Herpetology Notes, volume 11: 109-113 (2018) (published online on 27 January 2018)

Diet and parasites of the anuran cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest fragment

Peterson T. Leivas1,*, Fernando W. T. Leivas2 and Karla Campião1

Abstract. Anurans fit an important trophic position in ecosystems because they are both predators and prey of many invertebrate and vertebrate organisms. Here, we describe the diet and parasites associated with Physalaemus cuvieri Fitzinger, 1826 in disturbed areas within the Ombrophylous Forest, in the Atlantic Forest, Brazil. We collected 56 anuran specimens, and found preys of the Phylum Arthropoda, belonging to Insecta (85.7%) and Arachnida (14.3%). Among the Insecta, Isoptera had the highest frequency in the diet, followed by Hymenoptera, Hemiptera and Coleoptera. For Arachnida, Araneae had greatest percentage of occurrence in the diet followed by Acari. Among anuran specimens, 93% were infected by parasite belonging to seven helminth taxa, two of them acanthocephalans, and five nematodes. Overall, our results showed that P. cuvieri feeds mainly on insects (Isoptera, Hymenoptera, Coleoptera and Hemiptera), and has high prevalence of nematodes and acanthocephalans. These results point to the terrestrial of this anuran, once terrestrial insects were the main food items, and the directly transmitted nematodes are acquired through the soil. The diet in turn, influenced the acquisition of acanthocephalans, which have indirect life cycle and were transmitted by the ingestion of insects.

Key words: Amphibia, Brazil, Helminth, Parasite, Acanthocephala

Introduction and its prey and predators (Marcogliese, 2004; Dobson et al., 2008). Therefore, parasites provide complementary Anurans fit an important trophic position in terrestrial information on species dietary habits, in addition to that and aquatic ecosystems. They are predators and control obtained through stomach content analysis. Information populations of many invertebrate species, and are on parasite infection can indicate whether the studied also prey to many vertebrate and some invertebrate species feed on or is preyed by more than one trophic organisms (Toledo et al., 2007; Wells, 2007). In this level, and reveal individual feeding specializations sense, information on feeding habits and parasite infection are important functional facets of anuran within a population (Marcogliese, 2004). biodiversity, and may potentially aid to revealing how Physalaemus cuvieri Fitzinger, 1826 is an abundant each species interacts with its environment. anuran throughout its wide geographical range, which Many parasites are transmitted via predator- covers areas with an altitude of over 2,000 m between prey interactions and use different intermediate the north of’ South America in Brazil to Uruguay and hosts, representing excellent indicators of host diet Missiones in Argentina (Frost, 2017). It occurs over open (Marcogliese, 2004). In these cases, the occurrence of a fields, natural and anthropized areas, and reproduces in parasite in a host reflects interactions between the host temporary and permanent ponds (Haddad et al., 2013). Here, we describe the diet and parasites associated with P. cuvieri in disturbed areas within the Araucaria Forest, in the Atlantic Forest, Paraná, Brazil.

1 Universidade Federal do Paraná (UFPR), Centro Politécnico, Departamento de Zoologia. End. Av. Coronel Francisco Material and Methods Heráclito dos Santos, 210 - Jardim das Americas, Curitiba Anurans were collected in a natural area with anthropic - PR, CEP: 81531-970 - Caixa postal 19020. interference in Campina Grande do Sul, state of Paraná, 2 Universidade Federal do Paraná (UFPR), Departamento de Biodiversidade. Rua Pioneiro, 2153, Jardim Dallas, Palotina, Brazil (25º17’09”S e 49º00’05”W). The vegetation is PR, CEP 85950-000. mixed mountainous ombrophilous forest (Araucaria * Corresponding author. E-mail: [email protected] Forest) and the climate is subtropical Cfb following 110 Peterson T. Leivas et al.

