Herpetology Notes, volume 13: 271-279 (2020) (published online on 19 March 2020) Predation and parasitism on bromeligenous Snouted Treefrogs (Ololygon spp.) Leandro Talione Sabagh1,2,*, Gustavo Cauê de Oliveira Piccoli3, Lucio André Viana4, and Carlos Frederico Duarte Rocha2 Abstract. Among the hypotheses as an advantage for the use of bromeliads by frogs both as refuge and breeding site, is that these plants would constitute a “safe place” and/or a “predator-free environment”. Here we present some new records of antagonistic interactions involving bromeligenous Snouted Treefrog species of the genus Ololygon in a coastal Brazilian Rainforest. We report records of predation on Ololygon spp. tadpoles by damselfly larvae (Leptagrion) and by the spider Corinna demersa, and also predation on adults of the frog by a snake (Bothrops jararaca) and spiders. We also report the occurrence of parasitism of O. perpusilla adults by ticks (Ornithodorus sp.) and the register of a protozoan parasite (Isospora cruzi) in O. littorea faeces. We conclude that aside from the advantages for bromeligenous treefrogs to live in the bromeliads, living inside these plants does not result in a habitat free of predation and parasitism. Just as bromeligenous frogs evolved in association with bromeliads, so can other groups like predators and parasites. We still need consistent data on both predation and parasitism to better allow to infer to what extent bromeliads habitats are or not more or less safe for bromeligenous and/or bromelicolous amphibians. Keywords. Bromeliaceae, coccidia, damselfly larvae, Hylidae, spider predation, snake predation, tick Introduction advantage as low predation on tadpoles by invertebrates and by fishes (Hero et al., 1998, 2001; Summers and Frog species from distinct families (e.g., Hylidae, McKeon, 2004). Bufonidae, Cycloramphidae) seem to have independently Many members of Bromeliaceae having water storage evolved traits that allow them to occur in bromeliads. capacity play an important ecological role in certain In Neotropical region, bromeliads are a conspicuous habitats, functionally acting as ponds or islands for phytotelmata which can store from a few milliliters different aquatic and/or semi-aquatic organisms (Frank up to 20L of water (Benzing, 1980). Previous studies and Lounibos, 1987; Itescu, 2019). This water supply hypothesized that frogs that change their breeding site provided by tank-bromeliads generates a comparatively from ponds and streams to phytotelmata may take milder climate than the surroundings (Dias and Brescovit, 2004) creating an important microhabitat required by many species. Thus, terrestrial organisms also tend to associate with bromeliads to benefit from shelter (mainly in arid or in water-restricted 1 Departamento de Ecologia, Universidade Federal do Rio de environments), and as foraging site, since in bromeliads Janeiro, Avenida Carlos Chagas 373, Prédio CCS – Bloco there is a convergence of many organisms (Dias and A, Sala A1-08, Rio de Janeiro, Rio de Janeiro 21941-902, Brazil. Brescovit, 2004; Silva et al., 2011; Sabagh 2014; Piccoli 2 Departamento de Ecologia, Universidade do Estado do Rio de 2015). Such characteristics tend to attract diverse Janeiro, Rua São Francisco Xavier 524, Rio de Janeiro, Rio kinds of animals among vertebrates and invertebrates de Janeiro 20550-013, Brazil. (Kitching, 2001; Rocha et al., 2004). Many invertebrates 3 Departamento de Biologia Animal, Universidade Estadual de previously recorded as anurans predators are common Campinas, Campinas, São Paulo 13083-970, Brazil. bromeliads inhabitants, such as spiders (Menin et al., 4 Departamento de Ciências Biológicas e da Saúde, 2005), centipedes (Forti et al., 2007), damselfly larvae Universidade Federal do Amapá, Rodovia Juscelino Kubitschek - Km 2, Jardim Marco Zero, Macapá, Amapá (Heyer et al., 1975; Junior and Furieri, 2000), ostracods 68903-419, Brazil. (Müller, 1879; Gray et al., 2010), larvae and adults of * Corresponding author. E-mail: [email protected] water beetles (Oliveira et al., 2013; Gambale et al., 272 Leandro Talione Sabagh et al. 2014), and leeches (Gambale et al., 2014; Silva et al., during extensive field research (2008–2013). 2018). Some vertebrates known as anurans’ predator are Field and laboratory observations for terrestrial also found in bromeliad habitat (Rocha and Vrcibradic, predators.