NORTH-WESTERN JOURNAL OF ZOOLOGY 9 (1): 157-165 ©NwjZ, Oradea, Romania, 2013 Article No.: 131506 http://biozoojournals.3x.ro/nwjz/index.html
Feeding habits, microhabitat use, and daily activity period of Rhinella ornata (Anura, Bufonidae) from three Atlantic rainforest remnants in southeastern Brazil
Thiago MAIA-CARNEIRO1*, Mara Cíntia KIEFER2, Monique VAN SLUYS1,3 and Carlos Frederico Duarte ROCHA1
1. Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier 524, CEP 20550-019, Rio de Janeiro, Brazil. 2. Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense Caixa Postal 100436, Centro, 24020-971 Niterói, Rio de Janeiro, Brazil. 3. Life Sciences, Research and Conservation, Taronga Conservation Society Australia, Bradley's Head Road, Mosman, NSW 2088, Australia. [current address] *Corresponding author, T. Maia-Carneiro, E-mail: [email protected]
Received: 14. May 2012 / Accepted: 23. January 2013 / Available online: 12. February 2013 / Printed: June 2013
Abstract. Herein, we analyzed microhabitat use, daily activity period, and diet of three populations of Rhinella ornata from three Brazilian Atlantic rainforest remnants: Estação Ecológica Estadual Paraíso (EEEP), Reserva Ecológica de Guapiaçu (REGUA), and Morro São João (MSJ). Leaf litter (35.2%) and bare ground (29.4%) were the microhabitats where most anurans were first sighted. Activity was predominantly nocturnal, and juveniles, opposed to adults, were active also during daylight. Diet was composed predominantly by arthropods, mainly Formicidae and Coleoptera. Isoptera was of relevance in the MSJ’s
population. The similarity of the trophic niche (Oij) of R. ornata between populations in terms of numerical proportion of food categories consumed was 0.999 between EEEP and REGUA, 0.523 between EEEP and MSJ, and 0.505 between REGUA and MSJ, and in terms of volumetric proportion was 0.689 between EEEP and REGUA, 0.300 between EEEP and MSJ, and 0.126 between REGUA and MSJ. The mean number and the mean volume of food items consumed per individual were higher in MSJ, and there was no difference between EEEP and REGUA. These differences might have occurred due to differences in prey availability among these areas. These results reveal some level of variability in prey types consumed among populations. The number of food items was related with the SVL in EEEP, and the jaw width affected the volume of food items ingested in the three populations studied. This may occur due to smaller-sized prey become energetically less favorable with increase of anurans’ body size and also because smaller individuals are relatively constrained by jaw width. Flexibility in prey consumed may result in a low trophic similarity among different populations of R. ornata, and might represent an advantage in environments with varying prey availability.
Key words: activity, diet, inter-populational variation, habitat use, trophic ecology.
Introduction Carneiro et al. 2012). Some species exhibit varia- tion in these ecological parameters (Smith & Bragg Anuran communities of Atlantic rainforest have 1949, Duellman & Trueb 1986, Hodgkison & Hero been studied on different ecological perspectives 2003, Miranda et al. 2006, Dorigo et al. 2012), de- such as activity patterns (Rocha et al., 2000, 2001, pending on the ontogeny and on the changes of 2011), habitat use (Juncá 2006, Van Sluys et al. environmental characteristics. 