Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-20T17:59:51.413Z Has data issue: false hasContentIssue false
  • English
  • Français

Endoparasite community of anurans from an altitudinal rainforest enclave in a Brazilian semiarid area

Published online by Cambridge University Press:  19 August 2022

C.R. de Oliveira Open the ORCID record for C.R. de Oliveira [Opens in a new window] ,
W. Mascarenhas Open the ORCID record for W. Mascarenhas [Opens in a new window] ,
D. Batista-Oliveira Open the ORCID record for D. Batista-Oliveira [Opens in a new window] ,
K. de Castro Araújo Open the ORCID record for K. de Castro Araújo [Opens in a new window] ,
R.W. Ávila Open the ORCID record for R.W. Ávila [Opens in a new window]  and
D.M. Borges-Nojosa Open the ORCID record for D.M. Borges-Nojosa [Opens in a new window]
C.R. de Oliveira*
Affiliation:
Graduate Course of Ecology and Natural Resources, Department of Biology, Campus of Pici, Federal University of Ceará, Fortaleza - CE, Zip Code 60440-900, Brazil Regional Ophiology Center, Federal University of Ceará - UFC, Block 905, Science Center, PICI Campus, Fortaleza - CE, Zip Code: 60455-760, Brazil
W. Mascarenhas
Affiliation:
Institute for Educators Training, Laboratory of Biology and Ecology of Wild Animals, Federal University of Cariri, Brejo Santo, Ceará, Zip Code: 63260-000, Brazil
D. Batista-Oliveira
Affiliation:
Graduate Program in Biological Diversity and Natural Resources, Department of Biological Chemistry, Regional University of Cariri, Crato, Ceará, Zip Code: 63100-000, Brazil
K. de Castro Araújo
Affiliation:
Graduate Course of Ecology and Natural Resources, Department of Biology, Campus of Pici, Federal University of Ceará, Fortaleza - CE, Zip Code 60440-900, Brazil
R.W. Ávila
Affiliation:
Graduate Course of Ecology and Natural Resources, Department of Biology, Campus of Pici, Federal University of Ceará, Fortaleza - CE, Zip Code 60440-900, Brazil Regional Ophiology Center, Federal University of Ceará - UFC, Block 905, Science Center, PICI Campus, Fortaleza - CE, Zip Code: 60455-760, Brazil
D.M. Borges-Nojosa
Affiliation:
Graduate Course of Ecology and Natural Resources, Department of Biology, Campus of Pici, Federal University of Ceará, Fortaleza - CE, Zip Code 60440-900, Brazil Regional Ophiology Center, Federal University of Ceará - UFC, Block 905, Science Center, PICI Campus, Fortaleza - CE, Zip Code: 60455-760, Brazil
*
Author for correspondence: Cicero Ricardo de Oliveira, E-mail: riccicer@gmail.com
Rights & Permissions [Opens in a new window]

Abstract

In the present study, we aimed to describe the composition of endoparasites associated with anurans from an altitudinal rainforest enclave in northeastern Brazil. Additionally, we tested if microhabitat use influences endoparasite abundance and richness, as well as the hypothesis that larger frogs tend to be more parasitized. We sampled 306 individuals from 25 anuran species that were necropsied and analysed using a stereomicroscope. The total endoparasite prevalence was 79.08%, with a parasitic community consisting of 46 taxa. Overall, we found the common pattern described for Neotropical amphibians, which is the predominance of generalist and direct-cycle parasites. Twenty new host records and two possible new parasite species were found, highlighting the importance of this type of inventory. We also observed that microhabitat use was associated with a significant difference in parasite richness between groups, in which arboreal and terrestrial species, and aquatic and arboreal species contributed to these differences. Moreover, larger frogs tended to be more parasitized regarding only an interspecific view. Our results suggest that parasite richness is directly related to infection cycle and how the host exploits its habitat.

Keywords

helminthsparasiteamphibiansMaranguape mountain
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e62
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Introduction

Parasites are diverse organisms that are an integral part of nature, representing most of the global biodiversity and one of the most common life strategies on the planet (Windsor, Reference Windsor1998; Poulin & Morand, Reference Poulin and Morand2004; Kuris, Reference Kuris2008). Parasitic organisms are also ecologically important (Marcogliese, Reference Marcogliese2004; Poulin & Morand, Reference Poulin and Morand2004) because they are closely related to environmental conditions, and thus, might be considered potential indicators of environmental quality (Catalano et al., Reference Catalano, Whittington, Donnellan and Gillanders2013). Despite the increase of parasitological studies, the science as a whole is still far from having complete knowledge about the parasite biodiversity and ecology on Earth (Poulin & Morand, Reference Poulin and Morand2004). Therefore, inventories are the basis for studies, and determining which and how many species is part of an ecosystem is essential for understanding the diversity and functioning of organisms (Segalla et al., Reference Segalla, Berneck, Canedo, Caramaschi, Cruz, Garcia and Langone2021). In addition, these organisms are involved in various processes of nature regulation and might influence host population conditions because they interfere in crucial processes such as competition, migration, dispersal and speciation (Vitt & Caldwell, Reference Vitt and Caldwell2009; Matias et al., Reference Matias, Ferreira-Silva, Sousa and Ávila2018). Thus, knowledge about parasite diversity and distribution is important to understand the role of parasite–host ecological relationships on ecosystem dynamics (Poulin & Krasnov, Reference Poulin, Krasnov, Morand and Krasnov2010; Campião et al., Reference Campião, Ribas, Morais, Dias, Silva and Tavares2015b).

The altitudinal enclaves of humid montane forests known as ‘brejos-de-altitude’ [highland swamps] are isolated areas in the morphoclimatic domain of the Caatingas, which are marked by a high degree of endemism of their herpetofauna (Borges-Nojosa & Caramaschi, Reference Borges-Nojosa, Caramaschi, Leal, Tabarelli and Silva2003; Albuquerque et al., Reference Albuquerque, De Lima Araújo, El-Deir, De Lima, Souto, Bezerra and Severi2012; Borges-Nojosa et al., Reference Borges-Nojosa, Lima, Bezerra and Harris2016). As they are considered exceptional environments, due to local climatic conditions, they form isolated systems considered as unique elements (Vanzolini, Reference Vanzolini1981; Borges-Nojosa & Caramaschi, Reference Borges-Nojosa, Caramaschi, Leal, Tabarelli and Silva2003). Such areas are classified as of extreme biological importance (MMA, 2000; Sousa et al., Reference Sousa, Langguth and Gimenez2004), and responsible for the greatest richness of anurans in Ceará state, northeastern Brazil (Roberto & Loebmann, Reference Roberto and Loebmann2016). Despite the recent increase of parasitological studies dealing with anurans from these mountains (Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020; Mascarenhas et al., Reference Mascarenhas, Oliveira, Benício, Ávila and Ribeiro2021; Machado et al., Reference Machado, de Oliveira, Benício, Araújo and Ávila2022), their parasite diversity is still underestimated.

