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.