Abstract:

Parasites are an important component of the global biomass, having significant roles in several regulatory mechanisms in the ecosystem. Parasitism is one of the most common ecological interactions on the planet. Studies have shown that the helminth fauna of only 8% of amphibian species in Brazil have been studied, and this percentage is lower for the Odontophrynidae family, with only four of the 50 species kown to occur in Brazil having been investigated. Here, we present the helminth fauna of Proceratophrys ararype, an anuran endemic to the “Brejo de Altitude” Chapada do Araripe (Araripe Plateau), northeastern Brazil. The infection parameters analyzed were prevalence, mean intensity of infection and mean abundance of parasites. We used the Pearson’s linear correlation coefficient to check the correlations between the abundance of the parasites with the snout-vent length (SVL) of hosts. To verify the degree of aggregation of parasites in hosts, we used the dispersion index. Out of 40 specimens examined, 19 specimens were infected with at least one parasite. The overall prevalence was 47.5% with a mean infection intensity of 18.93 ± 10.77. The endoparasitic community associated with P. ararype consisted of six species of parasites, with Falcaustra mascula having the highest prevalence (25%). Most parasites had a uniform dispersion index in the hosts and their abundance was unrelated to host size. Here, we also present a compilation of all parasites associated with host species of the genus Proceratophrys from South America. Overall, we found 23 species of parasites associated with five host species (P. ararype, P. appendiculata, P. boiei, P. cristiceps, P. mantiqueira). Of these, two species of parasites (Oswaldocruzia mazzai and Strongyloides sp.) represent new records for the genus Proceratophrys. Our results demonstrate the lack of studies on amphibian helminth fauna and fill an important knowledge gap on the diversity of parasites of Proceratophrys ararype, an endemic frog from the Araripe Plateau, northeastern Brazil.

Keywords:
Parasitism; Nematoda; Anuran

Resumo:

Os parasitas são um componente importante da biomassa global, tendo papel significativo em vários mecanismos reguladores no ecossistema. O parasitismo é uma das interações ecológicas mais comuns no planeta. Estudos demonstraram que somente 8% da fauna de helmintos das espécies de anfíbios que ocorrem no Brasil foi estudada, sendo esta porcentagem mais baixa para a família Odontophrynidae, tendo sido investigadas apenas quatro das 50 espécies com ocorrência conhecida para o Brasil. Aqui, apresentamos a helmintofauna de Proceratophrys ararype, um anuro endêmico do “Brejo de Altitude” Chapada do Araripe, nordeste do Brasil. Os parâmetros de infecção analisados foram prevalência, intensidade média de infecção e abundância média de parasitas. Utilizamos o coeficiente de correlação linear de Pearson para verificar as correlações entre a abundância dos parasitas com o comprimento rostro-cloacal dos hospedeiros. Para verificar o grau de agregação dos parasitas nos hospedeiros, utilizamos o índice de dispersão. Dos 40 espécimes examinados, 19 estavam infectados com pelo menos um parasita. A prevalência geral foi de 47.5% com intensidade média de infecção de 18.93 ± 10.77. A comunidade endoparasitária associada a P. ararype constituiu de seis espécies de parasitas, com Falcaustra mascula tendo a maior prevalência (25%). A maioria dos parasitas apresentaram índice de dispersão uniforme nos hospedeiros e sua abundância não esteve relacionada ao tamanho do hospedeiro. Aqui, nós também apresentamos uma compilação de todos os parasitas associados as espécies de hospedeiros do gênero Proceratophrys na América do Sul. No geral, nós encontramos 23 espécies de parasitas associadas a cinco espécies de hospedeiros (P. ararype, P. appendiculata, P. boiei, P. cristiceps, P. mantiqueira). Destas, duas espécies de parasitas (Oswaldocruzia mazzai e Strongyloides sp.) representam novos registros para o gênero Proceratophrys. Nossos resultados demonstram a carência de estudos sobre a helmintofauna de anfíbios e preenchem uma importante lacuna de conhecimento sobre a diversidade de parasitas de Proceratophrys ararype, um sapo endêmico do Planalto do Araripe, nordeste do Brasil.