According to Aho (Reference Aho, Esch, Bush and Aho1990), anurans show low parasite richness that is variable and isolationist when compared to other vertebrate groups. However, some amphibian species may present a higher richness of helminths (Hamann et al., Reference Hamann, Kehr and González2006), being currently accepted that amphibians harbour rich and diverse helminth fauna (Campião et al., Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014; Oliveira et al., Reference Oliveira, Ávila and Morais2019; Mascarenhas et al., Reference Mascarenhas, Oliveira, Benício, Ávila and Ribeiro2021; Machado et al., Reference Machado, de Oliveira, Benício, Araújo and Ávila2022). Recently published studies (e.g. Campião et al., Reference Campião, Ribas, Morais, Dias, Silva and Tavares2015b; Lins et al., Reference Lins, Aguiar, Morais, Silva, Ávila and Silva2017; Oliveira et al., Reference Oliveira, Ávila and Morais2019; Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020; Mascarenhas et al., Reference Mascarenhas, Oliveira, Benício, Ávila and Ribeiro2021) report processes that influence the structure of helminth communities in amphibians, including host size, genus, diet, site of infection, species and behaviour. In addition, features of host habitats are key factors in parasite colonization (Goater et al., Reference Goater, Baldwin and Scrimgeour2005), drawing attention to the composition of parasite communities, which vary widely among host populations of the same species (Poulin et al., Reference Poulin, Blanar, Thieltges and Marcogliese2011; Bezerra et al., Reference Bezerra, Pinheiro, Melo, Zanchi-Silva, Queiroz, Anjos, Harris and Borges-Nojosa2016).

In the present study: (i) we aimed to describe the composition of endoparasites associated with anurans from an altitudinal rainforest enclave in northeastern Brazil; (ii) to test if microhabitat use influences endoparasite abundance and richness; and (iii) to test the hypothesis that larger frogs tend to be more parasitized.

Material and methods

Study area

Sampling took place in the Maranguape mountain, Ceará state, northeastern Brazil (fig. 1), a crystalline residual massif with a maximum altitude of 920 m, vegetation composed of humid forest covering the highest points, dry forest in the intermediate points gradually replacing the humid forest, and Caatinga in the lowlands (Borges-Nojosa & Caramaschi, Reference Borges-Nojosa, Caramaschi, Leal, Tabarelli and Silva2003). The climatic regime is defined by two distinct seasons: dry season from June to December, and rainy season from January to May, with average annual precipitation of 1300 mm, and temperatures ranging from 26°C to 28°C (Ceará, 2002; IPECE, 2017).

Fig. 1. Schematic map of the sampling points in Maranguape mountain, Ceará state, northeastern Brazil. Red triangles represent sampling points.

Sampling

Anuran sampling occurred during the rainy season, from April to May 2019 (15 days of sampling) and from February to May 2020 (17 days of sampling), through visual and auditory searches (Bernarde, Reference Bernarde2012). The sampling period started at dusk and extended until midnight (17:00–00:00 h), which is the time period when the majority of anuran species are most active in foraging and reproduction. For each individual, we determined the microhabitat use considering the site of capture (arboreal, aquatic or terrestrial).

The collected specimens were euthanized with a lethal injection of sodium thiopental (Thiopentax®), following the ethical procedures of the Federal Council of Veterinary Medicine ‒ CFMV (2013). Afterwards, we measured the mass with a Pesola scale (precision 0.1 g) and the snout–vent length (SVL) using a Mitutoyo® digital caliper (precision 0.01 mm). Voucher specimens were fixed in 10% formalin according to Calleffo (Reference Calleffo, Auricchio and Salomão2002) and deposited in the Herpetological Collection of the Federal University of Ceará (CHUFC – A 9762 to A 9953), Fortaleza, Brazil.

Parasitological procedures

We necropsied the anurans after performing a ventral incision and examined for the presence of endoparasites in the organs (gastrointestinal tract, lungs, liver and kidneys) and internal cavity using a stereomicroscope according to Amato et al. (Reference Amato, Boeger and Amato1991). For species identification, we collected and prepared the endoparasites following specialized methodologies according to each taxonomic group (Yamaguti, Reference Yamaguti1971; Schmidt, Reference Schmidt1986; Vicente et al., Reference Vicente, Rodrigues, Gomes and Pinto1991; Andrade, Reference Andrade2000). Temporary slides were analysed using a light microscope. Voucher specimens were deposited in the Parasitological Collection of the Universidade Federal do Ceará (CPUFC – 196 to 441), Fortaleza, Brazil.

We measured the following parasitological parameters according to Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997): prevalence (percentage of parasitized amphibians in each host species); mean intensity of infection (mean number of parasites in parasitized amphibians); and mean parasite abundance.

Statistical analyses

We used the non-parametric Kruskal–Wallis test (Shapiro–Wilk < 0.05) to investigate whether parasite richness and abundance vary in response to microhabitat used by anuran species (aquatic, arboreal and terrestrial), followed by Dunn's post-hoc test to investigate which groups contributed most to the differences (P-values adjusted with the Benjamini–Hochberg method). Regarding both interspecific and intraspecific views, we tested the influence of anuran body size (SVL and mass) on the abundance and richness of parasites with a linear mixed model, using host sex as a random effect. For this test, we used only anuran species with more than five individuals parasitized. Analyses and graphs were performed using the packages ggplot2 (Wickham, Reference Wickham2016), nlme (Pinheiro & Bates, Reference Pinheiro and Bates2000), vegan (Oksanen et al., Reference Oksanen, Blanchet and Kindt2016) and FSA (Ogle et al., Reference Ogle, Doll, Wheeler and Dinno2022) from R software (R core team, 2021).

Results

We sampled 306 individuals from 25 anuran species (fig. 2), of which 242 individuals (75 females, 161 males and six juveniles) were parasitized with at least one parasite taxon. We found 7042 helminth specimens, with an overall prevalence of 79.08%, mean infection intensity of 29.09 and total abundance of 23.01 ± 1.58. The endoparasite community consisted of 46 taxa. The most abundant taxa were Raillietnema spectans, Oswaldocruzia mazzai and Schrankiana schranki. The highest prevalence values were observed for Oswaldocruzia mazzai, Physaloptera sp. and Centrorhynchus sp. Endoparasite richness ranged from two to 17 parasites taxa per host, Oswaldocruzia mazzai and Physaloptera sp. being the most prevalent parasites (table 1).

Fig. 2. Anurans found in Maranguape mountain, Ceará state, northeastern Brazil: (A) Rhinella diptycha; (B) Rhinella granulosa; (C) Adelophryne maranguapensis; (D) Boana raniceps; (E) Corythomantis greeningi; (F) Dendropsophus minusculus; (G) Dendropsophus minutus; (H) Dendropsophus nanus; (I) Dendropsophus tapacurensis; (J) Scinax x-signatus; (K) Trachycephalus typhonius; (L) Adenomera juikitam; (M) Leptodactylus fuscus; (N) Leptodactylus macrosternum; (O). Leptodactylus mystaceus; (P) Leptodactylus pustulatus; (Q) Leptodactylus syphax; (R) Leptodactylus troglodytes; (S) Leptodactylus vastus; (T) Physalaemus cuvieri; (U) Elachistocleis piauiensis; (V) Proceratophrys cristiceps; (W) Proceratophrys renalis; (X) Pithecopus gonzagai; and (Y) Pristimantis relictus.

Table 1. The endoparasite community found in the anuran species from Maranguape mountain, Ceará state, northeastern Brazil.

n, number of parasites; N.H, number of infected hosts; P%, prevalence; M.I., mean intensity; R, range; Ab., abundance; S.E., standard error; S.I., site of infection; C, cavity; S, stomach; SI, small intestine; LI, large intestine; LV, liver; LG, lung; G, gallbladder; PA, pancreas; K, kidney; UB, urinary bladder; and UD, urinary duct.

The most parasitized anurans were Trachycephalus typhonius (n = 17), Pristimantis relictus (n = 17) and Physalaemus cuvieri (n = 15). Adelophryne maranguapensis was not parasitized, while Leptodactylus troglodytes (n = 2), Rhinella granulosa (n = 3) and Adenomera juikitam (n = 3) had few associated parasite taxa. In addition, we found 20 new host records and two possible new parasite species (table 2).

Table 2. List of endoparasites found in the anuran species from Maranguape mountain, Ceará state, northeastern Brazil and literature review for previous records.

n, number of hosts; P%, prevalence; and A.M., abundance.

a possible new species.

