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 811

ARTICLE
A tale of lost tails: pseudoautotomy in the Neotropical snake
genus Drymoluber (Serpentes: Colubridae)
H.C. Costa, M.R. Moura, and R.N. Feio

Abstract: Pseudoautotomy (no spontaneous tail breakage without regeneration) occurs in the snakes Drymoluber brazili (Gomes,
1918) and Drymoluber dichrous (Peters, 1863) throughout their geographic range. Examination of 197 specimens of D. dichrous and
60 D. brazili show, respectively, a frequency of tail breakage (FTB) in 26% and 40% of specimens, similar or higher than observed
Can. J. Zool. Downloaded from www.nrcresearchpress.com by CSP Staff on 09/03/14

for most species with pseudoautotomy. There is no sexual difference in FTB for D. brazili, and no relationship between tail
breakage and snout–vent length (SVL). For D. dicrous, tail breakage is more frequently observed in males when specimens
are <710 mm SVL, but for longer specimens, the FTB is higher in females; this strange pattern may not be explained by a single
hypothesis. The FTB does not vary significantly between disjunct populations of D. dichrous, suggesting that they are subject to
similar predation pressures and escape rates, or minor or no effect of habitat structure on predation risk. The FTB increases with
SVL in D. dichrous (but not in D. brazili, probably due to sample size), which is an indication that as the snake grows, the chance
of being injured increases and partial tail loss becomes an efficient defense. The multiple tail break hypothesis is not supported
for the genus Drymoluber Amaral, 1930, remaining restricted to taxa with specialized pseudoautotomy.

Key words: defensive behavior, Drymoluber, Woodland Racer, natural history, predation, pseudautotomy, tail breakage, urotomy.

Résumé : La pseudoautotomie (séparation non spontanée de la queue sans régénération) se produit chez les couleuvres
Drymoluber brazili (Gomes, 1918) et Drymoluber dichrous (Peters, 1863) dans toute leur aire de répartition géographique. L’examen de
For personal use only.

197 spécimens de D. dichrous et de 60 spécimens de D. brazili montre, respectivement, une fréquence de séparation de la queue
(FSQ) chez 26 % et 40 % des spécimens, soit des taux semblables ou supérieurs à ceux observés chez la plupart des espèces ayant
recours à la pseudoautotomie. Il n’y a pas de différence de la FSQ selon le sexe pour D. brazili, ni aucun lien entre la séparation
de la queue et la longueur museau–cloaque (LMC). Pour D. dicrous, la séparation de la queue est observée plus fréquemment chez
les mâles quand la LMC des spécimens est <710 mm, mais pour les spécimens plus longs, la FSQ est plus élevée chez les femelles;
une seule hypothèse pourrait ne pas suffire pour expliquer cette étrange distribution. La FSQ ne varie pas de manière significa-
tive entre différentes populations isolées de D. dichrous, ce qui donne à penser que ces populations sont caractérisées par des
pressions de prédation et des taux de fuite semblables, ou par des effets mineurs ou non existants de la structure de l’habitat sur
le risque de prédation. La FSQ augmente parallèlement à la LMC chez D. dichrous (mais non chez D. brazili, probablement en raison
de la taille de l’échantillon), ce qui indique que, à mesure que les couleuvres grandissent, la probabilité de blessure augmente et
la séparation partielle de la queue devient un moyen de défense efficace. L’hypothèse des séparations multiples de la queue n’est
pas appuyée pour le genre Drymoluber Amaral, 1930, cette hypothèse demeurant limitée aux taxons caractérisés par une
pseudoautotomie spécialisée. [Traduit par la Rédaction]

Mots-clés : comportement de défense, Drymoluber, histoire naturelle, prédation, pseudoautotomie, séparation de la queue.

Introduction
Reptiles employ several antipredator strategies from crypsis to
aposematic coloration, from death feigning to bite (Greene 1988).
One defensive behavior called urotomy is restricted to Lepidosauria,
and allows a specimen to lose its tail to an aggressor and escape
(Arnold 1984). Tail loss occurs at points of weakness and can be
intravertebral or intervertebral (Arnold 1984; Bateman and
Fleming 2009). Presence of intravertebral tail breakage seems to
be a plesiomorphic state in squamates, but has been indepen-
dently lost in members of many of its groups (Arnold 1984). How-
ever, in some agamids and snakes, urotomy was regained through
intervertebral breakage (Arnold 1984; Savage and Slowinski 1996;
Bateman and Fleming 2009). Most lizard species presenting tail
breakage are able to regenerate the tail through the development
of a cartilaginous rod replacing vertebrae, while snakes, amphis-
baenians, and some other lizards lack this ability (Arnold 1984;
Vitt and Caldwell 2009). To unify the terminology, Slowinski
and Savage (1995) and Savage and Slowinski (1996) proposed
“urotomy” for all types of tail breakage, while “autotomy” would
describe only autonomous intravertebral breakage with tail re-
generation (genus Sphenodon (Gray, 1831) and most lizards), and
“pseudoautotomy” (or pseudautotomy) occurs when there is an
intervertebral breakage with no spontaneous separation and no
regeneration (snakes and some lizards). The intervertebral break-
age with regeneration observed in some agamids (Arnold 1984) is
considered an “intermediate condition”, while the intravertebral
breakage without regeneration present in some Amphisbaenia
(Arnold 1984) is not cited by Savage and Slowinski (1996).
