South American Journal of Herpetology, 15, 2020, 1–12

© 2020 Brazilian Society of Herpetology

Reproductive Ecology of the Peruvian Earless

Toad Rhinella yunga (Amphibia, Bufonidae) with
Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski¹,²,*, Florencia A. Trama³, Federico L. Rizo Patrón³, Elicio Tapia⁴, Kim L. Hoke²

¹ Instituto Clodomiro Picado, Universidad de Costa Rica, Coronado, Costa Rica.

² Department of Biology, Colorado State University, Fort Collins, Colorado, 80523, USA.
³ Centro de Capacitación en Conservación y Desarrollo Sostenible, Oxapampa, Peru.
⁴ Centro Jambatu de Investigación y Conservación de Anfibios, Fundación Otonga, Quito, Ecuador.
* Corresponding author. Email: stynoski@gmail.com

Abstract. Rhinella yunga is a poorly studied but locally abundant endemic bufonid toad found only in two habitat islands of the buffer
zones surrounding the Yanachaga-Chemillén National Park and the Pui Pui Protected Forest in the Selva Central, Peru. Rhinella yunga is
unique because it lacks a complete tympanic ear and is larger than most toads lacking a tympanic ear. Here, we report on the natural history,
reproductive behavior, and territorial and release calls of R. yunga following field- and captivity-based observations across two breeding
seasons. We also provide a description of tadpole external morphology based on a developmental series of laboratory-reared larvae. We
found that R. yunga (1) uses low frequency calls (800–1,100 Hz) that are likely detectable without tympanic middle ears and (2) appears to
exhibit an unusual mating system with female competition at breeding ponds prior to male arrival. Under these conditions, the need to hear
male advertisement calls might have become unnecessary in this species.

Keywords. Earlessness; Female-female aggression; Mating system; Rhinella margaritifera group; Yanachaga-Chemillén National Park.

Resumen. Rhinella yunga es una especie de sapo de la familia Bufonidae endémica y poco estudiada, pero localmente abundante, encontrada
en sólo dos islas de hábitat dentro de las zonas de amortiguamiento que rodean el Parque Nacional Yanachaga-Chemillén y el Bosque
Protegido Pui Pui en la Selva Central, Perú. Rhinella yunga es única porque carece de un oído tímpano completo y es más grande que otros
sapos conocidos sin oídos tímpanos. Aquí, reportamos la historia natural, el comportamiento reproductivo y las llamadas territoriales y de
liberación de R. yunga según observaciones de campo y cautiverio a lo largo de dos temporadas de apareamiento. También proporcionamos
una descripción de la morfología externa del renacuajo basada en una serie de desarrollo de larvas criadas en laboratorio. Encontramos que
R. yunga (1) usa cantos de baja frecuencia (800–1,100 Hz) que son probablemente detectables sin oídos medios timpánicos y (2) parece
exhibir un inusual sistema de apareamiento con la competencia de hembras ante la llegada de machos. En estas condiciones, la necesidad de
escuchar llamadas posiblemente se ha vuelto innecesaria en esta especie.

INTRODUCTION
Rhinella yunga Moravec et al., 2014 is a medium-sized
toad from the R. margaritifera group found only in buffer
zones surrounding the Yanachaga-Chemillén National
Park and the Pui Pui Protected Forest in the Selva Central,
Peru (Moravec et  al., 2014). Very little information has
been reported about this endemic species since it was first
described in 2014 (Moravec et al., 2014; Tortorelli et al.,
2016). In the species description it was noted that the call
and tadpole are not known (Moravec et al., 2014).
Rhinella yunga is exceptional because unlike most
toads in the R.  margaritifera group (19 species; Vaz-Sil-
va et al., 2015), it lacks a complete tympanic ear (Fig. 1;
Moravec et  al., 2014; dos Santos et  al., 2015; Pereyra
et al., 2016). Many other bufonids also exhibit complete
or partial loss of the tympanic ear, including several Rhi-
nella outside the R.  margaritifera group (Pereyra et  al.,
2016). However, Rhinella species lacking some or all of
the tympanic ear are typically smaller than R. yunga (see
Table 1). Rhinella yunga inhabits mid-elevation cloud for-
ests (1,800–2,230 m above sea level [a.s.l.]) and adjacent
secondary and recovering pasture habitats, and it is ter-
restrial (in leaf litter and low vegetation) except when
mating in still, shallow water bodies (pers. obs.; Moravec
et al., 2014). In this study, we report on its natural history
and calls and discuss its “earless” status in the context of
its breeding behavior.
As a second goal, we describe the tadpole of Rhi-
nella yunga. Tadpole descriptions are available for many
species in the genus Rhinella, including some species in
the R. margaritifera group (R. castaneotica Caldwell, 1991,
R.  hoogmoedi Caramaschi and Pombal, 2006, R.  magnus-
soni Lima et  al., 2007, R.  margaritifera Laurenti, 1768,

