Helminth Diversity in Anurans from the State of Piauí, Northeastern Brazil: New Occurrences and Ecological Aspects in a Caatinga-Cerrado ecotonal areaAbstract
Ecological studies and inventories regarding parasitic helminths in Piauí remain limited. Thus, this study aimed to describe the helminth communities of anurans in the State of Piauí, Northeastern Brazil, and present an updated list of helminth parasites of anurans for this state. We examined 145 anurans of 20 species. Among them, 48 specimens distributed across 12 host species were parasitized. The helminth communities included 12 nematodes and one cestode. We found 20 dominant taxa in the communities, four codominant, and five unsuccessful species. Most helminth parasites exhibited aggregated distribution patterns, and some taxa were found parasitizing more than one host species. In our literature review, we found 32 taxa from three groups (Nematoda, Platyhelminthes, and Acanthocephala) in 21 anuran host species. We report 20 new records of helminth infections in several anuran hosts that have previously been studied in the helminth communities in the State of Piauí, Brazil. In addition, we report the first time in three previously unexamined host species in the region, and present for the first record of Cylindrotaenia americana in Physalaemus cuvieri. These results provide new data on helminth diversity in Piauí and contribute to a better understanding of local patterns of parasite biodiversity.
Key words
Anuran; Helminths; Nematodes; Parasitism; Platyhelminthes
INTRODUCTION
Ecological studies provide new insights into helminth communities by considering factors such as parasite transmission mode, life cycle, colonization ability, and local availability, as well as host characteristics such as diet, phylogenetic history, and geographical distribution (Poulin 1999, 2007, Wood & Johnson 2015, Campião et al. 2015a, b, 2016). Additionally, environmental variables such as climate, seasonality, and habitat heterogeneity can influence the composition of helminth communities (Thieltges et al. 2009, Poulin et al. 2011, Silva et al. 2018). The interaction between these complex factors drives significant variations in parasite abundance and diversity among different anuran populations (Campião & Dáttilo 2020).
In recent years, the increase in parasitological studies in Northeastern Brazil has contributed significantly to the knowledge of the parasite fauna of anurans and the geographical distribution of their helminth species (Martins-Sobrinho et al. 2017, Benício et al. 2022). However, ecological surveys on helminths in the State of Piauí are limited to four studies, most of which focus on new host or locality records, without analyzing the structure of helminth communities, which emphasizes the need for further studies to understand the biodiversity of these parasites associated with anurans in the region (Vieira et al. 2021, Benício et al. 2022, Silva–Souza et al. 2024, Uchôa et al. 2025).
Thus, studies on parasite diversity can give data from conservation strategies for anurans and their habitats (Hopkins 2007). The understanding of how these communities are structured can help prioritize conservation efforts for particularly vulnerable host species or unique parasite assemblages (Poulin 1999). Furthermore, understanding the factors influencing helminth transmission can assist in mitigating potential impacts on anuran populations (Poulin 1997, Campião et al. 2014).
In this context, we evaluated the composition, richness, and diversity of helminth communities at both component and infracommunity levels in 20 anurans from an area of the State of Piauí, Northeastern Brazil. We also analyzed species affinities between these helminth communities and provided an updated list of all helminth species recorded in the state.
MATERIALS AND METHODS
Study area
We collected anurans in a transitional Caatinga-Cerrado area at Fazenda Betânia (4°13’31.08” S, 42°16’1.22” W), municipality of Barras, State of Piauí, Brazil (Fig. 1). The study area comprises distinct phytophysiognomies, which are characteristic of Cerrado, Caatinga, “Cocais”, Semideciduous Seasonal Forest, and Riparian Forest (Benício et al. 2021). The hosts were captured during active nocturnal searches conducted in January and March 2017, corresponding to the rainy season, and were identified according to Benício et al. (2021). The host species nomenclature followed Frost (2025).
Site of sample collection in Fazenda Betânia, municipality of Barras, State of Piauí, Brazil.
All institutional, national, and international guidelines for animal care and use were applied and approved by the Animal Research Ethics Committee of the “Universidade Estadual do Piauí” under license (08943/2016 CEUA/UESPI). The present study was approved by Instituto “Chico Mendes de Conservação˜ da Biodiversidade” (ICMBio), Brazil (license number SISBIO: 54745-1).
