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Journal of Natural History
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/tnah20
Advertisement call, tadpole morphology,
and other natural history aspects of the
threatened poison frog Andinobates daleswansoni
(Dendrobatidae)
Sebastián Duarte-Marín, Cristian C. González-Acosta, Pedro Henrique Santos
Dias, Gustavo A. Arias-Álvarez & Fernando Vargas-Salinas
To cite this article: Sebastián Duarte-Marín, Cristian C. González-Acosta, Pedro Henrique
Santos Dias, Gustavo A. Arias-Álvarez & Fernando Vargas-Salinas (2020) Advertisement
call, tadpole morphology, and other natural history aspects of the threatened poison frog
Andinobates�daleswansoni (Dendrobatidae), Journal of Natural History, 54:45-46, 3005-3030, DOI:
10.1080/00222933.2021.1889068
To link to this article: https://doi.org/10.1080/00222933.2021.1889068
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Published online: 24 May 2021.
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Advertisement call, tadpole morphology, and other natural
history aspects of the threatened poison frog Andinobates
daleswansoni (Dendrobatidae)
Sebastián Duarte-Marín
a
, Cristian C. González-Acosta
a
,
Pedro Henrique Santos Dias
b
, Gustavo A. Arias-Álvarez
c
and
Fernando Vargas-Salinas
a
a
Grupo de Evolución, Ecología y Conservación EECO, Programa de Biología, Facultad de Ciencias Básicas
y Tecnologías, Universidad del Quindío, Armenia, Colombia;
b
Departamento de Zoologia, Instituto de
Biociências, Universidad de São Paulo, São Paulo, Brazil;
c
Grupo de estudio de artrópodos (GEA), Programa
de Biología, Facultad de Ciencias Básicas y Tecnologías, Universidad del Quindío, Armenia, Colombia
ABSTRACT
Describing natural history of species is important because it
would allow us to corroborate hypotheses about evolutionary
biology and improve conservations plans. We describe the adver-
tisement call, tadpole morphology, and other natural history
aspects of the poison frog Andinobates daleswansoni, an endemic
threatened species of the Colombian Andes. The advertisement
call consists of multiple pulsed notes, with an average dominant
frequency of 4052.81 ± 154.93 Hz. This call sounds similar to the
call of other Andinobates frogs, but there are clear dierences in
spectral and temporal features. Tadpoles have a depressed body,
low compressed dorsal and ventral tail ns with a rounded tip.
The oral disc has a labial tooth row formula of 2(2)/3(1), and a gap
in the marginal papillae of the lower lip, whose status as
a synapomorphy for the group A. bombetes is discussed. Like
other poison frogs, the diet of A. daleswansoni consists of small
arthropods (Acari, Hymenoptera, Coleoptera) that individuals cap-
ture in leaitter. We recorded tadpole transport by males to
phytotelmata in the Elephant Ear plant (Xanthosoma robustum)
which demonstrate that A. daleswansoni has a greater niche
breadth for tadpole development than previously recorded.
Acoustic interactions and physical ghts observed during an ago-
nistic behaviour on the part of two males of A. daleswansoni is
similar to those recorded in other poison frogs and possible
associated to the occupation of resources such as availability of
prey items and places for breeding.
ARTICLE HISTORY
Received 27 March 2020
Accepted 5 February 2021
KEYWORDS
Anura; dart-poison frogs;
bioacoustics; larval
morphology
Introduction
The family Dendrobatidae is composed of 201 anuran species of Neotropical distribution
(Frost 2021). In this family males call from specic territories, and following an elaborate
courtship, females lay their eggs in humid terrestrial microhabitats (Lötters et al. 2007).
CONTACT Sebastián Duarte-Marín sdm950811@gmail.com
Supplemental data for this article can be accessed here.
JOURNAL OF NATURAL HISTORY
2020, VOL. 54, NOS. 45–46, 3005–3030
https://doi.org/10.1080/00222933.2021.1889068
© 2021 Informa UK Limited, trading as Taylor & Francis Group
Published online 24 May 2021
Once tadpoles hatch, they are transported on the back of one of the parents, usually the
male, to waterbodies such as streams, terrestrial ponds, and pools in phytotelmata
(Silverstone 1975; Myers and Daly 1980; Brown et al. 2010; Summers and Tumulty 2014).
Many dendrobatids are toxic and exhibit warning colouration (Ruxton et al. 2018). The
charismatic appearance of these frogs makes them good ambassadors for promoting
amphibian conservation initiatives (Kahn et al. 2016). Their appeal, however, also makes
them targets of an illegal pet trade, and over collection is considered one of the causes of
population decline in several species (Rueda-Almonacid et al. 2004; IUCN 2017).
Diverse aspects of the biology of poison frogs have been well studied. For instance,
taxonomy and phylogenetic relationships (Silverstone 1975, 1976; Grant et al. 2006, 2017;
Brown et al. 2011), evolution of aposematism (Santos et al. 2003, 2014; Summers 2003;
Darst et al. 2005; Wang 2011; Rojas 2016), communication (Lötters et al. 2003; Erdtmann
and Amézquita 2009; Amézquita et al. 2011; Vargas-Salinas and Amézquita 2013a),
breeding behaviour and territoriality (Pröhl 2005; Schulte et al. 2010; Ringler et al.
2011), parental care (Weygoldt 1987; Summers and McKeon 2004; Summers et al. 2006;
Poelman and Dicke 2007; Summers and Tumulty 2014; Pašukonis et al. 2019), and spatial
movement ecology (Brown et al. 2009; Pašukonis et al. 2013, 2014a, 2014b, 2016, 2018;
Arcila-Pérez et al. 2020). Although these studies make it possible to know and predict
general patterns in the biology of dendrobatids, specic aspects of natural history for
numerous species are still unknown. Describing in detail what those little-known den-
drobatids do in their natural environment is important, since it would allow us to
corroborate hypotheses about various aspects of their biology, nd novel behaviours,
or even re-evaluate aspects that were believed to be well understood (Vitt 2013;
Tewksbury et al. 2014; Travis 2020).
Among the many natural history characteristics that require additional documentation
in dendrobatids are the features of their acoustic signals, the morphology of their
tadpoles, and their diets. The advertisement calls and tadpoles have been described for
more than 104 (51.7%) and 118 (58.7%) of dendrobatid species, respectively (e.g.
Silverstone 1975, 1976; Myers and Daly 1976, 1980; Coloma 1995; Twomey and Brown
2008; Páez-Vacas et al. 2010; Brown et al. 2011; Sanchez 2013; Dos Santos Dias et al. 2018).
Knowing advertisement call features of poison frogs has been useful for understanding,
for example, patterns of habitat use in noisy environments (Vargas-Salinas and Amézquita
2013a; Vargas-Salinas et al. 2014), coexistence of species (Amézquita et al. 2011), and
female mating preferences (Forsman and Hagman 2006; Medina et al. 2013). Morphology
of tadpoles in poison frogs have been important for species delimitation, for inferring
phylogenetic anities (Sanchez 2013; Grant et al. 2017; Dos Santos Dias et al. 2018), and
for understanding habitat use and ecological interactions prior to metamorphosis
(Poelman et al. 2013; Menin et al. 2017). Regarding diet of post-metamorphic individuals,
especially adults, it has been characterised in some species (e.g. Silverstone 1975; Toft
1995; Caldwell 1996; Biavati et al. 2004) and usually it has been correlated to the evolution
of aposematism (Santos et al. 2003; Saporito et al. 2004; Darst et al. 2005). Beyond its
importance in basic science, knowing natural history aspects of poison frogs can also be
used to monitor populations, and perhaps implement ex-situ rescue eorts when anthro-
pogenic impacts threaten extinction (Clemmons and Buchholz 1997; Gosling and
Sutherland 2000).
3006 S. DUARTE-MARÍN ET AL.
The dendrobatid genus Andinobates currently comprises 15 species distributed
mainly in the Colombian Andes, but also in Panama and Ecuador (Grant et al.
2006, 2017; Brown et al. 2011; Frost 2021). Andinobates frogs are diminutive, exhibit
bright aposematic colouration, males usually call from leaitter mounds or brome-
liads, and their small, grey or dark tadpoles develop in phytotelmata (Silverstone
1975; Ruiz-Carranza and Ramírez-Pinilla 1992; Brown et al. 2011). The call of these
species have been described as a ‘Buzz’ (Myers et al. 1984; Brown et al. 2011), the
tadpoles exhibit morphological attributes similar to those in species of other genera
of Dendrobatidae, such as depressed bodies and massive jaw sheaths (Grant et al.
2006, 2017), and their diet consists in small arthropods, specially ants and Acari
(Silverstone 1975; Valderrama-Vernaza et al. 2009; Gómez-Hoyos et al. 2014; Rivas
et al. 2019).
One of the most poorly known species of Andinobates is A. daleswansoni (Figure 1).
This species was rst described by Rueda-Almonacid et al. (2006), belongs to the
A. bombetes group (Brown et al. 2011), and is endemic to National Natural Park Selva
de Florencia and surrounding areas in the municipality of Pensilvania and Samaná,
department of Caldas, cordillera Central of Colombia (Velásquez-Álvarez et al. 2016;
Duarte-Marín et al. 2018). Here, we describe for the rst time the advertisement call, the
tadpole, and the diet of A. daleswansoni. In addition, we record males transporting
tadpoles on the back to phytotelmata other than those in bromeliads, and an agonistic
encounter by males.
