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Gastrointestinal Parasitism in Rescued Wild Birds
Neotropical Helminthology (Lima). Vol. 18, N
º
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Neotropical Helminthology
Neotropical Helminthology, 2024, vol. 18 (2), 241-247
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTHS INFECTING THE BOM JARDIM TOAD
RHINELLA DAPSILIS
FROM AN ATLANTIC FOREST ENCLAVE AT NORTHEASTERN BRAZIL
HELMINTOS INFECTANDO EL SAPO BOM JARDIM
RHINELLA DAPSILIS
DE UN ENCLAVE DE LA MATA ATLÁNTICA, BRASIL
HELMINTOS INFECTANDO O SAPO BOM JARDIM
RHINELLA DAPSILIS
DE UM ENCLAVE DA MATA ATLÂNTICA NORDESTE DO BRASIL
Vitoria Hellen Holanda¹
,
³
,
*; Dalilange Batista-Oliveira²
,
³ & Robson Waldemar Avila¹
,
²
,
³
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20242181841
Universidad Nacional
Federico Villarreal
Volume 18, Number 2 (jul - dic) 2024
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
Rhinella dapsilis (
Myers and Carvalho, 1945) is widespread in Amazonia, from Colombia to Brazil. Despite its huge
distribution, information on basic biological aspects is scarce, even more so regarding helminth parasites. Herein,
we present data on helminth infecting
R. dapsilis
from an Atlantic Forest enclave in Northeastern Brazil. Ten taxa were
found, nine nematodes and one acanthocephala n, Cosmocercidae and
Rhabdias
sp. were the most prevalent taxa. We
reported six new host records and expanded the knowledge about parasitism in Neotropical anurans.
Keywords:
Amphibian
–
Bufonidae – highland marshes
–
Parasites
RESUMEN
Rhinella dapsilis (
Myers and Carvalho, 1945) es ampliamente distribuida desde Colombia hasta Brasil. Sin embargo, a
pesar de su amplia distribución, las informaciones al respecto de los aspectos básicos de su biología son escasos, especial-
mente en cuanto a los parásitos helmínticos. Presentamos datos de infecciones por helmintos en
R
.
dapsilis
de una parte
¹ Department of Biology, Pici Campus, Federal University of Ceará, Fortaleza - CE Zip Code 60440-900, Brazil.
² Graduate Course of Ecology and Natural Resources, Department of Biology, Pici Campus, Federal University of Ceará,
Fortaleza - CE Zip Code 60440-900, Brazil.
³ Regional Ophiology Center, Federal University of Ceará, Block 905, Science Center, Pici Campus, Fortaleza - CE Zip Code
60455-760, Brazil.
* Corresponding author: hellenvictoriabio@gmail.com
Vitoria Hellen Holanda:
https://orcid.org/0009-0005-3959-9801
Dalilange Batista-Oliveira:
https://orcid.org/0000-0002-4140-6643
Robson Waldemar Avila:
https://orcid.org/0000-0003-3641-8321
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Holanda
et al.
242
de la Mata Atlántica en el Nordeste brasileño. Diez taxones fueron encontrados, entre ellos, nueve nematodos y uno
acantocéfalo. Cosmocercidae y
Rhabdias
sp. siendo los más frecuentes. Presentamos seis nuevos registros, expandiendo el
conocimiento sobre el parasitismo para los anuros Neotropicales.
Palabras-clave:
Anfbios – Bufonidae – Pantano de altitud – Parásitos
RESUMO
Rhinella dapsilis (
Myers and Carvalho, 1945) é amplamente distribuída na Amazônia, desde a Colômbia até o Brasil.
Apesar da ampla distribuição, informações sobre aspectos básicos de sua biologia são escassas, especialmente quanto a
parasitas helmínticos. Aqui apresentamos dados de helmintos infectando
R. dapsilis
de um enclave de Mata Atlântica
no nordeste brasileiro. Dez táxons foram encontrados, sendo 9 nematódeos e um acantocéfalo. Cosmocercidae e
Rhabdias
sp. foram os táxons mais prevalentes. Apresentamos seis novos registros e expandimos o conhecimento acerca
de parasitismo para anuros neotropicais.
