Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

Morphological aspects of Sticholecitha serpentis

(Plagiorchiida: Plagiorchiidae) in a new Viperidae host

in the Brazilian Amazon

Darlison Chagas-de-Souza1,2; https://orcid.org/0000-0002-7610-9665

Tássio Alves Coêlho1*,2; https://orcid.org/0000-0002-0264-4526

Ricardo Bassini-Silva3,4; https://orcid.org/0000-0002-9568-4120

Francisco Lazameth Ishiguro5; https://orcid.org/0000-0003-3972-6434

Hipócrates de Menezes Chalkidis5; https://orcid.org/0000-0002-7466-9669

Lúcio André Viana1,2; https://orcid.org/0000-0002-0932-0479

Lincoln Lima Corrêa6; https://orcid.org/0000-0002-6453-4824

1. Programa de Pós-Graduação em Biodiversidade Tropical (PPGBIO), Universidade Federal do Amapá, Macapá,

Amapá, Brazil; darlisondcs@hotmail.com, coelho.tassio@gmail.com (*Correspondence), lucviana74@gmail.com

2. Laboratório de Estudos Morfofisiológicos e Parasitários (LEMP), Departamento de Ciências Biológicas e da Saúde,

Universidade Federal do Amapá, Macapá, Amapá, Brazil

3. Laboratório de Coleções Zoológicas, Instituto Butantan, 05345-040, São Paulo, Brazil; ricardo.bassini@gmail.com

4. Departamento de Patologia, Reprodução e Saúde Única (DPRSU), Faculdade de Ciências Agrárias e Veterinárias,

Universidade Estadual Paulista “Júlio de Mesquita Filho”, 14884-900 Jaboticabal, São Paulo, Brazil

5. Centro Universitário da Amazônia (UNAMA), 68010-200, Santarém, Pará, Brazil; franciscolazameth@gmail.com,

hchalkidis@gmail.com

6. Instituto de Ciências e Tecnologia das Águas (ICTA), Universidade Federal do Oeste do Pará, 68015-110, Santarém,

Pará, Brazil; lincorre@gmail.com

Received 09-III-2024. Corrected 17-VI-2024. Accepted 10-IX-2024.

ABSTRACT

Introduction: Sticholecitha serpentis is a poorly studied parasite of the snakes’ esophagus, with an unclear tax-

onomy. Currently, there are few records of S. serpentis in snakes in Brazil. Although it has been recorded in snakes

of the family Viperidae, it has not yet been reported in Bothrops atrox.

Objectives: To present new morphological characters, as well as ecological and parasitic relationships of S. ser-

pentis with B. atrox.

Methods: The samples were obtained in a dryland area in the Tapajós National Forest, Pará State, Brazil. Ten

specimens of B. atrox were examined manually with the aid of tweezers, and three were positive for trematodes

identified as S. serpentis in the oral cavity.

Results: We provide scanning electron microscopy images, with detailed images of the S. serpentis tegument and

its spines, as well as details of the dorsal keel using light microscopy methods. Moreover, we report the first record

of S. serpentis parasitizing an Amazonian viperid, with infection frequency data of 30 %.

Conclusion: We emphasize that the new morphological data presented in this manuscript provide additional

information to facilitate the identification of this trematode in future studies.

Key words: snakes; Bothrops atrox; Trematoda; new morphological aspects.

https://doi.org/10.15517/rev.biol.trop..v72i1.58870

TERRESTRIAL ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

INTRODUCTION

The Amazon viper or the common lance-

head, Bothrops atrox (L., 1758) (Squamata:

Viperidae), is medium size and slightly robust

snake (Fraga et al., 2013; Monteiro et al., 2020).

This species can be differentiated from other

species of snakes by having a spear-shaped

head, with an olive-green color, uniform or

slightly darker comparing with its body, gener-

ally without spots (Da Silva et al., 2017). Besides

that, B. atrox presents a dark-brown post-

orbital line starting located on the eyes to the

sides of the oral cavity, covering the last three

supralabial scales, showing a golden bronze iris

color (Fraga et al., 2013; Monteiro et al., 2020).

