This work aims to provide information about the diversity of parasites associated with Proceratophrys

aridus Cruz, Nunes & Juncá, 2012 and to describe and compare the helminth fauna of this host to the other

inventoried species of the genus. The specimens were manually collected between 2012 and 2016 in ten

localities of Northeast Brazil. A total of 37 P. aridus were necropsied and analyzed for endoparasites, of

which 22 were parasitized with at least one helminth taxon. To verify the similarity between the parasitic

communities, a cluster analysis was performed using the Sorensen index. For this analysis, a matrix with

presence and absence data for the helminth species related to the Odontophrynidae taxon was built. A total

of 867 helminths were recovered, including nematodes, digenetics, and acanthocephalans, presenting a

richness of eight species: Aplectana membranosa (Schneider, 1866), Falcaustra mascula (Rud. 1819),

Rhabdias breviensis Nascimento, Gonçalves, Melo, Giese, Furtado, & Santos, 2013, Oswaldocruzia sp.,

Cosmocercidae larvae, unidentified trematodes, and cystacanths. The most abundant species with the

highest prevalence and mean intensity of infection was A. membranosa. This study provides three new

records of helminths parasitizing P. aridus, in addition to recording trematode and acanthocephalans

infections for this host in northeastern Brazil. Proceratophrys aridus is the species of the

Odontophrynidae family with the highest helminth richness ever recorded.

ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

HELMINTHS PARASITES OF THE FROG PROCERATOPHRYS ARIDUS CRUZ, NUNES, AND

JUNCÁ, 2012 (ANURA: ODONTOPHRYNIDAE) IN A SEMIARID REGION, BRAZIL

HELMINTOS PARÁSITOS DE LA RANA PROCERATOPHRYS ARIDUS CRUZ, NUNES Y JUNCÁ,

2012 (ANURA: ODONTOPHRYNIDAE) EN UNA REGIÓN SEMIÁRIDA, BRASIL

HELMINTOS PARASITAS DE PROCERATOPHRYS ARIDUS CRUZ, NUNES, AND JUNCÁ, 2012

(ANURA: ODONTOPHRYNIDAE) EM UMA REGIÃO DO SEMIÁRIDO, BRASIL

1 Laboratório de Herpetologia, Universidade Regional do Cariri (URCA), Rua Cel. Antônio Luiz Pimenta 1161, Campus

do Pimenta, CEP 63105-000, Crato, Ceará, Brazil.

2 UNESP – Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia,

Avenida Bento Lopes, sem número, Distrito de Rubião Junior, CEP 18618-970, Caixa postal 510, Botucatu, SP, Brasil

3 UFU – Universidade Federal de Uberlândia - Instituto de Ciências Agrárias, LMG-746, Km 1, Monte Carmelo,

38500-000, MG, Brasil.

*Corresponding author: charles.sousa.barroso@gmail.com

1* 2 2

Charles de Sousa Silva ; Edna Paulino de Alcantara ; Reinaldo José da Silva ;

1 3

Robson Waldemar Ávila & Drausio Honorio Morais

ABSTRACT

Keywords: Amphibian – Endoparasite – Host – Northeast – Neotropical realm – Semiarid

Neotropical Helminthology

169

Neotropical Helminthology, 2019, 13(2), jul-dic:169-179.

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

Volume13,Number2(jul-dec2019)

Parasitological inventories in amphibians from the

semiarid region are growing (Campião et al., 2014;

Teles et al., 2014, 2015; Araujo-Filho et al., 2015;

Teles et al., 2017; Martins-Sobrinho et al., 2017;

Lins et al., 2017; Alcantara et al., 2018; Oliveira et

al., 2019) and have revealed helminth fauna

associated with amphibians is rich and diverse. As

the sampling effort grows up, with new areas

sampled and new host are available the richness

tends to increased considerably (Campião et al.,

2014; 2015) and collaborate to elucidate the

patterns of composition and richness of helminths

associated with amphibians species.

Currently, there are around 49 species of

Odontophrynidae in Brazil (Segalla et al., 2019) in

this is inserted the genus Proceratophrys Miranda-

Ribeiro, 1920 that is currently composed for 40

species widespread along to south America with

records in Argentina, Brazil, and Paraguay (Frost,

2019). In Brazil, four species occur exclusively in

Caatinga biome, Proceratophrys cristiceps Müller,

INTRODUCTION

RESUMO

Palavras-chaves: Anfíbios – endoparasitas – hospedeiros – Nordeste – Reino Neotropical –Semiárido

Inventários parasitológicos de anfíbios da região semiárida contribuem para conhecer a diversidade de

parasitas associados a espécies da região Nordeste. Este trabalho tem como objetivo fornecer informações

sobre a diversidade de parasitas associados a Proceratophrys aridus Cruz, Nunes & Juncá, 2012 e

descrever e comparar a helmintofauna deste hospedeiro com as demais espécies inventariadas do gênero.

