Introduction
Amphibians play an important role in the parasitic networks of ecological communities, as they act as paratenic, intermediate, and definitive hosts for a wide range of parasites within food chains (Koprivnikar et al. Reference Koprivnikar, Forbes and Baker2006). Studies on helminth parasites of amphibians are fundamental for the conservation of this host group, as helminth play a key role in structuring host communities (Poulin Reference Poulin1999, Reference Poulin2001). Furthermore, changes in host–parasite community composition can serve as an important tool for amphibian conservation studies (Draghi et al. Reference Draghi, Drago, Saibene and Agostini2020). Moreover, because of their complex life cycles, helminth are highly susceptible to environmental imbalances and can therefore serve as effective indicators of ecosystem health (Sures Reference Sures2001; Scott Reference Scott2023).
Over the past decade, there has been a considerable increase in studies focusing on the helminth fauna of anurans from the Caatinga (Santos et al. Reference Santos, Torquato, Morais and Cascon2024a). Despite this progress, helminth assemblages are known from only a small portion of the anuran species inhabiting this semiarid domain (Benício et al. Reference Benício, Santos, Freire, Ávila, Silva and Fonseca2022). Brazil harbours approximately 1,251 amphibian species (Drummond et al. Reference Drummond, Santana, Lima and Toledo2026); however, helminth biodiversity in anurans remains markedly underestimated, as the helminth fauna has been documented for fewer than 10% of species (Campião et al. Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014a; Santos et al. Reference Santos, Torquato, Morais and Cascon2024a). Within the Caatinga, around 95 anuran species are currently recognised (Garda et al. Reference Garda, Stein, Machado, Lion, Juncá, Napoli, Silva and Tabarelli2017), but helminth records are available for only 34 of these, representing just 36.7% of the total anuran richness in this biome (Santos et al. Reference Santos, Torquato, Morais and Cascon2024a).
Scinax x-signatus (Spix, 1824) (Anura: Hylidae) is a widely distributed arboreal frog species in South America, occurring in Colombia, Venezuela, Guyana, Suriname, and Brazil (IUCN 2023). In Brazil, it occurs in forested areas of the Atlantic Forest, in the Cerrado, and within the Caatinga domain, and is usually found on vegetation near or above permanent, semi-permanent, and temporary water bodies (Izecksohn and Carvalho e Silva Reference Izecksohn and e Silva SP2001; IUCN 2023). This tree frog is frequently observed in residential and urban areas (Nogueira et al. Reference Nogueira, Bessa-Silva, Affonso and Sampaio2026) and has been classified as Least Concern by the International Union for Conservation of Nature (IUCN 2023). Due to its wide distribution across the Neotropical region, studies on helminth in this species are very recent and remain relatively scarce, being limited to only six publications from Brazil (Martins-Sobrinho et al. Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017; Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022; Sampaio et al. Reference Sampaio, Teixeira, Nascimento, Ribeiro, Almeida and Brito2022, Santos et al. Reference Santos, Teixeira, Nascimento and Brito2024b; Uchôa et al. Reference Uchôa, Oliveira, Andrade and Borges-Nojosa2025, Pitombeira et al. Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026), of which only three was conducted with hosts originating from the Caatinga domain (Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022, Sampaio et al. Reference Sampaio, Teixeira, Nascimento, Ribeiro, Almeida and Brito2022, Pitombeira et al. Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026).
Although South America harbours the greatest richness of Scinax Wagler, 1830 species, with a total of 76 species (Frost Reference Frost2026), knowledge of helminth biodiversity in these hosts remains limited, with records for only 13 species across 5 countries (Aguiar et al. Reference Aguiar, Morais, Cicchi and Silva2014; Reference Aguiar, Morais, Silva, Anjos, Foster and Silva2021; Campião et al. Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014a; Martins-Sobrinho et al. Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017; Chero et al. Reference Chero, Cruces, Cacique, Ponce, Iannacone, Alvariño, Sanchez, Sáez, Lopez and Silva2023). This highlights the need for further studies to improve our understanding of the parasitic biodiversity of Scinax in South America, as well as that of anurans in the region.
The present study aimed to record the helminth assemblage associated with the hylid frog Scinax x-signatus from a Caatinga area in the municipality of Petrolina, Pernambuco State, Brazil, and provides an updated overview of helminthological research and the biodiversity of these parasites in South American Scinax species.
Materials and methods
Study of the helminth community of Scinax x- signatus from the Caatinga
The present study was carried out with specimens of Scinax x-signatus collected in Caatinga remnants within the Campus de Ciências Agrárias (CCA) of the Universidade Federal do Vale do São Francisco (UNIVASF) (9°19′30.41″S; 40°33′0.20″W), in the municipality of Petrolina, Pernambuco State, Brazil. The Caatinga stricto sensu of the CCA, located in the ecoregion of the Depressão Sertaneja Meridional (adjacent to the São Francisco Dunes), is characterised by open vegetation, including xerophytic plants and deciduous and semi-deciduous species, with shorter trees up to 8 metres in height, forming a wooded steppe savanna, with patches of Deciduous Forest (Velloso et al. Reference Velloso, Sampaio and Pareyn2002).
Host specimens were collected through active nocturnal searches conducted in July 2019 (one specimen) and from 2022 to 2025 (13 specimens in 2022, six in 2023, two in 2024, and three in 2025). Live individuals, once captured, were immediately taken to the Laboratório de Fisiologia Animal of the UNIVASF for necropsy.
Hosts were euthanised with an overdose of benzocaine administered topically, according to the recommendations of the CONCEA (2018), and necropsied under a stereomicroscope. All hosts were measured for their snout-vent length (SVL, in mm) using a digital calliper, their body mass (g) was weighed on an analytical balance, and their gonads were examined to determine maturity level and sex. The host specimens were identified according to Araujo-Vieira et al. (Reference Araujo-Vieira, Pombal, Caramaschi, Novaes-e-Fagundes, Orrico and Faivovich2020), and voucher specimens were deposited in the Coleção Herpetológica do Museu de Fauna da Caatinga (MFCH – CEMAFAUNA Caatinga), of the UNIVASF, Petrolina, Pernambuco, Brazil.