Table 1. Prey items found in the diet of Physalaemus cuvieri in Campina Grande do Sul, State of Paraná, Brazil. (ON) number of each item occurred1 in diet;Table (PO%) 1. Prey itemspercentage found in ofthe occurrencediet of Physalaemus of the cuvieri class/subclass/order in Campina Grande in do the Sul, diet; State (POF%)of Paraná, percentage of occurrence of families2 in each highBrazil. taxa. (ON) number of each item occurred in diet; (PO%) percentage of occurrence of the orders in 3 the diet; (POF%) percentage of occurrence of families in each order. 4 Class/Subclass/Order Family ON PO% POF% Insecta 66 85.7 Isoptera 51 77.3 Hymenoptera 10 15.1 Formicidae 100 Coleoptera 4 6.1 Curculionidae 25 NI 75 Hemiptera 1 1.5 Tingidae 100 Arachnida 11 14.3 Araneae 9 81.8 Acari 2 18.2 5 6 7 8 9 10 Table 2. Parasites found in Physalaemus cuvieri in Campina Grande do Sul, State of Paraná, Brazil. Koppen’s classification11 (Alvares et al., 2013). The of parasite infection followed Bush et al. (1997), where sampling sites, at an approximateParasite taxa altitude of 918 m, parasitePrevalence prevalence (%) Meanrepresents Intensity the ± SDproportion of infected comprehend two permanentAcanthocephala ponds with vegetation. hosts in the population and mean intensity of infection is Collections were conductedAcanthocephalus in November saopaulensis 2015,Smales, 2007the number 28.6 of parasites 3in.7 ±each 4.3 infected host, all given during the night, with samplingCentrorhynchidae effort (cystacanths) of five hours, with mean42.8 and standard 2.8deviation. ± 1.7 using visual encounter basedNematoda on auditory search (Crump Aplectana sp. 10.7 2.8 ± 2.4 and Scoot, 1994). After the capture, specimens were Cosmocerca parva Travassos, 1925 Results 30.3 2.9 ± 3.2 immediately transported to the laboratory, where they Cosmocercidae We collected37.5 56 specimens2.4 ± 1.5 of P. cuvieri. Among the were euthanised accordingOswaldocruzia to the current lopesi legislation Travassos, 1938 at 19.6 3.1 ± 5.9 stomachs examined, 40% (n = 22) contained 1-16 items, the Conselho Federal de BiologiaRhabdias (CFBIOsp. - Resolution 7.01 1.6 ± 0.5 308). Voucher specimens12 were deposited at the Museu and 60% (n = 34) were empty. The diet of the species de História Natural do Capão da Imbuia, Curitiba, comprised preys of Arthropoda (PO=94%), belonging Paraná, Brazil. to Insecta and Arachnida (Table 1). Unidentified preys In laboratory, specimens were necropsied and had represented 6% of the diet. Insecta had the highest their stomach and intestine of each individual removed contribution in the diet, representing 85.7% of prey (Leivas et al., 2012). All organs, including the body and Arachnida represented 14.3% of prey items. To cavity, digestive tract, lungs, kidneys, and musculature Insecta, Isoptera had a highest importance (PO% = were also examined for helminth parasites. We then 77.3), followed by Hymenoptera (PO% = 15.12), quantified and identified all preys and all parasites to Coleoptera (PO% = 6.1) and Hemiptera (PO% = 1.5). the lowest taxonomic level possible. For identification, To Arachnida, Araneae had highest contribution in the nematodes were fixed in hot alcohol-formaldehyde- diet (PO% = 81.8) followed by Acari (PO% = 18.2) acetic acid (AFA) and acanthocephalans were (Table 1). Among the Coleoptera, Curculionidae had maintained in cold water until proboscis eversion and higher percentage of occurrence. Only Formicidae1 was then fixed in cold AFA. All helminths were preserved in predated in the order Hymenoptera, and Tingidae in the 70% ethyl alcohol. For identification, acanthocephalans order Hemiptera (Table 1). were stained with carmine and cleared with eugenol, Among these anurans specimens, 93% were infected while nematodes were cleared with lactophenol. by at least one parasite taxa. They were associated with In order to infer the contribution of the various seven helminth taxa, two of them acanthocephalans, food items (taxons) to the diet of the population, we and five nematodes (Table 2). Acanthocephalans were calculated the percentage of occurrence (PO%) of each the most frequent parasites in P. cuvieri, especially item. We also calculated the percentage of occurrence of considering those in larval stage (cystacanths). families in each order (Leivas et al., 2012). Descriptors Nematodes were also frequent, and among them, those 1 Table 1. Prey items found in the diet of Physalaemus cuvieri in Campina Grande do Sul, State of Paraná, 2 Brazil. (ON) number of each item occurred in diet; (PO%) percentage of occurrence of the orders in 3 the diet; (POF%) percentage of occurrence of families in each order. 4 Class/Subclass/Order Family ON PO% POF% Insecta 66 85.7 Isoptera 51 77.3 Hymenoptera 10 15.1 Formicidae 100 Coleoptera 4 6.1 Curculionidae 25 NI 75 Hemiptera 1 1.5 Tingidae 100 Arachnida 11 14.3 Araneae 9 81.8 Acari 2 18.2 5 Diet and parasites6 of the anuran Physalaemus cuvieri from a forest fragment 111 7 8 Table 2. Parasites found9 in Physalaemus cuvieri in Campina Grande do Sul, State of Paraná, Brazil. 10 Table 2. Parasites found in Physalaemus cuvieri in Campina Grande do Sul, State of Paraná, Brazil. 11 Parasite taxa Prevalence (%) Mean Intensity ± SD Acanthocephala Acanthocephalus saopaulensis Smales, 2007 28.6 3.7 ± 4.3 Centrorhynchidae (cystacanths) 42.8 2.8 ± 1.7 Nematoda Aplectana sp. 10.7 2.8 ± 2.4 Cosmocerca parva Travassos, 1925 30.3 2.9 ± 3.2 Cosmocercidae 37.5 2.4 ± 1.5 Oswaldocruzia lopesi Travassos, 1938 19.6 3.1 ± 5.9 Rhabdias sp. 7.01 1.6 ± 0.5 12

