ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

ORIGINAL ARTICLE /ARTÍCULO ORIGINAL COMMUNITY STRUCTURE OF PARASITES OF THE TREE FUSCOVARIUS (ANURA, ) FROM CAMPO BELO DO SUL, SANTA CATARINA, BRAZIL

ESTRUCTURA DE LA COMUNIDAD PARASITARIA DE LA RANA ARBORICOLA (ANURA, HYLIDAE) DE CAMPO BELO DO SUL, SANTA CATARINA, BRASIL

Viviane Gularte Tavares dos Santos1,2; Márcio Borges-Martins1,3 & Suzana B. Amato1,2

1 Departamento de Zoologia, Programa de Pós-graduação em Biologia , Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, 91501-970, Rio Grande do Sul, Brasil. 2 Laboratório de Helmintologia; Universidade Federal do Rio Grande do Sul, Porto Alegre, 91501-970, Rio Grande do Sul, Brasil. 3 Laboratório de Herpetologia. Universidade Federal do Rio Grande do Sul, Porto Alegre, 91501-970, Rio Grande do Sul, Brasil. E-mail: [email protected]; [email protected]; [email protected]

Neotropical Helminthology, 2016, 10(1), ene-jun: 41-50.

ABSTRACT

Sixty specimens of Scinax fuscovarius (Lutz, 1925) were collected between May 2009 and October 2011 at Campo Belo do Sul, State of Santa Catarina, Brazil, and necropsied in search of helminth parasites. Only four helminth species were found: Pseudoacanthocephalus sp. Petrochenko, 1958, Cosmocerca brasiliense Travassos, 1925, C. parva Travassos, 1925 and Physaloptera sp. Rudolphi, 1819 (larvae). The genus of the female cosmocercids could not be determined. Only 30% of the anurans were parasitized. Scinax fuscovarius presented low prevalence, infection intensity, and parasite richness. Sex and size of S. fuscovarius individuals did not influence the prevalence, abundance, and species richness of helminth parasites.

Keywords: Acanthocephala - anurans - helminth parasites - hylids - Nematoda - tree

RESUMEN

Sesenta ejemplares de Scinax fuscovarius (Lutz, 1925) fueron colectados entre mayo de 2009 y octubre de 2011 en Campo Belo do Sul, Estado de Santa Catarina, Brasil y necropsiados para el estudio de sus helmintos parásitos. Fueron halladas solamente cuatro especies de helmintos: Pseudoacanthocephalus sp. Petrochenko, 1958, Cosmocerca brasiliense Travassos, 1925, C. parva Travassos, 1925 and Physaloptera sp. Rudolphi, 1819. Las hembras de cosmocércidos no pudieron ser determinadas debido a la falta de caracteres taxonómicos. Solamente el 30% de los anuros estuvieron parasitados. Scinax fuscovarius presentó baja prevalencia, intensidad de infección y riqueza parasitaria. El sexo y el tamaño de S. fuscovarius no influyeron en la prevalencia, abundancia y riqueza de especies de helmintos parásitos.

Palabras clave: Acanthocephala – anuros - helmintos parásitos – hílidos – Nematoda – rana arborícola

41 Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Santos et al.

INTRODUCTION research and showing that the parasite richness is higher than that cited by Aho (1990).

