TRABAJO

Feeding habits of the bromeligenous treefrog Phyllodytes edelmoi Peixoto, Caramaschi & Freire, 2003 (Anura: Hylidae) from the State of Alagoas, Northeastern Brazil

Katyuscia Araujo-Vieira¹, Ubiratan Gonçalves², Jhonatan Guedes dos Santos³, Thame Gomes Ferreira⁴, Gabriel O. Skuk⁵

¹ División Herpetología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”-CONICET, Ángel Gallardo 470, C1405DJR, Buenos Aires, Argentina.

² Seção de Herpetologia, Museu de Historia Natural da Universidade Federal de Alagoas, Av. Amazonas, Prado (Praça da Faculdade), Maceió, Alagoas, Brazil.

³ Laboratório de Conservação no Século XXI, Instituto de Ciências Biológicas e da Saúde, Campus A.C. Simões, Universidade Federal de Alagoas, Av. Lourival Melo Mota s/n, Tabuleiro dos Martins CEP 57072-900, Maceió, Alagoas, Brazil.

⁴ Departamento de Ecologia e Biomonitoramento, Universidade Federal da Bahia, Rua Barão de Geremoabo, 147, Campus de Ondina, CEP 40170-290, Salvador, Bahia, Brazil.

⁵ Deceased March 19, 2011.

Recibido: 23/06/17
Revisado: 09/08/17
Aceptado: 26/09/17

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ABSTRACT

The hylid frog genus Phyllodytes comprised 12 species distributed in eastern Brazil and known to strictly inhabit inside bromeliads. In this study, we explore the feeding habits of P. edelmoi and test the prey selectivity of the species by comparing the prey items in the stomachs contents with the availability of preys in bromeliads. Our results show that P. edelmoi consumes high amounts of ants along the year, and therefore it could be considered an “ant specialist” species. This specialist feeding behaviour could be considered a synapomorphy of the genus Phyllodytes.

Key words: Atlantic Brazilian Forest; Heart-tongued frogs; Ant specialist; Ecology.

RESUMEN

Hábitos alimenticios de la rana bromélicola Phyllodytes edelmoi Peixoto, Caramaschi & Freire, 2003 (Anura: Hylidae) del Estado de Alagoas, Noreste de Brasil. El género de hílidos Phyllodytes está compuesto por 12 especies distribuidas en el este de Brasil y conocidas por habitar estrictamente bromeliáceas. En este estudio se exploran los hábitos alimenticios de P. edelmoi y se testea la selectividad de las presas por la especie comparando las presas encontradas en los estómagos con la disponibilidad de presas en las bromelias. Nuestros resultados muestran que P. edelmoi consume grandes cantidades de hormigas a lo largo del año, por lo que podría considerarse una especie "especializada en hormigas". Este comportamiento alimenticio espe­cializado podría ser considerado una sinapomorfia para el género Phyllodytes.

Palabras clave: Bosque Atlántico brasileño; Ranas con lengua de corazón; Especialista en hormigas; Ecología.

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INTRODUCTION

The hylid frog genus Phyllodytes Wagler, 1830 comprised 12 species distributed in eastern Brazil, from the north portion of the State of Rio de Janeiro to the State of Paraíba (Frost, 2017). These species are known to strictly inhabit inside bromeliads. The bromeliads are generally able to store water in a structure formed by their tightly-overlapping leaf bases. Phyllodytes uses the axils of these plants for refuge, foraging, and breeding (Bokermann, 1966; Peixoto et al., 2003; Caramaschi et al., 2004; Ferreira et al., 2012; Motta-Tavares et al., 2016). This dependence on bromeliads categorizes the species of Phyllodytes as bromeligenous (sensu Peixoto, 1995).

Phyllodytes edelmoi occurs in the Brazilian Atlantic Forest of Alagoas and Pernambuco states (Peixoto et al., 2003; Moura, 2011) at altitudes ranging from sea level to 500 m a.s.l. (Gonçalves and Palmeira, 2016). It can be found in terrestrial, rupicolous, or more frequently epiphytic bromeliads located at the border of the forest remnants or in open areas in the Atlantic Forest (Peixoto et al., 2003). The major threats to this species seems to be related to forest degradation and reduction in extent of remaining natural areas due to agricultural deve­lopment, wood extraction, human settlement, and collection of bromeliads (Eliza and Peixoto, 2004).