Palavras-chave:
Parasitismo; Nematoda; Anuros

Introduction

Currently, 50 species of the Odontophrynidae family have been identified, with the genus Miranda-Ribeiro, 1920 making up 40 species registered in Brazil, Argentina, and Paraguay (Segalla et al. 2019SEGALLA, M.V., CARAMASCHI, U., CRUZ, C.A.G., GARCIA, P.C.A., GRANT, T., HADDAD, C.F.B., SANTANA, D.J., TOLEDO, L.F. & LANGONE, J.A. 2019. Lista de espécies brasileiras-Brazilian Amphibians: List of Species. Herpetologia Brasileira 8:65-96., Mângia et al. 2020MÂNGIA, S., OLIVEIRA, E.F., SANTANA, D.J., KOROIVA, R., PAIVA, F. & GARDA, A.A. 2020. Revising the taxonomy of Proceratophrys Miranda-Ribeiro, 1920 (Anura: Odontophrynidae) from the Brazilian semiarid Caatinga: morphology, calls and molecules support a single widespread species. J. Zool. Syst. Evol. Res. 00:1-22. https://doi.org/10.1111/jzs.12365 (last access on 15/03/2020)
https://doi.org/10.1111/jzs.12365... , Frost 2021FROST, D.R. 2021. Amphibian species of the world: An online reference. Versão 6.1. New York: American Museum of Natural History. Disponível em <https://amphibiansoftheworld.amnh.org/index.php> (last access on 04/03/2021).
https://amphibiansoftheworld.amnh.org/in... ). Species of the genus Proceratophry can be clumped into four species groups, based on the morphological similarities of adult individuals (Cruz et al. 2005CRUZ, C.A.G., PRADO, G.M. & IZECKSOHN, E. 2005. Nova espécie de Proceratophrys Miranda-Ribeiro, 1920 do sudeste do Brasil (Amphibia, Anura, Leptodactylidae). Arq. Mus. Nac. 63:289-295., Prado & Pombal 2008PRADO, G.M. & POMBAL JR, J.P. 2008. Espécies de Proceratophrys Miranda-Ribeiro, 1920 com apêndices palpebrais (Anura; Cycloramphidae). Arq. Zool. 39:1-85. https://doi.org/10.11606/issn.2176-7793.v39i1p1-85 (last access on 12/08/2018)
https://doi.org/10.11606/issn.2176-7793.... , Mângia et al. 2018MÂNGIA, S., KOROIVA, R., NUNES, P.M.S., ROBERTO, I.J., ÁVILA, R.W., SANT’ANNA, A.C., SANTANA, D.J. & GARDA, A.A. 2018. A new species of Proceratophrys (Amphibia: Anura: Odontophrynidae) from the Araripe plateau, Ceará state, northeastern Brazil. Herpetologica 74:255-268. https://doi.org/10.1655/Herpetologica-D-16-00084.1 (last access on 04/08/2018)
https://doi.org/10.1655/Herpetologica-D-... ): P. appendiculata, P. bigibbosa, P. boiei and P. cristiceps species groups. The P. cristiceps group comprises 14 species including P. ararype Mângia, Koroiva, Nunes, Roberto, Ávila, Sant’Anna, Santana & Garda, 2018 (Ávila et al. 2011ÁVILA, R.W., KAWASHITA-RIBEIRO, R.A. & MORAIS, D.H. 2011. A new species of Proceratophrys (Anura: Cycloramphidae) from western Brazil. Zootaxa 2890:20-28., Brandão et al. 2013BRANDÃO, R.A., CARAMASCHI, U., VAZ-SILVA, W. & CAMPOS, L.A. 2013. Three new species of Proceratophrys Miranda-Ribeiro 1920 from Brazilian Cerrado (Anura, Odontophrynidae). Zootaxa 3750:321-347. http://dx.doi.org/10.11646/zootaxa.3750.4.2 (last access on 22/08/2018)
http://dx.doi.org/10.11646/zootaxa.3750.... , Mângia et al. 2018MÂNGIA, S., KOROIVA, R., NUNES, P.M.S., ROBERTO, I.J., ÁVILA, R.W., SANT’ANNA, A.C., SANTANA, D.J. & GARDA, A.A. 2018. A new species of Proceratophrys (Amphibia: Anura: Odontophrynidae) from the Araripe plateau, Ceará state, northeastern Brazil. Herpetologica 74:255-268. https://doi.org/10.1655/Herpetologica-D-16-00084.1 (last access on 04/08/2018)
https://doi.org/10.1655/Herpetologica-D-... ). This species was identified from specimens collected at the slope of Chapada do Araripe, a humid forest in the municipality of Crato, state of Ceará, northeastern Brazil. The distribution of this species is very restricted and limited to the slope of Chapada do Araripe (Mângia et al. 2018MÂNGIA, S., KOROIVA, R., NUNES, P.M.S., ROBERTO, I.J., ÁVILA, R.W., SANT’ANNA, A.C., SANTANA, D.J. & GARDA, A.A. 2018. A new species of Proceratophrys (Amphibia: Anura: Odontophrynidae) from the Araripe plateau, Ceará state, northeastern Brazil. Herpetologica 74:255-268. https://doi.org/10.1655/Herpetologica-D-16-00084.1 (last access on 04/08/2018)
https://doi.org/10.1655/Herpetologica-D-... ), a climate exception area in the Caatinga biome (Tabarelli & Silva 2003TABARELLI, T. & SILVA, J.M.C. 2003. Áreas e ações prioritárias para a conservação da biodiversidade da caatinga. In: Ecologia e conservação da caatinga (I.R. LEAL, M. TABARELLI, J.M.C. SILVA & M.L.B. BARROS, eds). UFPE, Recife, p.777-796.), where local climatic conditions shape isolated systems (Vanzolini 1981VANZOLINI, P.E. 1981. A quasi-historical approach to the natural history of the differentiation of reptiles in tropical geographic isolates. Pap. Avulsos Zool. 34:189-204., Borges-Nojosa & Caramaschi 2003BORGES-NOJOSA, D.M. & CARAMASCHI, U. 2003: Composição e análise comparativa da diversidade e das afinidades biogeográficas dos lagartos e anfisbenídeos (Squamata) dos brejos nordestinos. In: Ecologia e conservação da Caatinga (I. Leal, M. Tabarelle & J.M.C. Silva eds). UFPE, Recife, p.489-540.). Currently, information on the associated parasitic fauna of P. ararype is lacking.

The parasites are integral components of the global biomass, and one of the most common life forms on the planet (Kuris 2008KURIS, A.M. 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515-518. https://doi.org/10.1038/nature06970 (last access on 09/12/2019)
https://doi.org/10.1038/nature06970... , Poulin 2014POULIN, R. 2014. Parasite biodiversity revisited: frontiers and constraints. Int. J. Parasitol. 44:581-589., Oliveira et al. 2019OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... ). Among these parasites, the helminth fauna associated with amphibians is rich and diverse, despite being hidden within known biodiversity (Poulin 2014POULIN, R. 2014. Parasite biodiversity revisited: frontiers and constraints. Int. J. Parasitol. 44:581-589., Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... ). The study of parasitic fauna is extremely important due to the roles they have in several regulatory mechanisms within the ecosystem, including the negative effects they have on their hosts such as anaemia, anorexia, reduced survival and fertility, and competition (Vitt & Caldwell 2009VITT, L.J. & CALDWELL, J.P. 2009. Herpetology, an introductory biology of amphibians and reptiles. 3 ed. Elsevier, Amsterdam., Matias et al. 2018MATIAS, C.S.L., FERREIRA-SILVA, C., SOUSA, J.G.G. & ÁVILA, R.W. 2018. Helminths infecting the black false boa Pseudoboa nigra (Squamata: Dipsadidae) in northeastern Brazil. Acta. Herpetol. 13:171-175. https://doi.org/10.13128/Acta_Herpetol-23366 (last access on 07/09/2019)
https://doi.org/10.13128/Acta_Herpetol-2... ). The study of these organisms not only contributes to our knowledge of animal diversity, but also clarifies the parasite dynamics of the host (Brooks & Hoberg 2001BROOKS, D.R. & HOBERG, E.P. 2001. Parasite systematics in the 21st century: opportunities and obstacles. Trends Parasitol. 17:273-275. https://doi.org/10.1016/S1471-4922(01)01894-3 (last access on 26/11/2019)
https://doi.org/10.1016/S1471-4922(01)01... , Galli et al. 2001GALLI, P., CROSA, G., MARINIELLO, L., ORTIS, M. & D’AMELIO, S. 2001. Water quality as a determinant of the composition of fish parasites communities. Hydrobiologia 452:173-179. https://doi.org/10.1023/A:1011958422446 (last access on 03/12/2019)
https://doi.org/10.1023/A:1011958422446... , Poulin 2014POULIN, R. 2014. Parasite biodiversity revisited: frontiers and constraints. Int. J. Parasitol. 44:581-589.), because the richness of parasite species can be assumed as a characteristic of the host, where rates of parasite colonization vary according to biology of hosts (Poulin 2014POULIN, R. 2014. Parasite biodiversity revisited: frontiers and constraints. Int. J. Parasitol. 44:581-589., Campião et al. 2015CAMPIÃO, K.M., RIBAS, A.C.A., MORAIS, D.H., DIAS, O.T., SILVA, R.J. & TAVARES, L.E.R. 2015. How many parasites species a frog might have? Determinants of parasite diversity in south american anurans. PloS one 10:e0140577. https://doi.org/10.1371/journal.pone.0140577 (last access on 08/09/2018)
https://doi.org/10.1371/journal.pone.014... ).

