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

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.

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

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,

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

Bol. Soc. Zool. Uruguay (2ª época). 2022. Vol. 31 (1): ISSN 2393-6940e31.1.1

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.

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