The hylids are often recognized as generalist feeders (Ferreira et al., 2012), with strategies of op­portunistic foraging. However, prey characteristics such as size, movement, palatability, abundance, and nutritional value can influence on predation, as well as the abundance and availability of prey in the habitat (Ferreira et al., 2012; Pertel et al., 2010). Toft (1980; 1981) distinguished two patterns in the diet of tropical frogs: “ant specialists”, those eat more chitinous preys such as termites and ants; and “non-ant specialists”, those that ingest a varied spectrum of less chitinized arthropods such as spiders and grasshoppers.

Ants and termites are the dominant food items in the stomach contents of Phyllodytes luteolus (Fer­reira et al., 2012; Motta-Tavares et al., 2016). This specialization on colonial arthopods could be an advantage for this frog (Ferreira and Teixeira, 2009), since ants are abundant inside bromeliads in the Bra­zilian Atlantic Forest (Mestre et al., 2001; Juncá and Borges, 2002) and unpalatable to many predators be­cause of formic acid (Zug and Zug, 1979). However, in the absence of studies on prey availability in the bromeliads, they could not confirm to what extent P. luteolus specializes in these colonial insects (Ferreira et al., 2012; Motta-Tavares et al., 2016).

The present study aimed to explore the feeding habits of Phylodytes edelmoi and test the prey selectivity of the species by comparing the prey items into the stomachs with the availability of preys inside bromeliads. We also comment the occurrence of seasonal (rainy vs. dry seasons) differences in diet composition of this frog.

 

MATERIAL AND METHODS

Study area. The fieldwork was carried out from August 2004 to April 2005 at the locality of Serra da Saudinha (09°22'S, 35°45'W, about 1,210 ha), a remnant of Atlantic Forest, located at the Municipa­lity of Maceió, State of Alagoas, northeastern Brazil (Fig. 1). It is an area of crystalline rocks located in the extreme north-northwest of Maceió, surrounded by Tabuleiros Costeiros and formed by a granitic steep slope, deeply wrought in slopes between 160 and 300 m a.s.l (Assis, 2000; Gonçalves et al., 2012). This locality belongs to a sugar cane ethanol factory Usina Cachoeira and it is surrounded by sugar cane crops (Fig. 2B).

Figure 1. Location map of the study area. The red circle indicates the locality of Serra da Saudinha (09°22'S, 35°45'W, about 1,210 ha), Maceió, Alagoas, northeastern Brazil.

Figure 2. (A) Adult of Phyllodytes edelmoi in life (unvouchered specimen). Photo: Gabriel O. Skuk. (B) A remnant of the Atlantic Forest of Serra da Saudinha, surrounded by sugar cane crops. (C) and (D) Habitat of P. edelmoi.

The weather is hot and rainy, with a dry sea­son between October and April, and a rainy season between March and September. Mean annual temperature ranges from 10 to 30ºC and mean annual precipitation varies between 0 and 349 mm.

Data collection. A total of 33 individuals of Phyllodytes edelmoi (Fig. 2A) were captured by hand during day and night, from 0800 to 2300 h; then were euthanized with 2% lidocaine hydrochloride, immediately fixed in 10% formalin (to stop the diges­tion processes and preserve the stomach content), and stored in 70% ethanol. They are deposited in the Herpetological Collection of the Museu de História Natural da Universidade Federal de Alagoas (MU­FAL 8475-8477, 8479, 8481-8484, 8487-8511).

Stomachs were removed through an abdominal incision and preserved in 70% ethanol; their contents were analyzed quantitatively and qualitatively. The snout-vent length (SVL) of frogs was measured with a digital caliper under a stereomicroscope and rounded to the nearest 0.1 mm. Sex was determined by examination of secondary sexual characters (nuptial pads, vocal slits, and expansion of the vocal sac).

Bromeliads were cut off at their root base and transported to the laboratory in plastic bags. They were analyzed only when frogs were found inside the plants. Three genera of bromeliad plants were identified in the area studied: Aechmea, Canistrum (C. alagoanum and C. aurantiacum), and Hohenbergia (Fig. 2C, D). For each bromeliad, we calculated the volume (in cubic meters) using the formula: V = π radius2 height/3, where radius was the distance between the central axis and the longest leaf, and height was the distance from the root base to the tip of the longest leaf. Ten aglomerates of bromeliads (41 bromeliad plants) were examined totalizing a volume of 33.95 m3 in the rainy season (August and September, 2004 and April, 2005) and eight aglomerates (19 bromeliads plants) with a volume of 30.18 m3 in the dry season (October and November, 2004 and January, 2005). Although the number of bromeliad was different among seasons, the total volume of bromeliads analyzed was similar standardizing the sampling effort.