The latest checklist of helminths in South America stated that only about 8% of all amphibian species in Brazil have had their helminth fauna studied (Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... ). Of the Proceratophrys genus, the helminth fauna of only four species has been studied: P. tupinamba Prado & Pombal, 2008PRADO, G.M. & POMBAL JR, J.P. 2008. Espécies de Proceratophrys Miranda-Ribeiro, 1920 com apêndices palpebrais (Anura; Cycloramphidae). Arq. Zool. 39:1-85. https://doi.org/10.11606/issn.2176-7793.v39i1p1-85 (last access on 12/08/2018)
https://doi.org/10.11606/issn.2176-7793.... (Boquimpani-Freitas et al. 2001BOQUIMPANI-FREITAS, I.D., VRCIBRADIC, D., VICENTE, J.J., BURSEY, C.R., ROCHA, C.F.D. & SLUYS, M.V. 2001. Helminths of the horned leaf frog, Procetatophrys appendiculata, from southeastern Brazil. J. Helminthol. 75:233-236.), P. cristiceps Müller, 1883 (Teles et al. 2017TELES, D.A., BRITO, S.V., ARAÚJO-FILHO, J.A., TEIXEIRA, A.A.M., RIBEIRO, S.C., MESQUITA, D.O. & ALMEIDA, W.O. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetol. notes 10:525-527., Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179., Sampaio et al. 2020SAMPAIO, N.K.S, SILVA, E.G., PINTO, C.L.M., DUARTE, R.G., TEIXEIRA, A.A.M., ALMEIDA, W.O. & BRITO, S.V. 2020. Proceratophrys aridus Endoparasites. Herpetol. Rev. 51:302.), P. boiei Wied-Neuwied, 1824 (Toledo et al. 2018TOLEDO, G.M., SCHWARTZ, H.O., NOMURA, H.A.Q., AGUIAR, A., VELOTA, R.A.M.V., DA SILVA, R.J. & ANJOS, L.A. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. J. Helminthol. 92:438-444. https://doi.org/10.1017/S0022149X17000608 (last access on 12/09/2019)
https://doi.org/10.1017/S0022149X1700060... ), and P. mantiqueira Mângia, Santana, Cruz & Feio, 2014 (Almeida-Santos et al. 2017ALMEIDA-SANTOS, M., SIQUEIRA, C.C., ANJOS, L.A., VAN SLUYS, M., ROCHA, C.F.D. 2017. Ecological aspects of the horned leaf-frog Proceratophrys mantiqueira (Odontophrynidae) in an Atlantic Rainforest area of southeastern Brazil. Salamandra 53:413-422.). As such, studies on parasitism are of fundamental importance for the conservation of hosts, especially those with a restricted distribution, in addition to filling knowledge gaps in host-parasite interactions, since hosts, in general, are more susceptible to local extinctions (Pontes & Rocha 2011PONTES, J.A.L. & ROCHA, C.F.D. 2011. Leaf litter amphibians of brazilian atlantic rainflorest: current status of knowledge. Oecologia Aust. 15:750-761. http://dx.doi.org/10.4257/oeco.2011.1504.01 (last access on 04/03/2021)
http://dx.doi.org/10.4257/oeco.2011.1504... ). Here we describe the composition and patterns of parasitic infection of helminths associated with P. ararype, an endemic frog from Chapada do Araripe, northeastern Brazil, and also present a compilation of all parasites associated with host species of the genus Proceratophrys from South America.

Material and Methods

This study was conducted on the slope of Chapada do Araripe in the state of Ceará, Brazil, within the limits of the Environmental Protection Area of Chapada do Araripe (APA Araripe). The owerall landscape is characterized of different vegetation types, with cut-outs of humid forest (sampled area), dry forest, Cerrado and Cerradão (Ferreira-Silva et al. 2019FERREIRA-SILVA, C., RIBEIRO, S.C., ALCANTARA, E.P. & ÁVILA, R.W. 2019. Natural history of the rare and endangered snake Atractus ronnie (Serpentes: Colubridae) in northeastern Brazil. Phyllomedusa 18:77-87.). Specimens of P. ararype were collected at night from the following locations: (i) Clube Recreativo Grangeiro (7°16’47”S, 39°26’18”W, 706 m asl, WGS84) and Nascente (7°15’21”S, 39°28’08”W, 739 m asl, WGS84), both in the municipality of Crato; (ii) Sítio Farias (7°20’17”S, 39°23’43”W, 600 m asl, WGS84), in the municipality of Barbalha; and (iii) Sítio Aleixo (7°26’25”S, 39°05’27”W, 946 m asl, WGS84) and Sítio Riachão (7°27’05”S, 39°06’38”W, 931 m asl, WGS84), both in the municipality of Missão Velha. The sampling period extended from November 7, 2018 to February 22, 2019.

A total of 40 Proceratophrys specimens were collected using the active search method (visual and auditory) (Bernarde 2012BERNARDE, P.S. 2012. Anfíbios e répteis: introdução ao estudo da herpetofauna brasileira. 1 ed. Anolis Books, Curitiba.). Specimens were kept in individualized plastic containers and later euthanized by lethal injection of Lidocaine Hydrochloride (CFMV 2013CONSELHO FEDERAL DE MEDICINA VETERINÁRIA - CFMV 2013. Métodos de eutanásia. In: Guia brasileiro de boas práticas de eutanásia em animais (Comissão de ética, Bioética e bem-estar animal - CFMV, eds). ASCOM/CFMV, Brasília, p.28-29.). We measured the snout-vent lengths (SVL, in mm) of hosts using a digital caliper Mitutoyo® (precision 0.01 mm). Hosts were fixed according to Calleffo (2002)CALLEFFO, M.E.V. 2002. Anfíbios. In: Técnicas de coleta e preparação de vertebrados para fins científicos e didáticos (P. Auricchio & M.G. Salomão eds). Instituto Pau Brasil de História Natural, São Paulo, p.45-73. and deposited in the Herpetological Collection of the Regional University of Cariri, (URCA-H 15.579-15.616), Crato municipality and in the Herpetological Collection of the Federal University of Cariri (CHERP-UFCA 01-02), Brejo Santo municipality, both in the Ceará state, Brazil.

Specimens were necropsied and the organs (gastrointestinal tract, lungs, liver, kidneys and internal cavity) were harvested for analyses. Helminths were collected and fixed according to Amato et al. (1991)AMATO, J.F.R., BOEGER, W.A. & AMATO, S.B. 1991. Protocolos para laboratório-coleta e processamento de parasitos de pescado. Imprensa Universitária, Universidade Federal Rural do Rio de Janeiro, Seropédica. and Andrade (2000)ANDRADE, C.M. 2000 Meios e soluções comumente empregados em laboratórios. Editora Universidade Rural, Rio de Janeiro., the remaining food items were also accounted. For the identification of nematodes, we followed Vicente et al. (1991)VICENTE, J.J., RODRIGUES, H.O., GOMES, D.C. & PINTO, R.M. 1991. Nematóides do Brasil, 2ª parte: Nematóides de anfíbios. Rev. Bras. Zool. 7:549-626. https://doi.org/10.1590/S0101-81751990000400015 (last access on 05/05/2019)
https://doi.org/10.1590/S0101-8175199000... , in addition to recent studies on species descriptions. Analysed infection parameters include prevalence (P%), mean infection intensity (MII), and mean parasite abundance (MA), as previously described by Bush et al. (1997)BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. & SHOSTAK, A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83:575-583.. All the parasites were deposited in the Parasitology Collection of Universidade Federal do Cariri (CHERP-P-UFCA 01-29), Brejo Santo municipality, Ceará state, Brazil.

