especies. A su vez, estos se diferencian por el tamaño de la ventosa
abdominal. En A.carrikeri esta ventosa es más grande al ser comparada con las de A.nahumae y A.laetissimus. Además, el espiráculo en vista
dorsal y lateral es largo y conspicuo en A.nahumae, mientras que en A.laetissimus y A.carrikeri no es visible. Los renacuajos encontrados en la
Sierra Nevada de Santa Marta difieren de la mayoría de sus congéneres encontrados en la Cordillera Oriental y Central de Colombia, debido a
que los primeros no presentan una banda oscura sobre las aletas y la musculatura caudal. Por último, registramos algunos factores abióticos
del microhabitat donde se encuentran los renacuajos de A. nahumae (temperatura, oxígeno disuelto y profundidad del agua). Nuestros
resultados indican que la probabilidad de encontrar renacuajos de A.nahumae depende de la profundidad del agua en el arroyo.
INTRODUCTION
Atelopus Duméril and Bibron, 1841 (commonly
known as harlequin frogs) is one of the most threatened
amphibian genera on the planet due to several non-ex-
clusive factors, including infection by the pathogen fungi
Batracochytrium dendrobatidis, climate change, and habi-
tat destruction (La Marca etal., 2005; Stuart etal., 2008;
South American Journal of Herpetology, 15, 2020, 47–62
© 2020 Brazilian Society of Herpetology
Submitted: 02 October 2017
Accepted: 10 October 2018
Available Online: 31 March 2020
Handling Editor: Taran Grant
http://doi.org/10.2994/SAJH-D-17-00093.1
How to cite this article: Pérez-Gonzalez J.L., Rada M., Vargas-Salinas F., Rueda-Solano L.A. 2020. The tadpoles of two Atelopus species (Anura:
Bufonidae) from the Sierra Nevada de Santa Marta, Colombia, with notes on their ecology and comments on the mor phology of Atelopus lar vae. South
American Journal of Herpetology 15: 47–62. http://doi.org/10.2994/SAJH-D-17-00093.1
15, 2020, 47
02 October 2017
10 October 2018
31 March 2020
Taran Grant
SAJH-D-17-00093.1
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Lötters, 2009). Species of this genus inhabit a wide va-
riety of ecosystems ranging from Tropical rain forests at
sea level to paramos at approximately 4800m above sea
level (asl) and are distributed from Costa Rica in Central
America to Bolivia in South America (Gawor etal., 2012;
Frost, 2018). During the breeding season, it is common
to observe solitary or amplexed individuals alongside
streams; at the time of oviposition, the females attach a
string of eggs to submerged rocks and vegetation. Tad-
poles are usually found on sandy substrates or attached to
rocks in streams (Starrett, 1967; Lötters, 1996; Karraker
etal., 2006; Crump 2009). To date, 94 species of Atelopus
are recognized, of which 46 are found in Colombia (Frost,
2018). However, although Colombia is inhabited by the
greatest number of species of Atelopus, the tadpoles of
only five Colombian species have been described or il-
lustrated, including A. subornatus Werner, 1899 (Lynch,
1986; Enciso-Calle et al., 2017), A. mittermeieri Acosta-
Galvis et al., 2006 (tadpole described and illustrated
in the species description), A. carrikeri Ruthven, 1916
(Rueda-Solano etal., 2015), A.spumarius Cope, 1871 (Du-
ellman and Lynch, 1969), and A.ardila Coloma etal., 2010
(Gómez Castillo, 1982, 1993).
Here, we describe the external morphology of tad-
poles of Atelopus nahumae Ruiz-Carranza etal., 1994 and
A.laetissimus Ruiz-Carranza etal., 1994. Both species in-
habit forests between 1,500–2,800masl and are endemic
to the Sierra Nevada of Santa Marta (SNSM), an isolated
mountain range located in northern Colombia. We com-
pared external morphological features of the tadpoles of
A. nahumae and A. laetissimus with those of A. carrikeri,
another species endemic to the SNSM but distributed at
higher elevations (2,900–4,500masl; Rueda-Solano etal.,
2015) and with larval descriptions available in the litera-
ture. In addition, the distribution of some characters/
states related to dorsolateral color pattern and some oral
disc structures are reported and discussed for the tadpoles
described herein and for some undescribed Atelopus tad-
poles deposited in the Instituto de Ciencias Naturales of
the National University of Colombia in Bogotá. We explore
diagnostic information useful to delimit A. nahumae and
A.laetissimus species, which will serve as a basis for future
comparative studies that seek to elucidate the diversity of
morphological characters within Atelopus. Finally, we re-
corded microhabitat preferences of these two species.
MATERIALS AND METHODS
Collection sites
We collected tadpoles from four localities distrib-
uted across an elevational gradient in the SNSM (Fig.1).
Tadpoles of Atelopus laetissimus were collected from
two localities: the Estación Experimental San Lorenzo,
San Lorenzo stream, northwestern slope of the SNSM,
2,100masl (11°06′54.96″N, 74°03′03.46″W; WGS84), 11
April 2015, and in the Serranía de Cebolletas San Pedro
de la Sierra, Pascual stream, western slope of the SNSM,
2,200m asl (10°54′03.70″N, 73°55′04.50″W), 31 March
2016. Tadpoles of A.nahumae were collected on 12 April
2015, at the headwaters of the Gaira river, Serranía de San
Lorenzo, northwestern slope of the SNSM, 1,560 m asl
(11°10′02.0″N, 74°10′41.5″W). Tadpoles of A. carrikeri
were collected in the Serranía de Cebolletas on the western
slope of the SNSM, 3,500masl (10°54′03″N, 73°55′05″W).