Figure 1. Image of a calling male of Andinobates dalewansoni in the study area. Individual not
collected.
JOURNAL OF NATURAL HISTORY 3007
Material and methods
Area and species study
We conducted our study in the National Natural Park Selva de Florencia (hereafter Selva
de Florencia), in the village of Las Colonias, Sector of Montebello, Municipality of
Pensilvania, Department Caldas, Colombia (05º27ʹ29”N, 75º07ʹ4.7”W; Figure 2). Selva de
Florencia is 10,019 ha in size and it is located between 850 and 2400 metres above sea
level (masl). The study area exhibits a mean annual temperature between 17 and 22°C,
and a precipitation level >8000 mm/year (Ballesteros et al. 2009). The vegetation is
characteristic of native Andean and sub-Andean humid forest that has been fragmented
by forestry and livestock activities. Some areas within Selva de Florencia are being allowed
to recover, and are undergoing natural ecological succession back to mature forest
(Ballesteros et al. 2009; Duarte-Marín et al. 2018).
According to Rueda-Almonacid et al. (2006), the body size (snout-vent length, SVL) of
adult male Andinobates daleswansoni ranges between 17.8 and 18.5 mm (mean = 18.1 mm,
N = 3), while adult females range between 19.0 and 19.7 mm (mean = 19.5 mm, N = 3).
Figure 2. Aerial image of the Selva de Florencia National Natural Park (shadow brown area) and its
location in the Central Andes of Colombia. Red square represents the site where the study was
conducted. The red dots represent historical records of A. daleswansoni (Rueda-Almonacid et al. 2006;
Brown et al. 2011; Duarte-Marín et al. 2018), and the red star represents the type locality of the species
(‘El Estadero’, Municipality of Florencia, Caldas). The orange dots indicate records for Andinobates
opisthomelas, a morphological similar species to A. daleswansoni (Ruiz-Carranza et al. 1996; Brown
et al. 2011). Note that this study was performed in the municipality of Pensilvania, where
A. opisthomelas has not been recorded.
3008 S. DUARTE-MARÍN ET AL.
Andinobates opisthomelas a species with a body size (SVL males = 14.5–18.5 mm, SVL
females = 14.5–19.5 mm) similar to that of A. daleswansoni (Silverstone 1975; Brown et al.
2011), has also been recorded at Selva de Florencia. However, we are condent our study
focuses on A. daleswansoni because in this species there is a fusion of the rst toe with
the second toe, and the colouration of individuals consists of a bright red hood on the head,
shoulders and arms, and a golden brown on the back and legs. In contrast, in
A. opisthomelas does not have a fusion of the rst and second toe, and the colouration
includes a solid red dorsum, brown venter, and anks often reticulating blue and black
(Rueda-Almonacid et al. 2006; Brown et al. 2011). Furthermore, A. opisthomelas has not been
recorded in our specic study area (Figure 2).
Field procedures
We conducted four eld trips of 12 days each in June, July, August, September 2017
and October 2018. Three of us searched for frogs in the morning (08:00–11:00 h) and
in the afternoon (14:00–17:00 h), using visual and auditory encounter surveys (Crump
and Scott 1994). We conducted our surveys in forests and abandoned pine plantation
habitats. In both habitats, we focused on leaf litter, fallen tree trunks, mosses, rocks,
and leaf axils. When we encountered a frog, we recorded the date, hour, state of
activity (i.e. calling, feeding, agonistic behaviour, transporting tadpoles), and body size
(SVL). Males were identied in the eld based on calling behaviour, and the presence
of vocal slits and a subgular vocal sac in collected individuals; females were recog-
nised because the absence of vocal slits in collected individuals (Rueda-Almonacid
et al. 2006). We deposited vouchers of the study species in the Colección de Anbios
y Reptiles of the Biology programme at the Universidad del Quindío, Armenia,
Colombia (ARUQ). Specically, we collected and preserved one adult male (ARUQ
768), two adult females (ARUQ 767, 775) and three tadpoles (ARUQ 977, 978, 979).
Individuals were euthanised with 2% lidocaine, xed in 10% formalin, and then
preserved in 70% ethanol (Angulo et al. 2006). We removed a toe from the right
foot of each individual and preserved it in 96% ethanol for future genetic analysis
(Gonzalez and Arenas-Castro 2017).
Advertisement call description
Calling males were recorded using a Sennheiser ME66 unidirectional microphone
connected to a Marantz PMD660 digital recorder. For each calling male we recorded
body temperature using an Extech infrared thermometer (accuracy 0.1°C), and mea-
sured body size (SVL) with a digital stainless-steel caliper (± 0.1 mm). All recordings
were digitised at a minimum of 16 bits resolution and 44.1 kHz sampling rate. We
estimated the temporal (resolution = 1.16 ms) and spectral features of the advertise-
ment call using the software RAVEN Pro 1.4 (Bioacoustics Research Program 2010). We
elaborated oscillograms, spectrograms, and power diagrams using a Fast Fourier
transformation window of 256 points and the Blackman algorithm (Köhler et al.
2017). We measured call duration (ms), the number of notes per call, the number of
pulses per note, note and inter-note duration (ms) (Figure 3), and the dominant
frequency (Hz) at the beginning, middle, and towards the end of each call. Our
JOURNAL OF NATURAL HISTORY 3009
sampling unit for statistical analysis was the recorded male; that is, we calculated for
each calling male the mean value for call features (if applicable) and later, using such
mean values we calculated a new mean, a standard deviation and a range of call traits
values (i.e. N = 11 males). We deposited our recordings (in WAV format) at the
Colección de Sonidos Ambientales of the Instituto Alexander von Humboldt, Villa de
Leyva, Boyacá, Colombia (Table 1).
Tadpole description
The tadpole description is based on three specimens at developmental stages 25–26
(sensu Gosner 1960) that were collected from phytotelma. We measured the following
tadpoles’ features to the nearest 0.1 mm with a digital caliper as follows (Altig and
McDiamird 1999; Altig 2007): total length (TL), body length (BL), tail length (TAL), body
width (BW), body height (BH), tail height (TH), nostril to snout distance (NSD), eye to snout
distance (ESD), interorbital distance (IOD), eye to nostril distance (END), internarial dis-
tance (IND), oral disc width (ODW), and eye diameter (ED). The presence/absence of the
papillation in the margin of the lower lip was coded for several species of Dendrobatinae
(see Appendix A for a complete list of examined material), and a character matrix edited in
Mesquite v3.03 (Maddison and Maddison 2017). Parsimonious character optimisation was
performed in the software T.N.T. v1.5 (Golobo and Catalano 2016) onto the phylogenetic
hypothesis of Grant et al. (2017). Also, we discuss how dierent putative placements of
A. daleswansoni could aect the optimisation of characters in the A. bombetes species
group.
Figure 3. Oscillogram showing temporal call features calculated in this study for the description of the
advertisement call of the poison frog A. daleswansoni.
3010 S. DUARTE-MARÍN ET AL.
Table 1. Temporal and spectral features of the advertisement call in Andinobates daleswansoni. Body size (snout–vent length, SVL), temperature of male at
recording time, and voucher code in the Colección de Sonidos Ambientales of the Instituto Alexander von Humboldt, Villa de Leyva, Boyacá, Colombia (IAvH-CSA),
IAvH-CSA-18535 corresponds to ARUQ-768 voucher. Values are mean ± standard deviation, and range in parentheses. Data of body size and temperature data are
absent for some males because they could not be captured.
Call Voucher Number analysed calls SVL
(mm)
Tempt
(°C)
Call
duration (ms)
Note duration
(ms)
Internote duration
(ms)
Number of notes/call Dominant frequency (Hz)
IAvH–CSA-3597 6 17.21 18.2 2427.2 ± 78.6
(2350–2562)
3.8 ± 0.7
(3–5)
11.8 ± 0.4
(11–12)
138.3 ± 7.6
(128–147)
3761 ± 316.1
(3273–3962)
IAvH–CSA-18534 9 18.5 17.1 3622.8 ± 331.7
(3058–3917)
1.1 ± 0.3
(1–2)
13 ± 1.5
(12–16)
201.2 ± 15.7
(180–220)
4210.4 ± 151.7
(3962–4306)
IAvH–CSA-18535 8 23.7 17.1 3608.1 ± 199.5
(3341–3949)
3.6 ± 0.1
(2–5)
14.1 ± 1.3
(13–17)
181.9 ± 6.9
(175–194)
3892.1 ± 274.2
(3273–4134)
IAvH–CSA-18536 8 17.5 17.1 2342 ± 131
(2113–2511)
3.2 ± 0.5
(3–4)
9.6 ± 0.1
(9–11)
150.2 ± 8.7
(136–156)
4177 ± 121.6
(4134–4478)
IAvH–CSA-18537 7 16.7 17.4 2922.6 ± 154.4
(2719–3157)
2.4 ± 0.7
(2–4)
10.3 ± 0.1
(9–11)
187.4 ± 8.6
(177–202)
4109.1 ± 336.2
(3617–4306)
IAvH–CSA-18538 11 18.5 21.1 2532.4 ± 123.6
(2386–2687)
1.5 ± 0.5
(1–2)
10.2 ± 0.7
(9–12)
183.8 ± 8.7
(164–195)
4306 ± 76.9
(4134–4306)
IAvH–CSA-18539 10 23.7 17.5 2681.9 ± 227.9
(2256–2902)
1.5 ± 0.5
(1–2)
12.2 ± 0.1
(10–14)
181.1 ± 14.8
(158–199)
4065 ± 88.8
(3962–4134)
IAvH–CSA-18540 6 16.5 17 2185.6 ± 155.0
(1943–2358)
2.1 ± 0.7
(1–3)
11.6 ± 0.8
(11–13)
134.2 ± 8.1
(121–140)
3846.8 ± 140.9
(3617–3962)
IAvH–CSA-18541 2 2682 ± 18.3
(2669–2695)
3.5 ± 0.7
(3–4)
9.5 ± 0.5
(9–10)
173.5 ± 0.7
(173–174)
4220 ± 121.6
(4134–4306)
IAvH–CSA-18542 9 2685.2 ± 161.2
(2358–2813)
3.0 ± 0.4
(3–4)
11.0 ± 1.2
(10–14)
175.5 ± 9.8
(147–180)
4105.3 ± 0.10
(3962–4306)
IAvH–CSA-18543 5 1634.2 ± 130.7
(1492–1834)
4.4 ± 0.5
(4–5)
10.6 ± 0.5
(10–11)
92.6 ± 8.3
(90–105)
3961.8 ± 121.9
(3789–3962)
JOURNAL OF NATURAL HISTORY 3011
Diet description
To assess the diet of A. daleswansoni we evacuated stomach contents of 12 individuals
(randomly selected) by pressing the sides of their body with two ngers in a way that
extruded the stomach. We then collected the prey items, and prodded the stomach back
into the frog with a forceps with a rounded tip (A. Amézquita, personal communication).
