The diversity of helminths in host groups with a high diversity of species like anurans are still

underrepresented, especially in sites with severe environmental conditions such as arid and semiarid

regions is needed to understand the role of parasites at different levels of ecological . This knowledge

organization. This study aimed to evaluate the parasite composition a taxocenosis of anuran species,

describe the richness and diversity of helminths at the component and infracommunity levels, and

evaluate the influence of body size on the abundance and diversity of parasites. The anuran hosts were

collected at the Environmental Protection Area (EPA) Bica do Ipu in Brazilian semi-arid. The collected

hosts were euthanized, necropsied, and examined for helminth parasites. Helminths were identified and

the statistical tests were performed. A total of 15 host species composed this study and 1,216 helminths

were collected with mean abundance (MA) of 12.9 ± 3.38 and mean intensity of infection (MII) of 25.84 ±

6.44. The mean richness of helminth was 2.3 ± 0.53 (range = 6) and helminth diversity (H´) was 1.36.

Helminths infecting the studied amphibian hosts comprised 13 taxa: two cestode species, one

acanthocephalan, one trematode, and nine nematodes. The present study contributes to the knowledge of

the helminths infecting amphibians from Brazilian Caatinga, as well as the understanding of the diversity

patterns of parasitic infracommunities associated with amphibians.

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

Neotropical Helminthology, 2020, 14(2), jul-dic:207-216.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

HELMINTHS ASSOCIATED WITH 15 SPECIES OF ANURANS FROM THE IBIAPABA PLATEAU,

NORTHEASTERN BRAZIL

HELMINTOS ASOCIADOS CON 15 ESPECIES DE ANUROS DE LA MESETA DE IBIAPABA, EN EL

NORESTE DE BRASIL

1Universidade Federal da Paraíba, Programa de Pós-graduação em Ciências Biológicas- PPGCB (Zoologia). Via expressa

Padre Zé Jardim Cidade Universitária 58051001. João Pessoa, PB – Brasil, tel: (83) 32167025.

2Section of Parasitology, DBBVPZ, Universidade Estadual Paulista “Jülio Mesquita Filho”, Brazil, Research and Teaching

Laboratory of Wild Animals, Federal University of Uberlândia, Brazil

3Programa de Pós-graduação em Ecologia e Recursos Naturais, Bloco 209, Centro de Ciências, Universidade Federal do

Ceará- UFC, Campus do PICI, Av. Humberto Monte s/n, 60455-760 Fortaleza, Ceará, Brasil.

4UFU – Universidade Federal de Uberlândia - Instituto de Ciências Agrárias, LMG-746, Km 1, Monte Carmelo, 38500-000,

MG, Brasil.

* Corresponding author: aldenirferreira_@hotmail.com

1* 2 3

Aldenir Ferreira da Silva Neta ; Edna Paulino de Alcantara ; Cicero Ricardo de Oliveira ; Elvis Franklin

4 2 3

Fernandes de Carvalho³; Drausio Honorio Morais ; Reinaldo José da Silva & Robson Waldemar Ávila

Neotropical Helminthology

207

doi:10.24039/rnh2020142795

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14,Number2(jul-dec)2020

ABSTRACT

Keywords: Amphibians – Inventory – Endoparasites – Nematodes – Mountain swamp – Semi-arid

INTRODUCTION

208

RESUMEN

Palabras clave: Anfibios – Inventario – Endoparásitos – Nematodos – Pantano de montaña – Semiárido

La diversidad de los helmintos en los grupos de huéspedes con gran diversidad de especies como los

anfibios anuros siguen estando subrepresentados, especialmente en sitios con condiciones ambientales

severas como las regiones áridas y semiáridas. Este conocimiento es necesario para comprender el papel

de los parásitos en los diferentes niveles de la organización ecológica. Con el fin de evaluar la

composición del parásito una taxocenosis de las especies de anuros, describir la riqueza y diversidad de los

helmintos a nivel de componentes y de la infracomunidad; además de evaluar la influencia del tamaño del

cuerpo en la abundancia y diversidad de los parásitos, se realizó este estudio. Los anuros huéspedes se

recogieron en la Zona de Protección Ambiental (EPA) Bica do Ipu en el semiárido brasileño. Los

huéspedes recolectados fueron sometidos a eutanasia y a una necropsia en busca de parásitos. En

secuencia, se identificaron los helmintos y se realizaron las pruebas estadísticas. Un total de 15 especies de

huéspedes compusieron este estudio y se recogieron 1.216 helmintos con abundancia media (MA) de 12,9

± 3,38 y intensidad media de la infección (MII) de 25,84 ± 6,44. La riqueza media de helmintos fue de 2,3

± 0,53 (rango = 6), y la diversidad de helmintos (H) fue de 1,36. La comunidad de componentes de

helmintos que infectan a los anfibios huéspedes comprende 13 taxones: dos especies de cestodos, un

acantocéfalo, un trematodo y nueve nematodos. El presente estudio contribuye al conocimiento de los

helmintos que infectan a los anfibios de la Caatinga brasileña, así como a la comprensión de los patrones

de diversidad de las infracomunidades parasitarias asociadas a los anfibios.