Figure1. Geographic location and images of the study areas at Sierra Nevada de Santa Marta, northern Colombia, South America. The Atelopus species
in each of the four study areas are indicated on the map.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
48
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Field sampling, identifications, and comparisons
We performed visual encounter surveys along four
streams in the Sierra Nevada de Santa Marta to record
Atelopus larvae (Fig. 1). The collected tadpoles were eu-
thanized in lidocaine, fixed and preserved in 10% formal-
dehyde, and deposited in the herpetological collection of
the Universidad del Magdalena CBUMAG, Santa Marta,
Colombia (Atelopus laetissimus: CBUMAG-ANF: 0963 and
CBUMAG-ANF: 0971; A.nahumae: CBUMAG-ANF: 0961;
A.carrikeri CBUMAG-ANF: 0892).
Tadpole characters follow the terminology and defi-
nitions of McDiarmid and Altig (1999) and Mijares-Urru-
tia (1998) and the developmental stages were defined ac-
cording to Gosner (1960). We used the following variables
to describe the morphology of tadpoles for Atelopus nahu-
mae and A.laetissimus: total length (TL), body length (BL),
tail length (TAL), internarial distance (IND), interorbital
distance (IOD, taken from the medial edges of the cor-
neas), maximum tail height (MTH), maximum tail muscle
height (TMH), and tail muscle width (TMW). Measure-
ments were taken from a series of standardized (dorsal,
lateral, and ventral) photographs obtained from each
individual and species using a Sony Camera (DSC-H400)
and a stereoscope (Nikon H550S) with an Axion cam ERc
5s Camera (Carl Zeiss Gmbh, Gӧttingen, Germany) and
are reported as ±SD. The tadpoles of A.nahumae and
A.laetissimus were compared to tadpoles of 17 species of
the genus deposited in the amphibian collection of the In-
stituto de Ciencias Naturales of the National University
of Colombia in Bogotá (ICN; Appendix S1): A. angelito
Ardila-Robayo and Ruiz-Carranza, 1998, A. elegans Bou-
lenger, 1882, A. eusebianus Rivero and Granados-Díaz,
1993, A. famelicus Rivero and Morales, 1995, A. farci
Lynch, 1993, A. lozanoi Osorno-Muñoz et al., 2001,
A. mandingues Osorno-Muñoz et al., 2001, A. marinkel-
lei Cochran and Goin, 1970, A.minutulus Ruiz-Carranza
etal.,1988, A.mittermeieri, A.monohernandezii Ardila-Ro-
bayo etal., 2002, A.muisca Rueda-Almonacid and Hoyos,
1994, A.nicefori Rivero, 1963, A.quimbaya Ruiz-Carranza
and Osorno-Muñoz, 1994, A. sernai Ruiz-Carranza and
Osorno-Muñoz, 1994, A. simulatus Ruiz-Carranza and
Osorno-Muñoz, 1994, A.sonsonensis Vélez-Rodriguez and
Ruiz-Carranza, 1997.
Tadpole identification was based on the presence
of adults occurring on the same area or stream as lar-
vae, so we also collected postmetamorphic juveniles and
adults of Atelopus laetissimus (Fig.2A–D) and A.nahumae
Figure2. Individuals of Atelopus laetissimus. (A) Tadpole, CBUMAG: ANF 0963, stage 28–30 (sensu Gosner, 1960), (B) froglet, (C) juvenile, and (D)
adult male (not collected).
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
49
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(Fig.3A–D), which allowed us to assign the tadpoles to
the corresponding species on the basis of external mor-
phology.
Microhabitat
We recorded microhabitat preferences of tadpoles of
Atelopus laetissimus and A.nahumae, using the methodol-
ogy proposed by Rueda-Solano etal. (2015), but with the
following modifications: we selected four streams in the
Serranía de San Lorenzo, Quebradas San Lorenzo, Beto-
ma 1, Betoma 2, and Cascada Río Gaira (Fig.1), separated
from each other by more than 300m; in each stream, we
established a transect 50m long by 2m wide. We divided
each transect into 100 quadrants of one 1m² each and
then sampled half of them. In each sampled quadrant,
we determined presence/absence of tadpoles, depth of
the water column, level of O₂ dissolved (mg/L), and water
temperature with a multiparameter sensor (3420 set G
WTM 2FD46G). Water temperature in San Lorenzo Creek
was also monitored with a HOBO Pro V.2 data logger
U23–004 from 2014–2016, including a season of extreme
drought in 2015.
Data analysis
Photographs used to obtain the morphometric vari-
ables of tadpoles were processed using ImageJ (Schneider
et al., 2012). Two discriminant analyzes were performed
to establish which variables have the highest weight in dif-
ferentiating the tadpoles of Atelopus carrikeri, A.laetissimus,
and A.nahumae. The first analysis included all tadpoles; the
second analysis included only the individuals in develop-
mental stages ≥29. This latter analysis was performed to
control for the possible effect of small and morphologically
undifferentiated tadpoles. In both analyses, we standard-
ized morphometric variables by dividing them by TL. To de-
termine interspecific differences in body size at the end of
metamorphosis (Stage 46) for Atelopus laetissimus, A.nahu-
mae, and A.carrikeri, we performed an analysis of variance
(ANOVA). Finally, to evaluate microhabitat preferences for
A.nahumae and A.laetissimus (using tadpole presence/quad-
rant), a binary logistic regression was performed using the
environmental parameters (water depth, O₂ dissolved, and
water temperature) as the independent variables and the
presence/absence of tadpoles as the dependent variable. All
analyses were done using the statistical software IBM SPSS
Statistics for Windows, Version23.0. (IBM Corp, 2015).
Figure3. Individuals of Atelopus nahumae. (A) Tadpole, CBUMAG: ANF 0961, stage 33–35 (sensu Gosner, 1960), (B) froglet, (C) juvenile, and (D) adult
(not collected).
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
50
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RESULTS
We collected 298 specimens, including 235 tadpoles
and 63 froglets, divided among Atelopus carrikeri (n = 60),
A. laetissimus (n = 103), and A. nahumae (n = 135). The
tadpoles for the former two species represented 12 stages
of development, while tadpoles of the latter species rep-
resented 17 developmental stages (Table1, AppendixS2).