Current phylogenies suggest pseudoautotomy evolved indepen-
dently in agamids and snakes (Gauthier et al. 2012; Pyron et al.

Received 29 April 2014. Accepted 9 August 2014.

H.C. Costa and R.N. Feio. Universidade Federal de Viçosa, Departamento de Biologia Animal, Museu de Zoologia João Moojen. Vila Gianetti 32, Viçosa,
Minas Gerais, Brazil.
M.R. Moura. Universidade Federal de Minas Gerais, Departamento de Zoologia, Laboratório de Herpetologia. Avenida Antônio Carlos 6627, Pampulha,
Belo Horizonte, Minas Gerais, Brazil.
Corresponding author: H.C. Costa (e-mail: ccostah@gmail.com).

Can. J. Zool. 92: 811–816 (2014) dx.doi.org/10.1139/cjz-2014-0115 Published at www.nrcresearchpress.com/cjz on 9 August 2014.
 812
2013). Several independent evolutions of this trait have occurred
within snakes (mainly in taxa with relatively long tails), since
pseudoautotomy is recorded for some species of the families
Elapidae, Lamprophiidae (subfamilies Lamprophiinae, Psammophii-
nae, Pseudoxyrhophiine), and Colubridae (subfamilies Colubrinae,
Dipsadinae, Grayinae, Natricinae, Sybinophiinae) (e.g., Kaufman
and Gibbons 1975; Zug et al. 1979; Arnold 1984; Broadley 1987;
Mendelson 1992; Aubret et al. 2005; Sheehy 2006; Dourado et al.
2013). Some records of pseudoautotomy in snakes come from oc-
casional field observations of individuals that urotomized after
being grabbed by the tail (e.g., Sharma 1980; Cooper and Alfieri
1993; Ananjeva and Orlov 1994; Marco 2002; Hampton 2007;
Lockhart and Amiel 2011; Roberto 2011) (but for a case where the
snake fractured its own tail after twisting it tightly around the
body see Hoogmoed and Avila-Pires 2011). Another source of re-
cords comes from natural history or taxonomical studies where
Can. J. Zool. Downloaded from www.nrcresearchpress.com by CSP Staff on 09/03/14
broken tails are noted in some specimens, suggesting pseudo-
autotomy (e.g., Savage and Crother 1989; Prudente et al. 2007;
Leite et al. 2009; Cadle 2010, 2012; Gomes and Marques 2012;
Siqueira et al. 2013). Finally, there are studies analyzing pseudo-
autotomy statistically, testing one or more hypotheses (e.g., Mendelson
1992; Slowinski and Savage 1995; Fitch 2003; Pleguezuelos et al. 2010;
Todd and Wassersug 2010; Santos et al. 2011).
Recently, while reviewing the taxonomy of the Neotropical
colubrine snake genus Drymoluber Amaral, 1930 (Costa et al. 2013),
we observed a high frequency of broken tails in two species, sug-
gesting the occurrence of pseudoautotomy. Drymoluber comprises
three species: the Common Woodland Racer (Drymoluber dichrous
For personal use only.
(Peters, 1863)), with a disjunct distribution in northern South
America and the Atlantic Forest of Brazil (including its transi-
tional areas with the Caatinga and Cerrado ecoregions); Brazil’s
Woodland Racer (Drymoluber brazili (Gomes, 1918)) from the Cer-
rado, Caatinga, and Atlantic Forest of the lower Doce River (south-
eastern Brazil), and Atlantic Forest – Cerrado transitional areas;
and the Apurímac Woodland Racer (Drymoluber apurimacensis Lehr,
Carrillo and Hocking, 2004), restricted to the Apurímac Valley,
south of the Apurímac and Pampas rivers, in Peru (Costa et al.
2013). Drymoluber apurimacensis is known from only six specimens,
none presenting tail breakage (possibly a bias of sample size),
while breakage was common in D. dichrous and D. brazili. To in-
crease the knowledge on the natural history of Drymoluber and of
tail breakage on Neotropical snakes, specimens of D. dichrous and
D. brazili were examined to evaluate (i) the frequency of tail break-
age (FTB); (ii) the geographic variation in FTB in D. dichrous; (iii) sex-
ual difference in FTB; (iv) difference in FTB according to body size;
and (v) evidence for multiple tail breakage (Savage and Crother
1989; Mendelson 1992).
