Acta Herpetologica 11(1): 1-13, 2016 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-17147 Feeding habits of Mesoclemmys vanderhaegei (Testudines: Chelidae) Elizângela Silva Brito1,*, Franco Leandro Souza2, Christine Strüssmann3 1 Programa de Pós-graduação em Biologia de Água Doce e Pesca Interior, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, 69080–971 Manaus, Amazonas, Brazil. *Corresponding author. E-mail: eliz.chelidae@gmail.com 2 Centro de Ciências Biológicas e da Saúde, Universidade Federal de Mato Grosso do Sul, Av. Costa e Silva s/n, 79070–900 Campo Grande, Mato Grosso do Sul, Brazil 3 Departamento de Ciências Básicas e Produção Animal, Faculdade de Agronomia, Medicina Veterinária e Zootecnia, Universidade Federal de Mato Grosso, Av. Fernando Correa da Costa 2367, 78060–900 Cuiabá, Mato Grosso, Brazil Submitted on 2015, 10th October; revised on 2015, 10th December; accepted on 2016, 27th January Editor: Sebastiano Salvidio Abstract. We studied the feeding habits of Mesoclemmys vanderhaegei in small water bodies in the central region of the Brazilian Cerrado. We captured 80 individuals, 79 of which [41 (52%) females, 27 males (34%), 11 (14%) juve- niles] had stomach contents for analysis. We identified 64 food item categories. The turtles were eating more animal than plant material, aquatic invertebrates being the most conspicuous diet item found. Plant material was more abun- dant in females and rare in the diet of juveniles. Mesoclemmys vanderhaegei proved to be an omnivorous and oppor- tunistic chelonian, feeding on a wide range of food items. Although there are differences in the consumption of food items among sexes and age categories, the most consumed food categories were common in all water bodies sampled. Keywords. Cerrado ecoregion, diet, food habits, foraging ecology, freshwater turtle, prey items, stomach contents, stomach flushing. INTRODUCTION Studies of freshwater turtle trophic ecology have shown that feeding habits in populations of the same species vary with the availability of food, life stage, sex, presence of other species of turtles (Moll, 1976; Vogt, 1980; Fachín-Terán et al., 1994; Fachín-Terán et al., 1995), habitat type and sea- sonality, among other factors (Moll and Moll, 2000). Diet is one of the most often-discussed aspects of turtle natural history (Souza, 2004). Freshwater turtles in the family Chelidae are generally considered omnivo- rous (Souza, 2004), and ontogenetic dietary shifts are known in some species (e.g., Bouchard and Bjorndal, 2006). Variations in the diet of turtles in relation to size and sex appear to be important to avoid niche overlap and intraspecific competition (Fachín-Terán et al., 1995; Souza and Abe, 1998). Although some aquatic turtles possess a general morphology and behavior patterns adapted for carnivo- ry, a variety of plant items are also regularly consumed, including stems, flowers, leaves and fruit (Moll and Moll, 2004). Entirely or primarily carnivorous species can con- sume items ranging from zooplankton and a large num- ber of aquatic and non-aquatic invertebrates to verte- brates (Moll and Moll, 2004). Studies on feeding habits of turtles may involve direct observation (focal animal method, see Sabino, 1999), analysis of stomach contents (Legler, 1977) and/or fecal material (Caputo and Vogt, 2008) from live or preserved specimens. Knowledge of the composition and varia- tion in diet and feeding habits across different species can underpin broad ecological and evolutionary studies, as well as aid conservation and management planning (Sou- za, 2004). Human interference (e.g., trash, offering of arti- 2 Elizângela Silva Brito et alii ficial food, impoundments) may cause important changes in the diet of free-living aquatic organisms, as reported by Sabino et al. (2005), who found “obese” fish populations in areas subjected to intense public visitation in Southwest- ern Brazil. Changes in the availability of food resources due to water pollution can also reduce the amplitude of the trophic niche and enhance competition amongst sym- patric freshwater turtles (Luiselli et al., 2004). The Vanderhaege’s Toad-headed Turtle, Mesoclemmys vanderhaegei (Bour, 1973), is a central South American chelid most often recorded in water bodies within eco- systems with naturally open vegetation, such as the Cer- rado and Chaco (Brandão et al., 2002; Souza, 2005; Rue- da-Almonacid et al., 2007; Vinke et al., 2013; Marques et al., 2014). This species can occur in mountains and on high plateaus, in oligotrophic streams with clear water (Brandão et al., 2002; Brito et al., 2009; Brito et al., 2012). However, individuals have also been found in swampy lowland environments with heavy aquatic vegetation cov- er, as well as in medium-sized rivers (Vinke et al., 2013), dams and ponds (Marques et al., 2013, 2014). The species also occurs in urban environments, though less frequent- ly (Brito et al., 2012). Although generally considered carnivorous (Rueda- Almonacid et al., 2007; Vinke et al., 2013; Marques et al., 2014), no detailed studies of the feeding habits of Meso- clemmys vanderhaegei have been published. This study aims to identify and quantify the composition of the diet of M. vanderhaegei in streams in the Cerrado ecoregion of central Brazil. We investigate the effects of sex, age category, and site on dietary habits of this species and whether individuals are diet specialists or generalists. MATERIALS AND METHODS Study site The study was conducted in the Chapada dos Guima- rães National Park (15°25’S; 55°20’W; Datum WGS 84) and its immediate surroundings, in the Chapada dos Guimarães Fig. 1. Map illustrating study site in the Chapada dos Guimarães National Park and surrounding areas, Mato Grosso, Brazil. Black dots rep- resent sampled streams. 