Studies on Neotropical Fauna and Environment

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Geographical ecology of Tantilla melanocephala

(Squamata: Serpentes: Colubridae) in a
Neotropical region: a comparison of northeastern
Atlantic Forest and Caatinga populations

Felipe Araújo de Oliveira , Rafaela Cândido de França & Frederico Gustavo

Rodrigues França

To cite this article: Felipe Araújo de Oliveira , Rafaela Cândido de França & Frederico
Gustavo Rodrigues França (2020): Geographical ecology of Tantilla�melanocephala (Squamata:
Serpentes: Colubridae) in a Neotropical region: a comparison of northeastern Atlantic
Forest and Caatinga populations, Studies on Neotropical Fauna and Environment, DOI:
10.1080/01650521.2020.1817680

To link to this article: https://doi.org/10.1080/01650521.2020.1817680

Published online: 15 Oct 2020.

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 STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT
https://doi.org/10.1080/01650521.2020.1817680

ORIGINAL ARTICLE

Geographical ecology of Tantilla melanocephala (Squamata: Serpentes:

Colubridae) in a Neotropical region: a comparison of northeastern Atlantic
Forest and Caatinga populations
a b,c a,d
Felipe Araújo de Oliveira , Rafaela Cândido de França and Frederico Gustavo Rodrigues França
a
Programa de Pós-graduação em Ecologia e Monitoramento Ambiental, Universidade Federal da Paraíba, Rio Tinto, Brazil; bPrograma de
Pós-graduação em Ecologia e Conservação da Biodiversidade, Universidade Estadual de Santa Cruz, Ilhéus, Brazil; cHerpetology Section,
Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany; dDepartamento de Engenharia e Meio Ambiente, Universidade
Federal da Paraíba, Rio Tinto, Brazil

ABSTRACT ARTICLE HISTORY

Studying species with wide geographical distributions allows the evaluation of the effects of Received 11 May 2020
environmental variation and phylogenetic constraints on the ecology of these organisms. The Accepted 22 August 2020
snake Tantilla melanocephala is widely distributed across South America in different environ­ KEYWORDS
ments (Amazonia, Atlantic Forest, Cerrado, Caatinga, and Chaco). We compared the morphology, Diet; geographical variation;
diet, and reproduction of T. melanocephala inhabiting the northeastern Brazil in Atlantic Forest morphometry; reproduction;
and Caatinga. In total, 161 individuals were collected from the Atlantic Forest and 88 were snake
collected from Caatinga, and all had similar morphological and ecological traits. There was no
sexual dimorphism within the biomes, and no morphological differences between individuals
from both biomes. The species fed mainly on chilopods, and there were a few differences in the
centipede species consumed in each biome. The volume of consumed prey did not differ
between biomes, and clutch size was also similar (1–2 eggs), with differences during the egg-
laying period reflecting environmental differences. The species has a continuous reproductive
cycle in the Atlantic Forest and a seasonal reproductive cycle in Caatinga. Similarities in the
morphology and ecology of T. melanocephala in the Atlantic Forest and Caatinga suggests that
the species exhibits a high degree of phylogenetic conservatism.