The tadpole of Atelopus laetissimus
The following description is based on three individu-
als in stage 35. Measurements (in mm) for Atelopus laetissi-
mus are as follows (see also AppendixS2): TL=23.9±0.9;
BL = 8.6 ± 0.5; TAL = 15.3 ± 0.4); IND = 1.8 ± 0.2);
IOD = 1.7 ± 0.6; MTH =3.7 ± 0.3); TMH = 2.4 ± 0.9;
TMW=2.0±0.2. Body ovoid, elongate in dorsal view, de-
pressed in lateral view; snout broadly rounded in dorsal
view, rounded in lateral profile, chondrocranial elements
not visible; eyes located dorsally; nostrils small, semicir-
cular, with flat, non-protrusive margin, directed dorsolat-
erally, approximately equidistant between eyes and tip of
snout. Spiracle small, single, sinistral, 1/2 free, originat-
ing at midpoint of body, inconspicuous in dorsal and ven-
tral views; opening of spiracle directed posterolaterally,
diameter less than 1/2 of length of free tube. Vent tube
short, medial; caudal musculature robust anteriorly, nar-
rowing abruptly just posterior to midlength of tail. Dorsal
and ventral fin originating on the tail, narrower than cau-
dal musculature; tip of tail rounded. Mouth ventral, sur-
rounded by well-developed labia forming complete oral
disc; upper lip with bilateral anterior projections form-
ing conspicuous M-shaped structure. Marginal papillae
short, acuminate; one row of complete marginal papillae
anteriorly; few submarginal papilla present, located on
the medial and lateral regions of oral disc; posterior papil-
lae absent. Labial tooth row formula 2/3, length of rows
subequal. Upper jaw sheath strongly keratinized, arch-
shaped; lower jaw sheath V-shaped. Both jaws slightly
serrate. Abdominal sucker large, extending from posteri-
or labium to midbody, forming complete, round structure
(diameter 6.9 mm) with raised edge; abdominal sucker
moderately extended (Fig.4A–C).
Table1. Measurements (in mm) of the tadpoles of Atelopus carrikeri, A. laetissimus, and A. nahumae (±SD; range in parentheses). BL= body length;
TAL= tail length; TL= total length; IND= internarial distance; IOD= interorbital distance; MTH= maximum tail height; TMH= maximum tail muscle
height; TMW= tail muscle width. Individuals in stage 46 (sensu Gosner, 1960) not included.
Species Stage nBL TAL TL IND IOD MTH TMH TMW
A.carrikeri 25–28 41 9.0±0.16 15.0±2.6 24.0±3.9 1.8±0.4 2.2±0.5 3.2±0.8 1.7±0.4 1.7±0.3
(6.5–12.7) (8.3–20.2) (16.2–31.6) (1.3–2.9) (1.6–3.5) (1.7–4.8) (1.0–2.5) (1.0–2.3)
29–30 4 9.4±0.9 20.0±0.9 29.4±0.4 1.7±0.3 2.3±0.3 3.4±0.3 1.8±0.1 1.6±0.3
(8.6–10.6) (18.7–20.8) (28.9–29.9) (1.2–2.0) (2.0–2.7) (3.0–3.8) (1.7–1.9) (1.3–2.1)
33–34 2 11.9±1.0 21.6±2.4 33.5±3.3 2.5±0.0 3.5±0.2 4.8±0.5 4.1±0.9 2.4±0.3
(11.2–12.6) (19.9–23.3) (31.1–35.9) (2.6–2.5) (3.4–3.7) (4.4–5.2) (4.7–3.5) (2.2–2.7)
35–36 3 12.4±1.1 21.3±1.8 33.7±0.7 2.5±0.4 3.2±0.3 4.6±0.6 2.9±0.1 2.1±0.2
(11.2–13.2) (19.8–23.3) (32.9–34.4) (2.0–2.8) (2.9–3.5) (3.9–4.9) (2.8–3.0) (2.0–2.3)
42 3 13.3±1.7 24.2±2.7 37.4±1.7 2.0±0.1 3.3±0.5 4.2±0.7 2.3±0.4 2.5±0.7
(11.4–14.6) (21.0–26.0) (35.7–39.1) (1.9–2.2) (2.8–3.8) (3.4–4.7) (1.9–2.7) (2.1–3.3)
A.laetissimus 25–28 75 6.2±0.9 10.0±1.7 16.2±2.5 1.2±0.5 1.5±0.5 2.5±0.6 1.4±0.4 1.2±0.4
(3.9–8.4) (6.2–13.9) (10.7–20.9) (0.3–2.0) (0.7–2.9) (1.1–3.9) (0.5–2.3) (0.6–2.0)
29–30 3 7.8±0.2 13.1±0.8 20.9±0.1 1.6±0.3 1.5±0.4 3.0±0.2 1.8±0.2 1.9±0.3
(7.6–8.0) (12.5–14.0 (20.2–22.0) (1.3–1.9) (1.2–1.9) (2.8–3.2) (1.6–2.0) (1.7–2.2)
35–37 6 8.6±0.4 15.6±0.8 24.2±1.0 2.0±0.3 2.0±0.6 3.7±0.3 2.4±0.2 2.1±0.3
(8.1–8.9) (14.8–16.6) (22.9–25.3) (1.7–2.4) (1.4–2.7) (3.5–4.1) (2.2–2.5) (1.7–2.4)
41–42 13 9.8±0.9 17.3±1.6 27.2±2.0 2.1±0.3 3.5±0.9 4.4±0.6 2.7±0.3 2.6±0.5
(8.6–11.2) (15.2–20.8) (24.8–31.4) (1.4–2.6) (1.6–4.6) (3.3–5.5) (2.2–3.4) (1.7–3.5)
A.nahumae 26–28 14 4.2±0.3 7.6±0.5 11.8±0.6 0.9±0.2 0.8±0.0 1.8±0.3 1.1±0.1 0.9±0.1
(3.6–4.8) (6.9–8.6) (11.0–13.2) (0.7–0.2) (0.7–0.8) (1.3–2.3) (0.9–1.3) (0.8–1.0)
29–30 13 5.1±0.3 8.4±0.3 13.5±0.5 0.9±0.1 0.9±0.1 2.1±0.2 1.3±0.2 1.0±0.1
(4.5–5.5) (8.0–8.9) (12.6–14.1) (0.8–1.0) (0.8–1.1) (1.7–2.5) (1.0–1.6) (0.9–1.2)
31–34 26 5.5±0.5 9.1±0.6 14.6±1.0 1.0±0.1 1.0±0.1 2.5±0.3 1.4±0.2 1.1±0.1
(4.9–6.6) (8.2–10.4) (13.1–16.6) (0.7–1.1) (0.8–1.3) (2.1–3.0) (1.0–1.9) (0.9–1.5)
35–37 27 5.7±0.5 9.8±0.7 15.5±1.0 1.1±0.1 1.2±0.3 2.7±0.2 1.5±0.2 1.2±0.2
(4.8–6.9) (8.8–11.4) (14.1–17.6) (0.8–1.4) (0.9–1.8) (2.2–3.2) (1.2–2.0) (0.9–1.6)
39–45 5 7.2±0.9 8.2±4.8 15.3±4.5 1.2±0.2 2.2±0.6 2.5±0.1 1.7±0.4 1.5±0.6
(5.5–7.9) (1.8–12.0) (9.6–19.6) (0.9–1.4) (1.2–2.6) (2.4–2.5) (1.3–2.2) (0.9–2.3)