3Diet of Mesoclemmys vanderhaegei municipality, Mato Grosso state, central Brazil (Fig. 1). The area is located in the southwestern portion of the Cerrado ecoregion, a savanna-like vegetation that originally covered nearly two thousand square kilometers, mostly across central Brazil. Seven water bodies were sampled (Table 1), at altitudes between 600 and 800 m a.s.l. Obtention of specimens and stomach contents Captures were made between 05 of January and 30 of March 2007. Individuals were hand captured during visual searches or with the aid of baited funnel traps. For details of size, type and arrangement of funnel traps see Brito et al. (2009). At each collecting site, seven traps operated 24 hours a day, for six consecutive days (a total sampling effort of 1008 trap hours per site). Traps were visited three times a day (06:00, 14:00, and 21:00 h). Visual searches by two observers were conducted dur- ing trap visits, totaling 36 hours/observer at each collection site. Individuals were marked following the methods of Cagle (1939), measured (to the nearest 0.05 mm, with a 300 mm Ver- nier caliper: straight-line carapace length – CL, carapace width – CW; straight-line plastron length – PL; plastron width – PW), weighed (body mass, in g), and sexed, after which they were released at the capture site. Sex was determined by external examination of secondary sexual characteristics: chelid males usually possess a longer and thicker tail than females (Brito et al., 2009). Individuals in which sex could not be determined (n = 11; all with CL < 100 mm) were treated as juveniles and grouped together in this category. To sample the diet of M. vanderhaegei we collected stom- ach contents using the stomach flushing technique developed by Legler (1977). We considered the stomach empty when, after two consecutive flushing attempts, totaling 60 ml of water, indi- vidual turtles regurgitated nothing but water. Samples of stom- ach contents were stored in containers with 70% alcohol (plant samples and invertebrates) or 10% formalin (vertebrates). Diet analyses Stomach contents were examined under a stereo-micro- scope and the food items were quantified and identified to the lowest possible taxonomic level. Plant fragments that could not be identified because they were in an advanced state of decom- position were categorized as “unidentified plant material”. Parts of exoskeleton, legs, wings and antennae of invertebrates that could not be identified were grouped in the category “unidenti- fied Arthropoda”. Aquatic invertebrates were identified by using dichotomous keys (Pérez, 1988; Costa et al., 2006) and by con- sulting experts (see acknowledgements). Total length (mm) of entire prey was measured to the nearest 0.01 mm using a digital caliper (BTS®). Data on stomach contents were analysed by sex (females and males), age categories (adults and juveniles), and water bodies. For each food category we determined the frequency of occurrence, the numerical frequency, and percentage volume (Hyslop, 1980; Marrero, 1994), measured by the displacement of a water column in a 1 ml syringe (graduated to 0.01 ml incre- ments). When food item classes had a volume less than 0.01 ml, we regrouped such items into broader categories for volumetric analysis. The final analytical categories for volume were: aquatic invertebrates, non-aquatic invertebrates, fish, adult amphib- ians, larval amphibians, vertebrate bones (except fish), mam- malian teeth, reptile scales, unidentified animal material, stems, leaves, fruits, seeds, aquatic plants (submerged vegetation), uni- Table 1. Characteristics of seven capture sites of Mesoclemmys vanderhaegei in Chapada dos Guimarães municipality (Mato Grosso, Brazil) and number of turtles captured on each site. Abbreviations: Water body type: Le - lentic; Lo - lotic; Le/Lo - mixed. Natural/Human Impact- ed: N - natural; HI - human impacted. Presence of aquatic vegetation (submerged and floating): ++ abundant; + present; - absent. Bankside vegetation: Tr - trees; Sr - shrubs; Gr - grasses. Substrate: Mu - mud; Sa - sand; Ro - rock. Water body Captures Coordinates Water body type Natural/ Human impacted Submerged vegetation Floating vegetation Bankside vegetation Substrate Monjolinho 18 15º24’S 55º48’W Le/Lo HI ++ ++ Tr Mu/Sa Dam 1 7 15º26’S 55º45’W Le HI ++ + Gr Sa Dam 2 5 15º26’S 55º45’W Le HI + - Gr Sa Aldeia Velha 5 15º26’S 55º45’W Lo N + + Tr/Sr/Gr Sa/Ro Quineira 24 15º27’S 55º44’W Le/Lo HI ++ + Tr Mu/Sa Independência 8 15º24’S 55º50’W Lo N + - Tr/Sr Sa/Ro Congonhas 13 15º23’S 55º50’W Lo HI - - Tr/Sr/Gr Sa/Ro 4 Elizângela Silva Brito et alii dentified plant material, sediment (sand/stone), material from human activities (food scraps and religious rituals), periphyton, and