ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
NEMATODES PARASITES OF RHINELLA JIMI (STEVAUX, 2002) (ANURA: BUFONIDAE) IN
AREAS OF CAATINGA, NORTHEASTERN BRAZIL
NEMÁTODOS PARÁSITOS DE RHINELLA JIMI (STEVAUX, 2002) (ANURA: BUFONIDAE) EN
ÁREAS DE CAATINGA, NORDESTE DE BRASIL
ABSTRACT
Keywords: Helminth – Neotropical – Oswaldocruzia lopesi – Rhabdias – toads – Semiarid
Amphibians harbor a wide variety of parasites, acting as paratenic, intermediary and definitive hosts. Actually,
just 8% of Brazilian amphibians have been investigated regarding associated helminths. Herein, we analyzed
20 specimens of the toad Rhinella jimi Stevaux, 2002 from Ceará and Rio Grande do Norte states. Seven taxa
of nematodes were found infecting R. jimi (Oswaldocruzia lopesi Travassos, 1938, Raillietnema spectans
Gomes, 1964, Physaloptera sp., Parapharyngodon sp., Rhabdias sp., Cosmocercidae, and Unidentified
Nematoda larvae). All nematode species are new records for R. jimi. These results expand the Nematode
records for R. jimi as well as increase knowledge of the diversity of parasites in anurans in South America.
Neotropical Helminthology
265
Neotropical Helminthology, 2019, 13(2), jul-dic:265-271.
1* 2 2 3
Darciane Maria de Amorim ; Rosa Hermina de Oliveira ; Cristina Santos Dyna ; Dauana Mesquita Sousa ;
4 4 4 2, 4
Maria Erica Pereira Santos ; Lucineide dos Santos Lima ; Lídia Correia Pinto & Robson Waldemar Ávila
1Programa de Pós-Graduação em Ciência Animal Tropical, Universidade Federal Rural de
Pernambuco, Rua Dom Manoel de Medeiros SN, CEP 52171-900, Recife, PE, Brasil
2Programa de Pós-Graduação em Ecologia e Recursos Naturais, Universidade Federal do Ceará. Av.
Humberto Monte, Pici, 60455-970, Bloco 902, Fortaleza, CE, Brasil
3Rede de Biotecnologia do Nordeste, Universidade Federal do Maranhão - UFMA
4Programa de Pós-graduação em Bioprospecção Molecular, Departamento de Química Biológica,
Universidade Regional do Cariri – URCA, R. Cel. Antônio Luiz, 1161, Pimenta, CEP 63105-000, Crato, CE, Brasil
*Corresponding author: E-mail: darciamorim@hotmail.com
RESUMEN
Palabras clave: Helmintos – Neotropical – Oswaldocruzia lopesi – Rhabdias – Sapos – semiárido
Los anfibios hospedan una amplia variedad de parásitos, sea de forma temporal (hospedero paraténico),
intermediaria o definitiva. Solamente un 8% de los anfibios en Brasil han sido investigados con relación a sus
helmintos asociados, por lo que en este trabajo analizamos 20 especímenes de Rhinella jimi Stevaux, 2002
colectados en los estados de Ceará y Rio Grande do Norte, en la región Nordeste de Brasil. Siete taxones de
nematodos se encontraron infectando individuos de R. jimi (Oswaldocruzia lopesi Travassos, 1938,
Raillietnema spectans Gomes, 1964, Physaloptera sp., Parapharyngodon sp., Rhabdias sp., Cosmocercidae,
y una larva no identificada). Todas las especies encontradas representan nuevos registros de parásitos para R.
jimi, resultado que amplía los registros de nematodos para esta especie, así como aumentan el conocimiento de
la diversidad de parásitos en anuros para América del Sur.