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
51
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In life, the tadpoles of Atelopus laetissimus (Fig.2A)
are almost uniformly black with very minute metallic blue
or golden dorsal spots and a translucent to whitish border
around the snout. In ventral view, the oral and suctorial
discs are translucent. Tail musculature is cream with scat-
tered black spots in dorsal and ventral view; some individ-
uals have concentrated black spots in the dorsolateral area
close to the body junction and towards the end of the tail
in lateral view. The dorsal and ventral fins are translucent
with very minute dark spots. Changes in coloration were
observed during ontogenetic development: in early stages
the individuals have uniform white coloration and the
presence of light and dark bands interspersed with light
brown or light green lines on the dorsum and limbs when
the larva reaches stage 42 (Fig.2B). The same color pat-
tern was observed on forelimbs, once they had emerged
in stage 43. In preservative, the color pattern is similar
to that of living tadpoles, but it fades and loses its golden
and blue/white iridescent tones. The tail musculature be-
comes light cream (Fig.4A).
Natural history
Adult male Atelopus laetissimus were observed dur-
ing the day and night when calling, perched on vegeta-
tion at the border of streams, at a height of 20–100cm
from the water surface. Amplexus is axillary, and the un-
pigmented eggs are deposited beneath stones and in leaf
litter accumulated in the backwater areas of streams. The
egg string and jelly capsules are not attached to the sub-
strate. The string is indented and each capsule clearly dif-
ferentiated. Empty capsules occur at various points along
the string, similar to those reported in A.subornatus by
Lynch (1986). Tadpoles of A.laetissimus were abundant in
San Lorenzo Creek, and they exhibited nocturnal habits
(JLP-G, pers. obs, April 2015). Tadpoles developed at an
Figure4. Tadpole of Atelopus laetissimus in stage 27 (sensu Gosner 1960). (A) Lateral, (B) dorsal, and (C) ventral views. CBUMAG: ANF 0963.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
52
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average water temperature of 14.22°C±1.04 (n=4,527,
range=11–29°C) and hatch in stage 19. Postmetamorphs
and juveniles were found on vegetation bordering the ra-
vines at a height of 40–100cm from the ground level, af-
ter 4–5 months.
The tadpole of Atelopus nahumae
This description is based on 14 individuals in stage
35 (Fig.5A–C). Measurements (in mm) for Atelopus nahu-
mae are as follows (see also AppendixS2): TL=14.9±0.8;
BL = 5.6 ± 0.4; TAL = 9.8 ± 0.5; IND = 1.1 ± 0.1;
IOD = 1.1 ± 0.2; MTH = 2.6 ± 0.2; TMH = 1.6 ± 0.2;
TMW=1.2±0.1. Body ovoid, elongate in dorsal view, de-
pressed in lateral view; snout broadly rounded in dorsal
view, rounded in profile; chondrocranial elements not de-
tectable; eyes located dorsally; nostrils, small semicircu-
lar, with a flat, non-protrusive margin, directed dorsolat-
erally, equidistant between eyes and tip of snout. Spiracle,
small, single, sinistral, 1/3 free, originating at midpoint
of body, visible in dorsal and ventral views; spiracle open-
ing directed dorsoventrally, diameter less than 1/4 length
of free tube. Vent tube short, medial; caudal musculature
robust anteriorly, narrowing abruptly just posterior to
midlength of tail, terminating just anterior to end of tail.
Dorsal fin originating on body; ventral fin originating on
tail. Both fins narrower than caudal musculature, tip of
tail rounded. Mouth situated ventrally, surrounded by
well-developed labia forming complete oral disc; upper lip
with bilateral anterior projections forming conspicuous
M-shaped structure. Marginal papillae short, acuminate;
one row of marginal papillae anteriorly; submarginal pa-
pillae present. Labial row formula 2/3, length of rows sub-
equal. Upper jaw partially keratinized, arch-shaped; lower
jaw sheath V-shaped. Abdominal sucker small, extend-
Figure5. Tadpole of Atelopus nahumae in stage 35 (sensu Gosner 1960). (A) Lateral, (B) dorsal, and (C) ventral views. CBUMAG: ANF 0961.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
53
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ing from posterior labium to midbody, forming complete
round structure (4.7mm in diameter) with raised edge;
abdominal sucker slightly extended.