How to cite this article: . South American Journal of Herpetology 15: 1–12. http://doi.org/10.2994/SAJH-D-18-00030.1

Submitted: 17 April 2018 Handling Editor: Taran Grant

Accepted: 10 October 2018 http://doi.org/10.2994/SAJH-D-18-00030.1
Available Online: Published 
South American Journal of Herpetology, 15, 2020, 1–12

imately 1,400 mm of rain annually, with average tempera-

tures of 17–20°C across the year. December–February are
the warmest and wettest months, and June–August are
slightly cooler and much drier months. We took note of
the natural history, breeding behavior, and calls of indi-
viduals in their natural habitat. We collected four female
and five male adults (deposited at the Museo de Biodiver-
sidad del Perú; MUBI, Cusco, Peru; Appendix S1), measur-
ing snout–vent length (SVL) prior to preserving samples
in paraformaldehyde and storing them in 70% ethanol.
We also measured SVL of some individuals that were im-
mediately returned to the wild.
Calls were recorded with a Sony ICD‑UX533F IC re-
corder with ambient temperatures on rainy nights in the
range of 10–15°C as measured with a digital thermome-
Figure  1. Image of Rhinella yunga adult female, which lacks a visible ter. Release calls were recorded from a distance of < 0.5 m
tympanum (photo: E. Tapia). while toads were in captive conditions and territorial calls
were recorded from a distance of approximately 2 m in the
Table 1. Maximum snout–vent length (SVL) of adult Rhinella toads that field (see Toledo et al., 2015). We determined call param-
lack the entire tympanic ear (E) or at least the tympanum (T; see Pereyra eters (number of pulses, call duration, as well as median,
et al., 2016).
minimum, and maximum dominant frequency) and gen-
Maximum erated spectrograms and oscillograms with the seewave
Species reported Reference package (Sueur et  al., 2008) in R (3.1.3; R Core Team,
SVL (mm) 2015; see raw recordings in Audio S1 and S2 and analysis
Rhinella yunga (T) 75.0 Current study in Script S1).
Rhinella fissipes (T) 71.9 Padial et al., 2006 To obtain the focal clutch of tadpoles, we placed a
Rhinella quechua (T) 62.0 Gallardo, 1961 free-living amplectant pair in an aquarium containing 3 cm
Rhinella tenrec (E) 60.8 Grant and Bolivar, 2014 of water at the Centro de Capacitación en Conservación
Rhinella cristinae (E) 55.1 Vélez-Rodríguez and y Desarrollo Sostenible, Oxapampa, Peru (10°54′59.1″S,
Ruiz‑Carranza, 2002
75°37′13.2″W, datum WGS 84; 2,200 m a.s.l.). We chose
Rhinella justinianoi (T) 53.6 Harvey and Smith, 1994
to rear a single clutch to a range of tadpole stages rather
Rhinella paraguas (T) 51.4 Grant and Bolivar, 2014
than collect different stages from the wild in order to en-
Rhinella macrorhina (E) 50.2 Urbina et al., 2009
sure species identity. We measured egg (ovum) diameter
Rhinella castaneotica (T) 42.6 Ávila et al., 2010 from photos using ImageJ v.1.47t (Schneider et al., 2012).
Rhinella veraguensis (T) 41.0 Padial et al., 2009 After allowing eggs to hatch, we reared tadpoles to a range
Rhinella festae (E) 40.5 Duellman and Lynch, 1988 of stages, feeding ad libitum with a combination of spir-
Rhinella amboroensis (T) 38.5 Harvey and Smith, 1993 ulina and trout food pellets. We fixed tadpoles with 4%
Rhinella arborescandens (E) 38 Duellman and Schulte, 1992 paraformaldehyde and stored them in 70% ethanol. Some
tadpoles were deposited in the MUBI (Appendix S1) and
R. proboscidea Spix, 1824, R. scitula Caramaschi and Nie- others were sectioned for histological analysis in another
meyer, 2003; reviewed in Blotto et al., 2014). These de- study (Stynoski et al., in preparation). Using dial calipers
scriptions offer a rich source of data for the study of trait accurate to 0.1  mm under a stereomicroscope, we mea-
evolution and heterochrony (Haas, 2003; Aguayo et  al., sured morphometrics of tadpoles in an ontogenetic range
2009; Fabrezi and Goldberg, 2009; Blotto et al., 2014). according to Gosner (1960; see Table  2) following the
guidelines of Castillo-Trenn (2004), Rada et  al. (2007),
and Terán-Valdez et al. (2009). We measured total length,
MATERIALS AND METHODS body length, body maximum height, body maximum
width, maximum tail height, tail muscle height, tail mus-
Observations were made between December 2014 cle width, tail length, vent tube length, vent tube width,
and February 2016 in three major sampling areas along spiracle aperture, spiracle–snout length, oral disc width,
the buffer zone surrounding the Yanachaga-Chemillén eye maximum diameter, eye–snout distance, interocular
National Park in central Peru that correspond to three distance, eye–nostril distance, nostril–snout distance,
major watersheds in the area (Llamaquizú, San Daniel, and internarial distance. The description of general and
and San Alberto; same sites as in Chávez et  al., 2012; external oral morphology is based on a Stage 35 speci-
Moravec et al., 2014). This region of Peru receives approx- men.