Introduction pressures, such as precipitation, temperature, humidity,

Species with widely distributed populations, that occur
in different environmental conditions, can present dif­
ferences in ecological patterns (Mayr 1977; Pianka
1994). For example, we expect similar ecological
responses under similar environmental conditions
because of phylogenetic constraints. However, when
exposed to different selection pressures, populations
may exhibit geographical variations in ecology caused
by ecotypical adjustments (Vitt & Colli 1994; Pianka
2000; Collar et al. 2010). Natural selection and/or phe­
notypic plasticity cause populations to adjust their
morphology, behavior, and ecology to adapt to differ­
ing environments (Aubret et al. 2004).
Studies of widely distributed reptiles have high­
lighted the importance of both ecological and historical
factors in determining populations’ geographical
ranges (Fitch 1985; Qualls & Shine 1998). If ecological
factors are determinant, then populations of the same
species that are subjected to different environmental
or luminosity, may respond by evolving different char­
acteristics or strategies that are better adapted to the
environmental conditions experienced (Tinkle &
Dunham 1986; Vitt & Colli 1994; Mesquita & Colli
2003). However, even under different selection pres­
sures, species traits might be similar among popula­
tions if phylogenetic factors are determinant (Vitt &
Pianka 2005; Losos 2008). In addition, ecological pres­
sures and historical constraints can act together. The
Neotropical lizard species Ameivula ocellifera (Spix,
1825) and Tropidurus hispidus (Spix, 1825) differ in
their microhabitat use, diet, and reproductive cycle
between Caatinga and Atlantic Forest populations,
whereas body temperature and clutch size do not differ
(Albuquerque et al. 2018).
Because of body-shape limitations, snakes have
evolved high levels of phenotypic plasticity (Madsen &
Shine 1993), and geographical ecology studies have
reported both differences and similarities in population