2007), and feeding habits (Siqueira et al. 2006, The specific name Rhinella crucifer (Wied- Martins et al. 2010, Dorigo et al. 2012, Maia- Neuwied, 1821) encompass a complex group of Carneiro et al. 2012). Anurans seem to be active anurans with broad geographic distribution in At- predominantly at the crepuscular and nocturnal lantic rainforest and its areas of influence, and ac- periods (Rocha et al. 2000, 2001, 2011), use differ- tually is composed by five distinct species: R. cru- ent microhabitats (Juncá 2006, Almeida-Gomes et cifer, R. abei (Baldissera-Jr et al. 2004), R. henseli (A. al. 2007a,b, Galdino et al. 2008, Martins et al. 2010, Lutz, 1934), R. pombali (Baldissera-Jr et al. 2004), Dorigo et al. 2012, Maia-Carneiro et al. 2012), and and R. ornata (Spix, 1824) (all referred to as belong- their main food source are invertebrates that in- ing to the genus Bufo - Baldissera et al. 2004). habit leaf litter (Giaretta et al. 1998, Van Sluys et Rhinella ornata is found in Brazilian Atlantic rain- al. 2001, Marra et al. 2004, Sabagh & Carvalho-e- forest remnants from southern of the state of Silva 2008, Ferreira & Teixeira 2009, Almeida- Espírito Santo to the north of the state of Paraná, Santos et al. 2011, Dorigo et al. 2012, Maia- and possibly in northeastern Argentina in the 158 T. Maia-Carneiro et al. provinces of Missiones and Corrientes (Baldissera (hereafter VES; Crump & Scott 1994) and Pitfall Traps et al. 2004, Frost 2012). Individuals of this species with Drift Fences (Corn 1994). VES were performed by seem to be reasonably tolerant to changes in the transects (30 minutes) during which observers walked slowly through the forest carefully looking for anurans on habitat (Baldissera 2010, personal observation), oc- the floor, under and on logs, twigs, roots and stones, as curring both in forested and disturbed areas. well as on the vegetation. Some water bodies such as shal- Available data on the ecology of R. ornata is low rivulets and streams were also surveyed during VES. scarce and restricted to information on reproduc- Transects were conducted during the day, dusk and tive modes and strategies (Pombal-Jr. & Haddad night, totaling 267 hours of active search (34.5 hours in 2005, 2007), its importance to the energy flow be- each period in EEEP and in REGUA and 20 hours in each tween freshwater and terrestrial environments period in MSJ). Three pitfall traps systems were used for sampling in EEEP and in REGUA and two in MSJ. Each (Ohashi & Silva 2009), habitat usage (e.g., Silva et system consisted of ten 30-liter buckets buried in the al. 2008, Prado et al. 2009, Silva-Soares et al. 2010), ground and set approximately 5 m apart of each other, and daily activity (Ohashi & Silva 2009, Rocha et with soft plastic drift fences about 50 cm high extended al. 2011). Considering the few available knowl- between them. The ten buckets were arranged in line at edge with regard to biological parameters of this random points of the forest and checked once daily, al- species, in this study we investigated aspects of its ways in the morning. Pitfall traps were sampled for 20 ecology, which contribute to the understanding of days (600 bucket-days) in EEEP and in REGUA, and 15 days (300 bucket-days) in MSJ. its participation in the ecological processes.
Herein, we evaluate microhabitat use, daily activ- Data analyses ity period and feeding habits of R. ornata popula- We measured the snout-vent length (SVL) and jaw width tions from three remnants of Atlantic rainforest in (JW) of the sampled toads with a digital caliper (precision southeastern Brazil, analyzing the occurrence of of 0.01 mm). Individuals were categorized as adults or ju- inter-populational differences in these parameters. veniles by consulting Hartmann et al. (2010) and Baldis- sera et al. (2004), which provide mean SVL of adult males
