Skip to main content
NCBI home page
Helminthologia logoLink to Helminthologia
. 2018 Oct 27;55(4):292–305. doi: 10.2478/helm-2018-0032

Helminth Community Dynamics in a Population of Pseudopaludicola Pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian

C De S Silva 1,2,*, R W Ávila 1,2, D H Morais 2,3
PMCID: PMC6662005  PMID: 31662661

Summary

Climatic variation in low latitudes influences the dynamics and structure of parasite communities. Environmental changes caused by dry and rainy seasons alter prevalence and abundance of endoparasite communities. In addition to providing a list of the helminth species associated with the swamp frog Pseudopaludicola pocoto, this study aimed to investigate the effects of rainfall and temperature on parasitological descriptors of helminths associated with P. pocoto in an area of the semiarid zone. A total of 817 swamp frog specimens were collected between 2013 and 2017, with four sampling expeditions during the dry season and four during the rainy season. Environmental parameters of temperature and rainfall were compared to the parasitological descriptors of prevalence, abundance and mean infection intensity of the parasite community using a multivariate linear regression. A richness of eight parasite species was identified, including Nematoda (Rhabdias sp., Cosmocerca parva, Oxyascaris oxyascaris, Physaloptera sp., Brevimulticaecum sp., Spiroxys sp. and unidentified nematode) and Acanthocephala (cystacanths). Rainfall levels had a significant effect on the infection intensity of Rhabdias sp. being the presence of this species higher during the rainy season, whereas no influence of temperature was observed on the helminth community.

Keywords: Anura, Caatinga, helminthfauna, Neotropical, seasonality, semiarid

Introduction

Leptodactylidae is one of the ubiquitous frog families in the Neotropics, with great richness and abundance in the Caatinga biome (Roberto et al., 2013; Ávila, 2015). Leptodactylids occur in a wide variety of habitats, becoming exposed to several degrees of helminth infections (Goldberg et al., 2007; Bursey & Brooks, 2010; Hamann & González, 2010). The genus Pseudopaludicola currently comprises 22 species of small swamp frogs distributed in South America (Cardozo et al., 2018). To date, only two species had their helminth fauna investigated – Pseudopaludicola boliviana Parker, 1927, in which a richness of ten taxa was found, including trematodes, cestodes, nematodes and acanthocephalans (Duré et al., 2004; González & Hamann, 2012), and Pseudopaludicola falcipes Hensel, 1867, in which only the nematode Cosmocerca podicipinus Baker and Vaucher, 1984 was recorded (González & Hamann, 2004; 2009). Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014 was recently described from Northeast-Brazilian and is widely distributed in the Caatinga biome, however, there are still no studies on its ecology, only on its geographical distribution (Magalhães et al., 2014; Pereira et al., 2015; Silva et al., 2015; Lantyer-Silva et al., 2016 and Silva et al., 2017).

Several factors contribute to the dynamics and structure of parasite communities, like seasonality, environmental heterogeneity or factors associated with the host, such as spatial distribution, population density, and body size (Aho, 1990). Climate changes can cause some effects upon biological communities, like alterations on the abundance and transmission rates of helminths and also have an influence on host-parasite relations (Altizer et al., 2006; Koprivnikar et al., 2006; King et al., 2007; Koprivnikar & Poulin, 2009; Schotthoefer et al., 2011; Pizzato et al., 2013 and Brito et al., 2014). The prevalence and abundance of helminths are more influenced by seasonal variations in regions of median latitudes because cold seasons alter the acquisition of the parasite by the host (Pizzato et al., 2013). Meanwhile, in tropical areas, the prevalence and abundance of parasites can either increase or decrease between dry and rainy season (Choudhury & Dick, 2000). Thus, climatic factors, such as temperature, humidity, and rainfall levels can exert different effects upon parasitological descriptors of helminth infections.

Identifying what are the environmental factors that influence the helminth community can contribute towards the comprehension of how infection dynamics changes through time and space in order to unravel the mechanisms involved in host-parasite interactions. Besides providing a list of the helminths associated with P. pocoto, this study aims (I) to compare the similarity between the helminth communities associated with species of Pseudopaludicola and (II) to investigate the effects of rainfall and temperature upon the parasitological descriptors of prevalence (P), mean intensity of infection (MI), abundance, diversity, and migration of parasites between sites of infection in the helminths community associated with P. pocoto in Brazilian Northeast.

Material and Methods

This study was carried out in the Benguê Reservoir, Aiuaba, Ceará, Brazil (06°35’35”S, 40°08’31”W). Host samplings were performed from September 2013 to March 2017, with four expeditions during the dry season and four during the rainy season. This region is located in one of the driest areas of Ceará State, with mean annual rainfall levels of 560 mm (Funceme, 2016).

A total of 817 specimens of P. pocoto (573 males, mean snout-vent length [SVL] ± SD 13.97 ± 1.56 mm, range: 10.15 – 16.5 mm, 244 females, SVL: 15 , 1 ± 1,57 mm, range: 11,41 – 18,46 mm) were used for this study, being collected by hand for this parasitological and also specimens collected for other purposes and deposited in the Herpetology Collection of the Universidade Regional do Cariri - URCA-H, Crato, Ceará State were used. Specimens were euthanized with sodium thiopental, necropsied for helminths, fixed in 10 % formaldehyde and stored in 70 % ethanol.

Data on rainfall levels were gathered using monthly means from the Fundação Cearense de Meteorologia e Recursos Hídricos – FUNCEME (Foundation of Meteorology and Hydric Resources of Ceará State). For statistic analyses between rainfall and parasitological descriptors, a mean rainfall of every three months was extracted related to the period between the samplings (Figs. 1 and 2). The following parasitological descriptors: prevalence, mean intensity of infection, and abundance were calculated following Bush et al. 1997 using standard error and range. Aggregation of parasites was calculated using the Discrepancy Index (D) by Poulin 1998 which ranges from 0 to 1, where D = 0, all hosts harboring the same number of parasites; D = 1, all parasites found in a single host. This index was calculated in the software Quantitative Parasitology 3.0 (Rózsa et al., 2000).

Fig. 1.

Fig. 1

Open in a new tab

Monthly rainfall levels related to the sample period of P. pocoto in the municipality of Aiuaba, Ceará State, Brazil.

Source: FUNCEME

Fundação Cearense de Meteorologia e Recursos Hidricos

Fig. 2.

Fig. 2

Open in a new tab

Quarterly means of rains related to the sampling months of P. pocoto in the municipality of Aiuaba, Ceará State, Brazil.

Nematodes were found alive, washed in saline solution (0.9 % NaCl), fixed and preserved in 70 % ethanol. The nematodes were cleared in lactophenol or lactic acid while acanthocephalans were removed from their cysts, stained in carmine, and cleared in creosote. All endoparasites were observed and identified to the lowest possible level under a light microscope DMLB (Leica) and DM 5000B with interferential phase contrast, according to the literature (Yamaguti, 1961; Sprent, 1979; Vicente et al., 1991; Anderson, 2000 and Gibbons, 2010). All parasites were deposited at the Coleção Parasitológica do Laboratório de Zoologia from Universidade Regional do Cariri – LZ-URCA (Parasitological Collection of the Laboratory of Zoology).

