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HELMINTHS ASSOCIATED WITH 15 SPECIES OF ANURANS FROM THE IBIAPABA PLATEAU, NORTHEASTERN BRAZIL HELMINTOS ASOCIADOS CON 15 ESPECIES DE ANUROS DE LA MESETA DE IBIAPABA, EN EL NORESTE DE BRASIL

La diversidad de los helmintos en los grupos de huéspedes con gran diversidad de especies como los anfibios anuros siguen estando subrepresentados, especialmente en sitios con condiciones ambientales severas como las regiones áridas y semiáridas. Este conocimiento es necesario para comprender el papel de los parásitos en los diferentes niveles de la organización ecológica. Con el fin de evaluar la composición del parásito una taxocenosis de las especies de anuros, describir la riqueza y diversidad de los helmintos a nivel de componentes y de la infracomunidad; además de evaluar la influencia del tamaño del cuerpo en la abundancia y diversidad de los parásitos, se realizó este estudio. Los anuros huéspedes se recogieron en la Zona de Protección Ambiental (EPA) Bica do Ipu en el semiárido brasileño. Los huéspedes recolectados fueron sometidos a eutanasia y a una necropsia en busca de parásitos. En secuencia, se identificaron los helmintos y se realizaron las pruebas estadísticas. Un total de 15 especies de huéspedes compusieron este estudio y se recogieron 1.216 helmintos con abundancia media (MA) de 12,9 ± 3,38 y intensidad media de la infección (MII) de 25,84 ± 6,44. La riqueza media de helmintos fue de 2,3 ± 0,53 (rango = 6), y la diversidad de helmintos (H) fue de 1,36. La comunidad de componentes de helmintos que infectan a los anfibios huéspedes comprende 13 taxones: dos especies de cestodos, un acantocéfalo, un trematodo y nueve nematodos. El presente estudio contribuye al conocimiento de los helmintos que infectan a los anfibios de la Caatinga brasileña, así como a la comprensión de los patrones de diversidad de las infracomunidades parasitarias asociadas a los anfibios.

Amphibian's biology makes it an excellent model for evaluating patterns in the structure of helminth communities (Aho, 1990). They occupy a variety of habitats, have different patterns of life cycle, different reproductive strategies, and occupy various positions in food webs (Koprivnikar et al., 2012). Studies on amphibian parasites have increased in recent years (e.g. Campião et al., 2016a;Oliveira et al., 2019). However, information about the parasites of some amphibian groups is still scarce, and most of restricted to taxonomic descriptions or records of occurrence (Pinhão et al., 2009).
Brazil has the most diverse anuran fauna, with 1,137 species (Segalla et al., 2019). Nevertheless, there are helminth reports for only 185 (7%) species. About 164 helminth species are currently known for Brazilian amphibians, totaling 57% of the taxa described for South America. However, studies describing the ecological aspects of parasites associated with Brazilian amphibian taxocenosis remain underrepresented in the literature (Toledo et al., 2017;da Graça et al., 2017). Data scarcity is even more pronounced in Documenting parasite diversity and host relationships are needed to understand the role of parasites at different levels of ecological organization (Wood & Johnson, 2015). Parasites can affect host immunity and population dynamics, thus having effects on community composition and trophic interactions also acting on population control (Bittencourt & Rocha, 2003;Hudson, 2005). Although play essential roles in ecological processes, parasites remain taxonomically neglected and the actual number of species in different groups cannot yet be determined (Windsor, 1998;Poulin & Morand, 2004).
Helminths were fixed in hot alcohol and preserved in 70% ethyl alcohol. For identification, the nematodes were clarified in lactic acid, and cestodes, trematodes, and acanthocephalans were stained with hydrochloric carmine and cleared with creosote. Thereafter, the helminths were mounted in temporary slides and examined under the light microscope ZEISS Axio Imager M2. Species identification followed Travassos et al. (1969), Vicente et al. (1991), and recent bibliographies. The voucher species were deposited at the Herpetological Collection of Universidade Regional do Cariri.
Parasitological descriptors follow Bush et al. (1997): prevalence, intensity, and abundance of infection were calculated, followed by their respective standard errors. All values are expressed as the mean ± standard error (SE). Parasites' abundance data were tested for normality by the Kolmogorov-Smirnov test. To calculate the wealth and diversity of the community we use the species richness (= total number of helminth species), Shannon index (H′) (Zar, 2010). The Berger-Parker index of dominance (d) was used to determine the most dominant species (Magurran, 2004). Spearman's rank test (rs) was used to assess the relationship between the host body size and parasitological descriptors. Statistical analyses were performed using BioEstat 5.0 (Ayres et al., 2007) and software R platform, version 2.15.0 (RC team, 2017).