At laboratory, invertebrates inside bromeliads were extracted using a Berlese funnel (modified from Maranhão, 1976), which works by creating a temperature gradient over the sample such that invertebrates will move away from the higher temperatures and fall into a collecting recipient with 70% ethanol, where they are stored for examination.

Sampled specimens were identified under a stereomicroscope (Nikon, SMZ-800) to the taxonomic level of order (or family, in the case of Formicidae) following Borror and DeLong (1988) and Ruppert et al. (2004).

We measured preys volume (in cubic millimeters) in the stomachs and invertebrates inside bromeliads with the following procedure: each individual was photographed using a digital camera attached to a steromicroscope (Nikon SMZ-800) with a scale in millimeters. The photos were organized in different plates for each specimen of Phyllodytes edelmoi and for the bromeliads; then we used these photos to measure the width and length of each prey specimen employing the software ImageTool v3.0 (Wilcox et al., 2002). These measurements were used to calculate the volume, which was estimated using the formula for an ovoid spheroid: V = 4/3π (length/2) (width/2)² following Dunham (1983).

Statistical analysis. The homogeneity analysis of variances of frog SVL was performed using Levene F test (Levene, 1960). The Student’s t test was used to compare the SVL mean values between sexes. Frequency of occurrence for each prey type was calculated dividing the total number of stomachs containing an item prey by the total number of no empties stomachs. The diversity of prey consumed by each specimen and the diversity of invertebrates found in the bromeliads were estimated by the Shannon Diversity Index H'= -Σpi ln pi, where pi was the relative abundance of the prey taxon i in the stomachs or bromeliads (Magurran, 1988). Seasonal differences between diversity values were tested by t test for diversity. The equitability was calculated using the Shannon’s formula E=H'/ln S, where S was the number of different taxa in the stomachs or bromeliads (Magurran, 1988). A Spearman’s correlation test was performed to compare the diversity of prey consumed and that of invertebrates inside bromeliads (Vrcibradic and Rocha, 1995; Kolodiuk et al., 2010). The electivity was estimated by the Ivlev Index (Krebs, 1989) that ranges from -1 (total avoidance) to 1 (total preference).

A Spearman’s correlation test was performed to determine if there was correlation between frogs SVL and prey of maximum volume, the prey of minimum volume, and the mean volume of preys into the stomachs. To compare the volume of preys with the volume of invertebrates in the bromeliads, we considered as potential preys only invertebrates with the maximum volume equal or less than the maximum volume of the prey found into the frog stomachs, which was a Coleoptera of 24.7 mm3. The means volume of preys into the stomachs and invertebrates inside bromeliads were compared using a Student’s t test.

RESULTS

A total of 33 individuals of Phyllodytes edelmoi were collected inside bromeliads (17 females and 16 males). Males of P. edelmoi vocalize between 1900 and 0200 h on the bromeliad leaves, but in general during the day inhabit the axils and the central tube of these plants near or semi-submerged in the water. Phyllodytes edelmoi was found mainly in bromeliads of the genus Aechmea, and less frequently in smaller bromeliads of the genus Canistrum (C. aurantiacum and C. alagoanum). We did not find P. edelmoi in larger bromeliads of the genus Hohenbergia.

Morphology. The homogeneity of variances of males (n = 16) and females (n = 17) tested by Levene F test showed no significant differences (FLevene = 3.004, g.l. = 1, p = 0.097). The Student’s t test indicated that there was no significant differences (t = -0.079, g.l. = 22, p = 0.937) between the size of males (24.3 ± 1.6, 21.7-26.1 mm, n = 16) and females (24.3 ± 2.5, 20.1-28.3 mm, n = 16), after excluding an immature female, with a small SVL (MUFAL 8501, SVL 12.4 mm).

Spearman’s test showed significant and positive correlations between the SVL of Phyllodytes edemoi and the mean volume of preys consumed (Rho = 0.375, p= 0.032, n = 33) and the prey of maximum volume (Rho = 0.364, p= 0.038, n = 33), but there was no correlation between the SVL and the prey of minimum volume (Rho = -0.090, p= 0.620, n = 33).

