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Home , Bothrops jararacussu, Corinna (spider), Pachistopelma, Parasitism, Polybetes, Scinax acuminatus

Herpetology Notes, volume 13: 271-279 (2020) (published online on 19 March 2020)

Predation and 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 both as refuge and breeding site, is that these would constitute a “safe place” and/or a “predator-free environment”. Here we present some new records of antagonistic interactions involving bromeligenous Snouted Treefrog of the Ololygon in a coastal Brazilian Rainforest. We report records of on Ololygon spp. tadpoles by damselfly larvae (Leptagrion) and by the Corinna demersa, and also predation on adults of the by a ( jararaca) and . We also report the occurrence of parasitism of O. perpusilla adults by (Ornithodorus sp.) and the register of a protozoan parasite ( 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 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 are or not more or less safe for bromeligenous and/or bromelicolous .

Keywords. Bromeliaceae, coccidia, damselfly larvae, , spider predation, snake predation,

Introduction advantage as low predation on tadpoles by and by fishes (Hero et al., 1998, 2001; Summers and Frog species from distinct families (e.g., Hylidae, McKeon, 2004). Bufonidae, ) 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 (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 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, . 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 among and invertebrates de Janeiro 20550-013, Brazil. (Kitching, 2001; Rocha et al., 2004). Many invertebrates 3 Departamento de Biologia , 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), (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 (Oliveira et al., 2013; Gambale et al., 272 Leandro Talione Sabagh et al.

2014), and (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 or . () 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 () 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 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 . 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 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 and Ololygon sp. frogs, although we descriptions of the tadpoles their body length as being have recorded some few occurrences of snakes on leaves 36% of the total length in O. perpusilla (Peixoto, 1987) of Q. arvensis. During nighttime we found juveniles and 38% in O. littorea (Peixoto, 1988). Since both the of Bothrops jararacussu (n = 1) and of B. jararaca (n descriptions of these tadpoles did not present dispersion = 2) coiled like a sit-and-wait ambush behaviour on values (e.g. variance), we add 10% as standard error and bromeliad’s leaf axils. The three snakes were found in considered that a percentage of up to 40% of the total different days and bromeliads. body length of the tadpole tail would be non-damaged. Predation by spiders.—Spiders were easily detected In the case of the tadpoles of the non-described frog on leaves of the bromeliads in Sugar Loaf and species Ololygon sp., the measurements were made in Itacoatiara Inselbergs and also in Cardoso Island. At tadpoles having intact tails (n = 40) and considered the Sugar Loaf, we recorded one predation event of the same body length/total length proportion found in O. Brazilian wandering spider (armed-spider) Phoneutria perpusilla and in O. littorea tadpoles. In summary, we keyserlingi (Ctenidae) preying on Ololygon perpusilla considered as damaged tails those with length <40% of frog (Fig. 1B). At Itacoatiara, we also recorded one the tadpole total length for all species. predation event of Polybetes cf. rapidus (Sparassidae) Relationships of frogs with ticks and protozoans.