Host sampling and collection of parasites
The hosts were anesthetized, killed, measured the snout vent length (SVL) with a digital caliper (0.01 mm), weighed with an electronic precision balance (0.001g), and necropsied for helminthological examination. All internal organs were placed in Petri dishes with saline solution (NaCl 0.9%), dissected, and examined for parasites with a Leica EZ4 stereomicroscope (Wetzlar, Germany). The helminths were washed in saline solution, killed with heated 70% ethanol, and preserved in the same solution at room temperature.
The nematodes were cleared in 20% Amann’s Lactophenol and mounted on temporary slides. The cestodes were stained with Carmine acetic, differentiated in 1% hydrochloric alcohol, neutralized in alkaline alcohol, dehydrated in an increasing ethanol series, clarified in methyl salicylate, and mounted in Damar gum as permanent preparations (Amato et al. 1991).
All specimens were analyzed with an Olympus BX41 microscope (Olympus, Tokyo, Japan) coupled with a drawing tube (without zoom adjustment), and an Olympus BX53 microscope (Olympus America, Center Valley, Pennsylvania) equipped with differential interference contrast optics and a digital imaging system for morphological analysis. The parasites were identified based on keys and catalogs proposed by Vicente et al. (1991), Anderson (2009a, b), and species description articles.
Data analysis
The infection prevalence, mean intensity, and mean abundance were calculated according to Bush (1997) using Quantitative Parasitology 3.0 software. The structure of the helminth communities was investigated at the infracommunity (all helminth populations of a single host specimen) and community levels (all helminth infracommunities within the host populations).
We calculate the variance-to-mean ratio (ID) and the index of discrepancy of Poulin (D) for species with prevalence >10% to determine the distribution pattern of parasite infracommunities using the Quantitative Parasitology 3.0 software (Bush et al. 1990, Rózsa et al. 2000, Reiczigel et al.2005). The significance of ID for each parasite species was tested using d-statistics, where d > 1.96 = aggregate distribution; d < −1.96 = uniform distribution; −1.96 < d < 1.96 = random distribution (Ludwig & Reynolds 1988).
We used the method proposed by Thul et al. (1985) to calculate the importance of each parasite in the community. Thus, the helminth species were classified into four groups: dominant (I ≥ 1.0), codominant (0.01 ≤ I < 1.0), subordinate (0 < I < 0.01), and unsuccessful (I = 0), based on their prevalence, intensity, and maturity factor (equal to 1.0 if at least one mature specimen of species is found and equal to 0 if otherwise).
The composition of helminth families across host families was represented in a stacked bar chart, following González et al. (2021). We calculate the proportion of taxa within the helminth families relative to the total number of helminth taxa found in each host family. The chart was performed using ‘dplyr’ and ‘ggplot2’ packages in the R software version 4.4.0 (R Core Team). Bars were scaled to 100% to represent the proportional species richness.
Additionally, we performed a bibliographic search to compile records of helminth parasitic anurans from the State of Piauí, using seven electronic databases (Google, Google Scholar, PubMed, Scielo, Science Direct, Scopus, and Web of Science). The search employed the following strings: [(“Anurans”), (“Piauí”), and (“helminth” or “parasites” or “nematodes” or “platyhelminthes” or “acanthocephalan”)]. We organized the collected data into a table, which included published records, available data, and information from the present study.
RESULTS
We obtained 145 host individuals belonging to 20 species across four anuran families (Hylidae, Leptodactylidae, Bufonidae, and Microhylidae). The overall parasite prevalence was 33.1% (48 specimens infected out of 145 collected). A total of 12 host species are infected with at least one parasite taxon, while eight host species were not infected: Dendropsophus nanus (Boulenger, 1889), Dendropsophus minutus (Peters, 1872), Dendropsophus minusculus (Rivero, 1971), Dendropsophus soaresi (Caramaschi and Jim, 1983), Leptodactylus fuscus (Schneider, 1799), Leptodactylus troglodytes Lutz, 1926, Dermatonotus muelleri (Boettger, 1885), and Pleurodema diplolister (Peters, 1870). The parasite communities included 412 specimens from 13 taxa of parasitic helminths: Aplectana sp., Aplectana membranosa Schneider, 1866, Cosmocerca parva Travassos, 1925, Oxyascaris oxyascaris Travassos, 1920, Rhabdias breviensis Nascimento, Gonçalves, Melo, Giese, Furtado and Santos, 2013, Cosmocercidae gen. sp., Oswaldocruzia sp. (five morphotypes), and Physaloptera sp.; as well as one species of cestode: Cylindrotaenia americana Jewell, 1916 (Fig. 2) (Table I, II).