Richness (total number of helminths) and Brillouin’s index of diversity were used to describe the parasite community. Richness was estimated using species accumulation curve, in which the number of observed species is a function of the sampling effort, measured in number of individuals using the R software packages Biodiversity R and Vegan (R core team, 2014). The Shapiro-Wilks test was applied to evaluate the normality of prevalence data, mean intensity of infection, mean abundance (MA) and diversity. Thereby, diversity between seasons was compared using Wilcoxon’s test for paired samples and differences of prevalence, mean intensity of infection, and mean abundance between seasons was tested by Student t-test.

Using a data matrix with the presence/absence variables for the parasite species related to the genus Pseudopaludicola, the degree of similarity among these helminth communities was calculated using the Sorensen’s index (So), with a posterior analysis of clustering using the Cluster method using the unweighted pair-group average (UPGMA).

A multivariate regression was performed to assess the influence of rainfall levels and temperature and their interaction on prevalence, mean intensity of infection and abundance of the helminth community of P. pocoto. To evaluate whether there were alterations of infection sites between dry and rainy seasons, a contingency table was made with data on the abundance of species infection/sites. The helminths that did not vary sites between the seasons and the ones that were not frequent were excluded from the analyses not to have influence of these values upon the species that showed greater abundance and occupied different sites. To evaluate the significance of the results, a chi-square test was performed with the data organized as a contingency table of two factors (Gotelli & Ellison, 2011). All statistical analyses were performed using the software PAST 3.0.

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed according collection authorization issued by Chico Mendes’ Institute (ICMBio/SISBio) Nº 29613 – 1; 55467 – 1 for scientific activities aims and authorized by council from Universidade Regional do Cariri-Urca nº 00260/2016.1.

Results

From the 817 hosts necropsied, 406 were parasitized with at least on helminth taxon (P = 49.7 %, MI = 1 ± 0.51, MA = 0.49 ± 0.4, range = 1 – 8). From the 405 hosts sampled in the dry season, 193 were parasitized with at least one helminth taxon (P = 47.7 %,

MI = 1 ± 0.52, MA = 0.48 ± 0.6, range = 1 – 5), and from the 412 hosts sampled in the rainy season, 213 were parasitized with at least one helminth taxon (P = 51.7 %, MI = 1 ± 0.48, MA = 0.52 ± 0.6, range 1 – 8).

A total of 803 helminths specimens were collected, including nematodes and acanthocephalans, showing a richness of eight taxa (Rhabdias sp., Cosmocerca parva Travassos, 1925, Oxyascaris oxyascaris Travassos, 1920, Physaloptera sp., Brevimulticaecum sp., Spiroxys sp., unidentified nematode, and cystacanths) (Table 1). The infracommunity richness varied from one to three helminth species by host. The most abundant species recorded in this study were found in adult stage: Rhabdias sp. (N = 279), C. parva (N = 285), and O. oxyascaris (N = 157).

Table 1.

Helminth component community associated with Pseudopaludicola pocoto from the municipality of Aiuaba, Ceará State, Brazil.

Helminth P (%) MI MA IS Stage Range
Nematoda
Rhabdias sp.a 22.6 1.49 ± 1.7 0.34 Lungs Adult 1 – 8
Cosmocerca parva a,b 25.5 1.35 ± 1.4 0.34 St, SI and LI Adult 1 – 5
Oxyascaris oxyascaris a,b 12.3 1.54 ± 1.8 0.2 SI and LI Adult 1 – 7
Physaloptera sp.a 0.1 1 ± 1 0 St Larva 1
Spiroxys sp.a 0.1 1 ± 1 0 Cav Larva 1
Brevimulticaecum sp.a,b 0.1 1 ± 1 0 Cav Larva 1
Unidentified nematode 2.9 1.5 ± 2.3 0.4 St, SI and Cav Larva 1 – 4
Acanthocephala
Cystacanth 1.1 1.43 ± 1.79 0 Cav Cyst 1 – 3
Open in a new tab

P (%) - prevalence; MI – mean intensity of infection; MA– mean abundance; IS – infection site; St – stomach; SI – small intestine; LI – large intestine; Cav – body cavity; a – new record; b – new locality

The aggregation index of the helminths showed moderate values in the dry season (D = 0.52±0.5) and rainy season (D = 0.48±0.48). The Brillouin’s diversity index for the dry and rainy season were i = 1.42 and i = 1.29, respectively. There was no difference between seasons for prevalence (t= -0.0439; p = 0.96), mean intensity of infection (t = 1.359; p = 0.27) and mean abundance (t = -0.824; p = 0.47). The accumulation curve and the confidence interval showed a tendency to stabilization of richness of the helminths associated with this host in that location (Fig. 3).

Fig. 3.

Fig. 3

Open in a new tab

Species accumulation curve (black line) and confidence interval (gray) for the richness of the helminths associated with P. pocoto, from the municipality of Auiaba, Ceará State, Brazil.

The similarity between the communities of helminths of P. pocoto and P. boliviana and between P. pocoto and P. falcipes was of (So = 0), totally differing in their compositions of parasitic species. The proximity between P. boliviana and P. falcipes was of (So = 18.1 %). The distance between the communities analyzed and compared with the present study are represented in Figure 4.

Fig. 4.

Fig. 4

Open in a new tab

Dendogram based on Sorensen similarity index comparing the helminth communities associated by genus Pseudopaludicola.

There was no influence of rainfall or temperature or the interaction between both environmental variables on the community of

helminths P. pocoto (Table 2). However, the rainy season had a significant influence on intensity of infection of Rhabdias sp. (p = 0.0014), which was not found for the other abundant species (Table 2).

Table 2.

Effects of rainfall levels and temperature on the infection descriptors of the helminth community of Pseudopaludicola pocoto, from the municipality of Aiuaba, Ceará State, Brazil.

Prevalence Infection Intensity Abundance
Rainfall
Helminth community r 0.195 0.632 0.427
p 0.64 0.09 0.29
Rhabdias sp. r 0.464 0.91 0.556
p 0.24 0.0014* 0.15
C. parva r 0.118 0.574 0.284
p 0.78 0.14 0.49
O. oxyascaris r 0.298 0.02 0.372
p 0.47 0.95 0.36
Temperature
Helminth community r -0.428 0.672 -0.462
p 0.29 0.07 0.25
Rhabdias sp. r -0.582 -0.41 -0.5
p 0.13 0.31 0.2
C. parva r -0.485 -0.611 -0.54
p 0.22 0.11 0.17
O. oxyascaris r -0.265 0.371 -0.31
p 0.52 0.36 0.45
Rainfall: Temperature
Helminth community r 0.03 0.4 0.18
p 0.59 0.14 0.48
Open in a new tab

*Effects of rainfall levels on infection intensity of Rhabdias sp. (p-value < 0.05)

Regarding range of infection sites, Figure 5 shows the results of the most abundant species and the ones with greatest variation of sites. The chi-square test showed significant differences of the parasites migration patterns among the infection sites of the hosts between dry and rainy season for C. parva (p = 9.84e-17). Cosmocerca parva was more related to the stomach (n=129) in the dry season, while in the rainy season this species used both stomach (n=67) and the intestines (n=89). However, for O. oxyascaris (p = 0.0024), although significant, the test found variation in the abundance of infection of this species between dry and rainy season, but no changes in the infecting site. The values of abundance in each host’s site infection by season and total values are presented in Figure 6.