and females of R. ornata. Individuals which had SVL
smaller than that reported by these authors were consid- Material and Methods ered as juveniles. To evaluate the frequency of microhabi- Study areas tats used by R. ornata we considered only those individu- This study was carried out in three Atlantic rainforest als found during VES, which had the type of their sur- remnants in the state of Rio de Janeiro, southeastern Bra- roundings recorded when first seen (leaf litter, bare zil. The Estação Ecológica Estadual Paraíso (EEEP) ground, grass, rock, and wood). The daily activity period (22°29'S, 42°54'W), located in the municipalities of Gua- (diurnal, crepuscular and nocturnal) was estimated based pimirim and Cachoeiras de Macacu, occupies an area of on the number of individuals found active in each of the approximately 5,000 ha. The climate in EEEP is wet and three periods sampled during VES. warm, with mean annual precipitation ranging between Animal food items were identified through stereomi- 2,000 and 3,000 mm, and the mean annual temperature is croscope to the level of Order, and Family in the case of around 23°C (Kurtz & Araújo 2000). The Reserva Formicidae. Arthropod remains that could not be identi- Ecológica de Guapiaçú (REGUA) (22º24'S, 42º44'W) is lo- fied were grouped in the category “arthropod remains”. cated in the municipality of Cachoeiras de Macacu and The diet of R. ornata was analyzed in terms of number, has an area of 2,558 ha. In REGUA, the annual rainfall volume and frequency of occurrence of items. Food items varies from 2,000 mm to 2,500 mm, and mean tempera- were counted and measured in their length and width ture is around 24ºC (Rocha et al. 2007). These two re- with a digital caliper (precision of 0.01 mm) and their serves are within one of the largest portions of Atlantic volume was estimated using the formula of the ovoid- rainforest (60,000 ha) in Rio Janeiro and have areas with spheroid [V = 4 / 3.π. (L / 2) (W / 2) 2], where L is the different levels of conservation. Morro São João (MSJ) length and W is the width of the item (Dunham 1983). (22°33'S, 41°01'W) is an area of Atlantic rainforest in the The frequency of occurrence of each food item category in municipality of Casimiro de Abreu which has volcanic the diet was expressed as the number of stomachs that origin, reaching to 800 m elevation, and is covered by 640 contained the category. To assess the degree of trophic ha of secondary forest (Almeida-Gomes et al. 2008). The niche similarity among R. ornata populations we com- mean annual rainfall at the MSJ is 1,140 mm (data for the pared the numerical and volumetric proportions of food nearby city of Barra de São João) (Barbieri & Coe-Neto categories between populations through the Pianka’s 1999). Trophic Niche Overlap Index [Ojk = Σ pij pik / √ Σ (pij2) (pik2)], where pij and pik are the volumetric/numerical Data collection proportions of the food category i recorded in the diet of We collected individuals of R. ornata in EEEP during late populations j and k, respectively (Pianka 1973). Differ- September and early October 2004, in REGUA during late ences in the mean number and in the mean volume of October and November 2004 and in MSJ during late May items consumed among populations were tested using a and early June 2005 through Visual Encounter Surveys One-Way Analysis of Variance (ANOVA) followed by Ecology of Rhinella ornata 159