Helminth parasites recorded on anurans from the municipality of Barras, State of Piauí, Brazil. Prevalence (P), mean intensity (MI), mean abundance (MA) and importance value (I). Classification of helminths: dominant (I ≥ 1.0), codominant (0.01 ≤ I < 1.0), and unsuccessful species (I = 0).
Photomicrographs of the helminth species associated with anurans from municipality of Barras, State of Piauí, Brazil: (a) Cosmocerca parva male anterior region; (b) Cosmocerca parva male caudal region; (c) Aplectana membranosa male caudal region; (d) Oxyascaris oxyascaris female anterior region; (e) Oxyascaris oxyascaris female caudal region; (f) Oxyascaris oxyascaris female median region, showing the vulva; (g) Cylindrotaenia americana scolex region; (h) Cylindrotaenia americana strobila region; (i) Rhabdias breviensis female median region, showing the vulva.
Aplectana membranosa (n = 132), Oswaldocruzia sp. (n = 100), and O. oxyascaris (n = 56) were the most frequently observed. Some taxa were found parasitizing more than one host species (Table II). We identified 20 dominant, four codominant, and five unsuccessful species (Table I). Most of the helminths exhibited aggregated distribution patterns (Table III). All anuran families were infected by cosmocercids, which represented the highest proportion of taxa (77.18%). The Leptodactylidae family had the most significant number of helminth families (five), followed by Bufonidae (three), and Hylidae (three) (Fig. 3).
Dispersion index (DI), d-statistic (d), discrepancy index (D) and distribution for the parasite infracommunities (prevalence >10%) of anurans (n ≥ 5) from municipality of Barras, State of Piauí, Brazil. Distribution classification: d < 1.96, random distribution; d > 1.96, aggregate distribution.
Helminth community associated with 13 anuran species from a Caatinga-Cerrado area in Northeastern Brazil.
Composition (%) of helminth families parasitizing each anuran family from the municipality of Barras, State of Piauí, Brazil.
In our literature review, we identified 32 helminth taxa recorded in the State of Piauí, Brazil, distributed among three major groups: Nematoda (five families and ten genera), Platyhelminthes (two families and two genera), and Acanthocephala (two families and two genera). The most representative family was Cosmocercidae, with 16 taxa, followed by Molineidae (five), Rhabdiasidae (three), Physalopteridae (two), Nematotaeniidae (one), Polystomatidae (one), Centrorhynchidae (one), and Oligacanthorhynchidae (one), and one additional occurrence of Acanthocephala (cystacanth). These helminths were found parasitizing 21 anuran species belonging to the families Bufonidae, Hylidae, Leptodactylidae, Microhylidae, and Odontophrynidae.
DISCUSSION
The helminth communities in our study comprised 13 helminth taxa associated with a total of 12 anuran species. Notably, the composition of these parasites exhibited patterns consistent with findings from Northeastern Brazil, as many of the helminth taxa recorded previously were also found herein (Martins-Sobrinho et al. 2017, De Oliveira et al. 2019, Madelaire et al. 2020, Sousa-Machado et al. 2022, Benício et al. 2022, De Oliveira et al. 2022, Sampaio et al. 2022).
In Northeastern Brazil, several studies have documented helminths in anurans from the Hylidae, Leptodactylidae, and Bufonidae families (De Oliveira et al. 2019, 2024). Notably, we present the first record of helminths in the hylid frogs Boana raniceps (Cope, 1862) and Pithecopus gonzagai Andrade, Haga, Ferreira, Recco-Pimentel, Toledo, and Bruschi, 2020; and the leptodactylid frog Physalaemus albifrons (Spix, 1824), from the State of Piauí (Table IV). The new records from hosts and localities found in the present study reinforce the suggestion by Campião et al. (2015a) that, on average, four studies are needed to reveal 50% of the expected species richness of helminth parasites in anuran hosts.