2 Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke
South American Journal of Herpetology, 15, 2020, 1–12

Table 2. Measurements (in mm) of Rhinella yunga morphology across Gosner (1960) tadpole Stages 25–45 and one week after metamorphosis, following
the morphometrics protocol in Terán-Valdez et al. (2009).

25 26 35 37 39 40 44 45 1 week
Total length 14.0 14.2 16.7 17.5 19.0 20.3 19.0 9.6 8.4
Body length 5.9 5.8 7.9 8.6 8.1 8.5 7.8 7.3 8.4
Body height 3.0 3.0 4.0 3.8 3.8 3.6 3.7 3.2 3.4
Body width 4.0 4.1 5.2 5.5 5.4 5.8 4.7 3.2 3.5
Maximum tail height 3.0 3.3 3.8 4.0 4.1 4.0 3.6 1.0 N/A
Tail muscle height 1.9 2.1 2.1 2.1 2.5 2.5 2.1 0.7 N/A
Tail muscle width 1.0 0.6 1.0 1.2 1.4 1.0 0.9 0.8 N/A
Tail length 8.5 8.8 8.9 9.8 11.4 11.2 10.0 2.6 N/A
Vent tube length 1.1 0.8 1.6 1.4 1.8 1.2 N/A N/A N/A
Vent tube width 0.6 0.4 0.6 0.7 0.6 0.7 N/A N/A N/A
Spiracle aperture N/A 0.7 0.8 0.8 0.6 0.7 N/A N/A N/A
Spiracle–snout length N/A 4.4 5.7 6.1 6.2 6.1 N/A N/A N/A
Oral disc width 2.2 2.2 02.5 2.6 2.7 2.8 2.5 2.4 2.3
Eye diameter 0.9 0.8 1.1 1.3 0.9 1.2 1.1 1.0 1.0
Eye–snout distance 1.2 1.4 2.1 2.0 2.2 2.2 1.9 1.3 1.5
Interorbital distance 2.0 1.9 2.2 2.6 2.4 2.4 2.6 1.8 2.5
Eye–nostril distance 0.9 0.6 1.1 1.2 0.8 0.9 0.9 1.0 0.9
Nostril–snout 0.7 0.5 0.9 0.9 0.7 0.5 0.6 0.5 0.8
Internarial distance 1.0 0.9 1.1 1.6 1.4 1.1 1.2 1.2 1.4