Scheffe’s post hoc test (Zar 1999). The relationship be- and grass (40%), and in MSJ mostly leaf litter tween the number of food items consumed by individual (42.9%) and bare ground (42.9%) (Table 1). and the SVL and the relationship between the mean vol- The daily activity period was recorded for 18 ume of the five (or less when there was no more than five individuals, and most anurans were found during items in the stomach content) largest items ingested and the JW were tested by Simple Regression Analyses (Zar nocturnal transects (55.5%) (Table 2). In EEEP and 1999). in MSJ, the highest number of individuals was The results for the descriptive statistics are presented found during nocturnal transects (80% and 50%, throughout the text as mean ± standard deviation. All respectively). In REGUA, a similar number of in- data were tested for homocedasticity of variances and for dividuals were found during nocturnal (42.9%) the normality of distribution before performing statistical and diurnal (42.8%) transects. We found only ju- analyses, and were log-transformed to achieve these veniles (N = 5 individuals) during diurnal tran- premises when necessary (Zar 1999). All statistical analy- ses were done using SYSTAT 11® software. All specimens sects, three in REGUA (42.8%) and two in MSJ analyzed shall be deposited in the herpetological collec- (33.3%) (Table 2). tion of the Museu Nacional, Rio de Janeiro. As shown in the Table 3, of the total number of individuals, 39 were used for dietary analyses (two individuals from REGUA cannot be in- Results cluded). Only one individual from EEEP (9.0%) and one individual from MSJ (7.7%) had empty We collected 41 individuals of Rhinella ornata dur- stomachs. In EEEP and in REGUA, in numerical ing this study, 11 being in EEEP, 17 in REGUA, terms, the diet was composed predominantly by and 13 in MSJ. We recorded five microhabitat Formicidae (73.3% and 76.2%, respectively), fol- categories (leaf litter, bare ground, grass, rock, and lowed by Coleoptera (14.3% and 16.3%, respec- wood) for R. ornata (N = 17 individuals) from the tively). In MSJ, numerically, R. ornata consumed three populations. The leaf litter of the forest floor predominantly Isoptera (56%) and Formicidae (35.2%) and the bare ground (29.4%) were the mi- (32.4%). Volumetrically, in EEEP, Formicidae crohabitats where most toads were first sighted (35.2%) was the most important food item, fol- (Table 1). In EEEP, the toads used mainly wood lowed by Coleoptera (23.8%). In terms of volume, (40%), in REGUA predominantly leaf litter (40%) Orthoptera (33.6%), Formicidae (28.4%) and Col-
Table 1. Microhabitat use by individuals (frequency in %) of Rhinella ornata (N = 17) in Atlantic rainforest of the Estação Ecológica Estadual Paraíso (EEEP; N = 5), Reserva Ecológica de Guapiaçu (REGUA; N = 7) and Morro São João (MSJ; N = 5), in the state of Rio de Janeiro, southeastern Brazil. ] Locality Microhabitat Total (%) EEEP (%) REGUA (%) MSJ (%) Leaf litter 1 (20) 2 (40) 3 (42.9) 6 (35.2) Bare ground 1 (20) 1 (20) 3 (42.9) 5 (29.4) Grass _ 2 (40) _ 2 (11.8) Rock 1 (20) _ 1 (14.2) 2 (11.8) Wood 2 (40) _ _ 2 (11.8) Total 5 (100) 5 (100) 7 (100) 17 (100)
Table 2. Number and frequency (%) of juveniles (N = 5) and adults (N = 13) of Rhinella ornata (N = 18) recorded during diurnal, crepuscular and nocturnal transects of visual encounter surveys in Atlantic rainforest of the Esta- ção Ecológica Estadual Paraíso (EEEP; N = 5), Reserva Ecológica de Guapiaçu (REGUA; N = 7) and Morro São João (MSJ; N = 6) in the state of Rio de Janeiro, southeastern Brazil.