In life, the body is black with a conspicuous metal-
lic blue transverse band behind the eyes and two bluish
blotches between the nostrils and the snout tip. The
snout is translucent with very small dark spots, clear-
ing gradually towards the tip. The tail is black with dark
brown spots and the distal-most portion is translucent
(Fig.3A); in ventral view, the oral and suctorial discs are
translucent. The ventral and dorsal fins are translucent
with tiny dark spots. In lateral view, the tail musculature
is cream with scattered, minute, dark spots. During on-
togeny, the dorsum becomes dark brown with dark brown
blotches and small cream spots. Also, the hindlimbs are
yellowish in early and middle stages (30–39) and become
light brown by stage 42. The same color pattern was
observed on forelimbs, once they had emerged (Stage
43). In preservative, the color pattern is similar to that
of living tadpoles but fades and loses the bluish and iri-
descent tones. The tail musculature becomes light cream
(Fig.5A).
Figure6. Morphological measurements according to the developmental stage (sensu Gosner 1960) of tadpoles of Atelopus carrikeri (black dots), A.laetis-
simus (green dots), and A.nahumae (orange dots). Some dots overlap. Dots indicate mean values, error bars indicate standard deviation.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
54
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Natural history
Breeding activity of Atelopus nahumae was observed
from April to November at the headwaters of Gaira River.
Adult males were detected in both day and night on rocks
or vegetation beside the streams, ca.0–50cm from the wa-
ter. Amplexus was axillary and tadpole and juveniles were
observed over the entire year. The tadpoles were attached
to rocks at the margins of the medium-sized streams
(ca.3–4m wide), where the water flow was weaker. Un-
like A.laetissimus, juveniles of A.nahumae were found on
the ground on litter and rocks accumulated at the river
edges. Juveniles and adults were abundant (JLP-G, pers.
obs, April 2015).
Comparison with other Atelopus tadpoles of SNSM
In Atelopus nahumae, the abdominal sucker is short
relative to body length (7.6%), whereas in A.laetissimus it
is moderate (12.2%) and in A.carrikeri it is long (25%). In
A.laetissimus (Fig.4A,C) and A.carrikeri (Rueda-Solano
etal., 2015), the spiracle is small and less visible in ventral
and dorsal views than the large, conspicuous spiracle of
A.nahumae (Fig.5A,C). In all the stages of development,
the dorsal fins of A.laetissimus and A.carrikeri originate at
base of the tail, whereas the dorsal fin of A.nahumae origi-
nates on the posterior part of the body. In life, the dorsal
coloration of A. laetissimus is mostly black with minute
metallic blue or golden dorsal spots (Fig.2A); however,
they have a translucent or slightly whitish border around
the snout that is maintained throughout larval develop-
ment. The tadpole of A. nahumae is also black, but they
have metallic blue dots and one transverse band behind
the eyes; they are usually more colorful than their con-
geners found at SNSM and the translucent snout border
observed in A. laetissimus is less evident. Additionally,
A.nahumae has white spots of variable size distributed on
the body, accompanied by small golden blotches (Fig.3A).
The tadpole of A.carrikeri is also uniformly black or dark
brown with golden dots in all the stages of development
(Rueda-Solano etal., 2015).
Among these three Atelopus species, A.carrikeri had
the longest BL, TAL, and, therefore, TL in all stages of de-
velopment (Fig.6). However, TL for all three species was
different in stage 46 (n=63; F=15.852; df=2; P<0.001).
TL in A.carrikeri (n=7; 14.0±2.3mm) and A.laetissimus
(n=6; 14.6±0.9mm) was similar (HSD Tukey P<0.801),
while TL in A.nahumae (n=50; 11.3±1.6mm) was short-
er than A.laetissimus (HSD Tukey P<0.001) and A.car-
rikeri (HSD Tukey P<0.001). Tadpole measurements and
comparative data of Atelopus species from the literature
are shown in Tables1and2, respectively.
The first discriminant analysis performed with
morphometric measurements of the entire sample (i.e.,
including all developmental stages) showed differences
between Atelopus laetissimus, A.nahumae, and A.carrikeri
(Fig.7A). This analysis correctly separated 85.9% of the
tadpoles measured for the predicted groups. Function 1
accounted for 92.1% of the variance, with TL having the
Figure7. Discriminant analysis based on morphometric measurements of the tadpoles of Atelopus carrikeri (black dots), A.laetissimus (green dots), and
A.nahumae (orange dots). (A) tadpoles between developmental stages 25–45. (B) Tadpoles between developmental stages 29–45. Yellow squares indicate
the centroid value for each species.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
55
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Table2. Summary of external morphological characters scored in tadpoles of Atelopus. Species in bold are those with published descriptions and/or illustration occurring in Colombia. *= data inferred
from the tadpole’s illustration but not stated in the description by the author (pending corroboration); **= new information; ***= modification from the source.