Although invasive, this technique does not require killing individuals. Minutes after we
prodded the stomach back into the frog, they were observed foraging or calling. We
placed all stomach contents in cryogenic vials with 90% ethanol, and later identied the
prey items to the lowest taxonomic rank possible using Domínguez and Fernández (2009).
We calculated the relative frequency of consumed items.
Behavioural observations
All behavioural records were observed during morning outings. When a specic beha-
viour was detected (i.e. tadpole transport on the back, agonistic interactions), we stayed
between one and three metres from the focal individuals. During these observations no
sudden movements were made to avoid disturbing the frogs’ behaviour. Some photo-
graphs and videos were obtained with a Nikon D5200 camera. Focal observations were
made until the observed behaviour ended.
Results
General results
We encountered 36 males (mean SVL = 18.41 mm ± 1.56 SD, range = 16.5–23.7 mm), 2
females (mean SVL = 22.10 mm ± 1.13 SD, range = 21.30–22.9 mm), and 31 individuals
whose sex could not been determined (mean SVL = 15.07 mm ± 1.12 SD,
range = 12.11–19.1 mm). Based on the six sexed frogs recorded by Rueda-Almonacid
et al. (2006) and the 38 sexed frogs recorded by us, there was no sexual size dimorphism in
A. daleswansoni (t-test = 4.33; df = 43; P = 0.73).
Advertisement call description
We recorded 81 calls belonging to eleven males. Specic data about call features for each
male recorded are shown in Table 1. The advertisement call of A. daleswansoni (Figure 4) is
composed by multiple short notes with 1 to 3 pulses each, and similar to a ‘Buzz’ sound to the
human ear. The average number of notes per call was 164.1 ± 30.1 SD (range = 92.6–201.2,
N = 11 frogs), the mean duration of each note was 2.7 ms ± 1.0 SD (range = 1.1–4.4 ms,
N = 11), and are separated by intervals of 11.4 ms ± 1.3 SD (range = 9.6–14.1 ms, N = 11). On
average, advertisement calls lasted 2.6 s ± 0.5 s SD (range = 1.6–3.6 s, N = 11), and its
dominant frequency was 4052.8 Hz ± 154.9 SD (range = 3761–4306 Hz, N = 11).
Tadpole description
Body elliptical and depressed in lateral view (BH/BL = 0.33–0.44; Figure 5(a)). In dorsal
view (Figure 5(b)), body globular, wider anteriorly, snout truncated. Eyes are dorsal and,
3012 S. DUARTE-MARÍN ET AL.
directed anterolaterally. Nares reniform, located dorsally and directed anterolaterally, with
marginal rim and small triangular eshy projection on sagittal margin. Interobital distance
2.5 times eye diameter (IOD/ED 2.1–2.5). Mouth anteroventral, laterally emarginate,
bordered by single row of rounded, marginal papillae; upper lip with a large gap in
papillation; lower lip with a small, medial, gap in papillation; submarginal papillae absent
(Figure 6). Labial tooth row formula 2(2)/3(1); A-1 = A-2, P-1 = P-2 > P-3; A2 gap large. Jaw
sheaths present, serrate, and well keratinised; upper jaw sheath arch-shaped; lower jaw
sheath V-shaped. Spiracle sinistral, tubular, lateral, and located ventral to the body’s
midline. Spiracle posterolaterad in dorsal view, and dorsad at angle of 30–45° in lateral
view. Inner wall is present. Spiracle distally free from body, with elliptical opening.
Intestines coiled, short; switchback position dextral, with remaining organs visible, not
concealed by intestines. Vent tube dextral, positioned medially, tubular, located at the
Figure 4. Oscillogram, spectrogram, and power spectrum for the advertisement call of Andinobates
daleswansoni. Male body size: 23.7 mm, temperature of calling male: 17.1°C, voucher at the Colección
de Anfibios y Reptiles of the Biology programme at the Universidad del Quindío, Armenia, Colombia:
ARUQ-768. Voucher at Colección de Sonidos Ambientales of the Instituto Alexander von Humboldt,
Villa de Leyva, Boyacá, Colombia IAvH–CSA-18535. Ilustration by Dina Lucía Rivera-Robles.
JOURNAL OF NATURAL HISTORY 3013
level of ventral n, and fused ventrally to the n; right margin is shorter than left, and the
opening is elliptical. Tail long, with musculature not reaching the rounded tip. Dorsal n
arched, originating on the tail; ventral n also arched; dorsal n slightly deeper than
ventral n. Lateral line neuromasts are inconspicuous.
In preservation tadpole colour in dorsal view is light brown and evenly pigmented. In
ventral view, body translucent, pearl grey anteriorly, with few light brown spots; poster-
iorly, the venter is light brown due to the intestines contents; posterior portion of the
ileum is dark brown. Tail is light brown anteriorly; pearl grey posteriorly; ns are
translucent. Tadpole measurements (in mm) are the mean value ± standard deviation,
and range in parentheses based on three individuals at Gosner stages 25–26: TL
14.6 ± 4.0 (range = 10.0–19.3); BL 5.2 ± 0.9 (4.3–6.2); BW 3.6 ± 0.6 (3.0–4.2); BH
2.0 ± 0.3 (1.8–2.4); TH 1.7 ± 0.5 (1.4–2.4); NSD 0.8 ± 0.1 (0.7–0.9); ESD 1.8 ± 0.4 (1.4–2.2);
IOD 1.7 ± 0.3 (1.3–2.0); END 2.82 ± 0.3 (2.2–3.2); IND 1.5 ± 0.1 (1.2–1.7); ODW 1.6 ± 0.3
(1.3–1.9); ED 0.7 ± 0.1 (0.6–0.8). Parsimonious reconstruction of ancestral character-
states for the presence/absence of the papillation gap in the lower lip was ambiguous
(Figure 7). The gap was present in most of the species of the A. bombetes group,
however the lack of data for A. dorissswansonae rendered the optimisation of this
character state ambiguous.
Figure 5. The tadpole of Andinobates daleswansoni (Gosner Stage 26) in lateral (a), dorsal (b), and
ventral (c) views. Scale bar = 5.0 mm. Voucher at the Colección de Anfibios y Reptiles of the Biology
programme at the Universidad del Quindío, Armenia, Colombia: ARUQ-977.
3014 S. DUARTE-MARÍN ET AL.
Diet description
All of the 12 individuals for which the stomach was ushed had eaten. From among their
collective contents, we identied 90 dierent prey items. All prey were arthropods,
consisting of three classes, one subclass and eight orders (Table 2). Prey of the subclass
Acari had the highest relative frequency, followed by prey of the Order Hymenoptera, and
Coleoptera (Table 2).
Behavioural observations
Individuals were more common along the forest edge than in the forest interior. Males
called from fallen leaves, small cavities or tunnels in the ground, on moss, or associated
with tree roots. We observed four males transporting one or two tadpoles on their backs
(Figure 8). We found three tadpoles occupying tanks of the Elephant Ear plant
(Xanthosoma robustum; Araceae), growing in an abandoned pine plantation (Figure 8).
We documented a single agonistic interaction between two males (SVL = 19.0 and
17.2 mm) at 09:11 h on 15 October 2018. This bout consisted of vocalisations by both
males, the larger male followed the smaller one (Figure 9(a)); the ght included inguinal
grasping (Figure 9(b,c)), and beating with the forelimbs (Figure 9(d)). This ght lasted
Figure 6. Images of the oral disc (a, b), vent tube or spiracle (c), and limb buds of the tadpole of
Andinobates daleswansoni (Gosner Stage 26). Scale bar = 1.0 mm. Voucher at the Colección de Anfibios
y Reptiles of the Biology programme at the Universidad del Quindío, Armenia, Colombia: ARUQ-978.