Diurnal (%) Crepuscular (%) Nocturnal (%) Locality Total (%) Juveniles Adults Juveniles Adults Juveniles Adults EEEP _ _ _ 1 (20) 1 (20) 3 (60) 5 (27.8) REGUA 3 (42.8) _ _ 1 (14.3) 2 (28.6) 1 (14.3) 7 (38.9) MSJ 2 (33.3) _ _ 1 (16.7) 1 (16.7) 2 (33.3) 6 (33.3) 5 (27.8) _ _ 3 (16.7) 4 (22.2) 6 (33.3) TOTAL 18 (100) 5 (27.8) 3 (16.7) 10 (55.5) 160 T. Maia-Carneiro et al.
Table 3. Diet composition of Rhinella ornata (N = 39) from three Atlantic rainforest remnants in the state of Rio de Ja- neiro, southeastern Brazil, showing the number (N), volume (V, in mm3), and frequency of occurrence (F) of each food item (percentages in parentheses). In the first column L = larvae.
Prey Estação Ecológica Estadual Paraíso (n = 11) Reserva Ecológica de Guapiaçu (n = 15) N (%) V (%) F (%) N (%) V (%) F (%) Gastropoda ______Arachnida Araneae _ _ _ 1 (0.4) 9.8 (0.1) 1 (6.7) Diplopoda 1 (1.0) 8.2 (0.3) 1 (9) 2 (0.8) 16.6 (0.2) 2 (13.3) Chilopoda 1 (1.0) 6.2 (0.2) 1 (9) _ _ _ Hexapoda Collembola 2 (1.9) 2.2 (0.1) 1 (9) _ _ _ Microcoryphia 1 (1.0) 2.6 (0.1) 1 (9) _ _ _ Orthoptera 2 (1.9) 379.4 (14.8) 2 (18) 3 (1.3) 2240.5 (33.6) 3 (20.0) Isoptera 2 (1.9) 213 (8.3) 1 (9) 1 (0.4) 3.6 (0.1) 1 (6.7) Blattodea ______Hemiptera 4 (3.8) 205.5 (8.0) 3 (27) 5 (2.1) 370.4 (5.6) 5 (33.3) Coleoptera 15 (14.3) 608.8 (23.8) 6 (55) 39 (16.3) 1461.3 (21.9) 13 (86.7) Hymenoptera Formicidae 77 (73.3) 900.5 (35.2) 10 (91) 182 (76.2) 1898.5 (28.4) 15 (100) Other Hymenoptera _ _ _ 2 (0.8) 20.5 (0.3) 2 (13.3) Lepidoptera (L) _ _ _ 2 (0.8) 211.1 (3.2) 2 (13.3) Diptera (L) _ _ _ 2 (0.8) 11.2 (0.2) 1 (6.7) Arthropod remains ______Plant remains _ 231.1 (9.0) 8 (73) _ 429.8 (6.4) 1 (6.7) Total 105 (100) 2557.51 (100) _ 239 (100) 6673.3 (100) _
Prey Morro São João (n = 13) N (%) V (%) F (%) Gastropoda 3 (0.8) 27.4 (0.1) 1 (7.7) Arachnida Araneae 3 (0.8) 77.2 (0.4) 2 (15.4) Diplopoda 4 (1.0) 348.3 (1.6) 3 (23.1) Chilopoda 2 (0.5) 476.9 (2.2) 1 (7.7) Hexapoda Collembola _ _ _ Microcoryphia _ _ _ Orthoptera 3 (0.8) 874.4 (4.0) 2 (15.4) Isoptera 222 (55.9) 15991.7 (73.3) 9 (69.2) Blattodea 1 (0.3) 10.4 (0.05) 1 (7.7) Hemiptera 1 (0.3) 22.6 (0.1) 1 (7.7) Coleoptera 15 (3.8) 1333.6 (6.1) 7 (53.8) Hymenoptera Formicidae 129 (32.5) 1282.7 (5.9) 11 (84.6) Other Hymenoptera 10 (2.5) 392.9 (1.8) 1 (7.7) Lepidoptera (L) 3 (0.8) 213.2 (1.0) 2 (15.4) Diptera (L) _ _ _ Arthropod remains _ 48.1 (0.2) 1 (7.7) Plant remains _ 729.5 (3.3) 11 (84.6) Total 397 (100) 21828.9 (100) _
eoptera (21.9%) were predominant in REGUA. In als examined, and Coleoptera in 86.7% of them. In MSJ, volumetrically, Isoptera was the most impor- MSJ, in terms of frequency of occurrence, Formici- tant food item (73.3%), followed by Coleoptera dae (84.6%) and Isoptera (69.2%) were the most (6.1%). In terms of frequency, in EEEP, Formicidae consumed food items. was found in 91% of the toads analyzed, followed The trophic niche overlap (Oij) between popu- by vegetal residues (73%) and Coleoptera (55%). lations, in terms of numerical proportion of food In REGUA, Formicidae was found in all individu- categories consumed, was 0.999 between EEEP Ecology of Rhinella ornata 161
a. b.
Figure 1. Number (a) (in log) and volume (b) (mm3, log-transformed) of prey consumed by Rhinella ornata toads (N = 39) in Atlantic rainforest of the Estação Ecológica Estadual Paraíso (EEEP; N = 11), Reserva Ecológica de Gua- piaçu (REGUA; N = 15) and Morro São João (MSJ; N = 13), in the state of Rio de Janeiro, southeastern Brazil. Both number and volume of prey consumed were greater in MSJ than in EEEP and in REGUA, and there were no differ- ences between EEEP and REGUA.
