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Predation on snakes of Argentina: Effects of coloration and ring pattern on

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DOI: 10.1080/01650520600630725

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Studies on Neotropical Fauna and Environment, December 2006; 41(3): 183–188

ORIGINAL ARTICLE

Predation on snakes of Argentina: Effects of coloration and ring pattern

on coral and false coral snakes

CARLOS M. BUASSO1, GERARDO C. LEYNAUD1 & FELIX B. CRUZ2

1
Centro de Zoologı́a Aplicada, Universidad Nacional de Córdoba, Argentina, and 2CONICET – CRUB, Universidad
Nacional del Comahue, San Carlos de Bariloche, Argentina

(Received 5 March 2005; accepted 2 February 2006)

Abstract
The occurrence of coral snake coloration among unrelated venomous and non-venomous snake species has often been
explained in terms of warning coloration and mimicry. In Argentina, no field tests have been conducted to confirm this
mimetic association between one venomous coral species (Micrurus phyrrocryptus, Elapidae) and two non-venomous snake
species with a similar color pattern (Lystrophis pulcher and Oxyrhopus rhombifer, Colubridae). The aims of this work were to
test for the possible aposematic or cryptic function of the ring pattern and coloration of coral snakes and false coral snakes
from central Argentina, and to analyse whether the pattern is effective throughout the year. Predation on snakes was
estimated by using non-toxic plasticine replicas of ringed venomous and non-venomous snakes and unbanded green snakes
placed along transects in their natural habitat during the dry and rainy season. Ringed color pattern was attacked by
predators despite the background color. One of the replica types was attacked more than expected during the dry season,
suggesting that both shape and width of rings may influence the choice by predators. The reaction of predators towards
replicas that mimic snake species with ringed patterns is independent of the geographical region, and we can conclude that
mimicry characteristics are quite general when the true models are present in the area.

Keywords: Aposematic coloration, coral snakes, mimicry, predation, snakes

Introduction association between them (Greene & McDiarmid,

Venomous snakes, especially some species of the
family Elapidae, are common models for mimetic
associations (Pough et al., 1998). The presence of
bright, contrasting color bands in species of these
venomous snakes and in many species of the family
Colubridae (non-venomous or of low toxicity) adjust
to the Batesian model of mimetism (Greene &
McDiarmid, 1981; Campbell & Lamar, 1989). This
model is based on the assumption that, by being
similar to venomous snakes with aposematic color
patterns, non-venomous snakes are also avoided by
possible predators (Yanosky & Chani, 1988;
Campbell & Lamar, 1989; Brodie III & Moore,
1995; Greene, 1997; Pough et al., 1998). Parallel
variation in the coloration of non-venomous and
venomous snakes throughout different geographical
areas provides strong evidence for a mimetic
1981; Brodie & Janzen, 1995; Zug et al., 2001).
Encounters between predator and prey are rarely
observed in nature. Experimental tests to determine
whether colored snakes are avoided by predators and
whether such predators distinguish between the
ringed and ringless patterns have been conducted
using indirect evidence. Smith (1975) studied the
reactions of unexperienced birds on plain, long-
itudinally striped and ringed snake replicas in the lab
and gathered evidence for the innate avoidance of
replicas painted with the coral snake pattern. Field
experiments performed with artificial snake replicas
later demonstrated that free-ranging birds avoid all
ringed patterns found on sympatric snake species in
Costa Rican rain forests (Brodie III & Janzen, 1995).
Plasticine replicas of coral snakes have been used by
Brodie III (1993) to gather data on rates of
predation in nature. The soft plasticine, which

