Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
Boletín de la Sociedad Zoológica del Uruguay, 2022
Vol. 31 (1): e31.1.1
ISSN 2393-6940
We described natural history traits of the brown-
banded water snake Helicops angulatus from Eastern
Brazilian Amazon, one of the most threatened areas in
Amazonia. We recorded morphometric information,
feeding habits, and reproductive strategies from 97
mature females, 58 mature males, and 40 juveniles.
Females are larger than males, although males have
longer tail length. Females and males mature at different
sizes, with males becoming mature at smaller sizes. We
observed the presence of follicles and secondary eggs
throughout the year. However, we found two reproductive
peaks, in July and October, corresponding to the dry
season in the Amazon region. Diet consists mainly of
fishes, followed by frogs that use water bodies for
reproduction. Most prey were ingested headfirst
(82.35%), possibly to decrease risk of injuries during the
capture and ingestion. We found a positive relationship
between total length of the prey and snout-vent length of
snakes. Compared to other species, H. angulatus ingests
proportionally larger prey (22-44% of the snout-vent
length of snakes), probably optimizing energy gain.
Keywords: Biology, Diet, Neotropical, Water snake,
Oviparity, Reproduction.
Dimorfismo sexual, reproducción y biología
alimentaria de Helicops angulatus (Linnaeus, 1758)
(Colubridae: Hydropsini) en la Amazonia Oriental,
Brasil. Describimos los rasgos de la historia natural de la
serpiente de agua de bandas marrones Helicops
angulatus de la Amazonia oriental brasilera, una de las
áreas más amenazadas de la Amazonia. Registramos
información morfométrica, hábitos de alimentación y
estrategias reproductivas de 97 hembras maduras, 58
machos maduros y 40 juveniles. Las hembras son más
grandes que los machos, aunque los machos tienen
mayor largo de cola. Hembras y machos maduran con
diferentes tamaños, los machos maduran con tamaños
más pequeños. Observamos la presencia de folículos y
huevos secundarios durante todo el año. Sin embargo,
encontramos dos picos reproductivos, en julio y octubre,
correspondientes a la estación seca en la región
amazónica. La dieta consiste principalmente en peces,
seguida de ranas que utilizan cuerpos de agua para
reproducirse. La mayoría de las presas fueron ingeridas
de cabeza (82.35%), posiblemente para disminuir el
riesgo de lesiones durante la captura e ingestión.
Encontramos una relación positiva entre la longitud total
de la presa y la longitud hocico-respiradero de las
serpientes. En comparación con otras especies, H.
1,7* 3
Maria Cristina dos Santos-Costa , Pedro Santos Abe , Luiz Paulo Printes Albarelli ,
4,7 5 5
Ana Lúcia da Costa Prudente , Leandra Cardoso Pinheiro , Youszef Oliveira da Cunha Bitar
and Gleomar Fabiano Maschio
1 Laboratório de Ecologia e Zoologia de Vertebrados, Instituto de Ciências Biológicas, Universidade Federal do
Pará. Caixa Posta 419, CEP: 66075-110, Belém, Pará, Brazil.
2 Empresa Brasileira de Infraestrutura Aeroportuária. CEP: 64.006-010, Teresina, Piauí, Brazil.
3 Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Caixa Postal 09566, CEP: 66087-
441, Belém, Pará, Brazil.
4 Coordenação de Zoologia, Museu Paraense Emílio Goeldi. Caixa Posta 399, CEP: 66077-830, Belém,
Pará, Brazil.
5 Campus Universitário do Marajó-Soure, Universidade Federal do Pará. CEP: 68870-000, Soure, Pará, Brazil.
6 Instituto de Ciências Biológicas, Educação à Distância, Universidade Federal do Pará. Caixa Posta 419, CEP:
66075-110, Belém, Pará, Brazil.
7 Programa de Pós-Graduação em Zoologia, Universidade Federal do Pará e Museu Paraense Emílio Goeldi,
Caixa Posta 419, CEP: 66075-110, Belém, Pará, Brazil.
*Corresponding author:
Fecha de recepción: 24 de marzo de 2021
Fecha de aceptación: 07 de octubre de 2021
angulatus ingiere presas proporcionalmente más grandes
(22-44% de la longitud del hocico-respiradero de las
serpientes), probablemente optimizando la ganancia de
Palabras clave: Biología, Dieta, Neotropical,
Serpiente de agua, Oviparidad, Reproducción.