This snake has a wide distribution in the

Neotropical region, inhabiting the Andes in

Colombia, and other South American coun-

tries, such as Ecuador, Peru, Bolivia, Guyana,

Surinam, and Brazil, in an altitudinal range

from the sea level to 1 200 meters (Fraga et

al., 2013; Da Silva et al., 2017). Also, B. atrox is

predominantly nocturnal, but daytime activi-

ties are not uncommon (Egler et al., 1996). The

diet includes invertebrates, fish, amphibians,

reptiles, and small mammals (Bisneto & Kae-

fer, 2019). Recent studies regarding the biol-

ogy of this species, reveal that their juveniles

are arboreal and feed on ectodermal prey,

while the terrestrial adults feed on endothermic

prey, being possible that these preys may be

intermediate hosts for endoparasites, such as

nematodes and trematodes (Fraga et al., 2013;

Rodrigues et al., 2016).

Currently, there are 150 valid species of

parasitic trematodes of reptiles in South Amer-

ica, with 112 species recorded to the Brazilian

territory (Kohn & Fernandes, 2014). These

parasites can be found in various sites of infec-

tion in reptiles, and specifically, into the Pla-

giorchiidae, they have been recorded from the

intestine, lungs, tongue, trachea, esophagus,

stomach, ureters, kidney, rectum, cloaca, oral

cavity, oviduct, liver, heart, spleen, and mesen-

tery (Kohn & Fernandes, 2014).

Sticholecitha serpentis Prudhoe, 1949

(Trematoda: Plagiorchiidae), the only species

of the genus, described in Surinam in the

esophagus of the snake Chironius carinatus

L., 1758 (Squamata: Colubridae), is a poorly

known parasite with an unclear taxonomy.

This species has also been reported in Bothrops

moojeni Hoge, 1966 (Squamata: Viperidae) and

Xenodon severus (L., 1758) (Squamata: Colubri-

dae), both from São Paulo state, in Brazil (Kohn

& Fernandes, 2014).

RESUMEN

Aspectos morfológicos de Sticholecitha serpentis (Plagiorchiida: Plagiorchiidae)

en un nuevo hospedero de Viperidae en la Amazonia brasileña

Introducción: Sticholecitha serpentis es un parásito del esófago de serpientes poco estudiado y su sistemática no

está clara. Actualmente, existen pocos registros del parásito en serpientes en Brasil. Aunque ha sido registrada en

serpientes de la familia Viperidae, aún no ha sido reportada en Bothrops atrox.

Objetivos: Presentar novedades en aspectos morfológicos, relaciones ecológicas y parasitarias de S. serpentis,

parásito encontrado por primera vez en la cavidad bucal de B. atrox.

Métodos: Las muestras provienen de un área seca en la Floresta Nacional de Tapajós, Estado de Pará, Brasil. Diez

especímenes de B. atrox fueron examinados manualmente con la ayuda de pinzas. De estos individuos tres fueron

positivos para trematodos compatibles con S. serpentis en la cavidad oral.

Resultados: Se proporcionan imágenes de microscopía electrónica de barrido, con imágenes del tegumento de S.

serpentis y sus espinas, y detalles de la quilla dorsal mediante métodos de microscopía óptica. Además, se reporta

el primer registro de parasitismo por S. serpentis en un vipérido amazónico, con datos de frecuencia de infección

del 30 %.

Conclusión: Los nuevos datos morfológicos presentados en este manuscrito proporcionan información adicional

para facilitar la identificación de este tremátodo en futuros estudios.

Palabras clave: serpientes; Bothrops atrox; Trematoda; nuevos aspectos morfológicos.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

Currently, there are different studies about

the morphology of S. serpentis already high-

lighted by Prudhoe (1949), Artigas and Perez

(1969), Corrêa et al. (1990), Da Silva et al.

(1999), Silva and Barrella (2002), Barrella and

Silva (2003), Da Silva (2004), Silva (2005)

and Silva et al. (2005). Nevertheless, those

studies did not include enough morphological

aspects based on SEM micrographs, as well

as did not offer enough details on the surface

ultrastructure. Additionally, a fresh view of the

parasite shows the keel dorsal view without

histological sections.