Records of helminth parasites of anurans from the State of Piauí, Brasil. NH = New host record. NL = New locality record. *for Piauí state.
Nematodes, particularly generalists with a direct life cycle, predominated within the communities, while only one Platyhelminthes species (C. americana) was observed. Several studies have indicated that nematodes, especially members of the Cosmocercidae family, are the most prevalent helminth parasites of anurans in Northeastern Brazil and throughout South America (Campião et al. 2014, 2016, Graça et al. 2017, Martins-Sobrinho et al. 2017, Toledo et al. 2018, De Oliveira et al. 2022, Sampaio et al. 2022, Neves et al. 2024). Moreover, the timing of host sampling, particularly conducted during the rainy season, may have affected our findings by influencing fluctuations in host populations. According to Poulin et al. (2007), host size populations are directly related to the acquisition of generalist parasites in communities.
In our analysis, the nematodes A. membranosa, O. oxyascaris, and C. parva showed higher prevalence and importance values among the cosmocercids, with these species being dominant in almost all species of Bufonidae, Hylidae, and Leptodactylidae (Table I). Previous studies have also reported cosmocercids with high prevalence across diverse anuran families, reinforcing that these species exhibit low host specificity (Bursey et al. 2001, Campião et al. 2016, Toledo et al. 2018, González et al. 2021, De Oliveira et al. 2022, Sampaio et al. 2022, Benício et al. 2022, Euclydes & Campião 2024).
We observed a high diversity of Oswaldocruzia Travassos, 1917 species in Rhinella diptycha (Cope, 1862), Rhinella granulosa (Spix, 1824), Leptodactylus macrosternum Miranda-Ribeiro, 1926, and Leptodactylus vastus Lutz, 1930, represented by five morphotypes. The low number of male specimens in our samples makes diagnosis at the species, as specific male characteristics are essential for accurate identification. This limitation is similar to findings from other studies in the State of Piauí (Vieira et al. 2021, Silva-Sousa et al. 2024, Uchôa et al. 2025), except for Benício et al. (2022), who recorded O. lopesi Freitas and Lent, 1938 in L. vastus, and Uchôa et al. (2025), who recorded O. mazzai Travassos, 1935 in five anuran species. The diversity of morphotypes observed here suggests the potential discovery of new species of the genus in this region.
The anurans found in the present study represent the definitive host for most helminth specimens, except for Physaloptera sp. (larvae), which was found in four arboreal and one semi-aquatic host (Scinax aff. similis (Cochran, 1952), B. raniceps, Trachycephalus typhonius (Linnaeus, 1758), P. gonzagai, and Leptodactylus sp.). It was noted that these anurans may act as paratenic hosts and exhibited the lowest values of prevalence, intensity, abundance, and importance (unsuccessful species), suggesting potential accidental infection. These nematodes were predominantly recorded in terrestrial and semi-aquatic anurans, with some records in arboreal hosts (Martins-Sobrinho et al. 2017, Cardoso et al. 2021, Euclydes et al. 2022, González et al. 2021, Neves et al. 2024).
The generalist cestode C. americana was again recorded in R. granulosa (Da Silva– Souza et al. 2024), and it is the first time found in Physalaemus cuvieri Fitzinger, 1826 in the State of Piauí. The species was also reported from the Caatinga biome in the leptodactylids Ph. cicada Bokermann, 1966 and Pl. diplolister in the State of Ceará (Silva–Souza et al. 2024, De Oliveira et al. 2019, Uchôa et al. 2025).
Most helminths displayed a typical aggregated distribution pattern, which is a common trait for parasites. The overdispersed distributions of these taxa are thought to be influenced by stochastic environmental factors, differences in host susceptibility to infection, the host’s immune response, and mechanisms of parasite transmission (Hamann et al. 2012, González et al. 2021). However, the random dispersion observed in some helminths may be attributed to their very low parasite density, as also suggested by Kennedy (2009).