There are a few factors, such as host habit and Scinax fuscovarius (Lutz, 1925) occurs from diet that may influence parasite community south to southern Brazil and eastern Argentina, structure. Anurans are a much diversified Paraguay and Bolivia. It is found in open areas group of vertebrates with 7300 extant species such as pastures. At night during the which can be fossorial, arboreal, terrestrial, reproduction season they are found in still semi-aquatic or aquatic (Duellman & Trueb, water (lakes, ponds and wetlands), while at 1994; Frost, 2014). Aho (1990) observed that other periods they take refuge in trees. The semi-aquatic anurans had a tendency to present tadpoles are nektonic and feed on suspended greater helminth richness; terrestrial and matter. As adults, males measure from 37 to 47 aquatic anurans presented intermediate and mm, and females from 42 to 48 mm (Kwet & similar values, while fossorial and arboreal Di-Bernardo, 1999; Kwet et al., 2010). This anurans presented lower helminth richness. species is very abundant in several areas of southern Brazil, nevertheless, little is known There are some studies on anurans that about its parasite community structure. Being demonstrate a positive relationship between an arboreal species, S. fuscovarius is a good the host and the variability of the model to analyze if arboreal frogs have lower parasite community structure (Hamann & helminth richness as proposed by Aho (1990). Kehr, 1998; Bolek & Coggins, 2000; Muzzal et al., 2001; Bursey et al., 2001; Iannacone, This study aimed to: identify the helminth 2003; León-Règagnon et al., 2005; Luque et parasites of S. fuscovarius; analyze the parasite al., 2005; Brooks et al., 2006; Goldberg et al., community structure; and increase the 2007; González & Hamann, 2008; González, knowledge of the biology of these species with 2009; Santos & Amato, 2010; Hamann et al., parasitological data. 2010; Campião et al., 2010; Santos et al., 2013). Aquatic and/or semi-aquatic anurans tend to present a greater number of digenean MATERIAL AND METHODS species, because most of the anuran digeneans use aquatic or semi-aquatic arthropods as secondary intermediate hosts (Prudhoe & Sixty S. fuscovarius specimens (28 females, 31 Bray, 1982). males, one specimen with undetermined sex), were captured under license SISBIO (Number The diversity of parasite communities of the 026/2006), between June 2009 and December Neotropical anurans is unknown. Since this 2011, at the Municipality of Campo Belo do region concentrates the largest number of Sul (27°59' 42.19”S, 50°53'27.92”W, ranges global anuran richness, an adequate between 700-900 m.a.s.l), located in the description of their parasite diversity is Araucarias Plateau Region of the State of important to better understand some patterns Santa Catarina, southern Brazil. that are not well defined. Luque et al. (2005), Santos & Amato (2010), Santos et al. (2013) The specimens were manually collected and and Chero et al. (2014) presented results of sacrificed with lidocaine Geyer® 2% (local recent studies on Rhinella icterica (Spix, anesthetic), spread on the abdomen of the 1824), Rhinella fernandezae Gallardo, 1957 animal and absorbed by the skin; they were and Telmatobius jelskii (Peters, 1863) weighed and measured (snout-cloacal length). demonstrating the contribution of this kind of The sex of the host was identified through the

42 Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Parasite of the tree frog Scinax fuscovarius

coloration of the vocal sac (dark in males) and vouchered at the Helminthological Collection gonad examination of juveniles. of Instituto Oswaldo Cruz (CHIOC), FIOCRUZ, Rio de Janeiro, Rio de Janeiro Helminths were collected and placed in State, Brazil. All hosts examined were physiological saline solution 0.65%; they were vouchered at the Collection, fixed, stained and/or diaphanized following H e r p e t o l o g y L a b o r a t o r y, Z o o l o g y Amato & Amato (2010). The morphologic and Department, Universidade Federal do Rio biometric study was performed using an Grande do Sul, Porto Alegre, Rio Grande do Axiolab Zeiss microscope. The ecological Sul, Brazil. descriptors, prevalence, infection intensity, parasite abundance and richness followed Bush et al. (1997). RESULTS

Statistical analysis included only the parasite A total of 35 helminths, representing an species with prevalence greater than 10% average intensity of infection of 0.6 helminths / (Bush et al., 1997). The Mann-Whitney "U" host, were collected. Only acanthocephalans test was calculated to evaluate if the sex of the and nematodes were found (Table 1). The host was influenced by parasite abundance and parasite community was composed of four richness. Fisher's exact test was used to helminth species, Pseudoacanthocephalus sp., evaluate if the host's sex and size influenced Cosmocerca parva Travassos, 1925 and parasite prevalence. To evaluate if host size Cosmocerca brasiliense Travassos, 1925, and could influence the prevalence of helminth one species was represented by only a larval species, anurans were categorized as small or form, Physaloptera sp. Due to the lack of large frogs. t a x o n o m i c c h a r a c t e r s t h e f e m a l e Cosmocercidae Railliet, 1916 could not be

The Spearman correlation coefficient (rs) determined to genus and species. evaluated the influence of size on the parasite Acanthocephalans were not determined to the abundance and richness of the analyzed specific level because no males were found. helminth hosts. The Berger-Parker index (d) Besides the characteristics of the proboscis, it was used with a numerical measure of is necessary to observe the morphology and the dominance (Nering & Von Zuden, 2010). The n u m b e r o f c e m e n t g l a n d s o f representativity of helminth species richness Pseudoacanthocephalus species. found was analyzed with the program EstimateS 8.0 (Colwell, 2009) through the Of the 60 anurans collected, only 18 were collectors curve and the Chao 1 Index and ACE infected with parasite species. Nematodes ("Abundance-based Coverage Estimator"), accounted for 80% of the sample (three estimators based on abundance that quantify species), and 20% were represented by one rarity, and estimators based on incidence, ICE acanthocephalan species. A total of 23 ("Incidence Coverage Estimator-based") and nematodes and 12 acanthocephalans were Jackknife. Female Cosmocercidae were not collected. The nematodes infected 15 hosts considered in the species richness while acanthocephalans infected only three representativity analysis since these specimens hosts. did not show diagnostic characters that allow separation between Cosmocerca and Only Cosmocercidae females showed Aplectana. prevalence greater than 10% and were the dominant parasites (d = 0.47) of the sample. Representative helminth specimens were There was no influence of the sex of the host on