—At preying on Ololygon littorea. At Cardoso Island we Sugar Loaf and Costão de Itacoatiara Inselbergs we recorded independent events of three spider species carefully inspected 523 adult individuals of Ololygon preying on adults of Ololygon sp.: one P. keyserlingi; spp. looking for ectoparasites. In Cardoso Island we an unidentified Ctenidae; and Corinna demersa inspected about 50 individuals of Ololygon sp. looking (Corinnidae) recorded preying on adults (n = 4), froglets potential ectoparasites attached on their bodies. (n = 1) (Fig. 1C) and tadpoles (n = 1). Also, to assess potential parasitism by protozoans, In the laboratory, in all assays replicates C. demersa mainly coccidian ( ), we collected preyed on both adults and tadpoles of Ololygon sp. in the field five individuals of O. littorea and 12 Almost all adult predation (83.3 %) occurred within 48 individuals of O. perpusilla which were maintained hours. At the beginning of one of the observations, one individually inside plastic bags in order to obtain their adult female of C. demersa turned towards the water fresh faeces. Faeces were transferred from bags to inside the tube while the tadpole remained all time at the Falcon tubes and also kept individually and immersed bottom. The spider submerged after about 20 minutes in 2% potassium dichromate solution. Every day the and, moving on detritus and on the walls of the plastic solution was thoroughly stirred to oxygenate and tube, it approached and captured the tadpole. Having the promote sporulation of coccidia eventually present. tadpole between their chelicerae, C. demersa emerged After about five days, the samples were examined by and consumed the tadpole outside of water. the method of centrifugal flotation in saturated sugar Tadpole predation by Odonata larvae.—Based on our solution (Sheater’s method), using a microscope under observations of the feeding trials we can suggest that 400x magnification. Leptagrion andromache is a predator of O. perpusilla tadpoles. The tadpoles remained themselves most of the Results time with their belly joined the walls of the tank, moving Predation by snakes.—At Sugar Loaf Inselberg on 22 slowly while the damselfly remained most of the time June 2011 we found a juvenile of Bothrops jararaca at the aquarium bottom associated with debris. Those supposedly foraging on the bromeliad A. glaziouana. tadpoles originally having intact tails, were successively The snake was coiled, with the head elevated apparently losing portions of it, probably as result of the attacks waiting for a prey. At the same time in other nearby from damselfly larvae. In the 12th day, the damselfly bromeliads we saw at least three frogs (O. perpusilla). preyed on the tadpole (Fig. 1D-E), at that time having One of these frogs was carefully induced to move about only a half-part of its tail. towards to snake. After the first movement made by the The frequency of tadpoles having body length above frog, the snake promptly lunged capturing the frog by of natural percentage expected (⅔) in Sugar Loaf was its back near to the inguinal region of its body (Fig. 1A). 21.8% (n = 22), in Itacoatiara was 15.7% (n = 13) and 274 Leandro Talione Sabagh et al.

Figure 1. Disharmonic relationship on Ololygon spp. frogs in bromeliad habitat: juvenile of Bothrops jararaca and O. perpusilla on Alcantarea glaziouana bromeliad at Sugar Loaf (Pão-de-Açúcar) (A); Phoneutria keyserlingi preying on Ololygon perpusilla at Sugar Loaf (B); Corinna demersa and a bromeligenous Ololygon sp. at Cardoso Island (C); Leptagrion andromache larvae and Ololygon perpusilla tadpole in aquarium (D) and Leptagrion sp. in phytothelma at Sugar Loaf (E); and Ornithodorus sp. on O. perpusilla hand at Sugar Loaf (F). Photos by Leandro T. Sabagh (A, B, D, E and F) and Gustavo Cauê O. Piccoli (C). Predation and parasitism on bromeligenous Snouted Treefrogs 275 in Cardoso Island was 6.9% (n = 3). Although not diets (Martins et al., 2002; Toledo et al., 2007). When necessarily the damage on tadpole tails were caused by juveniles, the venomous snakes Bothrops jararaca and damselflies, it is possible that some interaction could be B. jararacussu are known as frog-eater (Hartmann et in course within the phytotelmata that could be harming al., 2003), including -frogs of the genus Ololygon the tadpoles, disturbing their swimming and leaving (Borges-Júnior et al., 2007). Also, there are some them more susceptible to predation by damselfly larvae reports regarding snakes foraging in bromeliads and or other aquatic predators. feeding on frogs that use these plants both as refuge and as breeding site (Carvalho, 1949; Rocha and Vrcibradic, Relationships of frogs with ticks and protozoans.