In the literature review, helminths of the family Cosmocercidae were the most frequently recorded, with A. membranosa standing out as the most common species. It was found in four different hosts (Scinax fuscovarius, L. vastus, R. granulosa, and R. diptycha), demonstrating its ability to parasitize multiple species regardless of their habits. Leptodactylus vastus is the most extensively researched in terms of its parasitic fauna in the State of Piauí (eight taxa), due to its wide distribution and local abundance. The review reinforces the importance of further research in the region, four anuran species are known to host only a single helminth taxon (Scinax x-signatus (Spix, 1824), Adenomera juikitam Carvalho and Giaretta, 2013, Ph. albifrons and L. fuscus), suggesting that helminth diversity may be currently underestimated.
Our study investigated helminth communities in 20 anuran species collected in an ecotonal area between the Cerrado-Caatinga from the State of Piauí, Northeastern Brazil. We identified 13 helminth taxa, and nematode generalists with direct life cycles showed the highest prevalence and dominance. We report 20 new records of helminth infections in hosts for several anurans that have previously been studied for parasites, and three new host species (B. raniceps, P. gonzagai, and P. albifrons) had not yet been investigated in Piauí. In addition, we present the first record of C. americana in P. cuvieri (Table IV).
Our results, together with previous studies (Campião et al. 2014, Cardoso et al. 2021, Neves et al. 2024, De Oliveira et al. 2024), reinforce the hypothesis that nematodes, specifically cosmocercids, are the most adapted group of parasites in anuran populations. Our data also support the hypothesis that parasite communities have an aggregated pattern of distribution. These results provide new data on helminth diversity in Piauí and contribute to a better understanding of local patterns of parasite biodiversity.
Acknowledgements
We are grateful to MSc. Luiz Felipe Ferreira Trindade for help in preparing the map. We are thankful to students from the Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” (Federal University of Pará, Belém, Brazil) and students from the Laboratory of Zoology and Parasitic Biology (State University of Piauí, Brazil) to help on collecting the hosts and the helminths. This study was supported by Fundação Amazônia de Amparo a Estudos e Pesquisa (FAPESPA) (001/2021 – PROGRAMA DE APOIO A NÚCLEOS EMERGENTES – Process number: 51/2021), Federal University of Pará, Fundação de Amparo à Pesquisa do Estado do Piauí (FAPEPI) for providing a research fellowship to (R.A.B., 301239/2022-3), State University of Piauí by research fellowship PIBIC-CNPq to (A. J. S. F, 2018-1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Research productivity scholarship of CNPq to F.T.V.M. (Process number 314116/ 2021–4).
References
- AMATO J, BOEGER W & AMATO S. 1991. Protocolos para laboratório: coleta e processamento de parasitos de pescado. Seropédica, RJ: Imprensa Universitária da UFRRJ.
- ANDERSON RC. 2009a. Nematode Parasites of Vertebrates: Their Development and Transmission. Wallingford, Oxon: CABI Publishing.
- ANDERSON RC. 2009b. Keys to the Nematode Parasites of Vertebrates. Wallingford: CABI Publishing.
- BENÍCIO RA, AVILA RW & FONSECA MG. 2021. Guia ilustrado dos anfíbios e répteis de Barras, Piauí. Teresina: EDUFPI.
- BENÍCIO RA, SANTOS RSD, FREIRE SM, ÁVILA RW, SILVA RJD & FONSECA MG. 2022. Diversity of helminth parasites in amphibians from northeastern Brazil. Biologia 77: 2571-2579.
- BURSEY CR, GOLDBERG SR & PARMELEE JR. 2001. Gastrointestinal helminths of 51 species of anurans from Reserva Cuzco Amazónico, Peru. Comp Parasitol 68: 21-35.
- BUSH AO. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83: 575-583.
- BUSH AO, AHO JM & KENNEDY CR. 1990. Ecological versus phylogenetic determinants of helminth parasite community richness. Evol Ecol 4: 1-20.
- CAMPIÃO KM & DÁTTILO W. 2020. Biological drivers of individual-based anuran–parasite networks under contrasting environmental conditions. J Helminthol 94: e167.
- CAMPIÃO KM, DIAS OT, SILVA RJ, FERREIRA VL & TAVARES LER. 2016. Living separately and facing similar problems: are frog helminth parasites determined by the host or by the habitat? Can J Zool 94: 761-765.
- CAMPIÃO KM, MORAIS DH, DIAS OT, AGUIAR A, TOLEDO GDM, TAVARES LER & SILVA RJD. 2014. Checklist of helminth parasites of amphibians from South America. Zootaxa 3843: 1-93.