Black arrow shows the gap in the marginal papillae.
JOURNAL OF NATURAL HISTORY 3015
approximately 39 minutes, and ended when the smaller male ed (see supplementary
videos at https://doi.org/10.6084/m9.gshare.11921037.v1).
Discussion
Advertisement call
Advertisement calls have been described for eleven of the 15 recognised species of
Andinobates (Table 3). However, most of these descriptions are incomplete; for example,
they lack data on note duration (Brown et al. 2011). The advertisement call of Andinobates
Figure 7. Most parsimonious ancestral character-state reconstruction of the presence/absence of the
papillation gap in the lower lip of Andinobates species onto the phylogenetic hypothesis of Grant et al.
(2017); trimmed in the figure to show only Andinobates and Ranitomeya. Note that the presence of the
gap optimises ambiguously.
3016 S. DUARTE-MARÍN ET AL.
consists of a ‘Buzz’ composed by a series of short notes (e.g. Myers and Daly 1976; Myers
et al. 1984; Batista et al. 2014), but there are some interspecic dierences in temporal call
features. For instance, the call duration in A. daleswansoni is longer than A. claudiae,
A. minutus, A. fulguritus and A. victimatus and similar to other Andinobates (Table 3); inter-
note duration in A. daleswansoni is shorter than in A. claudiae, but is longer than that in
the other species of the genus. Regarding spectral call features, A. daleswansoni have the
advertisement call with the lowest dominant frequency in the whole genus (Table 3).
A further detailed interspecic comparison of advertisement call features for
Andinobates is restrained here, because in most cases authors do not specify body size
and temperature of calling males (Table 3). In anurans, body size and call peak frequency
are inversely related, and it is common for body temperature aects values of temporal
attributes of calls (Gerhardt and Huber 2002; Vargas-Salinas and Amézquita 2014).
Therefore, we highlight the importance of recording the size and body temperature of
signallers when authors want to characterise advertisement call of poison frogs.
Tadpole morphology
With our description for Andinobates daleswansoni, the external tadpole morphology is
known for nine species of Andinobates (Silverstone 1975; Myers and Daly 1976, 1980; Ruiz-
Carranza and Ramírez-Pinilla 1992). Morphological features in the tadpole of
A. daleswansoni, such as a depressed body, massive jaw sheaths, low tail ns with rounded
tip, and ventrally dislocated spiracle, are also present in other species of the genus as well
as other Dendrobatini (sensu Grant et al. 2017; e.g. Myers et al. 1984; Caldwell and Myers
1990; Lynch 2006). This means that tadpole morphology in Andinobates as well as other
Table 2. Diet of the poison frog Andinobates daleswansoni based on the analysis of items content in
stomach of 12 frogs. The number of prey by taxa, and their relative frequency are shown.
Taxa No. of Prey Relative frequency
Phylum Arthropoda
Class Aracnida
Subclass Acari
49 0.544
Order Pseudoscorpionida 1 0.011
Class Entognatha
Order Collembola
5 0.055
Class Insecta
Order Coleoptera
Family Curculionidae
1 0.011
Family Ptilidae 2 0.022
Family Staphylinidae
Subfamiliy Oxytelinae
1 0.011
Subfamiliy Pselaphinae 5 0.055
Subfamiliy Oxytelinae 1 0.011
Order Diptera 3 0.033
Order Hemiptera 2 0.022
Order Hymenoptera
Superfamily Chalcidoidea
4 0.044
Superfamily Vespoidea
Subfamiliy Dolichoderinae
2 0.022
Subfamiliy Myrmicinae
Solenopsis
6 0.067
Strumygenys 2 0.022
Order Lepidoptera 3 0.033
Order Thysanoptera 3 0.033
JOURNAL OF NATURAL HISTORY 3017
Figure 8. Habitat and breeding microhabitat of Andinobates daleswansoni. Images of an abandoned
pine plantation shows (arrow) a plant of Xanthosoma robustum (Araceae), which is used for parents as
microhabitat for the metamorphosis of tadpoles (a); adult male transporting a tadpole on the back
observed in the leaf of a X. robustum (b); tadpole in a phytothelmata in the axis of X. robustum (c).
Pictures B and C by Andres Felipe Cardona.
3018 S. DUARTE-MARÍN ET AL.
Dendrobatini, is conservative. However, the absence of papillae in the medial region of
the lower lip, or the ventral gap, varies across species of Andinobates (Grant et al. 2017).
This ventral gap in the marginal papillae of the lower lip has been described in the larvae
of A. abditus (Myers and Daly 1976), A. bombetes (Myers and Daly 1980), A. opisthomelas
(Silverstone 1975), A. tolimensis (Bernal et al. 2007), A. virolinensis (Ruiz-Carranza and
Ramírez-Pinilla 1992) and A. cassidyhornae (P. H. dos Santos Dias, pers. obs.). Here we
conrm the presence of this ventral gap in the larvae of A. daleswansoni.
The presence of a gap in the marginal papillae of the lower lip has been
suggested as synapomorphy for the A. bombetes species group (e.g. Silverstone
1975). However, to unambiguously conrm this hypothesis, the condition of this
character still needs to be examined in the tadpole of A. dorisswansonae. There are
some possible scenarios (Figure 10(a–d)) would render the presence of such gap as
an unambiguous synapomorphy for the A. bombetes species group: 1) if the tadpole
of A. dorisswansonae (unknown at present), also exhibits a gap in the marginal
papillae of the lower lip (Figure 10(a)); 2) if A. daleswansoni is the sister taxa of
A. dorisswansonae (Figure 10(c)); or 3) if A. daleswansoni is the sister taxa of all the
species in the A. bombetes group (Figure 10(d)). Further evidence is needed to test
these scenarios. Note that if the tadpoles of A. dorisswansonae lack the gap, the
Figure 9. Images showing a sequence of the agonistic interaction between two males of Andinobates
daleswansoni. Note that one of the males is calling (a) and males exhibit different body positions (b,
c and d) through the interaction. See video in supplementary material.
JOURNAL OF NATURAL HISTORY 3019
Table 3. Summary of temporal and spectral features of the advertisement call for eleven species in the genus Andinobates. Values shown ranges because
descriptive analysis of such features was not published by the corresponding authors.
Species SVL Sample
Size
Duration call
(ms)
No.
Notes
Duration note
(ms)
Duration inter–note
(ms)
Peak frecuency
(Hz)
Source
A. bombetes 84 84 900–1700 98–190 – 8.8 4000–4800 Brown et al. 2011; Vargas–Salinas et al. 2013b,
2014
A. cassidyhornae – 7 1940 220–234 1.94 10.1 4320 Amezquita et al. 2013
A. daleswansoni 1809.36–3622.77 93–201 1.11–4.16 9.65–14.12 3761–4306 This study
A. dorisswansonae – – 1400–1600 72–78 – 6.5 4100–5410 Brown et al. 2011
A. opisthomelas – – 1600–2300 215–224 – – 5000–5500 Brown et al. 2011
A. tolimensis – – 840–990 – – 2.5 4730–5220 Brown et al. 2011
A. claudiae – 850–1030 55–65 – 18–24 5773–6079 Brown et al. 2011
A. geminisae 1 1600 87 7.8 – 4120–4740 Batista et al. 2014
A. minutus – 200–1100 20–71 – 1.2–3.2 5400–6400 Brown et al. 2011
A. fulguritus – 190–340 28–85 – 3.1–5.9 4834–5161 Brown et al. 2011; Lötters et al. 2007
A. victimatus 5 420–580 99–190 – – 5650–5860 Marquez et al. 2017
3020 S. DUARTE-MARÍN ET AL.
presence of the gap would be a synapomorphy for all the species of the A. bombetes
species group (Figure 10(b)).
Diet description
The diet of adult A. daleswansoni consists of a variety of small arthropods (Table 2), as
has been recorded for other species of the genus Andinobates (Silverstone 1975;
Figure 10. Alternative hypothetical reconstruction of characters considering the presence a) and
absence b) of the gap in the lower lip in tadpoles of A. dorisswasonae (unknown at present), and
considering two alternative phylogenetic placement of A. daleswansoni, as sister to A. dorisswasonae
c), and as sister to all species of the A. bombetes species group d). Note that under a, c, and d the
presence of the gap would optimise as a synapomorphy for the A. bombetes species group.
JOURNAL OF NATURAL HISTORY 3021
Valderrama-Vernaza et al. 2009; Gómez-Fernández et al. 2013; Gómez-Hoyos et al. 2014;
Agudelo-Cantero et al. 2015; Rivas et al. 2019). It is likely that the prey items consumed
by members of Andinobates is determined by their mouth dimensions and the avail-
ability of prey items in the microhabitat (Toft 1995; Caldwell 1996; Vitt and Caldwell
2014). However, the predominance of Acari, Hymenoptera and Coleoptera that we
recorded for A. daleswansoni also has been recorded in the diet of other poison frogs
with similar or larger mouth dimensions (Forti et al. 2011; Arce Domínguez and Rengifo
Mosquera 2013; Osorio-Domínguez et al. 2015; Pacheco et al. 2020). Acari,
Hymenoptera and Coleoptera in the diet of poison frogs is associated to the sequestra-
tion of chemical compounds used against predators (Daly et al. 2000; Santos et al. 2003;
Darst et al. 2005; Saporito et al. 2012; Tarvin et al. 2017). It is possible that
A. daleswansoni is an active forager, like other poison frogs (Donnelly 1991; Toft 1995;
Pröhl et al. 2010), but given that there are dendrobatids that exhibit an opportunistic
sit-and-wait foraging strategy (e.g. Colostethus beebei, Bourne 2001), data of arthropod
availability in the study area are necessary before we can condently determine the
foraging strategy in A. daleswansoni.