The collections and laboratory procedures were carried out in accordance with Ethics Committee for the Use of Animals (CEUA) – UNIVASF (Nos. 0005/29051, 0002/230621 and 0005/271023), Ministério do Meio Ambiente – ICMBio/SISBIO, Brazil (Nos 78052-1, 91121-1 and 68412-1), and Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado (SisGen) (Nos. A91D344 and AF80603).
Immediately after host euthanasia, necropsies were performed, and helminth were collected while still alive. Live helminth were fixed in heated 4% formalin, kept in this fixative at room temperature for 15 days, and subsequently preserved in 70% ethanol (Felix-Nascimento et al. Reference Felix-Nascimento, Vieira, Muniz-Pereira, Moura, Ribeiro and Oliveira2020). For taxonomic identification under a light microscope, nematodes were cleared in Amann’s lactophenol on temporary slides, whereas digenean adults and metacercariae, as well as acanthocephalan cystacanths, were stained with Mayer’s carmalum or Delafield’s haematoxylin and mounted on permanent slides using Canada balsam (Amato and Amato Reference Amato, Amato, Von Matter, Straube, V de Q, Accordi and Cândido2010).
Oxyascaris Travassos, 1920 (Nematoda: Cosmocercidae) species were identified according to Anderson et al. (Reference Anderson, Chabaud and Willmott2009), Baker and Vaucher (Reference Baker and Vaucher1985), Felix-Nascimento et al. (Reference Felix-Nascimento, Vieira, Muniz-Pereira, Moura, Ribeiro and Oliveira2020), and Santos et al. (Reference Santos, Willkens, Silva, Melo and Fernandes2023, Reference Santos, Trindade, Melo and González2026). Female specimens of Oxysomatium sp. (Nematoda: Cosmocercidae) were identified based on Anderson et al. (Reference Anderson, Chabaud and Willmott2009) and Felix-Nascimento et al. (Reference Felix-Nascimento, Vieira, Muniz-Pereira, Moura, Ribeiro and Oliveira2020), whereas specimens of Oswaldocruzia sp. (Nematoda: Molineidae) were identified according to Anderson et al. (Reference Anderson, Chabaud and Willmott2009). Digeneans were identified to the genus level following Jones et al. (Reference Jones, Bray and Gibson2005), and metacercariae were identified according to Hamann and González (Reference Hamann and González2009), with the systematic updates proposed by Achatz and Tkach (Reference Achatz and and Tkach2025). Acanthocephalan cystacanths were identified according to Oliveira et al. (Reference Oliveira, Mascarenhas and Müller2024). The ecological parameters of the helminth populations were calculated according to Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997).
Systematic literature search and review
We conducted a literature review to investigate previous records of helminth parasites in South American Scinax species using the databases Web of Science, ScienceDirect, Scopus, Scientific Electronic Library Online (SciELO), Google Scholar, and MEDLINE (PubMed). The following search terms were used in these combinations: ‘Scinax and Nematoda’; ‘Scinax and Trematoda’; ‘Scinax and Cestoda’; ‘Scinax and Acanthocephala’; ‘Scinax and helminth’; ‘Scinax, Neotropical and each helminth group’; ‘Scinax, South America and each helminth group’; ‘Scinax, each helminth group and each South American country’ (Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Peru, Suriname, Uruguay and Venezuela); and ‘Scinax, each helminth group and each South American biome’ (Amazonia, Atlantic Forest, Caatinga, Cerrado, Chaco, Pampa and Pantanal).
The literature search was conducted between September 2025 and May 2026. A total of 45 studies met the inclusion criteria described below and were included in the present review. Only articles published in peer-reviewed scientific journals were included in this review. Conference abstracts, theses, and dissertations were excluded because they may not have undergone rigorous peer review, are often of limited regional dissemination, and are frequently difficult to access. Studies retrieved from more than one database were considered only once to avoid duplication.
Helminth records for Scinax species were assigned to their respective biomes based on the geographical coordinates provided in the original publications. When geographical coordinates were unavailable, localities were georeferenced using the municipality, state, or province names through the Geocoding tool available on the SpeciesLink (2025) website. Biomes were assigned according to the classification proposed by Antonelli et al. (Reference Antonelli, Zizka, Carvalho, Scharn, Bacon, Silvestro and Condamine2018), based on the geographical coordinates of each record. The total number of Scinax species occurring in each South American country was obtained from Frost (Reference Frost2026).
Spatial data on helminth-parasitised Scinax species in South America were mapped using ArcGIS® version 11.5. Geographic coordinates were plotted in the WGS 84 coordinate system, and distribution maps were produced using base layers obtained from publicly available geographic datasets. Final maps were generated following standard cartographic conventions and exported at high resolution for publication. Graphics and tables were produced using Microsoft Excel®.
Results
Helminth community composition of Scinax x-signatus in the Caatinga of Petrolina, Pernambuco State, Brazil
A total of 25 specimens of Scinax x-signatus were analysed, comprising 11 adult females (SVL = 29.6–41.8 mm, body mass = 1.7–4.2 g), nine adult males (SVL = 30.9–34.6 mm, body mass = 1.7–2.8 g), and five juveniles (SVL = 23.9–27.5 mm, body mass = 0.6–1.4 g). Of these, 13 individuals were parasitised by at least 1 helminth species (Table 1), corresponding to an overall prevalence of 52%.
Helminth parasites of Scinax x-signatus from the Caatinga domain in the Vale do São Francisco region, Pernambuco State, Brazil, including ecological descriptors of parasite populations
Table 1. Long description
The table consists of seven columns: Helminth species, Site of infection, Total intensity, Prevalence, Mean intensity, Mean abundance, and Range.
Under the Nematoda group:
* Oswaldocruzia species (adult) (C H I O C X X X): Small intestine, Total intensity 3, Prevalence 8 percent, Mean intensity 1.5 plus or minus 0.71, Mean abundance 0.12 plus or minus 0.44, Range 0 to 2.
* Oxyascaris caudacutus (adults) (C H I O C X X X): Small intestine, Total intensity 20, Prevalence 20 percent, Mean intensity 4.0 plus or minus 2.77, Mean abundance 0.64 plus or minus 1.73, Range 0 to 8.
