Download Predation of six anuran species by the banded cat

Herpetology Notes, volume 7: 123-126 (2014) (published online on 11 April 2014)
Predation of six anuran species by the banded cat-eyed snake,
Leptodeira annulata (Serpentes: Dipsadidae), in the Caatinga
scrub of northeastern Bahia, Brazil
Carlos R. Santos-Silva1*, Igor S. Andrade 2, Maria L. N. Araújo 2, Lívia Claudia S. Barros2, Lidiane Gomes 2
and Stephen F. Ferrari3
Introduction
Material and methods
Snakes are the main predators of anurans in habitats
surrounding bodies of water (Sazima and Haddad,
1992; Wells, 2007; Bernarde and Abe, 2010). Some
snake species prey almost exclusively on amphibians,
which contribute up to 90% of their diets (Mushinsky et
al., 1982). However, detailed observations of predation
events are rare due to the difficulties of monitoring
these animals in the wild (Malkmus, 2000; Lima and
Colombo, 2008).
The banded cat-eyed snake, Leptodeira annulata, is
widely distributed in Neotropical wetlands between
Mexico and Argentina (Carvalho et al., 2005). The
snakes of this genus are typically batracophagous,
feeding on adult amphibians in shrubs or trees near
the water’s edge, or on their egg clutches or tadpoles
(Duellman, 1978; Martins and Oliveira, 1998; Jungfer
and Weygoldt, 1999; Bernarde and Abe 2010; Sales et
al., 2013). These snakes are opistoglyphic and have a
relatively simple form of venom, in comparison with
other snakes (Mebs, 1968; Nascimento et al., 2013).
The present study describes the behavior of L. annulata
during the predation of six anuran species in the Raso
da Catarina Ecological Station in the semi-arid zone of
northeastern Bahia, Brazil.
The events described here were recorded between
March 2010, and February 2011. The study site
was a temporary pond within the palm-dominated,
shrubby-arboreal Caatinga scrub in Jeremoabo, Bahia
(9.916944°S, 38.698611°W, datum SAD-69; elev. 444
m a.s.l.). Nocturnal observations were conducted at the
site between 18:00 h and 01:00 h. Snake length was
estimated based on photographs taken of each event
(see Costa-Pereira et al., 2010), with the snake being
compared with nearby objects (leaves, rocks, branches
and so on), which were measured in the field. Behavioral
data were collected ad libitum through continuous
observation (Del-Claro, 2004), focusing on the aspects
of the event considered to be most relevant in terms of
the predatory behavior. Photographs were taken of each
event, and have been deposited in the herpetological
collection of the Federal University of Sergipe (UFS)
in São Cristóvão, Sergipe, Brazil. The anuran species
were identified based on direct observation in the field
and comparisons with specimens deposited in the
herpetological collections at UFS and the Bahia State
University at Feira de Santana (UEFS).
Graduate Program in Ecology and Conservation, Universidade
Federal de Sergipe, 49100-000 São Cristóvão – SE, Brazil;
2
Department of Education, Universidade do Estado da Bahia,
Campus VIII, Paulo Afonso – BA, Brazil;
3
Department of Ecology, Universidade Federal de Sergipe, São
Cristóvão – SE, Brazil.
* Corresponding author: e-mail: [email protected]
1
Results
Six predation events involving Leptodeira annulata
were recorded, each involving a distinct anuran species.
The predation of Hypsiboas crepitans (Figure 1-a) was
observed on October 22nd, 2010, between 19:25 h and
19:52 h. This event involved the largest L. annulata
specimen (total length, TL = 850 mm) recorded in the
present study. The strike was not observed. The prey
was already dead and the ingestion process had begun
when the animals were sighted.
The predation on Phyllomedusa bahiana (Figure 1-b)
occurred on December 17th, 2010, between 22:22 h and
124
Carlos R. Santos-Silva et al.
Figure 1. Anurans captured by Leptodeira annulata in the Raso da Catarina Ecological Station, Bahia, Brazil, between March,
2010, and February, 2011: (a) Hypsiboas crepitans; (b) Phyllomedusa bahiana; (c) Rhinella granulosa; (d) Leptodactylus
troglodytes; (e) Scinax x-signatus; (f) Physalaemus kroyeri (Photos: Santos-Silva, C.R.).
00:15 h. This was the longest event recorded here. An
adult male P. bahiana was initially observed calling,
perched on dry branches at the water’s edge. A large L.
annulata (TL = 765 mm) attacked the frog, striking at
the mid region of the body, close to the hindlimbs. The
frog emitted distress calls and moved its forelimbs in an
effort to free itself by pulling on dry twigs while grasping
the neck of the snake with its left foot. The bitten area
of the frog’s body and the snake’s head became covered
with the peptide secretion produced by the glands of
P. bahiana. After approximately 29 minutes, the frog
succumbed to the attack and the snake pulled it into a
shrub (Capparis yco) and began swallowing it.