Diet. We found no empty stomachs in sampled specimens; therefore, stomach contents of the 33 in­dividuals of Phyllodytes edelmoi were analyzed, from which 14 were collected in the rainy season and 19 in the dry season. Stomach and bromeliads contents were classified into 28 prey items comprising eight invertebrate item groups (see Table 1).

Table 1. Diet composition of Phyllodytes edelmoi and invertebrates collected inside bromeliads in the rainy (14 individuals) and dry (19 individuals) seasons, locality of Serra da Saudinha, Maceió, Alagoas, northeastern Brazil.

A total of seven prey items were identified into the stomachs of Phyllodytes edelmoi, with Formicidae (ants) being the most abundant prey item (Table 1). Ants were present in the stomachs of all individuals analyzed. There was no significant difference in the diversity of preys items in stomachs of P. edelmoi between the rainy (H'rainy = 0.188) and dry (H'dry = 0.167) seasons (t = 4.04; p > 0.05). The equitability of preys consumed was similar in both seasons (Erainy = 0.105 and Edry = 0.104). Phyllodytes edelmoi eats predominantly ants along the seasons, with coleopterans and ostracods rarely present in the diet.

A total of 4,079 specimens of invertebrates were found inside bromeliads, from which 1,267 were collected during the rainy season and 2,812 during the dry season, being Formicidae (ants) the most abundant taxon in both seasons (Table 1). The higher number of specimens in the dry season was mainly due to the high number of ants (81.86%; 2,302 individuals).

The diversity of invertebrates was higher in the rainy season (H'rainy = 1.533) than dry season (H'dry = 0.887; t = 12.44; p > 0.01), and the equitability of invertebrates showed higher values in the rainy season [Erainy = 0.496] than dry season [Edry = 0.279)].

Furthermore, despite the values to near zero, the Ivlev index of electivity showed positive values for ants in the rainy (Ivrainy = 0.086) and dry seasons (Ivdry = 0.023). The Ivlev index was negative for Coleoptera in both seasons (Ivrainy = -0.938; Ivdry = -0.594), the second most abundant food item in bromeliads during dry season, and the fourth in rainy season. Isoptera (termites), the second most abundant food item in bromeliads during rainy season and the sixth in dry season, were absent in the diet of Phyl­lodytes edelmoi. Also, there was significant difference between the diversity of prey consumed and inver­tebrates in bromeliads (rs = 0.2831; p = 0.1442; n = 28); this could indicate a specialist diet of P. edelmoi, with a greater preference for ants.

In the analysis of volume, we examined 1,756 specimens of invertebrates found inside bromeliads with volume ≤ 24.7 mm3 (Table 2), and ants (n = 1,208) were still the most abundant item food in bromeliads in both rainy and dry seasons, followed by larvae (Diptera; n = 128), termites (n = 113), and coleopterans (n = 42). There was a significant differ­ence between the mean of volume of ants consumed (1.8 mm3) and that inside bromeliads (2.7 mm3) (t = -8.610; p < 0.001). It can indicate a preference for smaller ants, although Phyllodytes edelmoi could eat ants with a higher mean volume (mean volume of ants = 1.8 mm³, larger ant consumed = 17.0 mm³, larger ant into bromeliads = 24.7 mm³).

Table 2. Volume (in mm3) of preys found in the stomachs of Phyllodytes edelmoi (33 individuals) and the invertebrates collected inside bromeliads in both rainy and dry seasons, locality of Serra da Saudinha, Maceió, Alagoas, northeastern Brazil. Mean ± standard error, range into parenthesis.

 

DISCUSSION

We found Phyllodytes edelmoi mainly in bromeliads of the genus Aechmea and less frequently in the smaller bromeliads Canistrum alagoanum and C. aurantiacum. Another species of the genus from the Brazilian State of Espiríto Santo, Phyllodytes luteolus, inhabits mainly the bromeliads Aechmea nudicaulis and A. blanchetiana, and rarely the species Vriesea neoglutinosa (Schineider and Teixeira, 2001; Mageski et al., 2016). Mageski et al. (2016) also observed that P. luteolus selects these plants based on specific archi­tectural characteristics (e.g., number of leaves) and physicochemical characteristics of the water (e.g., conductivity). Similarly, Eterovick (1999) showed that P. luteolus selects deeper bromeliads with lower pH. Cunha and Napoli (2016) also mentioned that P. melanomystax prefers bromeliads without or with a small amount of debris. Although our observations were preliminary and we could not corroborate that P. edelmoi selected a particular species of bromeliad, the fact of the frogs were not find in all taxa exam­ined (e.g., Hohenbergia) could suggest some form of selection of these frogs for certain breeding sites.