—We 1998; Jungfer and Weygoldt, 1999), including tadpoles found only one individual tick in metalarvae stage, in the phytothelmata (Chan and Peterson, 2007). Ornithodorus sp. (Fig. 1F) attached to the left hand of one of one individuals of the frog Ololygon perpusilla. Predation by spiders.—Some spiders are often The tick’s body was turgid, allowing to infer that it registered in bromeliads, as sporadic visitors using was plenty of blood suggesting that this parasite may this microhabitat for both refuge and as foraging site fed on O. perpusilla. No other ectoparasite was found (Dias and Brescovit, 2004; Brasileiro and Oyamaguchi, associated to Ololygon spp. from Costão de Itacoatiara 2006; Pertrel et al., 2010). This seemed to be the case of and from Cardoso Island. Phoneutria keyserlingi and of Polybetes cf. rapidus two We found Coccidia in four of the five samples of faeces, spider species that does not have obligate relationship each one from one individual of O. littorea (prevalence with bromeliads. In environments where bromeliads are = 80.0 %). However, all samples of O. perpusilla densely distributed like our study sites, P. keyserlingi were negative for the presence of coccidia. Oocysts would use the bromeliad habitat during its entire from O. littorea samples were elongate-ellipsoidal and life cycle, including for and population asymmetric; wall smooth, 1 layer, L x W: 20.0 x 17.1 µ (n of juveniles. The spider P. keyserlingi is = 6); L/W ratio ~1.1; oocyst residuum and polar granule known to produce neurotoxic (Richardson et all absent. Sporocysts were subspheroidal, L x W: 14 x al., 2006) which is used to promptly subdue their prey 10 µ (n = 7); Stieda body and sub-Stieda body all absent; as we have had observed in the field. Spider species of sporocyst residuum a compact spheroidal mass of large this genus are nocturnal, have cursorial habits (Martins and small granules. Through these morphological and and Bertami, 2007) and usually ambush their preys on morphometric analysis, the parasite was identified as bromeliad leaves, during day time and probably use Isospora cruzi according to Carini (1936). bromeliads leaf axils as shelters. Polybetes spiders are known to be nocturnal, cursorial, aggressive, and with Discussion low toxicity venom (Rodríguez-Gil et al., 2007). Other spider species live strictly associated with Our study demonstrated the existence at least of two bromeliads and does not occur in other habitats as is the kinds of antagonistic interspecific interactions involved case of Corinna demersa, which is relatively abundant bromeligenous Ololygon treefrogs in a bromeliad and can be easily seen on Q. arvensis at Cardoso Island . These interactions occurred in both, tadpole (Piccoli, 2011, 2015). This spider lives in bromeliads and adult, life stages. The first of them is the predation during all its life using this habitat for growth, by snakes, the major terrestrial predators of frogs and, development and reproduction (Piccoli, 2011, 2015). especially in bromeliad habitat, spiders and odonata Moreover, C. demersa have hydrophobic bristles in the larvae. The second, are the events of parasitism by ticks abdomen which make respiration during submersion in and coccidian parasites. phytotelmata, a behaviour used for both foraging and Predation by snakes.—Our observation of Bothrops locomotor escape behaviour from predators (Piccoli, jararaca prey on Ololygon perpusilla and the feeding 2011). Adult females of C. demersa usually ambush behaviour is similar to that described by Hartmann et their prey when at shelter in the bromeliad leaf axils al. (2003), a form of prey ingestion common among and include aquatic and terrestrial bromeliad-dweller snakes. All snakes registered in Cardoso Island can organisms in their diet (Piccoli 2011, 2015). From our be considered potential predators of bromeligenous records of interaction between C. demersa and different Ololygon sp. Snakes are the main -predators life stages of Ololygon sp., we can infer that this spider of frogs (Toledo et al., 2007; Dorigo et al., 2014) and species may be among the main terrestrial many species of the genus Bothrops include frogs in their predators of the bromeligenous Ololygon in Cardoso 276 Leandro Talione Sabagh et al.