RESULTS in the afternoons prior to evenings in which breeding ac-

Natural history
Rhinella yunga were mostly observed being active at
night, with much less activity observed during the day
and at dusk. Other bufonid toads present in the area in-
clude R. leptoscelis Boulenger, 1912, Atelopus cf. reticulatus
Lötters et  al., 2002, and Atelopus oxapampae Lehr et  al.,
2008, which are all less common locally than R.  yunga
(pers. obs.; Chávez et al., 2012, Angulo et al., 2016). Frogs
other than bufonids include Hyalinobatrachium carlesvilai
Castroviejo-Fisher et  al., 2009, Scinax oreites Duellman
and Wiens, 1993, Ameerega planipaleae Morales and
Velazco, 1998, and a number of species in the family Stra-
bomantidae Hedges et al., 2008 (Chávez et al., 2012). At
higher elevations in this region, a smaller arboreal toad,
R. yanachaga Lehr et al., 2007, can be found, but overlap-
ping population ranges between R. yunga and R. yanacha-
ga have not been reported or observed (pers.  obs.; Lehr
et al., 2007; Chávez et al., 2012).
The species exhibits exceptional sexual dimorphism,
typical of the Rhinella margaritifera group (Moravec et al.,
2014; dos Santos et al., 2015; Fig. 2A–B). Females (n = 5,
SVL  ± SE: 66.7 ± 2.5 mm, range 60–75) are significantly
larger than males (n = 7, SVL 48.7 ± 1.6 mm, range 44–
55). Mature females, but not males, are characterized
by pronounced supraorbital crests, rectangular in shape
from a dorsal view (Fig.  2A). Males and females vary in
coloration from brown to grey to red in typical “dead leaf
pattern”. Males, but not females, turn to a golden yellow
tivity occurs (Fig. 2B).
Individuals were located during the day by walking
slowly and searching in leaf litter, rotting logs, and root
clumps at the bases of trees in primary and secondary
forest and adjacent deep pasture or by clearing and sift-
ing through the leaf litter. Habitats included recently cut
forest on very steep inclines (60%) near mountain ridges,
large boulders covered with vegetation in remnant pri-
mary forest patches, and abandoned eucalyptus in dense
understory secondary forest. Several juveniles and adult
females were found at least 300  m uphill from pools of
water. On wet nights in the breeding season, adult ani-
mals were present along the sides of roads and trails on
the ground, in breeding sites, and on low vegetation up
to approximately 30 cm in height. On two occasions after
significant handling, individuals released defensive secre-
tions from parotoid glands, which were thick and creamy
in consistency and bright yellow (Fig. 2C).
Reproductive behavior including
release and territorial calls
Observations of breeding behavior occurred on 10
or more nights during two consecutive breeding seasons.
Breeding behavior is generally observed at the onset and
peak of the wet season (December–February) but was oc-
casionally observed in other times of the year (April, Oc-
tober) when new puddles were formed by strong rains or
human activities. We observed similar behaviors multiple

Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke 3
South American Journal of Herpetology, 15, 2020, 1–12

