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Diet and Parasites of the Anuran Physalaemus Cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest Fragment

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Diet and Parasites of the Anuran Physalaemus Cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest Fragment Herpetology Notes, volume 11: 109-113 (2018) (published online on 27 January 2018) Diet and parasites of the anuran Physalaemus 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 habitat 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).
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