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

CONTACT Frederico Gustavo Rodrigues França [email protected]

© 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 the dry season in Brazilian Caatinga and so have
elegans (Baird & Girard, 1853) differs in feeding behavior a seasonal reproductive cycle, whereas in rain-
between coastal and inland populations but there is no predictable environments, such as the Atlantic Forest,
polymorphism (Arnold 1977, 1981), and the congeneric they reproduce continuously throughout the year (Vitt
species T. sirtalis (Linnaeus, 1758) exhibits remarkable 1980; Vitt & Vangilder 1983; Garda et al. 2012;
variation in reproductive traits, such as litter size and Albuquerque et al. 2018).
neonate size, across Canada (Gregory & Larsen 1993). The genus Tantilla (Colubridae: Sonorini) com­
The Australian carpet python Morelia spilota (Lacépède, prises approximately 69 species that are distributed
1804) exhibits geographical variations in sexual size from the southern United States to northeastearn
dimorphism throughout its distribution (Shine & Argentina (Wilson & Mata-Silva 2015; McCranie &
Fitzgerald 1995; Pearson et al. 2002), and the Japanese Smith 2017; Uetz et al. 2020). Two species occur in
snakes Elaphe quadrivirgata (Boie, 1826) and Elaphe cli­ Brazil, T. boipiranga (Sawaya & Sazima, 2003), which is
macophora (Boie, 1826) differ in body size, life history restricted to southeastern Brazil (Cassimiro 2003;
traits, and food preferences between island and mainland Sawaya & Sazima 2003; Silveira et al. 2009), and
populations (Hasegawa & Moriguchi 1989). The lance­ T. melanocephala (Linnaeus, 1758), which has one of
head Bothrops atrox (Linnaeus, 1758) and the rattlesnake the widest geographical distributions of all Neotropical
Crotalus durissus Linnaeus, 1758 exhibit geographical snakes, ranging from the Caribbean islands and
variations in venom phenotype (i.e. different proteins Panama in the north to Uruguay and northern
that belong to different groups of toxins) and toxicity Argentina in the south (Wilson & Mata-Silva 2015),
throughout their South American distributions (Nunez and occupying contrasting environments such as dense
et al. 2009; Boldrini-Franca et al. 2010). forest to open grasslands (Martins & Oliveira 1998;
The Neotropical region is ideal for investigating envir­ Cacciali & Brusquetti 2005; Marques et al. 2005;
onmental effects on populations of widely distributed spe­ França & Braz 2013).
cies because many reptile species have a wide distribution Marques and Puorto (1998) and Santos-Costa et al.
(Vanzolini 2002; Mesquita & Colli 2003; Gouveia et al. (2006) found sexual size dimorphism in
2016) and the region is a mosaic of biomes with several T. melanocephala in the southeastern Atlantic Forest
physiognomic types such as Caatinga, Cerrado, Chaco, and and eastern Amazonia, where the SVL of females is
Pantanal, and forested biomes such as Amazonia and the greater than that of males. This pattern of sexual
Atlantic Forest (Ab’Saber 1977). Because of structural and dimorphism is also found in the congeneric species
climatic differences among the biomes, there may be dis­ T. coronata Baird & Girard, 1853 (Todd et al. 2008)
similarities in life history traits, diet, morphology, and and other species of the tribe Sonorini (Shine 1994).
behavior among the reptile populations that inhabit Many snake species have larger females than males
them. In regions where precipitation is unpredictable because females must produce and carry eggs (Shine
(e.g. Caatinga), some populations reproduce continuously, 1994; Pearson et al. 2002; Pizzatto et al. 2008).