43 Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Santos et al.

the prevalence (p = 0.30), abundance (“U” = The collector curve (SOBs) did not reach the 372; p = 0.34) and parasite richness (“U” = asymptote; on the other hand, the estimators 436; p = 0.85), and the host size did not used ACE, ICE, Chao 1 and Jacknife reached influence the prevalence (p = 0.49), abundance stability (Figure 1), which indicates that 80%

(rs = 0.14; p = 0.27) and parasite richness (rs= to 100% of helminth species were sampled in 0.17; p = 0.19). this study.

8

7

6

5 Sobs 4 ACE Species richness 3 Chao 1 ICE 2 Jacknife 1

0 1 2 3 4 5 6 7 8 Number of hosts

Figure 1. Accumulated richness observed (SOBs) and estimated (ACE, Chao 1, ICE and Jacknife) of the helminth community of Scinax fuscovarius, Campo Belo do Sul, State of Santa Catarina, Brazil.

Table 1. Prevalence, intensity, mean intensity, mean abundance and infection site of parasite helminths of Scinax fuscovarius (n = 60), Campo Belo do Sul, State of Santa Catarina, Brazil.

Mean Mean Parasites Prevalence Intensity Infection site intensity abundance (%) ±SD ±SD Acanthocephala Pseudoacanthocephalus sp. 5 1 to 8 4,00 ± 3,61 0,2 ± 1,10 Small intestine CHIOC 38283; 38284 Nematoda Small/large Cosmocercidae 16,6 1 to 2 1,80 ± 1,87 0,3 ± 1,00 intestine CHIOC 38157 Small/large Cosmocerca parva 2 1 1 0,03 ± 0,18 intestine CHIOC 38158 Small/large Cosmocerca brasiliense 2 1 1 0,03 ± 0,18 intestine CHIOC 38159 Physaloptera sp. (larvae) 1,66 1 1 0,02 ± 0,13 Stomach CHIOC 38160 CHIOC = Helminth Collection of Instituto Oswaldo Cruz, with the numbers of representative specimens.

44 Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Parasite of the tree frog Scinax fuscovarius

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45 Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Santos et al.

DISCUSSION prevalence. In this study, the three parasite species (C. Analysis showed that S. fuscovarius had low brasiliense, C. parva and Physaloptera sp.) parasite richness, which is probably related to showed low prevalence and infection intensity. the species' habitat. The nematodes found On hylids the low vagility and the arboreal showed low prevalence and low infection habit probably contributes to a low infection intensities, and most hosts were parasitized occurrence by nematodes with cutaneous with only one helminth species. penetration (Hamann et al., 2010).

The parasite richness of S. fuscovarius is The genus Pseudoacanthocephalus different from those found in Rhinella icterica Petrochenko,1956 includes only parasite (Spix, 1824) (Santos et al., 2013), species of and reptiles. In South Leptodactylus latrans (Steffen, 1815) and A m e r i c a , t h e r e a r e r e c o r d s o f Physalaemus cuvieri Fitzinger, 1826, Pseudoacanthocephalus lutzi (Hamann, 1891) collected on the same area (Table 2); all four (= Acanthocephalus lutzi (Hamann, 1891); = species have distinct habits. However, the Acanthocephalus saopaulensis Smales, 2007) result obtained in this study corroborates in Brazil (Hartwich, 1956; Pinhão et al., 2009), Hamann & Kehr (1998), Bursey et al. (2001), Argentina (Lajmanovich & Ferrato, 1995), Goldberg et al. (2002) and González & Peru (Tantaléan, 1976), Uruguay (Cordero, Hamann (2008), which also found low values 1933; Hartwich, 1956) and Paraguay (Smales, of parasite richness on hylid anurans of South 2007). The infection by this acanthocephalan America. occurs by the ingestion of an arthropod; Arredondo & Pertierra (2009) suggest that The nematode species C. parva and C. aquatic insects are the intermediate hosts of P. brasiliense found in this study have direct lutzi. cycles (monoxenous) and infect their hosts through cutaneous penetration. Species of Hamann et al. (2010) analyzed the parasite Physaloptera have an indirect cycle community structure of from (heteroxenous) and are commonly found in Corrientes, Argentina, and found that this host anurans which, according to Anderson (2000), had high richness of helminth parasite species, act as paratenic hosts for Physaloptera species, with 21 species. However, only seven species while lizards, snakes and mammals act as were adult forms while the others were larval definitive hosts. forms. The results observed by these authors demonstrate the important role that this anuran According to Bursey et al. (2001), C. species plays in the food chain, occupying an brasiliense is the most common and greater intermediate position between the parasite and prevalence parasite species found on arboreal its definitive hosts (snakes, birds and anurans. Goldberg et al. (2007) working in the mammals). State of Pará, Brazil found low prevalence (10%) and an intensity equal to 1 for the Usually, the sex of the anuran does not parasite C. brasiliense in the species influence the structure of the parasite Dendropsophus cachimbo (Napoli and community, once they are evenly distributed Caramashi, 1999). González & Hamann between males and females. This pattern was (2008) found C. parva and Physaloptera sp. found on S. fuscovarius in which sex did not (larval form) in at influence the parasite richness, the helminth Corrientes, Argentina, which also showed low prevalence and abundance. This result