In anurans, there is usually a correlation between their body sizes and volume of preys consumed; this correlation could indicate the type of prey captured by the frogs (Toft, 1980). Positive correlations between body size and both mean prey volume and prey of maximum volume consumed; as well as the negative correlation between body size and the prey of minimum volume, could indicate that there is a slightly tendency for larger individu­als of Phyllodytes edelmoi to eat larger preys. Despite the fact that P. edelmoi is able to eat large preys (e.g., Isoptera and Coleoptera with volumes ≤ 24.7 mm3), our results showed that it ate predominantly ants along the sampled seasons (volume range of 0.1-17.0 mm3). Ferreira et al. (2012) reported that the mean prey size was positively correlated with the body size in individuals of P. luteolus from the State of Espírito Santo. They found that smaller specimens (SVL < 18.0 mm) fed mainly on ants, whereas larger specimens (SVL > 18.0 mm) fed mainly on termites. Another measurement, the jaw width, is also usually correlated with prey size (Parmelee, 1999; Lima et al., 2000). Although we did not test the influence of this measurement in the prey selection of P. edelmoi, Mota-Tavares et al. (2016) observed that the volume of prey consumed was influenced by the jaw width in at least two populations of P. luteolus from the Brazilian States of Bahia and Espírito Santo.

The composition of the diet of Phyllodytes edel­moi did not differ in both seasons, despite the higher values of diversity and equitability of invertebrates inside bromeliads for the rainy season. Ants were the predominant prey item, with coleopterans and ostracods rarely present in the diet. Therefore, the diet of P. edelmoi is relatively homogeneous along the seasons. However, the low values of diversity and equitability of invertebrates into bromeliads could be a consequence of the higher number of ants, which represent more than 60% of the available invertebrates in these plants.

Ants were the most abundant invertebrate collected inside bromeliads and, as mentioned above, the main prey item found in the stomachs of Phyllodytes edelmoi. Termites were the second item in abundance in bromeliads along the rainy season and the sixth in the dry season, but they were absent in the stomachs of P. edelmoi. On the other hand, P. luteolus eats ants and termites in similar proportions (Ferreira et al., 2012; Motta-Tavares et al., 2016). The preference of P. edelmoi for ants rather than termites could be a consequence of the higher numbers of ants in the bromeliads which can facilitate their capture and consumption by frogs.

Phyllodytes edelmoi can be classified as an “ant specialist” (sensu Toft, 1980; 1981). Evidences of this specialized diet are the presence of ants as main prey item for males and females and the frequency and high number of ants in the stomachs throughout the rainy and dry seasons. These results agree with Ferreira et al. (2012) and Motta-Tavares et al. (2016), who analyzed stomachs contents from males, fe­males, and juveniles of P. luteolus from four localities of the Brazilian Restinga in Bahia and Espírito Santo states. They found that P. luteolus eats preferentially ants and termites in all localities, having apparently a conservative diet, independently of the local pe­culiarities and differences among sites. Ferreira and Teixeira (2009) suggested that ant specialists have certain advantage by reducing food competition with other insectivores, since ants are unpalatable to many predators because of formic acid (Zug and Zug, 1979). Furthermore, similar to Phyllodytes luteolus, P. edelmoi can be classified into the Toft’s (1980; 1981) characterization as an active predator, those that eat preferentially small preys and have a high number of ants in their stomachs. The inver­tebrates hidden inside axils of the bromeliads also may encourage the active foraging habits of these frogs (Ferreira et al., 2012).

Ants and termites are usually present in the diet of hylid frogs (e.g., Labanick, 1976; Maneyro and Da Rosa, 2004; Vaz-Silva et al., 2005; Solé and Pelz, 2007; López et al., 2009; Moreno-Barbosa and Hoyos-Hoyos, 2014; Castro et al., 2016). However, these food items were not present in high numbers in their stomachs suggesting that they are no "ant specialists" (Toft 1980; 1981). Moreover, to better evaluate if these frogs have a diet specialized in ants and termites, it would be necessary to analyze the prey availability in their habitats (Díaz-Páez and Ortiz, 2003).

