Feeding behavior and ophiophagous habits of two poorly known Amazonian coral snakes, Micrurus albicinctus Amaral 1926 and Micrurus paraensis Cunha and Nascimento 1973 (Squamata, Elapidae)

Abstract

coral snakes belong to a monophyletic group composed of three genera (Micrurus, Leptomicrurus and Micruroides) and are distributed throughout the Americas. Micrurus is the most diverse genus, with approximately 60 species (Roze, 1996). Traditionally, South American Micrurus are divided into two main groups based on color pattern, specifically the distribution of black rings, either in triads or monads. Besides the color pattern, hemipenes characters support the monophyly of both groups (Slowinski, 1995; Slowinski and Keogh, 2000; Campbell and Lamar, 2004; Feitosa, 2006). Due to its cryptozoic and fossorial habits, natural history data of Micrurus species, such as diet or food behavior, are scarce. Apparently, snakes of the genus Micrurus in general are very specialized predators, with preference for vertebrate preys with elongated bodies (Martins and Oliveira, 1998; Campbell and Lamar, 2004). Moreover, it has been reported that several species consumed by Micrurus occupy a niche similar to the predator itself, which is generally cryptozoic and fossorial. For example, all of the reported prey taxa of M.lemniscatusin the Manaus region (e.g. snakes of the genera Typhlops, Atractus, Hydrops, Liophis, Micrurus and lizards of the genus Bachia) have strong cryptozoic tendencies (Martins and Oliveira, 1998).The literature records on the food items consumed by Micrurus are summarized in two main references, one for species from Manaus, Amazonas (Martins and Oliveira, 1998) and the other for Micrurusfrom the Western hemisphere (Campbell and Lamar, 2004). These records indicate that ophiophagy is common among Micrurus. In contrast to the dietary preferences, little is known about feeding behavior in Micrurus. This lack of information is likely due to their fossorial and secretive habits, which render proper field observations difficult. The few descriptions on Micrurus feeding behavior come from observations of captivity and are restricted to a few species. An exception is Micruruscorallinus Merrem 1820, from the Brazilian Atlantic Forest, for which there are several field and captive observations (Marques and Sazima, 1997; Serapicos and Merusse, 2002). M corallinus shows different handling techniques according to prey type. When feeding on amphisbaenids, the snake bites its prey, injecting the venom, and then releases it, swallowing it only after death. With snake prey items, the prey is held during the entire feeding sequence until its immobilization (Marques and Sazima, 1997). This difference is probably related to difficulties in obtaining cues about head orientation in amphisbaenids. The ventral scale overlap of lizards and other snakes is an important piece of information for Micrurus to determine the head orientation of prey (Greene, 1976; Marques and Sazima, 1997). Thus, the absence of ventral scale overlap in amphisbaenids makes bite-release a better strategy to avoid physical injury from the prey individuals (Marques and Sazima, 1997). In this paper we report on two feeding events observed in the field by two species of coral snakes with little known habits, both species being endemic to the Amazonian forest: M.paraensis and M.albicinctus. M.paraensis is distributed through the tropical forests of southern Surinam and Brazil, in the states of Pará, western Maranhão, southwest Mato Grosso and Rondônia (Feitosa, Prudente and Lima, 2007). M.albicinctus is known only from Brazil, and was registered in the