We used the Pearson’s linear correlation coefficient (r) to assess correlation between parasite abundance with host snout-vent length (SLV, in mm). The Mantel test was used to evaluate spatial autocorrelation between parasitic richness and sampled areas to verify if use the data as one or several parasite communities. The variance / mean ratio (s2/x̅), also known as the dispersion index (ID), and the k parameter of the negative binomial distribution, were used to determine the degree of parasite aggregation within the hosts. The higher the s2/x̅ ratio, and the lower the value of parameter k (closer to zero), the higher the level of aggregation (Pielou 1977PIELOU, E.C. 1977. Mathematical ecology. Wiley-Interscience Publication. New-York.).

To compile literature data on parasites associated with host species of the genus Proceratophrys from South America, we conducted a wide search in different databases (e.g., Google Academic, Scielo, Scopus) and in bibliographic reviews on the topic (e.g., Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... ).

Ethical Standards

The authors assert that all procedures contributing to this study comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals. The study was approved by the Ethical Committee of Universidade Regional do Cariri (CEUA/URCA, process number 00260/2016.1) and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio/SISBIO, number 66099-2).

Results

We examined 40 P. ararype specimens, of these 19 (five females and 14 males) were parasitized by 511 helminths, with a total prevalence of 47.5% and mean infection intensity of 18.93 ± 10.77. The P. ararype endoparasitic community was comprised of six parasite species: Aplectana membranosa Schneider, 1866, Falcaustra mascula Rudolphi, 1819, Oswaldocruzia mazzai Travassos, 1935, Physaloptera sp., Raillietnema spectans Gomes, 1964 and Strongyloides sp. Falcaustra mascula had the highest prevalence (25%) and R. spectans had the lowest prevalence (2.5%), the highest abundance rate (6.5), and a mean intensity of (260.0) (Table 1).

There was no correlation between parasite general abundance and host snout-vent length (R² = 0.01, p = 0.43), when analyzing the most prevalent parasite species individually, we also found no significant correlation between parasite abundance and SVL: A. membranosa (R² = 0.13, p = 0.79), Physaloptera sp. (R² = 0.34, p = 0.56), and F. mascula (R² = 0.18, p = 0.61). Additionally, spatial autocorrelation was not observed between sample areas and parasitized individuals (R² = 0.3545, p = 0.11667). Examination of pattern dispersion revealed that most helminth species had a uniform distribution among hosts (Table 2), that is, the growth in the number of infected individuals is directly proportional to the prevalence of infection.

In our literature data compilation, we found, in general, five host species (P. ararype, P. appendiculata, P. boiei, P. cristiceps, P. mantiqueira) being parasitized by 23 helminth species. Proceratophrys cristiceps was the host species with the highest number of associated parasitic helminths (n = 10 spp.). Physaloptera sp. was the only helminth common to all studied Proceratophrys species (Table 3). In this study we identified two additional species (O. mazzai and Strongyloides sp.) (Figure 1A, B) registered for the genus Proceratophrys.

Figure 1
New parasite records for Proceratophrys ararype. (A) Oswaldocruzia mazzai, posterior view with taxonomic diagnostic characteristics (spicula and copulating bag; in red, measure of the spicula). (B) Strongyloides sp., total view with taxonomic diagnostic characteristics (prolonged esophagus and ovary disposition).

Discussion

The genus Proceratophrys has 23 species of registered parasites (Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... , Almeida-Santos et al. 2017ALMEIDA-SANTOS, M., SIQUEIRA, C.C., ANJOS, L.A., VAN SLUYS, M., ROCHA, C.F.D. 2017. Ecological aspects of the horned leaf-frog Proceratophrys mantiqueira (Odontophrynidae) in an Atlantic Rainforest area of southeastern Brazil. Salamandra 53:413-422., Teles et al. 2017TELES, D.A., BRITO, S.V., ARAÚJO-FILHO, J.A., TEIXEIRA, A.A.M., RIBEIRO, S.C., MESQUITA, D.O. & ALMEIDA, W.O. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetol. notes 10:525-527., Toledo et al. 2018TOLEDO, G.M., SCHWARTZ, H.O., NOMURA, H.A.Q., AGUIAR, A., VELOTA, R.A.M.V., DA SILVA, R.J. & ANJOS, L.A. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. J. Helminthol. 92:438-444. https://doi.org/10.1017/S0022149X17000608 (last access on 12/09/2019)
https://doi.org/10.1017/S0022149X1700060... , Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179., Sampaio et al. 2020SAMPAIO, N.K.S, SILVA, E.G., PINTO, C.L.M., DUARTE, R.G., TEIXEIRA, A.A.M., ALMEIDA, W.O. & BRITO, S.V. 2020. Proceratophrys aridus Endoparasites. Herpetol. Rev. 51:302., this study). Like observations made in previous studies, we observed a particular parasitic community per host species, with Physaloptera sp. being the only helminth common to all studied Proceratophrys species (Table 3). This result could be due to the geographical locations of each species, which have different environmental conditions, and thereby affecting the composition and richness of biotic factors (Poulin & Krasnov 2010POULIN, R. & KRASNOV, B.R. 2010. Similarity and variability of parasite assemblages across geographical space. In: The biogeography of host-parasite interactions (S. Morand & B.R. Krasnov, eds). Oxford University, New York, p.115-128.). On the other hand, P. cristiceps, which has a wide geographical distribution (Mângia et al. 2020MÂNGIA, S., OLIVEIRA, E.F., SANTANA, D.J., KOROIVA, R., PAIVA, F. & GARDA, A.A. 2020. Revising the taxonomy of Proceratophrys Miranda-Ribeiro, 1920 (Anura: Odontophrynidae) from the Brazilian semiarid Caatinga: morphology, calls and molecules support a single widespread species. J. Zool. Syst. Evol. Res. 00:1-22. https://doi.org/10.1111/jzs.12365 (last access on 15/03/2020)
https://doi.org/10.1111/jzs.12365... ), was the best studied species (Teles et al. 2017TELES, D.A., BRITO, S.V., ARAÚJO-FILHO, J.A., TEIXEIRA, A.A.M., RIBEIRO, S.C., MESQUITA, D.O. & ALMEIDA, W.O. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetol. notes 10:525-527., Müller et al. 2018MÜLLER, M.I., MORAIS, D.H., COSTA-SILVA, G.J., AGUIAR, A., ÁVILA, R.W. & SILVA, R.J. 2018. Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): evidence for cryptic speciation. Zoologica Scripta 47:595-607. https://doi.org/10.1111/zsc.12304 (last access on 11/09/2019)
https://doi.org/10.1111/zsc.12304... , Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179., Sampaio et al. 2020SAMPAIO, N.K.S, SILVA, E.G., PINTO, C.L.M., DUARTE, R.G., TEIXEIRA, A.A.M., ALMEIDA, W.O. & BRITO, S.V. 2020. Proceratophrys aridus Endoparasites. Herpetol. Rev. 51:302.) and with the highest number of associated parasitic helminths (n = 10 spp.). This result emphasizes that habitat, along with the biology, life history of the host and study effort, can influence parasitic composition (Campião et al. 2015CAMPIÃO, K.M., RIBAS, A.C.A., MORAIS, D.H., DIAS, O.T., SILVA, R.J. & TAVARES, L.E.R. 2015. How many parasites species a frog might have? Determinants of parasite diversity in south american anurans. PloS one 10:e0140577. https://doi.org/10.1371/journal.pone.0140577 (last access on 08/09/2018)
https://doi.org/10.1371/journal.pone.014... ).