Conclusions

Our results showed that Phyllodytes edelmoi is an ant-specialist and use an active foraging strategy to capture ants, the most abundant food item inside bromeliads, and rarely eats other invertebrates. This specialist feeding behaviour commonly named as mymercophagy could be considered a synapomor­phy of the genus Phyllodytes, although this propo­sition requires additional trophic ecology studies. Furthermore, this study demonstrated that data on food resource availability are essential for the analy­sis of feeding ecology of frogs because they provide essential information for a useful categorization as generalist or specialist predators.

Acknowledgments

For access to the Herpetological Collection of the Museu de História Natural da Universidade Federal de Alagoas (MUFAL) and institutional specimen loans we thank Selma Torquato and Tami Mott. We also thank Filipe A. Nascimento, George Sena, Micheline Lima, Luana Moura, Gabriela Quintela, and Ana P. Tenório for their help and assistance in the field and Julián Faivovich, M. Celeste Luna, Cristiane N.S. Palmeira, and Fabio Machado for their comments on earlier drafts of the manuscript. Collecting permits were provided by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio 02 010.003061/05-58). Financial support and fellowships were provided by Alagoas Research Foundation (FAPEAL Procs.2004 0930160-1), São Paulo Research Foundation (FAPESP Procs. 2012/10000-5, 2013/50741-7), Consejo Nacional de Investigaciones Cientificas y Técnicas (PICT 404/2013, 820/2015), and Organización de los Es­tados Americanos (OEA).

LITERATURE CITED

1. Assis, J.S. 2000. Biogeografia e Conservação da Biodiversidade: Projeções para Alagoas. Edições Catavento. Maceió e São Paulo.         [ Links ]

2. Bokermann, W.C.A. 1966. O gênero Phyllodytes Wagler, 1830 (Anura, Hylidae). Anais da Academia Brasileira de Ciências 38: 335-344.         [ Links ]

3. Borror, D.J. & DeLong, D.M. 1988. Introdução ao estudo dos insetos. Edgard Blücher. São Paulo.         [ Links ]

4. Caramaschi, U.; Peixoto, O.L. & Rodrigues, M.T. 2004. Revalidation and redescription of Phyllodytes wuchereri (Peters, 1873) (Amphibia, Anura, Hylidae). Arquivos do Museu Nacional Rio de Janeiro 62: 185-191.         [ Links ]

5. Castro, I.M.; Rebouças, R. & Solé, M. 2016. Diet of Dendropsophus branneri (Cochran, 1948) (Anura: Hylidae) from a cocoa plantation in southern Bahia, Brazil. North-Western Journal of Zoology 12: 159-165.         [ Links ]

6. Cunha, M.S. & Napoli, M.F. 2016. Calling site selection by the bromeliad-dwelling treefrog Phyllodytes melanomystax (Amphibia: Anura: Hylidae) in a coastal sand dune habitat. Studies on Neotropical Fauna and Environment 51: 1-8.         [ Links ]

7. Díaz-Páez, H. & Ortiz, J.C. 2003. Hábitos alimentarios de Pleurodema thaul (Anura, Leptodactylidae), en Concepción, Chile. Gayana 67: 25-32.         [ Links ]

8. Dunham, A.E. 1983. Realized niche overlap, resource abundance, and intensity of interspecific competition. Pp. 261-280 in Lizard Ecology: Studies of a Model Organism (R.B. Huey; E.R. Pianka & T.W. Schoener, eds.). Cambridge, Harvard University Press, USA.         [ Links ]

9. Eterovick, P.C. 1999. Use and sharing of calling and retreat sites by Phyllodytes luteolus in a modified environment. Journal of Herpetology 33: 17-22.         [ Links ]

10. Ferreira, R.B. & Teixeira, R.L. 2009. Feeding patterns and use of reproductive habitat of the Striped Toad Rhinella crucifer (Anura: Bufonidae) from Southeastern Brazil. Acta Herpetologica 4: 125-134.         [ Links ]