Full text

The coral snakes belong to a monophyletic group
composed of three genera (Micrurus, Leptomicrurus
and Micruroides) and are distributed throughout the
Americas. Micrurus is the most diverse genus, with
approximately 60 species (Roze, 1996). Traditionally,
South American Micrurus are divided into two main
groups based on color pattern, specifically the distribution
of black rings, either in triads or monads. Besides
the color pattern, hemipenes characters support the
monophyly of both groups (Slowinski, 1995; Slowinski
and Keogh, 2000; Campbell and Lamar, 2004; Feitosa,
2006).
Due to its cryptozoic and fossorial habits, natural
history data of Micrurus species, such as diet or food
behavior, are scarce. Apparently, snakes of the genus
Micrurus in general are very specialized predators, with
preference for vertebrate preys with elongated bodies
(Martins and Oliveira, 1998; Campbell and Lamar,
2004). Moreover, it has been reported that several
species consumed by Micrurus occupy a niche similar
to the predator itself, which is generally cryptozoic and
fossorial. For example, all of the reported prey taxa of
M. lemniscatus in the Manaus region (e.g. snakes of the
genera Typhlops, Atractus, Hydrops, Liophis, Micrurus
and lizards of the genus Bachia) have strong cryptozoic
tendencies (Martins and Oliveira, 1998).The literature
records on the food items consumed by Micrurus are
summarized in two main references, one for species
from Manaus, Amazonas (Martins and Oliveira, 1998)
and the other for Micrurus from the Western hemisphere
(Campbell and Lamar, 2004). These records indicate
that ophiophagy is common among Micrurus.
In contrast to the dietary preferences, little is
known about feeding behavior in Micrurus. This
lack of information is likely due to their fossorial and
secretive habits, which render proper field observations
difficult. The few descriptions on Micrurus feeding
behavior come from observations of captivity and
are restricted to a few species. An exception is
Micrurus corallinus Merrem 1820, from the Brazilian
Atlantic Forest, for which there are several field and
captive observations (Marques and Sazima, 1997;
Serapicos and Merusse, 2002). M corallinus shows
different handling techniques according to prey type.
When feeding on amphisbaenids, the snake bites
its prey, injecting the venom, and then releases it,
swallowing it only after death. With snake prey items,
the prey is held during the entire feeding sequence until
its immobilization (Marques and Sazima, 1997). This
difference is probably related to difficulties in obtaining
cues about head orientation in amphisbaenids. The
ventral scale overlap of lizards and other snakes is
an important piece of information for Micrurus to
determine the head orientation of prey (Greene, 1976;
Marques and Sazima, 1997). Thus, the absence of
ventral scale overlap in amphisbaenids makes bite-
release a better strategy to avoid physical injury from
the prey individuals (Marques and Sazima, 1997).
In this paper we report on two feeding events observed
in the field by two species of coral snakes with little known
habits, both species being endemic to the Amazonian
forest: M. paraensis and M. albicinctus. M. paraensis
is distributed through the tropical forests of southern
Surinam and Brazil, in the states of Pará, western
Maranhão, southwest Mato Grosso and Rondônia
(Feitosa, Prudente and Lima, 2007). M. albicinctus
is known only from Brazil, and was registered in the
Herpetology Notes, volume 4: 369-372 (2011) (published online on 2 November 2011)
Feeding behavior and ophiophagous habits of two poorly known
amazonian coral snakes, Micrurus albicinctus Amaral 1926 and
Micrurus paraensis Cunha and Nascimento 1973
(Squamata, Elapidae).
Sergio Marques Souza1*, André Braga Junqueira2, Ana Catarina Conte Jakovac2, Paulo Apóstolo Assunção2 and
José Adaílton Correia2
1 Coleção de Mamíferos, Instituto Nacional de Pesquisas da
Amazônia (INPA), Av. André Araújo, Petrópolis, Manaus-
AM, CEP 69011-970, Brasil;
e-mail: sergio.bogao@gmail.com
2 Departamento de Botânica, Instituto Nacional de Pesquisas
da Amazônia (INPA), Av. André Araújo, Petrópolis, Manaus-
AM, CEP 69011-970, Brasil.
* Corresponding author.

Sergio Marques Souza et al.
370
states of Rondônia and Amazonas, near the border of
Colombia and Peru (Feitosa, 2006).
The first predation event occurred on March 15th,2010,
when SMS observed an adult M. paraensis (17.5 g
body mass, 429.0 mm snout-vent length (SVL), 88.0
mm tail length (TL)) feeding on an adult specimen of
Atractus albuquerquei (16.5 g body mass, 381.5 mm
SVL, 46 mm TL) at 08:50 am in a patch of secondary
forest surrounded by primary terra firme forest at RDS
do Juma (Juma Sustainable Development Reserve),
municipality of Novo Aripuanã, state of Amazonas,
Brazil (06.30753oS, 60.34924oW, Datum: SAD69, elev.
39 m). When the coral snake individual was found, it
had already swallowed almost the entire body of the A.
albuquerquei (ca. 350 mm) starting from the head. After
ca. 1 minute, the M. paraensis tried to hide with the prey
under the leaf litter. When the animals were handled to
prevent their escape, the predator began to make subtle
thrashes, elevating and coiling the tail and regurgitating
the Atractus, which was already dead. Both individuals
were collected and deposited in the Herpetological
Collection of Museu Paraense Emílio Goeldi under the
numbers MPEG 24313 (A. albuquerquei) and MPEG
24314 (M. paraensis).
Figure 1. a – Micrurus paraensis swallowing Atractus albuquerquei (SMS). b – Micrurus albicinctus swallowing Atractus sp.
(ABJ).