A key factor to understand evolutionary processes,
ecological adaptations, and furthermore conservation
status of snakes lays on the knowledge of their natural
history (Greene and Losos, 1988; McCallum and
McCallum, 2006). Breeding and feeding behavior are
the most investigated aspects of natural history in
snakes, which may be used in different studies such as
functional traits, phylogeny, biogeography, etc.
Although the number of studies focused on natural
history has grown in recent years, the Amazon region
still has many gaps in knowledge related to different
organisms, including snakes. This gap is mainly related
to difficulties in accessing areas farther from urban
centers, lack of investment in basic research and few
human resources. Thus, it is common to carry out
studies with animals that are already available in
scientific collections, and thus carry out studies with the
information that is added to each collected animal
(Marinoni and Peixoto, 2010).
Snakes show morphological and behavioral
adaptations that allowed, over time, their irradiation in
different environments, both terrestrial and aquatic.
The elongated body and the absence of limbs make the
snakes agile and capable of occupying a great diversity
of microhabitats, being able to prey on a wide variety of
items. In addition, the kinetic head allows the ingestion
of relatively large prey (Greene, 1983; Cundall and
Greene, 2000; Santos et al., 2016; Silva et al., 2017a).
Some taxa differ in their habits, especially when it
comes to breeding and feeding activity (Pizzatto,
Jordão and Marques, 2008; Alencar, Gaiarsa and
Martins, 2013; Silva, Oliveira, Nascimento, Machado
and Prudente, 2017b). This information may be
important to understand, for example, how those
behaviors vary and how they affect the species
distribution (Santos-Costa, Prudente and Di-Bernardo,
2006; Albarelli and Santos-Costa, 2010; Siqueira,
Nascimento and Santos-Costa, 2012; Nascimento,
Siqueira and Santos-Costa, 2013; Siqueira,
Nascimento, Montingelli and Santos-Costa, 2013).
The South American aquatic snake genus Helicops
(Wagler, 1830), has nineteen species and is distributed
almost everywhere found in South America, being
recorded in Venezuela, Colombia, Bolivia, Peru,
Guyana, Suriname, French Guiana, Trinidad, Ecuador,
Uruguay, Argentina, Paraguay, and Brazil (Duellman,
1978; Cunha and Nascimento, 1993; Uetz, Freed and
Hosek, 2021). Most species prey on fishes, frogs
(adults and tadpoles) and semi-aquatic lizards (Martins
and Oliveira, 1998; Ford and Ford, 2002, Aguiar and Di-
Bernardo, 2004, Ávila and Arruda, 2006, Sturaro and
Gomes, 2008, Santos-Costa, Maschio and Prudente,
2015; Teixeira, Montag and Santos-Costa, 2017).
There are thirteen viviparous species of Helicops,
with continuous or seasonal reproductive cycles (Ford
and Ford, 2002; Aguiar and Di-Bernardo, 2005; Ávila,
Ferreira and Arruda, 2006; Costa, Santana, Leal,
Koroiva and Garcia, 2016), three oviparous species (H.
hagmanni Roux, 1910, H. pastazae Shreve, 1934, and
H. gomesi Amaral, 1921), and a single species (H.
angulatus) with a bimodal reproductive pattern.
Specimens of Helicops angulatus are found in
Amazon Basin, Chititano Dry Forest, Cerrado,
Caatinga and in the northern portion of the Atlantic
Forest, mostly at low elevations (Nogueira et al., 2019).
They can be found in aquatic environments, as ponds,
rivers, streams and dams, in both forested and open
areas (Cunha and Nascimento, 1993; Martins and
Oliveira, 1998; Ford and Ford, 2002; Santos-Costa et
al., 2015). Oviparous populations of this species occur
from northern to northeastern and eastern South
America, while viviparous populations are found from
northwestern to mid-western South America (Cunha
and Nascimento, 1981; Dixon and Soini, 1983;
Rossman, 1984; Braz, Scartozzoni and Almeida-
Santos, 2016).
Herein, we describe some natural history traits of
Helicops angulatus from different locations in the
eastern Brazilian Amazon, providing information on
their reproduction (sexual dimorphism, reproductive
maturity, and reproductive seasonality) and feeding
habits (diet composition, frequency of food items,
relationship between predator and prey sizes).
We analyzed 195 Helicops angulatus preserved
specimens (97 mature females, 58 mature males, and
40 juveniles) from the Herpetological Collection of
Museu Paraense Emílio Goeldi (Appendix I).
