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Mesoamerican Herpetology March 2016 | Volume 3 | Number 1
Other Contributions Nature Notes
Thanatosis in four poorly known toads of the genus Incilius
(Amphibia: Anura) from the highlands of Costa Rica
Anurans are known to use myriad defensive strategies to avoid and deter predators, including cryptic and aposematic
coloration, immobility, fleeing, inflating the body, toxic skin compounds, fighting, and thanatosis (Toledo et al.,
2011). The behavior in which potential prey feign death to avoid predation is called thanatosis (Edmunds, 1974).
Feigning death might confuse a predator, and when combined with urination, defecation, or skin secretions makes
the prey species appear unpalatable to the predator or makes ingestion difficult (Rogers and Simpson, 2014).
Thanatosis occurs in diverse groups of animals, both invertebrates and vertebrates (Edmunds, 1974; Mângia and
Santana, 2013). In anurans, this behavior has been reported in 99 species in at least 16 families (Toledo et al., 2011;
Escobar-Lasso and González-Duran, 2012). Whereas thanatosis is known to occur in a large number of anuran
families, the number of species exhibiting this behavior is approximately 1.5% of the 6,554 known anuran species
(Frost, 2015), a small percentage likely due to the lack of natural history information available for most species.
Several semi-fossorial and diurnal species of toads inhabit highland areas of Costa Rica, where they live
in leaf-litter on the forest floor (Novak and Robinson, 1975; Boza and Solano, 2009). These species are poorly
known, and include Incilius chompipe, I. epioticus, I. guanacaste, and I. holdridgei. The first three of these species
formerly resided in the genus Crepidophryne (see Vaughan and Mendelson, 2007), but in a phylogenetic study
based on morphology, life history, and molecular data Mendelson et al. (2011) found Crepidophryne nested within
Incilius and placed the former genus in the synonymy of the latter. These toads are difficult to detect in nature and
some have been affected by population declines (Mendelson and Mulcahy, 2010; Abarca, 2012), so much of their
biology remains understudied. An important aspect of these toads is their locomotion, which primarily is accom-
plished through slow walking (Savage, 2002); thus, one might think they have few options against predatory attacks
and must use other methods for defense. Herein we describe a defensive behavior (thanatosis) in four Costa Rican
bufonid species.
The Study Species
From 2012 to 2014 we conducted a series of observations at four sites in the mountains of central and northwest-
ern Costa Rica: Cerro Chompipe, Provincia de Heredia (10.086388°N, 84.071111°W; elev. 2,070 m); Cascajal
de Coronado, Provincia de San José (10.029722°N, 83.93888°W; elev. 1,740 m); Río Macho de Orosi, Provincia
de Cartago (9.760555°N, 83.870555°W; elev. 2,000 m); and Parque Nacional Rincón de la Vieja, Provincia de
Guanacaste (10.808055°N, 85.3325°W; elev.
1,880 m). The life zones in these areas con-
sist of Premontane Rainforest and Lower
Montane Rainforest (Savage, 2002). We used
visual encounter surveys in appropriate hab-
itats to locate the toads. When finding indi-
viduals, we recorded their initial behavior
and within one minute gently touched them
with tweezers. We then captured the toads
by hand and turned them upside down on the
substrate, and recorded the time it took for
them to assume an upright position. When in-
dividuals remained in a “belly up” position,
we touched, tugged, and finally pressed their
extremities gently with tweezers.
We encountered three juveniles and
six adults of I. chompipe at Cerro Chompipe
and Coronado (Fig. 1); six juveniles and four
adults of I. epioticus at Río Macho (Fig. 2);
Fig 1. An adult Incilius chompipe from Cerro Chompipe, Parque
Nacional Braulio Carrillo, Provincia de Heredia, Costa Rica.
'© Juan G. Abarca
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Mesoamerican Herpetology March 2016 | Volume 3 | Number 1
Other Contributions Nature Notes
one juvenile and one adult of I. guanacaste
at Rincón de la Vieja (Fig. 3); and 14 ju-
veniles, two subadults, and two adults of I.
holdridgei at Cerro Chompipe. We present
accounts of the trials for each of the species
below.