Os espécimes foram coletados manualmente entre 2012 e 2016 em dez localidades do Nordeste do Brasil.

Um total de 37 P. aridus foram necropsiados e analisados para endoparasitas, dos quais 22 foram

parasitados com pelo menos um táxon helminto. Para verificar a similaridade entre as comunidades

parasitas, foi realizada uma análise de agrupamento utilizando o índice de Sorensen. Para esta análise, foi

construída uma matriz com dados de presença e ausência para as espécies de helmintos relacionados ao

táxon Odontophrynidae. Um total de 867 helmintos foram recuperados, incluindo nematóides,

digenéticos e acantocéfalos, apresentando uma riqueza de oito espécies: Aplectana membranosa

(Schneider, 1866), Falcaustra mascula (Rud. 1819), Rhabdias breviensis Nascimento, Gonçalves, Melo,

Giese, Furtado, & Santos, 2013, Oswaldocruzia sp., Larvas de Cosmocercidae, trematódeos não

identificados e cistacantos. As espécies mais abundantes com maior prevalência e intensidade média de

infecção foram A. membranosa. Este estudo fornece três novos registros de helmintos parasitando P.

aridus, além de registrar infecções por trematódeos e acantocéfalos neste hospedeiro no nordeste do

Brasil. Proceratophrys aridus é a espécie da família Odontophrynidae com maior riqueza em helmintos já

registrada.

1883, Proceratophrys caramaschii Cruz, Nunes &

Juncá, 2012, Proceratophrys aridus Cruz, Nunes

& Juncá, 2012, and Proceratophrys ararype

Mângia, Koroiva, Nunes, Roberto, Ávila,

Sant'Anna, Santana & Garda, 2018. These species

cited above, only P. aridus has been inventoried for

its helminth fauna (Teles et al., 2017; Muller et al.,

2018).

Teles et al. (2017) recorded four taxa for P. aridus

(Rhabdias sp., Raillietnema spectans Gomes,

1964, Physaloptera sp., and Cosmocercidae

larvae), while Muller et al. (2018) researching the

phylogeny of Rhabdias in Brazil, identified

through the molecular biology Rhabdias breviensis

Nascimento, Gonçalves, Melo, Giese, Furtado, &

Santos, 2013 associated in a population of P. aridus

in South of Ceará State. The aim this work is

provided information about the diversity of

helminths associated the P. aridus species

widespread along to three Northeastern State.

Besides, we describe and to compare the helminth

fauna associated the P. aridus with other species

inventories for the genus in other localities.

Neotropical Helminthology, 2019, 13(2), jul-dic

170

Sousa Silva et al.

The specimens were collected between 2012 and

2016 in different municipalities from Ceará State:

Aiuaba (6º34'25"S, 40º07'25"W), Barro

(7º10'36''S, 38º46'54''W), Farias Brito (6º55'50''S,

39º33'56''W), Mauriti (7º23'21"S, 38º46'28"W),

Crato (7°13'39”S, 39°25'05”W), Barbalha

(7°19'16”S, 39°18'01”W), Missão Velha

(7°14'36”S, 39°09'00”W) and Santana do Cariri

(7°11'28"S, 39°44'13”W).

The specimens deposited in Herpetological

collection from Cariri Regional University

regarding two more states from northeastern also

were included: Piauí, Santo Antônio de Lisboa

municipality (06º58'53” S, 41º14'03” W) and

Pernambuco, Exú municipality (07º30'43” S,

39º43'27” W) (Fig. 1). The sample sites are

characterized by presents warm semiarid tropical

climate and semiarid smooth tropical climate

(IPECE, 2016).

A total of 37 specimens of P. aridus were collected

manually through of active search, euthanized with

thiopental sodium injection and necropsied for

helminths. The number of individuals collected in

each locality sampled has been provided closely

with its parasitological descriptors (Table 1). The

specimens had the following organs analyzed

under stereomicroscopic: liver, lung, heart,

stomach, intestines, celomatic cavity, and kidneys.