Island. Relationships of frogs with ticks and protozoans.— Spiders have been suggested to be the main Ticks are usually ectoparasites of vertebrates including invertebrate-predator of frogs accounting for almost frogs, and the most common genus parasitizing anuran 50% of the recorded attacks on Anura (Toledo, species in Brazil is Amblyomma () (Guglielmone 2005). Predation by spiders, both on bromeligenous and Nava, 2010). The Argasid Ornithodorus, which is and bromelicolous (a frog that does not breed in uncommonly known to parasitize frogs, is usually found bromeliads but are often found on bromeliads) adult in and hosts (Barros-Battesti et al., 2015). frogs of species of several anuran families as Although we recorded tick parasitism in O. perpusilla miliaris (Cycloramphidae) (Pertrel et al., 2010) and in bromeliads, the prevalence was very low. There are Dendophryniscus leucomystax (Bufonidae), including few records of Ornithodorus spp. parasitizing anurans the bromeligenous Hylidae, Ololygon alcatraz (e.g., Rhinella spp. toads - Bufonidae) (Gonzalez-Rivas (Brasileiro and Oyamaguchi, 2006) may corroborate et al., 2012; Bermúdez et al., 2013). The only record the hypothesis that bromeliads are not a predator-free of Ornithodorus parasitizing anurans in Brazil is that habitat. of the rock frog Thoropa miliaris (Cycloramphidae) Our records of predation of Ololygon spp. by spiders parasited by Ornithodorus faccinii in Itinguçu waterfall points out the importance of these as (municipality of Itaguaí, Rio de Janeiro State) (Barros- predators of frogs in the bromeliad environment where Battesti et al., 2015). At Sugar Loaf Inselberg a they do not just prey on adult frogs but also on tadpoles. population of Thoropa miliaris lives in syntopy with O. The need for the use of the bromeliad habitat by both the perpusilla and also had Ornithodorus sp. attached on prey (Ololygon sp.) and by the predator (C. demersa) your bodies. Therefore, our register is the first record of results in a complex predator-prey interaction that can Argasidae ticks parasitizing frogs from Hylidae be a good system to study issues on foraging and anti- and the second record of frogs as hosts of Argasidae predatory behaviours. ticks in Brazil. The coccidia are (Phylum Apicomplexa) Tadpole predation by Odonata larvae.— Damselflies’ which probably, are among the most abundant and larvae are conspicuous predators in aquatic habitats and speciose parasites found in vertebrates, and have been commonly feed on tadpoles (Heyer et al., 1975; Gascon, little studied in (Duszynski et al., 2007). The 1989; Hero et al., 2001) as we observed. These occurrence of coccidia in O. littorea is the first record larvae are frequently reported as generalist top predators of this parasite in a species from the genus Ololygon. in bromeliad phytotelmata (Ngai and Srisvastava, 2006; However, Isospora cruzi was record parasitising Petermann et al., 2015) feeding also on tadpoles. In other four species of (a genus under which the Brazilian coast, the genus Leptagrion is the most species of Ololygon were previously considered): S. common bromeliad-dwelling odonate and comprises crospedospilus; S. fuscovarius; S. nasicus; and S. ruber a set of species strictly associated with bromeliad (Carini, 1936; Duszynski et al., 2007). phytotelmata (Santos, 1968). It probably prey on many bromeligenous tadpoles of different species. Leptagrion In conclusion, all of our records may stimulate new andromache has a large geographic distribution and was behavioural and ecological studies on the effects of common in all of our study sites, although in Cardoso predators and parasites on bromeligenous Ololygon Island we found other three species: L. elongatum; L. treefrogs. Also, this information may account for macrurum; and L. bocainensis. building