Incilius chompipe
When first observed within leaf-litter all
individuals remained motionless, but when
found on top of the leaf-litter they attempted
to escape by walking. When placed upside
down, all individuals remained belly up
from 20 to 160 sec (Fig. 4). The behavior
of juveniles and adults was similar, except
that when in the belly up position juve-
niles pulled their limbs close to their body
whereas adults maintained their limbs ex-
tended. When we touched their limbs all in-
dividuals remained immobile, but when we
tugged or pressed on the limbs they showed
no resistance and regained an upright posi-
tion. While in the belly up position the eyes
of the toads remained open. Additionally,
some individuals puffed up the body (Fig. 4)
and one showed a cloacal discharge.
Incilius epioticus
All individuals remained immobile when
discovered within the leaf-litter, but fled
when we found them on top. If touched,
they tried to escape by walking slowly.
After we turned them upside down, all
individuals remained belly up with their
limbs extended from a few to maximum of
120 sec. While in the belly up position the
toads remained immobile when we touched
the limbs, but they showed no resistance
and regained an upright position when we
tugged or pressed on the limbs. The eyes of all individuals remained open while in the belly up position, and all
adults puffed up their body.
Incilius guanacaste
Both adults and juveniles remained immobile when encountered within leaf-litter, but fled when found on top.
When touched, adults always tried to escape with short jumps, and when turned belly up they turned upright im-
mediately. The single juvenile remained immobile when touched, and stayed in the belly up position when turned
upside down, from five to 264 sec, with its limbs close or extended away from the body. Upon touching the limbs it
remained immobile, but when we tugged or pressed on the limbs it regained an upright position. Its eyes remained
open while exhibiting the death feigning behavior (Fig. 5).
Fig 2. An adult and two juveniles of Incilius epioticus from Río
Macho de Orosi, Provincia de Cartago, Costa Rica.
'© Juan G. Abarca
Fig 3. A juvenile Incilius guanacaste from Parque Nacional Rincón
de la Vieja, Provincia de Guanacaste, Costa Rica.
'© Juan G. Abarca
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Mesoamerican Herpetology March 2016 | Volume 3 | Number 1
Nature NotesOther Contributions
Incilius holdridgei
Some juveniles and subadults remained im-
mobile when found, but others attempted to
escape; when we touched them, however,
they all fled. When placed upside down
they remained belly up from 20 to 120 sec,
and in that position juveniles maintained
their limbs extended or close to the body
(Figs. 6, 7), but those of subadults were in
a stretched position. When we touched or
tugged on the limbs of juveniles and sub-
adults they maintained their death feigning
posture, but they regained an upright posi-
tion when we pressed the limbs. The eyes
of all individuals remained open while dis-
playing the death feigning behavior.
Of the two adults we encountered,
the first one fled by walking away, but
when we placed it upside down it turned
upright immediately. The second adult was
not as active and remained immobile when
placed upside down. This individual held
that position from 30 to 136 sec, with its
legs extended (Fig. 8). Like the juveniles,
it remained immobile when we touched or
tugged on the limbs, but when the limbs
were pressed it returned to an upright
position.
Discussion
Amphibian predators find prey by using
the following multi-step process: locating
the prey, identification, approach, subjuga-
tion, ingestion, and digestion (Toledo et al.,
2011). Potential prey items have developed
different defensive strategies to counter the
early stages of predation, especially loca-
tion and subjugation (Toledo et al., 2011).
Escobar-Lasso and González-Duran (2012)
suggested that thanatosis is a strategy used
to avoid subjugation. Thanatosis is not con-
sidered a spontaneous behavior, as it only
occurs after several attempts to escape or
manipulations are made by a possible predator (Beux dos Santos et al., 2010; Toledo et al., 2010). In our study
animals, the behavior occurred only when individuals were manipulated.