and REGUA, 0.523 between EEEP and MSJ, and (Scheffe, P = 0.864) (Fig. 1b). 0.505 between REGUA and MSJ. Considering The snout-vent length of R. ornata in this study volumetric proportion of food items the value of was 53.3 ± 14.0 mm (range: 29.6 – 71.6 mm, N = 11) Oij was 0.689 between EEEP and REGUA, 0.300 be- in EEEP, 41.4 ± 17.4 mm (range: 23.5 – 87.4 mm, N tween EEEP and MSJ, and 0.126 between REGUA = 17) in REGUA, and 56.6 ± 16.4 mm (range: 33.5 – and MSJ. 91.9 mm, N = 13) in MSJ. The number of food The mean number of food items consumed items was statistically significantly related (Simple was 10.5 ± 5.8 (range = 4.0 – 22.0, N = 10) in EEEP, Regression Analysis, R2 = 0.548, F1,8 = 9.685, P = 15.9 ± 9.5 (range = 5.0 – 33.0, N = 15) in REGUA, 0.014) to the SVL of individuals in EEEP, but this and 33.0 ± 22.0 (range = 14.0 – 75.0, N = 12) in MSJ. relationship did not occurred in REGUA (F1,13 =
There were statistically significant differences 0.293, P = 0.598), and in MSJ (F1,10 = 0.027, P =
(ANOVA, R2 = 0.365, F2,34 = 9.761, P < 0.001) in 0.873). number of food items consumed among popula- The jaw width of the toads in this study was tions, being higher in MSJ compared to EEEP 20.1 ± 5.6 mm (range: 11.1 – 27.4 mm, N = 10) in (Scheffe, P = 0.001) and to REGUA (Scheffe, P = EEEP, 15.2 ± 6.9 mm (range: 8.5 – 33.0 mm, N = 15) 0.014) (Fig. 1a). There was no statistically signifi- in REGUA, and 20.9 ± 6.6 mm (range: 12.1 – 37.2 cant difference in number of food items ingested mm, N = 12) in MSJ. The volume of largest food between EEEP and REGUA (Scheffe, P = 0.324) items consumed by R. ornata was significant re- (Fig. 1a). lated to JW in all populations studied (Simple Re-
The mean volume of the largest food items in- gression Analyses; EEEP: R2 = 0.794, F1,8 = 30.860, gested was 37.4 ± 31.2 mm³ (range = 1.3 – 83.8 P = 0.001; REGUA: R2 = 0.730, F1,13 = 35.140, P < mm³, N = 10) in EEEP, 65.9 ± 105.4 mm³ (range = 0.0001; MSJ: R2= 0.521, F1,10 = 10.870, P = 0.008). 4.4 – 360.6 mm³, N = 15) in REGUA, and 120.1 ± 82.8 mm³ (range = 51.8 – 292.7 mm³, N = 12) in MSJ. There was statistically significant differences Discussion
(ANOVA, R2 = 0.261, F2,34 = 6.016, P = 0.006) in the mean volume of the largest food items consumed Evaluation of our data indicated that Rhinella or- among populations. Individuals from MSJ con- nata occupy different microhabitats in the forest, sumed larger items when compared to individuals and use mostly leaf litter. Other studies have also from EEEP (Scheffe, P = 0.014) and from REGUA reported that these toads use a variety of habitats, (Scheffe, P = 0.025) (Fig. 1b). There was no statisti- including leaf litter in forests (Silva et al. 2008, cally significant difference in the mean volume of Prado et al. 2009, Silva-Soares et al. 2010, Rocha et food items ingested between EEEP and REGUA al. 2011). Despite this species can occur in human- 162 T. Maia-Carneiro et al. modified environments, data from literature (Silva 1981, Teixeira et al. 1999, Rosa et al. 2002, Sabagh et al. 2008, Prado et al. 2009, Silva-Soares et al. & Carvalho-e-Silva 2008, Duré et al. 2009, Ferreira 2010, Rocha et al. 2011) together with that of our & Teixeira 2009, Quiroga et al. 2009, Batista et al. study reveal that R. ornata are often associated to 2011). Some authors consider bufonids as oppor- the leaf litter of forest ground, which suggests tunistic foragers, and argue that the abundance of some level of dependence of forested areas. These formicids and coleopterans in their diets reflects toads seem to have a predominantly horizontal the availability of these prey types in the envi- habitat use, characterizing it as a terricolous spe- ronment (Smith & Bragg 1949, Berry & Bullock cies, such as other anuran species (Rocha et al. 1962, Evans & Lampo 1996, Batista et al. 2011). In 2000, 2001, 2011, Almeida-Gomes et al. 2007b, one of these studies (Smith and Bragg, 1949), the Martins et al. 2010), including bufonids (Silva et al. authors observed the bufonids Anaxyrus wood- 2008, Duré et al. 2009), which frequently use housii (Girard, 1854) and A. cognatus (Say, 1822) ground as microhabitat. (referred to as Bufo woodhousii woodhousii and B. Analysis of the results obtained in this study cognatus, respectively) during feeding and re- suggests that R. ornata has an extensive daily activ- ported occasional prey capture by the toads and ity period (daytime, dusk, and night), but with a no tendency