Behavioural observations
With respect to parental care, A. daleswansoni resembles congeneric species. The trans-
port of tadpoles to phytotelmata in bromeliads where they nish metamorphosis is
performed by males, who transport their ospring after egg hatching (Myers and Daly
1980; Brown et al. 2011; Summers and Tumulty 2014). The presence of tadpoles in
phytotelmata other than those in bromeliads indicates that A. daleswansoni has
a greater niche breadth for tadpole development than previously recorded. The record
of males using phytotelmata in the Elephant Ear plant X. robustum for depositing their
tadpoles is important, because illegal collection of bromeliads is considered one of the
threats for the conservation of this frog (Velásquez-Álvarez et al. 2016; IUCN 2017).
Protecting bromeliads is necessary for the conservation of many anuran species
(Sabagh et al. 2017), but for A. daleswansoni it may also be important to promote the
growth of X. robustum, and maybe other plants with phytotelmata, and therefore, oer
additional microhabitats for ospring.
In poison frogs of the genus Andinobates, males defend territories against conspecics
engaging in agonistic interactions through the use of auditory signals (Myers and Daly
1980; Brown et al. 2011; Marquez et al. 2017), and according to this study also through
physical interactions. Physical ghts have been also observed in Andinobates bombetes (L.F.
Arcila-Pérez and M.A. Atehortua-Vallejo, unpub. data). Acoustic interactions and physical
ghts are widespread behaviours in males of poison frogs (e.g. Dendrobates auratus,
Summers 1989; Oophaga pumilio, Pröhl 1997; O. granulifera, Phyllobates vittatus, Allobates
talamancae, Silverstoneia nubicola Summers 2000; O. histrionica; Méndez-Narváez and
Amézquita 2014). Territorial behaviour in poison frogs have been correlated to the occupa-
tion of resources such as bromeliads and prey items (Summers and McKeon 2004; Erich
2013; Ringler et al. 2013; Poelman et al. 2013; Vargas-Salinas and Amézquita 2013b).
Bromeliads are essential for the reproduction of many poison frogs (Summers and
McKeon 2004) while specic food items determine chemical defences and warming col-
ouration of individuals (Donnelly 1991; Saporito et al. 2010; Forti et al. 2011). However, we
3022 S. DUARTE-MARÍN ET AL.
did not quantied microhabitat features for testing which kind of resources are promoting
agonistic behaviours in A. daleswansoni, but it is expected to be similar to those in others
poison frogs.
Conclusions
The call of the poison frog A. daleswansoni to the human ear is similar to the call in co-
generic species; however, when a detailed and quantitative interspecic comparison was
feasible, dierences in spectral and temporal features of the advertisement call are
evident. Regarding the tadpole morphology, it is similar to other Andinobates and
Dendrobatinii. More studies are necessary to establish whether a gap in the marginal
papillae of the lower lip, is a synapomorphy for the group A. bombetes. Like other poison
frogs, males of A. daleswansoni prey on small arthropods present in leaitter. This species
can use phytotelmata other than those in bromeliads for tadpole development, and males
exhibit acoustic and physical agonistic interactions with conspecics males.
Highlights
●The advertisement call of A. daleswansoni is composed by multiple short notes with 1 to 3 pulses
each, and sounds similar to a ‘Buzz’.
●Tadpoles have a gap in the marginal papillae, whose status as a synapomorphy for the group
A. bombetes is discussed.
●Andinobates daleswansoni has a greater niche breadth for tadpole development than previously
recorded.
●The diet of A. daleswansoni consists of small arthropods (meanly Acari, Hymenoptera and
Coleoptera).
●An agonistic interaction between two males consisted of the ght included inguinal grasping
and beating with the forelimbs.
Acknowledgements
We thank Adolfo Amézquita (U. de los Andes), Ana Almendaríz (EPN), Antoine Fouquet (AF), David
Kizirian (AMNH), Frank Glaw (ZSM), Gregory Pauly (LACM), Jessa Watters (OMNH), Jesus Córova
(MUSM), John D. Lynch (ICN), Richard Glor (KU), Santiago Castroviejo-Fisher (MCP), and Taran Grant
(MZUSP; TG) for kindly granting access to the specimens under their care. Also, thanks to Catherine
Rodríguez Hurtado, Andrés Felipe Toro Cardona, Johan A. Giraldo Romero, Ricardo A. García Arango,
Milton Pineda Duque, José Alzate Henao, Simon D. Herrera, Gonzaga Bedoya and Paula A Navarro,
for their invaluable help in eldwork. Finally, thanks to the Biology programme of the University of
Quindío, Colombia, for logistic support during this research. Two anonymous reviewers greatly
improved previous versions of this manuscript.
Disclosure statement
No potential conict of interest was reported by the authors.
JOURNAL OF NATURAL HISTORY 3023
Ethical standard
The authors followed ethical procedures by the Animal Behaviour Society during all the observa-
tions and experiments performed in this study. Additionally, this study was made under the
memorandum #20172200002313 (June 01 of 2017) of the Parques Nacionales de Colombia.
Author contribution
SDM, CCGA and FVS conceived the study, SDM, CCGA and FVS collected data in the eld, SDM,
CCGA analyzed the data, PHD describe tadpole morphology and analyzed characters optimization,
GAA describe diet, SDM and FVS wrote the manuscript with the help of PHD and CCGA.
Funding
Thanks to Colombia’s National Natural Parks system, Wildlife Conservation Society (WCS) and the
Zoo Zurich for the nancial and logistical support to carry out this study under the Mono Hernández
Research Fund. Contributions by P.H.S. Dias were supported by the Fundação de Amparo à Pesquisa
do Estado de São Paulo (FAPESP; procs. #2012/10000-5, #2013/20420-4, and #2015/11239-0).
ORCID
Sebastián Duarte-Marín http://orcid.org/0000-0001-6201-7527
Cristian C. González-Acosta http://orcid.org/0000-0002-1663-6762
Pedro Henrique Santos Dias http://orcid.org/0000-0002-6428-6496
Gustavo A. Arias-Álvarez http://orcid.org/0000-0001-9990-4525
Fernando Vargas-Salinas http://orcid.org/0000-0003-1251-647X
References
Agudelo-Cantero GA, Castaño-valencia RS, Castro-herrera F, Fierro-Pérez L, Asencio-Santomio H.
2015. Diet of the blue-bellied poison frog Andinobates minutus (Anura: Dendrobatidae) in two
populations from the Colombian Pacic. J Herpetol. 49(3):452–461. doi:10.1670/13-202.
Altig R, McDiamird RW. 1999. Body plan. Development and morphology. In: McDiamird RW, Altig R,
editors. Tadpoles, the biology of Anuran Larvae. Chicago: Chicago University Press; p. 24–51.
Altig R. 2007. A primer for the morphology of anuran tadpoles. Herpetol Conserv Bio. 2(1):71–74.
Amézquita A, Flechas SV, Lima AP, Gasser H, Hödl W. 2011. Acoustic interference and recognition
space within a complex assemblage of dendrobatid frogs. P Natl Acad Sci. 108(41):17058–17063.
doi:10.1073/pnas.1104773108.
Amezquita A, Marquez R, Medina R, Mejia-Vargas D, Kahn TR, Suarez G, Mazariegos L. 2013. A new
species of Andean poison frog, Andinobates (Anura: Dendrobatidae), from the northwestern
Andes of Colombia. Zootaxa. 3620(1):163–178.
Angulo A, Rueda-Almonacid JV, Rodríguez-Mahecha JV, La Marca E. 2006. Técnicas de inventario
y monitoreo para los anbios de la región tropical andina. Conservación Internacional. Serie
Manuales de Campo Nº 2. Bogotá (Colombia): Panamericana Formas e Impresos S.A.
Arce Domínguez F, Rengifo Mosquera JT. 2013. Dieta de Phyllobates aurotaenia y Oophaga histrio-
nica (Anura: Dendrobatidae) en el municipio del Alto Baudo, Choco, Colombia. Act Zool Mex. 29
(2):255–268.
Arcila-Pérez LF, Atehortua-Vallejo M, Vargas-Salinas F. 2020. Homing in the rubí poison frog
Andinobates bombetes (Dendrobatidae). Copeia. 108(4):948–956. doi:10.1643/CE-19-284.
Ballesteros H, Arroyave JF, Walker R, Echeverry L, Acosta H, Betancourt AF, Diaz-Mesa J, Lopez MP,
Moreno-Ortiz E, Villegas H, et al. 2009. Plan de manejo 2008 – 2012. Parque Nacional Natural Selva
3024 S. DUARTE-MARÍN ET AL.
de Florencia. Corregimiento de Florencia - Samaná (Caldas): Parques Nacionales Naturales de
Colombia.
Batista A, Jaramillo CA, Ponce M, Crawford AJ. 2014. A new species of Andinobates (Amphibia:
Anura: Dendrobatidae) from west central Panama. Zootaxa. 3866(3):333–352. doi:10.11646/
zootaxa.3866.3.2.