We observed that microhabitat use was associated with a significant difference in parasite richness between groups (H = 13.35, P = 0.0012), in which Dunn's post-hoc test evidenced that arboreal and terrestrial species (P = 0.001) and aquatic and arboreal species (P = 0.023) contributed significantly to these differences (fig. 3). By contrast, parasite abundance did not vary significantly between groups (H = 5.2821, P > 0.05).

Fig. 3. Boxplot representing the parasite richness between the groups of microhabitats used by the anurans.

We also observed that larger frogs (SVL) tend to be more parasitized considering the parasite abundance (T = 2.148, P = 0.0328) and richness (T = 4.576, P = 0.0001), regardless of sex (intercept = 0.0041 and 0.1291, respectively) (fig. 4). Mass had no significant influence on both abovementioned parasitological descriptors (P > 0.05). In an intraspecific view, parasite load (richness and abundance) seemed not to be influenced by the size of each anuran species (table 3).

Fig. 4. Relationship of parasite richness (A) and abundance (B) with the host's body size (anuran interspecific view) from Maranguape mountain, Ceará state, northeastern Brazil.

Table 3. Relationship between parasite richness and abundance with anuran body size (snout–vent length (SVL) and mass), regarding an interspecific view, obtained through linear mixed models.

St. D. ± S.E., standard deviation and standard error.

Significant values and percentage of variation in response that is explained by the fixed effects (mass and SVL) are represented by P and T values. Random effects were obtained through the intercept values (RE).

Discussion

Communities of endoparasites associated with anurans generally show high richness and diversity (Campião et al., Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014); in the present study, we found 46 parasite taxa, corroborating this pattern. Following the same infection pattern found in other Neotropical anurans (Lins et al., Reference Lins, Aguiar, Morais, Silva, Ávila and Silva2017; Oliveira et al., Reference Oliveira, Ávila and Morais2019; Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020; Mascarenhas et al., Reference Mascarenhas, Oliveira, Benício, Ávila and Ribeiro2021), as well as in other vertebrate groups, such as reptiles (Brito et al., Reference Brito, Corso, Almeida, Ferreira, Almeida, Anjos and Vasconcellos2014; Carvalho et al., Reference Carvalho, Silva-Neta, Silva, Oliveira, Nunes, Souza and Ávila2018), mammals (Santos et al., Reference Santos, Silva, Fonseca and Oliveira2015; Biolchi et al., Reference Biolchi, Pontarolo, de Cássia Karvat and Pedrassani2021) and birds (Santos et al., Reference Santos, Silva, Fonseca and Oliveira2015), nematodes was the helminth group with the highest representation (65.2%) of the collected specimens. Nematodes are abundant in the number of species, generalists, and well distributed in the environment. Species with direct life cycle reach their hosts by oral ingestion or active penetration of infectious larvae through the skin, not requiring an intermediate host for their development (Anderson, Reference Anderson2000), which facilitates the dispersion and high incidence of infection of this parasite group. Although parasitological studies dealing with anuran communities in northeastern Brazil have recently increased, there are still important gaps in our knowledge about them. For example, of the 25 host species sampled herein, six have not been surveyed for parasites yet. In addition, we present 20 new host records (see table 2), reinforcing the importance of parasite checklists.

Due to the increase in parasitological studies (Mascarenhas et al., Reference Mascarenhas, Oliveira, Benício, Ávila and Ribeiro2021), it is quite common to find records of parasites not previously reported for host species (Aguiar et al., Reference Aguiar, Morais, Pyles and Silva2014; Silva et al., Reference Silva, Alcantara, Silva, Ávila and Morais2019). In the last decade, several studies on parasitism in Neotropical amphibians have been conducted (Madelaire et al., Reference Madelaire, Gomes and Da Silva2012; Aguiar et al., Reference Aguiar, Toledo, Anjos and Silva2015; Chero et al., Reference Chero, Cruces, Iannacone, Sáez, Alvariño, Luque and Morales2016; Amorim et al., Reference Amorim, Oliveira, Dyna, Sousa, Santos, Lima, Pinto and Ávila2019; Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020; Sani et al., Reference Sani, Rangel, dos Santos and Frezza2021; Machado et al., Reference Machado, de Oliveira, Benício, Araújo and Ávila2022), with the nematode parasites Falcaustra mascula, Ochoterenella sp., Oswaldocruzia mazzai, Oxyascaris oxyascaris, Physaloptera sp., Raillietnema spectans and Rhabdias sp. being the most commonly reported species. In our study, we found the same scenario, despite the low prevalence for some of the aforementioned species. This result is possibly due to the wide distribution of these parasites and their generalist habitats regarding host selection (Campião et al., Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014, Reference Campião, Ribas, Morais, Dias, Silva and Tavares2015b; Oliveira et al., Reference Oliveira, Ávila and Morais2019). In addition, the lack of taxonomic studies can be a limiting factor for an accurate identification of some parasite species distributed in the studied region. However, the description of new species has been increasing as parasitological studies progress (Felix-Nascimento et al., Reference Felix-Nascimento, Vieira, Muniz-Pereira and De Moura2020).

Oswaldocruzia mazzai showed the highest prevalence (27.12%) and was present in 60% of the parasitized host species in the anuran community in our study. This result may be related to the direct life cycle of this parasite and the simple mode of transmission (Anderson, Reference Anderson2000). The genus Physaloptera had the second highest prevalence (19.61%). Parasites of this group are commonly found in all anuran parasite studies and have also been observed in several classes of terrestrial vertebrates (Ogassawara et al., Reference Ogassawara, Benassi, Larsson, Leme and Hagiwara1986; Tung et al., Reference Tung, Hsiao, Yang, Chou, Lee, Wang and Lai2009; Cabral et al., Reference Cabral, Teles, Brito, Almeida, Dos Anjos, Guarnieri and Ribeiro2018). In amphibians, they are usually found in the larval stage, suggesting that these vertebrates are used as paratenic hosts. We also collected four individuals of Cosmocercoides sp. (one male and three females) in the large intestine of one specimen of Scinax x-signatus. The species was assigned to the genus Cosmocercoides due to the presence of a large number of rosette-like caudal papillae surrounded by punctuations. This is the first record of Cosmocercoides sp. for altitudinal rainforest enclave areas within the large Caatinga phytophysiognomy, nevertheless, further studies are necessary to define the species. Additionally, we also provide the first record of infection in Brazil of the species Parapharyngodon cf. duniae.

We also found nematode larvae parasitizing the small intestine and/or large intestine of several host species. Larvae of this type are commonly found in amphibian and reptile species (Ávila & Silva, Reference Ávila and Silva2010; Campião et al., Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014), and this larval stage may be associated with the monoxenous cycle of the parasite (Anderson, Reference Anderson2000), besides representing a recent infection and/or reproduction of the adult parasites in the host.

Platyhelminthes was the second most diverse phylum found in the present study, with 13 different taxa belonging to three classes (Cestoda, Monogenea and Trematoda). The most diverse class of Platyhelminthes was Trematoda with 11 taxa recorded. The aquatic habitat facilitates trematodes’ infection, which usually have snails as intermediate hosts (Madelaire et al., Reference Madelaire, Gomes and Da Silva2012). These parasites also use amphibians as intermediate hosts (Guillén-Hernández et al., Reference Guillén-Hernández, Salgado-Maldonado and Lamothe-Argumedo2000), found more often in aquatic and semiaquatic frogs such as leptodactylids (Campião et al., Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014; Oliveira et al., Reference Oliveira, Ávila and Morais2019). Catadiscus propinquus was the most abundant trematode and represents a new host record for Leptodactylus pustulatus. Indeed, some species are new host records; however, all trematodes had low prevalence considering the species pool (see table 2). Cestodes were represented by Cylindrotaenia americana, a cestode commonly found in Brazil, including in altitudinal rainforests’ enclaves (Oliveira et al., Reference Oliveira, Ávila and Morais2019; Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020). Herein, we provide the first record of this cestode in the treefrogs Dendropsophus minusculus and Dendropsophus nanus. Regarding monogenean parasites, we found 14 individuals of Polystoma cf. lopezromani parasitizing Corythomantis greeningi and Trachycephalus typhonius. Polystoma is the most diverse genus known in Polystomatidae (Sinnappah et al., Reference Sinnappah, Lim, Rohde, Tinsley, Combes and Verneau2001), having a direct life cycle, which can be completed in the gills of tadpoles or urinary duct of adult anurans (Bentz et al., Reference Bentz, Sinnappah-Kang, Lim, Lebedev, Combes and Verneau2006).