times at each of three distinct watersheds in the region
(Llamaquizú, San Daniel, and San Alberto).
At approximately 18:30–19:30 on nights with light
to moderate rainfall and occasionally on dry nights, adult
females could be found in puddles with 2–15  cm depth
of water and a radius of 0.5–3 m. Less commonly, we ob-
served breeding in shallow, permanent artificial and natu-
ral ponds (20–150 cm depth; Tortorelli et al., 2016) or in
shallow and slow flowing creeks or riffles at the edges of
larger streams (5–20  cm depth). Females were typically
perched in a conspicuous position such that driving slow-
ly in a car made it easy to locate them in puddles in the
road. They were hesitant to change position and allowed
researchers to approach quite closely before attempting
to escape, making it easy to capture them. If left undis-
turbed in a puddle where multiple females were present,
they would jump antagonistically at each other. In three
cases we also observed females wrestling for 2–5 h, which
always resulted in holds that differed from amplexus in
the placement of the front limbs being more inguinal than
axillar (Fig. 3A).
At approximately 20:00–23:00, male toads with
golden yellow coloration would appear from the forest
edge to the puddles. They did not make vocalizations and
were not aggressive with other males or females. Males
entered the water in the puddle and within minutes am-
plexed with one of the females (Fig.  2B). Amplexus and
egg deposition generally took place in the deepest parts of
puddles. We observed most frequently two and occasion-
ally up to six amplexed pairs in a given puddle, with the
number of pairs generally relative to the size of the pud-
dle. Size ratios (male:female) of three naturally amplexed
pairs were 0.72, 0.79, and 0.92. When held together in
captivity (0.5  m long plastic boxes), males occasionally
exhibited aggressive behavior, wrestling by pushing down
on each other’s heads or holding each other (Fig. 3B) with

Figure 2. Features of Rhinella yunga natural history: (A) male-female dimorphism and dorsal view of female supraorbital crest (photo: J.L. Stynoski);
(B) mating with dynamic color change to golden yellow in the male and axillary amplexus (photo: J.L. Stynoski); and (C) adult male exuding secretions
from parotoid glands (photo: F.P. Condori Ccarhuarupay).

4 Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke
South American Journal of Herpetology, 15, 2020, 1–12
Figure 3. Images showing aggressive behavior in Rhinella yunga: (A) female-female aggression in a puddle (photo: J.L. Stynoski); (B) male-male aggres-
sion in a plastic enclosure (photo: F.P. Condori Ccarhuarupay).
the male on the bottom often producing release calls. The
release call (n = 10 calls recorded among three males on
different nights; Fig. 4A; Audio S1) consists of a series of
10 ± 1.2 (range 6–13) short pulses lasting 2–2.5 s with a
dominant frequency of 863 Hz (range 689–947).
In addition to the release call, we also recorded a call
from males in three distinct sites on different nights near
the edge of secondary forest between 19:00 and 22:00
(Fig. 4B). It is important to note that this call can arguably
best be defined as a territorial call rather than an advertise-
ment call because the site of the call did not contain any
standing water for breeding and no other males or females
were noted nearby (see Toledo et  al., 2015). None of the
other typical reproductive behaviors described above were
seen to coincide with this call. The authors and site staff
have also heard this call on occasion in varied locations
around the breeding facility at different times of the year,
during and following sunset, with calls generally spaced at
least 30 min apart on a given night, not always on succes-
sive nights, and without an apparent link to the weather
that seems to be specifically associated with breeding be-
havior. Territorial calls (n = 3; Fig. 4B; Audio S2) consisted
of a series of 58, 60, or 62 notes lasting 10.5–11 s with a me-
dian dominant frequency of 1,032 Hz (range 861–1292).
Successful mating produced clear, flat, and loosely
spiraling strings of 500–1,500 pigmented eggs in single
rows, typical of toads in the Rhinella margaritifera group
(“uniserial”; Pereyra et  al., 2015; Fig.  5A). Females typi-
cally deposited eggs between 0:00–3:00  h regardless of
whether amplectant pairs were left in puddles for oviposi-
tion or moved to aquaria with 2–5 cm of water. Collected
eggs typically took 3–7 d to hatch. In the natural habitat,
Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke
adults did not attend eggs and no other form of parental
care was observed. Egg yolks (n  =  20 randomly selected
from three clutches) had a diameter of 1.99  ±  0.04  mm
(range 1.68–2.24). Based on observations in the laborato-
ry and in natural pools, the larval period is highly variable,
approximately 60–120 d. Mean SVL of individuals (n = 24)
at metamorphosis is 8.9 ± 0.5 mm (range 7.8–10.1).
Tadpole external morphology
Rhinella yunga tadpoles are benthic, lentic, exotro-
phic, and omnivorous pond-type larvae, as is typical for
the genus (Aguayo et al., 2009; Kolenc et al., 2013). They
are uniformly dark brown to black in coloration through-
out the tail and body musculature with some degree of
transparency in the tail fin at its margins, both in vivo and
following fixation and one year of storage (Fig.  5B–C).
Intestinal coils are slightly visible in vivo, but not follow-
ing fixation. Vent tube and spiracle are also pigmented
and visible up to Stage 41. There is no evidence of an ab-
dominal sucker, distinct from tadpoles of the sympatric
species R. leptoscelis (pers. obs.). Digit tips develop light
coloration between Stages 42 and 44 (Fig. 5D–E). Variable
dorsal spots and coloration appear at metamorphosis, in-
cluding occasionally a white dorsoventral stripe.
Rhinella yunga at tadpole Stage 35 (Fig. 6) is relatively
small (16.7 mm total length) both in body length (7.9 mm)
and tail length (8.9  mm). It has a body that is slightly
wider (5.2 mm) than tall (4.0 mm; see Table 2). The body
length is about half of the total length (tail length:total
length = 0.53) with a slightly flattened appearance (body
5
South American Journal of Herpetology, 15, 2020, 1–12