a comprehensive scheme of the web As in the above case of spiders, the feeding related to the bromeliad complex habitat including frogs, relationships between frogs and Odonata are not a conspicuous but neglected component from these unidirectional. The feeding relationship between communities. In a review study, Kitching (2001) argues odonates and treefrogs in bromeliad ecosystem appears that phytotelmata habitats are mostly environments free to be ontogenetic-dependent. While Leptagrion larvae of predators but, points out that when present, predators feed on bromeligenous tadpoles, adult frogs feed on may have a substantial impact on their prey. Additional Leptagrion adults as recorded by Santos (1984) in studies constructed with a specific design to compare stomachs of frogs collected inside bromeliads. Predatory predation and parasitism rates between bromeligenous habits of Leptagrion larvae on Ololygon tadpoles should and non-bromeligenous frogs should be performed to be affected by size, as larger predators would have more assess the potential effect of disharmonic relationships chance to consume smaller tadpoles. on those frogs that breeds in bromeliads. Predation and parasitism on bromeligenous Snouted Treefrogs 277

Acknowledgments. This study was supported by research Thamnodynastes Wagler, 1830 (Colubridae: Dipsadinae) in the grants from the Conselho Nacional de Desenvolvimento Atlantic rainforest of southeastern Brazil. Herpetological Notes Científico e Tecnológico (Grant n º150841/2017-5; Grant nº 7: 261–264. 304791/2010-5; Grant nº 470265/2010-8; Grant nº 161428/2015- Duellman, W.E., Marion, A.B., Hedges, S.B. (2016): Phylogenetics, 0), Fundação de Amparo à Pesquisa do Estado do Rio de classification, and of the treefrogs (Amphibia: Janeiro through “Cientistas do Nosso Estado” Program (Grant Anura: Arboranae). Zootaxa 4104: 1–109. nº E-26/102.765/2012 and Grant nº E-26/202.920/2015), and Duszynski, D.W., Bolek, M.G., Opton, S.J. (2007): Coccidia Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant nº (Apicomplexa: Eimeriidae) of amphibians of the world. Zootaxa 2012/51143-3). Instituto Estadual do Ambiente do Rio de Janeiro 1667: 1–77. (Process nº 024/2010), Secretaria Municipal de Meio Ambiente Forti, L.R., Fischer, H.Z., Encarnação, L.C. (2007): Treefrog do Rio de Janeiro (Process nº 14/000.196/2010), and Secretaria de Dendropsophus elegans (Wied-Neuwied, 1824) (Anura: Infraestrutura e Meio Ambiente do Estado de São Paulo (Process Hylidae) as a meal to Otostigmus tibialis Brölemann, 1902 nº 021/2008) provided collecting permits. We specially thanks (Chilopoda: Scolopendridae) in the Tropical Rainforest in Nicolau Serra-Freire (in Memorian) and Renner Luiz Cerqueira southeastern Brazil. Brazilian Journal of 67: 583–584. Baptista for identification of ticks and spiders respectively. Frank, J.H., Lounibos, L.P. (1987): Phytotelmata: swamps or islands? Florida Entomologist 70: 14–20. References Gambale, P.G., Batista, V.G., Oda, F.H., Campos, R.M., Takemoto, R.M., Bastos, R.P. (2014): Anuran larvae as prey and hosts of Barros-Battesti, D.M., Landulfo, G.A., Luz, H.R., Marcili, A., invertebrates in Neotropical aquatic habitats. Revista Chilena de Onofrio, V.C., Famadas, K.M. (2015): faccinii Historia Natural 87: 1–5. n. sp. (: Ixodida: Argasidae) parasitizing the frog Thoropa Gascon, C. (1989): Predador-prey size interaction in tropical ponds. miliaris (Amphibia: Anura: Cycloramphidae) in Brazil. Parasites Revista Brasileira de Zoologia 6: 701–706. &Vectors 8: 1–11. Ghizoni-Jr, I.R., Azevedo, M.A.G., Port-Carvalho M. (2000): Benzing, D.H. (1980): The Biology of the Bromeliads. California, Predação de Hyla nahdereri (Anura: Hylidae) por Cyclarhis USA, Mad River Press. gujanensis (Aves: Vireonidae) em Santa Catarina. Melopsittacus