Materials and methods
A total of 291 specimens of D. dichrous and 84 of D. brazili (see
Appendices I and II in Costa et al. 2013) were examined. Only adult
specimens with intact or healed tails were considered to avoid
those in which tail breakage could have occurred after collection.
Young specimens (those presenting a banded dorsal pattern)
were not analyzed because only 2 out of 78 D. dichrous and none
out of 20 D. brazili presented healed tails. Therefore, we included
197 specimens of D. dichrous and 60 specimens of D. brazili (Appendix A).
The following data from each specimen were considered for this
study: locality of collection; snout–vent length (SVL; measured
with a flexible ruler to the nearest 1 mm); sex (determined by the
presence or absence of hemipenes); condition of the tail (intact or
healed); number of subcaudal scales. For geographic analysis, we
grouped specimens of D. dichrous in two geographical units: GU1
(Andes, Amazonia, and Guiana Shield) and GU2 (Atlantic Forest
and its transitional areas with the Caatinga and Cerrado eco-
regions).
Can. J. Zool. Vol. 92, 2014
Data analysis
Data were analyzed by logistic regression, a generalized linear
modeling (GLM) under binomial errors suitable for modeling the
effects of one continuous explanatory variable (with or without
additional categorical covariates) on a binary response variable
(Logan 2010). We aimed to determine the effects of the continuous
explanatory variable “snout–vent length” (x variable) on the bi-
nary response variable “presence or absence of pseudoautotomy”
in Drymoluber specimens (y variable). To account for the potential
effects related to sex and geographical distribution, an additional
explanatory covariate recorded the sex (male or female for both
species) and geographical unit (only for D. dichrous) for each spec-
imen examined. Because of the large difference in the number of
specimens of D. brazili and D. dichrous available for analysis, we
chose not to consider “species” as a covariate, therefore analyzing
each species separately.
Logistic models differ from traditional linear regression models
because they do not describe the rate of change in the response
variable with change in the explanatory variable. Our logistic
model describes the chance of a Drymoluber specimen of a given
species and sex to present pseudoautotomy, thereby establishing
the chance of a relationship between the response and the predic-
tor. A linear model would be inappropriate in this case because it
is not bounded by logical probability limits of 0 and 1. Neither
would a classical ANOVA be appropriate, as the explanatory vari-
able (SVL) is continuous. Under the null hypothesis, there is an
equal chance of presence and absence of pseudoautotomy inde-
pendently of SVL values, while in an alternative hypothesis, we
expect to find a significant relationship represented by a sigmoid
curve with asymptotes towards 0 and 1 for lower and higher SVL
values, respectively. The choice of this sigmoid function would
also indicate a critical SVL above which Drymoluber specimens are
more likely to present tail breakage (i.e., likelihood >50%). This
critical size would correspond to the inflection point of the sig-
moid curve. Because the model includes covariates, deviance is
expected to be apportioned accordingly between continuous (i.e.,
SVL) and categorical variables terms, thereby reducing the chances of
obtaining spurious significance attributed to the snake’s SVL. De-
viance is the GLM’s measure of variation, analogous to “variance”
of Fisherian statistics.
As pointed out by Slowinski and Savage (1995), a more appro-
priate test of the multiple tail breakage hypothesis (for snakes
with healed tails) would involve a regression of the residual vari-
ation in the number of subcaudals (SC) against SVL, instead of a
simple regression of SVL against SC, since a homogeneity of vari-
ance is not expected in the latter. Therefore, we did a regression
of the absolute values of residuals (the unexplained deviations)
against SVL for all snakes with healed tails, also accounting for
covariates (sex and species).
Analyses followed recommendations by Crawley (2007) and
were performed under R version 3.0.1 software (R Core Team
2013), followed by residual analyses to verify error distribution
and the suitability of employed models, including checks for over-
dispersion. Model simplification was achieved by extracting non-
significant terms (p > 0.05) from the model, starting from the term
explaining less deviance. Each term deletion was followed by an
analysis of deviance with ␹2 test to recalculate the deviance ex-
plained by the remaining terms.
Results
Of 197 D. dichrous examined (130 males and 67 females), 52 (26%)
exhibited a healed tail (42 males (32% of that sex) and 10 females
(15% of that sex)). Of 60 D. brazili examined (32 males and 28 fe-
males), 24 (40%) exhibited a healed tail (14 males (44% of that sex)
and 10 females (36% of that sex)). Considering the geographical
units of D. dichrous, GU1 present 147 specimens (95 males and
52 females), 39 (26%) having a healed tail (32 males (33% of that sex)
Published by NRC Research Press
 Costa et al.
