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Diet of Adenomera Hylaedactyla (Cope, 1868) (Anura: Leptodactylidae) from an Urban Area in Southern Amapá, Eastern Amazon

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Diet of Adenomera Hylaedactyla (Cope, 1868) (Anura: Leptodactylidae) from an Urban Area in Southern Amapá, Eastern Amazon Herpetology Notes, volume 12: 841-845 (2019) (published online on 12 August 2019) Diet of Adenomera hylaedactyla (Cope, 1868) (Anura: Leptodactylidae) from an urban area in southern Amapá, eastern Amazon Patrick R. Sanches1, Fillipe Pedroso-Santos1, and Carlos Eduardo Costa-Campos1,* Abstract. We describe the diet composition of Adenomera hylaedactyla based on the analysis of the stomach contents of 30 specimens from an urban area in southern Amapá State, eastern Amazon, Brazil. We found 49 items belonging to 10 prey categories. The most important prey categories were Hymenoptera (ants) (IVI = 33.2) and Hemiptera (IVI = 13.8). The correlation between snout-vent length and volume of prey was not significant. Adenomera hylaedactyla has a narrow niche breadth and their diet comprises a wide variety of items similar to prey consumed by other species of Adenomera, being ants an important resource for species within this group. Keywords. Anura, diet, niche breadth, prey availability Introduction these toxins in their skin (Biavati et al., 2004; Wells, 2007). Most anurans are generalist predators and feed Species of the Adenomera marmorata group are small mainly on arthropods, as well as on other invertebrates frogs widely distributed throughout South America and vertebrates (Duellman and Trueb, 1994; Solé within the Amazon basin. The Napo Tropical Bullfrog et al., 2010). Usually anuran diet is determined by Adenomera hylaedactyla (Cope, 1868) is a nocturnal evolutionary, behavioral and morphological traits that frog included in the A. marmorata group and is widely influence the feeding strategies and selection of prey distributed in Amazonian forests through the Guianas, type (Duellman and Trueb, 1994; Wells, 2007; Solé et in Colombia, Venezuela, Ecuador, Peru, Bolivia al., 2009; Lima et al., 2010). As result, anurans exhibit and Brazil. It can be found occupying areas of open a plasticity in trophic chains, acting both as predator vegetation, such as stream and river edges. Also, it is and as prey (Toledo et al., 2007; Oliveira et al., 2013). generally associated with primary and secondary forest, As pointed out by Toft (1981) anurans can exist in forest edges and savannah (Kokubum and Sousa, 2008; a specialist-generalist continuum concerning prey Frost, 2018). specificity. Within this continuum, major anurans are Knowledge on the ecology of Amazonian anurans is considered generalists and opportunistic in the use of still scarce, given the great diversity present. Thereby food resources (Duellman and Trueb, 1994). However, studies related to natural history also have conservational some taxa, such as Dendrobatidae, evolved a specialized aspects, helping to identify environmental conditions diet associated with the purposeful uptake of alkaloids and consequences of habitat alterations, besides adding from of certain groups of arthropods, in order to retain a deep knowledge on life history of the species that compose the Amazonian fauna (Azevedo-Ramos and Gallati, 2001; Becker et al., 2010). The feeding habits of many species, including frogs of the A. marmoratus group remains poorly understood. In the present study we investigated the diet of A. hylaedactyla from an urban 1 Universidade Federal do Amapá, Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia, Campus area in southern Amapá, eastern Amazon, and calculate Marco Zero do Equador, 68.903-419, Macapá, AP, Brazil. niche breadth and an index of relative importance for * Corresponding author. E-mail: [email protected] each prey category. 842 Patrick R. Sanches et al. Material and methods We calculated the amplitude of trophic niche through Levins’ Trophic Niche Amplitude Index (B) describe in Fieldwork was carried out in a forest fragment Pianka (1986), in which p is the numerical or volumetric surrounded by disturbed areas in the municipality of proportion of prey category i, and n is the number of Santana (0.03583º S, 51.15917º W, Datum WGS84, 26 m a.s.l.), Amapá State, Brazil. The forest fragment prey categories. comprises secondary forest, flooded forest and deforested areas (Drummod et al., 2008). According Köppen-Geiger classification for areas of Equatorial climate the annual precipitation is approximately 2850 mm concentrated between February and May, with average of about 400 mm per month, and average annual For standardized Levins’ index (Bsta) values ranging temperature ranging from 25.8 to 29.0 °C (Alvares et from 0 - 0.50 we considered the species as a specialist, al., 