* Oxysomatium species (adult) (C H I O C X X X): Large intestine, Total intensity 2, Prevalence 4 percent, Mean intensity 2, Mean abundance 0.08 plus or minus 0.40, Range 2.
* Rhabdias species (adults) (C H I O C X X X): Lung, Total intensity 1, Prevalence 4 percent, Mean intensity 1, Mean abundance 0.04 plus or minus 0.20, Range 1.
Under the Digenea group:
* Lophosicyadiplostomum species (metacercariae) (C H I O C X X X): Mesentery, Total intensity 4, Prevalence 8 percent, Mean intensity 2.0 plus or minus 0.71, Mean abundance 0.12 plus or minus 0.34, Range 0 to 2.
* Catadiscus species (adults) (C H I O C X X X): Large intestine, Total intensity 3, Prevalence 4 percent, Mean intensity 3, Mean abundance 0.12 plus or minus 0.6, Range 3.
Under the Acanthocephala group:
* Centrorhynchus species (cystacanths) (C H I O C X X X): Mesentery, Total intensity 9, Prevalence 16 percent, Mean intensity 2.25 plus or minus 1.5, Mean abundance 0.36 plus or minus 0.99, Range 0 to 4.
a Indicate one host parasitised by this helminth species.
Infracommunity species richness varied from one to seven helminth species per host, comprising four adult nematodes: adults of Oswaldocruzia sp., Oxyascaris caudacutus (Freitas, Reference Freitas1958), Oxysomatium sp., and Rhabdias sp. (Rhabdiasidae); two digeneans: adults of Catadiscus sp. (Diplodiscidae) and metacercariae of Neodiplostomum sp. (Diplostomidae (= Lophosicyadiplostomum sp.); and one acanthocephalan: cystacanths of Centrorhynchus sp. (Centrorhynchidae) (Table 1). Specimens of Oxysomatium sp. could not be identified to species level because no males were recovered from their infrapopulations. Specimens of Oswaldocruzia were identified only to genus level because a single male specimen was available, precluding a reliable species-level identification. The single specimen of Rhabdias sp. had been fixed in 4% formalin, precluding molecular analysis and, consequently, species-level identification. Specimens of Catadiscus sp. were not identified to species owing to the large number of eggs within the uterus, which obscured the internal diagnostic structures.
Oxyascaris caudacutus was the most prevalent species, infecting 20% of the analysed hosts (Table 1), and also the helminth species with the highest mean intensity (4.0 ± 2.77) and mean abundance (0.64 ± 1.73) (Table 1). Three helminth taxa were observed in only one host specimen each (Oxysomatium sp., Rhabdias sp., and Catadiscus sp.) (Table 1).
An updated checklist of helminth taxa in South American Scinax species
Our literature survey showed that the first published record of helminth infecting South American Scinax dates back to the 1940s (Travassos, Reference Travassos1940), approximately 86 years ago (Table 2). Of these, 39 are original studies (Table 2), and 6 are compilations or checklists that synthesise data from previous studies (Table 2) (Argentina – González and Hamann Reference González and Hamann2015; Brazil – Vicente et al. Reference Vicente, Rodrigues, Gomes and Pinto1990; Campião et al. Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014a; Fernandes and Kohn Reference Fernandes and Kohn2014; Santos et al. Reference Santos, Torquato, Morais and Cascon2024a; Peru – Chero et al. Reference Chero, Cruces, Cacique, Ponce, Iannacone, Alvariño, Sanchez, Sáez, Lopez and Silva2023). These studies are restricted to helminth records from Scinax species in Argentina (11 manuscripts), Brazil (29 manuscripts), Ecuador (1 manuscript), Paraguay (2 manuscripts), and Peru (2 manuscripts) (Table 2; Figure 1).
Helminth–host associations in South American Scinax species
Table 2. Long description
The table is organized into six columns: Helminth taxa, Host species, State or province, Domain, Country, and Reference. It is divided into three major taxonomic sections.
1. Acanthocephala: Includes taxa such as Acanthocephalus caspanensis and Centrorhynchus species. Hosts include S. pedromedinae, S. acuminatus, and S. x-signatus. Locations span Amazonia, Chaco, and the Atlantic Forest in Peru, Paraguay, and Brazil.
2. Nematoda: This is the largest section, featuring taxa like Aplectana lopesi, Cosmocerca brasiliense, and Rhabdias species. Hosts include S. fuscovarius, S. nasicus, and S. ruber. Geographies include the Pantanal, Caatinga, and Cerrado domains across Brazil, Argentina, and Ecuador. Notable entries include new host records for Oswaldocruzia sp. and Oxyascaris caudacutus in S. x-signatus.
3. Platyhelminthes: Subdivided into Eucestoda (e.g., Cylindrotaenia americana) and Trematoda (e.g., Catadiscus inopinatus and Neodiplostomum species). Hosts include S. pedromedinae and S. nasicus, primarily located in Amazonia, Chaco, and the Pantanal across Peru, Argentina, and Brazil.
References cited include Bursey et al 2001, Campião et al 2014a, and several mentions of the current study for new host records.
Richness of South American Scinax species parasitised and not parasitised by helminth by country.
Figure 1. Long description
The y-axis is labeled Number of South American Scinax s p p. and ranges from 0 to 65 in increments of 5. The x-axis lists 13 countries from left to right. A legend at the bottom indicates that dark blue represents Scinax s p p. without helminth reports and orange represents Scinax s p p. with helminth reports.
Data by country:
* Argentina: 6 without, 2 with, total 8.
* Bolivia: 13 without, 0 with.
* Brazil: 48 without, 12 with, total 60.
* Chile: 0 for both.
* Colombia: 20 without, 0 with.
* Ecuador: 5 without, 1 with, total 6.
* French Guyana: 7 without, 0 with.
* Guyana: 7 without, 0 with.
* Paraguay: 7 without, 3 with, total 10.
* Peru: 7 without, 6 with, total 13.
* Suriname: 9 without, 0 with.
* Uruguay: 4 without, 0 with.