Species Gosner stage
Labial
tooth
row
formula
Submarginal
papillae
Spiracle
position
Vent
tube
Dorsal fin
origin
Dorsal color pattern
(ETOH)
Caudal
band Reference
Atelopus balios 20–42 2/3 Absent* 2/3 Short Tail*** Reticulated, black, and cream Absent Coloma and Lötters, 1996
Atelopus carbonerensis 34, 37, and 38 2/3 Absent* Posterior
(62.5%)*
Short Tail Reticulated, black, and cream Absent Mijarres-Urrutia and La Marca, 2005
Atelopus carrikeri 34 2/3 Present** Posterior Short Tail Uniformly pigmented, black Absent Rueda-Solano etal., 2015
Atelopus certus 25–38 2/3* Absent* 3/5 Short Tail*** Uniformly pigmented, black Absent Duellman and Lynch, 1969
42 2/0 3/6
44 0/0 3/7
Atelopus cruciger – 2/3 Absent* 3/5 Short Tail Uniformly pigmented, black Absent Mebs, 1980
Atelopus exiguus 31 2/3 Absent* Posterior Short Tail*** Uniformly pigmented, black Absent Coloma etal., 2000
Atelopus flavescens 28 2/3 Present Posterior Median Tail*** Uniformly pigmented, black Absent Lescure, 1981
25–28 Boistel etal., 2005
25–44 Posterior* Gawor etal., 2012
Atelopus franciscus 27, 30, and 34 2/3 Present – Short Tail*** Reticulated, black, and cream Absent Boistel etal., 2005
Atelopus ardila 18–29 2/3* Absent* – Short – Uniformly pigmented, black Absent Gómez Castillo, 1982, 1993
Atelopus laetissimus 35 2/3 Present Posterior Short Tail Uniformly pigmented, black Absent This study
Atelopus mindoensis 36 2/3 Absent* Posterior Short Tail*** Uniformly pigmented, black Absent Lötters, 2001
Atelopus mittermeieri 27–34 2/3 Present** Posterior* – Tail Reticulated, black, and cream Present Acosta-Galvis etal., 2006
Atelopus mucubajiensis 32, 34, and 36 2/3 Absent* Posterior
(73%)*
Short Tail Uniformly pigmented, black Absent Mijarres-Urrutia and La Marca, 2005
Atelopus nahumae 35 2/3 Present Posterior Short Body Reticulated, black, and cream Absent This study
Atelopus nanay 28 2/3 Absent* Posterior Short Tail *** Uniformly pigmented, black Absent Coloma, 2002
Atelopus peruensis 25–32 2/3** Absent* Posterior** – Tail ** Uniformly pigmented, black Absent Gray and Cannatella, 1985
Atelopuscf.pulcher 25–42 2/3 Absent* 3/5 Median Tail *** Reticulated, black, and cream Absent Gascon, 1989; Lötters etal., 2002; Boistel etal., 2005
Atelopus sorianoi 26 2/3 Absent* Posterior
(69.2%)*
Median Tail Reticulated, black, and cream Absent Mijarres-Urrutia and La Marca, 2005
Atelopus spumarius 37 2/3 Absent* 3/5 Short Tail *** Uniformly pigmented, black Absent Duellman and Lynch, 1969; Lötters etal., 2002
Atelopus subornatus 26 2/3 Present** Posterior** – Tail *** Reticulated, black, and cream Present Lynch, 1986
Atelopus tamaense 27 and 36 2/3 Absent* Posterior
(66%)*
Short Tail Reticulated, black, and cream Absent Mijarres-Urrutia and La Marca, 2005
Atelopus tricolor 33–34 2/3 Absent* Posterior Short Tail *** Reticulated, black, and cream Absent Lavilla etal., 1997
Atelopus varius 2/3 Absent* 2/3 Short Tail *** Reticulated, black, and cream Absent Starrett, 1967
Atelopus zeteki 36 2/3 Absent* Posterior Median* Tail *** Uniformly pigmented, black Absent Lindquist and Hetherington, 1998
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
56
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greatest weight in this Function. Function 2 accounted
for 7.9%, with IOD having the greatest weight. The sec-
ond discriminant analysis, performed using only tadpoles
at developmental stages 29–45 (Fig. 7B), clearly shows
the differences between the tadpoles of the three spe-
cies. This latter analysis correctly separated 99% of the
tadpoles. The main source of variance was TL (Function
1; 93.4% of variance), while tail width (TMW; Function 2)
represented the remaining 6.6% of the variance.
Microhabitat preference
The tadpoles of Atelopus laetissimus and A.nahumae
were collected in medium-sized, fast-flowing streams
(Table3). For A.nahumae, the logistic regression model
accounted for 50–78% of the probability of finding tad-
poles (Cox and Snell R² = 0.50; Nagelkerke R² =0.781;
Fig.8). Water depth best predicted the presence of tad-
poles, with the greatest probability of detection at 10cm
depth (n=107; Wald=5.23; P<0.022), but this probabil-
ity varies among streams. Water temperature (n =107,
=16.8°C, Wald=1.65, P=0.19) and dissolved oxygen
(n=107, =8.2mg/L, Wald=2.88, P=0.090) had no pre-
dictive power (Table3). Data were insufficient to perform
this analysis for A.laetissimus.
DISCUSSION
Our study increases to seven the number of Atelo-
pus species in Colombia with described tadpoles (Table2).
Generally, Atelopus tadpoles are quite similar. For ex-
ample, some of the most distinctive features observed in
these gastromyzophorous tadpoles are a depressed body,
robust caudal musculature, low fins, and a ventral mouth
surrounded by well-developed labia that form a large
and complete abdominal sucker (Lötters, 1996, 2001;
Altig and McDiarmid, 1999; see Table2). Despite these
similarities, several authors have suggested that certain
morphological traits, such as the relative size of the ab-
dominal sucker, the relative size of the tail, the presence
of submarginal papillae, and, in particular, the dorsal
color pattern, are useful in distinguishing among species
(Duellman and Lynch, 1969; Ruiz-Carranza and Osorno-
Muñoz, 1994; Ruiz-Carranza et al., 1994; Coloma and
Lötters, 1996; Coloma etal., 2000; Boistel etal., 2005).
The dorsal color pattern of Atelopus laetissimus,
A.nahumae, and A.carrikeri is constant throughout stages
25–42. The black dorsal color pattern with large white or
bluish-white spots, bands, or blotches in the tadpoles of
A.nahumae is also known for tadpoles of other species of
Atelopus, such as A.certus Barbour, 1923, A.carbonerensis
Rivero, 1974, A.subornatus, A.mittermeieri, and A.soria-
noi La Marca, 1983 (Duellman and Lynch, 1969; Lynch,
Figure8. Logistic regression analysis showing the relationship between
water depth and the presence of Atelopus nahumae tadpoles in streams of
four localities at Sierra Nevada de Santa Marta, Colombia.