unidentified material. Statistical analyses We used analysis of variance (ANOVA) to test if differ- ences existed in the proportions of animal and plant items con- sumed by different sexes and ages of M. vanderhaegei. For this analysis, food items of animal origin were grouped in four cat- egories: aquatic invertebrates, non-aquatic invertebrates, fish, and amphibians. We excluded the contributions of unidentified inver- tebrates and small bone fragments, scales and teeth of vertebrates, scarcely represented in our sample. Similarly, plant items were grouped into four categories: aquatic plants, fruits, leaves, and plant material not identified; seeds were excluded due to poor representativity. An ANOVA was also performed to investigate the differences between the consumption of animal and plant items as a whole. For both analyses, data on the proportions of each of the categories considered were transformed into arc sine square root, a transformation recommended when using frequen- cy-based data that is not normally distributed (Zar, 1996). The paired-samples t test (Zar, 1996) was used to compare frequency of occurrence of animal and plant material consumed by Meso- clemmys vanderhaegei in the seven water bodies sampled. To test the relationship between the total volume of ingest- ed plant matter and the carapace length (CL) of captured indi- viduals, and between the size of the entire ingested prey and CL, we employed a simple linear regression. For statistical anal- yses we used the application SYSTAT (Wilkinson, 1990). The level of significance in statistical tests was set at ≤ 0.05. Based on abundance (quantitative) and presence/absence (qualitative) data for the 12 food categories with higher values of frequency of occurrence, we performed an ordination analy- sis (non-metric multidimensional scaling – NMDS), using the application PcORD (version 4.0) to reduce the dimensionality of diet composition. We did this for male and female M. van- derhaegei (sites combined) and for each studied water body (sexes combined). To give the same weight to each sample (individual), we used the Bray-Curtis index as a measure of dis- similarity between matrices of abundance and presence/absence. RESULTS We captured 80 individuals of Mesoclemmys vander- haegei of which 79 had stomach contents. Of these, 41 (52%) were females, 27 were males (34%), and 11 (14%) were juveniles. We identified 64 food item categories. Items of ani- mal origin were found in 97% (n = 77) of individuals examined, and items of plant origin in 63% (n = 65). Among the animal items, invertebrates of the class Insec- ta were the most diverse (with material from 25 fami- lies in 11 orders; Table 2). Macro-invertebrate species at aquatic larval stage were the most frequently consumed insects, mainly from the orders Odonata, Diptera and Hemiptera. Non-aquatic invertebrates (Hymenoptera, Lepidoptera, Araneae, Diplopoda) were also present, though generally with a frequency of less than 5%. Among vertebrates, fish of the genus Astyanax (Characidae: Characiformes) were most commonly con- sumed. Amphibians occurred both at low frequency and small numbers when compared to other animal catego- ries, and were mostly tadpoles. For plant material, the most often consumed items were aquatic plants, fruits (mainly from Ficus sp., Moraceae, and from Mauri- tia flexuosa, Arecaceae) and leaves, plus periphyton and material from the unidentified category. Females of Mesoclemmys vanderhaegei consumed more plant material than either males or juveniles (Fig. 2), but recorded differences between the three categories were not significant (F3,27 = 0.26, P = 0.41). Juveniles con- sumed more animal items than adult males and females (F3,106 = 0.26, P = 0.02). Males consumed significantly more aquatic inver- tebrates than females (F3,76 = 0.33, P < 0.01). However, individuals in the two sexes did not differ in the con- sumption of non-aquatic invertebrates (F3,19 = 0.53, P = 0.06), fish (F3,6 = 0.67, P = 0.73) or amphibians (F3,12 = 0.76, P = 0.26). There was no significant relationship between turtle CL (n = 66) and the abundance of aquatic invertebrates consumed (R2 = 0.01, P = 0.38). Fig. 2. Frequency of occurrence of animal and plant material con- sumed by 79 individuals of Mesoclemmys vanderhaegei captured in the Chapada dos Guimarães region (Mato Grosso, Brazil) between January and March 2007. Abbreviations: F = females (n = 41), M = males (n = 27) and J = juveniles (individuals ≤ 100 mm; n = 11). 