Feeding behavior of Micrurus albicinctus and M. paraensis 371
The other event occurred on May 5th, 2010, at
09:50 am, in a terra firme tropical forest located at
Floresta Nacional do Jamari (Jamari National Forest),
municipality of Itapuã do Oeste, state of Rondônia,
Brazil (09.32247°S, 062.90208°W, Datum: SAD69,
elev. 140m). ABJ, ACCJ, PAA and JAC observed a
Micrurus albicinctus individual foraging in the leaf
litter and entering in a small hole at the base of a tree,
where it disappeared. Five minutes later, we detected the
same individual, leaving the burrow with an individual
of Atractus sp. in its mouth. The prey was probably
already dead, since it was motionless. The predator held
the prey by its anterior portion, approximately 3 cm
below the head. Afterwards the predator turned the prey
to reach its head and then started to chew and swallow
it. The Atractus sp. was swallowed in approximately 40
min. After swallowing it, the predator hid below the leaf
litter. Although we have not collected the two snakes,
their lengths were similar, with prey slightly smaller
than predator. Identification of species was made using
photographs of the event.
These are the first records of food items and feeding
behavior of M. paraensis and M. albicinctus. Both
species are ophiophagous and predate upon snakes with
cryptozoic habits, which seems to be a behavior shared
by most species of the genus Micrurus (Marques and
Sazima, 1997; Martins and Oliveira, 1998; Campbell
and Lamar, 2004). In both cases, the ratio of prey
total length (TTL) to predator SVL is high, reaching
0.99 in the case of M. paraensis (although we did not
measure it for M. albicinctus, it was clear that prey and
predator were similar in size). Although the individual
of M. paraensis did not finish swallowing the prey,
this probably was due to the stress caused by observers
manipulating the snake and not to prey size, since most
of the prey body had already been swallowed. As far as
we know, this is the greatest prey TTL / predator SVL
ratio registered for Micrurus (Marques and Sazima,
1997; Cisneros-Heredia, 2005).
M. albicinctus proved to be a predator that actively
hunts its prey in the leaf litter, instead of using the
sit-and-wait strategy. One relevant observation is that
M. albicinctus, as well as recorded for M. corallinus
(in captivity - Marques and Sazima, 1997), captures
and injects venom into its prey underground, but only
swallows the prey after dragging it to the surface. It is
difficult to test the veracity of this statement, because
the field records available in the literature (including
this one) are obviously biased to surface ingestions
rather than subterraneous ingestions. However, one
possible explanation is that, on the surface, the snake
is able to better handle the prey and maximize the
head-first ingestion. The head-first ingestion has
potential advantages for the predator, such a decrease
in the probability of injuries caused by prey defense
mechanisms (i.e. bites) and decrease of swallowing
time of prey (Greene, 1976).
Acknowledgements. The authors wish to thanks Fabio Röhe,
Francis Correia, Mario Cohn-Haft and Marconi Cerqueira for
field help. Miguel Trefaut Rodrigues, Ana Lúcia Prudente and
Alexandru Strugariu critically reviewed the manuscript and
helped in the species identification. Paulo Passos confirmed the
identification of M albicinctus prey. SMS’ research with Amazon
reptiles is supported by a scholarship from Conselho Nacional
de Desenvolvimento Científico e Tecnológico (CNPq). Vouchers
specimens were collected under the license No 14555-5 provided
from Instituto Chico Mendes de Conservação da Biodiversidade
(ICMBio - Brazil).
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Accepted by Alexandru Strugariu