Table3. Summary of microhabitat variables (n=104) for tadpoles of Atelopus nahumae in streams of the Serranía San Lorenzo, Sierra Nevada de Santa
Marta, Colombia. *=A.nahumae tadpoles present; ⁺=A.laetissimus tadpoles present.
Locality Variable Mean SD CV Range
Quebrada San Lorenzo⁺ 2,200masl Water temperature (°C) 13.8 0.0 0.0 13.7–13.8
Dissolved O₂ (mg/L) 8.1 0.1 0.0 7.9–8.2
Water depth (cm) 17.6 9.2 0.5 3.9–37.3
Betoma 1 2,100masl 14.8 0.3 0.0 14.5–15.3
7.3 0.4 0.0 6.6–7.7
4.6 1.2 0.3 2.5–6.4
Betoma 2 2,100masl 14.3 0.1 0.0 14.2–14.5
8.0 0.1 0.0 7.2–8.0
4.8 1.0 0.2 2.5–7.6
Cascada Rio Gaira* 1,560masl 16.8 0.2 0.0 16.4–17.5
8.2 0.1 0.0 8.1–8.4
14.1 6.8 0.5 5.9–30.5
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
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1986; Mijares-Urrutia and La Marca, 2005; Acosta-Galvis
etal., 2006). These tadpoles are usually found in low and
mid-elevation mountain ecosystems. In contrast, a color
pattern of black coloration or uniformly dark brown with
minute golden spots is characteristic of tadpoles that in-
habit high-elevation ecosystems like paramos (e.g., A.mu-
cubajiensis Rivero, 1974, A.peruensis Gray and Cannatella,
1985, A. exiguus Boettger, 1892, A. tamaense La Marca
etal.,1990, A.nanay Coloma, 2002). The biological role
of this phenomenon is unknown and has not been tested
experimentally in Atelopus, but several authors have hy-
pothesized that dark coloration has a thermoregulatory
function, increasing absorbance of solar radiation in the
cold environments that predominate at high elevations
(Duellman and Lynch, 1969; Gray and Cannatella, 1985;
Coloma etal., 2000; Coloma, 2002; Mijares-Urrutia and
La Marca, 2005; Rueda-Solano etal., 2015).
Whereas most Atelopus tadpoles have been described
as black (e.g., Duellman and Lynch, 1969; Coloma et al.,
2002; Rueda-Solano et al., 2015; see above), the presence
of a large, dark band on the fins and caudal musculature has
been widely overlooked. A large, black, vertical, caudal band
has been reported throughout all the stages of A. suborna-
tus (Fig.9) and A.mittermeieri (Lynch, 1986; Acosta-Galvis
etal., 2006) but is also present in several Colombian species
from the Cordillera Oriental (A. farci, A. muisca, A. minutulu s,
and A. monohernandezi; absent in A. lozanoi, A. mandingues,
and A. marinkellei; AppendixS3), Cordillera Central (A. an-
gelito, A. sonsonensis, A.eusebianus, A. quimbaya, and A. ser-
nai); absent in A.simulatus), Cordillera Occidental (A.fame-
licus and A. nicefori), and Gorgona Island (A. elegans), but
absent in SNSM (A.carrikeri, A . laetissimus, and A. nahumae;
Appendix S3). Finally, of the remaining 18 Atelopus species
with published descriptions (see Table2), none have a large
black band on the fins and caudal musculature.
Another characteristic that has gone largely unno-
ticed in tadpoles of the genus Atelopus is the presence of
submarginal papillae on the oral disc, described for A .fra n-
ciscus Lescure, 1974 and A.flavescens Duméril and Bibron,
1841 by Boistel etal. (2005) and observed by us in A.lae-
tissimus and A.nahumae (see Table2). Boistel etal. (2005)
discussed its presence/absence in A.cf.pulcher and A.sp.
from Central Amazonia, suggesting that the apparent ab-
sence might be an observational artifact (probably related
to preservation artifacts) and predicted that submarginal
papillae will be discovered when some described tadpoles
are reexamined. Here, we report for the first time the
presence of small, usually 2–4 submarginal papillae in the
previously described tadpoles of A. carrikeri and A. mit-
termeieri, and in the undescribed tadpoles of A. angelito,
A. elegans, A. eusebianus, A. lozanoi, A.famelicus, A. farci,
A. quimbaya, A. mandingues, A. marinkellei, A. minutulus,
A.monohernandezi, A.muisca, A.nicefori, A.sernai, A.son-
sonesis, and A.simulatus (AppendixS4). Our observations
corroborate Boistel etal.’s (2005) prediction.
Tadpoles of mid-elevation species like Atelopus la-
etissimus and A. subornatus tend to be larger than their
lowland counterparts (Lynch, 1986; Gascon, 1989; Lavil-
la etal., 1997; Acosta-Galvis et al., 2006). Similarly, the
tadpoles of high-elevation species (e.g., A. carriker i and
A.ardila) are larger than those of low and middle eleva-
tions (see Rueda-Solano et al., 2015). Among phyloge-
netically related species distributed on an altitudinal
gradient, those that inhabit higher altitudes are usually
larger (Ashton, 2002). According to our results and re-
ports on A. flavescens, A.balios Peters, 1973, and A. car-
rikeri, larval growth, measured as TL, ceases at stage 42
in A. balios (Coloma and Lötters, 1996) and stage 43 in
A. carrikeri, A. laetissimus, A. nahumae, (Rueda-Solano
etal., 2015) and A.flavescens (Gawor et al., 2012). Size
then gradually decreases, so that by stage 46 larval length
reaches the minimum values (14.5mm in A. laetissimus
and 11.3mm in A.nahumae). According to published re-
cords, the values of A.laetissimus are equivalent to those
reported for A. carrikeri (14.0 mm; Rueda-Solano et al.,
2015) and A.zeteki Dunn, 1933 (14.0mm; Lindquist and
Hetherington, 1998). These differences between species/
stages might have a genetic basis, but they might also be
affected by biotic or abiotic pressures, such as predators,
food sources, or temperature changes that cause develop-
ment to vary (Dahl etal., 2012).