In the original description, S. serpentis was

characterized by having externally well-devel-

oped suckers, with the ventral sucker medial to

the body, and a slightly protruding genital pore

on the left side. Their life cycle involves two sec-

ondary hosts, an invertebrate (gastropod) and a

vertebrate (fish or amphibian) (Prudhoe, 1949).

Studies on S. serpentis have been limited to the

esophagus and oral cavity of snakes (Barrella &

Silva, 2003; Prudhoe, 1949; Silva et al., 2005).

The objective of this study is to provide

enough data about the characters of S. serpentis

using SEM and light microscopy micrographs,

as well as, about the parasitism relationship

between this trematode and B. atrox collected

in the Brazilian Amazon.

MATERIALS AND METHODS

Host collection and capture area: The col-

lections occurred from January to May 2010 in

an area of the Amazonian Forest, located in the

Tapajós National Forest-FLONA conservation

unit, West of Pará State, Brazil (Fig. 1). The cap-

tures were made using the active visual search

method, limited by time on trails, secondary

roads, gallery forests, and residential areas, in

addition to occasional encounters as described

by Oliveira and Martins (2001).

The captured specimens were placed in

plastic boxes and sent to the Zoological Research

Laboratory of the Unama Centro Universitário

Fig. 1. Map showing the collection area of Bothrops atrox, hosts of Sticolecitha serpentis, in the conservation unit of the

Tapajós National Forest, Pará State, Brazil.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

da Amazônia, in Santarém municipality, Pará

State. In the laboratory, the snakes were sub-

mitted to physical examination and the para-

sites observed were collected for identification.

After that, the venom was extracted for bio-

chemical studies, the snakes were deposited

at the Coleção Herpetológica from Zoological

Research Laboratory by accession numbers:

HMC 66, 67, 60, 186, 59, 42, 156, 78, 141,

and 63.

Collection of parasites and morphologi-

cal analysis: During this examination, abnor-

malities in the oral cavity with the parasites

were observed collected with tweezers, fixed

and stored in an alcoholic solution of 70 %.

Sex, weight measurements, snout-vent length

(SVL), and tail length (TL) were also deter-

mined for the B. atrox specimens.

The trematodes collected were prepared by

the Carmine method, using Langeron acid in

permanent slides with Canadian balm (Amato

& Amato, 2010), and the morphological iden-

tification was carried out according to Yama-

guti (1971) and Travassos et al. (1969). Two

specimens of S. serpentis have been deposited

in UFOPA Parasitological Collection, at the

Laboratório de Ecologia e Comportamento

Animal (LECAn) under access numbers: UFO-

PA-P(Tre)001 and UFOPA-P(Tre)002. Also, the

material was analyzed under light microscopy

with a magnification of 100X to 400X at the

Microscopy and Sample Collection Labora-

tory of the Universidade Federal do Oeste

do Pará (UFOPA), Pará, Brazil. Samples were

photographed using a Zeiss Axioplan optical

microscope with an Axiocam ERc 5s camera.

The morphometric study was carried out with

the Blue Zen software 2nd edition. As well as for

the SEM micrographs, were obtained using a

Digital Scanning Microscope FEI, Quanta 250,

located at the Laboratório de Biologia Celular,

Instituto Butantan, São Paulo, Brazil.

Scanning electron microscopy: Exter-

nal morphology was evaluated by scanning

electron microscopy (SEM) previously fixed

in ethyl alcohol (70 %), transferred to glutar-

aldehyde solution (2.5 %) in 0.15 M phosphate

buffer (pH 7.3), and then subsequently fixed

in osmium tetroxide (1 %) in the same buffer,

for 2 h. The samples were dehydrated in an

increasing sequence of ethyl alcohol solutions

and washed in a solution of distilled water and

filtered water (1:1). Dehydration was carried

out with an increasing sequence of ethyl alcohol

solutions, and drying was carried out employ-

ing a critical point in CPD 020 (Balzer Union),

with liquid CO2. The samples were placed on

double-sided tape in Stub and covered with a

gold-palladium jet.