with several clutches per reproductive season and small Most Tantilla species feed almost exclusively on
clutch sizes and large eggs, whereas in regions with marked centipedes (Solórzano-López et al. 2012), but some
seasonality (e.g. Cerrado), reproductive cycles are reduced species, such as T. gracilis Baird & Girard, 1853, can
to one or a few clutches per reproductive season, with large consume other prey items such as coleopteran larvae
clutch sizes and small eggs (Colli et al. 2003; Mesquita & and snails (Cobb 2004). Tantilla melanocephala feeds
Colli 2003; Garda et al. 2012). In addition, the climatic primarily on centipedes throughout its distribution, but
unpredictability and horizontal structure of the phytophy­ may occasionally consume other arthropods (Cunha &
siognomies of the xeric Caatinga can constrain body shape, Nascimento 1978; Marques & Puorto 1998; França
sexual maturation, and food availability in comparison to et al. 2008). The diet specialization of the Sonorini
the Atlantic Forest (Garda et al. 2012; Albuquerque et al. tribe is directly related to fossorial or cryptozoic habits,
2018). and the cranial apparatus, including the maxillary arch
Many lizard and snake species can exhibit phenotypic and teeth (Savitzky 1983), indicates that this group is
variation or plasticity in morphological and reproductive phylogenetically conserved. Despite there being a high
traits due to the pressures experienced by populations in diversity and wide distribution of centipedes in the
different environments (Gotthard & Nylin 1995; Losos Neotropics (Minelli 2011), almost no information is
et al. 1997; Aubret et al. 2004). For example, Polychrus available of centipede richness and abundance in
acutirostris Spix, 1825, Tropidurus hispidus (Spix, 1825), Brazil (Foddai et al. 2000; Calvanese et al. 2014).
Philodryas nattereri Steindachner, 1870, and Philodryas Herein, we use the snake T. melanocephala as
olfersii (Lichtenstein, 1823), avoid reproduction during a model for testing differences among populations
 STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 3

living under different environmental conditions in housed at the Coleção Herpetológica da Universidade
Caatinga and northeastern Atlantic Forest. We investi­ de Brasília, the Coleção Herpetológica da Universidade
gate the morphology, diet, and reproduction to analyze da Paraíba, the Coleção do Laboratório de Anfíbios
geographical variations in the ecology of the species. e Répteis da Universidade Federal do Rio Grande do
We hypothesize that because of the different environ­ Norte, the Coleção Herpetológica da Universidade
mental conditions in the two biomes, these parameters Federal de Sergipe, the Museu de História Natural da
would differ between the populations. Specifically, we Universidade Federal de Alagoas, the Coleção
predict that the specimens found in Caatinga would be Herpetológica da Universidade Federal da Bahia, the
smaller and have a broader diet than specimens from Museu Nacional associated with Universidade Federal
the Atlantic Forest and would also exhibit pronounced do Rio de Janeiro, and the Coleção Herpetológica da
sexual dimorphism and continuous reproduction with Universidade Regional do Cariri (vouchers in
small clutch sizes and large eggs. Appendix 1).
We used a ruler (precision = 0.1 mm) to measure
the snout-vent length (SVL; measured from the tip of
Materials and methods
the snout to the vent), tail length (TL; measured from
We used the classification proposed by Ab’Saber (1977) for the cloaca to the end of the tail), and total length
morphoclimatic domains of South America. The Atlantic (TO = SVL + TL), and used a digital caliper
Forest extends along the Atlantic coast of Brazil and inland (precision = 0.01 mm) to measure body width (BW;
as far as Paraguay and Argentina, and originally covered measured in the median portion of the body); body
around 1,500,000 km2. It occupies a narrow strip of coast height (BH; measured in the median portion of the
with low elevations in northeastern Brazil and extends up body); head width (HW; largest head width measured
to 600 km inland in the south, reaching around 2,900 m at parietal scales level); head height (HH; measured at
above sea level in the Serra do Mar mountain range. We its highest point, at the level of the parietal scales); head
only used specimens from the northeastern Atlantic Forest length (HL; distance between the rostral scale and the
(Brazilian northeastern coast of Bahia, Sergipe, Alagoas, articulation of the quadrate bone with the mandible);
Pernambuco, Paraíba and Rio Grande do Norte states) to distance between nostrils (DN); and eye diameter (ED).