Neotropical Helminthology, 2020, 14(2), jul-dic

intracorporeal surface, increasing the possibilities

of oral and skin infection (Santos & Amato, 2010;

Campião et al., 2016b; Hamann et al., 2009).

Amphibian's biology makes it an excellent model

for evaluating patterns in the structure of helminth

communities (Aho, 1990). They occupy a variety

of habitats, have different patterns of life cycle,

different reproductive strategies, and occupy

various positions in food webs (Koprivnikar et al.,

2012). Studies on amphibian parasites have

increased in recent years (e.g. Campião et al.,

2016a; Oliveira et al., 2019). However,

information about the parasites of some amphibian

groups is still scarce, and most of restricted to

taxonomic descriptions or records of occurrence

(Pinhão et al., 2009).

Brazil has the most diverse anuran fauna, with

1,137 species (Segalla et al., 2019). Nevertheless,

there are helminth reports for only 185 (7%)

species. About 164 helminth species are currently

known for Brazilian amphibians, totaling 57% of

the taxa described for South America. However,

studies describing the ecological aspects of

parasites associated with Brazilian amphibian

taxocenosis remain underrepresented in the

literature (Toledo et al., 2017; da Graça et al.,

2017). Data scarcity is even more pronounced in

Documenting parasite diversity and host

relationships are needed to understand the role of

parasites at different levels of ecological

organization (Wood & Johnson, 2015). Parasites

can affect host immunity and population dynamics,

thus having effects on community composition and

trophic interactions also acting on population

control (Bittencourt & Rocha, 2003; Hudson,

2005). Although play essential roles in ecological

processes, parasites remain taxonomically

neglected and the actual number of species in

different groups cannot yet be determined

(Windsor, 1998; Poulin & Morand, 2004).

The interaction host-parasite is an outcome of their

coevolutionary history, diet, body size, sex,

infection site, geographic distribution, behavior,

host species, climatic characteristics, and host

phylogeny (Muzzall et al., 2001; Araujo-Filho et

al., 2017)–––. Anurans can act as definitive,

intermediate, and paratenic hosts of a wide variety

of helminths (Campião et al., 2009; Santos &

Amato, 2010; Campião et al., 2014). Body size is a

determining factor for the composition of the

anuran parasite community, due to the greater

amount of food eaten and added extra and

Silva Neta et al.

209

snout–vent length (SVL) of each specimen was

recorded. During necropsy, hosts were sexed and

the organs like gastrointestinal tract, lungs, liver,

and kidneys were separated and surveyed for

helminths under stereomicroscope. Voucher hosts

were fixed with 10% formalin, conserved with

70% ethanol and deposited at the Herpetological

Collection of the Universidade Regional do Cariri

(URCA 9127-9132, 9134-9143, 9145-9148, 9152-

9185, 9187-9202, 9107-9211, 9226-9229, 9232-

9239, 9241-9245), municipality of Crato, Ceará

state, Brazil.

Helminths were fixed in hot alcohol and preserved

in 70% ethyl alcohol. For identification, the

nematodes were clarified in lactic acid, and

cestodes, trematodes, and acanthocephalans were

stained with hydrochloric carmine and cleared with

creosote. Thereafter, the helminths were mounted

in temporary slides and examined under the light

microscope ZEISS Axio Imager M2. Species

identification followed Travassos et al. (1969),

Vicente et al. (1991), and recent bibliographies.

The voucher species were deposited at the

Herpetological Collection of Universidade

Regional do Cariri.

Parasitological descriptors follow Bush et al.

(1997): prevalence, intensity, and abundance of

infection were calculated, followed by their

respective standard errors. All values are expressed

as the mean ± standard error (SE). Parasites'

abundance data were tested for normality by the

Kolmogorov-Smirnov test. To calculate the wealth

and diversity of the community we use the species

richness (= total number of helminth species),

Shannon index (H′) (Zar, 2010). The

Berger–Parker index of dominance (d) was used to

determine the most dominant species (Magurran,

2004). Spearman's rank test (rs) was used to assess

the relationship between the host body size and

parasitological descriptors. Statistical analyses

were performed using BioEstat 5.0 (Ayres et al.,

2007) and software R platform, version 2.15.0 (RC

team, 2017).

Ethic aspects

Instituto Chico Mendes de Conservação da

Biodiversidade (ICMBIO) for collection permits

(ICMBio number 32758-1). To Comitê de Ética em

Pesquisa of the Universidade Regional do Cariri,

permits 00026/2015.

semi-arid regions where amphibians are strongly

influenced by unpredictable rainfall. Severe

environmental conditions in arid and semiarid

regions may limit species diversity by selecting

clades tolerant to such conditions while shaping

their ecology, natural history, and behavior (Garda

et al., 2017).

Therefore, the objectives of this study were: (1)

evaluate the parasite composition of 15 anuran

species; (2) describe the richness and diversity of

helminths at the component and infracommunity

levels; (3) to evaluate the influence of body size on

the abundance, diversity, and richness in anurans of

Caatinga, Brazil.