Acanthocephalans are extensively reported for reptiles (Matias et al., Reference Matias, Ferreira-Silva, Sousa and Ávila2018; Araújo et al., Reference Araújo, Silva, Machado, Oliveira and Ávila2020) and amphibians (Oliveira et al., Reference Oliveira, Ávila and Morais2019; Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020) as cystacanths. They are parasites with indirect life cycle, in which arthropods act as intermediate hosts, and fish, mammals or waterfowl as final hosts (Baker, Reference Baker2007). The presence of these cystacanths in amphibian hosts indicates that these species are used as paratenic hosts, possibly infected through the diet. In the present study, we found two genera represented by Centrorhynchus and Oligacanthorhynchus. Centrorhynchus sp. is the most common genus reported in Brazil for anuran hosts (Fabio, Reference Fabio1982; Smales, Reference Smales2007). Oligacanthorhynchus sp. are heteroxenous parasites and usually have mammals as final hosts (Richardson et al., Reference Richardson, Gardner and Allen2014). In South America, they are reported infecting Odontophrynus americanus (Silva et al., Reference Silva, Ávila and Morais2018) and Pleurodema diplolister (Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020). This study is the first record of Oligacanthorhynchus sp. for the anurans Leptodactylus vastus, Rhinella diptycha and Scinax x-signatus.

Regarding the phylum Annelida, we found four individuals of Dero (Allodero) lutzi in the urinary duct of Corythomantis greeningi, Scinax x-signatus and Trachycephalus typhonius. The genus Dero is known to use frogs for transport and as hosts (Oda et al., Reference Oda, Petsch, Ragonha, Batista, Takeda and Takemoto2015). This behaviour is stimulated by chemicals released by the amphibians, which are used by the parasite for dispersal (Lopez et al., Reference Lopez, Filizola, Deiss and Rios2005). Dero (Allodero) lutzi has been found parasitizing different amphibians, mainly arboreal species (Oda et al., Reference Oda, Petsch, Ragonha, Batista, Takeda and Takemoto2015), likely because these parasites are free-living inhabitants of bromeliad ponds and tree holes (Lopez et al., Reference Lopez, Rodrigues and Rios1999).

The characteristics and the way the host explores its habitat can influence the composition and structure of the helminth fauna, and explain the richness and diversity of the parasites associated with it (Poulin & Morand, Reference Poulin and Morand2004; Chandra & Gupta, Reference Chandra and Gupta2007; Euclydes et al., Reference Euclydes, Dudczak and Campião2021). Thus, anuran amphibians have a diverse parasite fauna due to their natural history (Prudhoe & Bray, Reference Prudhoe and Bray1982), which are generally associated with two types of environments, aquatic and terrestrial (Chandra & Gupta, Reference Chandra and Gupta2007). Species of arboreal amphibians tend to have low parasite richness, due to a possible reduction in the encounter with infective parasitic larvae. On the other hand, host anurans with terrestrial or semiaquatic habitats tend to have greater contact with the terrestrial environment when searching for water bodies, increasing the odds of contact with a greater number of parasites (Pizzatto et al., Reference Pizzatto, Kelehear and Shine2013; Euclydes et al., Reference Euclydes, Dudczak and Campião2021).

However, we observed that the arboreal habitat had great parasite richness. The higher number of individuals classified as arboreal (n = 163) in the present study may be an explanation for the significant relationship of arboreal habitat with parasite richness. Most species classified as arboreal were found during the reproductive period, in which anurans seek out puddles and mate for reproduction, passing through terrestrial and aquatic environments. This provides a greater likelihood of direct contact with infectious larvae, which allows a greater variety of parasites to become established in these animals (Chandra & Gupta, Reference Chandra and Gupta2007).

According to Todd (Reference Todd2007), endoparasitic helminths of amphibians require an aquatic environment for the development and transmission of their infective stages, as this promotes increased parasite transmission. However, we observed that the use of terrestrial and arboreal microhabitat contributed significantly to the abundance of parasites, showing that most helminth parasites of amphibians do not require an aquatic environment in the process of transmission and infection. Our data also indicated no relationship between host sex and parasite richness, but this result may have been influenced by the difference in the number of individuals of each sex analysed (Madeira & Sogayar, Reference Madeira and Sogayar1993). Moreover, most anuran hosts do not present differentiation in habitat use according to sex, being both subject to the same chances of infection by infective larvae available in the environment. It is also noteworthy that biotic factors such as the immune system and host age also affect parasitism, as they influence the life of both parasite and host (Pietrock & Marcogliese, Reference Pietrock and Marcogliese2004).

Overall, at an interspecific view, we observed that larger frogs tend to be more parasitized. Indeed, larger hosts can support a higher parasite load and even higher species richness because they offer greater microhabitat diversity favouring the development and reproduction of parasites (George-Nascimento et al., Reference George-Nascimento, Muñoz, Marquet and Poulin2004; Campião et al., Reference Campião, Ribas, Morais, Dias, Silva and Tavares2015b). However, this hypothesis was not supported in the present study at intraspecific views. This pattern was also found in other parasitological studies dealing with amphibians (e.g. Oliveira et al., Reference Oliveira, Ávila and Morais2019; Mascarenhas et al., Reference Mascarenhas, Oliveira, Benício, Ávila and Ribeiro2021; Machado et al., Reference Machado, de Oliveira, Benício, Araújo and Ávila2022). It seems that this hypothesis might be more evidenced concerning a species pool with anuran species of different sizes (e.g. Silva-Neta et al., Reference Silva-Neta, Alcantara, Oliveira, Carvalho, Morais, Silva and Ávila2020). Therefore, for congeneric species, we believe that other aspects such as microhabitat use, physiology, behaviour and seasonality, might have a greater influence on parasite load than the anuran size.

We conclude that the endoparasite composition of anurans from Maranguape mountain follow the common pattern described for Neotropical amphibians, showing high species richness and prevalence. We also recorded the first parasitological data for six anuran species and 20 new host records, which corroborates the hypothesis that amphibians are good models for parasite studies due to their way of life, behaviour and feeding. Furthermore, we stress the importance of parasite inventories for host species in understudied regions. We also emphasize that endoparasite composition has a significant relationship with the type of habitat used by the host due to the life cycle and mode of transmission of the parasites. As for the relationship between richness and host size, we indicate here that the size factor is predictive only if it has a large variation from the average host size.

Acknowledgements

We acknowledge Samuel Cardozo Ribeiro for helping in the analysis of the sampled material and the Laboratory of Edition, Translation and Revision of Academic texts (LETRARE), Universidade Federal do Ceará for revising the English version. We are also grateful to the Fundação Mata Atlântica Cearense for logistic support and the Herpetology Laboratories of Universidade Regional do Cariri and Universidade Estadual do Vale do Acaraú for fieldwork support.