Fig. 1. Probability of pseudoautotomy in Common Woodland Racer (Drymoluber dichrous) as a function of snout–vent length (SVL) and sex.
There is a significant interaction effect (␹冋1册
2
= 4.609, p = 0.031), where frequency of tail breakage increases with SVL in both sexes.
Can. J. Zool. Downloaded from www.nrcresearchpress.com by CSP Staff on 09/03/14
and 7 females (13% of that sex), whereas GU2 present 50 specimens
(35 males and 15 females), 13 (26%) with a healed tail (10 males (28%
of that sex) and 3 females (20% of that sex)).
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We did not find significant differences in the FTB between
D. dichrous geographical units GU1 and GU2 (␹冋1册 2
= 0.262, p = 0.608).
There is a significant interaction effect between SVL and sex (␹冋1册 2
= sybinophiine Scaphiodontophis annulatus (Duméril, Bibron, and
4.609, p = 0.031) for probability of pseudoautotomy in D. dichrous,
where FTB increases with SVL in both sexes (Fig. 1). However, we
did not find this same relationship between SVL and probability of
pseudoautotomy for D. brazili (␹冋2册 2
= 3.431, p = 0.179).
The inflection point of the sigmoid curve, above which Drymoluber
specimens are more likely to have had pseudoautotomy corre-
sponds to 759.22 mm SVL for females and 899.48 mm for males of
D. dichrous. These critical SVL correspond to 94% of the maximum
SVL for females and 77% of the maximum SVL for males. For SVL
values near 710 mm, both sexes have the same likelihood of
pseudoautotomy (Fig. 1).
Models built to test the multiple tail break hypothesis (MTBH)
showed no differences in relation to sex (␹冋1册 2
= 36.575, p = 0.085) or
species (␹冋1册 = 15.876, p = 0.259). Therefore, we opted for the use
2
of the simplest model, considering all Drymoluber specimens
together, regardless of species and sex. The initial regression
performed for SC against SVL was not significant (␹冋1册 2
= 5248,
p = 0.520), as well as the second regression for residuals against
SVL (␹冋1册
2
= 0004, p = 0.985), indicating that MTBH does not occur in
the genus Drymoluber.
Discussion
Frequency of tail stubs in D. dichrous (26%) and D. brazili (40%) is
similar or higher than that observed for most species with pseudo-
autotomy (e.g., Broadley 1987; White et al. 1982; Akani et al. 2002;
Fitch 2003; Bowen 2004; Gregory and Isaac 2005; Placyk and
Burghardt 2005; Pleguezuelos et al. 2010; Todd and Wassersug
2010; Santos et al. 2011; Siqueira et al. 2013). However, it is smaller
than the frequency observed for the colubrines Dendrophidion
dendrophis (Schlegel, 1837) (Olive Forest Racer) (59%; Dourado et al.
2013), Mastigodryas bifossatus (Raddi, 1820) (Rio Tropical Racer)
(46%–52%; Ferreira and Outeiral 1998; Dourado et al. 2013; but see
Leite et al. 2009), the dipsadines Coniophanes fissidens (Günther,
1858) (Yellowbelly Snake) (up to approximately 60%; Mendelson
1992), genus Enulius Cope, 1871, and genus Urotheca Bibron, 1843
813
(approximately 50%; Savage and Slowinski 1996), the psammo-
phines Natriciteres olivacea (Peters, 1854) (Olive Marsh Snake)