Species of the genus Aplectana are usually found infecting the large intestine of reptiles and amphibians, have a direct life cycle, and actively infect their hosts (Travassos 1931TRAVASSOS, L. 1931. Pesquisas helmintologicas realizadas em Hamburgo. IX Ensaio monographico da familia Cosmocercidae Trav., 1925 (Nematoda). Mem. Inst. Oswaldo Cruz 25:237-298., Anderson 2000ANDERSON R.C. 2000. Nematode parasites of vertebrates, their development and transmission. 2 ed. CABI Publishing, Wallingford., Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... , Lins et al. 2017LINS, A.G.S., AGUIAR, A., MORAIS, D.H., DA SILVA, L.A.F., ÁVILA, R.W. & SILVA, R.J. 2017. Helmintofauna de Leptodactylus syphax (Anura: Leptodactylidae) do bioma da Caatinga, nordeste do Brasil. Rev. Bras. Parasitol. Vet. 26:74-80. https://doi.org/10.1590/s1984-29612017013 (last access on 02/09/2019)
https://doi.org/10.1590/s1984-2961201701... ). This genus has been observed in four species of the Odontophrynidae family: Proceratophrys tupinamba and P. boiei, infected by A. delirae Fabio, 1971 (Boquimpani-Freitas et al. 2001BOQUIMPANI-FREITAS, I.D., VRCIBRADIC, D., VICENTE, J.J., BURSEY, C.R., ROCHA, C.F.D. & SLUYS, M.V. 2001. Helminths of the horned leaf frog, Procetatophrys appendiculata, from southeastern Brazil. J. Helminthol. 75:233-236., Klaion et al. 2011KLAION, T., GOMES, M.A., TAVARES, L.E.R., ROCHA, C.F.D. & SLUYS, M.V. 2011. Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic Rainforest remnants in southeastern Brazil. An. Acad. Bras. Ciênc. 83:1303-1312. https://doi.org/10.1590/S0001-37652011000400017 (last access on 04/06/2019)
https://doi.org/10.1590/S0001-3765201100... ), and P. cristiceps (Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179., Sampaio et al. 2020SAMPAIO, N.K.S, SILVA, E.G., PINTO, C.L.M., DUARTE, R.G., TEIXEIRA, A.A.M., ALMEIDA, W.O. & BRITO, S.V. 2020. Proceratophrys aridus Endoparasites. Herpetol. Rev. 51:302.) and Odontophrynus americanus Duméril & Bibron, 1841, infected by A. membranosa (Lent & Freitas 1948LENT, H. & FREITAS, J.F.T. 1948. Una colecao de nematodeos, parasitos de vertebrados, do museu de Historia Natural de Montevideo. Mem. Inst. Oswaldo Cruz 46:1-71. http://dx.doi.org/10.1590/s0074-02761948000100001 (last access on 12/10/2019)
http://dx.doi.org/10.1590/s0074-02761948... ). In this study, A. membranosa has also been registered for P. ararype, and it is the parasite with the second highest prevalence, abundance, and overall mean intensity. High indices were also found for Leptodactylus syphax (MII= 250.4) (Lins et al. 2017LINS, A.G.S., AGUIAR, A., MORAIS, D.H., DA SILVA, L.A.F., ÁVILA, R.W. & SILVA, R.J. 2017. Helmintofauna de Leptodactylus syphax (Anura: Leptodactylidae) do bioma da Caatinga, nordeste do Brasil. Rev. Bras. Parasitol. Vet. 26:74-80. https://doi.org/10.1590/s1984-29612017013 (last access on 02/09/2019)
https://doi.org/10.1590/s1984-2961201701... ) and P. cristiceps (MII= 65.5; cited as P. aridus by Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179.). High infection values ​​ can be explained by the low host vagility that contributes to increased parasite transmission (Mcalpine 1997MCALPINE, D.F. 1997. Helminth communities in bullfrogs (Rana catesbeiana), green frogs (R. clamitans), and leopard frogs (R. pipiens) from new brunswick, Canada. Can. J. Zool. 75:1883-1890. https://doi.org/10.1139/z97-818 (last access on 04/07/2019)
https://doi.org/10.1139/z97-818... ). Additionally, A. membranosa females produce large amounts of infective larvae in the environment, increasing infection rates (Lins et al. 2017LINS, A.G.S., AGUIAR, A., MORAIS, D.H., DA SILVA, L.A.F., ÁVILA, R.W. & SILVA, R.J. 2017. Helmintofauna de Leptodactylus syphax (Anura: Leptodactylidae) do bioma da Caatinga, nordeste do Brasil. Rev. Bras. Parasitol. Vet. 26:74-80. https://doi.org/10.1590/s1984-29612017013 (last access on 02/09/2019)
https://doi.org/10.1590/s1984-2961201701... ).

Falcaustra mascula has been shown to infect the small and large intestine of several amphibians (e.g., Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... , Toledo et al. 2015TOLEDO, G.M., MORAIS, D.H., SILVA, R.J. & ANJOS, L.A. 2015. Helminth communities of Leptodactylus latrans (Anura: Leptodactylidae) from the Atlantic rainforest, south-eastern Brazil. J. Helminthol. 89:250-254. https://doi.org/10.1017/S0022149X1300076X (last access on 12/09/2019)
https://doi.org/10.1017/S0022149X1300076... , Toledo et al. 2018TOLEDO, G.M., SCHWARTZ, H.O., NOMURA, H.A.Q., AGUIAR, A., VELOTA, R.A.M.V., DA SILVA, R.J. & ANJOS, L.A. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. J. Helminthol. 92:438-444. https://doi.org/10.1017/S0022149X17000608 (last access on 12/09/2019)
https://doi.org/10.1017/S0022149X1700060... , Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179.). Little is known about its modes of transmission. Anderson (2000)ANDERSON R.C. 2000. Nematode parasites of vertebrates, their development and transmission. 2 ed. CABI Publishing, Wallingford. suggested that the larvae reach its third development stage and then infect an intermediate invertebrate host, which in turn is ingested by amphibians. Toledo et al. (2018)TOLEDO, G.M., SCHWARTZ, H.O., NOMURA, H.A.Q., AGUIAR, A., VELOTA, R.A.M.V., DA SILVA, R.J. & ANJOS, L.A. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. J. Helminthol. 92:438-444. https://doi.org/10.1017/S0022149X17000608 (last access on 12/09/2019)
https://doi.org/10.1017/S0022149X1700060... found that among all host parasites F. mascula had the highest prevalence rate in Boana faber (Wied-Neuwied, 1821) (P = 9.1%), Leptodactylus latrans (Steffen, 1815) (P = 13.9%), and Rhinella icterica (Spix, 1824) (P = 33.3%). Therefore, our result for prevalence rate (P = 25%) is consistent with the literature data. One plausible explanation for the high infection rates observed for this parasite is that the intermediate host is an arthropod, which is a type of prey that is extensively consumed by anurans.