Fig. 5.

Fig. 5

Open in a new tab

Species/site relation between dry and rain season.

Fig. 6.

Fig. 6

Open in a new tab

Abundance values of infection by host site.

Discussion

Similar to other members of the Leptodactylidae, P. pocoto prefers semi-aquatic habitats (Frost, 2013), which is mirrored in the infection routes of its helminths, since the most abundant parasite species found in this study have direct life cycle. Nematodes were the most frequent taxa in the helminth community of P. pocoto in this study, with representatives of six families (Rhabdiasidae, Cosmocercidae, Oxyascarididae, Physalopteridae, Gnathostomatidae, Heterocheilidae). As in the present study, cosmocercids are the most frequently nematodes found among Leptodactylidae (Duré et al., 2004; González & Hamann, 2004; 2012; Santos & Amato, 2013; Campião et al., 2014).

The genus Rhabdias currently includes approximately eighty species, of which fifteen are valid for the Neotropical region (Kuzmin et al., 2016). From the species that occur in Brazil, seven are found in the amphibians and reptiles: Rhabdias androgyna Kloss, 1971, Rhabdias fuelleborni Travassos, 1926, Rhabdias hermafrodita Kloss, 1971, Rhabdias galactonoti Kuzmin, Melo, Silva-Filho and Santos, 2016, Rhabdias paraenses Santos, Melo, Nascimento, Nascimento, Giese and Furtado, 2011, Rhabdias breviensis Nascimento, Gonçalves, Melo, Giese, Furtado and Santos, 2013, and Rhabdias stenocephala Kuzmin, Melo, Silva-Filho and Santos, 2016 (Kuzmin et al., 2016).

The morphological and morphometric characters often used for the characterization of Rhabdias species largely overlap (Tkach et al., 2014). Currently, the most promising morphological characters with a tendency to accompany molecular data results are the shape and structure of the apical region, which are classified into five categories: (a) absence of lips, (b) six lips uniform in size and shape (c) four submedian and two pseudolabial lips, (d) two lateral pseudolabia and four in protuberance forms, and (e) species with only two pseudolabia (Tkach et al., 2014; Kuzmin, 2013). From the specimens collected, it was possible to identify that the apical morphological characteristics are consistent with the characteristics of the neotropical species, like the presence of six lips uniform in length and shape (Tkach et al., 2014). Morphometric analyzes performed for the Rhabdias specimens collected in this study demonstrate morphological characters of the apical region and morphometrics different from the species recorded for Brazil, which led us to the implementation of molecular analyzes for the certification of a possible new species for the genus and a later description (Figs. 7a and 7b).

Fig. 7.

Fig. 7

Open in a new tab

Photomicrography of the helminth species associated with Pseudopaludicola pocoto. a – anterior region of Rhabdias sp. focusing on esophagus and lateral wing; b – view of the mouth of Rhabdias sp.; c – posterior view of the male Cosmocerca parva, spicules and plectanas; d – anterior view of the male Oxyascaris oxyascaris, esophagus and lateral wing; e – view of the anterior portion of the male O. oxyascaris with emphasis on the mouth and lateral wing; f – anterior view of Physaloptera sp.; g – anterior view of the larva of Spiroxys sp.; h – anterior view of the larva of Brevimulcaecum sp.

Species of the genus Cosmocerca are widely distributed throughout all continents. The species Cosmocerca parva has a large distribution throughout Central and South America, thus having morphological and morphometric variations regarding body length, width and number of plectanas (5 – 7) (Rizvi et al., 2011). According to González and Hamann 2011 these variations occur according to the host and sometimes within the same individual. Even though the specimens found in this study present the same morphological characteristics as the ones described by Travassos 1925, the phenotypic plasticity observed is wide and the morphometric characters observed are smaller than those reported in the literature (Bursey et al., 2015) (Table 3), which may be related to the size of the host (Fig. 7c).

Table 3.

A selection of parameters in male individuals of Cosmocerca parva.

Cosmocerca parva
Travassos, 1925 Present study
Body length 1.42 – 2.01 1.38
Spicule length 90 – 110 89
Gubernaculum length 85 – 108 69
Number of plectanes 5 – 7 5
Lateral alae Present Present
Open in a new tab

Column 1 represents the metric range in μm of the morphometry of C. parva. (Revised from Bursey et al., 2015)

There are currently 30 species described for Cosmocerca, of which 10 are described for the Neotropical region (Bursey et al., 2015). Peru, Argentina and Brazil are the countries in South America with the highest numbers of infection records of C. parva in amphibians, respectively (Santos & Amato, 2013). In Brazil, the records of this helminth are mainly concentrated in the South and Southeast regions, infecting species of Brachycephalidae, Leptodactylidae, Hylodidae, Hylidae, and Bufonidae (Campião et al., 2014).

Oxyascaris oxyascaris was initially described parasitizing the snake Mastigodryas bifossatus Raddi, 1820 (= Drymobius bifossatus) in Rio de Janeiro (Vicente et al., 1991). Currently, the genus is composed of four other Oxyascaris species: Oxyascaris similis Travassos, 1920 (= Pteroxyascaris similis), Oxyascaris caudacutus Freitas, 1958, Oxyascaris mcdiarmidi Bursey and Goldberg, 2007 (Bursey & Goldberg, 2007). In Brazil, there are records of O. oxyascaris infecting amphibians of the Leptodactylidae family in the South and Southeast regions (Vicente et al., 1991). In the Northeast of Brazil, the records are restricted to the states of Bahia and Pernambuco (Teles et al., 2015). This species is identified by having a mouth with three lips, muscular esophagus followed by a glandular ventricle, equal spines, and gull-wing and caudal wings absent (Vicente et al., 1991) (Figs. 7d and 7e).