Bernal MH, Luna-Mora VF, Gallego O, Quevedo A. 2007. A new species of poison frog (Amphibia:
Dendrobatidae) from the Andean mountains of Tolima, Colombia. Zootaxa. 1638:59–68.
doi:10.11646/zootaxa.1638.1.5.
Biavati GM, Wiederhecker HC, Colli GR. 2004. Diet of Epipedobates avopictus (Anura:
Dendrobatidae) in a Neotropical savanna. J Herpetol. 38(4):510–518. doi:10.1670/30-04A.
Bioacoustics Research Program. 2010. Raven Pro: interactive sound analysis software [Computer
software]. Version 1.4. Ithaca (NY): The Cornell Lab of Ornithology. http://www.birds.cornell.edu/
raven.
Bourne GR. 2001. Color pattern, predator avoidance, and foraging behavior in the golden frog
Colestethus beebei (Anura: Dendrobatidae). Herpetol Rev. 32(4):225–228.
Brown JL, Morales V, Summers K. 2009. Home range size and location in relation to reproductive
resources in poison frogs (Dendrobatidae): a Monte Carlo approach using GIS data. Anim Behav.
77(2):547–554. doi:10.1016/j.anbehav.2008.10.002.
Brown JL, Morales V, Summers K. 2010. A key ecological trait drove the evolution of biparental care
and monogamy in an amphibian. T Am Natur. 175(4):436–446. doi:10.1086/650727.
Brown JL, Twomey E, Amézquita A, Barbosa De Souza M, Caldwell JP, Lötters S, Von May R,
Melo-Sampaio PR, Mejía-Vargas D, Perez-Peña P, et al. 2011. A taxonomic revision of the
Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae). Zootaxa. 3083
(1):1–120. doi:10.11646/zootaxa.3083.1.1.
Brown JL, Twomey E, Pepper M, Rodriguez MS. 2008. Revision of the Ranitomeya fantastica species
complex with description of two new species from Central Peru (Anura: Dendrobatidae). Zootaxa.
1823(1):1–24.
Caldwell JP. 1996. The evolution of myrmecophagy and its correlates in poison frogs (Family
Dendrobatidae). J Zool. 240(1):75–101. doi:10.1111/j.1469-7998.1996.tb05487.x.
Caldwell JP, Myers CW. 1990. A new poison frog from Amazonian Brazil, with further revision on the
quinquevittatus group of Dendrobates. Am Mus Novit. 2988:1–21.
Clemmons JR, Buchholz R. 1997. Behavioral approaches to conservation in the wild. Cambridge, UK:
Cambridge University Press.
Coloma LA. 1995. Ecuadorian frogs of the genus Colostethus (Anura: Dendrobatidae). Lawrence (KS):
Natural History Museum, University of Kansas.
Crump ML, Scott NJ. 1994. Visual encounter surveys. In: Heyer RW, Donnelly MA, McDiarmid RW,
Hayek LA, Foster MS, editors. Measuring and monitoring biological diversity. Standard methods
for amphibians. Washington and London: Smithsonian Institution Press; p. 84–92.
Daly JW, Garrao HM, Jain P, Spande TF, Snelling RR, Jaramillo C, Rand AS. 2000. Arthropod–frog
connection: decahydroquinoline and pyrrolizidine alkaloids common to microsympatric myrmi-
cine ants and dendrobatid frogs. J Chem Ecol. 26(1):73–85. doi:10.1023/A:1005437427326.
Darst CR, Menéndez-Guerrero PA, Coloma LA, Cannatella DC. 2005. Evolution of dietary specializa-
tion and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. T Am Natur.
165(1):56–69. doi:10.1086/426599.
Domínguez E, Fernández HR. 2009. Macroinvertebrados bentónicos sudamericanos: sistemática
y biología. Tucumán: Fundación Miguel Lillo.
Donnelly MA. 1991. Feeding patterns of the strawberry poison frog, Dendrobates pumilio (Anura:
Dendrobatidae). Copeia. 1991(3):723–730. doi:10.2307/1446399.
Dos Santos Dias PH, Anganoy-Criollo M, Guayasamin JM, Grant T. 2018. The tadpole of Epipedobates
darwinwallacei Cisneros-Heredia and Yánez-Muñoz, 2011 (Dendrobatidae: Colostethinae), with
new synapomorphies for Epipedobates. S Am J Herpetol. 13(1):54–63. doi:10.2994/SAJH-D-17-
00023.1.
JOURNAL OF NATURAL HISTORY 3025
Duarte-Marín S, González-Acosta C, Vargas-Salinas F. 2018. Estructura y composición de ensam-
blajes de anbios en tres tipos de hábitat en el Parque Nacional Natural Selva de Florencia,
Cordillera Central de Colombia. Rev Acad Cienc. 42(163):227–236.
Erdtmann L, Amézquita A. 2009. Dierential evolution of advertisement call traits in Dart-Poison
Frogs (Anura: Dendrobatidae). Ethology. 115(9):801–811. doi:10.1111/j.1439-0310.2009.01673.x.
Erich M. 2013. Bet-hedging in Tadpole deposition in the neotropical frog, Allobates femoralis
[doctoral dissertation]. Uniwien.
Forsman A, Hagman M. 2006. Calling is a honest indicator of paternal genetic quality in poison frogs.
Evolution. 60:2148–2157. doi:10.1111/j.0014-3820.2006.tb01852.x.
Forti LR, Tissiani ASO, Mott T, Strüssmann C. 2011. Diet of Ameerega braccata (Steindachner, 1864)
(Anura: Dendrobatidae) from Chapada dos Guimarães and Cuiabá, Mato Grosso State, Brazil. Braz
J Biol. 71(1):189–196. doi:10.1590/S1519-69842011000100027.
Frost DR. 2021. Amphibian species of the world: an online reference. Version 6.1. New York (USA):
American Museum of Natural History. [accessed 2021 Jan]. http://research.amnh.org/herpetol
ogy/amphibia/index.html.
Gerhardt HC, Huber F. 2002. Acoustic communication in insects and anurans: common problems
and diverse solutions. Chicago (IL): The University of Chicago Press.
Golobo PA, Catalano SA. 2016. TNT version 1.5, including a full implementation of phylogenetic
morphometrics. Cladistics. 32(3):221–238. doi:10.1111/cla.12160.
Gómez-Fernández D, Castaño S, Fierro L, Armbrecht I, Asencio-Santomio H. 2013. Diet of
Andinobates minutus (Anura: Dendrobatidae) in a tropical rainforest from La Palma island,
Colombia. Caldasia. 35(2):325–332.
Gómez-Hoyos DA, López-García MM, Soto-Garzón CA, Méndez-Rojas DM, Kahn TR, Velasco JA. 2014.
Geographic variation in the diet of the Cauca Poison Frog Andinobates bombetes (Anura:
Dendrobatidae) in the Andes of Colombia. Herpetol Notes. 7:559–564.
Gonzalez MA, Arenas-Castro H. 2017. Recolección de tejidos biológicos para análisis genéticos.
Bogotá (Colombia): Instituto de Investigación de Recursos Biológicos Alexander von Humboldt.
Gosling LM, Sutherland WJ. 2000. Behaviour and conservation. Cambridge (UK): Cambridge
University Press.
Grant T, Frost DR, Caldwell JP, Gagliardo R, Haddad CFB, Kok PJR, Means DB, Noonan BP,
Schargel WE, Wheeler WC. 2006. Phylogenetic systematics of dart-poison frogs and their relatives
(Amphibia: Athesphatanura: Dendrobatidae). B Am Mus Nat Hist. 2006(299):6–262.
Grant T, Rada M, Anganoy-Criollo M, Batista A, Dias PHS, Jeckel AM, Machado DJ, Rueda-Almonacid
JV. 2017. Phylogenetic systematics of dart-poison frogs and their relatives revisited (Anura:
Dendrobatoidea). S Am J Herpetol. 12:S1–S90. doi:10.2994/SAJH-D-17-00017.1.
IUCN SSC Amphibian Specialist Group. 2017. Andinobates daleswansoni. The IUCN Red List of
Threatened Species 2017: e.T136124A85906859. [accessed 2019 April and May]. http://dx.doi.
org/10.2305/IUCN.UK.2017-3.RLTS.T136124A85906859.
Kahn TR, La Marca E, Lötters S, Brown JL, Twomey E, Amézquita A. 2016. Aposematic poison frogs
(Dendrobatidae) of the Andean countries: Bolivia, Colombia, Ecuador, Perú and Venezuela.
Bogotá (DC-Colombia): International Conservation.
Köhler J, Jansen M, Rodríguez A, Kok PJ, Toledo LF, Emmrich M, Glaw F, Haddad CFB, Rödel MO,
Vences M. 2017. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and
recommendations for best practice. Zootaxa. 4251:1–124. doi:10.11646/zootaxa.4251.1.1.
Lötters S, Jungfer KH, Henkel FW, Schmidt W. 2007. Poison frogs: biology, species and captive
husbandry. Frankfurt (Germany): Chimaira.
Lötters S, Reichle S, Jungfer KH. 2003. Advertisement calls of Neotropical poison frogs (Amphibia:
Dendrobatidae) of the genera Colostethus, Dendrobates and Epipedobates, with notes on den-
drobatid call classication. J Nat Hist. 37(15):1899–1911. doi:10.1080/00222930110089157.