to move toward any direction. Other tendency for a nocturnal activity. Other studies authors consider bufonids to be ant-specialists also reported that individuals of this species were (Toft 1980, Flowers & Graves 1995, Isacch & Barg found at diurnal and nocturnal periods (Ohashi & 2002, Rosa et al. 2002) because of the high propor- Silva 2009, Rocha et al. 2011). These results are tion of this prey type in their diets. Herein, we similar to different leaf litter anuran species inhab- cannot affirm if the toads chose or consumed ants iting the Atlantic rainforest (e.g. Rocha et al. 2000, according to their supply, due to the absence of 2001, 2011; Almeida-Gomes et al. 2007b, Maia- data on prey availability in the environment. Carneiro et al. 2012). In general, amphibians have The consumption of a relatively high variety activity during the nocturnal period, avoiding food items by R. ornata in the three populations high temperatures and low atmospheric humidity studied suggests generalist and opportunistic for- during daytime. Nevertheless, some species can aging habits, with prey consumed according to its start the activity during the diurnal period (Smith availability in the environment. In this case, the & Bragg 1949, Almeida-Gomes et al. 2007b, Ohashi high occurrence of Isoptera in the diet of MSJ & Silva 2009, Rocha et al. 2011, Van Sluys & population could be explained by characteristics Guido-Castro, 2011). Though we found active ju- of the area. The EEEP and the REGUA are rela- veniles and adults at night, all individuals found tively large areas that have similar environmental active at the crepuscular period were adults, and characteristics and close proximity to each other only juveniles were found during daytime. In (ca. 9 km apart). On the other hand, the MSJ is a some bufonid species, juveniles tend to be active small fragment in an area of volcanic origin sur- during the diurnal period, as opposed to co- rounded by a matrix of crop and animal cultiva- specifics adults (Smith & Bragg 1949, Duellman & tion, located farthest from EEEP and REGUA, and Trueb 1986, Ohashi & Silva 2009), a trend similar with lower mean annual rainfall compared to to that we found in this study for R. ornata. these two areas. Moreover, the MSJ was sampled Evaluation of our data revealed that R. ornata only during the dry season, when arthropod consumed a variety of prey types, predominantly availability in the environment is usually reduced arthropods, mainly insects such as Formicidae, in tropical forests (Tanaka & Tanaka 1982, Levings Coleoptera and Isoptera, prey commonly found in & Windsor 1985, Pearson & Derr 1986), including the diet of anurans overall (e.g., Toft 1980, 1981, lower abundance of Formicidae when moisture Van Sluys & Rocha 1998, Teixeira et al. 1999, Van decreases (Levings 1983). These factors may have Sluys et al. 2001, Rosa et al. 2002, Marra et al. 2004, caused differences in prey availability, and conse- Bull 2006, Sabagh & Carvalho-e-Silva 2008, Duré quently in prey consumed by R. ornata among et al. 2009, Ferreira & Teixeira 2009, Quiroga et al. these areas. The individuals of R. ornata might 2009, Martins et al. 2010, Almeida-Santos et al. have largely consumed Isoptera to maintain a 2011, Dorigo et al. 2012, Maia-Carneiro et al. 2012). positive energetic balance under low prey avail- Formicidae was the most frequent prey item in the ability (see Schoener 1971) in MSJ. In Brazilian diet in all studied areas, a tendency already re- Cerrado Biome, there was a high consumption of corded for bufonids in general (Toft 1980,Toft Formicidae by Rhinella scitula (Caramaschi & Ecology of Rhinella ornata 163
Niemeyer, 2003) in the rainy season, and Isoptera mostly used by the individuals are frequently as- had lower relevance in its diet than during the dry sociated with the floor of forested areas, which season (Maragno & Souza 2011). These authors suggest some level of dependence of forests. An- suggested that the association between lower urans of this species are active mainly during the availability of ants and their lower mobility in the nocturnal period, though they can be found also at habitat in the dry season might have caused the dusk and daytime. Although Formicidae and Col- seasonal differences in prey consumption eoptera were important food items for R. ornata in (Maragno & Souza 2011). A similar event may general, this species have some degree of variabil- have