* Venezuela: 13 without, 0 with.
Brazil shows the highest total richness and the highest number of parasitised species. Chile is the only country with no species recorded in this dataset.
Integrating data from the present investigation with previous records, this study documents 78 helminth taxa belonging to four major groups (8 Acanthocephala, 45 Nematoda, 4 Cestoda, and 20 Trematoda), occurring across 13 South American Scinax species (Tables 2 and 3; Figures 2 and 3).
Richness of helminth taxa in South American Scinax species with records of parasitism.
Figure 2. Long description
The chart features a vertical axis listing thirteen species of the genus Scinax and a horizontal axis measuring Helminth richness from 0 to 40. The data is presented in stacked bars with four color-coded categories: Acanthocephala (dark blue), Trematoda (orange), Cestoda (green), and Nematoda (light blue).
* S dot nasicus: Total richness of 34, dominated by Trematoda and Nematoda.
* S dot fuscovarius: Total richness of 28, primarily Nematoda.
* S dot x-signatus: Total richness of 27, primarily Nematoda and Acanthocephala.
* S dot acuminatus: Total richness of 11, almost entirely Nematoda.
* S dot ruber: Total richness of 6, entirely Nematoda.
* S dot fuscomarginatus: Total richness of 6, split between Acanthocephala and Nematoda.
* S dot pedromedinae: Total richness of 4, containing all four taxa.
* S dot auratus: Total richness of 3, split between Acanthocephala and Nematoda.
* S dot ictericus: Total richness of 3, entirely Nematoda.
* S dot nebulosus: Total richness of 2, split between Acanthocephala and Nematoda.
* S dot garbei: Total richness of 2, entirely Nematoda.
* S dot hayii: Total richness of 2, entirely Nematoda.
* S dot similis: Total richness of 2, entirely Nematoda.
Nematoda is the most frequent taxon across all species, while Cestoda is the least frequent, appearing only in S dot nasicus, S dot fuscovarius, and S dot pedromedinae.
Distribution map of Scinax species parasitised by helminth across South American morphoclimatic domains.
Figure 3. Long description
A map of South America with a coordinate grid and a North arrow in the top right. The map is color-coded into six morphoclimatic domains. Amazonia in green covers the North and Northwest. Caatinga in yellow is in the Northeast. Cerrado in light orange occupies the center. The Atlantic Forest in light green runs along the East coast. The Chaco in tan and Pantanal in pink are in the center-west. Pampas in light brown is in the South.
Host species are marked with colored symbols. In the North and Northeast, red stars representing Scinax x-signatus are concentrated in the Caatinga and Atlantic Forest. Blue squares for Scinax nebulosus and orange squares for Scinax ruber are found in the Northern Amazonia and Western regions. In the central regions, black circles for Scinax fuscomarginatus and green circles for Scinax fuscovarius are scattered across the Cerrado and Pantanal. Yellow circles for Scinax nasicus and blue circles for Scinax acuminatus are primarily located in the Chaco and Pantanal regions. Other species like Scinax garbei, ictericus, similis, hayii, auratus, and pedromedinae appear as isolated points in their respective habitats. A scale bar at the bottom right indicates 0 to 1,500 kilometers.
Brazil accounts for the highest number of Scinax species parasitised by helminth, comprising 13 host species and a total richness of 55 helminth taxa (6 Acanthocephala, 41 Nematoda, 2 Cestoda, and 6 Trematoda), and also has the greatest number of published studies on helminth of this anuran genus (Table 2, Figure 1). Peru follows, with seven host species associated with seven helminth taxa (one Acanthocephala, four Nematoda, one Cestoda, and one Trematoda), while Argentina, despite having only two host species, totals 23 helminth taxa (1 Acanthocephala, 8 Nematoda, one Cestoda, and 14 Trematoda) (Table 2; Figure 1). Paraguay has two host species parasitised by four helminth taxa (two Acanthocephala and two Nematoda), whereas Ecuador has one host species associated with a single nematode taxon (Table 2; Figure 1). Scinax species occurring in other South American countries have not yet been reported as hosts of helminth (Figure 1).
Across South American morphoclimatic domains, the highest number of Scinax species with helminth records occurs in Amazonian areas of Brazil, Peru, and Ecuador, totalling seven parasitised species (Table 2, Figure 3). This is followed by the Atlantic Forest in Brazil and Paraguay, with five parasitised host species (Table 2, Figure 3). In a transition zone between the Atlantic Forest and the Cerrado in Brazil, two identified species and three unidentified taxa (S. cf. nasicus, S. cf. similis, and S. cf. ruber) have been recorded (Table 2; Figure 3). In addition, three Scinax species have been reported from the Brazilian Pantanal and from a transition zone between the Caatinga and the Cerrado, whereas two parasitised species have been recorded in the Brazilian Caatinga and in the Argentine Chaco. A single Scinax species has been recorded from the Brazilian Cerrado (Table 2, Figure 3).
Helminth-host List
Host-helminth list
Host-helminth associations in South American Scinax species
Table 3. Long description
The table lists host species in the first column and their associated helminth taxa in the subsequent four columns.
* Scinax acuminatus: Associated with Acanthocephala (Acanthocephalus caspanensis) and several Nematoda including Aplectana sp., Brevimulticaecum sp. larvae, Cosmocerca parva, Kathlaniidae gen. sp. larvae, Oxyascaris pilagorum, Oxyascaris caudacutus, Physaloptera sp. larvae, Rhabdias breviensis, Rhabdias cf. breviensis, and Rhabdochonidae gen. sp. larvae.
* Scinax auratus: Associated with Acanthocephala (Centrorhynchus sp. cystacanth) and Nematoda (Cosmocerca parva and Cosmocerca sp.).
* Scinax fuscomarginatus: Associated with Acanthocephala (Centrorhynchidae gen. sp. and Centrorhynchus sp. cystacanths) and Nematoda (Acuariidae gen. sp. larvae, Cosmocerca podicipinus, Cosmocercidae gen. sp., and Ochoterenella convoluta).