(43.6%; Broadley 1987) and some Psammophis Boie, 1827 (up to 45.9%
in a large sample of Psammophis subtaeniatus orientalis Broadley,
1977 (Eastern Striped-bellied Sand Snake); Broadley 1987), the
Duméril, 1854) (Guatemala Neckband Snake) (70%; Savage and
Slowinski 1996), and the elapid Notechis scutatus occidentalis Glauert,
1948 (Western Tiger Snake) (58%; Aubret et al. 2005). Inter- and
intra-specific variation in frequency of urotomy can be attrib-
uted to factors such as differences in predator abundance or
sample size (e.g., Bowen 2004; Placyk and Burghardt 2005; Santos
et al. 2011). Both factors could explain the differences here ob-
served between D. dichrous and D. brazili, since the two species
inhabit distinct environments (Costa et al. 2013), but also because
our sample size of D. brazili was only 30% of the sample size of
D. dichrous.
The lack of significant differences of tail-breakage frequency
between the two geographical units of D. dichrous may suggest that
both groups are subject to similar predation pressures and escape
rates, or even minor or no effect of habitat structure on predation
risk (Santos et al. 2011). Opposite results were found for large
samples of Thamnophis sirtalis sirtalis (L., 1758) (Common Garter
Snake) (523 specimens) from natural populations in the USA
(Placyk and Burghardt 2005) and Natrix maura (L., 1758) (Viperine
Water Snake) (397) from natural versus predator-free European
sites (Santos et al. 2011). Therefore, we cannot fully discard the
possibility of a bias in our results because of the unbalanced sam-
ple size between disjunct populations of D. dichrous (Bowen 2004;
Placyk and Burghardt 2005). However, absence of geographic vari-
ation in tail breakage was found in other species with larger sam-
ples (two from the Neotropics), such as Mastigodryas bifossatus (n =
537; Dourado et al. 2013), Thamnophis sauritus (L., 1766) (Eastern
Ribbon Snake) (n = 502; Willis et al. 1982), Thamnophis sirtalis (n =
685; Willis et al. 1982), and Coniophanes fissidens (n = 927; Mendelson
1992).
Our data do not support a difference in the FTB between
sexes in D. brazili. Similar findings were found for Coniophanes
fissidens (Zug et al. 1979; Mendelson 1992), Dendrophidion dendrophis
(Dourado et al. 2013), Mastigodryas bifossatus (Ferreira and Outeiral
1998; Dourado et al. 2013), Natrix maura (Santos et al. 2011), Nerodia
Published by NRC Research Press
 814
sipedon sipedon (L., 1758) (Northern Water Snake) (Bowen 2004),
Nerodia taxispilota (Holbrook, 1838) (Brown Water Snake) (White
et al. 1982), Notechis scutatus occidentalis (Aubret et al. 2005),
Rhinechis scalaris (Schinz, 1822) (Ladder Snake) (Pleguezuelos et al.
2010), Scaphiodontophis annulatus (Slowinski and Savage 1995),
and Thamnophis butleri (Cope, 1889) (Butler’s Garter Snake) (Willis
et al. 1982). Absence of sexual dimorphism in pseudoautotomy
could suggest that tail breakage does not involve survival differ-
ences between males and females. In fact, some studies indicate
tail stubs do not cause a significant survival cost at all (but see
Fitch 2003), due to a lack of relationship between tail breakage
and body condition (e.g., fat storage and growth), at least for spe-
cies with no important morphological caudal structures (Aubret
et al. 2005; Pleguezuelos et al. 2012).
On the other hand, studies have found a higher frequency of
broken tails in females of Thamnophis sauritus (Willis et al. 1982)
Can. J. Zool. Downloaded from www.nrcresearchpress.com by CSP Staff on 09/03/14
and Thamnophis sirtalis (Fitch 2003; Placyk and Burghardt 2005),
and in males of Natrix natrix (Gregory and Isaac 2005). According
to our data from D. dichrous (Fig. 1), males with SVL up to about
710 mm have higher probability of pseudoautotomy, while for
longer SVL, females are more prone to exhibit tail loss—SVL in
adult specimens of D. dichrous ranges from 415 to 10501 mm (mean
697 mm) in males and 415–801 mm (mean 607 mm) in females
(H.C. Costa, unpublished data). A higher FTB in females is usually
explained by the result of (i) fewer males surviving tail attacks,
possibly because of hemipenis damage (Bowen 2004; Placyk and
Burghardt 2005); (ii) males avoiding tail breakage, because it can
reflect a decrease in reproductive success (Shine et al. 1999);
(iii) the larger mass of females facilitates breakage (at least in
For personal use only.
species with females heavier than males, which appears to not be
the case in D. dichrous) (Fitch 2003); and (iv) the coincidence of the
species’ reproductive season with peaks of activity of predators,
increasing the risk of gravid snakes being attacked (Akani et al.
2002). In Natrix natrix, for which males exhibit more broken tails,
females usually reach larger sizes and grow faster than males,
leading Gregory and Isaac (2005) to argue that the higher injury
rate of males of a given size may be only an indicative that they are
older than similar-sized females. As we do not have any informa-
tion about growth rates of D. dichrous, is not possible to know if the
hypothesis of Gregory and Isaac (2005) could explain a higher FTB
in males <710 mm SVL than females of similar size.
A significant increase of incidence of pseudoautotomy with SVL
has been reported by most studies that tested this hypothesis
(White et al. 1982 (only for males); Willis et al. 1982; Mendelson
1992; Gregory and Isaac 2005; Pleguezuelos et al. 2010; Santos et al.
2011). Fitch (2003) and Dourado et al. (2013) found a higher FTB in
adult specimens, but did not test the “size-related hypothesis”
(Pleguezuelos et al. 2010).
The size-related hypothesis is confirmed for both sexes of
D. dichrous, suggesting that as the snake grows, the probability of
being injured increases and pseudoautotomy becomes an effi-
cient defensive strategy (e.g., Willis et al. 1982; Pleguezuelos et al.
2010). It also indicates that larger snakes may have been attacked
more frequently and survived (Mendelson 1992).