Correspondence: G. C. Leynaud, Centro de Zoologı́a Aplicada, Universidad Nacional de Córdoba, Rondeau 798, CC 122, 5000 Córdoba, Argentina.
Fax: +54 351 4332055. Email: gleynaud@efn.uncor.edu
ISSN 0165-0521 print/ISSN 1744-5140 online # 2006 Taylor & Francis
DOI: 10.1080/01650520600630725
184 C. M. Buasso et al.
retains the imprint of any predation attempt, can be
even used to identify predators. Using this method,
Brodie III (1993) demonstrated for the first time
that the coral snake pattern reduces avian predation
on replicas of both true coral snakes and coral snake
mimics. Thus, he showed a clear relationship
between the aposematic coloration and the conse-
quence of being avoided by predators (Brodie III,
1993; Brodie Jr & Brodie III, 1980). However, if a
replica resembles a model not present in the area it
will not be recognized as a dangerous prey and will
not evoke avoidance (Brodie & Janzen, 1995;
Pfennig et al., 2001). Therefore, only in areas where
predators coexist with an aposematically colored
venomous snake (5model) may the mimics profit by
being avoided by predators.
In Argentina several snake species are similar to
coral snakes of the genus Micrurus in ringed pattern
and coloration. The only species of venomous coral
snake in the province of Córdoba is Micrurus
pyrrhocryptus, with triads of black bands separated
by white or yellowish rings alternating with red
bands of the same width as the central black band
(Cei, 1993). Two non-venomous colubrid snakes of
similar size and coloration, Lystrophis pulcher and
Oxyrhopus rhombifer, occur in Córdoba (Cei, 1993).
No specific field studies have been conducted in
Argentina to analyze the possible benefits of the
mimetic association between these venomous and
non-venomous species, as well as of the aposematic
function of coloration of coral snakes or their
mimics, although this is a key point to understanding
the evolution of this mimicry complex.
Considering the long dry period at our study area
(Bucher, 1982) and the fact that the pressure exerted
on snakes by predators may increase as a conse-
quence of a decrease in plant cover or as a
consequence of a lower prey availability in this
critical period of the year, it is reasonable to think
that predators respond differently to the encounter
with snakes during the dry season. Therefore, we
decided to analyze predation on the different species
over the dry and wet seasons.
The general objective of this work was to
determine if artificial replicas of coral snakes
(Micrurus pyrrhocryptus) and of non-venomous
snakes with a similar color pattern are avoided by
predators in central Argentina. Specifically we aimed
to: (1) test the aposematic or cryptic function of
coloration and ring pattern on the body of Micrurus
pyrrhocryptus, Lystrophis pulcher and Oxyrhopus rhom-
bifer; (2) compare predation frequency on replicas of
the three species mentioned and of a non-mimic
snake (ringless: Philodryas patagoniensis); (3) check
seasonal differences in predation among the species
considered; and (4) analyze the behavior of snake
predators through the marks left on the artificial
replicas.
Materials and methods
Study area
Field work was conducted between October and
November 2001 (dry season) and March and April
2002 (rainy season), in Taninga (31u209S, 65u49W),
department of Pocho, province of Córdoba
(Argentina). The area corresponds to the Chaco
phytogeographic province, characterized by a
strongly seasonal climate (Bucher, 1982). Micrurus
pyrrhocryptus, Lystrophis pulcher, Oxyrhopus rhombifer
and Philodryas patagoniensis inhabit this region, and
are commonly seen in the field, however, no data are
available on their abundance and we therefore
arbitrarily assumed that the four species were equally
abundant.
Data collection and statistical analysis
Replicas of Micrurus pyrrhocryptus, Lystrophis pulcher,
Oxyrhopus rhombifer and Philodryas patagoniensis
(ringless green snake) were formed using pre-colored
(red, black, white and green) non-toxic plasticine
(Figure 1). Replicas were 250 mm long and 10 mm
in diameter, approximately the size of adult speci-
mens. They were threaded on to a wire frame and
anchored to the ground with a fishing line. The
replicas were allowed to air for 48 h before being
placed along transects, so that animals were not
attracted or repelled by the odour of the plasticine.
Thirty-six replicas, nine of each of the four types,
were placed along line transects at 10 m intervals in a
random order. Presence and position of marks of
attacks on the replicas were checked every 15 days.
Replicas were then reshaped or replaced when
necessary, and relocated to a new transect. A total
of 12 transects were used, six in the dry and six in the
wet season.
The replicas with ringed color pattern were placed
on two different backgrounds to check whether
predators responded to the aposematic effect of
coloration by not biting or whether replicas were not
attacked because they were camouflaged on the
natural background due to a cryptic effect of the
color pattern. Therefore, half of the replicas of each
species were placed on white paper sheets to
enhance the contrast and thus visibility of the
colored replicas, whereas the rest were placed
directly on natural ground. The role of aposematic
coloration was analyzed using 262 contingency
tables (x2, p,0.05).
Differences in the number of replicas attacked
per type (independently of the background) were
 Coral snake mimicry in Argentina 185