Financial support

This study was partially financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Financial code 001) for the scholarship granted to CRO (C.R.O., # 88882.454307/2019-01). RWA and DMBN thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting research grants (R.W.A., PQ # 303622/2015-6; 305988/2018-2; and 307722/2021-0; D.M.B.N., PQ # 309617/2012-0; and 311961/2016-9). Lastly, we thank CNPq for their financial support (Project PVE # 401800/2013-0).

Conflicts of interest

None.

Ethical standards

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals. Collection permit Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (#72384-1 and #73215-1) and Ethic Committee on Animal Use of the Federal University of Ceará (CEUA-UFC) (#CEUA 6314010321).

References

Aguiar, A, Morais, DR, Pyles, PC and Silva, RJ (2014) Evaluation of helminths associated with 14 amphibian species from a neotropical island near the southeast coast of Brazil. Herpetological Review 45(2), 227–236.Google Scholar
Aguiar, A, Toledo, GM, Anjos, LA and Silva, RJ (2015) Comunidades de helmintos parasitas de duas populações de Physalaemus cuvieri Fitzinger, 1826 (Anura: Leiuperidae) sob diferentes condições de integridade de habitat na Mata Atlântica do Brasil [Communities of helminth parasites of two populations of Physalaemus cuvieri Fitzinger, 1826 (Anura: Leiuperidae) under different habitat integrity conditions in the Atlantic Forest of Brazil]. Revista Brasileira de Biologia 75(4), 963–968. [In Portuguese.]Google Scholar
Aguiar, A, Morais, DH, Silva, LAF, Dos Anjos, LA, Foster, OC and Da Silva, RJ (2021) Biodiversity of anuran endoparasites from a transitional area between the Atlantic Forest and Cerrado biomes in Brazil: New records and remarks. Zootaxa 4948(1), 1–41.CrossRefGoogle ScholarPubMed
Aho, JM (1990) Helminth communities of amphibians and reptiles: Comparative approaches to understanding patterns and processes. pp. 157–195. In Esch, GW, Bush, AO and Aho, JM (Eds) Parasite communities: Patterns and processes. New York, Chapman & Hall.CrossRefGoogle Scholar
Albuquerque, UP, De Lima Araújo, E, El-Deir, ACA, De Lima, ALA, Souto, A, Bezerra, BM and Severi, W (2012) Caatinga revisited: ecology and conservation of an important seasonal dry forest. The Scientific World Journal 2012, 205182.CrossRefGoogle ScholarPubMed
Amato, JFR, Boeger, WA and Amato, SB (1991) Protocolos para laboratório – Coleta e processamento de parasitos de pescado [Laboratory protocols – collection and processing of fish parasites]. Rio de Janeiro, Imprensa Universitária – FRRJ. [In Portuguese.]Google Scholar
Amorim, DM, Oliveira, RH, Dyna, CS, Sousa, DM, Santos, MEP, Lima, LS, Pinto, LC and Ávila, RW (2019) Nematodes parasites of Rhinella jimi (Stevaux, 2002) (Anura: Bufonidae) in areas of Caatinga, Northeastern Brazil. Neotropical Helminthology 13(2), 265–271.Google Scholar
Anderson, RC (2000) Nematode parasites of vertebrates, their development and transmission. 2nd edition. 650 pp. Wallingford, Oxford, CABI Publishing.CrossRefGoogle Scholar
Andrade, C (2000) Meios e soluções comumente empregados em laboratórios [Media and solutions commonly used in laboratories]. Seropédica, UFRRJ. [In Portuguese.]Google Scholar
Araújo, KC, Silva, CDS, Machado, HDS, Oliveira, CR and Ávila, RW (2020) Endoparasites of Philodryas olfersii (Lichtenstein, 1823) in Restinga environments of the Parnaíba River Delta, Northeastern Brazil. Neotropical Helminthology 14(2), 129–141.Google Scholar
Ávila, RW and Silva, RJ (2010) Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. Journal of Venomous Animals and Toxins Including Tropical Diseases 16(4), 543–572.CrossRefGoogle Scholar
Baker, DG (2007) Flynn's parasites of laboratory animals: Second edition. 2nd edition. Oxford, UK, Blackwell Publishing Ltd.CrossRefGoogle Scholar
Bentz, S, Sinnappah-Kang, ND, Lim, LHS, Lebedev, B, Combes, C and Verneau, O (2006) Historical biogeography of amphibian parasites, genus Polystoma (Monogenea: Polystomatidae). Journal of Biogeography 33(4), 742–749.CrossRefGoogle Scholar
Bernarde, PS (2012) Anfíbios e répteis: introdução ao estudo da herpetofauna brasileira [Amphibians and reptiles: introduction to the study of Brazilian herpetofauna]. 1st edition. Curitiba, Anolis Books. [In Portuguese.]Google Scholar
Bezerra, CH, Pinheiro, LT, Melo, GC, Zanchi-Silva, D, Queiroz, MS, Anjos, LA, Harris, DJ and Borges-Nojosa, DM (2016) Assessing the influence of geographic distance in parasite communities of an exotic lizard. Acta Parasitologica 61(1), 136–143.CrossRefGoogle ScholarPubMed
Biolchi, J, Pontarolo, GH, de Cássia Karvat, D and Pedrassani, D (2021) Análise coproparasitológica de gambás-de-orelha-branca pertencentes a áreas urbanas e rurais do município de Canoinhas, norte de Santa Catarina [Coproparasitological analysis of white-eared skunks belonging to urban and rural areas of the municipality of Canoinhas, north of Santa Catarina]. Archives of Veterinary Science 26(2), 79–89. [In Portuguese.]Google Scholar
Borges-Nojosa, DM and Caramaschi, U (2003) Composição e análise comparativa da diversidade e das afinidades biogeográficas dos lagartos e anfisbenídeos (Squamata) dos brejos nordestinus [Composition and comparative analysis of the diversity and biogeographic affinities of lizards and amphisbaenids (Squamata) from the northeastern swamps]. pp. 489–540. In Leal, IR, Tabarelli, M and Silva, JMC (Eds) Ecologia e conservação da Caatinga [Ecology and conservation of the Caatinga]. Recife, UFPE. [In Portuguese.]Google Scholar
Borges-Nojosa, DM, Lima, DC, Bezerra, CH and Harris, DJ (2016) Two new species of Apostolepis Cope, 1862 (Serpentes: Elapomorphini) from Brejos de altitude in northeastern Brazil. Revista Nordestina de Zoologia 10(1), 74–94.Google Scholar
Brito, SV, Corso, G, Almeida, AM, Ferreira, FS, Almeida, WO, Anjos, LA and Vasconcellos, A (2014) Phylogeny and micro-habitats utilized by lizards determine the composition of their endoparasites in the semiarid Caatinga of Northeast Brazil. Parasitology Research 113(11), 3963–3972.CrossRefGoogle ScholarPubMed
Bursey, CR and Brooks, DR (2004) Parapharyngodos Dunniae n. sp. (Nematoda: Pharyngodonidae) in Phrynohyas venulosa (Anura: Hylidae) from the Área de Conservación Guanacaste, Costa Rica. Journal of Parasitology 90(1), 137–139.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83(4), 575–583.CrossRefGoogle Scholar
Cabral, AN, Teles, DA, Brito, SV, Almeida, WO, Dos Anjos, LA, Guarnieri, MC and Ribeiro, SC (2018) Helminth parasites of Mabuya arajara Rebouças-Spieker, 1981 (Lacertilia: Mabuyidae) from Chapada do Araripe, northeastern Brazil. Parasitology Research 117(4), 1185–1193.CrossRefGoogle ScholarPubMed
Calleffo, MEV (2002) Anfíbios [Amphibians]. pp. 45–73. In Auricchio, P and Salomão, MG (Eds) Técnicas de coleta e preparação de vertebrados para fins científicos e didáticos [Techniques for collecting and preparing vertebrates for scientific and educational purposes]. São Paulo, Instituto Pau Brasil de História Natural. [In Portuguese.]Google Scholar
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, G, Tavares, LER and Silva, RJ (2014) Checklist of helminth parasites of amphibians from South America. Zootaxa 3843(1), 1–93.CrossRefGoogle ScholarPubMed
Campião, KM, Ribas, A and Tavares, LER (2015a) Diversity and patterns of interaction of an anuran–parasite network in a neotropical wetland. Parasitology 142(14), 1751–1757.CrossRefGoogle Scholar
Campião, KM, Ribas, ACA, Morais, DH, Dias, OT, Silva, RJ and Tavares, LER (2015b) How many parasites species a frog might have? Determinants of parasite diversity in South American anurans. PLoS One 10(10), e0140577.CrossRefGoogle Scholar
Campião, KM, Silva, ICO, Dalazen, GT, Paiva, F and Tavares, LER (2016a) Helminth parasites of 11 anuran species from the Pantanal Wetland, Brazil. Comparative Parasitolgy 83(1), 92–100.CrossRefGoogle Scholar
Campião, KM, Ribas, ACA, Silva, IC, Dalazen, GT and Tavares, LER (2016b) Anuran helminth communities from contrasting nature reserve and pasture sites in the Pantanal wetland, Brazil. Journal of Helminthology 91(1), 91–96.CrossRefGoogle Scholar
Cañizales, I (2021) Helmintos endoparásitos en anuros de Venezuela: revisión sistemática y análisis de diversidad [Endoparasite helminths in anurans from Venezuela: systematic review and diversity analysis]. Acta Biologica Venezuelica 40(1), 109–127. [In Spanish.]Google Scholar