height:body width =  0.77). The tail height is similar to
the body height (tail height:body height =  0.95), with a
slight downward slant at the rounded tip and myomeres
evident but not at the tail tip. The dorsal fin originates
at the body-tail junction, curving slightly ventrally along
its length. The ventral fin, of similar height as the dorsal
fin, is conjoined with the vent tube at its origin, curving
gently down and then back up along its length. The body
is oval and smooth, with the snout appearing rounded to
truncate in dorsal view and rounded in lateral view. Nos-
trils are also oval, dorsolateral, and closer to the snout
than the eyes. Eyes are lateral and medium-sized. Lateral
line system and pineal end organ are barely evident. The
spiracle is single, short, and visible but not obvious dor-

Figure 4. Spectrograms and oscillograms of Rhinella yunga: (A) release call and (B) territorial call.

6 Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke
South American Journal of Herpetology, 15, 2020, 1–12

Figure 5. Photos of young Rhinella yunga (photos: J.L. Stynoski; Scale bars = 1 mm): (A) egg clutch resulting from captured amplectant pair; (B) dorsal
view of Stage 35 tadpole; (C) ventral view of Stage 35 tadpole; (D) dorsal view of juvenile one week post-metamorphosis; and (E) ventral view of juvenile
one week post-metamorphosis.

Figure 6. Illustration of Rhinella yunga tadpole at Stage 35 (Gosner, 1960; Illustrator: Selena Aguiniga): (A) dorsal view, (B) ventral view, (C) lateral view,
and (D) oral disc.

Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke 7
South American Journal of Herpetology, 15, 2020, 1–12

sally, mostly attached to the body, vent small and circular,
located sinistral and lateral along a dorsoventral axis in
the posterior portion of the body.
The oral disc of the tadpole is small to medium (oral
disc width:body width =  0.45), terminal, and cannot be
seen dorsally (Fig. 5B). Jaw sheaths are thin, pigmented,
and serrated distally, with the lower sheath V‑shaped and
the upper sheath curved. As is typical of tadpoles in the
R. margaritifera group (and other bufonid tadpoles, with
some exceptions), they exhibit a labial tooth row formula
of 2(2)/3 with labial tooth rows of similar length, submar-
ginal papillae absent, and wide ventral and dorsal gaps
in the marginal papillae (Haas, 2003; Menin et al., 2006;
Aguayo et al., 2009; Kolenc et al., 2013; Blotto et al., 2014).
DISCUSSION
In this study, we report on the reproductive ecology
of a bufonid toad that lacks a tympanic ear and is larger
and more terrestrial than many related species that also
lack tympanic ears. We found behavioral evidence in the
field that the mating system of this species does not rely
on calls to initiate mating behavior. In numerous sites on
different nights across two breeding seasons, we observed
females arriving to breeding sites and engaging in aggres-
sive interactions prior to the arrival of males and amplex-
us. These characteristics add to growing evidence that the
natural history and reproductive ecology of so-called ear-
less species is diverse, calling into question previous hy-
potheses that convergent earlessness is the product of a
shared selective force (Hetherington, 1992; Pereyra et al.,
2016). Furthermore, we recorded release and territorial
calls in a low frequency range (800–1,100  Hz). Territo-
rial calls in Rhinella yunga have a lower frequency, longer
duration, and more notes per call than all other species
in the R. margaritifera clade, although the temporal fea-
tures seem most similar to R. magnussoni (see Fig. 7 and
Table S1). Frogs are capable of using alternative hearing
pathways to sense substrate-borne and airborne vibra-