Anurans were sampled from the Environmental

Protection Area (EPA) Bica do Ipu (4°19'10” S,

40°43'04” W), Ipu municipality, Ceará state, Brazil

(Fig. 1). The EPA Bica do Ipu, is located at the

slopes of the Ibiapaba plateau with an extension of

3,500 ha approximately. The Ibiapaba plateau is a

highland marsh (known as brejo de altitude)

composed by a mosaic of phytophysiognomies

(Santos & Souza, 2012).

Amphibians (n = 92 specimens), comprising

representatives of five families: Bufonidae:

Rhinella jimi (Stevaux, 2002) (n = 1), Rhinella

granulosa (Spix, 1824) (n = 11); Hylidae:

Corythomantis greeningi Boulenger, 1896 (n = 1),

Scinax x-signatus (Spix, 1824) (n = 4);

Phyllomedusidae: Pithecopus nordestinus

(Caramaschi, 2006) (n = 4); Leptodactylidae:

Leptodactylus fuscus (Schneider, 1799) (n = 4),

Leptodactylus macrosternum Miranda-Ribeiro,

1926 (n = 4), Leptodactylus mystaceus (Spix,

1824) (n = 1), Leptodactylus vastus Lutz, 1930 (n

= 6), Physalaemus albifrons (Spix, 1824) (n = 21),

Physalaemus cicada Bokermann, 1966 (n = 9),

Physalaemus cuvieri Fitzinger, 1826 (n = 3),

Pleurodema diplolister (Peters, 1870) (n = 10),

Pseudopaludicola mystacalis (Cope, 1887) (n =

12); Odontophrynidae: Proceratophrys cristiceps

(Müller, 1883) (n = 1) were captured by hand

during visual surveys from 7 to 15 April 2014.

Specimens were euthanized with intraperitoneal

injection of Propofol (CFMV, 2013), after the

MATERIAL AND METHODS

Neotropical Helminthology, 2020, 14(2), jul-dic Helminths associated with anurans from Brazil

The richness found in the present study is similar to

other studies dealing with the helminth community

associated with anurans (Aguiar et al., 2014;

Campião et al., 2014; 2016a; da Graça et al., 2017;

Müller et al., 2018). However, it may be

underestimated because of unidentified species,

since the occurrence of cryptic species has already

been recorded for the region, as in Rhabdiasidae

(Müller et al., 2018). Also, larger numbers of

nematode species seem to be a general pattern for

South American amphibians (Campião et al.,

2014).

Monoxenous nematodes, such as R. spectans and

O. mazzai, infected more host species. According

to Anderson (2000), parasites with direct life cycles

have low specificity and simple mode of

transmission that can occur through egg ingestion

or larval penetration through the host skin.

Moreover, R. spectans and O. mazzai have been

recorded infecting several Brazilian anurans,

including P. diplolister, Dermatonotus muelleri

(Boettger, 1885), Leptodactylus latrans (Steffen,

1815), Rhinella crucifer (Wied Neuwied, 1821),

Rhinella icterica (Spix, 1824), L. fuscus, L.

mystaceus, Physalaemus albifrons, P. cicada, and

P. cuvieri (Campião et al., 2014; Teles et al., 2015;

Alcantara et al., 2018; Oliveira et al., 2019).

Cylindrotaenia americana is also a monoxenous

parasite infecting the intestinal mucosa (Stumpf,

1981). Actually, it has been reported in North and

South America, Asia, and Europe in hosts of the

families Bufonidae, Ranidae, Hylidae,

Brachycephalidae, and Dendrobatidae (Goldberg

& Bursey, 2008). In Brazil, there are records of this

cestode species infecting R. icterica, Rhinella

fernandezae (Gallardo, 1957), Ischnocnema

guentheri (Steindachner, 1864), Hypsiboas

prasinus (Burmeister, 1856) (Campião et al.,

2014), Ischnocnema parva (Girard, 1853),

Hylodes phyllodes Heyer & Cocroft, 1986 (Aguiar

et al., 2014), and P. cicada (Oliveira et al., 2019).

Pleurodema diplolister is a new host recorded for

C. americana.

A c a n t h o c e p h a l a n s o f t h e g e n u s

Oligacanthorhynchus are heteroxenous and

usually have mammals as final hosts (Gallas &

Of the 92 analyzed hosts, 44 (47.8%) were

parasitized with at least one helminth species. Only

three analyzed host species presented no infection

with helminth parasites (C. greening, R. jimi, and S.

x-signatus). A total of 1,190 helminths from 13 taxa

was recovered from 12 hosts of five anuran

families (Table 1), with mean abundance of 12.9 ±

3.38 and mean intensity of infection of 25.84 ±

6.44. Helminth diversity (H`) was 1.36. The mean

helminth richness was 2.3 ± 0.53 (max. = 6) species

per infected host.

Schrankiana sp. and Raillietnema spectans

Gomes, 1964 were the most abundant taxa (d =

0.39, d = 0.36 respectively). Oswaldocruzia mazzai

Travassos, 1935 and R. spectans were the helminth

taxa that infected the greatest number of host

species (8 and 9, respectively). The nematodes

Aplectana membranosa Schneider, 1866,

Ochoterenella sp., Parapharyngodon sp., and

Physaloptera sp. larvae were found only in anuran

species. The digenean Gorgoderina parvicava

Travassos, 1922 was found only in L. vastus.