The predation of Rhinella granulosa (Figure 1-c) was
observed on January 21st, 2011, between 19:16 h and
20:51 h. A medium-sized L. annulata (approximate
TL= 650 mm) was observed head-down in a vertical
position in the dry branches of a shrub (Croton sp.)
Predation of six anuran species by the banded cat-eyed snake, Leptodeira annulata
around 15 cm above the ground, when it attacked and
held on to a calling male R. granulosa by the middle of
its body. The toad emitted distress calls intensely and
moved its limbs during the first 5 min in an attempt to
free itself from the snake. Another 16 minutes passed
before the toad became completely motionless and was
presumably dead. It was then swallowed head-first. The
duration of the event, from the strike until the complete
ingestion of the prey, lasted 1 h and 35 min.
The predation on Leptodactylus troglodytes (Figure
1-d) occurred on February 23rd, 2011, between 19:48
h and 20:23 h. An adult female L. troglodytes was
observed at the water’s edge, close to a calling male
when it was captured by a large Leptodeira annulata
(TL = 740 mm) that was foraging actively in the dry
vegetation. The anuran was captured by a rapid strike to
the middle of its body, slightly closer to the forelimbs.
During the first six minutes, the anuran moved its limbs
vigorously in an attempt to escape the attack. The snake
then began to ingest the anuran by the head, together
with the left front limb, swallowing the animal as far
as the scapular girdle, when it stopped for five minutes,
until the prey had become completely motionless. The
snake swallowed the rest of the frog using rhythmic
movements of its mandible. During this process, the
snake’s fangs ruptured the inguinal tissue of the frog’s
body, causing its mature eggs to spill out.
The predation of Scinax x-signatus (Figure 1-e) was
observed on February 25th, 2011, between 22:16 h
and 22:32 h. A medium-sized L. annulata (TL = 600
mm) was observed foraging on the branches of a small
bush (Croton sp.) with its head pointing downwards
approximately 80 cm above the ground. It then seized
by the head a calling male S. x-signatus perched
approximately 10 cm away. Following the attack, the
frog inflated its body and moved its limbs rapidly in an
attempt to free itself during the next three minutes. The
snake held the prey by the head for another two minutes
until its movements had ceased completely, and then
it began to ingest the frog. The whole event lasted 16
minutes.
The predation on Physalaemus kroyeri (Figure 1-f)
occurred onFebruary 25th, 2011, between 22:23 h and
22:29 h. This event involved the smallest L. annulata (TL
= 480 mm) recorded here. The strike was not observed,
although the frog was still alive when the animals were
first encountered. The snake had the hindlimbs of the
frog in its mouth as far as the median portion of the
animal’s body, which was inflated. The frog was drawn
into the digestive tract of the snake while still moving its
125
eyes and forelimbs, through movements of the mandible
and then accommodated with lateral undulations and
peristaltic movements.
Discussion
The predation events recorded in this study were
consistent with those observed in other ecosystems, in
particular the relative vulnerability of anurans during
the reproductive season (Duellman and Trueb, 1986;
Pough et al., 1998; Haddad et al., 2008). In fact, all
but one event were recorded between December and
February, coinciding with the rainy season (Sick et al.
1987). Furthermore, only one of the events involved an
adult female (L. troglodytes), which is consistent with
the preference of predators for calling males (Pough et
al. 1992; Toledo, 2003).
This is the second study to report the predation
of adult Phyllomedusa tree frogs by L. annulata.
Nascimento et al. (2013) recorded the predation of
three phyllomedusine species (Phyllomedusa vaillanti,
Phyllomedusa tomopterna, and Phyllomedusa
tetraploidea) in Brazil, Peru, and Ecuador. These
records reinforce the conclusion that the toxins secreted
by these anurans are insufficient to protect them from
predation by L. annulata, although the exact mechanism
through which the snake counteracts this chemical
defense is unknown.
While L. annulata is known to prey on a wide range
of anuran species (Nascimento et al., 2013), only R.
granulosa had been previously recorded in its diet
(Vitt, 1996; Ávila and Morais, 2007). This reinforces
the importance of our results, given that the impact of
predation by this snake on anuran communities is poorly
known, as for other predators (Toledo, 2005).
Acknowledgements. We thank CEMAVE (Kleber Oliveira and
Antônio E. Barbosa) and Otávio Nolasco for providing logistics,
CAPES for a graduate stipend to CRS-S, CNPq for supporting
SFF, and IBAMA/RAN for the collecting permit (#22094-2).
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Accepted by Diogo Provete;
Managing Editor: Diogo Provete