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
https://journal.szu.org.uy
DOI: https://doi.org/10.26462/31.1.1
ABSTRACT
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.
RESUMEN
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.
SEXUAL DIMORPHISM, REPRODUCTION AND FEEDING BIOLOGY OF Helicops angulatus (LINNAEUS,
1758) (COLUBRIDAE: HYDROPSINI) IN EASTERN AMAZON, BRAZIL
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
6,7
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: mcsc64@gmail.com
Fecha de recepción: 24 de marzo de 2021
Fecha de aceptación: 07 de octubre de 2021
2
2
SANTOS-COSTA ET AL.
angulatus ingiere presas proporcionalmente más grandes
(22-44% de la longitud del hocico-respiradero de las
serpientes), probablemente optimizando la ganancia de
energía.
Palabras clave: Biología, Dieta, Neotropical,
Serpiente de agua, Oviparidad, Reproducción.
INTRODUCTION
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).
MATERIALS AND METHODS
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.
SANTOS-COSTA ET AL. 4
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
nMean SD MIN MAX nMean SD MIN MAX
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.
A
B
5Natural history of Helicops angulatus
Development Core Team; http:// www.R-project.org),
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 %
FISHES
Cichlidae
Crenicichla sp. 1 5.9 2 8
Apistogramma sp. 2 11.7 3 12
Aequidens sp. 1 5.9 1 4
Callichthyidae
Corydoras sp. 1 5.9 1 4
Species unknow 1 5.9 1 4
Curimatidae
Cyphocharax sp. 1 5.9 2 8
Erythrinidae
Hoplias malabaricus 1 5.9 1 4
Species unknow 1 5.9 1 4
Gymnotidae
Gymnotus sp. 3 17.6 3 12
Lebiasinidae
Copella sp. 1 5.9 4 16
Pyrrhulina sp. 1 5.9 3 12
FROGS
Bufonidae
Rhinella gr. margaritifera 1 5.9 1 4
Hylidae
Boana boans 1 5.9 1 4
Leptodactylidae
Adenomera sp. 1 5.9 1 4
TOTAL 1 7 2 5
SANTOS-COSTA ET AL.
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,
2014).
RESULTS
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.
angulatus.
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).
DISCUSSION
Our results confirm the oviparity in Helicops
angulatus populations of the eastern Amazon, as
suggested by Braz et al. (2016), who found
6
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.
reproductive bimodality, a rare phenomenon in snakes.
Populations from North, Mid-East and Northeast
regions of South America are oviparous, while
populations from Northwest to Mid-West of South
America are viviparous (Braz et al., 2016). Some
hypotheses suggest that viviparous condition may
have arisen during unfavorable environmental
scenarios, leading to the retention of embryos in
periods of low temperatures, lack of resources and
large predatory pressure (Seigel and Ford, 1987;
Shine, 1995).
Unlike other biomes, climate seasonality is not
observed in most of the Amazon, with little variation in
air temperature and humidity throughout the year, and
a wide availability of aquatic environments, supporting
a wide supply of prey (Duellman, 1978; Santos-Costa
et al., 2015). In aquatic environments, seasonal
variation in food availability is low when compared to
terrestrial environments (Junk, Bayley and Sparks,
1989). With the rise of the water level during rainy
seasons, there is a natural expansion in the area of
water bodies, increasing habitat availability for fishes
and reducing their density because of their dispersion.
However, with the decrease of water level during dry
season, there occurs a reduction in the area of water
bodies, reducing habitat availability for fishes and
increasing their density (see Okada, Agostinho,
Petrere and Penczak, 2003; Luz-Agostinho et al.,
2009). Such variation on water level probably affects
aquatic snakes that consume mainly fishes (Starace,
1998; Lopez and Giraudo, 2003; Ávila et al., 2006), as
Eunectes murinus (Linnaeus, 1758), Hydrodynastes
gigas (Duméril, Bibron and Duméril, 1854), Helicops
leopardinus (Schlegel, 1837), and Helicops angulatus.
One explanation to the absence of a well-defined
reproductive season is the continuous availability of
food throughout the year. Aquatic environments and
their surroundings, where H. angulatus mainly inhabits,
provide higher fish availability during dry season
(Montag, Freitas, Wosiacki and Barthem, 2008;
Castello, Isaac and Thapa, 2015) and greater frog
availability during rainy season (Duellman, 1978; Hödl,
1990).
We observed that H. angulatus mature females are
larger than males (snout-vent length), although males
become mature at smaller sizes, confirming what
seems to be a common condition for the Tribe
Hydropsini (Ford and Ford, 2002; Aguiar and Di-
Bernardo, 2005; Ávila et al., 2006). This pattern may be
considered an evolutionary advantage for some
groups of snakes, because with a larger internal space,
individuals may store more energy reserves (Bonnet,
Shine, Naulleau and Vacher-Vallas, 1998), which is
considered essential for the viability and larger storage
of eggs and/or embryos (Shine, 1978; King, 2000).