Cylindrotaenia americana Jewell, 1916 (Cestoda),

and Oligacanthorhynchus sp. (Acanthocephala)

were found only in P. diplolister (Table 1).

The highest intensity of parasites was found in the

rufous frog L. fuscus (n = 446). Pleurodema

diplolister and R. granulosa were the hosts

exhibiting the highest helminth richness (n = 6).

The diversity of the helminths tended to be greatest

in P. cicada (H' = 1.15) followed by L. vastus (H'=

1.03) (Table 2).

The overall host body size correlated positively

with richness (rs = 0.542, p < 0.001) and abundance

of parasites (rs = 0.578, p < 0.001). Considering the

analysis of each anuran host species, it was also

observed a significant positive correlation with

abundance and parasite richness for P. albifrons

(abundance/length: rs = 0.489, p = 0.02;

richness/length: rs = 0.475, p = 0.02) and P.

diplolister (abundance/length: rs = 0.882, p <

0.001; richness/length: rs = 0.740, p = 0.01).

However, for L. vastus, the relation of abundance

and length was negatively correlated (rs = -0.941, p

= 0.01) (Table 3).

210

RESULTS DISCUSSION

Neotropical Helminthology, 2020, 14(2), jul-dic Silva Neta et al.

(11)

Parasite taxa d % MA ± SE Range

Number of parasites/host species

Lfus

(4)

Lmac

(4)

Lmys

(1)

Lvas

(6)

Phal

(21)

Phci

(9)

Phcu

(3)

Pinor

(4)

Pldi

(10)

Prca

(1)

Psmy

(12)

Rhgr

Acantocephala

Oligacanthorhynchus sp. 0.003 1.1 0.01 ± 0.01 4 4

Cestoda

Cylindrotaenia americana 0.003 1.1 0.01 ± 0.01 4 4

Unidentiﬁed 10 10

Digenea

Gorgoderina parvicava 0.0008 1.1 0.01 ± 0.01 10 10

Nematoda

Aplectana membranosa 0.0008 1.1 0.01 ± 0.01 1 1

Falcaustra mascula 0.04 4.35 0.58 ± 0.36 1-31 49 1

Ochoterenella sp. 0.0008 1.1 0.01 ± 0.01 1 1

Oswaldocruzia mazzai 0.18 18.5 2.34 ± 1.19 1-104 104 60 16 20 1 12 1 1

Parapharyngodon sp. 0.0008 1.1 0.01 ± 0.01 1 1

Physaloptera sp. larvae 0.0008 1.1 0.01 ± 0.01 1 1

Raillietnema spectans 0.36 19.6 4.59 ± 2.16 1-180 20 56 4 9 4 3 2 218 109

Rhabdias sp. 0.007 3.3 0.09 ± 0.07 1-7 1 1 7

Table 1. Helminths recorded in the 12 host species collected in the Environmental Protection Area (EPA) Bica do Ipu, Ceará, Brazi. Dominance

(d), prevalence (%), mean abundance (MA) ± standard deviation (SE), range and number of parasites/host species are presented. Lfus =

Leptodactylus fuscus; Lmac = L. macrosternum; Lmys = L. mystaceus; Lvas = L. vastus; Phal = Physalaemus albifrons; Phci = P. cicada; Phcu

= P. cuvieri; Pinor = Pithecopus nordestinus; Pldi = Pleurodema diplolister; Prca = Proceratophrys caramaschii; Psmy = Pseudopaludicola

mystacalis; Rhgr = Rhinella granulosa. The number in parenthesis is the number of studied hosts.

211

Neotropical Helminthology, 2020, 14(2), jul-dic Helminths associated with anurans from Brazil

and three Amazonian strains infecting anurans in

the northeast region: Rhabdias breviensis

Nascimento et al. 2013 in R. granulosa from Piauí

state, Rhabdias pseudosphaerocephala Kuzmin,

Tkach & Brooks, 2007 in Rhinella jimi from Piauí

and Ceará states, and R. cf. stenocephala in

Leptodactylus vastus and L. macrosternum.

Rhabdias spp. are pulmonary parasites of anurans

and lizards (Baker, 1987; Teles et al., 2015;

Campião et al., 2016a; Toledo et al., 2017; Teles et

al., 2018). Rhabdias spp. are cryptic species, so

only with classical taxonomy, without the help of

molecular, it was not possible to precisely identify

the species.

Variation in host specificity may determine the

structure of helminth communities (Toledo et al.,

Silvera, 2012; Richardson et al., 2014). Eventually,

some vertebrates can act as paratenic hosts

(Yamaguti, 1963; Goldberg & Bursey, 2004), in

this case, the parasites can encyst until they reach

the proper host (Baker, 2007). In South America,

Oligacanthorhynchus sp. was recorded infecting

Odontophrynus americanus (Duméril & Bibron,

1841) in Paraguay (Campião et al., 2014). Thus P.

di pl oli st er is a new host record for

Oligacanthorhynchus sp.