5Diet of Mesoclemmys vanderhaegei Table 2. Composition of stomach contents of 79 individuals of Mesoclemmys vanderhaegei from Chapada dos Guimarães, Mato Grosso, Bra- zil, sampled between January and March 2007. Frequency of occurrence and numerical frequency of each prey type by sex and age category: M - adult males (n = 27); F - adult females (n = 41); J - juveniles (individuals ≤ 100 mm; n = 11). Abbreviations: n.i. - not identified due to digestion state. Food items’ life stage: A - adult (invertebrates and vertebrates; I - imago (invertebrates only); L - larva (vertebrates only); P - pupa. FOOD ITEMS Frequency of occurrence Numerical frequency M F J M F J INVERTEBRATES 322.09 268.05 418.14 74.47 57.71 75.16 Odonata - Anisoptera (I) 14.81 (4) 9.75 (4) 9.09 (1) 1.11 (4) 1.31 (5) 1.07 (1) Libellulidae (I) 25.92 (7) 19.51 (8) 9.09 (1) 15.59 (56) 12.36 (47) 3.22 (3) Gomphidae (I) 11.11 (3) 4.87 (2) 2.50 (9) 1.31 (5) Aeshnidae (I) 14.81 (4) 17.07 (7) 2.78 (10) 2.89 (11) Odonata - Zygoptera (I) 2.43 (1) 0.26 (1) Coenagrionidae (I) 2.43 (1) 0.26 (1) Lestidae (I) 14.81 (4) 9.75 (4) 20.89 (75) 7.63 (29) Blattaria (A) 2.43 (1) 0.26 (1) Orthoptera (A) 14.81 (4) 12.19 (5) 18.18 (2) 1.11 (4) 1.31 (5) 2.14 (2) Neuroptera (I) 4.87 (2) 9.09 (1) 0.52 (2) 1.07 (1) Corydalidae (I) 3.70 (1) 0.27 (1) Diptera (I) 3.70 (1) 4.87 (2) 9.09 (1) 0.27 (1) 0.78 (3) 4.30 (4) Diptera - Culicomorpha (A) 3.70 (1) 14.63 (6) 9.09 (1) 0.27 (1) 1.57 (6) 1.07 (1) Chironomidae (P) 29.62 (8) 17.07 (7) 18.18 (2) 3.34 (12) 2.89 (11) 2.15 (2) Culicidae (P) 3.70 (1) 4.87 (2) 3.34 (12) 1.31 (5) Simuliidae (P) 3.70 (1) 9.09 (1) 1.11 (4) 2.15 (2) Diptera - Brachycera (A) Sarcophagidae (A) 2.43 (1) 0.26 (1) Hemiptera (A) 14.81 (4) 12.19 (5) 1.11 (4) 1.31 (5) Hemiptera - Auchenorrhyncha (A) 14.81 (4) 2.43 (1) 27.27 (3) 1.39 (5) 0.26 (1) 8.60 (8) Hemiptera - Heteroptera Belostomatidae (A) 3.70 (1) 9.09 (1) 0.27 (1) 1.07 (1) Corixidae (A) 2.43 (1) 9.09 (1) 0.26 (1) 1.07 (1) Naucoridae (A) 9.09 (1) 0.26 (1) 1.07 (1) Pleidae (A) 3.70 (1) 18.18 (2) 0.27 (1) 3.22 (3) Trichoptera - Annulipalpia (I) 11.11 (3) 7.31 (3) 9.09 (1) 1.11 (4) 1.05 (4) 1.07 (1) Hydropsychidae (I) 7.31 (3) 18.18 (2) 1.31 (5) 2.15 (2) Macronema sp. (I) 7.40 (2) 2.43 (1) 18.18 (2) 1.11 (4) 0.52 (2) 5.37 (5) Polycentropodidae (I) 2.43 (1) 9.09 (1) 0.52 (2) 4.30 (4) Trichoptera - Integripalpia Leptoceridae (I) 3.70 (1) 9.09 (1) 0.27 (1) 1.07 (1) Coleoptera (A) 3.70 (1) 12.19 (5) 18.18 (2) 1.31 (5) 2.15 (2) Coleoptera (I) 2.43 (1) 9.09 (1) 0.26 (1) 1.07 (1) Coleoptera - Adephaga (A) Dytiscidae (A) 3.70 (1) 7.31 (3) 9.09 (1) 1.11 (4) 1.05 (4) 1.07 (1) Coleoptera - Elateroidea (A) Elateridae (A) 3.70 (1) 0.27 (1) Ephemeroptera (I) 14.81 (4) 2.43 (1) 9.09 (1) 1.94 (7) 0.52 (2) 1.07 (1) Ephemeroptera - Pisciforma (I) Baetidae (I) 14.81 (4) 4.87 (2) 9.09 (1) 5.57 (20) 0.78 (3) 5.37 (5) Hymenoptera (A) 9.75 (4) 18.18 (2) 1.31 (5) 2.15 (2) Formicidae (A) 3.70 (1) 9.75 (4) 18.18 (2) 0.27 (1) 1.57 (6) 2.15 (2) (continued) 6 Elizângela Silva Brito et alii Among the four categories of commonly eaten plant material, there was a significant difference between sexes and age categories for the consumption of leaves (F3,11 = 1.00, P < 0.01), aquatic plants (F3,21 = 0.96, P < 0.01), and plant material not identified (F3,19 = 0.86, P < 0.01), but not for fruit (F3,14 = 0.17, P = 0.35). Females were the largest consumers of plants. The two axes of the NMDS captured much of the variation of M. vanderhaegei diet (62% for qualitative data – presence/absence, and 59% for quantitative data – abundance), but it was not possible to separate the diets of males and females (Fig. 3). Items of animal origin represented the largest pro- portion of stomach contents volume for females (46%), males (53%), and juveniles (75%; Table 3). For all these three categories, sediment constituted less than 1% of total stomach contents volume. For animal prey the commonest food items by volume were fish and aquatic invertebrates, for plants it was fruits. Periphyton also occupied large volumes. Although periphyton was the bulkiest item, only four individuals (one juvenile, one female and two males, 5% of stomachs analyzed) con- tained this type of food item. In 4% of females and juve- niles and 7% of males, the stomachs contained material from human activities: e.g. beans, eggshell and popcorn. This type of material represented 15% of the volume of the diet of individuals caught in Congonhas stream, the FOOD ITEMS Frequency of occurrence Numerical frequency M F J M F J Lepidoptera (I) 2.43 (1) 0.26 (1) Cossidae (I) 3.70 (1) 0.27 (1) Notodontidae (I) 3.70 (1) 9.09 (1) 0.27 (1) 1.07 (1) Araneae 3.70 (1) 2.43 (1) 0.27 (1) 0.26 (1) Diplopoda (A) 2.43 (1) 0.26 (1) Oligochaeta 3.70 (1) 0.55 (2) Unidentified Arthropoda (I) 3.70 (1) 4.87 (2) 18.18 (2) 0.27 (1) 0.78 (3) 2.15 (2) Unidentified Arthropoda (A) 55.55 (15) 41.46 (17) 72.72 (8) 5.57 (20) 8.94 (34) 10.75 (10) AMPHIBIANS 18.05 7.30 9.09 2.49 1.04 1.07 Leptodactylidae (L) 3.70 (1) 0.27 (1) Hylidae - Dendropsophus minutus (A+L) 4.87 (2) 0.78 (3) AMPHIBIANS (n.i.) (A) 7.40 (2) 0.55 (2) AMPHIBIANS (n.i.) (L) 7.40 (2) 2.43 (1) 9.09 (1) 1.67 (6) 0.26 (1) 1.07 (1) FISH 48.13 58.51 27.27 5.54 12.09 3.22 Astyanax sp. 37.03 (10) 53.65 (22) 27.27 (3) 4.45 (16) 11.57 (44) 3.22 (3) Rivulus sp. 3.70 (1) 0.27 (1) Vertebrate bones (n.i.) 3.70 (1) 0.55 (2) Reptile scales 3.70 (1) 2.43 (1) 0.27 (1) 0.26 (1) Mammalian teeth (n.i) 2.43 (1) 0.26 (1) PLANT MATERIAL 96.26 136.55 72.72 7.75 22.06 8.59 Aquatic plants (submerged vegetation) 22.22 (6) 34.14 (14) 18.18 (2) 2.22 (8) 4.73 (18) 2.15 (2) Stems 7.40 (2) 14.63 (6) 9.09 (1) 0.55 (2) 1.57 (6) 1.07 (1) Leaves 18.51 (5) 21.95 (9) 18.18 (2) 1.11 (4) 2.36 (9) 2.15 (2) Seeds 3.70 (1) 2.43 (1) 0.27 (1) 0.26 (1) Fruit of Ficus sp. (fig) 11.11 (3) 17.07 (7) 0.83 (3) 8.15 (31) Fruit of Mauritia flexuosa (buriti) 7.40 (2) 17.07 (7) 18.18 (2) 0.55 (2) 1.84 (7) 2.15 (2) Unidentified plant material 25.92 (7) 29.26 (12) 9.09 (1) 2.22 (8) 3.15 (12) 1.07 (1) ALGAE Periphyton 7.40 (2) 3.70 (1) 3.70 (1) 0.27 (1) 0.27 (1) 0.27 (1) MATERIAL FROM HUMAN ACTIVITIES (religious food-offerings) 29.62 (8) 7.30 (3) 9.09 (1) 6.12 (22) 4.99 (19) 5.37 (5) SEDIMENT (sand/gravel) 29.62 (8) 14.62 (6) 54.54 (6) 3.06 (11) 1.57 (6) 6.44 (6) Table 2. (continued). 