Bermúdez, S.C.E., Miranda, R.J., Kadoch, N. (2013): Reporte 3: 137–139. de larvas de Ornithodoros puertoricensis Fox 1947 (Ixodida: Gonzalez-Rivas, C.J., Castillo, G.N., Acosta, J.C., Venzal, J.M., Argasidae) parasitando a Rhinella marina (L. 1758) (Anura: Guglielmone, A.A. (2012): Primer reporte de parasitismo de una Bufonidae) en David, Chiriquí, Panamá. Puente Biológico 5: garrapata blanda del género Ornithodoros (Ixodida: Argasidae) 81–85. sobre Rhinella arenarum (Anura: Bufonidae) en el departamento Bernarde, O.S., Abe, A.S. (2010): Hábitos alimentares de serpentes de Valle Fértil, San Juan, . Cuadernos de Herpetología em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10: 26: 95–97. 167–173. Gray, E. P., Nunziata, S., Snodgrass, J.W., Ownby, D.R., Havel, J. Bernardi, J.V.E., Landim, P.B.M., Barreto, C.L., Monteiro, R.C. E. (2010): Predation on Green Frog Eggs (Rana clamitans) by (2005): Spatial study of the vegetation gradient from Cardoso Ostracoda. Copeia 2010: 452–456. Island State Park, SP, Brazil. Holos Environment 5: 1–22. Guglielmone, A.A., Nava, S. (2010): Hosts of Amblyomma Borges-Júnior, V.N.T., Oliveira, L.G., Rocha, C.F.D., Van-Sluys, dissimile Koch, 1844 and Amblyomma rotundatum Koch, 1844 M. (2007): Natural history notes. Scinax trapicheiroi. Predation. (Acari: Ixodidae). Zootaxa 2541: 27–49. Herpetological Review 38: 196–197. Hartmann, P.A., Hartmann, M.T., Giasson, L.O.M. (2003): Uso Brasileiro, C.A., Oyamaguchi, H.M. (2006): Natural histoy notes. do hábitat e alimentação em juvenis de Bothrops jararaca Scinax alcatraz. Predation. Herpetological Review 37: 451– (Serpentes, Viperidae) na Mata Atlântica do sudeste do Brasil. 451. Phyllomedusa 2: 35–41. Carini, A. (1936): Isospora cruzi, parasita dell’ intestine di alcune Hero, J.M., Gascon, C., Magnusson, W.E. (1998): Direct and ile del Brasile. Archivio Italiano di Scienze Mediche Coloniali e indirect effects of predation on tadpole structure in di Parassitologia 17: 610–613. the Amazon rainforest. Austral 23: 474–482. Carvalho, A.L. (1949): Notas sobre os hábitos de Dendrophryniscus Hero, J.M., Magnusson, W.E., Rocha, C.F.D., Catterall, C.P. (2001): brevipollicatus Espada (Amphibia, Anura). Revista Brasileira de Antipredator defenses influence the distribution of Biologia 9: 223–227. prey species in the Central Amazon Rain Forest. Biotropica 33: Chan, B.K., Peterson, A.L. (2007): Natural history notes. 131–141. Dendrobates auratus. Larval predation. Herpetological Review Heyer, R.W., McDiarmid, R.W., Weigmann, D.L. (1975): Tadpoles, 38: 321–322. predation and pond habitats in the tropics. Biotropica 7: 100– Dias, S.C., Brescovit, A.D. (2004): Microhabitat selection and 111. co-occurrence of Pachistopelma rufonigrum Pocock (Araneae, Itescu, Y. (2019): Are island-like systems biologically similar to Theraphosidae) and Nothroctenus fuxico sp. nov. (Araneae, islands? A review of the evidence. Ecography 42: 1298–1314. Ctenidae) in tank bromeliads from Serra de Itabaiana, Sergipe, Jungfer, K.H., Weygoldt, P. (1999): Biparental care in the Brazil. Revista Brasileira de Zoologia 21: 789–796. tadpole-feeding Amazonian treefrog Osteocephalus oophagus. Dorigo, T.A., Vrcibradic, D., Borges-Junior, V.N.T. (2014): Amphibia-Reptilia 20: 235–249. New records of anuran predation by snakes of the genus Junior, P.M., Furieri, K.S. (2000): Ecology of Leptagrian perlongum 278 Leandro Talione Sabagh et al.