Physaloptera are parasites of all classes of terrestrial vertebrates (Anderson, 2000; Gorgani et al., 2013). Currently, the following species have been registered for South America and Brazil, infecting reptiles and mammals: Physaloptera liophis Vicente and Santos, 1974, Physaloptera obtusissima (= P. monodens) Molin, 1860, Physaloptera tubinambae Pereira, Alves, Rocha, Lima and Luque,

2012, Physaloptera praeputialis Linstow, 1889, Physaloptera lutzi Cristofaro, Guimarães and Rodrigues, 1976, Physaloptera retusa Rudolphi, 1819 and P. bainae Pereira, Alves, Rocha, Lima and Luque, 2014 (Ávila & Silva, 2010; Ávila et al., 2012; Pereira et al., 2014 and Ramos et al., 2016). As for amphibians there is a record of infection by Physalopteridae larvae in the municipality of Angicos (RN) in the host Rhinella granulosa Spix, 1824 (Madelaire et al., in press). The specimens of Physaloptera sp. found in this study present a cephalic colarete formed by the cuticle reflected on the lips and having a mouth with two large, lateral, simple, triangular lips, each provided with a variable number of apical teeth and externally with papillae (Vicente et al., 1991) (Fig. 7f).

The genus Spiroxys is widely distributed throughout the Eurasian Palearctic, North Africa, North America and Neotropical countries (Hasegawa et al., 1998; Mascarenhas & Muller, 2015). Two species of the genus are found in Brazil, Spiroxys contortus Rudolphi 1819, described for the South and Southeast and Spiroxys figueiredoi Freitas and Dobbin 1962, with records for the North-Northeast, Southeast and Central-West regions infecting species of chelonians and snakes (Vicente et al., 1993; Bernadon et al., 2013; Mascarenhas and Muller, 2015 and Viana et al., 2016). Species of the genus Spiroxys are currently divided into three groups: (a) characterized by the presence of teeth in each lobe of the pseudolabium, (b) with teeth only in the median lobe and finally Roca and García, 2008 proposed a third group (c) that are without teeth, found in the Eastern, Australian and Ethiopian zoogeographic regions (Purwaningsih, 2015). The species that occur in Brazil, S. contortus and S. figuereidoi, are included in the second group (Mascarenhas & Muller, 2015; Fig. 7g).

Brevimulticaecum species are described occurring in the continents of Africa, America and Oceania (Vieira et al., 2010). The genus is characterized by having smooth lips with winged margins and absence of dentigerous furrows, excretory pore located anterior to the nerve ring and ventricle with short appendages (González & Hamann, 2013). Immature individuals of Brevimulticaecum were recorded infecting species such as the Brazilian snake Bothrops neuwiedi Wagler in Spix, 1824, the treefrog Dendropsophus minutus Peters, 1872 and in the freshwater fishes Gymnotus carapo Linnaeus 1758 and Loricariichthys brunneus Hancok 1828 (Sprent, 1979; Moravec and Kaiser, 1994; Moravec et al., 1997 and Vieira et al., 2010) (Fig. 7h).

Accumulation curve based on sampling effort proved to be satisfactory, since the sample reached the asymptote and was representative for sampling the helminth species associated with P. pocoto. The helminths richness in P. pocoto (S=8) is higher among species of Pseudopaludicola (Duré et al., 2004; González & Hamann, 2004; 2012). The richness of the helminth infrapopulation of P. pocoto varied from one to three species per host, which may be explained by the body size that is a factor influencing the richness and composition of helminth communities (Campião et al., 2015). Duré et al. 2004 studied the helminth fauna of P. boliviana and found a greater species diversity, with representatives of Trematoda (70 %) showing the greatest richness and intensity of infection (Table 4). The cluster analysis indicates that there is more proximity between the helminth communities of P. boliviana and P. falcipes than between P. pocoto and this is due to the fact that P. boliviana and P. falcipes are sympatric species, and the low similarity between them can be explained by the low sampling of helminths in P. falcipes (Fig. 4). In addition, we must also consider that this difference between the community of helminths of P. pocoto and the other species of the genus may be due to geographical and environmental differences. The Argentine province of Corrientes, where the species P. boliviana was studied, is characterized by wide habitat heterogeneity, many temporary and permanent water bodies, and gleyic arenosols (Duré et al., 2004; IUSS, 2015). Thus, aquatic environments can facilitate the occurrence of trematodes, considering that the life cycle of these helminths is heteroxenic, and that in at least one of the phases of parasite transmission is found free in a liquid environment (Travassos, 1950).

Table 4.

List of helminths related to the species of the genus Pseudopaludicola.

Host Helminths Locality References
Pseudopaludicola boliviana Trematoda
Catadiscus sp.
Haematoloechus sp.
Gorgoderina sp.
Bursotrema sp.
Plagiorchiata sp.
Travtrema sp.
Echinostomatidae sp. Corrientes, Argentina Duré, 2004; González and Hamann, 2012
Cestoda
Eucestoda sp.
Nematoda
Cosmocerca sp.
Cosmocerca podicipinus
Acanthocephala
centrorhynchus sp.
Pseudopaludicola falcipes Nematoda Corrientes, Argentina González and Hamann, 2004; 2009
Cosmocerca podicipinus
Pseudopaludicola pocoto Nematoda
Rhabdias sp.
Cosmocerca parva
Oxyascaris oxyascaris
Physaloptera sp.
Spiroxys sp. Ceará, Brazil Present study
Brevimulticaecum sp.
Unidentified nematode
Acanthocephala
Cystacanth
Open in a new tab

Pseudopaludicola pocoto showed a component community mainly composed of nematodes, which may be related to the characteristics of its habitat. The municipality of Aiuaba shows low rainfall levels, annual temperature typical of semiarid climate, and soil composed of arenosols-argillaceous matter (Ipece, 2016). Nematodes are abundant in terrestrial habitats (Ruppert & Barnes, 1996), and the occurrence of these worms in the same habitat as P. pocoto enable the encounter of parasites and hosts. The greater abundance of Rhabdias sp., C. parva and O. oxyascaris found in all samplings of this present study suggest that the larvae of these nematode species are present in the habitat throughout the year. This fact can be favored by some habitat characteristics such as high soil humidity, allowing the eggs of these parasites to remain viable in the soil throughout the year giving rise to new larval forms and thus allowing continuity to infection by penetration through the skin in the host (Anderson, 2000; Brito et al., 2014).

Although the study period is insufficient to access long-term bioclimatic predictions on parasite infections of amphibians, the results found herein showed a significant effect of environmental changes on the parasite community, which corroborate other results for the Brazilian semi-arid. Brito et al. 2014 found a significant effect of climate variations on the abundance of the helminth community infecting lizards of the family Tropiduridae. In this present study, the environmental changes had an effect on the intensity of infection of Rhabdias sp. (Table 2). This lung parasite showed high prevalence in all sampling periods, but was even higher during the rainy season, which may be due to the high humidity in this period. However, climate interaction and rainfall levels did not have effects on the helminth community and species C. parva and O. oxyascaris in the present study. The investigation of which other variables, like sun radiation, salinity, humidity, and soil pH, are influencing the maintenance of parasite communities is an interesting premise for future studies.