2013). and 0.51 - 1.0 we considered as a generalist feeder. We We collected 23 males (mean snout vent length [SVL] analyzed niche breadth using the software Ecological ± SD = 16.66 ± 1.53 mm), and 7 females (mean SVL Methodology (Krebs, 1999). ± SD = 19.52 ± 0.96 mm) of A. hylaedactyla along We performed a Spearman correlation test to the edges of a small stream during the dry season in determine the existence of correlation between snout- seasonally flooded depressions. We carried out three vent length (SVL) and body weight with the volume nocturnal inventories between November 22 and 24, of the largest prey for each individual. Statistical tests 2017 through active visual search and auditory surveys were performed using BioEstat 5.0 software (Ayres et (Crump et al., 1994), starting around 20:00h. al., 2007). Sexual differences in body size (snout-vent We euthanized the specimens in situ with using 5% length) were tested with the Student t-test. Analyzes xylocaine, soon after we fixed in 10% formalin to stop used to quantify the amplitude of the ecological niche of the digestion processes. The specimens collected were the species were carried out in the program Ecosim 7.0 stored in 70% alcohol and had they stomachs dissected (Gotelli and Entsminger, 2001). All statistical analysis to access the food content (Heyer et al., 1994). We were performed with a significance level of α = 0.05. extracted the stomach contents of anurans through a ventral incision and stored all contents found in 70% Results alcohol. Afterwards we identified the prey categories at the level of order and family (Formicidae) under stereo We collected 30 specimens of A. hylaedactyla, with microscopes with the aid of dichotomy keys provided SVL ranging from 13.1 to 19.1 mm (16.66 ± 1.53 mm) by Rafael et al. (2012). and 17.8 to 20.7 mm (19.52 ± 0.96 mm) for males and For each identified prey category, we calculated females, respectively. The body mass of males varied the number, volume and frequency of occurrence in from 0.1 to 1.0 g (0.5 ± 0.2 g) and females varied from absolute and percentage values. We calculated volume 0.6 to 1.2 g (0.8 ± 0.2 g). Six individuals had an empty by using the measure of length and weight of each stomach, of which five were male and one female. Adult prey item found and we applied the Ellipsoid Volume males were significantly smaller than adult females in Formula: where l = the prey length and w = the prey terms of SVL (t = -4.2896; p < 0.001), and body mass (t width (Magnusson et al., 2003). = -3.7208, p = 0.0004). We found forty-nine items belonging to 10 categories of prey (Table 1). The most numerically abundant prey were Formicidae (44.89%) and Acari (12.24%), while the most representative regarding volume were Hemiptera We assessed the importance value index (IVI) of each (28.61%) and Araneae (22.80%). The importance prey in the diet using the sum of the percentages of value index showed that the diet of A. hylaedactyla was number (N%), frequency (F%) and volume (V%) (cf. dominated by the prey taxa Formicidae (IVI = 33.2) Gadsden and Palácios-Orona, 1997). and Hemiptera (IVI = 13.8). The prey volume has not increased with SVL or weight, as our analysis showed no significant correlation between SVL and volume of prey (rs = 0.0051, p = 0.9821, Figure 1) and weight and Table 1. Prey consumed by Adenomera hylaedactyla (n = 30) in a várzea forest, municipality of Santana, Diet of AdenomeraAmapá, Brazil. hylaedactyla N = number; from F =an frequency urban area of prey; in eastern V = volume Amazon of prey; IVI = importance value index. Values 843 and their relative percentages Table 1. Prey consumed by Adenomera hylaedactyla (n = 30) in a várzea forest, municipality of Santana, Amapá, Brazil. N = number; F = frequency of prey; V = volume of prey; IVI = importance value index. Values and their relative percentages Prey N N% F F% V V% IVI Acari 6 12.2 5 11.1 2.35 1.4 8.2 Araneae 3 6.1 3 6.7 39.26 22.8 11.9 Coleoptera 5 10.2 5 11.1 15.12 8.8 10.1 Coleoptera Larvae 2 4.1 2 4.4 27.58 16.1 8.9 Collembola 3 6.1 3 6.7 4.72 2.7 5.2 Diptera 2 4.1 2 4.4 3.58 2.1 3.5 Diptera Larvae 2 4.1 1 2.3 2.56 1.5 2.6 Hemiptera 3 6.1 3 6.7 49.28 28.6 13.8 Hymenoptera 1 2.1 1 2.2 9.73 5.6 3.3 Formicidae 22 44.9 20 44.4 17.98 10.4 33.3 Total 49 100 45 100 172.21 100 100.8 volume of prey (rs = -0.0865, p = 0.7019, Figure 2). The hylaedactyla (Vitt and Caldwell, 1994), in general the standardized Levins’ index (Bsta) was 0.34. diet seems to be similar among the species. Diet composition of A. hylaedactyla revealed Discussion Formicidae as the most important prey category and has Five previous studies have examined the stomach already been observed in the diet of A. thomei (Rebouças content of Adenomera species, A. hylaedactyla (Vitt and and Solé, 2015) and A.
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