CONTACT Frederico Gustavo Rodrigues França fredericogrf@gmail.com

© 2020 Informa UK Limited, trading as Taylor & Francis Group

Published online 15 Oct 2020

2 F. A. DE OLIVEIRA ET AL.
characteristics. The North American snake Thamnophis
elegans (Baird & Girard, 1853) differs in feeding behavior
between coastal and inland populations but there is no
polymorphism (Arnold 1977, 1981), and the congeneric
species T. sirtalis (Linnaeus, 1758) exhibits remarkable
variation in reproductive traits, such as litter size and
neonate size, across Canada (Gregory & Larsen 1993).
The Australian carpet python Morelia spilota (Lacépède,
1804) exhibits geographical variations in sexual size
dimorphism throughout its distribution (Shine &
Fitzgerald 1995; Pearson et al. 2002), and the Japanese
snakes Elaphe quadrivirgata (Boie, 1826) and Elaphe cli­
macophora (Boie, 1826) differ in body size, life history
traits, and food preferences between island and mainland
populations (Hasegawa & Moriguchi 1989). The lance­
head Bothrops atrox (Linnaeus, 1758) and the rattlesnake
Crotalus durissus Linnaeus, 1758 exhibit geographical
variations in venom phenotype (i.e. different proteins
that belong to different groups of toxins) and toxicity
throughout their South American distributions (Nunez
et al. 2009; Boldrini-Franca et al. 2010).
The Neotropical region is ideal for investigating envir­
onmental effects on populations of widely distributed spe­
cies because many reptile species have a wide distribution
(Vanzolini 2002; Mesquita & Colli 2003; Gouveia et al.
2016) and the region is a mosaic of biomes with several
physiognomic types such as Caatinga, Cerrado, Chaco, and
Pantanal, and forested biomes such as Amazonia and the
Atlantic Forest (Ab’Saber 1977). Because of structural and
climatic differences among the biomes, there may be dis­
similarities in life history traits, diet, morphology, and
behavior among the reptile populations that inhabit
them. In regions where precipitation is unpredictable
(e.g. Caatinga), some populations reproduce continuously,
with several clutches per reproductive season and small
clutch sizes and large eggs, whereas in regions with marked
seasonality (e.g. Cerrado), reproductive cycles are reduced
to one or a few clutches per reproductive season, with large
clutch sizes and small eggs (Colli et al. 2003; Mesquita &
Colli 2003; Garda et al. 2012). In addition, the climatic
unpredictability and horizontal structure of the phytophy­
siognomies of the xeric Caatinga can constrain body shape,
sexual maturation, and food availability in comparison to
the Atlantic Forest (Garda et al. 2012; Albuquerque et al.
2018).
Many lizard and snake species can exhibit phenotypic
variation or plasticity in morphological and reproductive
traits due to the pressures experienced by populations in
different environments (Gotthard & Nylin 1995; Losos
et al. 1997; Aubret et al. 2004). For example, Polychrus
acutirostris Spix, 1825, Tropidurus hispidus (Spix, 1825),
Philodryas nattereri Steindachner, 1870, and Philodryas
olfersii (Lichtenstein, 1823), avoid reproduction during
the dry season in Brazilian Caatinga and so have
a seasonal reproductive cycle, whereas in rain-
predictable environments, such as the Atlantic Forest,
they reproduce continuously throughout the year (Vitt
1980; Vitt & Vangilder 1983; Garda et al. 2012;
Albuquerque et al. 2018).
The genus Tantilla (Colubridae: Sonorini) com­
prises approximately 69 species that are distributed
from the southern United States to northeastearn
Argentina (Wilson & Mata-Silva 2015; McCranie &
Smith 2017; Uetz et al. 2020). Two species occur in
Brazil, T. boipiranga (Sawaya & Sazima, 2003), which is
restricted to southeastern Brazil (Cassimiro 2003;
Sawaya & Sazima 2003; Silveira et al. 2009), and
T. melanocephala (Linnaeus, 1758), which has one of
the widest geographical distributions of all Neotropical
snakes, ranging from the Caribbean islands and
Panama in the north to Uruguay and northern
Argentina in the south (Wilson & Mata-Silva 2015),
and occupying contrasting environments such as dense
forest to open grasslands (Martins & Oliveira 1998;
Cacciali & Brusquetti 2005; Marques et al. 2005;
França & Braz 2013).
Marques and Puorto (1998) and Santos-Costa et al.
(2006) found sexual size dimorphism in
T. melanocephala in the southeastern Atlantic Forest
and eastern Amazonia, where the SVL of females is
greater than that of males. This pattern of sexual
dimorphism is also found in the congeneric species
T. coronata Baird & Girard, 1853 (Todd et al. 2008)
and other species of the tribe Sonorini (Shine 1994).
Many snake species have larger females than males
because females must produce and carry eggs (Shine
1994; Pearson et al. 2002; Pizzatto et al. 2008).
Most Tantilla species feed almost exclusively on
centipedes (Solórzano-López et al. 2012), but some
species, such as T. gracilis Baird & Girard, 1853, can
consume other prey items such as coleopteran larvae
and snails (Cobb 2004). Tantilla melanocephala feeds
primarily on centipedes throughout its distribution, but
may occasionally consume other arthropods (Cunha &
Nascimento 1978; Marques & Puorto 1998; França
et al. 2008). The diet specialization of the Sonorini
tribe is directly related to fossorial or cryptozoic habits,
and the cranial apparatus, including the maxillary arch
and teeth (Savitzky 1983), indicates that this group is
phylogenetically conserved. Despite there being a high
diversity and wide distribution of centipedes in the
Neotropics (Minelli 2011), almost no information is
available of centipede richness and abundance in
Brazil (Foddai et al. 2000; Calvanese et al. 2014).
Herein, we use the snake T. melanocephala as
a model for testing differences among populations