Koprivnikar & Poulin 2009 observed the effects of temperature on cercariae species, in which the temperature was a significant variable increasing the growth rate of these parasites. However, the behavior of these helminths differs in subtropical areas as compared to tropical areas (Choudhury & Dick, 2000; Pizzato et al., 2013). For the present study, the temperature did not have a significant influence on the helminth infection rates. Although, a suppressing effect could be observed on the helminth as the temperature increased, even without statistic significance (Table 2).

Environmental changes influence the feeding behavior of hosts (Brito et al., 2014), which can affect the infracommunity diversity and infrapopulation abundance of helminths. The migration pattern between the seasons of C. parva and O. oxyascaris within the infection sites of P. pocoto can indicate greater resource availability within the host during the rainy season. This justifies an increase in the occurrence of C. parva in the intestinal tract of the host, being found simultaneously with O. oxyascaris in the same infection site during that season. However, there might be a greater resource competition in the intestinal tract during the rainy season which may lead C. parva to unexplored sites within the host (Esch et al., 1990). Still, the occurrence of C. parva in the stomach during the dry season can indicate that this species is not a good competitor and by occupying the first organ of the digestive tract this parasite has more chances to obtain food resources (Fig.5).

The low occurrence of the species Brevimulticaecum sp., Spiroxys sp. and Physaloptera sp. can be explained by the climate conditions of the habitat and also by their life cycle since the three species were recorded during high levels of rainfall. However, the low prevalence and abundance of these nematodes can be related to the fact that species with complex life cycles suffer decrease in population density during trophic transmission (Poulin & Largrue, 2015). Another explanation that justifies the low values of the parasitological descriptors for these genera recorded in this work is the sample effort, which was important to reveal rare species associated with this host. These parasite larvae can be found infecting amphibians that act as second intermediate or paratenic hosts (Sprent, 1979; Vicente et al., 1993; Moravec et al., 1997; Goldberg & Bursey, 2007; Goldberg et al., 2009 and González & Hamann, 2013). The precise identification of these helminths was not possible because only one specimen of each was found.

Investigating and describing the effects of environmental changes on endoparasites associated with members of the family Leptodactylidae can help to elucidate such effects on the dynamics of parasite communities. Besides, inventories of parasite fauna can contribute to studies on host-parasite relation of leptodactylids because they generate new information on the helminths associated with these hosts and provide new guides to identification (Poulin et al., 2015). The present study provides new helminth records for Pseudopaludicola, and also new records on the range and distribution of some helminth species in the Northeast-Brazilian. The Caatinga biome, with its habitat heterogeneity concentrated in the semiarid, encompasses a diverse fauna of amphibians (Camurugi et al., 2010; Andrade et al., 2014; Borges-Leite et al., 2014 and Cavalcanti et al., 2014). Nevertheless, there is still a scarce knowledge of diversity of helminths endoparasites associated with these amphibians.

Acknowledgements

The authors thank the FUNCAP (Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico) for financial support. RWA thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for providing research fellowship (PQ # 303622/2015-6). The Laboratory of Herpetology of the Universidade Regional do Cariri for the technical support to develop this study. To Chico Mendes’ Institute (ICMBio/SISBio) for the collection authorization Nº 29613 – 1; 55467 – 1, for scientific activities aims. To Carlos Alberto de Souza Rodrigues Filho for helping with the graphics. We are also thankful to Samuel Cardozo Ribeiro and Karla Magalhães Campião for essential contribution to the manuscript.