Currently, the genus Rhabdias is composed of 84

species (Kuzmin & Tkach, 2018), being 18

reported in Neotropical anurans (Kuzmin et al.,

2016; Willkens et al., 2020). Müller et al. (2018)

assessing the molecular diversity of Rhabdias in

Brazil, reports the occurrence of cryptic species

Component community Lfus

(4)

Lmac

(4)

Lmys

(1)

Lvas

(6)

Phal

(21)

Phci

(9)

Phcu

(3)

Pinor

(4)

Pldi

(10)

Prca

(1)

Psmy

(12)

Rhgr

(11)

Richness

4 2 1 4

1 6

Diversity (H′) 0.72

0.08 0 1.03

0.98

1.15

0.69

0.46

0 0.98

Dominance (d)

0.70

0.90 - 0.60

0.60

0.50

0.90

- 0.50

Dominant species S Om - Fm Om Rs - Rs Rs - - S

S = Schrankiana sp.; Om = Oswaldocruzia mazzai; Fm = Falcaustra mascula; Rs = Raillietnema spectans.

Table 2. Ecological indices of parasite communities from species of anuran hosts collected in the Environmental

Protection Area (EPA) Bica do Ipu, Ceará, Brazi. Lfus = Leptodactylus fuscus; Lmac = L. macrosternum; Lmys = L.

mystaceus; Lvas = L. vastus; Phal = Physalaemus albifrons; Phci = P. cicada; Phcu = P. cuvieri; Pinor =

Pithecopus nordestinus; Pldi = Pleurodema diplolister; Prca = Proceratophrys caramaschii; Psmy =

Pseudopaludicola mystacalis; Rhgr = Rhinella granulosa. The number in parenthesis is the number of studied hosts.

212

Neotropical Helminthology, 2020, 14(2), jul-dic Silva Neta et al.

Table 3. Spearman correlation (r ) between richness/abundance and the body size of anuran hosts collected in

Ibiapaba plateau, Northeastern Brazil. N – number of studied hosts. *values statistically significative (p < 0.05).

Hosts

Richness Abundance

rs p rs p

Physalaemus albifrons

0.47 0.029* 0.48 0.02*

Physalaemus cicada

0.54 0.11 0.63 0.05

Pleurodema diplolister

0.74 0.010* 0.88 < 0.001*

Leptodactylus fuscus

0.25 0.75 0.20 0.91

Rhinella granulosa

-0,06 0.83 -0.51 0.11

Leptodactylus macrosternum

-0.25 0.75 -1.00 0.08

Pseudopaludicola mystacalis

0.50 0.10 0.50 0.10

Leptodactylus vastus

-0.75 0.10 -0.94 0.01*

Total hosts 84 0,54 < 0.001* 0.57 < 0.001*

213

ACKNOWLEDGMENTS

Neotropical Helminthology, 2020, 14(2), jul-dic Helminths associated with anurans from Brazil

abundance of parasite species. According to Toledo

et al. (2017), this fact may be related to the greater

surface area available for colonization by parasites,

as well as the greater intake and more diversified

diet of larger frogs. However, an interesting case

was observed for L. vastus, in which the abundance

of parasites were negatively correlated with host

size, contrasting to the pattern mentioned above

(Poulin, 2004; Yoder & Coggins, 2007; Ibrahim,

2008; Hamann et al., 2012, 2013; Campião et al.,

2016b; Toledo et al., 2015, 2017).

The present study contributes to the knowledge of

the helminths infecting amphibians from Brazilian

Caatinga, as well as the understanding of the

diversity patterns of parasitic infracommunities

associated with amphibians.

We thank the Conselho Nacional de

Desenvolvimento Científico e Tecnológico

(CNPq) by the grants to A.F.S.N. (#141572/2019-

1), E.P.A. (#141322/2018-7), R.W.A.

(#303622/2015-6; #305988/2018-2), D.H.M.

(#313241/2018-0) and R.J.S. (#309125/2017–0),

PROTAX (#440496/2015–2) and the financial

support of Coordenação de Aperfeiçoamento de

Pessoal d e Nível Superior - C APES

(#88887.501922/2020-00) and Fundação de

Amparo à Pesquisa do Estado de São Paulo –

FAPESP (#2016/50377–1).

2017). Herein, R. spectans, O. mazzai,

Schrankiana sp., and Rhabdias sp. may be

considered generalists and infected more than one

host species. Thus, sympatric hosts, although

phylogenetically distant may share some helminth

taxa, as they are exposed to similar environmental

conditions (Krasnov et al., 2012; Lima et al., 2012;

Brito et al., 2014). Schrankiana sp. has been

recorded in amphibians from the Hylidae and

Leptodactylidae families (Goldberg et al., 2007;

Campião et al., 2014; Müller et al., 2018; Oliveira

et al., 2019). This is the first record for Bufonidae

®. granulosa).

The high pattern of infection, abundance, and

prevalence was evident among individuals of R.

granulosa and L. fuscus. In general, members of

the Leptodactylidae are associated with terrestrial

habitats being frequently found closer to water

bodies, which may expose then to both aquatic and

terrestrial parasites (Campião et al., 2016a).