Palavras-chave: Anfíbios – Bufonidae – Brejos de altitude – Parasitas
INTRODUCTION
Rhinella dapsilis
(Myers and Carvalho, 1945), is a leaf-
litter toad widely distributed in Amazonia, occurring in
Colombia, Peru, Ecuador and Brazil (Ávila
et al
., 2018;
Frost, 2024). In Brazil,
R. dapsilis
occurs in Amazonia
at Acre, Amapá, Amazonas and Pará states, also being
recorded in transition zones at Cerrado (Goiás, Maranhão
and Tocantins states) and Atlantic Forest (Pernambuco
and Alagoas states), including in a rainforest enclave
inside Caatinga domain in Ceará state (Fouquet
et al
.,
2024). As many of the species within the
R. margaritifera
group,
R. dapsilis
have serious taxonomic problems, with
diferentiation between
R. margaritifera
being extremely
difcult (Caramaschi & Pombal, 2006; Vaz-Silva
et al.
,
2015; Ávila
et al
., 2018; Pereyra
et al
., 2021; Fouquet
et al
.,
2024). Despite this huge distribution, very little is known
about its basic biological aspects, with habitat use, diet and
defensive behavior already published (Brito
et al
., 2013).
To date, 25 helminths are known to infect
R. dapsilis
(most
of the records under the name
R. margaritifera
) from Peru,
Ecuador and Brazil (Campião
et al
., 2014; Willkens
et
al
., 2016; Chero
et al
., 2023). Tose records, however,
are restricted to Amazonia, without studies from Atlantic
Forest populations. Tis lack of knowledge difcult the
understanding of host-parasite relationships (Campião
et
al.
, 2009; Santos & Amato, 2010; Santos
et al
., 2013).
Herein, we examined the helminths infecting
R. dapsilis
from an Atlantic Forest enclave in Northeastern Brazil.
MATERIAL AND METHODS
Specimens of
R. dapsilis
were collected at the Guaramiranga
municipality (4° 15
′
46
″
S, 38° 55
′
58
″
O), located at
the Baturité massif, a rainforest enclave within Caatinga
Domain, Brazil. Te climate is classifed as tropical sub-
hot humid and tropical hot humid, with 1,737.5 mm
of rainfall per year and average temperatures of 24º to
26º. Te rainy season occurs from January to May and
the vegetation is characterized by evergreen and seasonal
evergreen forest, classifed as a remnant of the Atlantic
Forest (IPECE, 2017; Silvera
et al
., 2020).
Specimens of
R. dapsilis
were collected from 2019 to 2024
through active searches or pitfall traps with drift fences
and deposited at Coleção Herpetológica da Universidade
Federal do Ceará (CHUFC-A 9975, 12286-89, 12664-68,
12670, 12283-85, 12290-93). Eighteen individuals were
collected, euthanized with a lethal injection of lidocaine
(collecting permit SISBIO 29613-1).
Te snout-vent length (SVL) of the specimens were
measured with a digital caliper, necropsied through
a midventral incision and all organs and body cavity
were dissected for the search of parasitic helminths. Te
helminths were collected and preserved according to
Amato
et al
. (1991), Andrade (2000) and Sulieman
et al
.
(2015). For identifcation, the nematodes were clarifed
in lactic acid, while acanthocephalans were stained
according to the hydrochloric carmine protocols and then
Helminths infecting
Rhinella dapsilis
243
Neotropical Helminthology (Lima). Vol. 18, N
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clarifed with eugenol on temporary slides (Amato
et al
.,
1991). Helminth identifcation was performed following
Yamaguti (1961), Sprent (1978), Vicente
et al
. (1991),
Anderson (2000) and Gibbons (2010).
Slides were analyzed under a microscope with a compu-
terized image analysis system. Voucher helminths were
deposited at Coleção Parasitológica of the Universidade
Federal do Ceará. Parasitological descriptors (prevalence,
mean intensity of infection and abundance) were calcula-
ted according to the specifcations of Bush et al. (1997).
Ethic aspects
: Tis study was approved by the Animal
Ethics Committee of the Universidade Federal do Ceará
(CEUA-UFC, process # CEUA 6314010321).