occurred in MSJ, resulting in greater con- ity in the prey types that they can eat. These toads sumption of Isoptera by R. ornata. can change the most consumed food items, with The results of the overlap index couple to the other prey types being important depending on argument of differences in prey availability among the population. Such flexibility in prey consumed areas, since the overlaps (both in numerical and may result in a low trophic similarity among dif- volumetric terms) of prey consumed were highest ferent populations of this species, and might rep- between EEEP and REGUA and lowest between resent an advantage in environments with varying EEEP and MSJ and between REGUA and MSJ. prey availability. This presumably occurred due to the higher con- sumption of Isoptera in MSJ compared to EEEP and to REGUA, a prey type that was also impor- Acknowledgements. This study was supported by tant in the diet of Rhinella granulosa (Spix, 1824) in research grants from the Conselho Nacional de northeastern Argentina (probably due to its high Desenvolvimento Científico e Tecnológico (CNPq) to availability in the local environment - Duré et al. C.F.D. Rocha (processes 304791/2010-5 and 470265/2010- 2009), and of R. scitula in the Cerrado (Maragno & 8), M. Van Sluys (process 307773/2008-6) and M.C. Kiefer Souza 2011). Although Formicidae and Coleoptera (process 150353/2003-0). C.F.D. Rocha also received a were important prey in the diet of R. ornata, these grant from the Fundação de Amparo à Pesquisa do toads apparently might feed on different prey Estado do Rio de Janeiro (FAPERJ) through the “Programa Cientistas do Nosso Estado” (process E- types depending of local prey availability. Some 26/102.404.2009). M.C. Kiefer also received research authors suggested that the consumption of plant scholarship from FAPERJ (Process No. E- material may sometimes be voluntary (Silva et al. 26/171.168/2006). T. Maia-Carneiro received a MSc 1989, Das 1996), however, plant remains such as scholarship from the Coordenação de Aperfeiçoamento seeds, twigs and leaves found in the diet of R. or- de Pessoal de Nível Superior (CAPES) and, actually, nata were considered as result of accidental inges- receives PhD scholarship from CAPES. We also thank P. tion at the moment of prey capture by the indi- Almeida-Santos for her help with laboratory analyses and D. Vrcibradic for his aid and helpful suggestions in an viduals because of its low volumetric importance. earlier version of the manuscript. We also thank for the Analysis of our data indicated that larger help of friends during data collection. toads consume more and larger prey, similar to other studies with anurans (Lima & Moreira 1993, Van Sluys et al. 2001, Marra et al. 2004, Dietl et al. 2009, Martins et al. 2010). This trend is expected References because anurans do not chew food, eating their Almeida-Gomes, M., Hatano, F.H., Van Sluys, M., Rocha, C.F.D. prey whole (Duellman & Trueb 1986), therefore (2007a): Diet and microhabitat use by two Hylodinae species probably as smaller prey become energetically less (Anura, Cycloramphidae) living in sympatry and syntopy in a Brazilian Atlantic Rainforest area. Iheringia 97(1): 27-30. favorable with increasing of the body size of an- Almeida-Gomes, M., Van Sluys, M., Rocha, C.F.D. (2007b): urans the consumption of more and larger prey Ecological observations on the leaf-litter frog Adenomera may result in a positive energetic balance. Fur- marmorata in an Atlantic rainforest area of southeastern Brazil. Herpetological Journal 17: 81-85. thermore, smaller-sized individuals are relatively Almeida-Gomes, M., Vrcibradic, D., Siqueira, C.C., Kiefer, M.C., constrained by jaw width concerning prey sizes Klaion, T., Almeida-Santos, P., Nascimento, D., Ariani, C.V., that can be swallowed by them. Borges-Júnior, V.N.T., Freitas-Filho, R.F., Van Sluys, M., Rocha, C.F.D. (2008): Herpetofauna of an Atlantic rainforest área Overall, evaluation of our data showed that (Morro São João) in Rio de Janeiro State, Brazil. Anais da Rhinella ornata is an anuran species which has a Academia Brasileira de Ciências 80: 291-300. predominantly horizontal habitat use. Though this Almeida-Santos, M., Siqueira, C.C., Van Sluys, M., Rocha, C.F.D. (2011): Ecology of the Brazilian fleafrog Brachycephalus didactylus species is reasonably tolerant to environments (Terrarana: Brachycephalidae). 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