The following parasitological descriptors:

prevalence (P), mean intensity of infection (IMI),

and mean abundance (AM) has been calculated

following Bush et al. (1997) using standard error

and range.

The helminths were found alive, washed in saline

solution (0.9% NaCl), fixed and preserved in 70%

ethanol. The nematodes were cleared in

l a c t o p h e n o l o r l a c t i c a c i d w h i l e t h e

acanthocephalans were removed their cysts,

stained in carmim and cleared in creosote. All the

e n d o p a r a s i t e s w e r e o b s e r v e d u n d e r

stereomicroscopic of light DMLB (Leica) and DM

5000B with interferential phase contrast and

identified at the lowest possible level according to

the work of Yamaguti (1961), Sprent (1978),

Vicente et al. (1991), Anderson (2000) and

Gibbons (2010). The helminths were deposited

under the number CHIBB 8819 – 8838 in the

Helminthological Collection of the Institute of

Biosciences (CHIBB), São Paulo State University

(UNESP), municipality of Botucatu, SP, Brazil.

To verify the similarity between parasites

communities was building a matrix of data with

variables presence / absent to helminths species

related to Odontophrynidae family. The degree of

similarity between these communities of helminths

was calculated employing Sorensen index (So),

with a later clustering analyse using Cluster

method utilizing the mean of the unweighted pairs

(UPGMA). All analyzed were performed using the

software PAST 3.0.

Ethical Approval and/or Informed Consent

All procedures performed in studies involving

animals were in accordance with the ethical

standards of the institution or practice at which the

studies were conducted. The sampling of the

anuran specimens was authorized by the Instituto

Chico Mendes de Conservacão da Biodiversidade -

ICMBio (permit 29613-1) and to the ethics

committee of the Regional University of Cariri

(CEUA / URCA, process nº 00260 / 2016.1).

A total 37 host analyzed, 22 were parasitized at

least one helminth taxa (P = 59.5%; IMI = 185.1

±467.9; AM = 110.1 ±40.5; range 1-190). A total of

867 helminths were collected, included nematodes,

digenetics, and acanthocephalans, presenting a

richness of eight species: Aplectana membranosa

(Schneider, 1866), Falcaustra mascula (Rudolphi,

1819), R. breviensis (Nascimento, Gonçalves,

Melo, Giese, Furtado & Santos 2013),

O s w a l d o c r u z i a sp., P h y s a l o p t e r a s p . ,

Cosmocercidae larvae, trematodes unidentified

and cystacanths (Table 2). The most abundant

species with the highest prevalence and mean

intensity of infection was A. membranosa (n = 625;

P = 27%; IMI = 65.5 ±107.1).

The similarity between the helminth communities

of the five species of Odontophrynidae inventoried

was considered low, with P. aridus and

Proceratophrys mantiqueira Mângia, Santana,

MATERIALS AND METHODS

RESULTS

171

Neotropical Helminthology, 2019, 13(2), jul-dic Parasites of the frog Proceratophrys aridus

Figure 1. Sampled localities of Proceratophrys aridus collected in northeast Brazil. Source: QGIS 2.18.

Figure 2. Cluster analysis of species of the Odontophrynidae family for helminth fauna composition, cophenetic correlation

coefficient (ccc) = 0.92.

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Neotropical Helminthology, 2019, 13(2), jul-dic Sousa Silva et al.

between the other helminths communities of

species Proceratophrys genus were P. tupinamba e

P. boiei (So = 36.3%), P. tupinamba e P.

mantiqueira (So = 16.7%) e P. tupinamba e O.

americanus (So = 0), P. boiei e O. americanus (So

= 12.5%), P. boiei e P. mantiqueira (So = 22.2%) e

O. americanus e P. mantiqueira (So = 0) (Fig. 2).

Cruz & Feio, 2014 (So = 28.6%) being those with

the highest similarity among their parasite

populations, followed by P. aridus and

Proceratophrys boiei (Wied-Neuwied, 1825) (So =

15.3%), P. aridus and Proceratophrys tupinamba

Prado & Pombal, 2008 (So = 12.5%) and P. aridus

and Odontophrynus americanus (Duméril &

Bibron, 1841) (So = 9.5%). The similarities

Table 1. Parasitological descriptors of helminths associated P. aridus in ten municipalities from Northeastern

region, Brazil. Prevalence (%), mean abundance (AM), mean intensity of infection (IMI), standard error (SD), and

range.