Specimens were collected in Eastern Amazon
(Brazilian State of Pará) in 15 sites located between
o o o o
5 00” and 0 00” S and 55 00” and 44 00” W (Fig. 1).
Local climate is hot-humid throughout the year in all 15
sampled sites (AFi according to Köppen
classification), with a marked dry season between June
and November (mean rainfall: 88 mm) and a marked
rainy season between December and May (mean
rainfall: 300 mm) (Albuquerque, Souza, Oliveira and Jr.
Souza, 2010). Mean annual temperature varies
between 23 and 27 °C, and the mean air relative
humidity is around 85% (CPTEC / INPE, 2013). All
localities here addressed were originally covered by
tropical rainforest, but, currently, many of them exhibit
high deforestation rates, driven by the expansion of
agricultural frontiers, road construction, among others
Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
3Natural history of Helicops angulatus
human interventions (Peres et al., 2010; Vieira and
Almeida, 2013). Climate changes caused by
deforestation have increased the dry periods in the
Amazon Basin, affecting organisms associated with
aquatic environments, including aquatic snakes such
as H. angulatus (Ruiz-Vásquez, Arias, Martínez and
Espinoza, 2020).
For each specimen, we collected the following
measurements (in millimeters): snout–vent length
(SVL), tail length (TL), number of ventral scales (VS)
and number of subcaudal scales (ScS). The data was
log-transformed in order to deal with the assumptions
of normality and homogeneity of variance beyond the
homogeneity of inclination (parallelism) and to test the
interaction between the factor (sex) and covariates
(SVL). We tested normal distribution using the
Kolmogorov-Smirnov test, and tested the homogeneity
of variance using F test (Fisher). This data was used to
test sexual dimorphism in body and tail size of H.
angulatus. We used one-way analysis of covariance
(ANCOVA), with sex as factor and SVL as a covariate to
analyze sexual dimorphism in TL measures (see
Maschio et al., 2021). We analyzed sexual dimorphism
in the VS and ScS using Bartlett test (Bartlett, 1937).
For samples with normal and homogeneous
distribution, we used Student's T test, while for samples
with normal distribution, but no homogeneity of
variances, we used Welch's T test (Welch, 1958;
Zimmerman and Zumbo, 1993). All analyses were ran
using statistical R package version 2.15.1 (R
Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
Fig. 1. Collection localities of the specimens of Helicops angulatus examined for this study (black dots), Eastern Amazon,
Pará, Brazil.
Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
Table 1. Measures of mature females and males of H. angulatus in Eastern Amazon, Pará, Brazil, showing the number of specimens
examined (n), mean, standard deviation (SD) and minimum (MIN) and maximum (MAX) sizes. Legend: SVL = snout–vent length; TL =
tail length; VS= number of ventral scales and ScS = number of subcaudal scales. *specimens with damaged tail were excluded.
Mature females Mature males
SVL (mm) 97 474.0 75.7 336 676 58 343.0 44.0 228 442
TL (mm)* 85 217.6 37.4 136 344 44 213.0 43.0 111 319
VS 79 112.2 3.4 101 123 35 107.1 3.8 99 115
ScS* 79 74.5 5.7 56 89 35 87.1 6.0 73 101
Fig. 2. Percentage of sexually
immature and mature males (A) and
females (B) of Helicops angulatus from
the Eastern Amazon, Pará, Brazil,
species according to size classes.
Black = immature, grey = mature.
5Natural history of Helicops angulatus
Development Core Team; http://,
with 0.05 significance level (α).
We analyzed sexually mature individuals from
every month of the year to unveil if reproduction occurs
throughout the year (no seasonality) or if it is restricted
to a specific period (seasonally adjusted).
Furthermore, we used the following data to determine
in which size males and females become mature: size
of the largest ovarian follicle or oviductal egg; number
of vitellogenic follicles (> 10 mm) or oviductal eggs to
estimate fecundity; maximum diameter of a deferent
duct at its distal end close to the cloaca (Almeida-
Santos et al., 2006); and testicle length and width (all to
the nearest 0.1 mm). Size at sexual maturity for
females was Welch's based on the smallest (SVL)
female with vitellogenic follicles or oviductal eggs and
oviducts enlarged (Shine, 1977). Males were
considered mature when they had enlarged and turgid
testicles, and thickened convoluted deferent ducts
(Shine, 1988; Almeida-Santos, Pizzatto and Marques,
2006). Specimens with umbilical scar were considered
newborn (Santos-Costa et al., 2006). We performed an
analysis of the reproductive cycle from adult
specimens, observing the temporal distribution of eggs
in the oviduct using circular analysis. For this analysis,
we used software ORIANA version 4 (Kovach, 2016).