Host body size can influence the establishment of

parasite communities; usually larger individuals

offer larger colonization areas providing adequate

resources for parasite development and

reproduction (Poulin, 2004; Campião et al.,

2016b). Besides, some studies suggest that body

size influence on species richness and abundance

of parasitic helminths (Yoder & Coggins, 2007;

Ibrahim, 2008; Hamann et al., 2012, 2013; Toledo

et al., 2015, 2017). In the present study, the overall

size and the size of some amphibian individuals

were a determining factor in the richness and

Figure 1. Map of the study site in the municipality of Ipu, Ceará state, northeastern Brazil.

214

Aguiar, A, Morais, DH, Cicchi, PJP & Silva, RJ.

2014. Evaluation of helminths associated

with 14 amphibian species from a

neotropical Island near the southeast coast

of Brazil. Herpetology Review, vol. 45, pp.

227–236.

Aho, JM. 1990. Helminth communities of

amphibians and reptiles: comparative

approaches to understanding patterns and

processes. In: Parasite Communities:

Patterns and Processes. Springer

Netherlands, Dordrecht, pp 157–195.

Alcantara, EP, Ferreira-Silva, C, 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.

Anderson, RC. 2000. Nematode parasites of

vertebrates. Their development and

transmission., 2 ed. Guelph, Ontario,

Canada.

Araujo-Filho, JA, Brito, SV, Lima, VF, Pereira,

AMA, Mesquita, DO, Albuquerque, RJ &

Almeida, WO. 2017. Influence of temporal

variation and host condition on helminth

abundance in the lizard Tropidurus hispidus

from north-eastern Brazil. Journal of

Helminthology, vol. 91, pp. 312–319.

Ayres, M, Ayres Jr, M, Ayres, LD & Santos, AA.

2007. Aplicações estatísticas nas áreas das

ciências bio-médicas. Instituto Mamirauá,

Belém.

Baker, DG. 2007. Flynn's Parasites of Laboratory

Animals: 2 ed., Second. Blackwell

Publishing Ltd, Oxford, UK.

Baker, MR. 1987. Rhabdias collaris n. sp.

(Nematoda: Rhabdiasidae) from frogs of

Tanzania. Systematic Parasitology, vol. 9,

pp.199–201.

Bittencourt, EB & Rocha, CFD. 2003. Host-

ectoparasite Specificity in a Small Mammal

Community in an Area of Atlantic Rain

Forest (Ilha Grande, State of Rio de

Janeiro), Southeastern Brazil. Memórias do

Instituto Oswaldo Cruz, vol. 98, pp.

793–798.

Brito, SV, Corso, G, Almeida, AM, Ferreira, FS,

Almeida, WO, Anjos, LA, Mesquita, DO &

BIBLIOGRAPHIC REFERENCES Vasconcelos, A. 2014. Phylogeny and

micro-habitats utilized by lizards determine

the composition of their endoparasites in

the semiarid Caatinga of Northeast Brazil.

Parasitology Research, vol. 113, pp

3963–3972.

Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.

1997. Parasitology Meets Ecology on Its

Own Terms: Margolis et al. Revisited.

Journal of Parasitology, vol. 83, pp. 575.

Campião, KM, Da Silva, RJ & Ferreira, VL. 2009.

Helminth parasites of Leptodactylus

podicipinus (Anura: Leptodactylidae) from

south-eastern Pantanal, State of Mato

Grosso do Sul, Brazil. Journal of

Helminthology, vol. 83, pp. 345–349.

Campião KM, Morais DH, Dias OT, Aguiar, A,

Toledo, GM, Tavares, LER & Silva, RJ.

2014. Checklist of Helminth parasites of

Amphibians from South America. Zootaxa,

vol. 3843, pp. 1–93.

Campião KM, Silva, ICO, Dalazen, GT, Paiva, F &

Tavares, LER. 2016a. Helminth parasites of

11 anuran species from the Pantanal

Wetland, Brazil. Comparative Parasitology,

vol. 83, pp. 92–100.

Campião, KM, Dias, OT, Silva, RJ, Ferreira, VL &

Tavares, LER. 2016b. Living apart and

having similar trouble: Are frog helminth

parasites determined by the host or by the

habitat? Canadian Journal of Zoology, vol.

94, pp. 761–765.

CFMV. Conselho Federal de Medicina Veterinária.

2013. Métodos de eutanasia. In: Guia

brasileiro de boas práticas para eutanásia

em animais. Comissao de Ética, Bioética e

Bem-da.

Graça, RJ, Oda, FH, Lima, FS, Guerra, V,

Gambale, PG & Takemoto, RM. 2017.

Metazoan endoparasites of 18 anuran

species from the mesophytic semideciduous

Atlantic Forest in southern Brazil. Journal

of Natural History, vol. 51, pp. 705–729.

Gallas, M & Silvera, EF. 2012. Pathologies of

O l i g a c a n t h o r h y n c h u s p a r d a l i s

(Acanthocephala, Oligacanthorhynchidae)

in Leopardus tigrinus (Carnivora, Felidae)

in Southern Brazil. Revista Brasileira de

Parasitologia Veterinária, vol. 21, pp.