Figure 1. Color patterns of the four snakes (left) and the respective plasticine replicas (right). (A) Micrurus phyrrocryptus; (B) Lystrophis
pulcher; (C) Oxyrhopus rhombifer; (D) Philodryas patagoniensis.
186 C. M. Buasso et al.

number of replicas attacked and the sequence of

days that they were exposed (Figure 2) shows an
ascending straight line, indicating that the number of
attacks did not decrease throughout the experiment.
Although the replicas were exposed for a relatively
long period of time, predators did not become
accustomed to their presence.

Influence of background color

Figure 2. Accumulated number of attacks after a sequence of 90
sampling days.
analyzed using Friedman test. A multiple compar-
ison test (Dunn’s test, p,0.05) was used when
significant differences among replicas were detected.
The frequency of marks recorded on the ends (at
30 mm or less of each end) or at mid-body of the
models was analyzed using 262 contingency tables
(x2, p,0.05).
Marks can be easily distinguished through their
shape and size: birds leave a V-shaped mark and
mammals leave a tooth mark or a U-shaped mark.
Marks other than those made by typical predators of
snakes (opossums, foxes, skunks, hawks, owls or
large tyrant birds) such as rodents were discarded.
Results
Attacks on replicas by predators
Of a total of 432 replicas placed in 12 transects, 77
(17.8%) showed marks of attacks by predators. Of
all the imprints recorded on the surface of the
replicas, 37 corresponded to birds and 40 to
carnivorous mammals. Among the potential preda-
tors of snakes in the sampling area we observed the
following bird species: Milvago chimango, Polyborus
plancus (Falconidae), Buteo polyosoma (Accipitridae)
and Pitangus sulphuratus (Tyrannidae); and the
following mammals: Didelphis albiventris
(Didelphidae), Dusicyon griseus (Canidae) and
Conepatus castaneus (Mustelidae). The accumulated
There were no significant differences in the number
of attacks to replicas placed on natural ground or on
white paper (Table I), showing that the replicas were
noticed on both backgrounds.
Response of predators to coloration of artificial replicas
The frequency of attacks on replicas was strongly
influenced by the ring pattern and body coloration.
Significant differences were detected in the number
of attacks received by the different types of replica
(Friedman test, x2514.91, p50.002). The number
of marks found on the unbanded replicas (48%) was
significantly greater than on the three replicas with
ringed patterns (M. pyrrhocryptus, 18%; L. pulcher,
14%; O. rhombifer, 20%). The latter did not show
significant differences among them (Dunn’s test,
p,0.05).
The analysis of the data obtained in each season
indicated that the number of attacks recorded
showed significant differences among replica types
(Friedman test, x259.404, p50.024 for the rainy
season and x258.647, p50.034 for the dry season).
The number of attacks on replicas with ringed
patterns in the rainy season did not differ from each
other and was significantly lower than the number of
attacks on the plain replicas (Figure 3). In the dry
season, however, attacks recorded on the replicas of
O. rhombifer and P. patagonienis did not differ
significantly, and were greater than those recorded
on replicas of M. pyrrhocryptus and L. pulcher
(Dunn’s test, p,0.05) (Figure 3).
Position of attacks
The number of marks on the ends of the replicas was
significantly higher (p,0.05) than on the mid-body

Table I. Comparison of the number of attacks to ringed snake replicas placed on different backgrounds (262 contingency table, x2 test,
p,0.05).