Data analysis: The ecological terms per-

cent infected (%), mean intensity, and mean

abundance (IC = confidence intervals) were

used according to Bush et al. (1997). These

parameters were calculated using Quantitative

Parasitology 3.0 software (Reiczigel et al., 2019).

RESULTS

Ten specimens of B. atrox were examined,

seven females and three males with SVL: 580.8

mm ± 118.52 mm, and TL: 97.6 mm ± 63.68

mm. During the physical examination, three

specimens presented parasitism by trematodes:

HMC186 = 21 parasites in the mouth; HMC156

= 26 parasites; and HMC59 = 53 in the mouth

and 19 in the esophagus. All the parasites found

were adults and the morphometric measure-

ments are shown in Table 1.

The preparations described in the Method-

ology were made and the 25 trematodes were

identified as S. serpentis (Trematoda: Plagior-

chiidae). More details are in the ‘Taxonomic

Summary’ section. The percent infected of S.

serpentis on their hosts was 30 %, with a mean

infection intensity of 39.67 (IC = 21.0-56.67)

worms/host and a mean abundance of 11.90

(IC = 2.10-33.50).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

Taxonomic Summary

Class Trematoda Rudolphi, 1808

Subclass Digenea

Family Plagiorchiidae Lühe, 1901

Sticholecitha serpentis Prudhoe, 1949

Host: Bothrops atrox (Squamata:

Viperidae).

Geographical location: Amazonian For-

est, Pará State, Brazil (3º 02’ 39.07” S & 54º 57’

04.24” W).

Infection site: Oral cavity and esophagus.

Morphological description: The descrip-

tion presented here is based on the analysis

of 25 specimens of S. serpentis examined. In

nature, it has a milky color with a well-high-

lighted cup-shaped oral sucker in the anterior

region and a cup-shaped ventral sucker located

in the equatorial region. The genital pore stands

out with a slightly lighter placement than the

body on the left lateral extremity. The body

has a navicular shape, being flat or slightly

concave ventrally, with an evident elevation of

a keel dorsally, having a thin cuticle armed with

sharp spines.

The large leafy-shaped uterus, when con-

sidered its proportion to the total body size,

can occupy up to one-third of the total size,

presenting a slightly yellowish color (Fig. 2A).

In Carmine, the pharynx stands out wider than

long, and the testicles can present rounded

shapes varying the globose with a smooth

appearance. The cirrus pouch is elongated in

shape and can extend from the ventral sucker

region to the genital pore.

The lobous ovary located close to the

ventral sucker, with small vitellogenic glands

in granular-lobed form, lateralized to the body

(Fig. 2B). It was possible to compare the varia-

tions with parasites from other hosts (Table 1),

demonstrating that the parasite in this study is

smaller in comparison to others.

SEM photographs are displayed an elon-

gated body in boat-shaped (Fig. 3), with details

of the oral sucker (Fig. 3A) and the acetabulum

(Fig. 3B), presented body longer than wide,

with tegument covered by microspines, and two

well-defined spines on the ventral and posterior

regions of the body (Fig. 3C). The oral sucker is

oval, with circular striated grooves at the base,

and a robust labial portion protruding at the

apical region, which is longer than it is wide.

The oral sucker measures 160 µm long by 150

µm wide, and there are no spines along the

entire edge (Fig. 3A). In addition, the dermis

Table 1

Morphometry of the external and internal structures of adult individuals of Sticholecitha serpentis.