* Scinax fuscovarius: Shows high diversity across all four taxa. Acanthocephala include Centrorhynchidae gen. sp. and Pseudoacanthocephalus sp. Nematoda include Aplectana lopesi, Aplectana membranosa, Aplectana sp., Ascarididae gen sp. larvae, Cosmocerca brasiliense, Cosmocerca freitasi, Cosmocerca parva, Cosmocerca sp., Cosmocercidae gen. sp., Cosmocercoidea fam. gen. sp., Oxyascaris caudacutus, Philometridae gen. sp., Physaloptera sp. larvae, Raillietnema sp., Rhabdias breviensis, Rhabdias sp., Rhabdias cf. breviensis, Rhabdias cf. elegans, Rhabdias cf. fuelleborni, Schrankiana formulosa, Spiroxys sp. larvae, and Spirurida fam. gen. sp. larvae. Eucestoda include Proteocephalidae gen. sp. cyst and Spirometra sp. spargana. Trematoda include Mesocoelium monas and Neascus sp. metacercariae.
* Scinax garbei: Associated with Nematoda (Cosmocerca brasiliense and Cosmocerca parva).
* Scinax hayii: Associated with Nematoda (Physaloptera sp. larvae and Rhabdias sp.).
* Scinax ictericus: Associated with Nematoda (Cosmocerca brasiliense, Cosmocerca parva, and Physaloptera sp. larvae).
* Scinax nasicus: Associated with all four taxa. Acanthocephala include Centrorhynchidae gen. sp. and Centrorhynchus sp. cystacanths. Nematoda include Ascarididae gen sp. larvae, Brevimulticaecum sp. larvae, Cosmocerca parva, Cosmocerca podicipinus, Cosmocerca sp., Cosmocercidae gen. sp., Cosmocercoidea fam. gen. sp., Gyrinicola chabaudi, Oxyascaris caudacutus, Oxyascaris sp., Physaloptera sp. larvae, Physalopteroides venancioi, Physocephalus sp. larvae, Rhabdochonidae gen. sp. larvae, and Strongyloides pereirai. Eucestoda include Cylindrotaenia sp. Trematoda include Apharingostrigea sp., Bursotrema tetracotyloides, Catadiscus inopinatus, Diplostomoidea fam. gen. sp., Diplostomulum sp., Echinostomatidae gen. sp., Glypthelmins sp., Gorgoderina rochalimai, Lophosyciadiplostomum aff. nephrocystis, Mesocoelium monas, Nephrostomum sp., Opisthogonimus sp., Plagiorchiidae gen. sp., Strigeidae gen. sp., Styphlodora sp., and Travtrema aff. stenocotyle.
* Scinax nebulosus: Associated with Acanthocephala (Centrorhynchus sp. cystacanth) and Nematoda (Ochoterenella convoluta).
* Scinax pedromedinae: Associated with all four taxa including Acanthocephala gen. sp. cystacanth, Nematoda (Cosmocerca brasiliense), Eucestoda (Cylindrotaenia americana), and Trematoda (Glypthelmins parva).
* S. similis: Associated with Nematoda (Cosmocercidae gen. sp. and Oxyascaris caudacutus).
* Scinax ruber: Associated with Nematoda (Aplectana membranosa, Cosmocerca brasiliense, Cosmocercidae gen. sp., Physaloptera sp. larvae, Physalopteroides venancioi, and Rhabdias cf. pseudosphaerocephala).
* Scinax x-signatus: Associated with Acanthocephala (Centrorhynchidae gen. sp., Centrorhynchus sp., Oligacanthorhynchus sp., and Oncicola sp.), Nematoda (Aplectana membranosa, Brevimulticaecum sp., Cosmocerca parva, Cosmocerca podicipinus, Cosmocerca sp., Cosmocercidae gen. sp., Cosmocercoides sp., Ochoterenella convoluta, Ochoterenella sp., Oswaldocruzia sp., Oxyascaris caudacutus, Oxyascaris oxyascaris, Oxysomatium sp., Physaloptera sp., Rhabdias breviensis, Rhabdias fuelleborni, Rhabdias sp., Schrankiana sp., Spiroxys sp., and Strongyloides sp.), and Trematoda (Catadiscus sp. and Lophosicyadiplostomum sp.). New host records are noted for Catadiscus sp., Oswaldocruzia sp., Oxyascaris caudacutus, and Oxysomatium sp.
Discussion
Helminth richness in populations of Scinax x-signatus in Brazil
The component helminth community of S. x-signatus examined in this study was partly composed of taxa previously recorded in this host, including the nematode Rhabdias sp. in the Atlantic Forest (Martins-Sobrinho et al. Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017) and Caatinga (Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022; Santos et al. Reference Santos, Torquato, Morais and Cascon2024a; Pitombeira et al. Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026), metacercariae of the trematode Neodiplostomum sp. previously reported from Caatinga populations (Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022; Santos et al. Reference Santos, Torquato, Morais and Cascon2024a; Pitombeira et al. Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026), and cystacanths of the acanthocephalan Centrorhynchus sp., recorded in this host in the Caatinga (Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022; Santos et al. Reference Santos, Torquato, Morais and Cascon2024a), Cerrado (Santos et al. Reference Santos, Teixeira, Nascimento and Brito2024b), and Atlantic Forest (Martins-Sobrinho et al. Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017). However, most helminth records in the present study correspond to taxa not previously associated with this host, including Oswaldocruzia sp., Oxyascaris caudacutus, Oxysomatium sp., and Catadiscus sp., thus representing new host records.
The helminth richness observed in S. x-signatus in the present study was lower than that reported by Oliveira et al. (Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022) (richness = 12; hosts examined = 23), who studied this host species in Maranguape Mountain, an Atlantic Forest area in Ceará State, and by Pitombeira et al. (Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026) (richness = 11; hosts examined = 57), who investigated helminth parasitising several anuran species from different Caatinga areas in Ceará State. However, the richness recorded here was higher than that reported by Martins-Sobrinho et al. (Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017) (richness = 3; hosts examined = 11) for this host from an Atlantic Forest area in Pernambuco State, by Santos et al. (Reference Santos, Teixeira, Nascimento and Brito2024b) from a Cerrado area in Maranhão State (richness = 3; hosts examined = 31), and by Uchôa et al. (Reference Uchôa, Oliveira, Andrade and Borges-Nojosa2025), who studied this host in a transition zone between the Caatinga and Cerrado in Piauí State (richness = 2; hosts examined = 6) (Table 4).