Locality

Host % AM±SD IMI±SD Range

Aiuaba, CE

36.2±16.7 102.7±34.4 0-190

Barro, CE

15.6±0.4 19.5±70.7 0-75

Farias Brito, CE

33.3

1±1 0.33 0-1

Santana do Cariri, CE

66.7

1.5±1 1 0-2

Nova Olinda, CE

100

1±1 1 0-1

Crato, CE

100

1 1 0-1

Barbalha, CE

100

3 3 0-3

Mauriti, CE

100

24 24 1-24

Exú, PE

100

16 16 1-16

St. Ant. de Lisboa, PI 1100 1 1 0-1

Table 2. Helminth component community of P. aridus (n=37) from ten municipalities from northeast region, Brazil.

Prevalence (%), mean abundance (AM) and mean intensity of infection (IMI) following by standard error (SD), site

of infection (SI), and range. (*) new records.

Helminths

AM±SD

IMI±SD

Range

Locality

Nematoda

Aplectana membranosa*

16.9±4.32

65.5±107.1

Li, Si

1-181

Ba, Ma, No,

Bo, Ab

Falcaustra mascula*

2.7

0.05±0.16

2±2

0-2

Rhabdias

breviensis

13.5

0.14±0.24

1±0.9

1-5

Cr, No, Bo

Oswaldocruzia

sp.

2.7

0.03±0.08

1±1

0-1

Physaloptera

sp.

5.4

0.51±1.95

9.5±15.82

2-19

Bo, Ab

Cosmocercidae larvae

10.8

5.22±0.16

48.25±150.1

S, Li, Si

1-170

Ex, Sc, Ab, Fb

Digenea

Trematoda unidentied*

2.7

0.54±1.62

20±20

0-20

Acanthocephala

Cystacanth

5.4

0.05

1±0.97

1-2

Sa, Bo

(Site of infection: Cc = Coelomic cavity; Lung= L; Kidney = Kd; S = Stomach; Li = Large intestine; Si = Small intestine. Locality: Ba

– Barbalha, Ma – Mauriti, No - Nova Olinda, Bo - Barro, Ab - Aiuaba, Sc - Santana do Cariri, Cr - Crato, Fb - Farias Brito, Ex – Exú,

and Sa - Santo Antônio de Lisboa).

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Neotropical Helminthology, 2019, 13(2), jul-dic Parasites of the frog Proceratophrys aridus

Table 3. List of helminths related to the species of the family Odontophrynidae.

Host Parasites References

O. americanus

Myxidium immersum, Lutz 1889 Cordero (1928)

Oligacanthorhynchus sp. Smales (2007)

Rhabdias elegans

Gutierrez, 1945

González & Hamann

(2009)

Cosmocerca parva

Travassos, 1925

Cosmocerca podicipinus, Baker and Vaucher, 1984

C. uruguayensis

Lent & Freitas 1948

Hamann &

González

(2009); Campião et

al.

(2014)

Travtrema

aff. stenocotyle

Cohn, 1902

Echinostomatidae gen. sp.

Aplectana

membranosa

(Schneider, 1866) Miranda,

1924

meridionalis

Lent & Freitas 1948

Styphlodora

sp.

Opisthogonimus

sp.

O. cf. barrioi

Falcaustra sanjuanensis

González, Sanabria &

Quiroga, 2013

González et al.

(2013)

P. tupinamba

Aplectana delirae

Fabio, 1971

Boquimpani-Freitas et

al. (2001)

Cosmocerca brasiliense

Travassos, 1925

Cosmocerca cruzi

Rodrigues & Fabio, 1970

Physaloptera sp.

Rhabdias androgyna

Kloss 1971

Schulzia travassosi

Durette-Desset, Baker and

Vaucher, 1985

Unidentied Cestoda

P. boiei

Aplectana delirae

Fabio, 1971

Klaion et al. (2011)

Cosmocerca parva

Travassos, 1925

Oxyascaris oxyascaris

Travassos, 1920

Physaloptera

sp.

P. mantiqueira

Cosmocercidae

larvae

Almeida-Santos et al.

(2017)

Physaloptera sp.

Oxyascaris sp.

Oswaldocruzia lopesi

Freitas & Lent, 1938

Rhabdias sp.

P. aridus

Rhabdias

breviensis

Teles et al. (2017)

Muller et al. (2018)

Present study

Railietnema spectans

Physaloptera

sp.

Cosmocercidae larvae

Aplectana membranosa

Falcaustra mascula

Oswaldocruzia sp.