Water depth had the greatest predictive power when
the microhabitat preferences were evaluated in tadpoles
of Atelopus nahumae (Fig.8). This depth might be corre-
lated with other factors like low speed of the current in
which the tadpoles develop (Boistel et al., 2005). Like-
wise, a certain depth could increase the survival of tad-
poles; however, this does not explain the absence of tad-
poles in streams with similar depths (see Rueda-Solano
et al., 2015). Alternatively, reproductive behavior could
determine the presence/absence of the tadpoles (Rocha
Usuga etal., 2017). Field observations suggest that A.la-
etissimus, A. nahumae, and A. zeteki (see Karraker, 2006;
Rocha Usuga etal., 2017) use certain streams exclusively
during the dry season for reproduction and oviposition.
This behavior and the seasonality of the rain could deter-
mine the probability of detecting tadpoles of these species
in the streams. In A.balios, A.flavescens, and A.zeteki, the
variable that best predicts the presence of tadpoles is dis-
solved oxygen, because they require high oxygen concen-
trations for their development and survival (see Lescure,
1981; Coloma and Lötters, 1996; Lindquist and Hether-
ington, 1998). However, for A. carrikeri (Rueda-Solano
etal., 2015) and A. nahumae, and perhaps A.laetissimus
as well, dissolved oxygen has no predictive power to de-
termine the presence of tadpoles in streams of the study
area, because the concentration of dissolved oxygen in the
water is always high and varies little.
The description of the tadpoles of Atelopus laetissi-
mus and A.nahumae from the SNSM offers information
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
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for the taxonomic delimitation of these two species,
serves as a basis for future comparative studies that
seek to elucidate the diversity of morphological charac-
ters within Atelopus, and enables knowledge about their
ecology and reproductive behavior to be improved. To
date, almost half of the known diversity of Atelopus (46
species) occurs in Colombia (Frost, 2018); however,
the tadpoles of only seven species (including the pres-
ent work) have been described or illustrated. Finally, in
terms of future studies on Atelopus tadpoles, compara-
tive revisions of internal morphology are needed; these
studies would ideally include data on buccopharyngeal
cavity structures, cranial muscles, and chondrocrani-
um.
Figure9. Presence of dark band on the fins and caudal musculature in Atelopus subornatus (arrow). (A) CZUT-A: 2256-4 in life, stage 36, (not to scale;
photo: Marvin Anganoy Criollo); (B–C) ICN 31435, stage 31.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
59
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ACKNOWLEDGMENTS
This work is part of the project Atelopus: Monitoring
harlequins frogs of the Sierra Nevada of Santa Marta, Co-
lombia. We thank the Conservation Leadership Program
for financial support. Thanks to John D. Lynch (ICN) for
facilitating access to tadpole specimens under his care, and
to Taran Grant (USP) for his support and facilities during
JLP’s stay at his laboratory. This research benefitted from
discussions with Pedro H. Dias and Marvin Anganoy-
Criollo and suggestion/corrections of Diego. F Cisneros-
Heredia. María A. Pinto, Juan P. Ramírez, and Esteban
Betancur clarified and shared valuable information about
the dorsum color and catalogue numbers of some At-
elopus species. Fieldwork was conducted in collaboration
with Albertina P. Lima, William Magnusson, Teresa C.S.
Avila-Pires, and Marinus Steven Hoogmoed, the students
of the Herpetology group of the University of Magdalena
(Los Froglets), Fundación Atelopus, and the administra-
tors of the Sierra Nevada of Santa Marta Natural National
Park (PNN, Caribbean territorial). María Camila Basto,
Lilia Mejía, Lizeth Jiménez, and José Ángel Rincón pro-
vided technical support. Thanks to Molly Womack and
Santiago Herrera, who reviewed or commented on early
versions of the manuscript. Scholarship grant support to
MAR was provided by Coordenação de Aperfeiçoamento
de Pessoal de Nível Superior (CAPES, PEC-PG) and PNPD
programs (Proc. 2016.1.263.41.6). Fieldwork and other
facilities of MAR were supported by a grant of FAPESP
(Proc. 2012/10000-5 and Proc. 2008/50928-1). The col-
lection of amphibians in Colombia was authorized by the
Ministerio de Ambiente, Vivienda y Desarrollo Territo-
rial of Colombia and Corporación Autónoma Regional del
Magdalena (Resolución 0425 de 2015). This study was
Jose Luis Peréz Gonzalez’s undergraduate thesis directed
by LARS (Beto Rueda).
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South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
61
Downloaded From: https://bioone.org/journals/South-American-Journal-of-Herpetology on 31 Mar 2020
Terms of Use: https://bioone.org/terms-of-useAccess provided by Universidad Antioquia

ONLINE SUPPORTING INFORMATION
The following Supporting Information is available for this article online:
Appendix S1. Specimens examined for comparisons (tadpole lot).
Appendix S2. Morphological measurements (mm) and developmental stages (Gosner, 1960) for 60 tadpoles of Atelopus
carrikeri, 103 of A. laetissimus, and 135 of A. nahumae, including larvae in stage 46.
Appendix S3. Species/specimens examined for occurrence of large dark band on the fins and caudal musculature.
Appendix S4. Species/specimens examined for the occurrence of submarginal papillae on the oral disc.
South American Journal of Herpetology, 15, 2020, 47–62
The Tadpoles of Two Atelopus Species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia ,
with Notes on their Ecology and Comments on the Morphology of A telopus L arvae
José Luis Pérez-Gonzalez, Marco Rada, Fernando Vargas-Salinas, Luis Alberto Rueda-Solano
62
Downloaded From: https://bioone.org/journals/South-American-Journal-of-Herpetology on 31 Mar 2020
Terms of Use: https://bioone.org/terms-of-useAccess provided by Universidad Antioquia