Helminth parasites of Scinax x-signatus from Brazil and respective collection localities
Table 4. Long description
The table is organized into three columns: Helminth species; Locality, State (Biome); and Reference. It is divided into three taxonomic sections.
1. Acanthocephala section:
* Centrorhynchus species (cystacanths) found in Maranguape mountain, Ceara (Caatinga); Estacao Ecologica do Tapacura, Pernambuco (Atlantic Forest); Petrolina, Pernambuco (Caatinga); and Itamacaoca Protection Reserve, Maranhao (Cerrado).
* Oligacanthorhynchus species (cystacanths) in Maranguape mountain, Ceara (Caatinga).
* Centrorhynchidae gen. sp. (cystacanths) in Aiuaba, Barro, and Farias Brito, Ceara (Caatinga).
* Oncicola species and unidentified Acanthocephala in Itamacaoca Protection Reserve, Maranhao (Cerrado).
2. Nematoda section:
* Aplectana membranosa in Maranguape mountain and Granjeiro, Ceara (Caatinga).
* Brevimulticaecum species (larvae) in Estacao Ecologica do Tapacura, Pernambuco (Atlantic Forest) and Barro and Santana do Cariri, Ceara (Caatinga).
* Cosmocerca parva and Cosmocerca rara in Maranguape mountain, Ceara (Caatinga).
* Cosmocerca species in Granjeiro, Ceara (Caatinga).
* Cosmocercidae gen. sp. in Barro, Ceara (Caatinga) and Sete Cidades National Park (Caatinga/Cerrado).
* Ochoterenella species in Barra, Piaui (Caatinga/Cerrado).
* Oswaldocruzia species, Oxyascaris caudacutus, and Oxysomatium species in Petrolina, Pernambuco (Caatinga), noted as new host records in the current study.
* Physaloptera species (larvae) in Maranguape mountain, Granjeiro, and Crato, Ceara (Caatinga).
* Rhabdias breviensis and Rhabdias fuelleborni in Ceara (Caatinga).
* Rhabdias species in Pernambuco (Atlantic Forest and Caatinga) and Ceara (Caatinga).
* Schrankiana species, Spiroxys species (larvae), and Strongyloides species in various Ceara (Caatinga) localities.
3. Digenea section:
* Catadiscus species in Petrolina, Pernambuco (Caatinga), noted as a new host record.
* Lophosicyadiplostomum species (metacercariae) in Maranguape mountain (Ceara), Petrolina (Pernambuco), and Barro and Crato (Ceara), all within the Caatinga biome.
Our results are more similar to those reported by Sampaio et al. (Reference Sampaio, Teixeira, Nascimento, Ribeiro, Almeida and Brito2022) (richness = 5; hosts examined = 33) for anurans from a Caatinga area in Ceará State. This variation in parasite richness among S. x-signatus populations from different localities may be related to differences in sample size, as evidenced by the heterogeneity in sampling effort across studies on this host, as well as to methodological approaches (Poulin & Morand Reference Poulin and Morand2004, Campião et al. Reference Campião, Ribas and Tavares2015). However, as widely recognised, these differences may reflect variation in environmental and ecological conditions (Campião et al. Reference Campião, Silva and Ferreira2014b; Neely et al. Reference Neely, Souza, Martins, Marshall, Buttimer, Assis, Medina, Whetstone, Lyra, Ribeiro, Greenspan, Haddad, Anjos and Becker2024), as distinct environments can harbour different intermediate hosts, as well as differences in diet composition (Leung & Koprivnikar Reference Leung and Koprivnikar2019) and other factors known to influence parasite richness, including host trophic position (Chen et al. Reference Chen, Liu, Davis, Jordán, Hwang and Shao2008), host body size (Poulin Reference Poulin1997; Campião et al. Reference Campião, Ribas and Tavares2015), host geographical range (Campião et al. Reference Campião, Ribas and Tavares2015), and local host diversity, given that parasite diversity may reflect the diversity of host communities (Poulin Reference Poulin2014).
Current knowledge of helminth infecting Scinax x-signatus is limited to seven original studies, including the present one (Table 4; Figure 4), and two compilations (Santos et al. Reference Santos, Torquato, Morais and Cascon2024a; Félix et al. Reference Félix, Neves, Rebêlo, Cardoso, Oliveira, Silva, Benício, Freire and Melo2026), reporting a total of 27 helminth taxa (5 Acanthocephala, 20 Nematoda, and 2 Trematoda) (Table 4) (Martins-Sobrinho et al. Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017; Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022; Sampaio et al. Reference Sampaio, Teixeira, Nascimento, Ribeiro, Almeida and Brito2022; Santos et al. Reference Santos, Teixeira, Nascimento and Brito2024b; Uchôa et al. Reference Uchôa, Oliveira, Andrade and Borges-Nojosa2025; Pitombeira et al. Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026). Most records originate from hosts collected in the Caatinga of Brazil (Table 4; Figure 4). Given that S. x-signatus is widely distributed across Colombia, Venezuela, Guyana, Suriname, French Guiana, and the northern, north-eastern, and south-eastern regions of Brazil (Araujo-Vieira et al. Reference Araujo-Vieira, Lourenço, Lacerda, Lyra, Blotto, Ron, Baldo, Pereyra, Suárez-Mayorga, Baêta, Ferreira, Barrio-Amorós, Borteiro, Brandão, Brasileiro, Donnelly, Dubeux, Köhler, Kolenc, Leite, Maciel, Nunes, Orrico, Peloso, Pezzuti, Reichle, Rojas-Runjaic, da Silva, Sturaro, Langone, Garcia, Rodrigues, Frost, Wheeler, Grant, Pombal, Haddad and Faivovich2023), the currently available data almost certainly underestimate the richness and geographical distribution of its helminth fauna.
Distribution map of helminth records in Scinax x-signatus across morphoclimatic domains in Brazil.