avoid bias caused by the different climate and elevation of We calculated body size based on the scores of an
the south (Galindo Leal & Câmara 2003). The northeastern isometric vector with p−0.5 values, where p is the num­
Atlantic Forest has a humid, tropical climate (Aw accord­ ber of variables used (Jolicoeur 1963; Somers 1986).
ing to the Köppen system of climate classification), a wet Juveniles were removed from the analysis (Table 1).
season that runs between February and October, a mean We used a multivariate analysis of variance
annual precipitation of 1,700 mm (Galindo Leal & Câmara (MANOVA) to test for morphological differences
2003), and a mean monthly temperature between 20° and (SVL, TL, BW, BH, HW, HH, HL, DN, and ED)
25°C (Nimer 1972). The vegetation is a mosaic of physiog­ between the Atlantic Forest and Caatinga populations,
nomic subtypes: evergreen, semi-deciduous, and open for­ and an analysis of variance (ANOVA) and a non-
ests, plus transitional areas (Veloso et al. 1991). parametric Kruskal-Wallis test to test for sexual
The Caatinga covers around 850,000 km2 in north­ dimorphism (SVL, TL, HL, and TO) within each
eastern Brazil and has a dry, tropical climate (Bw biome. We used a generalized linear model (GLM) to
according to the Köppen system of climate classifica­ test for the effects of sex and biome on SVL. We
tion). It has hot summers with unpredictable precipita­ assumed a Gaussian (or normal) distribution for the
tion that ranges between 300 and 800 mm from GLM (Tabachnick & Fidell 2007).
January to March (50–70% of precipitation restricted We analyzed stomach and gut contents using
to these months), and in some years no rain falls. It has a stereoscope and identified food items to genus level
mean annual temperatures between 26° and 28°C with if possible. The lengths and widths of intact prey were
a maximum of 42°C, and is subject to high solar measured using a digital caliper (precision = 0.01 mm)
radiation, little cloud cover, low humidity, and high to estimate the volume, based on the formula for an
evapotranspiration (Nimer 1989; Prado 2003). The ellipsoid volume (Vitt et al. 1996):
typical vegetation is xerophilous woodland that � � � �2
includes many deciduous and thorny species (Veloso 4 1 1
V ¼ π length � width ;
et al. 1991). 3 2 2
We analyzed 249 T. melanocephala individuals, 161
from the Atlantic Forest and 88 from Caatinga, from We used a Student’s t-test to determine whether
72 locations in total (Figure 1). The specimens were 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 and 44 (42 adult and two immature) males and 44 (40
forming an analysis of covariance (ANCOVA), with adult and four immature) females were from Caatinga.
SVL as a covariate. The smallest reproductive males had SVLs of 170 and
To identify the sex, we dissected the individuals and 160 mm in the Atlantic Forest and Caatinga, respec­
directly examined the gonads. We measured the length tively, and the smallest reproductive females had SVLs
and width of the right and left testicles and considered of 175 and 180 mm in the Atlantic Forest and
males with well-developed testicles and a convoluted epi­ Caatinga, respectively. No significant differences in
didymis as reproductively active (Shine 1977; Almeida- the morphological measurements were found between
Santos et al. 2014). For females, we measured the length the biomes (MANOVA: F1,213 = 5.37, P > 0.0001), and
and width of the largest follicle and all of the eggs, and there was no significant sexual dimorphism in indivi­
considered those that had vitellogenic follicles (≥5 mm) duals from the Atlantic Forest (Kruskal-Wallis test:
in the ovaries, eggs in the oviduct, or a flaccid oviduct that X2 = 0.24, df = 1.136, P= 0.62) or from Caatinga
indicated recent egg laying (Shine 1977; Almeida-Santos (ANOVA: F1,75 = 0.46, P= 0.50). Neither SVL nor TL
et al. 2014) as reproductive females. We calculated the significantly differed between males and females or
mean volume of eggs and testicles using the ellipsoid between the Atlantic Forest and Caatinga populations
volume formula described above. (GLM of SVL: F3,245 = 0.31, P = 0.27; GLM of TL:
We used a two-way ANOVA to test for differences in F3,211 = 7.14, P = 0.13).