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Volume13,Number2(jul-dec2019)
266
Amphibians harbor a wide variety of parasites,
acting as paratenic, intermediary and definitive
hosts (Santos et al., 2013; Campião et al., 2014;
Teles et al., 2018). Environmental characteristics,
different patterns of life cycles and reproductive
strategies are the main factors influencing helminth
infection in amphibians (Aho, 1990; Campião et
al., 2012; 2014; Toledo et al., 2017; Sena et al.,
2018).
Brazil has the highest diversity of amphibians in
the world, especially in anurans with 1040 species
(Segalla et al., 2016). Most studies on helminths
infecting amphibians in South America are from
Brazilian species (Santos et al., 2013; Campião et
al., 2014; Martins-Sobrinho et al., 2017; Teles et
al., 2018). However, only 8% of Brazilian
amphibians have been studied so far regarding
helminth associated (Santos et al., 2013; Campião
et al., 2014; Teles et al., 2018).
Rhinella jimi (Stevaux, 2002) is a widespread
bufonid inhabiting Caatinga areas from
Northeastern Brazil (Stevaux, 2002; Loebernan &
Roberto & Loebmann, 2016, Segalla et al., 2016).
The species is also found frequently in rural and
urban areas, being an opportunistic feeder of
insects and small vertebrates (Moreira & Barreto,
1996; ), and status of conservation Stevaux, 2002
least concern (LC) according to the IUCN (2019).
According to Campião et al. (2014) and Müller et
al. (2018), only six species of helminths have been
reported for R. jimi: the trematode Gorgoderina
rochalimae Dobin Jr., 1957 and the nematodes
Aplectana membranosa Schneider, 1866; Miranda,
1924, Oswaldocruzia subauricularis Rudolphi,
1819; Rhabdias fuelleborni Travassos, 1926,
Rhabdias sphaerocephala Goodey, 1924 and
Rhabdias pseudosphaerocephala Kuzmin et al.,
2007. Herein, we present data on nematodes
infection in the toad Rhinella jimi from areas of
Caatinga of two Brazilian states.
We analyzed a total of 20 specimens of R. jimi,
being 5 adult males (mean snout-vent length (SVL)
= 108.34 ± 38.92), 2 adult females (mean SVL =
99.59 ± 41.30) and 13 juveniles (mean SVL = 66.60
± 15.65). Specimens were collected manually from
2006 to 2014, in eight municipalities on Ceará
state: Aiuaba (n=2) (06° 36′ S, 40° 07′ W),
Acopiara (n=1) (6° 5' S, 39° 27' W), Caucaia (n=1)
(3° 44' S, 38° 39' W), Barbalha (n=2) (7° 18′ S, 39°
18′ W), Farias Brito (n=1) (06º 55' S 39º 33' W),
Santana do Cariri (n=1) (7° 11' S, 39° 44' W), Nova
Olinda (n=5) (7° 34' S, 39° 4' W), and Brejo Santo
(n=1) (7° 29' S, 38° 58' W); Additionally, six
specimens from the municipality of João Câmara
(05° 33′ S, 35° 56′ W) in the state of Rio Grande do
Norte were also examined. Caatinga covers these
areas with a semiarid climate (IDEMA, 2008;
IPECE, 2016).
After the capture, specimens were euthanized with
le tha l inj ec t io n o f s odi um T hi ope nta l
(Thiopentax®), and have their SVL measured with
a digital caliper (precision 0.01 mm). Sex was
determined by visual inspection of gonads.
Specimens were then fixed in formalin 10%
(Franco & Salomão, 2002) and deposited in the
Coleção Herpetológica da Universidade Regional
do Cariri (URCA–H 471–476, 1737, 3024, 3164,
3413, 4192, 4193, 4875, 7956, 8399, 8400–8403,
8928). Toads were necropsied with a midventral
incision and all organs and coelomic cavity were
searched for helminths. These parasites found were
preserved in 70% ethyl alcohol.
Nematodes found were mounted in temporary
slides (Yamaguti, 1961), cleared in lactophenol and
analyzed under microscope with computerized
image analysis system (Carl Zeiss Microimaging
GmbH, Gottingen, Germany). Thereafter, the
helminths were deposited in the Coleção
Parasitológica da Universidade Regional do Cariri
(URCA-P).