RESULTS
A total of 770 helminths were found infecting
R.
dapsilis
, comprising 10 taxa. Te helminths belonged to
the phyllum Nematoda (767 individuals from 9 taxa)
and Acanthocephala (3 individuals from 1 taxa). Te
parasites showed an overall prevalence of 100%, mean
overall infection intensity of 45.33 ± 6.40 and mean
overall abundance of 45.33 ± 6.40. Te highest helminth
abundance was Cosmocercidae, followed by
Rhabdias
sp. and
Oxysomatium petrolinensis
(Félix-Nascimento
2020) (Table 1). Most endoparasites found to
R. dapsilis
were located on the lungs (n= 324), followed by the
large intestine (n= 295). By contrast, the body cavity
and bladder were less infected with a total of 4 and 8
endoparasites, respectively. Six taxa were reported for the
frst time infecting
R. dapsilis
(Table 1).
Table 1.
Parasitological indices of helminths in
Rhinella dapsilis
from Baturité Massif. Development stage (DS), Larvae
(L), Adult (A), Prevalence values (P%), number of endoparasites (NE), mean intensity of infection and standard devia-
tion (MII ± SD), mean abundance (MA), site of infection (Site): BC=Body cavity; ST= stomach; LI= large intestine; SI=
small intestine, LU= lungs; UB= Urinary Bladder. * New record for
R. dapsilis
.
Endoparasites DS P% NE MII±SD MA Site
Acanthocephala
Centrorhynchus
sp.*L11.13--BC
Nematoda
Aplectana membranosa
*A11.19--SI/ LI
Cosmocerca parva
A11.110--SI/ LI
Cosmocercidae gen. sp.A77.829219.5±13.516.2±14.3SI/ LI/UB
Foleyella
sp.*A5.51--ST
Oswaldocruzia mazzai
A16.75117±12.32.8±7.8LU
Oxysomatium petrolinensis
*A5.584--LI
Physaloptera
sp.L61.1382.6±2.21.6±2.1ST/SI/ LI
Rhabdias
sp.*A83.327316.6±11.215.7±11.6ST/ LU
Strongyloides
sp.*A5.59--SI
DISCUSSION
Most of the parasites found here belong to the family
Cosmocercidae. Like many studies (Lins
et al
., 2017
;
Oliveira
et al
., 2019), Cosmocercidae gen. sp. is not
identifed due to difculties in determining morphological
characters or the absence of males, in which reproductive
organs are essential for species determination. Te
species of the family, including the identifed species here
(
Aplectana membranosa
(Schneider 1866),
Cosmocerca
parva
(Travassos, 1925) and
Oxysomatium petrolinensis
)
have a direct life cycle, and their hosts become infected
by ingesting infective larvae or actively penetrating larvae
present in the soil (Anderson, 2000). Of the species found
here, only
C. parva
have been already reported for
R. dapsilis
(as
R. margaritifera
; Campião
et al
., 2014).
A. membranosa
have been reported infecting other six bufonids (Campião
et al
., 2014) and
O. petrolinensis
were recently described
infecting
Leptodactylus macrosternum
(Miranda-Ribeiro,
1926). Other cosmocercids reported infecting
R. dapsilis
(=
R. margaritifera
) are
Aplectana hylambatis
(Baylis,
1927),
Cosmocerca podicipinus (
Bursey
et al
., 2001), and
Neotropical Helminthology (Lima). Vol. 18, N
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et al.
244
Cosmocerca
sp. and
Raillietnema ibañezi
(Cordova, 1998)
(Campião
et al
., 2014; Chero
et al
., 2023).
Nematodes of the genus
Rhabdias
are lung parasites of
amphibians and reptiles, which directly infects its hosts
by active penetration into the skin (Langford & Janovy,
2009; Kuzmin
et al
., 2022). Identifcation is very difcult
due to the high morphological similarity, and Müller
et
al
. (2018) strongly suggests the use of molecular data for
species recognition. Tis is the frst record of
Rhabdias
sp.
infecting
R. dapsilis
, although
R. sphaerocephala
have been
already reported (Chero
et al
., 2023).