The absence of a relationship between SVL and probability of
pseudoautotomy in D. brazili is an unexpected result, found (but
not discussed) only for females of Nerodia taxispilota (White et al.
1982). The small sample of D. brazili may be the cause of this result
(Bowen 2004).
It is important to note that there is an ontogenetic shift in
dorsal coloration in the genus Drymoluber. Specimens smaller than
400 mm usually have a cross-banded pattern that changes to uni-
form dorsal coloration in larger individuals (Costa et al. 2013).
1The maximum snout–vent length recorded for Drymoluber dichrous (1050 mm) is from FMNH 109807, not from MPEG 17235 as mistakenly cited by Costa et al.
(2013).
Can. J. Zool. Vol. 92, 2014
Seventy-eight specimens of D. dichrous and 20 specimens of
D. brazili examined in our previous study (Costa et al. 2013) exhib-
ited cross-banded coloration, but only two D. dichrous had healed
tails. The distinct color pattern and the near absence of healed
tails in smaller specimens led us to exclude them from all analy-
ses, but it deserves comment.
It is usually suggested that smaller specimens present fewer
healed tails than adults because they spend more time hidden
under cover to avoid predation, while adults are more exposed
(Gregory and Isaac 2005). But in a study using recapture data,
Willis et al. (1982) argued that although injury may not cause
immediate death, it may kill a juvenile before it can attain a larger
size; thus, the lower frequency of healed tails in small specimens
could also be explained because they usually do not survive after
being injured with tail loss.
It is also possible that the cross-banded pattern of small speci-
mens of the genus Drymoluber plays a role in their lower FTB.
Young Drymoluber may mimic coral snakes (Brodie and Brodie
2004), reducing predation rates especially by birds (Brodie 1993).
The color pattern may also conceal the snake when it is immobile
and create a deflective illusion during flight (Jackson et al. 1976;
Pleguezuelos et al. 2010). All these would favor small banded spec-
imens to rarely need to break the tail for defense.
Savage and Slowinski (1996) suggest that in species with both
coral snake coloration and pseudoautotomy, the ability to break
the tail evolved first, providing an effective defense for dull-
colored specimens. This is an interesting hypothesis that fits well
the patterns observed for the genus Drymoluber. However, tail
breakage and ontogenetic shift in coloration are also present in
the genus Mastigodryas Amaral, 1935 (see Dourado et al. 2013), the
sister genus of Drymoluber (Pyron et al. 2013) and other close re-
lated genera (e.g., some Chironius; Sheehy 2006), suggesting that
if Savage and Slowinski’s hypothesis is correct, pseudoautotomy
should have evolved in the most common ancestor of those taxa.
Tail stumps of larger (= older) Drymoluber specimens are not
significantly shorter than those of smaller specimens, not sup-
porting MTBH. Up to now, Scaphiodontophis Taylor and Smith, 1943
is the only genus for which MTBH has been confirmed (Slowinski
and Savage 1995). Scaphiodontophis has a long tail thickened along
its entire length, which facilitates breakage. This feature is shared
only with the genera Urotheca and Enulius, and is known as “spe-
cialized pseudoautotomy” (Slowinski and Savage 1995; Savage and
Slowinski 1996). It is possible that only species with specialized
pseudoautotomy are able to experience multiple tail breaks
(Savage and Slowinski 1996).
Pseudoautotomy is an intriguing, yet understudied, behavior.
Herein, we provide the first contribution on this topic for the
Neotropical snake genus Drymoluber, testing different nonexclu-
sive hypotheses. Our results suggest the need for more research to
(i) evaluate reproduction and activity patterns of males and fe-
males (e.g., Marques et al. 2009); (ii) determine the fate of small
specimens after attack (Willis et al. 1982); (iii) evaluate the effects
of tail breakage on body condition (Pleguezuelos et al. 2012);
(iv) evaluate the effectiveness of juvenile dorsal color pattern to
avoid predation (Brodie 1993); and (v) evaluate the relationship
between pseudoautotomy and the evolution of banded color pat-
tern (Savage and Slowinski 1996) in juveniles of some colubrines.
After all, lost tails may tell more tales.
Acknowledgements
H.C.C. thanks Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior (CAPES) and the Smithsonian Institution for scholar-
ships provided during the execution of his M.Sc. (2008–2010); M.R.M.