In thanatosis, the limbs can be moved without showing resistance and individuals maintained their eyes open
(Toledo et al., 2010; Rogers and Simpson, 2014). During thanatosis, the limbs also might change position (Toledo
et al., 2010). The same characteristics were evident in our observations, and thus we consider the described be-
havior as thanatosis. The toads remained motionless when we touched any part of their body, but ended thanatosis
Fig 4. An adult Incilius chompipe in thanatosis behavior at Cerro
Chompipe, Parque Nacional Braulio Carrillo, Provincia de Heredia,
Costa Rica. '© Juan G. Abarca
Fig 5. A juvenile Incilius guanacaste in thanatosis behavior at Parque
Nacional Rincón de la Vieja, Provincia de Guanacaste, Costa Rica.
'© Juan G. Abarca
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Mesoamerican Herpetology March 2016 | Volume 3 | Number 1
Nature Notes
behavior when we pressed or stretched their
limbs. Toledo et al. (2010) noted that an-
urans remain motionless while displaying
thanatosis, even when touched. A camou-
flaged prey item near a predator could be
touched but remain undetected, so in this
case maintaining thanatosis is a good strat-
egy. Thanatosis may be inefficient if the
prey item feels bites, because this means
that the predator would know the location
of the prey and that it is still alive.
The species of Incilius in this study
might have developed thanatosis as a de-
fensive strategy against certain predators.
In the tepuis of the Guyanan Highlands
in South America, toads the genus
Oreophrynella have developed strategies to
defend themselves against specific preda-
tors (McDiarmid and Gorzula, 1989). Birds
and snakes are known to prey on toads of
the genus Incilius (Sandoval et al., 2015;
Nascimento et al., 2013), but specific pred-
ators have not been documented for the four
species in this study. Novak and Robinson
(1975) reported that individuals of I. hol-
dridgei have been found mutilated, missing
a part or all of a limb, and suggested the
presence of undiscovered predators and
noted that the role of birds was unknown.
In this regard, Acosta and Morún (2014) re-
ported on a bird (Catharus frantzii) taking
a frog (Craugastor podiciferus) by the legs
and repeatedly hitting it against the forest
floor, to a point where the frog fell on its
back; the bird then flew off with its prey to
ingest it. Accordingly, if a toad were to fall
on its back during a similar predatory at-
tack and maintained thanatosis behavior, it
might go unnoticed. Thanatosis, therefore,
could be an effective mechanism against
predators that need movement to find their
prey, such as diurnal birds (Toledo et al.,
2011). The presence of mutilated limbs
(Novak and Robinson, 1975) suggests that the toads in this study might be able to survive predatory attacks by birds
by using this mechanism.
We observed thanatosis behavior in the juveniles of all the species in this study, but in some cases adults did
not show it (i.e., I. guanacaste and I. holdridgei); perhaps young individuals were less able to make a quick escape,
and thus relied more on camouflage (Toledo et al., 2011; Mângia and Santana, 2013; Rogers and Simpson, 2014).
Here, we suggest that young individuals tend to show more thanatosis behavior because their short legs cover less
ground than those of adults while walking to escape. Additionally, because of their small size camouflage might be
more efficient during the thanatosis. Differences on the effectiveness of escaping and camouflage between the age
Other Contributions
Fig 6. A juvenile Incilius holdridgei with its limbs close to body while
exhibiting thanatosis behavior at Cerro Chompipe, Parque Nacional
Braulio Carrillo, Provincia de Heredia, Costa Rica.
'© Juan G. Abarca
Fig 7. A juvenile Incilius holdridgei with its limbs extended while
exhibiting thanatosis behavior at Cerro Chompipe, Parque Nacional
Braulio Carrillo, Provincia de Heredia, Costa Rica.
'© Juan G. Abarca
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Mesoamerican Herpetology March 2016 | Volume 3 | Number 1
Other Contributions Nature Notes
classes in these species only can be corrob-
orated by further studies.