In fact, high fecundity was observed in H.
angulatus, as well as in other Helicops, as H.
infrataeniatus Jan, 1875 (Aguiar and Di-Bernardo,
2005) and H. leopardinus (Schlegel, 1837) (Ávila et al.,
2006). Although H. angulatus females are larger, males
have a proportionally larger tail, as in many other
species of snakes, which is a relatively common
7Natural history of Helicops angulatus
Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1
Fig. 4. Relationship between snout-vent length (SVL in mm) and total prey length (in mm) found in Helicops angulatus,
2
Eastern Amazon, Pará, Brazil. (R = 0.3775).
Total prey length
pattern in Serpentes (Shine, 1993; Shine et al., 1999).
Greater length of the tail in males may also provide
greater ability of movement, decreasing the metabolic
costs to maintain their body (Anderson, 1994).
We observed a higher number of females with eggs
during the dry season (11 eggs from July to October),
and identified two reproductive peaks: one in early dry
season (June and July) and other in late dry season
(October). Some studies indicate that continuous
reproductive cycle is a common pattern for tropical
snakes (Santos-Costa et al., 2006; Siqueira et al.,
2012; Nascimento et al., 2013). However, recent
studies show that some species may present seasonal
reproduction, as Anilius scytale (Linnaeus, 1758)
(Maschio, Prudente, Lima and Feitosa, 2007) and
Drymarchon corais Boie, 1827 (Prudente et al., 2014)
or two annual reproductive cycles, as observed in
Imantodes cenchoa Linnaeus, 1758 (Souza, Prudente
and Maschio, 2014). These findings suggest that, in
addition to historical factors, also contemporary
factors, such as environmental conditions and
behavioral traits may play an important role on the
snake's reproductive strategies (Cadle and Greene,
1993). Helicops angulatus feeds primarily on fishes
that forage at the bottom of lentic water bodies (Godoy,
1975; Isaac, Guidelly, França and Pavanelli, 2004;
Teixeira et al., 2017), as Gymnotus, Copella,
Apistogramma, Cyphocharax, Aequidens, Crenicichla,
Corydoras and Hoplias juveniles. However, H.
angulatus shows a wider diet range, capturing
terrestrial frogs that build foam nests in leaf litter, as
Adenomera sp., or frogs that lay eggs directly into the
water, as Rhinella gr. margaritifera (Laurenti, 1768)
(terrestrial) and even the tree frog Boana boans
(Linnaeus, 1758) that lay eggs in temporary ponds
(Duellman, 1978; Kwet and Di-Bernardo, 1999; Bartlett
and Bartlett, 2003). Based on the behavior of anurans
and studies on foraging habitats, it is probable that
Helicops angulatus forages primarily into the water and
eventually on the ground (Teixeira et al., 2017). Similar
behavior was observed for H. infrataeniatus and H.
leopardinus, which also capture terrestrial frogs
(Aguiar and Di-Bernardo, 2004; Ávila et al., 2006).
H. angulatus captured relatively large prey
(22–44% of the snake's size), in contrast to what is
observed in H. infrataeniatus, which ingests smaller
prey (5–15% of its length) (Aguiar and Di-Bernardo,
2004). This feeding behavior can vary within the genus
Helicops, indicating that it is not a conservative
characteristic for the group. In our study, we observed
that the environments where H. angulatus was found
present a diversity of prey (fish and frogs) with different
sizes, and that capturing larger prey would be more
advantageous to maximize foraging efficiency (see
Mushinsky, 1987; Ávila et al., 2006). This pattern also
explains why H. angulatus captures their prey mainly
headfirst, since it reduces the risk of injury caused
especially by fishes with lateral and dorsal fins. Pinto
and Lema (2002) observed two species of captive
snakes and concluded that capturing prey headfirst
reduces time and effort during swallowing, the amount
of energy spent, vulnerability period and risk of injuries
caused by their prey (Maschio, Prudente, Rodrigues
and Hoogmoed, 2010; Prudente et al., 2014; Souza et
al., 2014).
Detailed investigation on feeding habits and
reproductive characteristics of Helicops angulatus, as
well as information on the biology of other snakes, may
support studies on the functioning of populations and
communities in tropical environments. In addition, this
information may be useful to support co-evolutionary
studies, since food preferences and reproductive
strategies of a given species may be either related to
the environment where it lives (environmental
response, e.g., environmental filtering, niche
divergence) or to a shared evolutionary history,
especially in the case of phylogenetically related
species, e.g., Hydropsini (evolutionary response, e.g.,
niche conservation). Finally, data on the reproduction
of Helicops angulatus may be supplemented with the
analysis of gonads through techniques of scanning
electron microscopy, providing more detailed
information on the reproductive cycle of this species
that we could not observe in this study.