living under different environmental conditions in
Caatinga and northeastern Atlantic Forest. We investi­
gate the morphology, diet, and reproduction to analyze
geographical variations in the ecology of the species.
We hypothesize that because of the different environ­
mental conditions in the two biomes, these parameters
would differ between the populations. Specifically, we
predict that the specimens found in Caatinga would be
smaller and have a broader diet than specimens from
the Atlantic Forest and would also exhibit pronounced
sexual dimorphism and continuous reproduction with
small clutch sizes and large eggs.
Materials and methods
We used the classification proposed by Ab’Saber (1977) for
morphoclimatic domains of South America. The Atlantic
Forest extends along the Atlantic coast of Brazil and inland
as far as Paraguay and Argentina, and originally covered
around 1,500,000 km2. It occupies a narrow strip of coast
with low elevations in northeastern Brazil and extends up
to 600 km inland in the south, reaching around 2,900 m
above sea level in the Serra do Mar mountain range. We
only used specimens from the northeastern Atlantic Forest
(Brazilian northeastern coast of Bahia, Sergipe, Alagoas,
Pernambuco, Paraíba and Rio Grande do Norte states) to
avoid bias caused by the different climate and elevation of
the south (Galindo Leal & Câmara 2003). The northeastern
Atlantic Forest has a humid, tropical climate (Aw accord­
ing to the Köppen system of climate classification), a wet
season that runs between February and October, a mean
annual precipitation of 1,700 mm (Galindo Leal & Câmara
2003), and a mean monthly temperature between 20° and
25°C (Nimer 1972). The vegetation is a mosaic of physiog­
nomic subtypes: evergreen, semi-deciduous, and open for­
ests, plus transitional areas (Veloso et al. 1991).
The Caatinga covers around 850,000 km2 in north­
eastern Brazil and has a dry, tropical climate (Bw
according to the Köppen system of climate classifica­
tion). It has hot summers with unpredictable precipita­
tion that ranges between 300 and 800 mm from
January to March (50–70% of precipitation restricted
to these months), and in some years no rain falls. It has
mean annual temperatures between 26° and 28°C with
a maximum of 42°C, and is subject to high solar
radiation, little cloud cover, low humidity, and high
evapotranspiration (Nimer 1989; Prado 2003). The
typical vegetation is xerophilous woodland that
includes many deciduous and thorny species (Veloso
et al. 1991).
We analyzed 249 T. melanocephala individuals, 161
from the Atlantic Forest and 88 from Caatinga, from
72 locations in total (Figure 1). The specimens were
STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 3
housed at the Coleção Herpetológica da Universidade
de Brasília, the Coleção Herpetológica da Universidade
da Paraíba, the Coleção do Laboratório de Anfíbios
e Répteis da Universidade Federal do Rio Grande do
Norte, the Coleção Herpetológica da Universidade
Federal de Sergipe, the Museu de História Natural da
Universidade Federal de Alagoas, the Coleção
Herpetológica da Universidade Federal da Bahia, the
Museu Nacional associated with Universidade Federal
do Rio de Janeiro, and the Coleção Herpetológica da
Universidade Regional do Cariri (vouchers in
Appendix 1).
We used a ruler (precision = 0.1 mm) to measure
the snout-vent length (SVL; measured from the tip of
the snout to the vent), tail length (TL; measured from
the cloaca to the end of the tail), and total length
(TO = SVL + TL), and used a digital caliper
(precision = 0.01 mm) to measure body width (BW;
measured in the median portion of the body); body
height (BH; measured in the median portion of the
body); head width (HW; largest head width measured
at parietal scales level); head height (HH; measured at
its highest point, at the level of the parietal scales); head
length (HL; distance between the rostral scale and the
articulation of the quadrate bone with the mandible);
distance between nostrils (DN); and eye diameter (ED).
We calculated body size based on the scores of an
isometric vector with p−0.5 values, where p is the num­
ber of variables used (Jolicoeur 1963; Somers 1986).
Juveniles were removed from the analysis (Table 1).
We used a multivariate analysis of variance
(MANOVA) to test for morphological differences
(SVL, TL, BW, BH, HW, HH, HL, DN, and ED)
between the Atlantic Forest and Caatinga populations,
and an analysis of variance (ANOVA) and a non-
parametric Kruskal-Wallis test to test for sexual
dimorphism (SVL, TL, HL, and TO) within each
biome. We used a generalized linear model (GLM) to
test for the effects of sex and biome on SVL. We
assumed a Gaussian (or normal) distribution for the
GLM (Tabachnick & Fidell 2007).
We analyzed stomach and gut contents using
a stereoscope and identified food items to genus level
if possible. The lengths and widths of intact prey were
measured using a digital caliper (precision = 0.01 mm)
to estimate the volume, based on the formula for an
ellipsoid volume (Vitt et al. 1996):
� � � �2
4 1 1
V ¼ π length � width ;
3 2 2
We used a Student’s t-test to determine whether
there were differences in prey richness between biomes,
4 F. A. DE OLIVEIRA ET AL.