Carvalho, ED, Silva-Neta, AFD, Silva, CDS, Oliveira, CR, Nunes, JDCX, Souza, TG and Ávila, RW (2018) Helminths infecting the cat-eyed snake Leptodeira Annulata Linnaeus 1758 (Squamata: Dipsadidae) in a Semiarid region of Brazil. Helminthologia 55(4), 281–285.CrossRefGoogle Scholar
Catalano, SR, Whittington, ID, Donnellan, SC and Gillanders, BM (2013) Parasites as biological tags to assess host population structure: Guidelines, recent genetic advances and comments on a holistic approach. International Journal for Parasitology: Parasites and Wildlife 3(2), 220–226.Google ScholarPubMed
Ceará (2002) Zoneamento ambiental e plano de manejo da área de proteção ambiental (APA) da serra de Maranguape (CE). Fortaleza, SEMACE. [In Portuquese.]Google Scholar
CFMV – Conselho Federal de Medicina Veterinária (2013) Métodos de eutanásia [Euthanasia methods]. pp. 28–29. In Comissão de ética, Bioética e bem-estar animal - CFMV, (Eds) Guia brasileiro de boas práticas de eutanásia em animais [Brazilian guide to good practices of euthanasia in animals.] Brasília, ASCOM/CFMV. [In Portuguese.]Google Scholar
Chandra, P and Gupta, N (2007) Habitat preference and seasonal fluctuations in the helminthofauna of amphibian hosts of Rohilkhand Zone, India. Asian Journal of Experimental Sciences 21(1), 69–78.Google Scholar
Chero, J, Cruces, C, Iannacone, J, Sáez, G, Alvariño, L, Luque, J and Morales, V (2016) Comunidad de helmintos parásitos del sapo espinoso Rhinella spinulosa (Wiegmann, 1834) (Anura: Bufonidae) de Perú [Community of parasitic helminths of the spiny frog Rhinella spinulosa (Wiegmann, 1834) (Anura: Bufonidae) from Peru]. Revista de Investigaciones Veterinarias del Perú 27(1), 114–129. [In Spanish.]CrossRefGoogle Scholar
Euclydes, L, Dudczak, AC and Campião, KM (2021) Anuran's habitat use drives the functional diversity of nematode parasite communities. Parasitology Research 120(3), 993–1001.CrossRefGoogle ScholarPubMed
Fabio, SP (1982) Helmintos de populações simpátricas de algumas espécies de anfíbios anuros da Família Leptodactylidae [Helminths from sympatric populations of some species of anuran amphibians of the Leptodactylidae Family]. Arquivos da Universidade Federal do Rio de Janeiro 5(1), 69–83. [In Portuiguese.]Google Scholar
Felix-Nascimento, G, Vieira, FM, Muniz-Pereira, LC and De Moura, GJB (2020) Two new species of Cosmocercidae (Nematoda: Cosmocercoidea) of Leptodactylus macrosternum Miranda-Ribeiro (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Zootaxa 4877(2), 274–290.CrossRefGoogle ScholarPubMed
George-Nascimento, M, Muñoz, G, Marquet, PA and Poulin, R (2004) Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecology Letters 7(7), 527–531.CrossRefGoogle Scholar
Goater, CP, Baldwin, RE and Scrimgeour, GJ (2005) Physicochemical determinant community structure in whitefish (Coregonus clupeaformes) from adjacent lakes in Northern Alberta, Canada. Parasitology 131(5), 713–722.CrossRefGoogle Scholar
González, CI and Hamann, MI (2011) Cosmocercid nematodes of three species of frogs (Anura: Hylidae) from Corrientes, Argentina. Comparative Parasitology 78(1), 212–216.CrossRefGoogle Scholar
González, CE and Hamann, MI (2015) Checklist of nematode parasites of amphibians from Argentina. Zootaxa 3980(4), 451–476.CrossRefGoogle ScholarPubMed
Graça, RJ, Oda, FH, Lima, FS, Guerra, V, Gambale, PG and Takemoto, RM (2017) Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil. Journal of Natural History 51(13–14), 705–729.CrossRefGoogle Scholar
Guillén-Hernández, S, Salgado-Maldonado, G and Lamothe-Argumedo, R (2000) Digeneans (Plathelminthes: Trematoda) of seven sympatric species of anurans from Los Tuxtlas, Veracruz, Mexico. Studies on Neotropical Fauna and Environment 35(1), 10–13.CrossRefGoogle Scholar
Hamann, MI and Kehr, AI (1998) Variación espacio temporal en infrapoblaciones de helmintos y su relación con las fluctuaciones poblacionales de Hyla nana (Anura, Hylidae) [Spatial temporal variation in helminths infrapopulations and their relationship with the population fluctuations of Hyla nana (Anura, Hylidae)]. Cuadernos de Herpetología 12(2), 23–33. [In Spanish.]Google Scholar
Hamann, MI, Kehr, AI and González, CE (2006) Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis (Anura: Leptodactylidae) in two contrasting environments from northeastern Argentina. Journal of Parasitology 92(6), 1171–1179.CrossRefGoogle ScholarPubMed
IPECE – Instituto de Pesquisa e Estratégia Econômica do Ceará (2017) Perfil municipal: Maranguape [Municipal profile: Maranguape]. Accessed at http://www.ipece.ce.gov.br. (accessed 21 July 2021). [In Portuguese.]Google Scholar
Kuris, AM (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454(7203), 515–518.CrossRefGoogle ScholarPubMed
Lins, AGS, Aguiar, A, Morais, DH, Silva, LAF, Ávila, RW and Silva, RJ (2017) Helminth fauna of Leptodactylus syphax (Anura: Leptodactylidae) from Caatinga biome, northeastern Brazil. Brazilian Journal of Veterinary Parasitology 26(1), 74–80.Google ScholarPubMed
Lopez, LCS, Rodrigues, PJFP and Rios, RI (1999) Frogs and snakes as phoretic dispersal agents of bromeliad ostracods (Elpidium) and Annelids (Dero). Biotropica 31(4), 705–708.CrossRefGoogle Scholar
Lopez, LCS, Filizola, B, Deiss, I and Rios, RI (2005) Phoretic behaviour of bromeliad annelids (Dero) and ostracods (Elpidium) using frogs and lizards as dispersal vectors. Hydrobiologia 549(1), 15–22.CrossRefGoogle Scholar
Machado, HTS, de Oliveira, SS, Benício, RA, Araújo, KC and Ávila, RW (2022) Helminths infecting sympatric congeneric treefrogs in northeastern Brazil. Acta Parasitologica 67(2), 658–667.CrossRefGoogle Scholar
Madeira, NG and Sogayar, MIL (1993) Prevalencia de Demodex folliculorum e Demodex brevis em uma amostra da população de Botucatu, São Paulo, Brasil [Prevalence of Demodex folliculorum and Demodex brevis in a population sample from Botucatu, São Paulo, Brazil]. Revista da Sociedade Brasileira de Medicina Tropical 26(4), 221–224. [In Portuguese.]CrossRefGoogle Scholar
Madelaire, CB, Gomes, FR and Da Silva, RJ (2012) Helmintos parasitas de Hypsiboas prasinus (Anura: Hylidae) de dois fragmentos de floresta atlântica, Estado de São Paulo, Brasil [Parasitic helminths of Hypsiboas prasinus (Anura: Hylidae) from two fragments of Atlantic forest, State of São Paulo, Brazil]. Journal of Parasitology 98(3), 560–564. [In Portuguese.]CrossRefGoogle Scholar
Marcogliese, DJ (2004) Parasites: small players with crucial roles in the ecological theatre. Ecohealth 1(2), 151–164.CrossRefGoogle Scholar
Martins-Sobrinho, PM, Silva, WGDO, Santos, EGD, Moura, GJBD and Oliveira, JBD (2017) Helminths of some tree frogs of the families Hylidae and Phyllomedusidae in an Atlantic rainforest fragment, Brazil. Journal of Natural History 51(27-28), 1639–1648.CrossRefGoogle Scholar
Mascarenhas, W, Oliveira, CR, Benício, RA, Ávila, RW and Ribeiro, SC (2021) Nematodes of Proceratophrys ararype (Anura: Odontophrynidae), an endemic frog from the Araripe Plateau, northeastern Brazil. Biota Neotropica 21, e20201164.CrossRefGoogle Scholar
Matias, CSL, Ferreira-Silva, C, Sousa, JGG and Ávila, RW (2018) Helminths infecting the black false boa Pseudoboa nigra (Squamata: Dipsadidae) in northeastern Brazil. Acta Herpetologica 13(2), 171–175.Google Scholar
Ministério do Meio Ambiente - MMA. (2000) Avaliação e para a conservação ações prioritárias da biodiversidade da Mata Atlântica e Campos Sulinos [Assessment and conservation priority actions for the biodiversity of the Atlantic Forest and Campos Sulinos]. Brasilia, Secretaria de Biodiversidade e Florestas (SBF), Ministério do Meio Ambiente (MMA). [In Portuguese.]Google Scholar
Morais, DH (2013) Aspectos ecológicos da helmintofauna de anfíbios Leptodactylidae (ANURA) no Estado do Mato Grosso, Brasil [Ecological aspects of the helminth fauna of amphibians Leptodactylidae (ANURA) in the State of Mato Grosso, Brazil]. Doctorate thesis, UNESP—Campus de Botucatu, Botucatu-SP. [In Portuguese.]Google Scholar
Morais, DH, Aguiar, A, Campião, KM, Tavares, LER, Almeida, WO, Ávila, RW and Silva, RJ (2017) New records of Dero (Allodero) lutzi, an oligochaete parasite of the urinary tract of South American Anurans. Herpetological Review 48(4), 739–743.Google Scholar