46 Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Parasite of the tree frog Scinax fuscovarius

corroborates other studies (Yoder & Coggins, Etiele Senna. To “Florestal Gateados” for 1996; McAlpine, 1997; Barton, 1999; allowing the collection of specimens on their Goldberg et al., 2002; Hamann et al., 2006a,b; property. Phillip J. Scholl for kindly reviewing Santos & Amato, 2010; Santos et al., 2013). the English version. To CAPES for the scholarship granted to the first author. To On the other hand, some authors suggest that FAPERGS for the financial support granted to the host size influences the parasite richness this research. and the helminth prevalence and abundance (Baker, 1984; McAlpine, 1997; Gillilland & Muzzall, 1999; Bolek & Coggins, 2003; Chero BIBLIOGRAPHIC REFERENCES et al., 2016). In this study, however, this correlation was not observed, since size did not influence the parasite community structure of Aho, J.M. 1990. Helminth communities of S. fuscovarius, this result corroborates with amphibians and reptiles: comparative Chero et al. (2014). This result may indicate approaches to understanding patterns that, regardless of size, all individuals are and processes. In: Esch GW, Bush, AO, susceptible to infection by Cosmocercidae. Aho, JM (eds.) Parasite communities: patterns and processes, Chapman and The estimators did not reach an asymptote and Hall, London. pp.157-190. this result may be related to the low number of Amato, JFR & Amato SB. 2010. Técnicas infected anurans, but the estimated values did gerais para coleta e preparação de not extrapolate and remained close to helmintos endoparasitos de aves. In: Von observed. The parasite richness of S. Matter, S, Straube, FC, Accordi, I, fuscovarius is, probably, between four and five Piacentini, V, Cândido-Jr. JF (eds). species. Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e The results obtained in this study was Levantamento, Technical Books corroborated by Hamann et al. (2010) who Editora, Rio de Janeiro, 518pp. suggested that the sit-and-wait strategy and the Anderson, RC. 2000. Nematode Parasites of particular diet of these anurans are determining Vertebrates. Their Development and factors for the low parasite richness found. The Transmission. 2nd Ed. CABI Publishing, limited movement and the arboreal habit of Wallingford, Oxon (UK). 650 pp. this species also contribute to the low Arredondo, NJ & Pertierra AAG. 2009. occurrence of nematodes that parasitize Pseudoacanthocephalus lutzi (Hamann, anurans through cutaneous penetration. The 1891) comb.n. (Acanthocephala: absence of digenetic is probably related to the E c h i n o r h y n c h i d a e ) f o r little contact of these anurans with the aquatic Acanthocephalus lutzi (Hamann, 1891), environment. parasite of South American amphibians. Folia Parasitologica, vol.56, pp. 295- 304. ACKNOWLEDGEMENTS Baker, MR. 1984. Nematode parasitism in amphibian and reptiles. Canadian Journal of Zoology, vol. 62, pp. 747-757. Authors would like to thank the herpetologists Barton, DP. 1999. Ecology of helminth Rafael Balestrin, Patrick Colombo, Martin communities in tropical Australian Schossler, Daniel Bühler and Simoni Leonardi Amphibians. International Journal for for field assistence, and to Mariana Gliesh and Parasitology, vol. 29, pp. 921-926.

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