- CAMPIÃO KM, RIBAS A & TAVARES LER. 2015a. Diversity and patterns of interaction of an anuran–parasite network in a neotropical wetland. Parasitology 142: 1751-1757.
- CAMPIÃO KM, RIBAS ACDA, MORAIS DH, SILVA RJD, TAVARES LER. 2015b. How Many Parasites Species a Frog Might Have? Determinants of Parasite Diversity in South American Anurans. PLoS ONE 10(10): 1-12.
- CARDOSO EL, JESUS RF, SILVA-FILHO HF, WILLKENS Y, SANTANA GL, SANTOS AN, SANTOS JN & MELO FTV. 2021. Do environmental and host variables influence the parasite community of Leptodactylus fuscus (Anura: Leptodactylidae) in Amazon Region? J Parasitol 107: 904-910.
- DE OLIVEIRA CR, ÁVILA RW & MORAIS DH. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga biome, Brazil. Acta Parasitol 64: 205-212.
- DE OLIVEIRA CR, MASCARENHAS W, BATISTA-OLIVEIRA D, DE CASTRO ARAÚJO K, ÁVILA RW & BORGES-NOJOSA DM. 2022. Endoparasite community of anurans from an altitudinal rainforest enclave in a Brazilian semiarid area. J Helminthol 96: e62.
- DE OLIVEIRA SS, MACHADO HTS, ARAÚJO KC, SILVA CS & ÁVILA RW. 2024. Nematodes associated with Leptodactylus cf. mystaceus (Anura: Leptodactylidae) in agricultural landscapes of Ibiapaba plateau, Ceará state, Brazil. Caldasia 46(2): 371-380.
- EUCLYDES L, DUDCZAK AC & CAMPIÃO KM. 2022. Anuran’s habitat use drives the functional diversity of nematode parasite communities. Parasitol Res 120: 993-1001.
- EUCLYDES R & CAMPIÃO KM. 2024. Patterns in parasite diversity and interactions with anurans from the Atlantic Forest. Parasitol Int 102: 102914.
-
FROST DR. 2025. Amphibian Species of the World: an Online Reference. Version 6.2. American Museum of Natural History, New York, USA. https://amphibiansoftheworld.amnh.org/index.php
» https://amphibiansoftheworld.amnh.org/index.php - GONZÁLEZ CE, HAMANN MI & DURÉ MI. 2021. Nematodes of amphibians from the South American Chaco: distribution, host specificity and ecological aspects. Diversity 13: 321.
- GRAÇA RJ, ODA FH, LIMA FS, GUERRA V, GAMBALE PG & TAKEMOTO RM. 2017. Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil. J Nat Hist 51: 705-729.
- HAMANN MI, KEHR AI & GONZALEZ CE. 2012. Community structure of helminth parasites of Leptodactylus bufonius (Anura: Leptodactylidae) from northeastern Argentina. Zool Stud 51: 1454-1463.
- HOPKINS WA. 2007. Amphibians as models for studying environmental change. ILAR J. 48(3): 270-277.
- KENNEDY CR. 2009. The ecology of parasites of freshwater fishes: the search for patterns. Parasitology 136: 1653-1662.
- LUDWIG JA & REYNOLDS JF. 1988. Statistical ecology: a primer in methods and computing. New York: John Wiley & Sons, 337 p.
- MADELAIRE CB, FRANCESCHINI L, MORAIS DH, GOMES FR & DA SILVA RJ. 2020. Helminth parasites of three anuran species during reproduction and drought in the Brazilian semiarid Caatinga region. J Parasitol 106: 334-340.
- MARTINS-SOBRINHO PM, SILVA WGO, SANTOS EG, MOURA GJB & OLIVEIRA JB. 2017. Helminths of some tree frogs of the families Hylidae and Phyllomedusidae in an Atlantic rainforest fragment. Braz J Nat Hist 51: 1639-1648.
- MÜLLER MI, MORAIS DH, COSTA-SILVA GJ, AGUIAR A, ÁVILA RW & DA SILVA RJ. 2018. Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): evidence for cryptic speciation. Zool Scr 47: 595-607.