Figure 1. Geographical distribution of Tantilla melanocephala in Caatinga and the northeastern Atlantic Forest.
 STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 5

Table 1. Morphological measurements of male and female Tantilla melanocephala from the Atlantic Forest and Caatinga, presented as
means and standard errors. All of the measurements are in millimeters. SVL = snout-vent length; TL = tail length; TBL = total body length;
HL = head length; HW = head width; HH = head height; BN = between nostrils; ED = eye diameter; BH = body height; BW = body width;
VS = ventral scales; SC = subcaudal scales; LDT = largest diameter of the testes; LDE = largest diameter of the eggs.
Females Males
Atlantic Forest Caatinga Atlantic Forest Caatinga
SVL 225.0 ± 48.96 (86–303; N = 81) 232.0 ± 36.24 (180–349; N = 40) 215.0 ± 22.40 (152–263; N = 80) 226.0 ± 33.75 (160–313; N = 42)
TL 60.0 ± 15.47 (13–84; N = 67) 66.0 ± 11.29 (45–90; N = 36) 67.0 ± 8.31 (45–87; N = 71) 70.0 ± 13.78 (43–91; N = 36)
TBL 287.0 ± 65.12 (165–380; N = 67) 295.0 ± 41.24 (229–367; N = 36) 279.0 ± 29.08 (197–337; N = 71) 288.0 ± 44.70 (206–385; N = 36)
HL 8.21 ± 1.34 (4.60–11.37; N = 81) 9.12 ± 1.32 (7.27–13.6; N = 40) 8.40 ± 0.76 (6.38–11.89; N = 80) 9.45 ± 1.20 (6.80–13; N = 42)
HW 4.82 ± 0.81 (2.90–6.54; N = 81) 4.88 ± 0.81 (3.81–8.01; N = 40) 4.96 ± 0.43 (4–5.81; N = 80) 5.25 ± 0.69 (3.57–7.11; N = 42)
HH 3.43 ± 0.82 (3.43–5.61; N = 81) 3.53 ± 0.82 (2.44–6.69; N = 40) 3.78 ± 0.77 (2.73–8.20; N = 80) 4.02 ± 0.76 (2.40–5.84; N = 42)
BN 1.94 ± 0.39 (0.92–2.82; N = 81) 2.08 ± 0.39 (1.57–3.6; N = 40) 2.04 ± 0.24 (1.48–2.51; N = 80) 2.27 ± 0.37 (1.24–3.13; N = 42)
ED 1.1 ± 0.23 (0.60–1.7; N = 81) 1.16 ± 0.21 (0.87–1.83; N = 40) 1.15 ± 0.18 (0.76–1.71; N = 80) 1.21 ± 0.23 (0.74–2.20; N = 42)
BH 4.90 ± 1.31 (1.92–8.25; N = 81) 5.27 ± 1.32 (2.19–8.44; N = 40) 5.01 ± 1.01 (0.92–7.40; N = 80) 5.90 ± 1.02 (3.80–7.59; N = 42)
BW 5.38 ± 1.15 (2.34–7.6; N = 81) 5.56 ± 1.10 (4.3–8.86; N = 40) 5.63 ± 1.01 (0.79–9.50; N = 80) 6.22 ± 0,97 (3.90–8.56; N = 42)
VS 153.0 ± 7.28 (135–167; N = 79) 152.5 ± 5.82 (142–169; N = 40) 146.0 ± 4.83 (134–158; N = 74) 146.0 ± 7.46 (134–160; N = 42)
SC 50.0 ± 4.34 (43–63; N = 65) 53.0 ± 5.70 (44–67; N = 36) 56.0 ± 3.99 (42–63; N = 67) 55.5 ± 6.71 (41–67; N = 36)
LDT 7.78 ± 1.52 (4.21–11.28; N = 54) 8.52 ± 2.22 (4.23–12.34; N = 29)
LDE 17.39 ± 8.37 (9.05–40; N = 21) 17.75 ± 8.21(9.05–40; N = 20)