308–312.

Garda, AA, Stein, MG, Machado, RB, Lion, MB,

Juncá, FA & Napoli, MF. 2017. Ecology,

Neotropical Helminthology, 2020, 14(2), jul-dic Silva Neta et al.

Biogeography, and Conservation of

Amphibians of the Caatinga. In: JMC,

Silva, I, Leal, M, Tabarelli (eds) Caatinga.

Springer International Publishing, Cham,

pp 133–149.

Goldberg, SR & Bursey, CR. 2004. Coelomic

metazoan endoparasites of 15 colubrid and

two elapid snake species from Costa Rica.

Caribbean Journal of Science, vol. 40, pp.

62–69.

Goldberg, SR & Bursey, CR. 2008. Helminths from

fifteen species of frogs (Anura, Hylidae)

from Costa Rica. Phyllomedusa, vol. 7, pp.

25–33.

Goldberg, SR, Bursey, CR, Caldwell, JP, Vitt, LJ &

Costa, GC. 2007. Gastrointestinal

helminths from six species of frogs and three

species of lizards, sympatric in Pará State,

Brazil. Comparative Parasitology, vol. 74,

pp. 327–342.

Hamann, MI, Kehr, AI, González, CE, Duré, MI &

Schaefer, EF. 2009. Parasite and

reproductive features of Scinax nasicus

(Anura: hylidae) from a South American

subtropical area. Interciencia, vol. 34, pp.

214–218.

Hamann, MI, Kehr, AI & González, CE. 2012.

Community structure of helminth parasites

of Leptodactylus bufonius (Anura:

Leptodactylidae) from northeastern

Argentina. Zoological Studies, vol. 51, pp.

1454–1463.

Hamann, M.I., Kehr, A.I. & González, C.E. 2013.

Helminth communities in the burrowing

toad, Rhinella fernandezae, from

northeastern Argentina. Biologia, vol. 68,

pp.1155–1162.

Hudson, P. 2005. Parasites, diversity, and the

ecosystem. In: F, Thomas, TF, Reanud, JF,

Guegan (eds) Parasitism and Ecosystems.

Oxford University Press, New York, pp

1–12.

Ibrahim, MM. 2008. Helminth infracommunities of

the maculated toad Amietophrynus

regularis (Anura: Bufonidae) from Ismailia,

Egypt. Diseases of aquatic organisms, vol.

82, pp. 19–26.

Koprivnikar, J, Marcogliese, DJ, Rohr, JR,

Orlofske, SA, Raffel, TR & Johnson, PTJ.

2012. Macroparasite infections of

amphibians: What can they tell us?

Ecohealth, vol. 9, pp. 342–360.

215

Krasnov, BR, Fortuna, MA, Mouillot, D,

Khokhlova, IS, Shenbrot, GI & Poulin, R.

2012. Phylogenetic signal in module

composition and species connectivity in

compartmentalized host-parasite networks.

The American Naturalist, vol. 179, pp.

501–511.

Kuzmin, Y & Tkach, VV. 2018. Rhabdias. In:

World Wide We b Electron. P u bl.

http://izan.kiev.ua/ppages/rhabdias/list.htm

. Accessed 3 Mar 2019.

Kuzmin, Y, Melo, FTV, Silva-Filho, HF & Santos,

JN. 2016. Two new species of Rhabdias

Stiles et Hassall, 1905 (Nematoda:

Rhabdiasidae) from anuran amphibians in

Para, Brazil. Folia Parasitologica, vol. 63,

pp. 3-10.

Lima, DP, Giacomini, HC, Takemoto, RM,

Agostinho, AA & Bini, LM. 2012. Patterns

of interactions of a large fish-parasite

network in a tropical floodplain. Journal of

Animal Ecology, vol. 81, pp. 905–913.

Magurran, AE. 2004. Measuring Biological

Diversity. Blackwell Publishing Company,

Oxford.

Müller, MI, Morais, DH, Costa-Silva, GJ, Aguiar,

A, Ávia, RW & Silva, RJ. 2018. Diversity in

t he g e nu s Rhabd ias ( N em a to d a,

Rhabdiasidae): Evidence for cryptic

speciation. Zoologica Scripta, vol. 47, pp.

595–607.

Muzzall, PM, Gillilland, MG, Summer, CS &

Mehne, CJ. 2001. Helminth communities of

green frogs Rana clamitans Latreille, from

Southwestern Michigan. Journal of

Parasitology, vol. 87, pp. 962.

Oliveira, CR, Ávila, RW & Morais, DH. 2019.

He lmi nth s ass oci at e d wi t h th re e

P h y s a l a e m u s s p e c i e s ( A n u r a :

Leptodactylidae) from Caatinga Biome,

Brazil. Acta Parasitologica, vol. 64, pp.

205–212.

Pinhão, R, Wunderlich, A, Anjos, LA & da Silva,

RJ. 2009. Helminths of toad Rhinella

icterica (bufonidae), from the municipality

of Botucatu, São Paulo State, Brazil.