7Diet of Mesoclemmys vanderhaegei only locality in which such items were recorded from M. vanderhaegei stomachs. In all water bodies sampled, diet items of animal ori- gin were more commonly consumed than those of plant origin (t = 2.77; df = 6; P = 0.03; Fig. 4). Water bodies where there was greatest consumption of plant items were mostly dammed streams (Monjolinho, Quineira, Dam 1, and Dam 2), all anthropogenic environments. Fruit con- sumption was recorded only in Monjolinho and Quineira dammed streams. The volume of plant (R2 < 0.03, P = 0.13) and ani- mal material (R2 < 0.01, P = 0.72) in the stomachs was not significantly related to the CL of individuals caught. Similarly, there was no significant relationship between prey size and the CL of captured individuals (R2 = 0.01, P = 0.13, n = 45 entire prey). Qualitative data on sampling sites captured much of the variation in the diet between water bodies (63%), but the resulting ordination did not allow us to group water bodies according to the consumed food items (Fig. 5). DISCUSSION In the area, and during the period of study, Meso- clemmys vanderhaegei was found to be omnivorous with a general tendency to carnivory, as briefly pointed in a recent species’s account by Marques et al. (2014). In many communities of vertebrates, omnivorous species represent the greater part of the consumers (Polis, 1991; Polis and Strong, 1996), and species identified as primar- ily carnivorous may include plant material in their diet (McTigue and Zimmerman, 1991). Omnivory has been reported frequently among members of the family Cheli- dae (e.g., Medem, 1960; Mittermeier et al., 1978; Souza, 2004; Caputo and Vogt, 2008; Martins et al., 2010). How- ever, some species of this family, such as Chelus fimbria- tus, Hydromedusa tectifera, Phrynops hilarii, and Platemys platycephala are exclusively carnivorous (Vogt and Villar- real, 1993; Alcalde et al., 2010). Mesoclemmys vanderhaegei is one of the largest aquat- ic vertebrates in the water bodies studied, along with the Cuvier’s Dwarf Caiman (Paleosuchus palpebrosus) and the Green Anaconda (Eunectes murinus), and like these two, appears to occupy the higher levels of the local trophic chain (E. Brito, pers. comm. 2007). Items of animal ori- gin were those most frequently used by all age and sex categories of M. vanderhaegei, with aquatic invertebrates being the most important, both in terms of proportional contribution to the diet and as number of individuals. High consumption of aquatic invertebrates (larvae and pupae) is frequently recorded for freshwater turtles (e.g., Lagler, 1943; Moll, 1990; Souza and Abe, 1998, 2000; Moll and Moll, 2004; Caputo and Vogt, 2008; Bonino et al., 2009; Alcalde et al., 2010; Martins et al., 2010; Brasil et al., 2011). However, consumed non-aquatic invertebrates Fig. 3. Non-metric multidimensional scaling (NMDS) plots of food items consumed by Mesoclemmys vanderhaegei from Chapada dos Gui- marães, Mato Grosso, Brazil, according to (A) presence/absence and (B) abundance. Only turtles that were sexed were considered (n = 69; F - females; M - males). 8 Elizângela Silva Brito et alii include adults of Orthoptera, Coleoptera and Formicidae, indicating that M. vanderhaegei is an opportunistic preda- tor, a feature common among aquatic turtles (Moll, 1976; Chessman, 1984; Souza and Abe, 1998, 2000; Luiselli et al., 2004; Alcalde et al., 2010; Brasil et al. 2011). Fish, particularly those of the genus Astyanax (Char- aciformes), are among the three most common animal items consumed by M. vanderhaegei. They are also the commonest prey item by volume recorded during the study. Although they are known to be important in the diet of carnivorous and omnivorous freshwater turtles belonging to suborder Cryptodira, fish are generally con- sidered to be more easily captured by individuals belong- ing to those turtle species with longer necks (Moll and Moll, 2004) – the Pleurodira – for which Hydromedusa tectifera is a good example (Alcalde et al., 2010). On sev- eral occasions during the field study, individuals of M. vanderhaegei were observed to chase fish of the genus Astyanax. However, none of these attempts resulted in a successful capture. It appeared that individuals of M. van- derhaegei soon gave up chasing individuals when they were not caught immediately and would go in pursuit of other fish when there were schools on site (E. Brito, pers. comm. 2005). At least five species of Astyanax occur in the Chapada dos Guimarães National Park, all of them considered regular and abundant members of the local fish community (ICMBio, 2009). Additionally, species in the genus Astyanax can form large schools (e.g., Suzuki and Orsi, 2008). Some of the individuals from these schools occasionally enter in the funnel traps (E. Brito, pers. comm. 2007), where they could be more easily cap- tured by imprisoned turtles and result in an overestima- tion of fish as a prey for M. vanderhaegei. Although both sexes have higher consumption of animal