Oda, FH, Petsch, DK, Ragonha, FH, Batista, VG, Takeda, AM and Takemoto, RM (2015) Dero (Allodero) lutzi Michaelsen, 1926 (Oligochaeta: Naididae) associated with Scinax fuscovarius (Lutz, 1925) (Anura: Hylidae) from semi-deciduous Atlantic Rain Forest, southern Brazil. Brazilian Journal of Biology 75(1), 86–90.CrossRefGoogle ScholarPubMed
Ogassawara, S, Benassi, S, Larsson, CE, Leme, PTZ and Hagiwara, MK (1986) Prevalência de infecções helmínticas em gatos na cidade de São Paulo [Prevalence of helminth infections in cats in the city of São Paulo]. Revista da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo 23(2), 145–149. [In Portuguese.]CrossRefGoogle Scholar
Ogle, DH, Doll, JC, Wheeler, P and Dinno, A (2022) FSA: Fisheries stock analysis. R package version 0.9.3. Available at https://github.com/fishR-Core-Team/FSA (accessed 26/05/2022).Google Scholar
Oksanen, J, Blanchet, FG, Kindt, R, et al. (2016) Vegan: Community Eecology Ppackage. R package version 2.3–3. Available at https://CRAN.R-project.org/package=vegan (accessed 26/05/2022 ).Google Scholar
Oliveira, CR, Ávila, RW and Morais, DH (2019) Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitologica 64(1), 205–212.CrossRefGoogle ScholarPubMed
Pietrock, M and Marcogliese, DJ (2004) Response to Morley and Lewis: freeliving endohelminths: the influence of multiple factors. Trends in Parasitology 3(20), 115-116.CrossRefGoogle Scholar
Pinheiro, JC and Bates, DM (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag New York.CrossRefGoogle Scholar
Pizzatto, L, Kelehear, C and Shine, R (2013) Seasonal dynamics of the lungworm, Rhabdias pseudosphaerocephala, in recently colonised cane toad (Rhinella marina) populations in tropical Australia. International Journal for Parasitology 43(9), 753–761.CrossRefGoogle ScholarPubMed
Poulin, R and Krasnov, BR (2010) Similarity and variability of parasite assemblages across geographical space. pp. 115–128. In Morand, S and Krasnov, BR (Eds) The biogeography of hostparasite interactions. New York, Oxford University.Google Scholar
Poulin, R and Morand, S (2004) Parasite biodiversity. Washington, D.C., USA, Smithsonian Institution Books.Google Scholar
Poulin, R, Blanar, CA, Thieltges, DW and Marcogliese, DJ (2011) The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34(4), 540–551.CrossRefGoogle Scholar
Prudhoe, S and Bray, RA (1982) Platyhelminth parasites of the Amphibia. Oxford, British Museum (Natural History); Oxford University Press.Google Scholar
Queiroz, MS, Pontes, MR, Neto, MC, Campião, KM and Anjos, LA (2020) Helminths of 8 anuran species from a remnant riparian forest in the Cerrado biome, Brazil. Herpetology Notes 13, 463–478.Google Scholar
R Development Core Team. (2021). R: A language and environment for statistical computing: R Foundation for Statistical Computing version 4.1.1. (software). Austria.Google Scholar
Richardson, DJ, Gardner, SL and Allen, JW (2014) Redescription of Oligacanthorhynchus microcephalus (Oligacanthorhynchidae). Comparative Parasitology 81(1), 53–60.CrossRefGoogle Scholar
Roberto, IJ and Loebmann, D (2016) Composition, distribution patterns, and conservation priority areas for the Herpetofauna of the State of Ceará, Northeastern Brazil. Salamandra 52(2), 134–152.Google Scholar
Sani, AA, Rangel, GT, dos Santos, LC and Frezza, TF (2021) Helmintos parasitos de répteis e anfíbios no estado de São Paulo, Brasil [Parasitic helminths of reptiles and amphibians in the state of São Paulo, Brazil]. Interfaces Científicas-Saúde e Ambiente 8(3), 32–59. [In Portuguese.]Google Scholar
Santos, VGT and Amato, SB (2013) Species of Cosmocerca (Nematoda, Cosmocercidae) in Anurans from southern Santa Catarina State, Brazil. Comparative Parasitology 80(1), 123–129.CrossRefGoogle Scholar
Santos, PMDS, Silva, SGND, Fonseca, CFD and Oliveira, JBD (2015) Parasitos de aves e mamíferos silvestres em cativeiro no estado de Pernambuco [Parasites of wild birds and mammals in captivity in the state of Pernambuco]. Pesquisa Veterinária Brasileira 35(9), 788–794. [In Portuguese.]CrossRefGoogle Scholar
Schmidt, GD (1986) CRC handbook of tapeworm identification. Boca Raton, Florida, CRC Press.Google Scholar
Segalla, MV, Berneck, B, Canedo, C, Caramaschi, U, Cruz, CAG, Garcia, PCA and Langone, JA (2021) Brazilian amphibians: list of species. Herpetologia Brasileira 10(1), 121–216.Google Scholar
Silva-Neta, AF, Alcantara, EP, Oliveira, CR, Carvalho, EFF, Morais, DH, Silva, RJ and Ávila, RW (2020) Helminths associated with 15 species of anurans from the Ibiapaba Plateau, Northeastern Brazil. Neotropical Helminthology 14(2), 197–206.Google Scholar
Silva, CDS, Ávila, RW and Morais, DH (2018) Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4), 292–305.CrossRefGoogle Scholar
Silva, CS, Alcantara, EP, Silva, RJ, Ávila, RW and Morais, DH (2019) Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotropical Helminthology 13(2), 169–179.Google Scholar
Sinnappah, ND, Lim, LHS, Rohde, K, Tinsley, R, Combes, C and Verneau, O (2001) A endomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution 18(2), 189–201.CrossRefGoogle Scholar
Smales, LR (2007) Acanthocephala in amphibians (Anura) and reptiles (Squamata) from Brazil and Paraguay with description of a new species. Journal of Parasitology 93(2), 392–398.CrossRefGoogle ScholarPubMed
Sousa, MAN, Langguth, A and Gimenez, EA (2004) Brejos de altitude em Pernambuco e Paraíba: história natural, ecologia e conservação [Highland swamps in Pernambuco and Paraíba: Natural history, ecology and conservation]. pp. 229–254. Brasília: MMA. [In Portuguese.]Google Scholar
Teles, DA, Brito, SV, Araújo–Filho, JA, Teixeira, AAM, Ribeiro, SC, Mesquita, DO and Almeida, WO (2017) Nematode parasites of proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the caatinga domain of the neotropical region in Brazil. Herpetological Notes 10(2017), 525–527.Google Scholar
Teles, DA, Brito, SV, Araujo Filho, JA, Ribeiro, SC, Teixeira, AA, Mesquita, DO and Almeida, WO (2018) Nematodes of the Rhinella granulosa Spix, 1824 (Anura: Bufonidae) from the semiarid northeastern Caatinga Region of Brazil. Comparative Parasitology 85(2), 208–211.CrossRefGoogle Scholar
Todd, BD (2007) Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in Amphibians. The American Naturalist 170(5), 793–799.CrossRefGoogle ScholarPubMed
Toledo, GM, Fonseca, MG, Iannacone, J, Callirgos, JMC, Vidaurre, CUM and da Silva, RJ (2017) Parasitic helminths from Rhinella marina (Linnaeus, 1758) (Anura: Bufonidae) from Tarapoto, Peru. The Biologist (Lima) 15(2), 459–468.Google Scholar
Travassos, L, Freitas, JF and Kohn, A (1969) Trematódeos do Brazil [Brazil trematodes]. Memórias do Instituto Oswaldo Cruz 67(1), 1–886. [In Portuguese.]Google Scholar
Tung, KC, Hsiao, FC, Yang, CH, Chou, CC, Lee, WM, Wang, KS and Lai, CH (2009) Surveillance of endoparasitic infections and the first report of Physaloptera sp. and Sarcocystis spp. in farm rodents and shrews in central Taiwan. Journal of Veterinary Medical Science 71(1), 43–47.CrossRefGoogle ScholarPubMed
Vanzolini, PE (1981) A quasi-historical approach to the natural history of the differentiation of reptiles in tropical geographic isolates. Papéis Avulsos de Zoologia 34(19), 189–204.Google Scholar
Vicente, JJ, Rodrigues, HO, Gomes, DC and Pinto, RM (1991) Nematóides do Brasil, 2ª parte: Nematóides de anfíbios [Nematodes of Brazil, 2nd part: nematodes of amphibians]. Revista Brasileira de Zoologia 7(4), 549–626. [In Portuguese.]CrossRefGoogle Scholar
Vieira, EF, Lima, VD, Félix, AJS, Costa, MAT, Moura Pires, S, Santos, BMR and de Andrade, EB (2021) Fauna parasitária de Leptodactylus macrosternum (Anura: Leptodactylidae) no município de União–PI [Parasitic fauna of Leptodactylus macrosternum (Anura: Leptodactylidae) in the municipality of União-PI]. Brazilian Journal of Development 7(5), 49679–49692. [In Portuguese.]Google Scholar
Vitt, LJ and Caldwell, JP (2009) Herpetology, an introductory biology of amphibians and reptiles. 3rd edition. Amsterdam, Elsevier.Google Scholar
Wickham, H (2016) Ggplot2: Elegant graphics for data analysis. New York, Springer-Verlag.CrossRefGoogle Scholar
Windsor, DA (1998) Controversies in parasitology, most of the species on Earth are parasites. International Journal for Parasitology 28(12), 1939–1941.CrossRefGoogle Scholar
Yamaguti, S (1971) Systema Helminthum - Trematodes. Vol. I. London, Interscience Publishers.Google Scholar
Figure 0