—In Sugar Loaf we record the predation 1998). These predators can feed on tadpoles, adult frogs, of O. perpusilla by a juvenile of Bothrops jararaca or eggs. (Viperidae) juvenile that was foraging on A. glaziouana. The Ololygon “perpusilla” group includes small In Cardoso Island we also recorded occurrence of treefrogs, whose all life cycle occurs inside bromeliads Bothrops spp. upon bromeliads (Q. arvensis). (Peixoto, 1995). This group is endemic to the Brazilian In Cardoso Island we conducted laboratorial Atlantic Forest. Specifically, we recorded data on experiments (assays) in order to assess potential antagonistic relationships involving bromeligenous predation behaviour of the bromeliad-dweller spider Ololygon perpusilla (Lutz and Lutz, 1939), Ololygon Corinna demersa (Corinnidae) on tadpoles and adults littorea Peixoto, 1988, and an unnamed Ololygon of Ololygon sp. We conducted trials to evaluate the species from two Inselbergs areas in Rio de Janeiro and potential of the spider C. demersa preying on the frog one ‘restinga’ area in the south coast of São Paulo State, for feeding purposes. In each assay we placed together southeastern Brazil. We took new records of predation on a small bromeliad (having inside its axial some on bromeligenous tadpoles by damselfly larvae and by dead leaves and water to better simulate the natural spiders and predation on frog adults by a snake species bromeliad environment) adult females of the spider and by spiders. In addition, we report new events with individuals of Ololygon sp. (both adults and of parasitism for bromeligenous frogs by ticks and tadpoles) inside plastic vials, closing the vial opening intestinal protozoans. using a mesh to prevent animals to escape. We made 10 replicates of the experiment using only tadpoles and six Materials and Methods using only adult frogs as potential prey. Study sites.—Field sampling was carried out in We daily observed the recipients in order to see any two coastal Inselberg areas in Rio de Janeiro State, predation event and made a final inspection after five southeastern Brazil: at the Natural Monument of days, registering the final condition: adult or tadpole Sugar Loaf (Monumento Natural do Pão-de-Açúcar) still alive, dead or not present – which we assumed (22.9510ºS, 43.1515ºW), and at Costão de Itacoatiara as ingestion after predation by the spider. In addition, (22.9786ºS, 43.0274ºW), State Park of Serra da Tiririca to observe the steps involved in the spider behaviour (Parque Estadual da Serra da Tiririca). The vegetation during predation on tadpoles we made additional assay in both inselbergs is mainly composed by saxicolous in falcon tubes (80 ml) having 50 ml of a mix of water herbaceous plants and bromeliads, which are the most and detritus. abundant plants (Meirelles et al., 1999). Among the Predation of tadpoles by aquatic predator (Odonata latter, Alcantarea glaziouana (Leme) is dominant in larvae).—We observed many tadpoles of Ololygon both areas. perpusilla and O. littorea with their tails damaged, The third area sampled was the “forest restinga” (sensu suspicious of predation attempts made by damselfly Bernardi et al., 2005) (25.0720ºS, 47.9236ºW) from the larvae of genus Leptagrion (Odonata, Coenagrionidae), State Park of Cardoso Island (Parque Estadual da Ilha which is an aquatic top predator among the main do Cardoso), Cananéia, São Paulo State. This Restinga bromeliad-dwellers in the studied areas. To test this area have canopy height relatively continuous (ca. 9 m) hypothesis and evaluate the potential of damselfly with predominance of Myrtacea trees and the understory larvae as tadpole predators we conducted assays using composed mainly by orchids and bromeliads. The a small cylindrical glass aquarium provided with non- bromeliad species Quesnelia arvensis (Vell.) Mez was filtered water from A. glaziouana bromeliads in which the most abundant bromeliad in the area and is oftenly we placed together one tadpole of O. perpusilla and used by bromeligenous frogs. one specimen of Leptagrion andromache. We daily Each of the three sites had one distinct species of observed the system and registered presence (or not) of Ololygon: O. perpusilla occurred in Sugar Loaf (Pão- tadpole and damselfly larvae. de-Açúcar), O. littorea in Costão de Itacoatiara, and an Additionally, to quantify the frequency of individuals undescribed Ololygon species referred here as Ololygon with damaged tails, we used field observations from: 101 sp. occurred in Cardoso Island. All records were O. perpusilla tadpoles collected from 61 A. glaziouana obtained by direct observations during active searches bromeliads from Sugar Loaf inselberg; 83 of O. littorea Predation and parasitism on bromeligenous Snouted Treefrogs 273 from 57 A. glaziouana in Itacoatiara inselberg; and 43 When the frog stopped resisting to the attack, the snake of Ololygon sp. from 44 Quesnelia arvensis in Cardoso ingested it headfirst. Island. We measured their total length and body length At Cardoso Island we recorded no predation events to the nearest 0.1 mm using callipers. Based on the involving snakes and Ololygon sp. frogs, although we descriptions