and compared prey volume between biomes by per­
forming an analysis of covariance (ANCOVA), with
SVL as a covariate.
To identify the sex, we dissected the individuals and
directly examined the gonads. We measured the length
and width of the right and left testicles and considered
males with well-developed testicles and a convoluted epi­
didymis as reproductively active (Shine 1977; Almeida-
Santos et al. 2014). For females, we measured the length
and width of the largest follicle and all of the eggs, and
considered those that had vitellogenic follicles (≥5 mm)
in the ovaries, eggs in the oviduct, or a flaccid oviduct that
indicated recent egg laying (Shine 1977; Almeida-Santos
et al. 2014) as reproductive females. We calculated the
mean volume of eggs and testicles using the ellipsoid
volume formula described above.
We used a two-way ANOVA to test for differences in
testicle volume between the biomes, a Student’s t-test to test
for differences in clutch size between the biomes, and an
ANCOVA with SVL as a covariate and biome as a factor to
test for differences in egg volume between the biomes.
We log10-transformed all of the morphometric vari­
ables prior to analysis to normalize the data, and trea­
ted outliers according to Tabachnick and Fidell (2007).
Statistical significance was set at α = 0.05. All of the
statistical analyses were performed in R version 3.2.0
(R Core Team 2015).
Results
Of the 249 T. melanocephala specimens revised, 80 (78
adults and two immature) males and 81 (72 adults and
nine immature) females were from the Atlantic Forest,
and 44 (42 adult and two immature) males and 44 (40
adult and four immature) females were from Caatinga.
The smallest reproductive males had SVLs of 170 and
160 mm in the Atlantic Forest and Caatinga, respec­
tively, and the smallest reproductive females had SVLs
of 175 and 180 mm in the Atlantic Forest and
Caatinga, respectively. No significant differences in
the morphological measurements were found between
the biomes (MANOVA: F1,213 = 5.37, P > 0.0001), and
there was no significant sexual dimorphism in indivi­
duals from the Atlantic Forest (Kruskal-Wallis test:
X2 = 0.24, df = 1.136, P= 0.62) or from Caatinga
(ANOVA: F1,75 = 0.46, P= 0.50). Neither SVL nor TL
significantly differed between males and females or
between the Atlantic Forest and Caatinga populations
(GLM of SVL: F3,245 = 0.31, P = 0.27; GLM of TL:
F3,211 = 7.14, P = 0.13).
We dissected 154 specimens, of which 41 (27%) had
stomach or gut contents. Twenty items were impossible
to identify, eight could only be identified to the Class
Chilopoda, and 13 were identified to genus level. We
found individuals from one order
(Scolopendromorpha), two families (Scolopendridae
and Cryptopidae), and four genera (Scolopendra,
Arthrorabdus, Otostigmus, and Cryptops) (Table 2).
We found no significant difference in diet richness
between the Atlantic Forest and Caatinga (Student’s
t-test: t= 0.079, df = 5, P= 0.94), and there was no significant
difference in prey volume between biomes (with snake SVL
as a covariate) (ANCOVA: F1,8 = 0.205, P= 0.66).
We obtained reproductive data for 61 adult males
and 78 adult females from the Atlantic Forest and 29
adult males and 36 adult females from Caatinga. In all
6 F. A. DE OLIVEIRA ET AL.
Table 2. Diet composition of Tantilla melanocephala from Caatinga and the Atlantic Forest. N = number; F = frequency; V = volume.
Caatinga (NS = 58)
Prey Item N F%
Class Chilopoda
Order Scolopendromorpha
Family Cryptopidae
Cryptops 1 6.00
Family Scolopendridae
Arthrorabdus - -
Otostigmus - -
Scolopendra 6 38.00
Unidentified
Pieces of arthropods 6 38.00
Digested material 3 19.00
Total 16
males, we found no significant difference between the
volumes of the left and right testicles (Student’s t-test:
t = 1.65, df = 88, P= 0.099). Testicle volume varied in
relation to the SVL (two-way ANOVA: F1,87 = 20.47,