Calvert, 1909: a bromeliad-dweller odonata species. Boletim do of habitat size on trophic structure in bromeliad invertebrate Museu de Zoologia Mello Leitão 11/12: 135–148. communities. Ecology 96: 428–439 Kitching, R. L. (2001): Food webs in phytotelmata: “bottom-up” Piccoli, G.C.O. (2011): História natural da aranha Corinna sp. and “top-down” explanations for community structure. Annual nov. (Corinnidae): interações com bromélias e comportamento Review of 46: 729–760. de submersão em fitotelmata. Unpublished M.Sc. dissertation, Loebmann, D., Solé, M., Kwet, A. (2008): Predation on spawn Universidade Estadual Paulista, São José do Rio Preto, Brasil. and adults of Chaunus dorbignyi (Duméril and Bibron, 1841) Piccoli, G.C.O. (2015): Um predador generalista na fronteira entre (Amphibia, Anura) by leeches (Hirudinea) in southern Brazil. ecossistemas: interações tróficas e os processos ecossistêmicos Amphibia 7: 31–34. bromelícolas. Unpublished PhD thesis, Universidade Estadual Marques, O.A.V., Sazima, I., Marques, O.A., Duleba, W. (2004): Paulista, São José do Rio Preto, Brasil. História natural dos répteis da estação ecológica Juréia-Itatins. Richardson, M., Pimenta, A.M.C., Bemquerer, M.P., Santoro, In: Estação Ecológica Juréia-Itatins: Ambiente Físico, Flora e M.M., Beirao, P.S.L., Lima, M.E., Figueiredo, S.G., Bloch- Fauna, p. 257–277. Marques, O.A.V., Duleba, W., Eds., São Jr., C., Vasconcelos, E.A.R., Campos, F.A.P., Gomes, P.C., Paulo, Brasil, Holos Editora. Cordeiro, M.N. (2006): Comparison of the partial proteomes Martins, M., Marques, A.O., Sazima, I. (2002): Ecological and of the of Brazilian spiders of the genus Phoneutria. phylogenetic correlates of feeding habits in Neotropical pitvipers Comparative Biochemistry and Physiology 142: 173–187. of the genus Bothrops. In: Biology of the Vipers, p. 307–328. Rocha, C.F.D., Vrcibradic, D. (1998): as predators of Schuett, G. W., Hoggren, M., Douglas, M.E., Eds., Utah, USA, vertebrates and preys in a restinga habitat of southeastern Brazil. Eagle Mountain Publishing. Ciência e Cultura 50: 364–368. Martins R., Bertani, R. (2007): The non-Amazonian species of Rocha, C.F.D., Vrcibradic, D., Van-Sluys, M. (1999): Natural history the Brazilian wandering spiders of the genus Phoneutria Perty, notes. Chironius multiventris foveatus. Prey. Herpetological 1833 (Araneae: Ctenidae), with the description of a new species. Review 30: 99–100. Zootaxa 1526: 1–36. Rocha, C.F.D., Cogliatti-Carvalho, L., Almeida, D.R., Freitas, Meirelles, S.T., Pivello, V.R., Joly, C.A. (1999): The vegetation of A.F.N. (2000): Bromeliads: amplifiers. Journal of granite rock outcrops in Rio de Janeiro, Brazil and the need of Bromeliad Society 50: 81–83. this protection. Environment Conservation 26: 10–20. Rocha, C.F.D., Cogliatti-Carvalho, L., Nunes-Freitas, A.F., Rocha- Menin M., Rodrigues, D.J., Azevedo, C.S. (2005): Predation on Pessôa, T.C., Dias, A.D.S., Ariani, C.V., Morgado, L.N. (2004): amphibians by spiders (Arachnida: Araneae) in the Neotropical Conservando uma larga porção da diversidade biológica através region. Phyllomedusa 4: 39–47. da conservação de Bromeliaceae. Vidalia 2: 52–72. Müller, F. (1879): Descripção do Elpidium bromeliarium crustáceo Rodel, M., Range, F., Seppanen, J., Source, R.N. (2002): Caviar in da família dos Cytherídeos. Arquivos do Museu Nacional 4: the rain forest: monkeys as frog-spawn predators in Tai National 27–34. Park, Ivory Coast. Journal of Tropical Ecology 18: 289–294. Ngai, J.T., Srivastava, D.S. (2006): Predators accelerate nutrient Rodríguez-Gil, S.G., Merani, S.M., Scioscia, L.C., Mola, M.L. cycling in a bromeliad ecosystem. Science 314: 963–963. (2007): Cytogenetics in three species of Polybetes Simon Oliveira, H.F., Oliveira, D. B., Ávila, R.W. (2013): Predation on 1897 from Argentina (Araneae, Sparassidae) I. Karyotype adults of Scinax x-signatus (Hylidae) and Physalaemus cuvieri and chromosome banding pattern. Journal of Arachnology 35: (Leiuperidae) by diving beetles (Coleoptera: : 227–237. Megadytes sp.). Herpetology Notes 6: 299–300. Sabagh, L.T., Ferreira, V.L., Rocha, C.F.D. (2010): Living together, Peixoto, O.L. (1987): Caracterização do grupo “perpusilla” e sometimes feeding in a