items than of plants, the consumption is propor- tionately greater in females than in males. Similar stud- ies in other species of Chelidae give conflicting results for this aspect: for the Neotropical species Phrynops Table 3. Composition of stomach contents of 79 individuals of Mesoclemmys vanderhaegei from Chapada dos Guimarães, Mato Grosso, Bra- zil, sampled between January and March 2007. Volume (V) - in ml and in percentual - of each food item category, by sex and age category: M - adult males (n = 27); F - adult females (n = 41); J - juveniles (individuals ≤ 100 mm; n = 11). Food items’ life stage: A - adult; L - larva. Food item category Age category M F J V (ml) V (%) V (ml) V (%) V (ml) V (%) INVERTEBRATES 10.98 16.96 15.91 17.11 2.27 17.53 Aquatic invertebrates 8.41 12.99 13.39 14.40 1.06 8.19 Non-aquatic invertebrates 2.57 3.97 2.52 2.71 1.21 9.34 VERTEBRATES 10.58 16.32 26.05 28.01 7.46 57.55 Amphibians (A) 0.12 0.19 0.00 0.00 0.00 0.00 Amphibians (L) 1.92 2.96 0.06 0.06 0.02 0.15 Fish 7.86 12.13 23.24 24.99 7.44 57.40 Vertebrate bones (except fish) 0.10 0.15 0.00 0.00 0.00 0.00 Mammalian teeth 0.00 0.00 0.05 0.05 0.00 0.00 Reptilian scales 0.08 0.12 0.60 0.65 0.00 0.00 Unidentified vertebrates 0.50 0.77 2.10 2.26 0.00 0.00 PLANT MATERIAL 1.76 3.64 15.05 16.16 0.77 5.94 Stems 0.19 0.29 1.18 1.27 0.02 0.15 Leaves 0.13 0.20 0.05 0.05 0.04 0.31 Fruits 1.34 2.07 12.04 12.95 0.50 3.86 Seeds 0.10 0.15 0.02 0.02 0.00 0.00 Aquatic plant (submerged vegetation) 0.16 0.25 0.87 0.94 0.11 0.85 Unidentified plant material 0.44 0.68 0.89 0.96 0.10 0.77 SEDIMENT (sand/gravel) 0.07 0.11 0.06 0.06 0.04 0.31 MATERIAL FROM HUMAN ACTIVITIES (religious food-offerings) 2.61 4.03 7.05 7.58 0.50 3.86 ALGAE - Periphyton 26.60 41.26 20.89 27.17 1.30 9.87 UNIDENTIFIED MATERIAL 11.30 17.67 8.00 3.88 0.62 4.93 9Diet of Mesoclemmys vanderhaegei geoffroanus, no significant differences were found in diet composition of males and females (Fachín-Terán et al., 1994), while in Emydura krefftii from Australia (Georges, 1982), and Acanthochelys spixii, in the Brazilian Cerrado (Brasil et al., 2011), females consumed more plant mate- rial, while males ate more animal items. Considering the different reproductive strategies of the sexes, with females having to increase their weight and maintain nutritional reserves during egg develop- ment and laying (Schoener, 1971), such differences in the diets of males and females are not unexpected. The fact that our study found no differences in the compo- sition and abundance of food items consumed by male and female M. vanderhaegei suggests a possible food niche overlap between the two sexes. This could be relat- ed to the opportunistic consumption of the most abun- dant items in the environment by both sexes. Although another chelid – Phrynops geoffroanus – is frequently recorded in lower sections of the streams studied, no other freshwater turtle but M. vanderhaegei occurs at the study site. Therefore, it is also possible that in the absence of competition, individuals in this species have such a broad niche that there is no need for between- sex partitioning. The occurrence of dietary changes in the presence of potential competitors is an interesting hypothesis that could be tested for M. vanderhaegei, in the drainages mentioned here. On the contrary, the greater frequency of occur- rence of plant materials in the stomachs of individuals of Mesoclemmys vanderhaegei may be simply the result of accidental ingestion during predation of animal items. In fact, when analyzing the diet of omnivorous turtles, it is often not possible to determine whether the plant mate- rial was ingested intentionally or accidentally (Parmenter and Avery, 1990; Lindeman, 1996; Rowe and Parsons, 2000). Another aspect potentially indicating accidental ingestion of plant items was the fact that only small frag- ments of such material were found in the stomach con- tents. On the other hand, the large volume of periphyton found in four stomachs of M. vanderhaegei during our study is suggestive of deliberate intake (Tables 2 and 3). The same can be inferred for bulkier plant items – fruits of Ficus sp. and exocarp and mesocarp of Mauritia flexu- osa were found almost whole in the stomachs, suggesting that they had been purposely ingested. In general, chelid turtles appear to supplement their diets with fruits or seeds, particularly when these items are readily available or when aquatic prey becomes more dispersed, as in the rainy season (Fachín-Terán et al., 1995; Lima et al., 1997; Caputo and Vogt, 2008). Our results reinforce the sug- gestion by Caputo and Vogt (2008) that turtle diets ide- ally should be investigated by using both stomach flush- ing and fecal analyses. In a study of the diet of Rhinemys rufipes in Brazilian Amazonia, those authors found that bulky stomach contents (e.g., large fruit seeds), generally not regurgitated by turtles by using the stomach flushing Fig. 4. Frequency of occurrence of animal and plant material con- sumed by Mesoclemmys vanderhaegei in the seven water bodies sampled in the Chapada dos Guimarães region, Mato Grosso, Bra- zil. Subtitle: AV - Aldeia Velha stream; Co - Congonhas stream; In - Independência stream; Mo - Monjolinho stream; Qui - Quineira stream; D1 - Dam 1; D2 - Dam 2. Fig. 5. Non-metric multidimensional scaling (NMDS) plots of food items consumed by Mesoclemmys vanderhaegei in the seven sites sampled in Chapada dos Guimarães municipality, Mato Grosso, Brazil. A = Independência stream; C = Congonhas stream; V = Aldeia Velha stream; L = Dam 1; D = Dam 2; M = Monjolinho stream; Q = Quineira stream. 