belonging to the family Cosmocercidade had the highest as ants and termites. The predominance of Isoptera prevalences and intensities of infection. Cosmocercidae and Hymenoptera we report here corroborates this includes both the Aplectana and Cosmocerca species, classification and, some differences observed in the diet and individuals that were identified only to family level are probably reflecting the availability and abundance are females, which cannot be identified to more accurate of Isoptera e Hymenoptera (Formicidae) in the studied taxonomic levels based solely on their morphology area (Falico et al., 2012). (Table 2). Similar to the generalism in the diet, all parasites found in P. cuvieri are generalists, being reported for several other anuran species (Campião et al., 2014a). Toledo et Discussion 1 al. (2013) and Aguiar et al. (2015) described the helminth Our results showed that P. cuvieri is a forager that fauna parasitizing P. cuvieri from southeastern Brazil. feeds on various groups of prey, but predominantly Although some parasite species co-occurred, these on insects, and have high prevalence and intensity of studies describe a different parasite community in terms parasite infection. Considering other studies about the of intensities of infection, indicating some geographical trophic interactions of this anuran, the results indicate variation in parasite community composition for this host that both the diet and parasites of P. cuvieri vary little species. As in this study, Aguiar et al. (2015) report the along its distributional range (Toledo et al., 2013, infection of Aplectana sp., C. parva, and A. saopaulensis, Oliveira et al., 2015; Aguiar et al., 2015). Therefore, but all these occurred in higher prevalence and intensity the foraging behaviour of P. cuvieri seems to reflect of infection in this study. Indeed, parasite communities local resource availability, indicating local interactions are acquired from the local pool of parasites, and may between prey and predator, as well as the role of this vary along the geographical distribution of the host anuran as a resource for parasites. (Poulin, 2003; Campião et al., 2014b). Moreover, the The prey items in the diet of P. cuvieri reported here higher prevalence and intensity of parasite infection includes preys of different sizes (ex. Coleoptera e Acari) observed here might be related to the high anthropogenic and movement abilities (ex. Araneae e Isoptera). Theses influence in the study area (Schotthoefer et al., 2011). results agree with the opportunistic and “sit-and-wait Our results indicate high success of parasites transmitted feeding strategy” reported for the specie (Toledo et both directly and trophically. All nematode species al., 2007). Physalaemus cuvieri preyed on arthropods, reported here have direct life cycle and are acquired predominantly Insecta (Hymenoptera: Formicidae and through the contact with soil, by skin penetration of the Isoptera) and Arachnida (Araneae and Acari), which infective larvae (Anderson, 2000). On the other hand, seems to be a pattern in the diet of this and other species the high prevalence of acanthocephalans indicates that of Physalaemus in Brazil (Santos et al., 2004; Oliveira the feeding habits of P. cuvieri are contributing to the et al., 2015; Menin, et al., 2015; Moser et al., 2017). acquisition of these parasites. Acanthocephalans have Particularly, P. cuvieri is known as an “ant-specialist” complex life cycles, which include an invertebrate (Toft, 1980), because individuals tend to have a high intermediate host, a vertebrate definitive host, and may predation rate of organisms with terrestrial habits such include paratenic (facultative) host (Kennedy, 2006). 112 Peterson T. Leivas et al.

Physalaemus cuvieri is acting as a definitive host for A. Campião, K.M., Morais, D.H., Dias, O.T., Aguiar, A., Toledo, G., saopaulensis, which were found in adult stages in the Tavares, L.E.R., da Silva, R.J. (2014a): Checklist of Helminth intestines. A different morphotype of acanthocephalan parasites of from South America. Zootaxa 30:3843(1):1-93. was also found as cystacanths within the stomach Campião, K.M., Ferreira, V.L., da Silva, R. J (2014b): Helminth musculature and in the mesentery. These larval stages parasite communities of allopatric populations of the could not be identified to more precise taxonomic level Leptodactylus podicipinus from Pantanal, Brazil. Journal of due to the lack of morphological features. However, its Helminthology 88: 13-19. occurrence indicates that P. cuvieri is either intermediate Crump, M.L., Scott Jr., N.J. (1994): Visual encounter surveys. or paratenic host to these parasites. 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Accepted by Mirco Solé