No. of replicas attacked

Type of ringed replica White paper Natural background x2 p

Micrurus phyrrocryptus 8 6 0.08 0.77

Lystrophis pulcher 5 6 0.00 1.00
Oxyrhopus rhombifer 6 9 0.31 0.57

Figure 3. Seasonal variation in the number of attacks to replicas
representing four species exposed in 12 successive transects in the
rainy and dry seasons of 2001/2002. Different letters indicate
significant differences (lowercase letters: rainy season; uppercase
letters: dry season) (Dunn’s test, p,0.05).
in three of the four different types of replicas (M.
pyrrhocryptus, L. pulcher, O. rhombifer and P. patago-
nienis) (Table II). Seven replicas with numerous
marks throughout the body were discarded.
Discussion
The occurrence of marks on the replicas indicates
that vertebrate predators were not able to readily
distinguish between the plasticine and true snakes.
Since the frequency of attacks during the sampling
period did not decrease, predators apparently did
not seem to learn that replicas were inedible items.
The accumulation of marks on the ends of the
replicas showed that predators attacked them as they
would do with true, potentially dangerous snakes.
Thus, our experiments did not appear to alter the
behavior of predators.
The difference in the proportion of attacks
between plain replicas and those with color ringed
pattern suggests an advantage of possessing the
ringed ‘‘coral snake’’ pattern to avoid predation.
Thus, our findings agree with a similar study on
coral and false coral snake species from Costa Rica
(Brodie III, 1993). These results also show that the
reaction of predators towards replicas that mimic
Table II. Position of bite marks recorded on snake replicas (262
contingency table, x2 test, p,0.05).
Position of mark
Type of replica Body end Mid-body x2 p
Micrurus phyrrocryptus 12 2 11.57 0.007
Lystrophis pulcher 6 3 0.89 0.340
Oxyrhopus rhombifer 13 2 13.30 0.003
Philodryas patagoniensis 26 6 22.50 0.000
Coral snake mimicry in Argentina 187
snake species with ringed patterns is independent of
the geographical region. Consequently, we can
conclude that mimicry characteristics are quite
general when the true models are present in the
area. Pfennig et al. (2001) first demonstrated that
coral snake mimicking species are not protected
when living in regions where their models are absent.
The fact that background color had no influence
on the number of bite marks indicates that coral
snake replicas were equally visible on both highly
contrasting white paper and natural ground. Thus,
we can reject the hypothesis that the colored
ring pattern does have a cryptic or disruptive
effect making detection of the replicas difficult for
predators.
Predators may detect subtle differences between
the ring patterns of the snake species. This conclu-
sion is suggested by the higher number of attacks to
replicas of O. rhombifer during the dry season. This
species is more yellowish than the other species and
its black rings are rhomboids. Consequently, O.
rhombifer is less similar to the model M. pyrrhocryp-
tus. These results suggest that both shape and width
of the central ring may influence the choice of prey
made by predators and the risk taken. The impor-
tance of ring width in the comparison of the
proportion of attacks between coral snakes and false
coral snakes has also been pointed out in other
studies (Greene & McDiarmid, 1981; Hinman et al.,
1997).
Predation level was generally higher in the rainy
season. However, the proportion of aposematic
replicas attacked in the dry season was higher, but
this was due to the significant increase in attacks to
O. rhombifer replicas, suggesting that predators
would take higher risks when either food availability
is lower or when the need for food is higher, for
example in birds during the breeding season in
spring (Codesido & Bilenca, 2004). We can there-
fore conclude that L. pulcher is a better mimic of M.
pyrrhocryptus than O. rhombifer, at least during the
dry season in Córdoba.
Acknowledgments
We would like to thank M. Chiaraviglio, J. Navarro,
M. Martella and an anonymous reviewer for their
suggestions during the preparation of the manu-
script. Anne Zillikens, E. Buasso and J. Brasca
improved the English version.
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