P > 0.0001) and between biomes (two-way ANOVA:
F1,87 = 10.01, P = 0.002), but there was no significant
interaction between SVL and biome (two-way
ANOVA: F1,86 = 2.94, P = 0.09). Regarding females,
36 individuals from the Atlantic Forest had vitellogenic
follicles and 21 were carrying eggs, whereas 12 indivi­
duals from Caatinga had vitellogenic follicles and seven
had eggs (Figure 2). Clutch size (1–2 eggs per female)
was similar between females from the Atlantic Forest
and Caatinga, except for a single female
(SVL = 290 mm; TO = 365 mm) from Caatinga that
had four eggs. We found no significant difference in
clutch size between females from the Atlantic Forest
and those from Caatinga (Student’s t-test: t = 0.92,
df = 12, P= 0.37), and there was no significant differ­
ence in egg volume between the biomes with female
SVL as a covariate (ANCOVA: F1,24 = 0.97, P= 0.32).
Discussion
There were no significant morphological differences
between Tantilla melanocephala populations in
Caatinga and the Atlantic Forest. The mean body size
of the species found here did not differs from the
central Brazilian Cerrado, the southeastern Atlantic
Forest, and eastern Amazonia, and males reach sexual
maturity at a smaller size than females in all biomes
(Marques & Puorto 1998; Santos-Costa et al. 2006;
França et al. 2008). Therefore, the general morphology
of the species seems to be highly conserved. Although
we found that the mean and maximum female size was
slightly greater than that of male size both in Caatinga
and the northeastern Atlantic Forest, the differences
were not statistically significant. Tantilla melanoce­
phala does not produce large clutches (generally only
Atlantic Forest (NS = 96)
3
V (mm ) V% N F% V (mm3) V%
70 9.00 - - - -
- - 1 4.00 87.17 22.00
- - 1 4.00 27.11 7.00
442.24 59.00 3 12.00 187.42 48.00
231.72 32.00 2 8.00 88.43 23.00
- - 18 72.00 - -
743.96 25 390.13
one or two eggs), so sexual size dimorphism may not
be evident in all populations.
The morphological similarities of different
T. melanocephala populations could also be caused by
the generalist habits exhibited by the species. Tantilla
melanocephala is nocturnal and fossorial, and can inha­
bit varied habitats such as primary forests, grasslands,
savannas, coastal environments, and even urban areas
(Wilson & Mata-Silva 2015). Therefore, even in con­
trasting biomes such as Caatinga and the Atlantic
Forest, T. melanocephala individuals can exhibit similar
ecological preferences that are reflected in similar
morphologies.
Regarding feeding behavior, Otostigmus spp. and
Scolopendra spp. seem to be the most frequent type of
prey consumed by T. melanocephalla found in
Caatinga, Atlantic Forest and Cerrado (Marques &
Puorto 1998; França et al. 2008). In addition, all of
the centipedes found in the snakes’ stomachs were
consumed head-first. Marques and Puorto (1998)
reported the same pattern of ingestion, suggesting
that centipedes can inflict damage, so snakes first
immobilize the prey to avoid injury (Cundall &
Greene 2000). Tantilla melanocephala uses venom to
immobilize the centipede until it ceases struggling
(Marques & Puorto 1998). Unfortunately, head-first
ingestion damages the prey’s head, making it impossi­
ble under a stereoscope to identify many prey items to
the genus or family levels. Unidentified centipedes
accounted for over 40% of all the prey items revised,
and this number was similar to unidentified items in
the southeastern Atlantic Forest (Marques & Puorto
1998). Also, there was no correlation between prey
size and snake size, and large T. melanocephala indivi­
duals did not necessarily eat large centipedes. We did
not find any diet shifts caused by ontogenetic differ­
ences and juveniles and adults consumed the same
kind of prey, as is the case in other species of Tantilla
(Cobb 2004). The identification to genus level of
 STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 7