Figure 7. Parameters of calls by species of toads in the Rhinella margaritifera group: (A) dominant frequency (Hz) of call according to average male snout–
vent length (SVL) and (B) number of notes per call according to call duration (s). Call data (see Table S1) were reported in Ryan and Tuttle (1983; R. alata
Thominot, 1884), Köhler and Lötters (1999; R. castaneotica), Ávila et al. (2018; R. gildae Vaz-Silva et al., 2015), Joventino Roberto et al. (2011; R. hoogmoe-
di), Fouquet et al. (2007; R. lescurei Fouquet et al., 2007 and R. martyi Fouquet et al., 2007), Lima et al. (2007; R. magnussoni), Köhler et al. (1997; R. mar-
garitifera), Caldwell and Shepard (2007; R. ocellata Günther, 1858), Ávila et al. (2010; R. paraguayensis Ávila et al., 2010), Zimmerman and Bogart (1988;
R. proboscidea), and the current study (R. yunga). Call data were not available for R. scitula, R. acutirostris Spix, 1824, R. dapsilis Myers and Carvalho, 1945,
R. roqueana Melin, 1941, R. sclerocephala Mijarres-Urrutia and Arends‑R., 2001, R. stanlaii Lötters and Köhler, 2000, or R. sebbeni Vaz-Silva et al., 2015.