Ethic aspects: The collecting methods were
defined and authorized by the regulatory the ethics
committee of Universidade Regional do Cariri
(CEUA/URCA, process No. 00260/2016.1).
Of the 20 toads examined, 13 (65%) were infected
INTRODUCTION
Neotropical Helminthology, 2019, 13(2), jul-dic
MATERIAL AND METHODS RESULTS
Amorim et al.
267
by at least one species of Nematode, and 191
nematodes specimens were recovered.
Seven taxa of nematodes were found infecting R.
jimi: Oswaldocruzia lopesi Travassos, 1938,
Raillietnema spectans Gomes, 1964, Physaloptera
sp., Parapharyngodon sp., Rhabdias sp.,
unidentified Cosmocercidae Travassos, 1925, and
encysted larvae of unidentified nematodes. All
represent are new records for R. jimi (Table 1).
Table 1. Site of infection of the Nematodes community associated with Rhinella jimi in areas of Caatinga,
Northeastern Brazil.
Nematoda Site of infection
Oswaldocruzia lopesi
Stomach, Small intestines
Physaloptera sp.
Stomach
Cosmocercidae
Large intestines, Small intestines
Parapharyngodon sp.
Large intestines, Small intestines, Stomach
Encysted larvae (unidentied nematodes)
Small intestines
Raillietnema spectans Large intestines
Rhabdias sp. Lungs
Nematoda phylum was the only one recorded
infecting the toad R. jimi in the present study,
likewise other parasitological studies with species
of the genus Rhinella (e.g. Santos, et al., 2013;
Teles et al., 2018). The exclusive infection by
nematodes may be related to host life cycle and
foraging strategies (Yoder & Coggins 2007; Santos
et al., 2013). In anurans, the occurrence of
nematodes may be associated with the time spent in
water or on land (Aho, 1990; Anderson, 2000;
Yoder & Coggins 2007; Santos et al., 2013). In
terrestrial habitats most nematodes infect anurans
by skin penetration or egg ingestion, which may
explain the infection in individuals of the genus
Rhinella (Aho, 1990; Anderson, 2000; Bolek &
Coggins 2000, Santos et al., 2013; Teles et al.,
2018).
All nematodes found in the study present are
monoxenous, except Physaloptera sp. Species of
the genus Physaloptera have already been
recorded infecting the stomach of mammals, fish,
reptiles and amphibians, including anurans of the
Bufonidae family, where this parasite is commonly
recorded in larval stage (Anderson, 2000; Ávila &
Silva, 2010; Santos et al., 2013; Aguiar et al., 2014;
Campião et al., 2014; Teles et al., 2018). In the
DISCUSSION present study, we recorded an adult specimen,
however, due to the preservation conditions, it was
not possible to identify to species level. Infection
by parasites of this genus may occur by ingestion of
parasitized arthropods (Anderson, 2000; Campião
et al., 2014, 2015).
Unidentified nematodes of the Cosmocercidae
family are frequently recorded infecting reptiles
and amphibians (Avila & Silva, 2010; Campião et
al., 2014) and have been found to parasite anurans
of the genus Rhinella (Santos et al., 2013; Campião
et al., 2014; Toledo et al., 2017; Teles et al., 2018).
These parasites can cause infection when ingested
or penetrated through the skin of the host
(Anderson, 2000). Encysted larvae of unidentified
nematodes were also recorded in the present study.
The occurrence suggests that R. jimi may be acting
as intermediate or paratenic hosts of these parasites
(Anderson, 2000).