Figure 2. Reproductive cycle of Tantilla melanocephala in A) the Atlantic Forest and B) Caatinga. Seasonal variations in the
diameters of ovarian follicles (filled circles) and eggs (empty circles).

centipedes that are consumed by T. melanocephala in
other areas of its distribution, such as Amazonia,
Chaco, and Cerrado, would elucidate the patterns of
prey consumption and feeding behavior of the species.
Both environmental and historical factors seem to
influence reptile life history parameters (Dunham &
Miles 1985; Vitt 1992; Mesquita & Colli 2010), as
observed for T. melanocephala. The species reproduc­
tive period differed between the populations, support­
ing the statement of Santos-Costa et al. (2006) that
reproductive variation is related to different environ­
mental conditions in the species’ geographical range. In
the northeastern Atlantic Forest we found eggs and
vitellogenic follicles throughout the year, indicating
that this population has a continuous reproductive
cycle, as seen in eastern Amazonia (Santos-Costa
et al. 2006). However, in Caatinga, eggs and vitello­
genic follicles were only present between January and
April, with one record in October, suggesting that this
population has a seasonal reproductive cycle, as found
8 F. A. DE OLIVEIRA ET AL.
in the southeastern Atlantic Forest (Marques & Puorto
1998). Thus T. melanocephala shows a similar pattern
in the reproductive period as other lizards and snakes
with wide geographical ranges, which also inhabit both
the Caatinga and the Atlantic Forest (Vitt 1980; Vitt &
Vangilder 1983; Garda et al. 2012; Albuquerque et al.
2018). However, the underlying determinants of seaso­
nal and continuous reproductive cycles in tropical rep­
tiles are unknown, but are probably related to
environmental variables such as temperature, moisture,
and photoperiod (Vitt & Vangilder 1983; Pizzatto et al.
2008).
Clutch sizes in Caatinga and the Atlantic Forest
were similar to those reported in other studies
(Marques & Puorto 1998; Santos-Costa et al. 2006),
which suggests that clutch size in T. melanocephala
may be constrained by phylogenetic conservation (his­
torical factors). Most reproductive females had vitello­
genic follicles and eggs mainly in the right oviduct, as
described by Marques and Puorto (1998); however, we
did not find any significant differences in size or mor­
phology between the left and right ovaries. In
T. coronata, there is also normal production of follicles
in both ovaries, but only the right oviduct is functional
(Aldridge & Semlitsch 1992). The absence of a left
oviduct occurs in other species of Tantilla (Clark Jr
1970). In addition, other reproductive attributes did
not significantly differ between the Atlantic Forest
and Caatinga populations, such as egg volume and
the correlation between female size and egg volume,
which shows that the reproductive patterns of
T. melanocephala are determined by phylogeny.
Acknowledgments
We thank D. Mesquita (UFPB), G. Vieira (UFPB), M. Napoli
(UFBA), R. Lira (UFBA), P. Passos (MNRJ), R. Fernandes
(MNRJ), R. Faria (UFS), R. Ávila (URCA), and A. Garda
(UFRN) for permission to work with Tantilla specimens
from Brazilian collections and museums. We also thank
I. Pedrosa and R. Brandão for critical comments of previous
drafts.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
F. O. Araújo thanks Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES) for a master’s scholar­
ship. R. C. França thanks Fundação de Amparo à Pesquisa do
Estado da Bahia (FAPESB) for a PhD scholarship [BOL0353/
2016] and Brazilian National Council for Scientific and
Technological Development (CNPq) for a Doutorado
Sanduíche no Exterior (SWE) scholarship [208442/2017-0].
F. G. R. França thanks CNPq for financial support [Universal
grant 404671/2016-0].
ORCID
Felipe Araújo de Oliveira http://orcid.org/0000-0002-
2289-7002
Rafaela Cândido de França http://orcid.org/0000-0001-
5034-6796
Frederico Gustavo Rodrigues França http://orcid.org/
0000-0001-6989-2455
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