Unidentied Trematoda

Cystacanth

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Neotropical Helminthology, 2019, 13(2), jul-dic Sousa Silva et al.

Proceratophrys aridus is the species of the genus

that presented the highest richness of parasites

among the others investigated (Cordero, 1928;

Boquimpani-Freitas et al., 2001; Smales, 2007;

González & Hamann, 2009; Hamann & González,

2009; Klaion, 2011; Almeida-Santos et al., 2017;

Teles et al., 2017) (Table 3). This can be explained

in the function of the sampled effort, the richness of

parasite species is directly influenced by this

variable (Campião et al., 2015). Thus, in this study,

the sampled effort was important for growing up

the richness of helminths associated P. aridus

among congeners.

Brazil is one of the countries of South America that

more research helminths of amphibians (Martins-

Sobrinho et al., 2017). The present study provides

three new records of helminths parasitizing P.

aridus in the northeast region from Brazil.

Regarding other works as Almeida-Santos et al.

(2017) and Teles et al. (2017) we recording besides

of infection by nematodes, the presence of

digenetic trematodes and cystacanths associated in

this host, thus totalizing fifteen species of

Nematoda, one record of Cestoda, Trematoda, and

cystacanth for the genus Proceratophrys.

The Aplectana genus currently is composed of 28

species distributed in the Neotropical realm

(Gomez et al., 2017). In this study, A. membranosa

was species that present the highest prevalence and

intensity of infection. Considered monoxenic cycle

life this parasite, the infection occurs through the

penetration of the host skin (Anderson, 2000), thus

the terrestrial habit and forage behavior of the host

can have the exposure it highest risk of infection for

this parasite.

In Brazil, occurs nine species of the genus

Aplectana that infecting amphibians: A.

crossodactyli (Vicente & Santos, 1970), A. crucifer

Travassos, 1925, A. delirae Fábio, 1971, A. lopesi

Silva, 1954, A. membranosa (Schneider, 1866), A.

meridionalis Lent & Freitas, 1948, A. micropenis

Travassos, 1925, A. pintoi Travassos, 1925 and A.

vellardi Travassos, 1926. In Brazilian Northeast,

only A. membranosa has records infecting hosts

Leptodactylus labyrinthicus (Spix, 1824), L.

syphax Bokermann, 1969 and Dermatonotus

muelleri (Boettger, 1885) (Vicente et al., 1991;

Lins et al., 2017; Alcantara et al., 2018). This work

presents the first record of infection by A.

m e mb r a no s a p arasi tizi n g a speci es of

Proceratophrys genus.

The genus Falcaustra Lane, 1915 has 13 species

distributed throughout the Neotropical realm

(Bursey et al., 2018). In Brazil, there are records of

the occurrence of three species parasitizing

amphibians, lizards and snakes: Falcaustra

belemensis Baker and Bain, 1981 (Goldberg et al.,

2007), F. tikasinghi (Schoenecker, Schmidt &

Everard, 1977) Baker & Bain, 1981 (Baker & Bain

1981; González et al., 2013) and F. mascula

(Rudolphi, 1819; Gomes & Vicente, 1966; Vicente

et al., 1991; Goldberg et al., 2007; Teles et al.,

2014). Little is known about the life cycle of F.

mascula, however, some evidence indicates that it

has a heteroxenic cycle (Anderson, 2000; González

et al., 2013; Teles et al., 2014). Procetatophrys

aridus represents the second species of the

Odontophrynidae family to be recorded infected by

the genus Falcaustra (González et al., 2013).

To R. breviensis, Muller et al. (2018) reports the

multiple lineages presence of this species in Brazil.

One of this lineages has been recorded in the

Northeast region (Piauí and South Ceará state)

associated Leptodactulus fuscus (Schneider,

1799), Rhinella jimi (Stevaux, 2002) and P. aridus.

This reports confirm the presence of this species

outside type locality (Pará, Amazônic Region)

expanding their spacial distribution and their hosts,

which until then were only Leptodactylidae,

evidencing its generalist character. Our reports

overlap other records as Muller et al. (2018)

confirm the presence of this lineage of R. breviensis

in the Northeast region. The records of Teles et al.

(2017) and Muller et al. (2018) were both from

Aiuaba locality, Ceará state, thus the records of

Rhabdias sp. in effect is R. breviensis.