ACKNOWLEDGEMENTS
We are grateful to Museu Paraense Emílio Goeldi
for granting access to the specimens examined. We
wish to thank Sistema Nacional de Pesquisa em
Biodiversidade (SISBIOTA Brasil, CNPq, process
563355 / 2010-7) and Programa de Pesquisa em
Biodiversidade (PPBio) for financial and logistical
support. We thank Wolmar Wosiacki and Luciano
Montag for identifying the fish species, to CNPq for the
concession of a Master's scholarship grants to P.S.A.
Capes supported this project with a doctorate
scholarship grants to LCP and YOCB. ALCP was
supported by Conselho Nacional de Desenvolvimento
Científico e Tecnológica (Process Pq 305475/2014-2;
PROTAX 44.0413/2015-0).
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Editor de Sección: Raúl Maneyro
11 Natural history of Helicops angulatus
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Appendix I.
Accession numbers of Herpetological Collection of
Museu Paraense Emílio Goeldi. Helicops angulatus.
Brazil: Pará: Ananindeua: MPEG 18942, MPEG
19830 Augusto Correa: MPEG 548, MPEG 567,
MPEG 651, MPEG 669, MPEG 2355, MPEG 3895,
MPEG 4592, MPEG 5333, MPEG 5334, MPEG 5347,
MPEG 5352, MPEG 5353, MPEG 6455, MPEG 6538,
MPEG 6675, MPEG 67311, MPEG 10003, MPEG
10731, MPEG 12470, MPEG 10739, MPEG 10741
Belém: MPEG 17313, MPEG 18557, MPEG 18758,
MPEG 19586, MPEG 19718, MPEG 19594
Benevides: MPEG 20155 Bragança: MPEG 3007,
MPEG 7861, MPEG 8329, MPEG 8331, MPEG 8332,
MPEG 8361, MPEG 8363, MPEG 9968, MPEG 11335,
MPEG 11386, MPEG 11387, MPEG 12998, MPEG
17311. Castanhal: MPEG 1536, MPEG 4038, MPEG
4039, MPEG 4040, MPEG 4400, MPEG 4410, MPEG
4773, MPEG 7170, MPEG 8651, MPEG 10775, MPEG
11791, MPEG 12470, MPEG 12608, MPEG 12999.
Mãe do Rio: MPEG 18677. Marabá: MPEG 17053,
MPEG 17081, MPEG 18880, MPEG 19365, MPEG
19366, MPEG 19367, MPEG 19368, MPEG 19369
Maracanã: MPEG 1583, MPEG 1584, MPEG 1885,
MPEG 1886, MPEG 2091, MPEG 2408, MPEG 2409,
MPEG 2557, MPEG 2558, MPEG 2783, MPEG 2784,
MPEG 2785, MPEG 2786, MPEG 2787, MPEG 2789,
MPEG 2803, MPEG 3336, MPEG 3396, MPEG 4076,
MPEG 4079, MPEG 4843, MPEG 4854, MPEG 5796.
Ourém: MPEG 4220, MPEG 4993, MPEG 4996,
MPEG 5007, MPEG 5010, MPEG 5011, MPEG 7000,
MPEG 7002, MPEG 7025, MPEG 7026. Santarém:
MPEG 19052. Santarém Novo: MPEG 1842, MPEG
1843, MPEG 3244, MPEG 3245, MPEG 4139, MPEG
4140, MPEG 4148, MPEG 4150, MPEG 4152, MPEG
7054, MPEG 7073. São Domingos do Capim: MPEG
8062. São Miguel do Guamá: MPEG 20987, MPEG
20988, MPEG 21006, MPEG 21007.Viseu: MPEG
1030, MPEG 1043, MPEG 1049, MPEG 1050, MPEG
1051, MPEG 1052, MPEG 1060, MPEG 1352, MPEG
2308, MPEG 2309, MPEG 2310, MPEG 2311, MPEG
2312, MPEG 2314, MPEG 2315, MPEG 3077, MPEG
3079, MPEG 3080, MPEG 3081, MPEG 3082, MPEG
3084, MPEG 3086, MPEG 3088, MPEG 3754, MPEG
3755, MPEG 4500, MPEG 4502, MPEG 5285, MPEG
5286, MPEG 5291, MPEG 5302, MPEG 6570, MPEG
6576, MPEG 6577, MPEG 6578, MPEG 8873, MPEG
8872, MPEG 8875, MPEG 8876, MPEG 10013, MPEG
10018, MPEG 10071, MPEG 10073, MPEG 10078,
MPEG 10888, MPEG 13247, MPEG 13248, MPEG
13249, MPEG 13250, MPEG 13251, MPEG 13252,
MPEG 13340, MPEG 13899, MPEG 13900, MPEG
13901, MPEG 13903, MPEG 13904, MPEG 14009,
MPEG 14010, MPEG 14011, MPEG 14012, MPEG
14013, MPEG 14457, MPEG 14459, MPEG 14461,
MPEG 15070, MPEG 15071, MPEG 15072, MPEG
15073, MPEG 15074, MPEG 15075, MPEG 15076,
MPEG 15338, MPEG 15711, MPEG 15787, MPEG
15858, MPEG 16010, MPEG 16310, MPEG 16311.
12
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