Ethic aspects
Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO) for collection permits (ICMBio number 32758-1). To Comitê de Ética em Pesquisa of the Universidade Regional do Cariri, permits 00026/2015. semi-arid regions where amphibians are strongly influenced by unpredictable rainfall. Severe environmental conditions in arid and semiarid regions may limit species diversity by selecting clades tolerant to such conditions while shaping their ecology, natural history, and behavior (Garda et al., 2017).
Therefore, the objectives of this study were: (1) evaluate the parasite composition of 15 anuran species; (2) describe the richness and diversity of helminths at the component and infracommunity levels; (3) to evaluate the influence of body size on the abundance, diversity, and richness in anurans of Caatinga, Brazil.

MATERIAL AND METHODS
The richness found in the present study is similar to other studies dealing with the helminth community associated with anurans Campião et al., 2014;2016a;da Graça et al., 2017;Müller et al., 2018). However, it may be underestimated because of unidentified species, since the occurrence of cryptic species has already been recorded for the region, as in Rhabdiasidae (Müller et al., 2018). Also, larger numbers of nematode species seem to be a general pattern for South American amphibians (Campião et al., 2014).
A c a n t h o c e p h a l a n s o f t h e g e n u s Oligacanthorhynchus are heteroxenous and usually have mammals as final hosts (Gallas & Of the 92 analyzed hosts, 44 (47.8%) were parasitized with at least one helminth species. Only three analyzed host species presented no infection with helminth parasites (C. greening, R. jimi, and S. x-signatus). A total of 1,190 helminths from 13 taxa was recovered from 12 hosts of five anuran families (Table 1), with mean abundance of 12.9 ± 3.38 and mean intensity of infection of 25.84 ± 6.44. Helminth diversity (H`) was 1.36. The mean helminth richness was 2.3 ± 0.53 (max. = 6) species per infected host.
The highest intensity of parasites was found in the rufous frog L. fuscus (n = 446). Pleurodema diplolister and R. granulosa were the hosts exhibiting the highest helminth richness (n = 6). The diversity of the helminths tended to be greatest in P. cicada (H' = 1.15) followed by L. vastus (H'= 1.03) ( Table 2).

RESULTS DISCUSSION
Variation in host specificity may determine the structure of helminth communities (Toledo et al., Silvera, 2012;Richardson et al., 2014). Eventually, some vertebrates can act as paratenic hosts (Yamaguti, 1963;Goldberg & Bursey, 2004), in this case, the parasites can encyst until they reach the proper host (Baker, 2007). In South America, Oligacanthorhynchus sp. was recorded infecting Odontophrynus americanus (Duméril & Bibron, 1841) in Paraguay (Campião et al., 2014). Thus P. d i p l o l i s t e r i s a n e w h o s t r e c o r d f o r Oligacanthorhynchus sp.

ACKNOWLEDGMENTS
Neotropical Helminthology, 2020, 14(2), jul-dic Helminths associated with anurans from Brazil abundance of parasite species. According to Toledo et al. (2017), this fact may be related to the greater surface area available for colonization by parasites, as well as the greater intake and more diversified diet of larger frogs. However, an interesting case was observed for L. vastus, in which the abundance of parasites were negatively correlated with host size, contrasting to the pattern mentioned above (Poulin, 2004;Yoder & Coggins, 2007;Ibrahim, 2008;Hamann et al., 2012Hamann et al., , 2013Campião et al., 2016b;Toledo et al., 2015Toledo et al., , 2017.
The present study contributes to the knowledge of the helminths infecting amphibians from Brazilian Caatinga, as well as the understanding of the diversity patterns of parasitic infracommunities associated with amphibians.
We t h a n k , and Rhabdias sp. may be considered generalists and infected more than one host species. Thus, sympatric hosts, although phylogenetically distant may share some helminth taxa, as they are exposed to similar environmental conditions (Krasnov et al., 2012;Lima et al., 2012;Brito et al., 2014). Schrankiana sp. has been recorded in amphibians from the Hylidae and Leptodactylidae families (Goldberg et al., 2007;Campião et al., 2014;Müller et al., 2018;Oliveira et al., 2019). This is the first record for Bufonidae ®. granulosa).
The high pattern of infection, abundance, and prevalence was evident among individuals of R. granulosa and L. fuscus. In general, members of the Leptodactylidae are associated with terrestrial habitats being frequently found closer to water bodies, which may expose then to both aquatic and terrestrial parasites (Campião et al., 2016a).
Host body size can influence the establishment of parasite communities; usually larger individuals offer larger colonization areas providing adequate resources for parasite development and reproduction (Poulin, 2004;Campião et al., 2016b). Besides, some studies suggest that body size influence on species richness and abundance of parasitic helminths (Yoder & Coggins, 2007;Ibrahim, 2008;Hamann et al., 2012Hamann et al., , 2013Toledo et al., 2015Toledo et al., , 2017. In the present study, the overall size and the size of some amphibian individuals were a determining factor in the richness and