10 Elizângela Silva Brito et alii technique, do however appear in analyses of fecal con- tents (Caputo and Vogt, 2008). The consumption of animal items in greater numeri- cal frequency and percentage volume by juveniles than by adult males and females corroborates what is reported elsewhere. The record of ontogenetic diet changes in che- lonian species is common and usually juvenile freshwa- ter turtles are more carnivorous, while adult freshwater turtles are more herbivorous (Clark and Gibbons, 1969; Moll, 1976; Parmenter and Avery, 1990; Kennett and Tory, 1996; Spencer et al., 1998) or omnivorous (Boucha- rd and Bjorndal, 2006). This change may be related to protein requirements for growth (Schoener, 1971), con- sidering that the juvenile turtles are more susceptible to predation and need to grow fast. Change in diet upon reaching reproductive maturity has also been reported in Emydura krefftii (Chelidae), a species where juveniles are carnivorous and adults omnivorous (Georges, 1982), and in Hydromedusa maximiliani (Chelidae) (Souza and Abe, 1998), where small crabs accounted for 75% of all food items consumed by juveniles but only 5% of the food items consumed by adults. A curious result of this study is the similarity of M. vanderhaegei diet in water bodies with apparently very different environmental characteristics. In Congonhas Stream, for example, there are no fish (J. Penha, pers. comm. 2007) but a sporadic supply of biological material from human activities does occur (picnics and religious food-offerings). This material comprised a large variety of fruits (e.g., kiwi, grapevines, pear, peach, apple, banana, watermelon), vegetables (okra), cooked grains (rice, pop- corn), beans, and eggs, arranged in plastic or wood trays, at the margins of the stream. The broad trophic plasticity recorded for M. vanderhaegei indicates that individuals of this species have very generalist diets. The identifica- tion of unusual food items, for example, scales of rep- tiles (snakes and lizards) and mammalian teeth, as well as material from human activities (see Table 2), may also reflect a common tendency for freshwater turtles to be scavengers (Souza, 2004). The categories of food eaten by individuals of M. vanderhaegei indicate that they may forage in several dif- ferent strata of the water column. Benthic foraging was indicated by the consumption of such aquatic inverte- brates as Trichoptera (which live mostly under rocks, logs and plant materials, in running water; Pérez, 1988) and Odonata (whose larvae have strong associations with lentic and aquatic vegetation, but may also occur in lotic environments, where they live buried in the sand; Pérez, 1988). Meanwhile, the consumption of large amounts of fish (Astyanax sp.), of fruits (e.g., Ficus sp.), and of non- aquatic invertebrates active on understory vegetation (e.g. various ant species) indicate that individuals of M. van- derhaegei also forage both nektonically and directly from the surface. As with most omnivorous vertebrates, in which feed- ing is related to a variety of foraging opportunities in their habitat, female, male and juvenile M. vanderhae- gei all showed a mixed diet of plants and animals items. While a mixed diet implies less efficient digestion, since it requires a diverse gut microflora, it also involves less loss of time and energy in the search for more nutritious foods (Bjorndal, 1991). In addition, a mixed plant-animal diet provides a broader spectrum of nutrients than does an item-restricted diet, which may explain why most organisms are to some extent omnivorous and hence have an enhanced ability to optimize their nutritional balance (Bjorndal, 1991). The present study provides detailed information on the diet of Mesoclemmys vanderhaegei in natural and anthropogenic disturbed environments in headwater streams in Cerrado. Much of the original area occupied by this ecoregion is presently modified by anthropogen- ic changes derived from agriculture. Such modifications have strongly impacted aquatic ecosystems, severely alter- ing species composition, functioning and structure of freshwater habitats throughout Cerrado (Agostinho et al., 2005), in such an extent that this ecoregion is considered a global biodiversity hotspot (Klink and Machado, 2005). A close relative of M. vanderhaegei – Mesoclemmys hogei, native to another Brazilian hotspot, the Atlantic Forest – was recently recognized by the governmental environ- mental agency as Critically Endangered, being the first and the only continental Brazilian chelonian to be con- sidered as a threatened species (ICMbio, 2015). Addition- al studies on actual and potential effects of anthropogenic and natural disturbances on the feeding habits of M. van- derhaegei, among other biological aspects, might help to prevent extinction risks to this species. ACKNOWLEDGMENTS The authors are grateful to environmental analysts and