Measured

structures

Sticholecitha serpentis

(n = 25) Present study

Sticholecitha serpentis

(n = 25) Silva et al. 2005

Sticholecitha serpentis

(n = 25) Prudhoe, 1949

Body L3.30 (2.9-3.5) 7.41 (6.23-8.12) 6.8 (5.20-8.40)

W1.00 (0.80-1.2) 1.58 (1.39-1.68) 1.6 (1.20-2.0)

Oral sucker L0.38 (0.32-0.45) 0.62 (0.56-0.71) 0.56-0.65 (in diameter)

W0.37 (0.31-0.42) 0.63 (0.61-0.66)

Acetabulum L 0.33 (0.28-0.40) 0.79 (0.70-0.85) –

W0.31 (0.27-0.35) 0.59 (0.53-0.63) –

Pharynx L0.19 (0.15-0.22) 0.25 (0.21-0.30) 0.21-0.25 (in diameter)

W0.21 (0.17-0.24) 0.28 (0.26-0.30)

Right testes L0.26 (0.23-0.29) 0.47 (0.43-0.51) 0.62 (0.5-0.75)

W0.30 (0.26-0.34) 0.52 (0.46-0.56) 0.47 (0.45-0.50)

Left testes L0.25 (0.19-0.29) 0.47 (0.42-0.55) 0.45 (0.40-0.50)

W0.23 (0.19-0.27) 0.42 (0.38-0.44) 0.47 (0.46-048)

Ovary L0.20 (0.17-0.23) 0.34 (0.29-0.38) 0.48-0.50 (in diameter)

W0.22 (0.18-0.24) 0.34 (0.32-0.37)

L: Length, W: Width; the values in parentheses (in mm) represent the range).

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

has a raised, volcano-like area with spines at the

base and center, but none at the apical margins

(Fig. 3B). The dermal border is circular and has

grooves due to its muscular origin and fixation,

making it a muscularized structure. The cavity

on the inner edge’s measures 109 µm in length

by 85 µm in width, while on the outer edges, it

measures 91 µm in length by 98 µm in width

(Fig. 3B).

The dorsal keel appears as a prominent ele-

vation from a horizontal view of the parasite’s

body, with discrete undulations in the median

to caudal region, with a marked lowering in

the first anterior third (Fig. 4). In addition, the

first anterior third is marked by the presence

of rugosities and furrows in a longitudinal

direction. In the second third, from the median

region to the end of the distal caudal region of

the parasite body, the roughness and furrows

are horizontal (Fig. 4).

DISCUSSION

This is the first record of the association of

S. serpentis and B. atrox. Until now, the records

of parasitism by this trematode are restricted to

Surinam, parasitizing the C. carinatus (Prud-

hoe, 1949); and in Porto Primavera, São Paulo

State, Brazil, parasitizing B. moojeni (Barrella

& Silva, 2003; Silva et al., 2005) and unidenti-

fied locality in Brazil, parasitizing X. severus

Fig. 2. Adult specimen of Sticolecitha serpentis. A. External

structures observed in natura (OS-Oral Sucker Cup Shaped,

GP-Genital Pore, AC-Acetabulum), B. Internal structures

observed after staining in Carmine (PH-Pharynx,

GP-Genital Pore, OV-Ovary, RT-Right testes, LT-Left

testes, U-Leaf Shaped Uterus), C. Schematic drawing

(OS-Oral Sucker Cup Shaped, GP-Genital Pore, VS-Ventral

Sucker, PH-Pharynx, CP-Cirrus Pouch, GP-Genital Pore,

OV-Ovary, RT-Right testes, LT-Left testes, U-Uterus),

D. Reproductive organs (CP-Cirrus Pouch, OV-Ovary,

RT-Right testes, LT-Left testes).

Fig. 3. Photographs on SEM of adult specimen of Sticolecitha

serpentis. A. Oral sucker, B. Ventral Sucker, C. Details of

tegument with microspines.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

(Freitas, 1956). So, this study reports the new

host to S. serpentis and the first record of

this species parasitizing a viperid snake in the

Brazilian Amazon.