Published by NRC Research Press
 Costa et al.
thanks Conselho Nacional de Desenvolvimento Científico e Tec-
nológico (CNPq) for Ph.D. scholarship; RNF thanks CNPq for produc-
tivity fellowship. We thank G.R. Colli, M.A. Brasil, and M.C.M. Viana
(CHUNB); P.C.A. Garcia and P.S. Santos (UFMG); J.H.C. Delabie (CZGB);
F.L. Franco and V.J. Germano (IBSP); M.R.S. Pires and B. Imai
(LZV); L. Sarmento and F. Lanschi (MBML); G.M.F. Pontes (MCP);
L.B. Nascimento (MCN); H. Zaher and C. Mello (MZUSP); A.J.S. Argôlo
(UESC); R. Fernandes and M. Gomes (MNRJ); A.L.C. Prudente,
J.F.M. Sarmento, A. Travassos, and P.C.R. Almeida (MPEG); P.S. Bernarde
(UFACF); D.M. Borges-Nojosa and D.C. Lima (UFC); M.A. Carvalho
(UFMT); D. Frost and D. Kizirian (AMNH); A. Resetar and K.M. Kelly
(FMNH); and R. Heyer, R. McDiarmid, K. Tighe, J.F. Jacobs, and
R. Wilson (USNM) for allowing access to specimens under their
care. We also thank the Burger family, F. Godoy, R. Heyer and
M. Heyer, J.F. Jacobs, K.M. Kelly, L. Matheson, R. McDiarmid,
M.M. Morais, Jr., P. Nunes, P.L.V. Peloso, A. Resetar, D.C. Rodrigues,
Can. J. Zool. Downloaded from www.nrcresearchpress.com by CSP Staff on 09/03/14
M.J. Sturaro, K. Tighe, F. Wilkinson, R. Wilson, and A. Wynn for
their contribution before and during the stay of H.C.C. in the USA.
Finally, we thank R. MacCulloch for his review and comments that
improved the manuscript.
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Appendix A
Can. J. Zool. Downloaded from www.nrcresearchpress.com by CSP Staff on 09/03/14
Specimens examined for this study (for locality details see Costa
et al. 2013). An asterisk (*) indicates healed tail.
Collections acronyms—AMNH: American Museum of Natural
History, New York, New York, USA; ANSP: Academy of Natural
Sciences of Philadelphia, Philadelphia, Pennsylvania, USA;
CHUNB: Coleção Herpetológica da Universidade de Brasília, Bra-
sília, Distrito Federal, Brazil; CZGB: Coleção Zoológica Gregório
Bondar, Ilhéus, Bahia, Brazil; FMNH: Field Museum of Natural
History, Chicago, Illinois, USA; IBSP: Instituto Butantan, São
Paulo, São Paulo, Brazil; LZV: Laboratório de Zoologia de Verteb-
rados, Universidade Federal de Ouro Preto, Ouro Preto, Minas
Gerais, Brazil; MBML: Museu de Biologia Mello Leitão, Santa Te-
resa, Espírito Santo, Brazil; MCP: Museu de Ciências e Tecnologia,
For personal use only.
PUC-RS, Porto Alegre, Rio Grande do Sul, Brazil; MCNR: Museu de
Ciências Naturais, PUC-MG, Belo Horizonte, Minas Gerais, Brazil;
MNRJ: Museu Nacional, Universidade Federal do Rio de Janeiro,
Rio de Janeiro, Rio de Janeiro, Brazil; MPEG: Museu Paraense
Emílio Goeldi, Belém, Pará, Brazil; MZUESC: Museu de Zoologia
da Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil;
MZUFV: Museu de Zoologia João Moojen, Universidade Federal de
Viçosa, Viçosa, Minas Gerais, Brazil; MZUSP: Museu de Zoologia
da Universidade de São Paulo, São Paulo, São Paulo, Brazil;
UFACF: Universidade Federal do Acre, Campus Floresta, Cruzeiro
do Sul, Acre, Brazil; UFC: Universidade Federal do Ceará, For-
taleza, Ceará, Brazil; UFMG: Coleção Herpetológica da Universi-
dade Federal de Minas Gerais, Belo Horizonte, Minas Gerais,
Brazil; UFMT: Universidade Federal do Mato Grosso, Cuiabá, Mato
Grosso, Brazil; USNM: National Museum of Natural History,
Smithsonian Institution, Washington, District of Columbia, USA;
ZMB: Museum für Naturkunde Berlin, Berlin, Germany.
Drymoluber brazili—Males: CHUNB 3839, CHUNB 37345,
CHUNB 3747*, IBSP 383, IBSP 574*, IBSP 696, IBSP 741*, IBSP 7675,
IBSP 8103, IBSP 8836*, IBSP 10188*, IBSP 10465*, IBSP 12692, IBSP
16595, IBSP 18309, IBSP 18992, IBSP 22415, IBSP 23693*, IBSP 25379,
Can. J. Zool. Vol. 92, 2014
IBSP 26688*, IBSP 26716, IBSP 31692, IBSP 32657*, IBSP 33120, IBSP
33668*, IBSP 34369*, IBSP 46996, IBSP 62650*, MCNR 1736, MZUSP
7544*, MZUSP 15507*, UFMT 6970. Females: IBSP 573, IBSP 2717*,
IBSP 8925, IBSP 9144, IBSP 1286, IBSP 1707*, IBSP 10018, IBSP 17019*,
IBSP 17224, IBSP 18053*, IBSP 21928*, IBSP 22515, IBSP 24422, IBSP
25187, IBSP 32624, IBSP 32897, IBSP 33660, IBSP 37413*, IBSP
40475, IBSP 40779*, IBSP 76968, MCNR 1538, MZUESC 3815, MZUFV
780*, MZUSP 7807*, MZUSP 7988*, MZUSP 15506, UFMT 728.