Lynch JD. 2006. The tadpoles of frogs and toads found in the lowlands of northern Colombia. Rev
Acad Cienc. 30(116):443–457.
Maddison W, Maddison D. 2017. Mesquite: a modular system for evolutionary analysis. Version 3.31.
[accessed 2019 Jun 15]. http://mesquiteproject.org.
3026 S. DUARTE-MARÍN ET AL.
Marquez R, Mejia-Vargas D, Palacios-Rodriguez P, Ramírez-Castañeda V, Amézquita A. 2017. A new
species of Andinobates (Anura: Dendrobatidae) from the Urabá region of Colombia. Zootaxa.
4290(3):531–546. doi:10.11646/zootaxa.4290.3.7.
Medina I, Wang I, Salazar C, Amézquita A. 2013. Hybridization promotes color polymorphism in the
aposematic harlequin poison frog, Oophaga histrionica. Ecol Evol. 3:4388–4400. doi:10.1002/
ece3.794.
Méndez-Narváez J, Amézquita A. 2014. Physical combat in the poison-arrow frog, Kokoé-pá
(Oophaga histrionica) from Arusí, Choco, Colombia. Herpetol Notes. 7:1–2.
Menin M, Pinto RMC, Pegorini RJ, Da Silva MR. 2017. Redescription of the tadpole of Ameerega
hahneli (Boulenger, 1884)(Anura: Dendrobatidae) with notes on ontogenetic variations and
development habitats. S Am J Herpetol. 12(3):236–243. doi:10.2994/SAJH-D-17-00052.1.
Myers CW, Daly JW. 1976. Preliminary evaluation of skin toxins and vocalizations in taxonomic and
evolutionary studies of poison-dart frogs (Dendrobatidae). B Am Mus Nat Hist. 157(3):177–259.
Myers CW, Daly JW. 1980. Taxonomy and ecology of Dendrobates bombetes, a new Andean poison
frog with new skin toxins. Am Mus Novit. 2692:1–23.
Myers CW, Daly JW, Martínez V. 1984. An arboreal poison frog (Dendrobates) from western Panama.
Am Mus Novit. 2783:1–20.
Osorio-Domínguez D, Valenzuela L, Bermúdez-Rivas C, Castaño S. 2015. Descripción de la dieta de
una población de Oophaga histrionica (Athesphatanura: Dendrobatidae) en un enclave seco del
Valle del Cauca, Colombia. Rev Bio Neot. 5(1):29–35.
Pacheco EO, Ceron K, Akieda PS, Santana DJ. 2020. Diet and morphometry of two poison frog
species (Anura, Dendrobatidae) from the plateaus surrounding the Pantanal of Mato Grosso do
Sul state, Brazil. Stud Neo Fau Env. 55(1):1–9.
Páez-Vacas MI, Coloma L, Santos JC. 2010. Systematics of the Hyloxalus bocagei complex (Anura:
Dendrobatidae), description of two new cryptic species, and recognition of H. maculosus.
Zootaxa. 2711(1):1–75. doi:10.11646/zootaxa.2711.1.1.
Pašukonis A, Loretto MC, Hödl W. 2018. Map-like navigation from distances exceeding routine
movements in the three-striped poison frog (Ameerega trivittata). J Exp Biol. 221(2):jeb169714.
doi:10.1242/jeb.169714.
Pašukonis A, Loretto MC, Landler L, Ringler M, Hödl W. 2014b. Homing trajectories and initial
orientation in a Neotropical territorial frog, Allobates femoralis (Dendrobatidae). Front Zool. 11
(1):29. doi:10.1186/1742-9994-11-29.
Pašukonis A, Loretto MC, Rojas B. 2019. How far do tadpoles travel in the rainforest? Parent-assisted
dispersal in poison frogs. Evol Ecol. 33(4):613–623. doi:10.1007/s10682-019-09994-z.
Pašukonis A, Ringler M, Brandl HB, Mangione R, Ringler E, Hödl W. 2013. The homing frog: high
homing performance in a territorial dendrobatid frog Allobates femoralis (Dendrobatidae).
Ethology. 119(9):762–768. doi:10.1111/eth.12116.
Pašukonis A, Trenkwalder K, Ringler M, Ringler E, Mangione R, Steininger J, Warrington L, Hödl W.
2016. The signicance of spatial memory for water nding in a tadpole-transporting frog. Anim
Behav. 116:89–98. doi:10.1016/j.anbehav.2016.02.023.
Pašukonis A, Warrington I, Ringler M, Hödl W. 2014a. Poison frogs rely on experience to nd the way
home in the rainforest. Biol Letters. 10(11):20140642. doi:10.1098/rsbl.2014.0642.
Poelman EH, Dicke M. 2007. Oering ospring as food to cannibals: oviposition strategies of
Amazonian poison frogs (Dendrobates ventrimaculatus). Evol Ecol. 21(2):215–227. doi:10.1007/
s10682-006-9000-8.
Poelman EH, Van Wijngaarden RP, Raaijmakers CE. 2013. Amazon poison frogs (Ranitomeya ama-
zonica) use dierent phytotelm characteristics to determine their suitability for egg and tadpole
deposition. Evol Ecol. 27(4):661–674. doi:10.1007/s10682-013-9633-3.
Pröhl H. 1997. Patrón reproductivo en Dendrobates pumilio (Anura: Dendrobatidae). Rev Biol
Neotrop. 45:1669–1676.
Pröhl H. 2005. Territorial behavior in dendrobatid frogs. J Herpeto. 39(3):354–365. doi:10.1670/162-
04A.1.
JOURNAL OF NATURAL HISTORY 3027
Pröhl H, Mebs D, Ospina SM, Staudt K. 2010. Foraging behaviour and territoriality of the strawberry
poison frog (Oophaga pumilio) in dependence of the presence of ants. Amphibia-Reptilia. 31
(2):217–227. doi:10.1163/156853810791069100.
Ringler E, Pašukonis A, Hödl W, Ringler M. 2013. Tadpole transport logistics in a Neotropical poison
frog: indications for strategic planning and adaptive plasticity in anuran parental care. Front Zool.
10(1):67. doi:10.1186/1742-9994-10-67.
Ringler M, Ringler E, Magana Mendoza D, Hödl W. 2011. Intrusion experiments to measure territory
size: development of the method, tests through simulations, and application in the frog Allobates
femoralis. PLoS ONE. 6(10):e25844. doi:10.1371/journal.pone.0025844.
Rivas LM, García JB, Rengifo JT. 2019. Composición dietarías de dos especies del género Andinobates
(Anura: Dendrobatidae) en el bosque pluvial tropical en el departamento del Chocó, Colombia.
B Cient Mus Hist Nat. 23(1):85–97.
Rojas B. 2016. Behavioural, ecological, and evolutionary aspects of diversity in frog colour patterns.
Biol Rev. 92(2):1059–1080.
Rueda-Almonacid JV, Lynch JD, Amézquita A. 2004. Libro Rojo de los Anbios de Colombia. Serie
Libros de Especies Amenazadas de Colombia. Bogotá (DC-Colombia): Instituto de Ciencias
Naturales-Universidad Nacional de Colombia, Ministerio del Medio Ambiente.
Rueda-Almonacid JV, Rada M, Sánchez-Pacheco SJ, Velásquez-Álvarez AA, Quevedo-Gil A. 2006. Two
new and exceptional poison dart frogs of the genus Dendrobates (Anura: Dendrobatidae) from
the Northeastern Flank of the cordillera Central of Colombia. Zootaxa. 1259:39–54.
Ruiz-Carranza PM, Ardila-Robayo MC, Lynch JD. 1996. Lista actualizada de la fauna de Amphibia de
Colombia. Rev Acad Col Cienc Ex Fís Nat. 20(77):365–415.
Ruiz-Carranza PM, Ramírez-Pinilla MP. 1992. Una nueva especies de Minyobates (Anura:
Dendrobatidae) de Colombia. Lozania Bogotá. 61:1–16.
Ruxton GD, Allen WL, Sherratt TN, Speed MP. 2018. Avoiding attack: the evolutionary ecology of
crypsis, warning signals and mimicry. New York (NY): Oxford University Press.
Sabagh LT, Ferreira RB, Rocha CFD. 2017. Host bromeliads and their associated frog species: further
considerations on the importance of species interactions for conservation. Symbiosis. 73
(3):201–211. doi:10.1007/s13199-017-0500-9.
Sanchez DA. 2013. Larval morphology of dart-poison frogs (Anura: Dendrobatoidea: Aromobatidae
and Dendrobatidae). Zootaxa. 3637(5):569–591. doi:10.11646/zootaxa.3637.5.5.
Santos JC, Baquero M, Barrio-Amoros C, Coloma LA, Erdtmann LK, Lima AP, Cannatella DC. 2014.
Aposematism increases acoustic diversication and speciation in poison frogs. P Roy Soc B-Bio
Sci. 281(1796):20141761–20141761.
Santos JC, Coloma LA, Cannatella DC. 2003. Multiple, recurring origins of aposematism and diet
specialization in poison frogs. P Natl Acad Sci USA. 100(22):12792–12797. doi:10.1073/
pnas.2133521100.