testicle volume between the biomes, a Student’s t-test to test We dissected 154 specimens, of which 41 (27%) had
for differences in clutch size between the biomes, and an stomach or gut contents. Twenty items were impossible
ANCOVA with SVL as a covariate and biome as a factor to to identify, eight could only be identified to the Class
test for differences in egg volume between the biomes. Chilopoda, and 13 were identified to genus level. We
We log10-transformed all of the morphometric vari­ found individuals from one order
ables prior to analysis to normalize the data, and trea­ (Scolopendromorpha), two families (Scolopendridae
ted outliers according to Tabachnick and Fidell (2007). and Cryptopidae), and four genera (Scolopendra,
Statistical significance was set at α = 0.05. All of the Arthrorabdus, Otostigmus, and Cryptops) (Table 2).
statistical analyses were performed in R version 3.2.0 We found no significant difference in diet richness
(R Core Team 2015). 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
Results as a covariate) (ANCOVA: F1,8 = 0.205, P= 0.66).
Of the 249 T. melanocephala specimens revised, 80 (78 We obtained reproductive data for 61 adult males
adults and two immature) males and 81 (72 adults and and 78 adult females from the Atlantic Forest and 29
nine immature) females were from the Atlantic Forest, 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) Atlantic Forest (NS = 96)
3
Prey Item N F% V (mm ) V% N F% V (mm3) V%
Class Chilopoda
Order Scolopendromorpha
Family Cryptopidae
Cryptops 1 6.00 70 9.00 - - - -
Family Scolopendridae
Arthrorabdus - - - - 1 4.00 87.17 22.00
Otostigmus - - - - 1 4.00 27.11 7.00
Scolopendra 6 38.00 442.24 59.00 3 12.00 187.42 48.00
Unidentified
Pieces of arthropods 6 38.00 231.72 32.00 2 8.00 88.43 23.00
Digested material 3 19.00 - - 18 72.00 - -
Total 16 743.96 25 390.13

males, we found no significant difference between the one or two eggs), so sexual size dimorphism may not
volumes of the left and right testicles (Student’s t-test: be evident in all populations.
t = 1.65, df = 88, P= 0.099). Testicle volume varied in The morphological similarities of different
relation to the SVL (two-way ANOVA: F1,87 = 20.47, T. melanocephala populations could also be caused by
P > 0.0001) and between biomes (two-way ANOVA: the generalist habits exhibited by the species. Tantilla
F1,87 = 10.01, P = 0.002), but there was no significant melanocephala is nocturnal and fossorial, and can inha­
interaction between SVL and biome (two-way bit varied habitats such as primary forests, grasslands,
ANOVA: F1,86 = 2.94, P = 0.09). Regarding females, savannas, coastal environments, and even urban areas
36 individuals from the Atlantic Forest had vitellogenic (Wilson & Mata-Silva 2015). Therefore, even in con­
follicles and 21 were carrying eggs, whereas 12 indivi­ trasting biomes such as Caatinga and the Atlantic
duals from Caatinga had vitellogenic follicles and seven Forest, T. melanocephala individuals can exhibit similar
had eggs (Figure 2). Clutch size (1–2 eggs per female) ecological preferences that are reflected in similar
was similar between females from the Atlantic Forest morphologies.