Oswaldocruzia mazzai have been shown to infect a variety of anuran hosts (e.g., Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... , Teles et al. 2015TELES, D.A., SOUSA, J.G.G., TEIXEIRA, A.A.M., SILVA, M.C., OLIVEIRA, R.H., SILVA, M.R.M. & ÁVILA, R.W. 2015. Helminths of the frog Pleurodema diplolister (Anura, Leiuperidae) from the Caatinga in Pernambuco state, northeast Brazil. Braz. J. Biol. 75:251-253. https://doi.org/10.1590/1519-6984.08513 (last access on 12/09/2019)
https://doi.org/10.1590/1519-6984.08513... , Alcantara et al. 2018ALCANTARA, E.P., FERREIRA-SILVA, C., SILVA, L.A.F., LINS, A.G.S., ÁVILA, R.W., MORAIS, D.H. & SILVA, R.J. 2018. Helminths of Dermatonotus muelleri (Anura: Microhylidae) from Northeastern Brazil. J. Parasitol. 104:550-556., Oliveira et al. 2019OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... ) but our study is the first to record a species of the genus Proceratophrys as a host of O. mazzai. The low host specificity is usual for some groups of helminths (Campião et al. 2015CAMPIÃO, K.M., RIBAS, A.C.A., MORAIS, D.H., DIAS, O.T., SILVA, R.J. & TAVARES, L.E.R. 2015. How many parasites species a frog might have? Determinants of parasite diversity in south american anurans. PloS one 10:e0140577. https://doi.org/10.1371/journal.pone.0140577 (last access on 08/09/2018)
https://doi.org/10.1371/journal.pone.014... , Oliveira et al. 2019OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... ). The great diversity of hosts registered for O. mazzai is related to the direct life cycle, and the simple mode of transmission that can occur by ingesting eggs or larval penetration into the host’s skin (Anderson 2000ANDERSON R.C. 2000. Nematode parasites of vertebrates, their development and transmission. 2 ed. CABI Publishing, Wallingford.).

Nematodes of the Physaloptera genus have a worldwide geographical distribution and have been recorded in several classes of terrestrial vertebrates, including felines (Ogassawara 1986OGASSAWARA, S., BENASSI, S., LARSSON, C.E., LEME, P.T.Z. & HAGIWARA, M.K. 1986. Prevalência de infecções helmínticas em gatos na cidade de São Paulo. Rev. Fac. Med. Vet. Zootec. Univ. S. Paulo 23:145-149. https://doi.org/10.11606/issn.2318-3659.v23i2p145-149 (last access on 03/06/2019)
https://doi.org/10.11606/issn.2318-3659.... ), rodents (Tung et al. 2009TUNG, K.C., HSIAO, F.C., YANG, C.H., CHOU, C.C., LEE, W.M., WANG, K.S. & LAI, C.H. 2009. Surveillance of endoparasitic infections and the first report of Physaloptera sp. and Sarcocystis spp. in farm rodents and shrews in central Taiwan. J. Vet. Med. Scien. 71:43-47. https://doi.org/10.1292/jvms.71.43 (last access on 04/10/2019)
https://doi.org/10.1292/jvms.71.43... ), lizards (Da Silva et al. 2008DA SILVA, A.S., ZANETTE, R.A., TOCHETTO, C., OLIVEIRA, C.B., SOARES, J.F., OTTO, M.A. & MONTEIRO, S.G. 2008. Parasitismo por Physaloptera sp., Kalicephalus sp. e Cryptosporidium sp. em lagarto (Tupinambis teguixin) no Rio Grande do Sul, Brasil. Rev. Bras. Zoociência 10:269-272., Cabral et al. 2018CABRAL, A.N., TELES, D.A., BRITO, S.V., ALMEIDA, W.O., DOS ANJOS, L.A., GUARNIERI, M.C. & RIBEIRO, S.C. 2018. Helminth parasites of Mabuya arajara Rebouças-Spieker, 1981 (Lacertilia: Mabuyidae) from Chapada do Araripe, northeastern Brazil. Parasitol. Res. 117:1185-1193. https://doi.org/10.1007/s00436-018-5797-7 (last access on 16/04/2020)
https://doi.org/10.1007/s00436-018-5797-... ) and anurans (Da Graça et al. 2017DA GRAÇA, R.J., ODA, F.H., LIMA, F.S., GUERRA, V., GAMBALE, P.G. & TAKEMOTO, R.M. 2017. Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil. J. Nat. Hist. 51:705-729. https://doi.org/10.1080/00222933.2017.1296197 (last access on 29/09/2019)
https://doi.org/10.1080/00222933.2017.12... ). This parasite was usual for all studied Proceratophrys species (see Table 3). In amphibians, this parasite is usually found in larval stage, making it difficult to identify at the species level, and is suggestive that these amphibians are not definitive hosts. Although there is not enough data about its life cycle, nematodes of this genus are known to use insects during their intermediate phase (Anderson 2000ANDERSON R.C. 2000. Nematode parasites of vertebrates, their development and transmission. 2 ed. CABI Publishing, Wallingford.). Additionally, the acquisition of Physaloptera by anuran hosts occurs through the ingestion of infected insects, mainly Orthoptera (Klaion et al. 2011KLAION, T., GOMES, M.A., TAVARES, L.E.R., ROCHA, C.F.D. & SLUYS, M.V. 2011. Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic Rainforest remnants in southeastern Brazil. An. Acad. Bras. Ciênc. 83:1303-1312. https://doi.org/10.1590/S0001-37652011000400017 (last access on 04/06/2019)
https://doi.org/10.1590/S0001-3765201100... ).

The Strongyloides genus has a low specificity, with records for several classes, including mammals (occasionally humans), birds, reptiles, and amphibians (Little 1966LITTLE, M.D. 1966. Seven new species of Strongyloides (Nematoda) from Louisiana. J. Parasitol. 52:85-97. https://doi.org/10.2307/3276397 (last access on 29/10/2019)
https://doi.org/10.2307/3276397... , Urquhart et al. 1998URQUHART, G.M., ARMOUR, J., DUNCAN, J.L. & JENNINGS, F.W. 1998. Parasitologia Veterinária. 2ª ed. Guanabara Koogan, Rio de Janeiro.). Although there is a lack of detailed biology on this parasite, it is known to have a direct or indirect life cycle, with the former being the most usual (Santos et al. 2010SANTOS, K.R., CARLOS, B.C., PADUAN, K.S., KADRI, S.M., BARRELLA, T.H., AMARANTE, M.R.V., RIBOLLA, P.E.M. & SILVA, R.J. 2010. Morphological and molecular characterization of Strongyloides ophidiae (Nematoda, Strongyloididae). J. Helminthol. 84:136-142. https://doi.org/10.1017/S0022149X09990381 (last access on 04/10/2019)
https://doi.org/10.1017/S0022149X0999038... ). The infection occurs on land through skin penetration or ingestion of infected preys (Mati & Melo 2014MATI, V.L.T. & MELO, A.L. 2014. Some aspects of the life history and morphology of Strongyloides ophidiae Pereira, 1929 (Rhabditida: Strongyloididae) in Liophis miliaris (Squamata: Dipsadidae). Neotrop. Helminthol. 8:203-216., Sulieman et al. 2015SULIEMAN, Y., AFIFI, A., AWAD, H.M. & PENGSAKUL, T. 2015. Helminth parasites of the subdesert toad, Amietophrynus (Bufo) xeros (Anura: Bufonidae). Int. J. Res. - Granthaalayah 3:75-83.). Even though this nematode infects several amphibian species (Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... , Sulieman et al. 2015SULIEMAN, Y., AFIFI, A., AWAD, H.M. & PENGSAKUL, T. 2015. Helminth parasites of the subdesert toad, Amietophrynus (Bufo) xeros (Anura: Bufonidae). Int. J. Res. - Granthaalayah 3:75-83.), this is the first record of the genus Strongyloides acting as a parasite for species of the Odontophrynidae family.