- NEVES JKS, CARDOSO EL, REBÊLO GL, FÉLIX AJS, MACHADO SA, COSTA-CAMPOS CE & MELO FTV. 2024. Filling the gaps on parasites of Osteocephalus: helminth community structure of Osteocephalus cabrerai (Anura: Hylidae) from the Brazilian Amazon. Int J Parasitol Parasites Wildl 25: 100996.
- POULIN R. 1997. Species richness of parasite assemblages: evolution and patterns. Annu Rev Ecol Evol Syst 28: 341-358.
- POULIN R. 1999. The functional importance of parasites in animal communities: many roles at many levels? Int J Parasitol 29: 903-914.
- POULIN R. 2007. The structure of parasite communities in fish hosts: Ecology meets geography and climate. Parasitologia 49: 169-172.
- POULIN R, BLANAR CA, THIELTGES DW & MARCOGLIESE DJ. 2011. The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34: 540-551.
- REICZIGEL J, LANG Z, RÓZSA L & TÓTHMÉRÉSZ B. 2005. Properties of crowding indices and statistical tools to analyze parasite crowding data. J Parasitol 91: 245-252.
- RÓZSA L, REICZIGEL J & MAJOROS G. 2000. Quantifying parasites in samples of hosts. J Parasitol 86: 228-232.
- SAMPAIO NKS, TEIXEIRA AAM, DO NASCIMENTO JM, RIBEIRO SC, ALMEIDA WO & BRITO SV. 2022. Endoparasite community structure of an anuran assemblage in the Caatinga, Northeastern Neotropical Region. J Helminthol 96: e78, 1-8.
- SOUSA-MACHADO HT, DE OLIVEIRA SS, BENÍCIO RA, DE CASTRO ARAÚJO K & ÁVILA RW. 2022. Helminths infecting sympatric congeneric treefrogs in Northeastern Brazil. Acta Parasitol 67: 1-10.
- SILVA CS, ÁVILA RW & MORAIS DH. 2018. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55: 292.
- SILVA-SOUSA LFS, PIRES SM, CARVALHO TRC, RODRIGUES JPS, LIMA EVS, FONSECA MG, BENÍCIO RA & FREIRE SM. 2024. Helminths infecting Rhinella diptycha Cope, 1862 and Rhinella granulosa Spix, 1824 from Northeastern Brazil. Neotrop Helminthol 18: 79-92.
- TAVARES LER, CAMPIÃO KM, COSTA-PEREIRA R & PAIVA F. 2017. Helmintos endoparasitos de vertebrados silvestres em Mato Grosso do Sul, Brasil. Iheringia Sér Zool 107: e2017106.
- THUL JE, FORRESTER DJ & ABERCROMBIE CL. 1985. Ecology of parasitic helminths of wood ducks, Aix sponsa, in the Atlantic flyway. Proc Helminthol Soc Wash 52: 297-310.
- THIELTGES DW, FERGUSON MA, JONES CS, KRAKAU M, DE MONTAUDOUIN X, NOBLE LR, REISE K & POULIN R. 2009. Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160: 163-173.
- TOLEDO GM, SCHWARTZ HO, NOMURA HAQ, AGUIAR A, VELOTA RAMV, DA SILVA RJ & ANJOS LA. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. J Helminthol 92: 438-444.
- UCHÔA JS, OLIVEIRA P, SOARES AR, LIMA DS, RODRIGUES R & PEREIRA FB. 2025. Endoparásitos associados a anfíbios anuros en un área de conservación del Parque Nacional de Sete Cidades, estado de Piauí, Brasil. Neotrop Helminthol 19.
- VICENTE JJ, RODRIGUES HO, GOMES DC & PINTO RM. 1991. Nematóides do Brasil 2ª parte: nematoides de anfíbios. Rev Bras Zool 7: 549-626.
- VIEIRA EF, LIMA VD, FÉLIX AJS, COSTA MAT, PIRES SM, SANTOS BMR, FREIRE SM & DE ANDRADE EB. 2021. Fauna parasitária de Leptodactylus macrosternum (Anura: Leptodactylidae) no município de União - PI. Braz J Dev 7: 49679-49692.
- WOOD CL & JOHNSON PTJ. 2015. A world without parasites: exploring the hidden ecology of infection. Front Ecol Environ 13: 425-434.
Edited by
-
Handling editor
Patricia Alvarenga
Data will be made available upon reasonable request.