Footnotes

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aho J.M. Esch G.W., Bush A.O., Aho J.M. Parasite Communities: Patterns and Processes. Volume 1. New York: Chapman & Hall; 1990. Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes, Chapman and Hall, London, U. K; p. 355. [Google Scholar]
  2. Anderson R.C. Nematode parasites of vertebrates, their development and transmission. Wallingford, UK: CABI Publishing; 2000. p. 650pp. 2nd Edition. [Google Scholar]
  3. Andrade E.B., Almeida J.R.S.L., Andrade G.V.. Anurans from the municipality of Ilha Grande, Parnaíba River Delta, Piauí, Northeastern Brazil. Herpetol. Notes. 2014;7:219–226. [Google Scholar]
  4. Altizer S., Dobson A., Hosseini P., Hudson P., Pascual M., Rohani P.. Seasonality and the dynamics of infectious diseases. Ecol. Lett. 2006;9:467–484. doi: 10.1111/j.1461-0248.2005.00879.x. doi: 10.1111/j.1461-0248.2005.00879.x. ÁVILA, R.W., SILVA, R.J. (2010): Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. J. Venom. Anim. Toxins incl. Trop. Dis., 16: 543–572. [DOI] [PubMed] [Google Scholar]
  5. Ávila R.W., Anjos L.A., Ribeiro S.C., Morais D.M., Silva R.J., Almeida W.O.. Nematodes of lizards (Reptilia: Squamata) from Caatinga Biome, Northeastern Brazil. Comp. Parasitol. 2012;79:56–63. doi: 10.1654/4518.1. [DOI] [Google Scholar]
  6. Ávila R.W. Herpetofauna do sul do Ceará e sertão pernambucano Herpetofauna of Southern from Ceará and sertão Pernambuco 1st. Crato, Ceará: 2015. p. 160pp. Edition. (In Portuguese) [Google Scholar]
  7. Bernadon F.F., Valente A.L., Muller G.. Gastrointestinal helminths of the Argentine side-necked turtle, Phrynops hilarii (Dumé ril & Bibron, 1835) (Testudines, Chelidae) in South Brazil. Pan-American J. Aqua. Sci. 2013;8(1):55–57. [Google Scholar]
  8. Borges-Leite M.J., Rodrigues J.F.M., Borges-Nojosa D.M.. Herpetofauna of a Coastal Region of Northeastern Brazil. Herpetol. Notes. 2014;7:405–413. [Google Scholar]
  9. Brito S.V., Ferreira F.S., Ribeiro S.C., Anjos L.A., Almeida W.O., Mesquita D.O., Vasconcellos A.. Spatial-temporal variation of parasites in Cnemidophorus ocellifer (Teiidae) and Tropidurus hispidus and Tropidurus semitaeniatus (Tropiduridae) from Caatinga areas in Northeastern Brazil. Parasitol. Res. 2014;113:1163–1169. doi: 10.1007/s00436-014-3754-7. [DOI] [PubMed] [Google Scholar]
  10. Bursey C.R., Goldberg S.R.. A new species of Oxyascaris (Nematoda, Cosmocercidae) in the Costa Rica brook frog, Duellmanohyla uranochroa (Anura, Hylidae) Acta Parasitol. 2007;52(1):58–61. doi: 10.2478/s11686-007-0007-2. [DOI] [Google Scholar]
  11. Bursey C.R., Brooks D.R.. Nematode parasites of 41 anuran species from the area de conservacion Guanacaste, Costa Rica. Comp. Parasitol. 2010;77(2):221–231. doi: 10.1654/4418.1. [DOI] [Google Scholar]
  12. Bursey C.R., Goldberg S.R., Siler C.D., Brown R.M.. A new species of Cosmocerca (Nematoda: Cosmocercidae) and other helminths in Cyrtodactylus gubaot (Squamata: Gekkonidae) from the Philippines. Acta Parasitol. 2015;60(4):675–681. doi: 10.1515/ap-2015-0096. [DOI] [PubMed] [Google Scholar]
  13. Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W.. Parasitology meets ecology on its own terms: Margolis et al revisited. J. Parasitol. 1997;83(4):575–583. doi: 10.2307/3284227. [DOI] [PubMed] [Google Scholar]
  14. Campião K.M., Morais D.H., Dias O.T., Aguiar A., Toledo G., Tavares L.E.R., Silva R.J.. Checklist of helminth parasites of amphibians from South America. Zootaxa. 2014;3843(1):1–93. doi: 10.11646/zootaxa.3843.1. [DOI] [PubMed] [Google Scholar]
  15. Campião K.M., Ribas A.C.A., Morais D.H., Dias O.T., Silva R.J., Tavares L.E.R.. How many parasites species a frog might have? Determinants of parasite diversity in South American anurans. PlosONE. 2015;10:1–12. doi: 10.1371/journal.pone.0140577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Camurugi F., Lima T.M., Mercês E.A., Juncá F.A.. Anurans of the Reserva Ecológica da Michelin, municipality of Igrapiúna, state of Bahia, Brazil. Biota neotrop. 2010;10:305–312. doi: 10.1590/S1676-06032010000200032. [DOI] [Google Scholar]
  17. Cardozo D.E., Baldo D., Pupin N., Gasparini J.L., Haddad C.F.B.. A new species of (Anura, Leiuperinae) from Espírito Santo, Brazil. Peer J. 2018;6:4766. doi: 10.7717/peerj.4766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Cavalcanti L.B.Q., Costa T.B., Colli G.R., Costa G.C., França F.G.R., Mesquita D.O., Palmeira C.N.S., Pelegrin N., Soares A.H.B., Tucker D.B., Garda A.A.. Herpetofauna of protected areas in the Caatinga II: Serra da Capivara National Park, Piauí, Brazil. Check List. 2014;10(1):18–27. doi: 10.15560/10.1.18. [DOI] [Google Scholar]
  19. Choudhury A., Dick T.A.. Richness and diversity of helminth communities in tropical freshwater fishes: empirical evidence. J. Biogeogr. 2000;27(4):935–956. doi: 10.1046/j.1365-2699.2000.00450.x. [DOI] [Google Scholar]
  20. Duré M.I., Schaefer E.F., Hamann M.I., Kehr A.I.. Consideraciones ecológicas sobre la dieta, la reproducción y el parasitismo de Pseudopaludicola boliviana (Anura, Leptodactylidae) de Corrientes, Argentina [Ecological considerations on diet, reproduction and parasitism of Bolivian Pseudopaludicola (Anura, Leptodactylidae) of Corrientes, Argentina] Phyllomedusa. 2004;3(2):121–131. [Google Scholar]
  21. Esch G.W., Shostak A.W., Marcogliese D.J., Goater T.M. Esch G.W., Bush A.O., Aho J.M. Parasite Communities: Patterns and Processes. Volume 1. New York, Chapman & Hall: 1990. Patterns and processes in helminth parasite communities: an overview; p. 355. [Google Scholar]
  22. Frost D.R. Amphibian species of the world: an online reference, American Museum of Natural History. New York, USA: 2013. http://research.amnh.org/vz/herpetology/amphibia/index.php version 6.0. [Google Scholar]
  23. FUNDAÇÃO CEARENSE DE METEOROLOGIA E RECURSOS HÍDRICOS. FUNCEME [Foundation of Meteorology and Hydric Resources of Ceará State] Zoneamento Geoambiental do Ceará: Mesorregião do Sul cearense Retrieved December. 2016;08:2016. http://www.funceme.br/ from. Retrieved December 08, 2016 (In Portuguese) [Google Scholar]
  24. Gibbons L. Keys to the nematode parasites of vertebrates. CABI International; Wallingford, U.K: 2010. Supplementary Volume. [Google Scholar]
  25. Goldberg S.R., Bursey C.R., Caldwell J.P., Vitt L.J., Costa G.C.. Gastrointestinal helminths from six species of frogs and three species of lizards sympatric in Pará state, Brazil. Comp. Parasitol. 2007;74(2):327–342. doi: 10.1654/4268.1. [DOI] [Google Scholar]