Rhabdias Stiles & Hassal, 1905, are common
pulmonary parasites of amphibians and reptiles
(Anderson, 2000; Ávila & Silva, 2010; Campião et
al., 2014). Infection in anurans may occur by direct
penetration into the skin of the host, however the
life cycle of these parasites is alternated between a
free and parasitic life stage, but only females act as
parasites, infecting the lungs of their hosts
(Anderson, 2000). In South America there are more
Neotropical Helminthology, 2019, 13(2), jul-dic Nematodes parasites of Rhinella jimi
268
than 19 Rhabdias species reported parasitizing
amphibians (Kuzmin et al., 2016., Muller et al.,
2018), including R. jimi, infected by R. fuelleborni,
R. sphaerocephala and R. pseudosphaerocephala
(Vicente et al., 1991; Campião et al., 2014; Kuzmin
et al., 2016; Muller et al., 2018).
The molineid Oswaldocruzia lopesi usually infects
the stomachs of lizards and amphibians (Ávila &
Silva; Campião et al., 2014). In toads of the genus
Rhinella, O. lopesi have already been reported
intecting R. icterica, R. margaritifera and R.
marina (Campião et al., 2014). The nematode
Raillietnema spectans is a common anuran parasite
(Vicente et al., 1991; Campião et al., 2014;
Alcântara et al., 2018; Teles et al., 2018). In Brazil,
it has been reported infecting Leptodactylus
latrans, Pleurodema diplolister, Dermatonotus
muelleri, R. crucifer, R. icterica, R. diptycha, R.
granulosa, and R. jimi (Vicente, et al., 1991;
Campião et al., 2014; Teles, et al., 2015; Alcântara
et al., 2018; Teles et al., 2018; present study).
Infection by Parapharyngodon spp., can occur by
coprophagy or through ingestion of infected larvae
(Anderson, 2000). Despite being considered
typical parasites of lizards, many studies report
their occurrence in anurans (e.g Ramallo et al.,
2002; Bursey et al., 2013; Araújo-Filho et al.,
2015; Alcântara et al., 2018). To date it has been
recorded infecting species of the families
Eleutherodactylidae, Hylidae and Microhylidae
and Bufonidae (Campião et al., 2014; Araújo-Filho
et al., 2015; Alcântara et al., 2018), including R.
marina, R. icterica and R. jimi (Luque et al., 2005;
Bursey et al., 2013, present study).
Rhinella jimi was infected by seven nematode taxa,
all new host records. Previous studies with Anurans
of genus Rhinella in South America recorded
helminth richness for R. fernandezae, R. major, R.
icterica greater than 10 species (Luque et al., 2005;
Santos & Amato et al., 2010; Hamann et al., 2013;
Santos et al., 2013; Hamann & González, 2015;
Toledo et al., 2017). However, individuals of
Rhinella genus recorded so far regarding
occurrence of helminths, a large (R. jimi; R.
marina, R. diptycha (=R. schneideri), R. spinulosa,
R. bergi, R. granulosa, R. limensis, R. poeppigii)
has richness less than 9 (Galicia-Guerrero et al.,
20022; Chero et al., 2015; 2016; Espínola-Novelo
et al., 2017; Toledo et al., 2017; Teles et al., 2018,
present study). Compared to other South American
bufonids, R. jimi presented a relatively high
parasite richness (e.g. Santos & Amato, 2010;
Toledo et al., 2017; Teles at al., 2018). The species
richness recorded in R. jimi may be related to the
environmental conditions that may favor infection,
as well as the low nematode specificity (Aho, 1990;
Bolek & Coggins 2000; Campião et al., 2012; Sena
et al., 2018).
In conclusion R. jimi presented seven new
nematode registries, demonstrating that the
parasites richness associated with Bufonidae
Family, especially genus Rhinella, is more diverse
than one currently documented. This study
contributed to increase inventory of helminths for
Anurans in South America.
We are grateful to Conselho Nacional de
Desenvolvimento Científico e Tecnológico - CNPq
for a research grant to RWA (# 303622/2015-6;
305988/2018-2). To the ethics committee of
Universidade Regional do Cariri (CEUA/URCA,
process No. 00260/2016.1). To Waltecio O.
Almeida for helping and permission of use of the
microscope in the Laboratório de Zoologia
Universidade Regional do Cariri.
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