and Caatinga, except for a single female Regarding feeding behavior, Otostigmus spp. and
(SVL = 290 mm; TO = 365 mm) from Caatinga that Scolopendra spp. seem to be the most frequent type of
had four eggs. We found no significant difference in prey consumed by T. melanocephalla found in
clutch size between females from the Atlantic Forest Caatinga, Atlantic Forest and Cerrado (Marques &
and those from Caatinga (Student’s t-test: t = 0.92, Puorto 1998; França et al. 2008). In addition, all of
df = 12, P= 0.37), and there was no significant differ­ the centipedes found in the snakes’ stomachs were
ence in egg volume between the biomes with female consumed head-first. Marques and Puorto (1998)
SVL as a covariate (ANCOVA: F1,24 = 0.97, P= 0.32). reported the same pattern of ingestion, suggesting
that centipedes can inflict damage, so snakes first
immobilize the prey to avoid injury (Cundall &
Discussion
Greene 2000). Tantilla melanocephala uses venom to
There were no significant morphological differences immobilize the centipede until it ceases struggling
between Tantilla melanocephala populations in (Marques & Puorto 1998). Unfortunately, head-first
Caatinga and the Atlantic Forest. The mean body size ingestion damages the prey’s head, making it impossi­
of the species found here did not differs from the ble under a stereoscope to identify many prey items to
central Brazilian Cerrado, the southeastern Atlantic the genus or family levels. Unidentified centipedes
Forest, and eastern Amazonia, and males reach sexual accounted for over 40% of all the prey items revised,
maturity at a smaller size than females in all biomes and this number was similar to unidentified items in
(Marques & Puorto 1998; Santos-Costa et al. 2006; the southeastern Atlantic Forest (Marques & Puorto
França et al. 2008). Therefore, the general morphology 1998). Also, there was no correlation between prey
of the species seems to be highly conserved. Although size and snake size, and large T. melanocephala indivi­
we found that the mean and maximum female size was duals did not necessarily eat large centipedes. We did
slightly greater than that of male size both in Caatinga not find any diet shifts caused by ontogenetic differ­
and the northeastern Atlantic Forest, the differences ences and juveniles and adults consumed the same
were not statistically significant. Tantilla melanoce­ kind of prey, as is the case in other species of Tantilla
phala does not produce large clutches (generally only (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 reproductive variation is related to different environ­
other areas of its distribution, such as Amazonia, mental conditions in the species’ geographical range. In
Chaco, and Cerrado, would elucidate the patterns of the northeastern Atlantic Forest we found eggs and
prey consumption and feeding behavior of the species. vitellogenic follicles throughout the year, indicating
Both environmental and historical factors seem to that this population has a continuous reproductive
influence reptile life history parameters (Dunham & cycle, as seen in eastern Amazonia (Santos-Costa
Miles 1985; Vitt 1992; Mesquita & Colli 2010), as et al. 2006). However, in Caatinga, eggs and vitello­
observed for T. melanocephala. The species reproduc­ genic follicles were only present between January and
tive period differed between the populations, support­ April, with one record in October, suggesting that this
ing the statement of Santos-Costa et al. (2006) that population has a seasonal reproductive cycle, as found
8 F. A. DE OLIVEIRA ET AL.

in the southeastern Atlantic Forest (Marques & Puorto Technological Development (CNPq) for a Doutorado
1998). Thus T. melanocephala shows a similar pattern Sanduíche no Exterior (SWE) scholarship [208442/2017-0].
in the reproductive period as other lizards and snakes F. G. R. França thanks CNPq for financial support [Universal
grant 404671/2016-0].
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. ORCID
2018). However, the underlying determinants of seaso­ Felipe Araújo de Oliveira http://orcid.org/0000-0002-
nal and continuous reproductive cycles in tropical rep­ 2289-7002
tiles are unknown, but are probably related to Rafaela Cândido de França http://orcid.org/0000-0001-
environmental variables such as temperature, moisture, 5034-6796
Frederico Gustavo Rodrigues França http://orcid.org/
and photoperiod (Vitt & Vangilder 1983; Pizzatto et al.
0000-0001-6989-2455
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), References
which suggests that clutch size in T. melanocephala
Ab’Saber AN. 1977. Os domínios morfoclimáticos na
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