To analyze prey consumption by H. angulatus, we
made an abdominal incision in 170 specimens and
removed all prey items in the stomach and/or intestine
(if present). We obtained information on ecological prey
through literature. We recorded how prey were
ingested according to the position of the head in the
stomach of the snake (headfirst or tail first). Whenever
possible, we measured all the prey ingested by H.
angulatus. When prey was fish, we measured the
distance from rostrum to tail fin, while for frogs and
lizards we measured snout-cloaca distance. We tested
the correlation between prey and snakes' length with a
Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
Table 2. Prey frequencies of Helicops angulatus from Eastern Amazon, State of Pará, Brazil.
Snakes with prey items Prey frequency
Prey taxa n % n %
Crenicichla sp. 1 5.9 2 8
Apistogramma sp. 2 11.7 3 12
Aequidens sp. 1 5.9 1 4
Corydoras sp. 1 5.9 1 4
Species unknow 1 5.9 1 4
Cyphocharax sp. 1 5.9 2 8
Hoplias malabaricus 1 5.9 1 4
Species unknow 1 5.9 1 4
Gymnotus sp. 3 17.6 3 12
Copella sp. 1 5.9 4 16
Pyrrhulina sp. 1 5.9 3 12
Rhinella gr. margaritifera 1 5.9 1 4
Boana boans 1 5.9 1 4
Adenomera sp. 1 5.9 1 4
TOTAL 1 7 2 5
Pearson's correlation test. For prey in advanced stage
of decomposition, we compared with three similar-
sized specimens from the same species deposited in
the herpetological collection of Museu Paraense Emílio
Goeldi (see Prudente, Menks, Silva and Maschio,
The smallest mature female was 336 mm SVL,
whereas the smallest mature male was 228 mm SVL
(Table 1). Males (SVL mean = 343 mm) became
sexually mature with SVL smaller than females (SVL
mean = 474 mm) (t = 12.015, F = 2.9684, P <0.0001,
N female = 97; N male = 58). In addition, mature
males had significantly higher tail sizes than mature
females (Parallelism 1.125 f = 3.053 and P = 0.083,
ANCOVA f = 46.133 and P <0.001).
1, 126
We observed that 97% of males became sexually
mature with SVL greater than 301 mm (Fig. 2A), while
93% of females became sexually mature with SVL
greater than 351 mm (Fig. 2B). We also observed that
approximately 50% of males were already sexually
mature at length class ranging between 251 and 300
mm, while no females were mature at that same range
size (Fig. 2A–B). Larger mature male SVL was 442
mm, while larger mature female SVL was 676 mm,
supporting the existence of sexual bi-maturity in H.
We recorded 19 females with eggs throughout the
year (March: N = 3; April: N = 1, June: N = 2; July: N = 5;
September: N = 1, October: N = 5; November: N = 1;
December: N= 1). Two females found in March had
embryos at early development stage. We found two
reproductive peaks: in July and October, during dry
season in Amazon (Fig 3). Juveniles were observed in
almost every month of the year: March (N = 5), April (N
= 2), May (N = 2), June (N = 1), July (N = 5), September
(N = 3), October (N = 11), November (N = 5) and
December (N = 6). In addition, we did not observe any
difference between number of vitellogenic follicles and
number of eggs (Mann-Whitney U = 107.0, Z = 1.5, P =
0.29, N = 40).
From the 170 Helicops angulatus specimens, 17
(10%) had any prey item in the stomach, with fishes
representing 82.4% and frogs representing 17.7%
(Table 2). We identified nine fish species, distributed in
six families. From the 25 prey identified, most were
ingested headfirst (N = 14; 56%), while only 12% were
ingested tail first (N = 3). In eight cases (32%), we were
not able to identify if the head or tail was ingested first
due to advanced stage of decomposition. Prey total
length corresponded to 22% to 44% of the snout-vent
length of the snakes, suggesting that H. angulatus
tends to feed on proportionately large prey. In addition,
we found a positive relationship between prey total
length and snakes snout-vent length, Pearson
Correlation, r = 0.61, P = 0.02 (Fig. 4).
Our results confirm the oviparity in Helicops
angulatus populations of the eastern Amazon, as
suggested by Braz et al. (2016), who found
Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
Fig. 3. Egg distribution over the seasonal
period of Helicops angulatus, Eastern
Amazon, Pará, Brazil.