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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: [email protected]
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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).

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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.