As shown in other studies involving Pla-

giorchiidae and other trematodes (Byrd & Sco-

field, 1952; Byrd & Scofield, 1954; Corrêa et

al., 1990; Pinto & De Melo, 2012; Sogandares-

Bernal & Grenier, 1971; Sue & Platt, 1999), the

life cycle of S. serpentis in B. atrox, can be con-

sidered invertebrate and vertebrate intermedi-

ate hosts. We conjecture that the eggs of the

parasite are dispersed in the aquatic or terres-

trial habitat, where they are consumed by snails,

which are considered to be the first hosts. The

secondary intermediate host, which in this case

could be an anuran, can be infected in two

different ways: by ingestion of invertebrates

infected with metacercariae or by ingestion,

aspiration, or coming into direct contact with

infective metacercariae in their anuran larval

forms (tadpoles). Consequently, considering

the feeding habits of B. atrox, which includes

amphibians in its diet (Bisneto & Kaefer, 2019),

Fig. 4. Ligh microscopy photographs of adult specimen of Sticolecitha serpentis showing dorsal keel. A. Dorsal view, B. Lateral

dorsal view, C. Horizontal view with details of the keel in SEM photograph.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

the intermediate host is preyed upon and thus

the parasite completes its life cycle in its defini-

tive host.

Ingesting parasitized adult amphibians

is suggested as a hypothesis of infection in

the studies of Corrêa et al. (1990), where a

Bothrops insularis (Amaral, 1922) (Squamata:

Viperidae) kept in captivity with controlled diet

became infected with Ochetosoma heterocoe-

lium (Travassos, 1921) after feeding on a Hyla

sp. amphibian, suggesting this as a probable

secondary host. Anurans are predators of gas-

tropods and are known components of the diet

of B. atrox (Bisneto & Kaefer, 2019; Da Silva et

al., 2010; Solé et al., 2017; Solé et al., 2019).

Our study found a lower infection fre-

quency compared to Barrella and Silva (2003)

results. They reported a total prevalence of 68

% in fifty analyzed B. moojeni, with 1 to 15

trematodes per animal being the most com-

mon finding. Only one snake had a total of 51

parasites. We analyzed the same infection sites

as Barrella and Silva (2003) and found 21 to 51

parasites in the mouths of three B. atrox. Only

one individual was infected with 19 S. serpentis

in the esophagus. These parasites are typically

present in high numbers within their hosts.

Due to the low number of studies involving S.

serpentis, there is limited integrated informa-

tion regarding its distribution, taxonomy, para-

site ecology, and molecular characterization. As

a result, the systematic of this species is poorly

known (Artigas & Perez, 1969; Prudhoe, 1949).

It should be emphasized that there are currently

no DNA sequences available for S. serpentis in

any nucleotide database.

Also, the present study aimed to contribute

to the knowledge of the species S. serpentis,

with detailed morphological descriptions and

SEM images that had never been done before.

The new aspects presented, demonstrate that

through the usual technique for trematodes,

unfortunately, the dorsal keel is pressed, mak-

ing its visualization difficult. However, in his-

tological study, the dorsal keel is visualized, as

presented by Silva (2005). Nevertheless, in our

study, we present a fresh parasite visualization,

as well as SEM photographs that demonstrate

the well-defined dorsal keel. Therefore, we are

showing, through different techniques, infor-

mation that will help in the identification of S.

serpentis in further studies. Furthermore, we

emphasize the need for molecular studies to

better understand the phylogenetic position of

the group and the relationship with their verte-

brate hosts.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives. Ethics approval: This study

was approved by the Animal Use Committee

from the Federal University of Western Pará

(Authorization #1020180044). Wild animals

were collected with the approval from the

Brazilian Institute of Environment and Renew-

able Natural Resources, authorized through the

Biodiversity Information and Authorization

System-SISBIO nº. 66047-4.

ACKNOWLEDGMENTS

To Beatriz Mauricio of the Laboratory of

Cellular Biology of the Butantan Institute for

the images obtained through the Scanning

Electron Microscopy. The authors would thank

for Dr. Reinaldo José Da Silva at São Paulo

State University for the helpful of identifica-

tion this parasite. This work was supported

by the Coordenação de Aperfeiçoamento de

Pessoal de Nível Superior (CAPES) under the

Grant # 88887.636892/2021-00 (DCS) and Pro-

cess #88887.598663/2021-00 (TAC); and by

Fundação de Amparo à Pesquisa do Estado

de São Paulo under the Grant FAPESP no.

2017/01416-7 (RB-S), 2018/24667-8 (RB-S),

2020/11755-6 (RB-S).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58870, enero-diciembre 2024 (Publicado Set. 18, 2024)

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