11. Ferreira R.F.; Schineider, J.A.P. & Teixeira, R.L. 2012. Diet, fecundity and use of bromeliads by Phyllodytes luteolus (Anura: Hylidae) in southeastern Brazil. Journal of Herpetology 46: 19-24.         [ Links ]

12. Freire, E.M.X. & Peixoto, O.L. 2004. Phyllodytes edelmoi. The IUCN Red List of Threatened Species. Version 2017-2. Available from: http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T55832A11376763. Last access: September 26, 2017.         [ Links ]

13. Frost, D.R. 2017. Amphibian Species of the World: an Online Reference. Version 6.0. Available from: http:// research.amnh.org/herpetology/amphibia/index.html. Last access: January 20, 2017.         [ Links ]

14. Gonçalves, U. & Palmeira, C.N.S. 2016. Herpetofauna. Pp. 36-85. In: Restauração do Rio Coruripe. Um Projeto de Resgate Socioambiental. Gráfica Moura Ramos, Maceió, Alagoas, Brazil.         [ Links ]

15. Gonçalves, U. 2012. Fauna da Serra da Mão. In: Inventário da Biota da Serra da Mão, Alagoas (A. Menezes, ed.). Instituto do Meio Ambiente do Estado de Alagoas, Alagoas, Brazil.         [ Links ]

16. Juncá, F. & Borges, C.L.S. 2002. Fauna associada a bromélias terrícolas da Serra da Jibóia, Bahia. Sitientibus Série Ciências Biológicas 2: 73-81.         [ Links ]

17. Kolodiuk, M.F.; Ribeiro, L.B. & Freire, E.M.X. 2010. Diet and foraging behavior of two species of Tropidurus (Squamata, Tropiduridae) in the Caatinga of northeastern Brazil. South American Journal of Herpetology 5: 35-44.         [ Links ]

18. Krebs, C.J. 1989. Ecological Methodology. Harper and Row Publishers. New York.         [ Links ]

19. Labanick, G.M. 1976. Prey Availability, Consumption and selection in the Cricket Frog, Acris crepitans (Amphibia, Anura, Hylidae). Journal of Herpetology 10: 293-298.         [ Links ]

20. Lantyer-Silva, A.S.F.; Sole, M. & Zina, J. 2014. Reproductive biology of a bromeligenous frog endemic to the Atlantic Forest: Aparasphenodon arapapa Pimenta, Napoli and Haddad, 2009 (Anura: Hylidae). Anais da Academia Brasileira de Ciências 86: 865-880.         [ Links ]

21. Levene, H. 1960. Robust tests for equality of variances. Pp. 278-292 in Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling (I. Olkin, H. Hotelling, et alia, eds.). Stanford University Press, USA.         [ Links ]

22. Lima, A. P.; Magnusson, W.E. & Williams, D.G. 2000. Differences in diet among frogs and lizards coexisting in subtropical forests of Australia. Journal of Herpetology 34: 40-46.         [ Links ]

23. López, J.A.; Scarabotti, P.A.; Medrano, M.C. & Ghirardi, R. 2009. Is the red spotted green frog Hypsiboas punctatus (Anura: Hylidae) selecting its preys? The importance of prey availability. Revista de Biología Tropical 57: 847-857.         [ Links ]

24. Mageski, M.M.; Ferreira, M.R.B.; Beard, K.H.; Costa, L.C.; Jesus, L.P.R.; Medeiros, C.C. & Ferreira, P.D. 2016. Bromeliad selection by Phyllodytes luteolus (Anura, Hylidae): the influence of plant structure and water quality factors. Journal of Herpetology 50: 108-112.         [ Links ]

25. Magurran, A.E. 1988. Ecological Diversity and its Measurement. Cambridge University Press. United Kingdom.         [ Links ]

26. Maneyro, R. & Da Rosa, I. 2004. Temporal and spatial changes in the diet of Hyla pulchella Duméril and Bibron, 1841 (Anura: Hylidae) in Southern Uruguay. Phyllomedusa 3: 101-114.         [ Links ]

27. Maranhão, Z.C. 1976. Entomologia Geral. Nobel. São Paulo.         [ Links ]

28. Mestre, L.A.M.; Aranha, J.M.R &. Esper, M.L.P. 2001. Macroinvertebrate fauna associated to bromeliad Vriesea inflata of the Atlantic Forest (Paraná State, south Brazil). Brazilian Archives of Biology and Technology 44: 89-94.         [ Links ]