Figure 4. Long description
A geographical map of Northeastern Brazil with a coordinate grid and a scale bar of 0 to 200 kilometers. An inset map at the top right shows the entire country of Brazil with a red shaded box over the Northeastern region. The main map is divided into four colored morphoclimatic domains. Amazônia is green in the Northwest. Cerrado is pink in the West. Caatinga is yellow covering the central and largest portion. Mata Atlântica is teal along the Eastern coast.
Data points are distributed as follows. In the North within the Cerrado is a black hexagon for Santos et al. 2024b. Near the border of Cerrado and Caatinga is a green rectangle for Uchôa et al. 2025. In the Northern Caatinga is a light blue square for Oliveira et al. 2022. In the central Caatinga, a cluster of four purple triangles represents Pitombeira et al. 2026, surrounding a single black diamond for Sampaio et al. 2022. On the Eastern coast in the Mata Atlântica is a yellow circle for Martins-Sobrinho et al. 2017. In the Southern Caatinga is a red star representing the Current study. State abbreviations include P A, M A, C E, R N, P B, P E, A L, S E, B A, T O, G O, M G, and P I.
In this host, most acanthocephalan records correspond to the cystacanth stage, whereas all Physaloptera records correspond to larval stages (Table 4), a pattern consistent with a potential role of Scinax species as paratenic hosts in the life cycles of these parasites. The occurrence of trematode metacercariae suggests that S. x-signatus also functions as a potential intermediate or paratenic host (Oliveira et al. Reference Oliveira, Mascarenhas, Batista-Oliveira, Castro Araújo, Ávila and Borges-Nojosa2022; Sampaio et al. Reference Sampaio, Teixeira, Nascimento, Ribeiro, Almeida and Brito2022; Pitombeira et al. Reference Pitombeira, Silva, Aguiar, Yamada, Ávila, Silva and Morais2026). This pattern, whereby Scinax x-signatus acts as a potential intermediate and paratenic host for helminth, has also been reported for several other South American anuran species (Campião et al. Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014a; Chero et al. Reference Chero, Cruces, Cacique, Ponce, Iannacone, Alvariño, Sanchez, Sáez, Lopez and Silva2023), reflecting the intermediate trophic position typically occupied by these vertebrates within their ecosystems (Camacho and Araujo Reference Camacho and Araujo2025).
An overview of helminth parasitism in South American Scinax
The genus Scinax currently comprises approximately 79 species, with a distribution extending from Mexico to South America (Frost Reference Frost2026). Despite the broad geographic range of the genus, being represented in all South American countries except Chile, knowledge of its helminth fauna remains markedly limited. Of the 76 species occurring naturally on the continent (see Frost Reference Frost2026), only 17.1% (13 species) have documented records of helminth parasitism (Table 2, Figure 1). This conspicuous gap highlights the incipient state of parasitological knowledge within the genus.
Brazil harbours the highest richness of Scinax species in South America (60 species) (Drummond et al. Reference Drummond, Santana, Lima and Toledo2026) and, correspondingly, the greatest number of South American species reported as parasitised by helminth (13 species) (Table 2; Figures 1 and 3). However, this absolute richness does not translate into a higher proportion of parasitised species. Indeed, only 21.7% of Brazilian Scinax species have documented helminth records, a proportion lower than that observed in Peru (46.1%; six species), Paraguay (42.8%; three species), and Argentina (25%; two species), but higher than in Ecuador (16.6%; one species) (Table 2; Figure 1). These differences are unlikely to reflect true biological patterns, but rather disparities in Scinax species diversity among countries, variation in the diversity of morphoclimatic domains within each country, as well as differences in sampling effort and research intensity.
The relatively low proportion of parasitised Scinax species in Brazil (Table 2; Figure 1) likely reflects its large territorial extent and environmental heterogeneity, which hinder comprehensive sampling and leave many areas underexplored. This limitation extends across South America, where helminth of Scinax have been recorded in fewer than half of the countries (Argentina, Brazil, Peru, Ecuador, and Paraguay), revealing a marked geographical bias and substantial knowledge gaps (Table 2; Figure 3). Consequently, understanding of host–parasite associations in this genus remains incomplete, highlighting the need for expanded studies, particularly in underexplored regions.
A large proportion of helminth records in South American Scinax species is concentrated in S. nasicus, S. fuscovarius, and S. x-signatus (Tables 2 and 3; Figures 2 and 3). Scinax nasicus exhibits the highest richness (34 taxa), most of which (23 taxa) are associated with populations from humid Chaco areas in Corrientes Province, Argentina (Table 2, Figures 2 and 3). Scinax fuscovarius shows 28 helminth taxa recorded across multiple South American domains, predominantly in Brazilian regions (Atlantic Forest, Caatinga, Cerrado, and Pantanal), with an additional record from Paraguay (Table 2, Figures 2 and 3). Scinax x-signatus, distributed across the Caatinga, Cerrado, and Atlantic Forest in Brazil (Izecksohn and Carvalho-e-Silva Reference Izecksohn and e Silva SP2001), is associated with 27 helminth taxa, most records originating from semiarid Caatinga populations (Table 2; Figure 2). These high levels of parasite richness, concentrated in only three Scinax species, likely reflect the greater sampling effort focused on these hosts, further indicating that current knowledge of helminth diversity in Scinax remains insufficient and likely underestimated.