Saporito RA, Donnelly MA, Madden AA, Garrao HM, Spande TF. 2010. Sex-related dierences in
alkaloid chemical defenses of the dendrobatid frog Oophaga pumilio from Cayo Nancy, Bocas del
Toro, Panama. J Nat Pro. 73(3):317–321.
Saporito RA, Donnelly MA, Spande TF, Garrao HM. 2012. A review of chemical ecology in poison
frogs. Chemoecology. 22:159–168. doi:10.1007/s00049-011-0088-0.
Saporito RA, Garrao HM, Donnelly MA, Edwards AL, Longino JT, Daly JW. 2004. Formicine ants: an
arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. P Natl Acad Sci USA.
101(21):8045–8050. doi:10.1073/pnas.0402365101.
Schulte LM, Rödder D, Schulte R, Lötters S. 2010. Preference and competition for breeding
plants in coexisting Ranitomeya species (Dendrobatidae): does height play a role.
Salamandra. 46(3):180–184.
Schulte R. 1990. Redescubrimiento y redenicion de Dendrobates mysterious (Myers, 1982) de la
Cordillera del Condor. Bol. Lima. 12:57–68.
Silverstone PA. 1975. A revision of the poison-arrow frogs of the genus Dendrobates Wagler. Nat Hist
Mus La Count Sci Bull. 21:1–55.
3028 S. DUARTE-MARÍN ET AL.
Silverstone PA. 1976. A revision of the poison-arrow frogs of the genus Phyllobates Bibron in Sagra
(Family Dendrobatidae). Revisión de las ranas venenosas del género Phyllobates Bibron en Sagra
(Familia Dendrobatidae). Nat Hist. 27:1–53.
Summers K. 1989. Sexual selection and intra-femalecompetition in the green poison-dart frog,
Dendrobates auratus. Ani Behav. 37:797–805. doi:10.1016/0003-3472(89)90064-X.
Summers K. 2000. Mating and aggressive behaviour in dendrobatid frogs from Corcovado National
Park, Costa Rica: a comparative study. Behaviour. 137(1):7–24. doi:10.1163/156853900501845.
Summers K. 2003. Convergent evolution of bright coloration and toxicity in frogs. P Nat Acad Sci.
100(22):12533–12534. doi:10.1073/pnas.2335928100.
Summers K, McKeon CS. 2004. The evolutionary ecology of phytotelmata use in Neotropical poison
frogs. Miscellaneous publications. Mus Zool U Mich. 193:55–73.
Summers K, Mckeon CS, Heying H. 2006. The evolution of parental care and egg size: a comparative
analysis in frogs. P Roy Soc B-Bio Sci. 273(1587):687–692.
Summers K, Tumulty J. 2014. Parental care, sexual selection, and mating systems in neotropical
poison frogs. In: Macedo RG, Machado G, editors. Sexual selection: perspectives and models from
the neotropics. Elsevier: Academic Press; p. 289–320.
Tarvin RD, Powell EA, Santos JC, Ron SR, Cannatella DC. 2017. The birth of aposematism: high
phenotypic divergence and low genetic diversity in a young clade of poison frogs. Mol Phyl Evo.
109:283–295. doi:10.1016/j.ympev.2016.12.035.
Tewksbury JJ, Anderson JG, Bakker JD, Billo TJ, Dunwiddie PW, Groom MJ, Hampton SE, Herman SG,
Levey DJ, Machnicki NJ. 2014. Natural history’s place in science and society. BioScience.
64:300–310. doi:10.1093/biosci/biu032.
Toft CA. 1995. Evolution of diet specialization in poison-dart frogs (Dendrobatidae). Herpetologica.
51(2):202–216.
Travis J. 2020. Where is natural history in ecological, evolutionary, and behavioral science? Am Nat.
196(1):1–8. doi:10.1086/708765.
Twomey E, Brown JL. 2008. Spotted poison frogs: rediscovery of a lost species and a new genus (Anura:
Dendrobatidae) from northwestern Peru. Herpetologica. 64(1):121–137. doi:10.1655/07-009.1.
Valderrama-Vernaza M, Ramírez-Pinilla MP, Serrano-Cardozo VH. 2009. Diet of the Andean frog
Ranitomeya virolinensis (Athesphatanura: Dendrobatidae). J Herpetol. 114–123. doi:10.1670/07-
247R1.1.
Vargas-Salinas F, Amézquita A. 2013a. Stream noise, hybridization, and uncoupled evolution of call
traits in two lineages of poison frogs: Oophaga histrionica and Oophaga lehmanni. Plos ONE. 8
(10):e77545. doi:10.1371/journal.pone.0077545.
Vargas-Salinas F, Amézquita A. 2013b. Trac noise correlates with calling time but not spatial
distribution in the threatened poison frog Andinobates bombetes. Behaviour. 150(6):569–584.
doi:10.1163/1568539X-00003068.
Vargas-Salinas F, Amézquita A. 2014. Stream noise, call frequency, and the composition of anuran
species assemblages. Evol Ecol. 28:341–359. doi:10.1007/s10682-013-9675-6.
Vargas-Salinas F, Dorado-Correa A, Amézquita A. 2014. Microclimate and stream noise predict
geographic divergence in the auditory signal of a threatened poison frog. Biotropica.
46:748–755. doi:10.1111/btp.12169.
Velásquez-Álvarez AA, Rada M, Kahn TR. 2016. Dale Swanson´s poison frog Andinobates daleswan-
soni Rueda-Almonacid, Rada, Sánchez-Pacheco, Velásquez-Álvarez, and Queedo-Gil 2006. In:
Kahn TR, La Marca E, Lötters S, Brown JL, Twomey E, Amézquita A, editors. Aposematic poison
frogs (Dendrobatidae) of the Andean Countries: Bolivia, Colombia, Ecuador, Perú and Venezuela.
Arlington (USA): Conservation International Tropical Field Guides Series; p. 263–267.
Vitt LJ. 2013. Walking the natural-history trail. Herpetologica. 69:105–117. doi:10.1655/HERPETOLOGICA-
D-13-00027.
Vitt LJ, Caldwell JP. 2014. Herpetology: an introductory biology of amphibians and reptiles.
California: Academic press.
Wang IJ. 2011. Inversely related aposematic traits: reduced conspicuousness evolves with increased
toxicity in a polymorphic poison-dart frog. Evol: Int J Org Evol. 65(6):1637–1649. doi:10.1111/
j.1558-5646.2011.01257.x.
JOURNAL OF NATURAL HISTORY 3029
Weygoldt P. 1987. Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae).
J Zool Syst Evol Res. 25(1):51–67. doi:10.1111/j.1439-0469.1987.tb00913.x.
Appendix A
List of examined tadpoles (given in lots). Acronyms: AMNH, American Museum of Natural History;
AF, Antoine Fouquet eld series; EPN, Escuela Politécnica Nacional, Departamento de Ciencias
Biológicas, Colección HerpetologíaICN, Instituto de Ciencias Naturales, Universidad Nacional de
Colombia; KU, University of Kansas, Natural History Museum; LACM, Natural History Museum of
Los Angeles County; MCP, Museu de Ciências e Tecnologia, PUCRS; MZUSP, Museo de Zoologia da
Universidade de São Paulo; OMNH, The Sam Noble Oklahoma State Museum of Natural History; PD,
Pedro Dias eld series; TG, Taran Grant eld series; ZSM, Zoologische Staatssammlung München.
Species Source Papillation gap in the lower lip
Andinobates and Ranitomeya
Andinobates altobuyensis AMNH 102101 absent
Andinobates bombetes ICN 42287 present
Andinobates cassidyhornae Universidad de Los Andes (no catalogue number) present
Andinobates daleswansoni This study present
Andinobates fulguritus LACM 71907 absent
Andinobates minutus ICN 46096; KU 116744 absent
Andinobates opisthomelas ICN 34620; LACM 61067 present
Andinobates sp Chocó Universidad de Los Andes (no catalogue number) absent
Andinobates tolimensis Bernal et al. (2007) present
Andinobates virolinensis ICN 28412 present
Ranitomeya amazonica AF 3301; TG 3667 absent
Ranitomeya benedicta Brown et al. 2008 absent
Ranitomeya cyanovittata MCP 13605 absent
Ranitomeya defleri PD 23 absent
Ranitomeya fantastica Brown absent
Ranitomeya imitator KU 215613 absent
Ranitomeya reticulata AMNH 14161 absent
Ranitomeya sirensis MUSM 27565 absent
Ranitomeya summersi Brown et al. 2008 absent
Ranitomeya toraro MCP 13614 absent
Ranitomeya uakarii Brown et al. 2011 absent
Ranitomeya vanzolinii OMNH 36060 absent
Ranitomeya variabilis ZSM 008/2010 absent
Ranitomeya ventrimaculata ICN 53026 absent
Other Dendrobatinae
Adelphobates galactonotus MZUSP 77116 absent
Adelphobates castaneoticus MZUSP 67225 absent
Dendrobates leucomelas AMNH 137308 absent
Dendrobates truncatus ICN 54630 absent
Excidobates captyvus Twomey and Brown (2008) absent
Excidobates condor EPN 14337 absent
Excidobates mysteriosus Schulte (1990) absent
Minyobates steyrmarki AMNH 14972 absent
Oophaga arborea AMNH 117643 absent
Oophaga histrionica LACM 71908 absent
3030 S. DUARTE-MARÍN ET AL.