29. Moreno-Barbosa, S.E. & Hoyos-Hoyos, J.M. 2014. Ontogeny of the diet in Anurans (Amphibia) collected at La Vieja River Basin in the Departamento of Quindio (Colombia). Caldasia 36: 365-372.         [ Links ]

30. Motta-Tavares, T.; Maia-Carneiro, T.; Dantas, L.F.; Sluys, M.V.; Hatano, F.H.; Vrcibradic, D. & Rocha, C.F.D. 2016. Ecology of the bromeligenous frog Phyllodytes luteolus (Anura, Hylidae) from three resting remnants across Brazil’s coast. Anais da Academia Brasileira de Ciências 88: 93-104.

31. Moura, G.J.B.; Santos, E.M.; Oliveira, M.A.B. & Cabral, M.C.C. 2011. Herpetologia do Estado de Pernambuco. Ministério do Meio Ambiente. Brasília.         [ Links ]

32. Parmelee, J.R. 1999. Trophic ecology of a tropical anuran assemblage. Scientific Papers Natural History Museum the University of Kansas 11: 1-59.         [ Links ]

33. Peixoto, O.L. 1995. Associação de anuros e bromeliáceas na mata Atlântica. Revista da Universidade Rural, Serie Ciências da Vida, Seropédica 17: 75-83.         [ Links ]

34. Peixoto, O. L.; Caramaschi, U. & Freire, E.M.X. 2003. Two new species of Phyllodytes (Anura: Hylidae) from the State of Alagoas, Northeastern Brazil. Herpetologica 59: 235-246.         [ Links ]

35. Pertel, W.; Teixeira, R.L. & Ferreira, R.B. 2010. Comparison of diet and use of bromeliads between a bromelicolous and a bromeligenous anuran at an inselberg in the southeastern of Brazil. Caldasia 32: 149-159.         [ Links ]

36. Ruppert, E.E.; Fox, R.S. & Barnes, R.D. 2004. Invertebrate Zoology: A Functional Evolutionary Approach. Thomson, Brooks Cole. Belmonte, California.         [ Links ]

37. Schineider, J.A.P. & Teixeira, R.L. 2001. Relacionamento entre anfíbios anuros e bromélias da Restinga de Regência, Linhares, Espírito Santo, Brasil. Iheringia 62: 263-268.         [ Links ]

38. Solé, M. & Pelz, B. 2007. Do male tree frogs feed during the breeding season? Stomach flushing of five syntopic hylid species in Rio Grande do Sul, Brazil. Journal of Natural History 41: 2757-2763.         [ Links ]

39. Toft, C.A. 1980. Feeding ecology of thirtheen syntopic species of anurans in a seasonal tropical environment. Oecologia 45: 131-141.         [ Links ]

40. Toft, C.A. 1981. Feeding ecology of Panamanian litter anurans: patterns in diet and foraging mode. Journal of Herpetology 15: 129-144.         [ Links ]

41. Toft, C.A. 1985. Resource partitioning in amphibians and reptiles. Copeia 1985: 1-21.         [ Links ]

42. Vaz-Silva, W.; Frota, J.G.; Prates-Júnior, P.H. & Silva, J.S.B. 2005. Dieta de Lysapsus laevis Parker, 1935 (Anura: Hylidae) do médio Rio Tapajós, Pará, Brasil. Comunicação do Museu de Ciência e Tecnologia da PUCRS 18: 3-12.         [ Links ]

43. Vrcibradic, D. & Rocha, C.F.D. 1995. Ecological observations on the scincid lizard Mabuya agilis in a Brazilian restinga habitat Herpetological Review 26: 129-131.         [ Links ]

44. Wagler, J. 1830. Natürliches System der Amphibien, mit vorangehender Classification der Säugthiere und Vogel. Ein Beitrag zur vergleichenden Zoologie. München, Stuttgart and Tübingen. J.G. Cotta.         [ Links ]

45. Wilcox, D.; Dove, B.; McDavid, D. & Greer, D. 2002. Image tool for Windows, v 3.0. The University of Texas, Health Science Center in San Antonio. Texas. USA.         [ Links ]

46. Zug, R.G. & Zug, P.B. 1979. The Marine Toad, Bufo marinus: a natural history resume of native populations. Smithsonian Contributions to Zoology 284: 1-58.         [ Links ]