Nematodes of the genus
Physaloptera
have been recorded
infecting the stomachs of mammals, fsh, reptiles, and
amphibians (Anderson, 2000; Macedo
et al
., 2023). Tey
are usually found in larval stages parasitizing amphibians
that act as intermediate or paratenic hosts (Anderson,
2000). Tis is the frst record of larvae of
Physaloptera
sp.
infecting
R. dapsilis
, but
Physaloptera retusa
was already
reported (Campião
et al
., 2014).
Nematodes of the genus
Strongyloides
can either infect
their hosts direct or indirectly (Graham
et al
., 2023).
Infection occurs through skin penetration or ingestion
of infected prey (Mati & Melo, 2014; Hallinger
et al
.,
2020). Other bufonids have already been infected by
Strongyloides
spp. (Campião
et al
., 2014). Tis is the frst
record of
Strongyloides
sp. infecting
R. dapsilis
.
Oswaldocruzia
spp. also infects its hosts directly by ingestion
of eggs or larval penetration of the host’s skin (Kirillova,
2020). Many amphibians have been reported as hosts of
O.
mazzai
(Travassos, 1935), including
R. dapsilis
(Campião
et al
., 2014). Besides
O. mazzai
, other four species of
Oswaldocruzia
have been reported infecting
R. dapsilis
:
O.
albareti
(Slimane & Desset, 1996),
O. chambrieri
(Slimane
& Desset, 1993),
O. lescurei (
Slimane & Desset, 1996),
O.
lopesi
(Gonçalves et al., 2002)
, O. proencai (González and
Hamann, 2008)
,
O. subauricularis
(Vicente
et al.
, 1991)
(Campião
et al
., 2014; Chero
et al
., 2023).
Te genus
Centrorhynchus
infects birds of the Falconiformes
and Strigiformes orders as defnitive hosts and has
invertebrates as intermediate hosts, with reptiles and
amphibians serving as paratenic hosts (Torres & Puga, 1996;
Oliveira
et al
., 2024). Cystacanths of
Centrorhynchus
sp. are
found in several amphibians, including bufonids (Campião
et al
., 2014). Previously, only unidentifed cystacanths have
been reported infecting
R. dapsilis
(Chero
et al
., 2023).
Te genus
Foleyella
currently has three species infecting
frogs in South America,
F. convoluta
(Walton, 1935),
F.
scalaris
(Walton, 1935) and
F. vellardi
(Travassos, 1929)
that have been recorded infecting frogs of the Hylidae,
Leptodactylidae and Bufonidae in Brazil. In our study,
we found a single female specimen, which makes the
identifcation difcult at species level.
Despite the recent increase in studies dealing with helminth
parasites of Neotropical amphibians (Mascarenhas
et al
.,
2021; Quirino
et al
., 2023), the majority of the species
are still unstudied (Campião
et al
., 2015). Even in widely
distributed species with available information of helminths,
new records of parasites are often published (Campião
et
al
., 2014; 2015). In our study, 60% of the helminths are
new records for
R. dapsilis
, raising to 31 helminth taxa
actually known to infect this toad. Tis highlights the
need for more studies dealing with helminths infecting
amphibians, in order to expand the knowledge in the
Neotropical region.
Author contributions: CRediT (Contributor Roles
Taxonomy)
VHH
= Vitoria Hellen Holanda
DBO
= Dalilange Batista Oliveira
RWA
= Robson Waldemar Ávila
Conceptualization
: VHH
Data curation
: VHH, DBO, RWA
Formal Analysis
: VHH, DBO, RWA
Funding acquisition
: RWA
Investigation
: VHH, DBO, RWA
Methodology
: VHH, RWA
Project administration
: VHH
Resources
: VHH, DBO, RWA
Software
: VHH, RWA
Supervision
: RWA, DBO
Validation
: VHH, DBO, RWA
Visualization
: VHH, DBO, RWA
Writing – original draft
: VHH, RWA
Writing – review & editing
: RWA, DBO
ACKNOWLEDGEMENTS
RWA thanks to CNPq (PQ #307722/2021-0) and
to Fundação Cearense de Apoio ao Desenvolvimento
Científco e Tecnológico (FUNCAP) (#FC3-0198-
00006.01.00/22; UNI-0210-00556.01.00/23) for
research funding.
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