Thanatosis behavior can improve the
effectiveness of cryptic colors for camou-
flage (Rogers and Simpson, 2014). Non-
toxic species usually display cryptic colors
(Blount et al., 2009), and thanatosis occurs
mostly in non-toxic frogs (Escobar-Lasso
and González-Duran, 2012), suggesting
that there is a negative correlation between
thanatosis and toxicity. Nonetheless, in the
family Bufonidae it also occurs in species
with some level of toxicity, such as in gen-
era Dendrophryniscus, Melanophryniscus,
Osornophryne, Rhinella, and Incilius
(Toledo and Haddad, 2009; Toledo et al.,
2010). We cannot assign our study species
to a toxicity category, because information
on their toxicity is unavailable and we did
not observe any discharge from their paro-
toid glands. Thanatosis, however, can serve
more as a defensive strategy against preda-
tors by affecting their vision for hunting, such as in birds and snakes (Toledo et al., 2011). More observations are
necessary to identify potential predators of the species in this study; nevertheless, this report of thanatosis increases
the available natural history information of highland bufonids in Costa Rica.
Acknowledgments.––We thank Warren Calvo Siles, Roberto Cordero, and Josimar Estrella for facilitating
access to some localities, Marco Ramírez, José Antonio Cambronero, Michael Méndez, Rolando Ramírez, Ana
Hernández, and Olivier Geib for valuable field assistance, Otto Monge and Mason Ryan for kindly reviewing the
manuscript, and César Barrio-Amorós, Twan Leenders, and Louis Porras for comments that improved the final ver-
sion of this note. A research permit was provided by the Ministerio de Ambiente y Energía (MINAE) (ResoluciónN°
015-2014-ACCVC-PI, and SINAC-SE-GASP-PI-R-059-2015).
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Katherine SánChez Paniagua1 and Juan g. abarCa2
1Escuela de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales. Universidad Nacional. Heredia, Apdo. 86-
3000, Heredia, Costa Rica. E-mail: kpsa89@gmail.com
2Sistema de Estudios de Posgrado, Facultad de Microbiología, Universidad de Costa Rica, San Pedro Montes de Oca,
Apdo. 20–60 San José, Costa Rica. E-mail: barcazajuan@gmail.com (Corresponding author)
Reptilia: Crocodylia
Crocodylus acutus (Cuvier, 1807). Predation on a Brown Pelican (Pelecanus occidentalis) in the ocean. The
American Crocodile (Crocodylus acutus) has a wide distribution that extends from the southern tip of Florida,
United States, and the Caribbean islands of Cuba, Hispaniola, and Jamaica to the Yucatan Peninsula in Mexico, then
southward to Colombia and Venezuela, and on the Pacific from northern Sinaloa, Mexico, to northern Peru (Ponce-
Campos et al, 2012). In Costa Rica, C. acutus is known to occur on both versants in large rivers and streams, often in
brackish water near the mouths of rivers, as well as in salt and freshwater marshes, mangrove swamps, and swamp
forests, at elevations below 200 m (Savage, 2002). Although typically associated with brackish estuaries and large
rivers and streams, C. acutus occasionally ventures into marine environments (Savage 2002), indicating some toler-
ance of saltwater (Wheatley et al., 2012; Platt et al., 2013). Data on the habits and diet of C. acutus inhabiting ma-
rine or coastal areas, however, remain poorly studied, compared with those of more inland areas (Platt et al., 2013).
On 6 January 2016 at ca. 1000 h, we observed a C. acutus preying on a Brown Pelican (Pelecanus occi-
dentalis) along the shoreline of Playa Naranjo, Sector Santa Rosa, Area de Conservación Guanacaste, Provincia
de Guanacaste, Costa Rica. The event occurred directly across the shore from Laguna El Limbo, an area of beach
surrounded by mangroves (10°46'14.11"N, 85°39'42.68"W, WGS 84) in Tropical Dry Forest. At the time of the