The parasite Raillietnema spectans was initially described in the large intestine of leptodactylids and bufonids (Alcântara et al. 2018), and it has been registered for several other species: Rhinella crucifer (Wied-Neuwied, 1821), R. icterica and Leptodactylus latrans (Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... ), Pleurodema diplolister (Peters, 1870) (Teles et al. 2015TELES, D.A., SOUSA, J.G.G., TEIXEIRA, A.A.M., SILVA, M.C., OLIVEIRA, R.H., SILVA, M.R.M. & ÁVILA, R.W. 2015. Helminths of the frog Pleurodema diplolister (Anura, Leiuperidae) from the Caatinga in Pernambuco state, northeast Brazil. Braz. J. Biol. 75:251-253. https://doi.org/10.1590/1519-6984.08513 (last access on 12/09/2019)
https://doi.org/10.1590/1519-6984.08513... ), Physalaemus albifrons (Spix, 1824), P. cicada Bokermann, 1966 P. cuvieriFitzinger, 1826 (Oliveira et al. 2019OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... ), and Dermatonotus muelleri (Boettger, 1885) (Alcantara et al. 2018ALCANTARA, E.P., FERREIRA-SILVA, C., SILVA, L.A.F., LINS, A.G.S., ÁVILA, R.W., MORAIS, D.H. & SILVA, R.J. 2018. Helminths of Dermatonotus muelleri (Anura: Microhylidae) from Northeastern Brazil. J. Parasitol. 104:550-556.). This parasite is known to presents a direct life cycle and transmission that occurs via ingestion or penetration of larvae in the skin (Anderson 2000ANDERSON R.C. 2000. Nematode parasites of vertebrates, their development and transmission. 2 ed. CABI Publishing, Wallingford.). In this study, R. spectans had the lowest prevalence, contrary to the results from Alcântara et al. (2018) and Oliveira et al. (2019)OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... . This low prevalence may be related to host phylogeny, which is reflected in the structuring of parasitic interactions (Krasnov et al. 2012KRASNOV, B.R., FORTUNA, M.A., MOUILLOT, D., KHOKHLOVA, I.S., SHENBROT, G.I. & POULIN, R. 2012. Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. Am. Nat. 179:501-511. https://doi.org/10.1086/664612 (last access on 01/11/2019)
https://doi.org/10.1086/664612... ), or geographical, biological, and life history effects on the host, which can influence parasitic composition (Campião et al. 2015CAMPIÃO, K.M., RIBAS, A.C.A., MORAIS, D.H., DIAS, O.T., SILVA, R.J. & TAVARES, L.E.R. 2015. How many parasites species a frog might have? Determinants of parasite diversity in south american anurans. PloS one 10:e0140577. https://doi.org/10.1371/journal.pone.0140577 (last access on 08/09/2018)
https://doi.org/10.1371/journal.pone.014... ).

Helminths registered for the genus Proceratophrys are usually found in other taxa of amphibians, and therefore can be considered generalists (Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... , Müller et al. 2018MÜLLER, M.I., MORAIS, D.H., COSTA-SILVA, G.J., AGUIAR, A., ÁVILA, R.W. & SILVA, R.J. 2018. Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): evidence for cryptic speciation. Zoologica Scripta 47:595-607. https://doi.org/10.1111/zsc.12304 (last access on 11/09/2019)
https://doi.org/10.1111/zsc.12304... , Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179.). Nevertheless, studies on Procetatophrys cristiceps (Teles et al. 2017TELES, D.A., BRITO, S.V., ARAÚJO-FILHO, J.A., TEIXEIRA, A.A.M., RIBEIRO, S.C., MESQUITA, D.O. & ALMEIDA, W.O. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetol. notes 10:525-527., Müller et al. 2018MÜLLER, M.I., MORAIS, D.H., COSTA-SILVA, G.J., AGUIAR, A., ÁVILA, R.W. & SILVA, R.J. 2018. Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): evidence for cryptic speciation. Zoologica Scripta 47:595-607. https://doi.org/10.1111/zsc.12304 (last access on 11/09/2019)
https://doi.org/10.1111/zsc.12304... , Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179.), and P. ararype (this study), in northeastern Brazil, and on P. boiei, P. mantiqueira and P. tupinamba, in humid forests of southeastern Brazil (Boquimpani-Freitas et al. 2001BOQUIMPANI-FREITAS, I.D., VRCIBRADIC, D., VICENTE, J.J., BURSEY, C.R., ROCHA, C.F.D. & SLUYS, M.V. 2001. Helminths of the horned leaf frog, Procetatophrys appendiculata, from southeastern Brazil. J. Helminthol. 75:233-236., Klaion et al. 2011KLAION, T., GOMES, M.A., TAVARES, L.E.R., ROCHA, C.F.D. & SLUYS, M.V. 2011. Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic Rainforest remnants in southeastern Brazil. An. Acad. Bras. Ciênc. 83:1303-1312. https://doi.org/10.1590/S0001-37652011000400017 (last access on 04/06/2019)
https://doi.org/10.1590/S0001-3765201100... , Almeida-Santos et al. 2017ALMEIDA-SANTOS, M., SIQUEIRA, C.C., ANJOS, L.A., VAN SLUYS, M., ROCHA, C.F.D. 2017. Ecological aspects of the horned leaf-frog Proceratophrys mantiqueira (Odontophrynidae) in an Atlantic Rainforest area of southeastern Brazil. Salamandra 53:413-422., Toledo et al. 2018TOLEDO, G.M., SCHWARTZ, H.O., NOMURA, H.A.Q., AGUIAR, A., VELOTA, R.A.M.V., DA SILVA, R.J. & ANJOS, L.A. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. J. Helminthol. 92:438-444. https://doi.org/10.1017/S0022149X17000608 (last access on 12/09/2019)
https://doi.org/10.1017/S0022149X1700060... ), show a greater similarity between helminth communities in locally close hosts. These results suggest that geographic distribution of the host, and the different local conditions, could influence the composition of helminth fauna.