Fig. 1. Schematic map of the sampling points in Maranguape mountain, Ceará state, northeastern Brazil. Red triangles represent sampling points.

Figure 1

Fig. 2. Anurans found in Maranguape mountain, Ceará state, northeastern Brazil: (A) Rhinella diptycha; (B) Rhinella granulosa; (C) Adelophryne maranguapensis; (D) Boana raniceps; (E) Corythomantis greeningi; (F) Dendropsophus minusculus; (G) Dendropsophus minutus; (H) Dendropsophus nanus; (I) Dendropsophus tapacurensis; (J) Scinax x-signatus; (K) Trachycephalus typhonius; (L) Adenomera juikitam; (M) Leptodactylus fuscus; (N) Leptodactylus macrosternum; (O). Leptodactylus mystaceus; (P) Leptodactylus pustulatus; (Q) Leptodactylus syphax; (R) Leptodactylus troglodytes; (S) Leptodactylus vastus; (T) Physalaemus cuvieri; (U) Elachistocleis piauiensis; (V) Proceratophrys cristiceps; (W) Proceratophrys renalis; (X) Pithecopus gonzagai; and (Y) Pristimantis relictus.

Figure 2

Table 1. The endoparasite community found in the anuran species from Maranguape mountain, Ceará state, northeastern Brazil.

Figure 3

Table 2. List of endoparasites found in the anuran species from Maranguape mountain, Ceará state, northeastern Brazil and literature review for previous records.

Figure 4

Fig. 3. Boxplot representing the parasite richness between the groups of microhabitats used by the anurans.

Figure 5

Fig. 4. Relationship of parasite richness (A) and abundance (B) with the host's body size (anuran interspecific view) from Maranguape mountain, Ceará state, northeastern Brazil.

Figure 6

Table 3. Relationship between parasite richness and abundance with anuran body size (snout–vent length (SVL) and mass), regarding an interspecific view, obtained through linear mixed models.