The genus Oswaldocruzia Travassos, 1917 has 88

species around the world (Svitin & Kuzmin, 2012),

43 reported in Neotropical realm, 14 in a South

America, only eight recorded in amphibians and

reptiles in Brazil designated to following

Bufonidae, Ceratophynidae, Craugastoridae,

Dendrobatidae, Hylidae, Leptodactylidae e

Microhylidae taxa (Guerreiro, 2013; Campião et

DISCUSSION

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Neotropical Helminthology, 2019, 13(2), jul-dic Parasites of the frog Proceratophrys aridus

al., 2014; Willkens et al., 2016). Almeida-Santos et

al. (2017) reported for the first time O. lopesi

Freitas and Lent, 1938 in P. mantiquiera in rain

forest in Brazilian southeastern. We present the

second records for the family and the first to P.

aridus, expanding this relation from the Brazilian

northeast.

Proceratophrys genus composes a taxon of diurnal

toads, rugged skin that lives in litter leaf.

Considering the ecological aspects similarity such

as foraging mode and diet of the four species

investigated for this genus, we observed that these

aspects were not determinant for the helminth

assemblage composition. (Boquimpani-Freitas et

al., 2001; Almeida-Santos et al., 2017). By the

other hand, the geographical distance between the

species can be a factor considered (Poulin, 2018).

The low similarity between the communities of

helminths of P. aridus and their congeners can be

explained by the distribution of these species

(Poulin, 2003; Poulin et al., 2011).

Procetatophrys aridus has a restricted occurrence

in the Brazilian Northeast (Cruz et al., 2012), while

P. tupinamba, P. mantiqueira and P. boiei occur

mainly in humid forests of southeastern Brazil

(Boquimpani-Freitas et al., 2001; Klaion et al.,

2011; Almeida-Santos et al., 2017), a factor that

justifies higher values of similarity between the

helminth communities among these sympatric

hosts. Besides, the phylogenetic proximity may

also justify the similarities between the species P.

tupinamba and P. mantiqueira (Proceratophrys

a p p e n d i c u l a t a group) and P. b o i e i

(Proceratophrys boiei group) (Prado & Pombal Jr.,

2008; Almeida-Santos et al., 2017; Mângia et al.,

2018).

All helminths associated with Procetatophrys

genus can be considered generalists because they

occur in several other amphibian taxa (González &

Hamann, 2008; Campião et al., 2014; Muller et al.,

2018). However, it should be considered that

species that compose the community of P. boiei

parasites such as Cosmocerca parva Travassos,

1925 and Oxyascaris oxyascaris Travassos, 1920

also have records for the northeastern region (Teles

et al., 2015; Silva et al., 2018). The non-occurrence

of these species in this study does not imply that

they do not parasite P. aridus but may be related

mainly to the effort employed, corroborating the

implications of the sample effort relationship with

the richness of parasite species (Campião et al.,

2015). Besides, the proximity between the

communities of P. aridus and P. mantiqueira is due

more to the number of helminth taxa not

determined than the species shared by these hosts.

Parasitic communities provide great models for

exploring various subjects related to interspecific

associations, community structure, and species

richness or diversity determinants (Poulin, 2018).

The higher species and localities are inventoried

concerning their helminth fauna, the greater the

data set that will able to available to trace the

distribution, occurrence, and coevolution patterns

of endoparasite and their host relationships.

To the Coordenação de Aperfeiçoamento de

Pessoal de Nível Superior-CAPES-for research

fellowships to D. H. Morais (CAPES/PNPD

22005013001P4) and Fundação para o apoio e a

Pesquisa do Estado de São Paulo (FAPESP/

12/24945-1). R.W.A. thanks Conselho Nacional de

Desenvolvimento Científico e Tecnológico

(CNPq) for providing research fellowship (PQ #

303622/2015-6305988/2018-2) and D.H.M (PQ

process #313241/2018-0).

Alcantara, EP, Silva, CF, Silva, LAF, Lins, AGS,

Ávila, RW, Morais, DH & Silva, RJ. 2018.

Helminths of Dermatonotus muelleri

(Anura: Microhylidae) from Northeastern

Brazil. Journal of Parasitology, vol. 104, pp.

550-556.

Almeida-Santos, M, Siqueira, CC, Anjos, LA,

Sluys, MV & Rocha, CFD. 2017.

Ecological aspects of the horned leaf-frog

P r o c e r a t o p h r y s m a n t i q u e i r a

(Odontophrynidae) in an Atlantic

Rainforest area of southeastern Brazil.

Salamandra vol. 53, pp. 413–422.

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