Neotropical Helminthology, vol. 3, pp.

35–40.

Poulin, R. 2004. Macroecological patterns of

species richness in parasite assemblages.

Basic and Applied Ecology, vol. 5, pp.

423–434.

Neotropical Helminthology, 2020, 14(2), jul-dic Helminths associated with anurans from Brazil

216

Poulin, R & Morand, S. 2004. Parasite

Biodiversity. Smithsonian Institution

Books, Washington.

R C team. 2017. R: A Language and Environment

for Statistical Computing. R Found Stat

Comput.

Richardson, DJ, Gardner, SL & Allen, JW. 2014.

Redescription of Oligacanthorhynchus

microcephalus (Oligacanthorhynchidae).

Comparative Parasitology, vol. 81, pp.

53–60.

Santos, FLA & Souza, MJN. 2012. Caracterização

geoambiental do Planalto cuestiforme da

Ibiapaba – Ceará. Revista Geonorte, vol. 3,

pp. 301–309.

Santos, VGT & Amato, SB. 2010. Helminth fauna

of Rhinella fernandezae (Anura: Bufonidae)

from the Rio Grande do Sul Coastland,

Brazil: Analysis of the parasite community.

Journal of Parasitologu, vol. 96, pp.

823–826.

Segalla, MV, Caramaschi, U, Cruz, CAG, Garcia,

PCA, Grant, T, Haddad, CFB, Santana, DJ,

Toledo, LF & Langone, JA. 2019. Brazilian

amphibians: List of species. Herpetologia

Brasileira, vol. 8, pp. 65–97.

Stumpf, IVK. 1981. Ciclo evolutivo da

Cylindrotaenia americana Jewell, 1916

(Cyclophyllidea: Nematotaeniidae) em

Bufo ictericus Spix, 1824. Acta Biologica

Paraense, vol. 10, pp. 31-39.

Teles, D, Sousa, JGG, Teixeira, AAM, Silva, MC,

Oliveira, RH, Silva, MRM & Ávila, RW.

2015. Helminths of the frog Pleurodema

diplolister (Anura, Leiuperidae) from the

Caatinga in Pernambuco State, Northeast

Brazil. Brazilian Journal of Biology, vol. 75,

pp. 251–253.

Teles, DA, Brito, SV, Araujo-Filho, JA, Ribeiro,

SC, Teixeira, AAM, Mesquita, DO &

Almeida, WO. 2018. Nematodes of the

Rhinella granulosa Spix, 1824 (Anura:

Bufonidae) from the Semiarid Northeastern

Caatinga Region of Brazil. Comparative

Parasitology, vol. 85, pp. 208–211.

Toledo, G.M., Morais, D.H., Silva, R.J. & Anjos,

L.A. 2015. Helminth communities of

L e p t o d a c t y l u s l a t r a n s ( A n u r a :

Leptodactylidae) from the Atlantic

rainforest, south-eastern Brazil. Journal of

Helminthology 89, 250–254.

Toledo, GM, Schwartz, HO, Nomura, HAQ,

Aguiar, A, Velota, RAMV, Silva, RJ &

Anjos, LA. 2017. Helminth community

structure of 13 species of anurans from

Atlantic rainforest remnants, Brazil.

Journal of Helminthology, vol. 92, pp.

438–444.

Travassos, L, Freitas, JFT & Kohn, A. 1969.

Trematódeos do Brasil. Memórias do

Instituto Oswaldo Cruz, vol. 67, pp. 1–886.

Vicente, JJ, Rodrigues, HO, Gomes, DC & Pinto,

RM. 1991. Nematoides do Brasil 2a parte:

Nematoides de anfíbios. Revista Brasileira

de Zoologia, vol. 7, pp. 549– 626.

Willkens Y, Rebêlo GL, Santos JN, Furtado, AP,

Vilela, RV, Tkach, VV, Kuzmin, Y & Melo,

FTV. 2020. Rhabdias glaurungi sp. nov.

(Nematoda: Rhabdiasidae), parasite of

Scinax gr. ruber (Laurenti, 1768) (Anura:

Hylidae), from the Brazilian Amazon.

Journal of Helminthology, vol. 94, e54.

Windsor, DA. 1998. Con trove rsie s in

Parasitology, most of the species on earth

are parasites. International Journal for

Parasitology, vol. 28, pp. 1939–1941.

Wood, CL & Johnson, PTJ. 2015. A world without

parasites: Exploring the hidden ecology of

infection. Frontiers in Ecology and the

Environment, vol. 13, pp. 425–434.

Yamaguti, S. 1963. Systema Helminthum:

Acanthocephala. Interscience Publishers,

New York,

Yoder, H.R. & Coggins, J.R. 2007. Helminth

communities in five species of sympatric

amphibians from three adjacent ephemeral

ponds in southeastern Wisconsin. Journal of

Parasitology, vol. 93, pp. 755–761.

Zar, JH. 2010. Biostatistical Analysis, 5th ed.

Prentice-Hall, Upper Saddle River.

Received July 22, 2020.

Accepted September 11, 2020.

Neotropical Helminthology, 2020, 14(2), jul-dic Silva Neta et al.