  26. Goldberg S.R., Bursey C.R.. Helminths of two species of frogs Lithobates taylori and Lithobates vaillanti (Ranidae), from Costa Rica. Caribb. J. Sci. 2007;43(1):65–72. doi: 10.18475/cjos.v43i1.a6. [DOI] [Google Scholar]
  27. Goldberg S.R., Bursey C.R., Caldwell J.P., Shepard D.B.. Gastrointestinal helminths of six sympatric species of Leptodactylus from Tocantins state, Brazil. Comp. Parasitol. 2009;76(2):258–266. doi: 10.1654/4368.1. [DOI] [Google Scholar]
  28. González C.E., Hamann M.I.. Primer registro of Cosmcoerca podicipinus Baker y Vaucher, 1984 (Nematoda, Cosmocercidae) en Pseudopaludicola falcipes (Hensel, 1867) (Amphibia, Leptodactylidae) en Argentina [First record of Cosmcoerca podicipinus Baker and Vaucher, 1984 (Nematoda, Cosmocercidae) in Pseudopaludicola falcipes (Hensel, 1867) (Amphibia, Leptodactylidae) in Argentina] Facena. 2004;20:65–72. (In Portuguese) [Google Scholar]
  29. González C.E., Hamann M.I.. Seasonal occurrence of Cosmocerca podicipinus (Nematoda: Cosmocercidae) in Pseudopaludicula falcipes (Amphibia, Leiuperidae) from the agricultural area in Corrientes, Argentina. Revta. Ib.-lat. Parasitol. 2009;68:173–179. doi: 10.1007/s00436-012-3034-3. [DOI] [PubMed] [Google Scholar]
  30. González C.E., Hamann M.I.. Cosmocercid nematodes of three species of frogs (Anura: Hylidae) from Corrientes, Argentina. Comp. Parasitol. 2011;78(1):212–216. doi: 10.1654/4470.1. [DOI] [Google Scholar]
  31. González C.E., Hamann M.I.. Seasonal occurrence of Cosmocerca podicipinus (Nematoda: Cosmocercidae) in Pseudopaludicola boliviana (Anura: Leiuperidae) from natural environments in Corrientes Province, Argentina and aspects of its population structure. Parasitol. Res. 2012;111:1923–1928. doi: 10.1007/s00436-012-3034-3. [DOI] [PubMed] [Google Scholar]
  32. González C.E., Hamann M.I.. First record of Brevimulticaecum larvae (Nematoda, Heterocheilidae) in amphibians from northern Argentina. J. Biol. 2013;73(2):451–452. doi: 10.1590/S1519-69842013000200031. [DOI] [PubMed] [Google Scholar]
  33. Gorgani T., Naem S., Farshid A.A., Otranto D.. Scanning electron microscopy observations of the hedgehog stomach worm, Physaloptera clausa (Spirurida: Physalopteridae) Parasit. vect. 2013;6:87. doi: 10.1186/1756-3305-6-87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Gotelli N.J., Ellison A.M. Princípios de estatística em ecologia Principles of statistic em ecology. Porto Alegre, Brasil, Artmed: 2011. p. 528pp. 1st Edition. In Portuguese. [Google Scholar]
  35. Hamann M.I., González C.E.. Helminth community structure of Scinax nasicus (Anura: Hylidae) from a South American subtropical area. Dis. Aquat. Organ. 2010;93:71–82. doi: 10.3354/dao02276. [DOI] [PubMed] [Google Scholar]
  36. Hasegawa H., Miyata A., Doi T.. Spiroxys hanzaki n. sp. (Nematoda: Gnathostomatidae) collected from the giant salamander, Andrias japonicus (Caudata: Cryptobranchidae) in Japan. J. Parasitol. 1998;84:831–834. [PubMed] [Google Scholar]
  37. INSTITUTO DE PESQUISA E ESTRATÉGIA ECONÔMICA DO CEARÁ. IPECE [Institute of Research and Economic Strategy of Ceará] Perfil Básico Municipal do Município de Aiuaba. Retrieved November. 2016;05:2016. http://www.ipece.ce.gov.br/perfil_basico_municipal/2016/Aiuaba.pdf from. (In Portuguese) [Google Scholar]
  38. King K.C., Mclaughlin J.D., Gendron A.D., Pauli B.D., Giroux J., Rondeau B., Boily M., Juneau P., Marcogliese D.J.. Impacts of agriculture on the Parasite communities of Northern leopard frogs Rana pipiens in southern Quebec, Canada. Parasitology. 2007;134:2063–2080. doi: 10.1017/S0031182007003277. [DOI] [PubMed] [Google Scholar]
  39. Koprivnikar J., Baker R.L., Forbes M.R.. Environmental factors influencing trematode prevalence in grey tree frog Hyla versicolor tadpoles in Southern Ontario. J. Parasitol. 2006;92(5):997–1001. doi: 10.1645/GE-771R.1. [DOI] [PubMed] [Google Scholar]
  40. Koprivnikar J., Poulin R.. Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitol. Res. 2009;105:957–965. doi: 10.1007/s00436-009-1477-y. [DOI] [PubMed] [Google Scholar]
  41. Kuzmin Y.. Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa. 2013;3639(1):001–076. doi: 10.11646/zootaxa.3639.1.1. [DOI] [PubMed] [Google Scholar]
  42. Kuzmin Y., Melo F.T.V., Silva-Filho H.F., Santos J.N.. Two new species of Rhabdias Stiles et Hassall,1905 (Nematoda: Rhabdiasidae) from anuran amphibians in Pará, Brazil. Folia Parasitol. 2016;63:15. doi: 10.14411/fp.2016.015. https://10.14411/fp.2016.015 DOI. [DOI] [PubMed] [Google Scholar]
  43. Lantyer-Silva A.S.F., Matos M.A., Gogliath M., Marciano-Jr E., Nicola P.A.. New records of Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014 (Amphibia: Anura: Leptodactylidae) in the Caatinga Biome, Brazil. Check list. 2016;12(6):1–4. doi: 10.15560/12.6.1989. [DOI] [Google Scholar]
  44. Madelaire C.B., Franceschini L., Gomes F.R., Silva R.J.. (in press): Helminth parasites of three anuran species during reproduction and drought in the Brazilian semi-arid Caatinga region. doi: 10.1645/16-130. [DOI] [PubMed] [Google Scholar]
  45. Magalhães F.M., Loebmann D., Kokubum M.N.C., Haddad C.F.B., Garda A.A.. A new species of Pseudopaludicola (Anura: Leptodactylidae: Leiuperinae) from Northeastern Brazil. Herpetologica. 2014;70(1):77–88. doi: 10.1655/HERPETOLOGICA-D-13-00054. [DOI] [Google Scholar]
  46. Mascarenhas C.S., Muller G.. Spiroxys contortus (Gnathostomatidae) and Falcaustra affinis (Kathlaniidae) from Trachemys dorbigni (Emydidae) in Southern Brazil. Comp. Parasitol. 2015;82(1):129–136. doi: 10.1654/4726.1. [DOI] [Google Scholar]
  47. Moravec F., Kaiser H.. Brevimulticaecum sp. larvae (Nematoda: Anisakidae) from the frog Hyla minuta Peters in Trinidad. J. Parasitol. 1994;80(1):154–156. [PubMed] [Google Scholar]
  48. Moravec F., Prouza A., Royero R.. Some nematodes of freshwater fishes in Venezuela. Folia Parasitol. 1997;44(1):33–47. [PubMed] [Google Scholar]
  49. Pereira F.B., Alves P.V., Rocha B.M., Lima S.S., Luque J.L.. Physaloptera bainae n. sp. (Nematoda: Physalopteridae) Parasitic in Salvator merianae (Squamata: Teiidae), with a Key to Physaloptera species parasitizing reptiles from Brazil. J. Parasitol. 2014;100(2):221–227. doi: 10.1645/13-281.1. [DOI] [PubMed] [Google Scholar]