similar way: the case of the syntopic revalidação da posição taxonômica de Ololygon perpusilla hylid frogs Hypsiboas raniceps and Scinax acuminatus (Anura: perpusilla e Ololygon perpusilla v-signata (Amphibia, Anura, Hylidae) in the Pantanal of Miranda, Mato Grosso do Sul State, Hylidae). Arquivos da Universidade Federal Rural do Rio de Brazil. Brazilian Journal of Biology 70: 955–959. Janeiro 10: 37–49. Sabagh, L.T. (2010): Ecologia de girinos de duas espécies de Peixoto, O.L. (1988): Sobre o “status” taxonômico de Hyla anuros (Scinax perpusillus e S. littoreus) que habitam bromélias catharinae alcatraz B. Lutz 1973, com a descrição de uma nova em Inselbergs no estado do Rio de Janeiro. Unpublished M.Sc. espécie para o grupo “perpusilla” (Amphibia, Anura, Hylidae). dissertation, Universidade Federal do Rio de Janeiro, Rio de Acta Biologica Leopoldesia 10: 253–267. Janeiro, Brasil. Peixoto, O.L. (1995): Associação de anuros a bromeliáceas na Sabagh, L.T. (2014): Interações entre anuros, bromélias e a Mata Atlântica. Revista Universidade Rural Série Ciências Vida comunidade bromelícola associada em três unidades de 17: 75–83. conservação no Estado do Rio de Janeiro. Unpublished PhD Pertel, W.R.L., Teixeira, R.L., Ferreira, R.B. (2010): Comparison thesis, Universidade do Estado do Rio de Janeiro, Rio de of diet and use of bromeliads between a bromelicolous and a Janeiro, Brasil. bromeligenous anuran at an inselberg in the southeastern of Santos, N.D. (1966): Contribuição ao conhecimento da fauna do Brazil. Caldasia 32: 149–159. Estado da Guanabara. 56. Notas sobre coenagriídeos (Odonata) Petermann, J.S., Farjalla, V.F., Jocque, M., Kratina, P., MacDonald, que se criam em bromélias. Atas da Sociedade de Biologia do A. A.M., Marino, N.A., Omena, P.M., Piccoli, G.C.O., Rio de Janeiro 10: 83–85. Richardson, B.A., Richardson, M.J., Romero, G.Q., Videla, M., Santos, N.D. (1968): Descrição de Leptagrion dardanoi sp. n. Srivastava, D.S. (2015): Dominant predators mediate the impact (Odonata, Coenagrionidae). Atas da Sociedade de Biologia do Predation and parasitism on bromeligenous Snouted Treefrogs 279

Rio de Janeiro 12: 63–65. Santos, N.D. (1984): Odonatas que se criam em bromélias de restinga no litoral fluminense. In: Restingas. Origem, Estruturas, Processos, p. 351-354. Lacerda, L.D., Araújo, D.S.D., Cerqueira, R., Turq, B., Eds., Niterói, Brasil, CEUFF. Sazima, I., Haddad, C.F.B. (1992). Répteis da Serra do Japi: notas sobre história natural. In: História Natural da Serra do Japi – Ecologia e Preservação de uma Área Florestal no Sudeste do Brasil, p. 212–236. Leitão-Filho, H.F., Morellato, L.P.C., Eds., Campinas, Brasil, Editora Unicamp. Sillett, T.S., James, A., Sillett, K.B. (1997): Bromeliad foraging specialization and diet selection of Pseudocalaptes lawrencii (Furnariidae). Ornithological Monographs 48: 733–742. Silva, H.R., Carvalho, A.L.G., Bittencourt-Silva, G.B. (2011): Selecting a hiding place: anuran diversity and the use of bromeliads in a threatened coastal sand dune habitat in Brazil. Biotropica 43: 218–227. Silva, I.C.O., Pacheco, E.O., Silva, L.A., Carvalho, P.S., Santana, D.J., Tavares, L.E.R. (2018): Metazoan parasites of Odontophrynus americanus (Anura: Odontophrynidae) from the Serra da Bodoquena mountain range, Mato Grosso do Sul, Brazil. Herpetology Notes 11: 343–347. Summers, K., McKeon, C.S. (2004): The of phytotelmata use in Neotropical poison frogs. Miscellaneous Publications, Museum of Zoology, University of Michigan 193: 55–73. Toledo, L. F. (2005): Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetological Review 36: 395–400. Toledo, L.F., Ribeiro, R.S., Haddad, C.F.B. (2007): Anurans as prey: an exploratory analysis and size relationships between predators and their prey. Journal of Zoology 271: 170–177.

Accepted by Fabrício Oda