Except for the three Scinax species exhibiting the highest helminth richness in South America, the remaining species show relatively low helminth richness (Tables 2 and 3; Figure 2). This pattern may be partly explained by the restricted geographical distribution of some species, the limited number of helminthological studies conducted on them, or the small sample sizes of hosts examined in the studies. For instance, Scinax pedromedinae, restricted to the western Amazon Basin from northern Bolivia to Colombia, including Brazil and Peru (Hoogmoed and Avila-Pires Reference Hoogmoed and Avila-Pires2012; Araujo-Vieira et al. Reference Araujo-Vieira, Lourenço, Lacerda, Lyra, Blotto, Ron, Baldo, Pereyra, Suárez-Mayorga, Baêta, Ferreira, Barrio-Amorós, Borteiro, Brandão, Brasileiro, Donnelly, Dubeux, Köhler, Kolenc, Leite, Maciel, Nunes, Orrico, Peloso, Pezzuti, Reichle, Rojas-Runjaic, da Silva, Sturaro, Langone, Garcia, Rodrigues, Frost, Wheeler, Grant, Pombal, Haddad and Faivovich2023), has been reported in only a single study documenting two helminth species from hosts in Reserva Manu (former Reserva Cuzco Amazonico), Peru (Bursey et al. Reference Bursey, Goldberg and Parmalee2001) (Table 2, Figure 3). Similarly, Scinax auratus, an endemic species to Brazil distributed across the north-eastern extension of Brazil, from Minas Gerais through eastern Bahia, Alagoas, and Sergipe to Paraíba (Santana et al. Reference Santana, Costa, Drummond and Feio2009), has also been investigated in only one study, which reported three helminth species from hosts in the Estação Ecológica do Tapacurá, Pernambuco State (Martins-Sobrinho et al. Reference Martins-Sobrinho, Silva, Santos, Moura and Oliveira2017) (Table 2, Figure 3).
Likewise, even widely distributed Scinax species may show limited helminth records. This is the case for S. garbei, which occurs across several countries in northern South America, occurring across Bolivia, Brazil, Venezuela, Ecuador, Colombia, and Peru (Silva e Silva and Costa-Campos Reference Silva e Silva and Costa-Campos2014), yet has only two helminth species reported, based on a single study involving hosts from the Peruvian Amazon (Bursey et al. Reference Bursey, Goldberg and Parmalee2001) (Table 2, Figure 3). Overall, the scarcity of helminthological studies and records for most South American Scinax species highlights the need for further research to better characterise host–parasite associations across the genus.
Nematodes are the most representative helminth taxa in South American Scinax species, accounting for approximately 58.4% of the total recorded taxa (n = 45), followed by trematodes (26%; n = 20), acanthocephalans (10.4%; n = 8), and cestodes (5.2%; n = 4) (Tables 2 and 3). This pattern is consistent with previous South American compilations that included other anuran taxa (Campião et al. Reference Campião, Morais, Dias, Aguiar, Toledo, Tavares and Silva2014a; Chero et al. Reference Chero, Cruces, Cacique, Ponce, Iannacone, Alvariño, Sanchez, Sáez, Lopez and Silva2023).
It is noteworthy that a considerable proportion of the recorded taxa corresponds to larval stages of helminth. These larval stages are associated with all major helminth groups (Tables 2 and 3); however, most records (78.6%) are linked to Scinax populations occurring in morphoclimatic domains with greater availability of water resources, such as the Amazon, Atlantic Forest, humid Chaco, and Pantanal (Table 2).
This pattern largely involves taxa whose first intermediate hosts depend on aquatic environments, including molluscs in the life cycles of trematodes and nematodes of the family Kathlaniidae (Bartlett and Anderson Reference Bartlett and Anderson1985), as well as aquatic copepods in the life cycles of cestodes (Proteocephalidae and Spirometra sp.) (de Chambrier et al. Reference de Chambrier, Alves, Schuster and Scholz2021; Kuchta et al. Reference Kuchta, Phillips and Scholz2024). It also includes nematodes such as Spiroxys sp. (Moravec Reference Moravec1998), Physocephalus sp. (Schuster et al. Reference Schuster, Sivakumar, Ismail and Baumann2016; Demkowska-Kutrzepa et al. Reference Demkowska-Kutrzepa, Szczepaniak, Roczeń-Karczmarz, Palumbo, Studzińska, Różański and Tomczuk2021), and philometrids (Moravec Reference Moravec1980), as well as aquatic insects acting as intermediate hosts in the life cycle of rhabdochonid nematodes (Hirosawa et al. Reference Hirasawa, Urabe and Yuma2004). Larval stages of all these taxa and groups have been recorded parasitising South American Scinax species (Tables 2 and 3). However, some helminth with non-aquatic first intermediate hosts also occurs, such as larval Physaloptera sp. (terrestrial arthropods) (Felix-Nascimento et al. Reference Felix-Nascimento, Vieira, Gomes, Albinati, Muniz-Pereira, Moura, Ribeiro and Oliveira2022) and larval Brevimulticaecum sp. (anurans as intermediate or paratenic hosts) (Moravec and Kaiser 1994, González and Hamann Reference González and Hamann2013).
A total of 74% (n = 54) of the taxa recorded in Scinax species from South America could not be identified to species level. Accurate species identification is essential for reliable estimates of parasite diversity and community structure, as unidentified taxa may lead to underestimation of richness and biased comparisons among communities (Poulin Reference Poulin2019). However, species-level identification of parasites remains challenging, requiring specialised taxonomic expertise and time, and may be enhanced using molecular tools when available, which highlights the need to increase the number of taxonomic specialists in helminth involved in studies of wildlife fauna.
It is evident that improved knowledge of the biodiversity of helminth parasites of Scinax in South America has followed an increase in studies since the 2000s (Figure 5). In the present study, we found that of the 46 publications on helminth of these hosts, approximately 82% (38 publications) were produced in the 21st century (Figure 5), indicating that, over approximately 85 years of helminthological research on Scinax in the continent, most of this biodiversity has been documented only in the last 26 years. Although studies on helminth of South American anurans remain underestimated, given the high species richness of these vertebrates, these data demonstrate a considerable increase in research in recent years. This trend likely reflects the consolidation of a greater number of research groups focusing on herpetofauna and their ecological interactions across the continent, as well as increased efforts to document and catalogue this parasitological biodiversity.
Cumulative number of studies reporting helminth records in Scinax species in South America over the decades.
Financial support
Fabiano M. Vieira was supported by Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), state of Pernambuco, Brazil (Processes: DCR-0023-2.13/24 and APQ-0625-2.13/24) and by a research grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process: 303233/2024-9). Judith R. M. Souza was supported by a undergraduate research fellow from CNPq, Brazil (Process: 186011/2025.3). Carla A. C. Carvalho was supported by a Doctoral fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) (Process: 88887.111960/2025-00).
Competing interest
None.