  50. Pereira E.N., Teles M.J.L., Santos E.M.. Herpetofauna em remanescente de Caatinga no Sertão de Pernambuco, Brasil [Herpetofauna in remnant of Caatinga from Sertão of Pernambuco, Brazil] Bol. Mus. Biol. Mello Leitão. 2015;37(1):29–43. (In Portuguese) PIZZATO, L., KELEHEAR, C., SHINE, R. (2013): Seasonal dynamics of the lungworm, Rhabdias pseudosphaerocephala in recently colonised cane toad Rhinella marina populations in tropical Australia. Int. J. Parasitol. 43: 753–761. [Google Scholar]
  51. Poulin R.. Comparison of three estimators of species richness in parasite component communities. J. Parasitol. 1998;84(3):485–90. doi: 10.2307/3284710. [DOI] [PubMed] [Google Scholar]
  52. Poulin R., Largrue C.. The ups and downs of life: population expansion and bottlenecks of helminth parasites through their complex life cycle. Parasitology. 2015;142(6):791–799. doi: 10.1017/S0031182014001917. [DOI] [PubMed] [Google Scholar]
  53. Poulin R., Besson A.A., Morin M.B., Randhawa H.S.. Missing links: testing the completeness of host-parasite checklists. Parasitol. 2015;143(1):114–122. doi: 10.1017/S0031182015001559. doi: 10.1017/S0031182015001559. PURWANINGSIH, M.E. (2015): Parasitic nematodes from turtles: new species and new record from Indonesia. J. Coast. Life Med. 3(8) 607–611. [DOI] [PubMed] [Google Scholar]
  54. A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: 2014. R CORE TEAM. Version 3.4.1 [computer software] [Google Scholar]
  55. Ramos D.G.S., Santos A.R.G.L.O., Freitas L.C., Correa S.H.R., Kempe G.V., Morgado T.O., Aguiar D.M., Wolf R.W., Rossi R.V., Sinkoc A.L., Pacheco R.C.. Endoparasites of wild animals from three biomes in the state of Mato Grosso, Brazil. Arq. Bras. Med. Vet. Zootec. 2016;68:571–578. doi: 10.1590/1678-4162-8157. [DOI] [Google Scholar]
  56. Rizvi A.N., Bursey C.R., Bhutia P.T.. Cosmocerca kalesari sp. nov. (Nematoda, Cosmocercidae) in Euphlyctis cyanophlyctis (Amphibia, Anura) from Kalesar wildlife sanctuary, Haryana, India. Acta Parasitol. 2011;56(2):202–207. doi: 10.2478/s11686-011-0028-8. ROBERTO, I.J., RIBEIRO, S.C., LOEBMAN, D. (2013): Amphibians of the state of Piauí, Northeastern Brazil: a preliminary assessment. Biota Neotrop., 13(1) 322–330. [DOI] [Google Scholar]
  57. Roca V., García G.. A new species of the genus Spiroxys (Nematoda: Gnathostomatidae) from Madagascan pleurodiran turtles (Pelomedusidae) J. Helminthol. 2008;82(4):301–303. doi: 10.1017/S0022149X08996966. [DOI] [PubMed] [Google Scholar]
  58. Rózsa L., Reiczigel J., Majoros G.. Quantifying parasites in samples of hosts. J. Parasitol. 2000;86(2):228–232. doi: 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  59. Ruppert E.E., Barnes R.D. Zoologia dos Invertebrados Invertebrate Zoology. Roca: 1996. p. 1145pp. 6th Edition. In Portuguese. [Google Scholar]
  60. Santos V.G.T., Amato S.B.. Species of Cosmocerca (Nematoda, Cosmocercidae) in anurans from Southern Santa Catarina State, Brazil. Comp. Parasitol. 2013;80(1):123–129. doi: 10.1654/4608.1. [DOI] [Google Scholar]
  61. Schotthoefer A.M., Rohr J.R., Cole R.A., Koehler A.V., Johnson C.M., Johnson L.B., Beasley V.R.. Effects of wetland vs. landscape variables on parasite communities of Rana pipiens links to anthropogenic factors. Ecol. Appl. 2011;21(4):1257–1271. doi: 10.1890/10-0374.1. [DOI] [PubMed] [Google Scholar]
  62. Silva I.C., Lima M.S.C.S., Santos M.C.O., Souza P.S., Pederassi J.. Geographic distribution: Pseudopaludicola pocoto. Herpetol. Rev. 2015;46:213. [Google Scholar]
  63. Silva C.S., Roberto I.J., Ávila R.W., Morais D.H.. New records and geographic distribution map of Pseudopaludicola pocoto (Anura: Leptodactylidae: Leiuperinae) in Northeastern Brazil. Pesq. Ens. Ciênc. Exat. Nat. 2017;2(2):131–135. [Google Scholar]
  64. Sprent J.F.A.. Ascaridoid nematodes of amphibians and reptiles: Multicaecum and Brevimulticaecum. J. Helminthol. 1979;53(1):91–116. doi: 10.1017/s0022149x00005782. [DOI] [PubMed] [Google Scholar]
  65. Teles D.A., Sousa J.G.G., Teixeira A.A.M., Silva M.C., Oliveira R.H., Silva M.R.M., Ávila R.W.. Helminths of the frog Pleurodema diplolister (Anura, Leiuperidae) from the Caatinga in Pernambuco State, Northeast Brazil. Braz. J. Biol. 2015;75(1):251–253. doi: 10.1590/1519-6984.08513. [DOI] [PubMed] [Google Scholar]
  66. Tkach V.V., Kuzmin Y., Snyder S.D.. Molecular insight into systematics, host associations, life cycles and geographic distribution of the nematode family Rhabdiasidae. Int. J. Parasitol. 2014;44(5):273–284. doi: 10.1016/j.ijpara.2013.12.005. [DOI] [PubMed] [Google Scholar]
  67. Travassos L.. Contribuições para o conhecimento da fauna helmintológica dos batráchios do Brasil. Nematódeos intestinais [Contributions to the knowledge of the helminthofauna of the Batráchios from Brazil. Intestinal nematodes] Sci. Med. 1925;3:673–687. (In Portuguese) [Google Scholar]
  68. Travassos L. Introdução ao estudo da helmintologia Introduction to study of helminthology. Instituto Oswaldo Cruz; Rio de Janeiro: 1950. p. 95pp. 1st Edition. In Portuguese. [Google Scholar]
  69. Viana D.C., Rodrigues J.F.M., Madelaire C.B., Santos A.C.G., Sousa A.L.. Nematoda of Kinosternon scorpioides (Testudines: Kinosternidae) from northeast of Brazil. The J. Parasitol. 2016;102(1):165–166. doi: 10.1645/15-788. [DOI] [PubMed] [Google Scholar]
  70. Vicente J.J., Rodrigues H.O., Gomes D.C., Pinto R.M.. Nematóides do Brasil. Parte II: Nematóides de anfíbios Nematodes of Brazil. Part II: Nematodes of amphibians. Revta. Bras. Zool. 1991;7:549–626. In Portuguese) [Google Scholar]
  71. Vicente J.J., Rodrigues H.O., Gomes D.C., Pinto R.M.. Nematóides do Brasil. Parte III: Nematóides de Répteis Nematodes of Brazil. Part III: Nematodes of Reptiles. Rev. Bras. Zool. 1993;10:19–168. [Google Scholar]
  72. Vieira K.R.I., Vicentina A.W., Paiva F., Pozo C.F., Borges F.A., Adriano E.A., Costa F.E.S., Tavares L.E.R.. Brevimulticaecum sp. (Nematoda: Heterocheilidae) larvae parasitic in freshwater fish in the Pantanal wetland, Brazil. Vet. Parasitol. 2010;172(3-4):350–354. doi: 10.1016/j.vetpar.2010.05.003. [DOI] [PubMed] [Google Scholar]
  73. International soil classification system for naming soils and creating legends for soil maps. World soil resources reports N. 106 FAO, Rome. Retrieved March. 2015;07:2017. http://www.fao.org/soils-portal/soil-survey/soil-classification/world-reference-base/en/ WORLD REFERENCE BASE FOR SOIL RESOURCES - IUSS WORKING GROUP WRB. from. [Google Scholar]
  74. Yamaguti S. Systema Helminthum – Vol. III Nematodes Interscience (Wiley) ondon: 1961. p. 1261. [Google Scholar]

Articles from Helminthologia are provided here courtesy of De Gruyter

RESOURCES