We did not find correlation between parasitism and host size. This result contrasts with those found for the genus Leptodactylus, where body size accounted for 17% of the variation in species composition, compared to the 3% accounted for the host’s habitat (Campião et al. 2016aCAMPIÃO, K.M., DIAS, O.T., SILVA, R.J., FERREIRA, V.L. & TAVARES, L.E.R. 2016a: Living apart and having similar trouble: are frog helminth parasites determined by the host or by the habitat? Can. J. Zool. 94:761-765. https://doi.org/10.1139/cjz-2016-0066 (last access on 02/10/2018)
https://doi.org/10.1139/cjz-2016-0066... ). However, our results were similar to those described by Oliveira et al. (2019)OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... for Physalaemus species. This similarity between the results may be due to the smaller size variation, when species are analysed separately, as observed for Physalaemus by Oliveira et al. (2019)OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... and for Proceratophrys in this study, different from that observed in the genus Leptodactylus by Campião et al. (2016a)CAMPIÃO, K.M., DIAS, O.T., SILVA, R.J., FERREIRA, V.L. & TAVARES, L.E.R. 2016a: Living apart and having similar trouble: are frog helminth parasites determined by the host or by the habitat? Can. J. Zool. 94:761-765. https://doi.org/10.1139/cjz-2016-0066 (last access on 02/10/2018)
https://doi.org/10.1139/cjz-2016-0066... . Thus, the diversity of parasites in Proceratophrys ararype does not appear to be influenced by the size of the hosts.

The dispersion of parasites in Procetatophrys ararype was uniform for most species (Table 2). One of the most usual characteristics of parasitic infections in populations of vertebrate hosts is aggregation, because these infections rarely happen or are due to the high lethality in infected hosts, which cannot survive for long periods (Von Zuben 1997VON ZUBEN, C.J. 1997. Implicações da agregação espacial de parasitas para a dinâmica populacional na interação hospedeiro-parasita. Rev. Saúde Pública 31:523-530. https://doi.org/10.1590/S0034-89101997000600014 (last access on 04/11/2019)
https://doi.org/10.1590/S0034-8910199700... ). Therefore, the uniform dispersion model, predominant in the helminth species of this study, may be due to parasite mortality, a process dependent on the density and mortality of the host induced by the parasite. Additionally, regular or uniform distribution is also observed if there is strict competition between individuals, or if there is positive antagonism, causing a constant minimum distance between individuals (Odum & Barrett 2008ODUM, E.P. & BARRETT, G.W. 2008. Fundamentos de Ecologia. 5ª ed. Cengage Learning, São Paulo.).

Anurans have the supracommunity pattern of diversified generalist helminth parasites with low host specificity and wide distribution (Campião et al. 2014CAMPIÃO, K.M., MORAIS, D.H., DIAS, O.T., AGUIAR, A., TOLEDO, G., TAVARES, L.E.R., & DA SILVA, R.J. 2014. Checklist of helminth parasites of amphibians from south america. Zootaxa 3843:1-93. http://dx.doi.org/10.11646/zootaxa.3843.1.1 (last access on 03/09/2018)
http://dx.doi.org/10.11646/zootaxa.3843.... ). Due to the increase in studies conducted on this topic (e.g., Campião et al. 2016aCAMPIÃO, K.M., DIAS, O.T., SILVA, R.J., FERREIRA, V.L. & TAVARES, L.E.R. 2016a: Living apart and having similar trouble: are frog helminth parasites determined by the host or by the habitat? Can. J. Zool. 94:761-765. https://doi.org/10.1139/cjz-2016-0066 (last access on 02/10/2018)
https://doi.org/10.1139/cjz-2016-0066... , bCAMPIÃO, K.M., SILVA, I.C.O., DALAZEN, G.T., PAIVA, F. & TAVARES, L.E.R. 2016b. Helminth parasites of 11 anuran species from the pantanal wetland, Brazil. Comp. Parasitol. 83:92-100. https://doi.org/10.1654/1525-2647-83.1.92 (last access on 12/11/2019)
https://doi.org/10.1654/1525-2647-83.1.9... , Lins et al. 2017LINS, A.G.S., AGUIAR, A., MORAIS, D.H., DA SILVA, L.A.F., ÁVILA, R.W. & SILVA, R.J. 2017. Helmintofauna de Leptodactylus syphax (Anura: Leptodactylidae) do bioma da Caatinga, nordeste do Brasil. Rev. Bras. Parasitol. Vet. 26:74-80. https://doi.org/10.1590/s1984-29612017013 (last access on 02/09/2019)
https://doi.org/10.1590/s1984-2961201701... , Teles et al. 2017TELES, D.A., BRITO, S.V., ARAÚJO-FILHO, J.A., TEIXEIRA, A.A.M., RIBEIRO, S.C., MESQUITA, D.O. & ALMEIDA, W.O. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetol. notes 10:525-527., Leivas et al. 2018LEIVAS, P.T., LEIVAS, F.W.T. & CAMPIÃO, K.M. 2018. Diet and parasites of the anuran Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest fragment. Herpetol. Notes 11:109-113., Alcantara et al. 2018ALCANTARA, E.P., FERREIRA-SILVA, C., SILVA, L.A.F., LINS, A.G.S., ÁVILA, R.W., MORAIS, D.H. & SILVA, R.J. 2018. Helminths of Dermatonotus muelleri (Anura: Microhylidae) from Northeastern Brazil. J. Parasitol. 104:550-556., Oliveira et al. 2019OLIVEIRA, C.R., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitol. 64:205-212. https://doi.org/10.2478/s11686-018-00022-88 (last access on 22/08/2019)
https://doi.org/10.2478/s11686-018-00022... ), it is quite common to find new records of hosts containing parasites that have not previously been described for the species (e.g., Aguiar et al. 2014AGUIAR, A., MORAIS, D.R., PYLES, P.C. & SILVA, R.J. 2014. Evaluation of helminths associated with 14 amphibian species from a neotropical island near the southeast coast of Brazil. Herpetol. Rev. 2:227-236., Silva et al. 2019SILVA, C.S., ALCANTARA, E.P., SILVA, R.J., ÁVILA, R.W. & MORAIS, D.H. 2019. Helminths parasites of the frog Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 (Anura: Odontophrynidae) in a semiarid region, Brazil. Neotrop. Helminthol. 13:169-179.). In this study, we present new records on species of parasites (O. mazzai and Strongyloides sp.) for the genus Proceratophrys, increasing the total number to 21 helminths. Additionally, all helminth species found represent their first records for Procetatophrys ararype, a frog endemic to the Brejo de Altitude Chapada do Araripe, Northeastern Brazil.

Acknowledgements

We would like to thank Raimundo Marques de Almeida, Paula Danielly Figueiredo Silva, and Teresinha Pereira Machado Roberto for granting access to the collection site; to Editage (www.editage.com) for English language editing.

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for the scholarship granted (Financial Code 001 and 88882.454307/2019-01); the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico - FUNCAP for productivity scholarship (Code BP3-0139-00323.01.00/18 and BP4 00172-00223.01.01/20); the Universidade Federal do Cariri-UFCA for Costing Notice for Research Projects; and the Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq for research grants (RWA, 305988/2018-2; RAB, 155556/2018-5).

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