8 Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke
South American Journal of Herpetology, 15, 2020, 1–12
tions below ~1,100  Hz (reviewed in Jaslow et  al., 1988;
Lindquist et al., 1998), and R. yunga is sensitive in the fre-
quency range of these calls (Womack et al., 2017). Given
the mating system of this species, the ability for females
to hear male advertisement calls might have become un-
necessary. It is worth noting that R. yunga is the only spe-
cies in the R.  margaritifera group that lacks a complete
tympanic ear (Moravec et  al., 2014), although over 200
of the more than 580 species of bufonid toads lack a tym-
panic middle ear (Pereyra et al., 2016). Whether the evo-
lution of the observed natural history traits preceded or
followed the evolutionary loss of the tympanic ear in this
species is not known.
Female-female aggression in a territorial or mating
context is an exception to the rule, but has been noted
in a number of other groups of anurans including numer-
ous poison frogs in the family Dendrobatidae Cope, 1865
(Summers, 1989; Haase and Prohl, 2002; Brown et  al.,
2008), Eleutherodactylus coqui Thomas, 1966 (Stewart and
Rand, 1991), and a bufonid, Atelopus varius Lichtenstein
and Martens, 1856 (Crump, 1988). Female competition
or calling is also known in species that exhibit extensive
male parental care such as Alytes muletensis Sanchíz and
Adrover, 1979 (Bush and Bell, 1997) and Limnonectes
palavanensis Boulenger, 1894 (Dicroglossidae Ander-
son, 1971; Goyes Vallejos, 2016). Among bufonid toads,
female choice based on male size or call parameters (as
in Sclerophrys capensis Tschudi, 1838; Cherry, 1993) and
scramble competition (reviewed in Pereyra et  al., 2016)
are better known mating systems. Density-dependent
shifts between calling and active-searching as male strat-
egies for locating mates have been observed in other bu-
fonid toads such as Bufo bufo Linneaus, 1758 (Höglund
and Robertson, 1988), Epidalea calamita Laurenti, 1768
(Arak, 1988), Incilius valliceps Wiegmann, 1833 (Wagner
and Sullivan, 1992), Anaxyrus americanus Holbrook, 1836
(Sullivan, 1992), A. canorus Camp, 1916 (Kagarise Sher-
man, 1980), A.  fowleri Hinckley, 1882 (Sullivan, 1986),
and A. cognatus Say in James, 1822 (Krupa, 1989). Obser-
vations of female-female aggression, especially in the con-
text of pre-mating competitions, are of particular interest
when considering the outstanding sexual dimorphism of
the Rhinella margaritifera group in which females possess
impressive supraorbital crests and males are much less
ornamented (dos Santos et al., 2015). It is puzzling why
R. yunga, which to our knowledge lacks explosive breed-
ing, male parental care, unusually limited resources, or
other unusual traits of reproductive value, would employ
a mating strategy involving female competition prior to
amplexus with males. Limited breeding spaces or female-
biased sex ratio could play a role (Crump, 1988; Haase and
Prohl, 2002). However, we stress that the observations re-
ported here are descriptive, and we strongly encourage ex-
perimental studies to determine what role female-female
competition plays in sexual selection in R. yunga.
Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke
Previous work on this species noted that males col-
lected from puddles were “in breeding condition” but did
not mention their color change (n  =  3; Moravec et  al.,
2014). In all cases in which we observed males in or ap-
proaching puddles on nights with active breeding, they
had changed color to a bright golden yellow, and in cases
in which males were seen in or around puddles at other
times, they remained the “dead leaf” pattern and color.
In a separate study, we also observed that males turned
yellow following injections of leuprolide acetate, a lutein-
izing hormone releasing hormone agonist that stimulates
breeding behaviors in many anurans (Stynoski et al., un-
publ. data.). Males in four other species of bufonids are
known to dynamically change to a yellow color prior to
breeding events, in some cases returning to normal color-
ation very soon after egg fertilization (Doucet and Men-
nill, 2010; reviewed in Bell and Zamudio, 2012). It is pos-
sible that a chemical- or weather-based cue plays a role
in signaling females to enter puddles to compete and also
to signal female receptivity to males who dramatically
change color before entering puddles to seek amplexus.
The tadpole description provided here should allow
identification of Rhinella yunga tadpoles as distinct from
sympatric bufonid species, because R. leptoscelis and At-
elopus tadpoles are stream-dwelling and gastromyzopho-
rous rather than pond-type (Stynoski et al., unpubl. data).
More intensive examination of tadpole buccopharyngeal
and musculoskeletal morphology is likely necessary to
identify species-specific characteristics to distinguish the
tadpole from others in this genus and group which exhibit
limited larval morphological diversity (Blotto et al., 2014;
Haad et al., 2014).
ACKNOWLEDGMENTS
We thank M. Womack, C. Tortorelli, D. Gannon, F.P.
Condori Ccarhuarupay, J.C. Chaparro, A. Delgado, and F.
Arroyo for assistance with field work and tadpole rearing.
We also thank S. Aguiniga for scientific illustrations. This
study was conducted with approval of IACUC at Colo-
rado State University (protocol 15–5715A) and USA and
Peruvian authorities (research permit 195–2015–SER-
FOR–DGGSPFFS, export permit 003004–SERFOR). This
research was funded by the National Science Foundation
(IOS‑1350346) and a postdoctoral fellowship to JLS from
the American Association of University Women.
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ONLINE SUPPORTING INFORMATION

The following Supporting Information is available for this article online:

Appendix S1. Specimens examined.

Audio S1. Rhinella yunga release call in a .wav file.

Audio S2. Rhinella yunga territorial call in a .wav file.

Script S1. R code used to generate call spectrograms and oscillograms as well as graphs comparing call parameters among
toads in the margaritifera group.

Table S1. Data from listed references regarding parameters of calls produced by toads in the Rhinella margaritifera group.

12 Reproductive Ecology of the Peruvian Earless Toad Rhinella yunga (Amphibia, Bufonidae) with Descriptions of Calls, Tadpole, and Female Competition
Jennifer L. Stynoski, Florencia A. Trama, Federico L. Rizo Patrón, Elicio Tapia, Kim L. Hoke