Drymoluber dichrous—Males: AMNH 22491, AMNH 23374,
AMNH 36614, AMNH 49074, AMNH 52318*, AMNH 54479, AMNH
54699, AMNH 54919*, AMNH 54930*, AMNH 55609, AMNH 91812,
AMNH 104610, AMNH 119926*, AMNH 130505, ANSP 3920, UFMG
1398*, CHUNB 12791, CZGB 846, CZGB 331*, CZGB 666, CZGB 2101*,
CZGB 2121, CZGB 3342*, CZGB 4441*, CZGB 5430, CZGB 6826, CZGB
7385, CZGB 7396, CZGB 7717*, CZGB 7981, FMNH 11259, FMNH
75688*, FMNH 40206*, FMNH 109807*, IBSP 3122, IBSP 6208, IBSP
7221, IBSP 7706*, IBSP 25411, IBSP 5089*, IBSP 51703*, IBSP 52140*,
IBSP 52828*, IBSP 69567, MBML 483, MCP 7618, MNRJ 4858*, MNRJ
9240, MNRJ 9297, MPEG 421, MPEG 1838, MPEG 2647*, MPEG 2652,
MPEG 2670*, MPEG 4041*, MPEG 8400, MPEG 8607*, MPEG 10811,
MPEG 11099*, MPEG 11155, MPEG 11698, MPEG 12106*, MPEG
12228, MPEG 12229, MPEG 12230*, MPEG 12257*, MPEG 14406, MPEG
15189, MPEG 15321, MPEG 16207*, MPEG 16982*, MPEG 17057*,
MPEG 17233, MPEG 17437, MPEG 17481*, MPEG 17494, MPEG 17566,
MPEG 17915, MPEG 17995, MPEG 18240, MPEG 18759, MPEG
19750*, MPEG 20044, MPEG 20108, MPEG 20331, MPEG 20384, MZUESC
636, MZUESC 1383, MZUESC 1993, MZUESC 2540, MZUESC 5697,
MZUESC 5801, MZUFV 779, MZUFV 1208, MZUFV 1422, MZUSP
4207, MZUSP 4391, MZUSP 5467*, MZUSP 6098*, MZUSP 7378,
MZUSP 8500, MZUSP 9351, MZUSP 9644*, MZUSP 9645, MZUSP
10298, MZUSP 10423, MZUSP 10424, MZUSP 10763*, MZUSP 11303,
MZUSP 14284, MZUSP 14285, MZUSP 14286*, UFC 2083, UFC 2128,
UFC 2177, UFC 2201*, UFC 2204*, UFC 2220, UFC 2221, UFC 2730*,
UFMT 919, UFMT 1997*, USNM 197267, USNM 204133*, USNM
217185*, USNM 247501, USNM 247694, USNM 316601, USNM
316602, ZMB 1661. Females: AMNH 23354, AMNH 52191, AMNH
52295, AMNH 54541, AMNH 55276, AMNH 55628, AMNH 57258*,
AMNH 119431, CZGB 339, CZGB 1222, CZGB 1269, CZGB 3164, CZGB
3176, CZGB 5180, CZGB 6809*, CZGB 6825, CZGB 7059, CZGB 7397,
IB 2198*, IB 3141, IB 52003, IB 53256*, LZV 373*, MCP 7617, MPEG
8688, MPEG 10832, MPEG 16551, MPEG 17443, MPEG 17446, MPEG
17829, MPEG 17841, MPEG 17849, MPEG 17897, MPEG 17996,
MPEG 19007, MPEG 20000, MPEG 20146, MPEG 20298, MPEG 20330,
MPEG 20762, MPEG 20765, MPEG 20766*, MPEG 20800, MZUSP
4390, MZUSP 6388, MZUSP 6389, MZUSP 10422, MZUSP 11444,
UFACF 663, UFACF 720*, UFACF 741, UFACF 801*, UFACF 1333, UFC
2101, UFC 2104*, UFC 2205, UFC 2211, USNM 83946, USNM 193807,
USNM 204126, USNM 204128, USNM 204129, USNM 247500, USNM
283952*, USNM 289091, USNM 332470, USNM 566261.
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