experts from the Chapada do Guimarães Nation- al Park for their support during field data collection. We also thank the Centro Nacional de Pesquisa e Con- servação de Répteis e Anfíbios (RAN) for licenses to cap- ture M. vanderhaegei (permit # RAN/IBAMA 031/2005). Thanks are also due to Pastor Henrique, Murcio, and the authorities from Chapada dos Guimarães for allow- ing field study at properties under their care, respectively, the Buriti Evangelical School, the Aldeia Velha farm, and Parque Municipal do Quineira. We particularly thank 11Diet of Mesoclemmys vanderhaegei all the people who assisted in the collection of field data and CAPES for a scholarship grant to ESB and a PRO- DOC (Programa de Apoio a Projetos Institucionais com a Participação de Recém-Doutores) grant to CS that led to the completion of the field work. Wesley Oliveira, from LETA (Laboratório de Ecologia e Taxonomia de Artrópo- des), helped to identify aquatic invertebrates. CS and FLS thank CNPq for Research Productivity Grants (processes # 309541/2012-3 and 303006/2014-5, respectively). Rafael Valadão helped with the map. Adrian Barnett and Rich- ard Carl Vogt helped with the English and gave sugges- tions that improved the text. We also thank two anony- mous reviewers. REFERENCES Agostinho, A.A., Thomaz, S.M., Gomes, L.C. (2005): Conservation of the biodiversity of Brazil’s inland waters. Conserv. Biol. 19: 646-652. Alcalde, L., Derocco, N.N., Rosset, S.D. (2010): Feed- ing in syntopy: diet of Hydromedusa tectifera and Phrynops hilarii. Chelonian Conserv. Biol. 9: 33-44. Brasil, M.A., Horta, G.F., Fraxe Neto, H. J., Barros, T. O., Colli, R.G. (2011): Feeding ecology of Acanthochelys spixii (Testudines, Chelidae) in the Cerrado of central Brazil. Chelonian Conserv. Biol. 10: 91-101. Bjorndal, K.A. (1991): Diet mixing: non additive interac- tions of diet items in an omnivorous freshwater turtle. Ecology 72: 1234-1241. Bonino, M.F., Lescano, J.N., Haro, J., Leynaud, G.C. (2009): Diet of Hydromedusa tectifera (Testudines- Chelidae) in a mountain stream of Córdoba province, Argentina. Amphibia-Reptilia 30: 545-554. Bouchard, S.S., Bjordal, K.A. (2006): Ontogenetic Diet Shifts and Digestive Constraints in the Omnivorous Freshwater Turtle Trachemys scripta. Physiol. Bio- chem. Zool. 79: 150-158. Brandão, R.A., Zerbini, G.J., Sebben, A., Molina, F.B. (2002): Notes on distribution and habitats of Acantho- chelys spixii and Phrynops vanderhaegei (Testudines, Chelidae) in central Brazil. Bol. Asoc. Herpetol. Esp. 13: 11-15. Brito, E.S., Strussmann, C., Penha, J.M.F. (2009): Popu- lation structure of Mesoclemmys vanderhaegei (Bour, 1973) (Testudines: Chelidae) in the Cerrado of Cha- pada dos Guimarães, Mato Grosso, Brazil. Biota Neo- trop. 9: 245-248. Brito, E.S, Strüssmann, C., Kawashita-Ribeiro, R.A., Morais, D.H., Ávila, R.W., Campos, V.A. (2012): New records and distribution extensions of three species of Mesoclemmys Gray, 1863 (Testudines: Chelidae) in Mato Grosso state, Brazil, with observations on terres- trial movements. Check List 8: 294-297. Cagle, F.R. (1939): A system of marking turtles for future identification. Copeia 1939: 170-173. Caputo, F.P., Vogt, R.C. (2008): Stomach flushing vs. fecal analysis: the example of Phrynops rufipes (Testudines: Chelidae). Copeia 2008: 301-305. Chessman, B.C. (1984): Food of the snake-necked turtle, Chelodina longicollis (Shaw) (Testudines: Chelidae) in the Murray Valley, Victoria and New South Wales. Aust. Wildlife Res. 11: 573-578. Clark, D.B., Gibbons, J.K. (1969): Dietary shift in the tur- tle Pseudemys scripta (Schoepff ) from youth to matu- rity. Copeia 1969: 704-106. Costa, C., Ide, S., Simonka, C.E. (2006): Insetos imaturos: Metamorfose e identificação. Editora Holos, Ribeirão Preto, Brasil. Fachín-Terán, A., Vogt, R.C., Gomez, M.F. (1994): Ali- mentación de tres especies de tortugas Chelidae en Costa Marques, Rondônia. Bol. Lima 16: 409-416. Fachín-Terán, A., Vogt, R.C., Gómez, M.F. (1995): Food habits of an assemblage of five species of turtles in the Rio Guaporé, Rondonia, Brazil. J. Herpetol. 29: 536-547. Georges, A. (1982): Diet of the Australian freshwater tur- tle Emydura kreffti (Chelonia: Chelidae), in an unpro- ductive lentic environment. Copeia 1982: 331-336. Hyslop, E.J. (1980): Stomach content analysis, a review of methods and their application. J. Fish Biol. 17: 411- 430. ICMbio - Instituto Chico Mendes de Conservação da Biodiversidade. (2009): Plano de Manejo do Parque Nacional da Chapada dos Guimarães. http://icmbio. gov.br/parnaguimaraes/downloads.html. ICMbio – Instituto Chico Mendes de Conservação da Biodiversidade. (2015): Répteis – Quelônios continen- tais. http://www.icmbio.gov.br/portal/biodiversidade/ fauna-brasileira/estado-de-conservacao/7385-repteis- mesoclemmys-hogei-cagado-de-hogei-2.html. Kennett, R.M., Tory, O. (1996): Diet of two freshwater turtles, Chelodina rugosa and Elseya dentata (Tes- tudines: Chelidae) from the wet-dry tropics of north- ern Australia. Copeia 1996: 409-419. Klink, C.A., Machado, R.B. (2005): Conservation of the Brazilian Cerrado. Conserv. Biol. 19: 707-713. Lagler, F.K. (1943): Food habits and economic relations of the turtles of Michigan with special reference to fish management. Am. Midl. Nat. 29: 257-312. Legler, J.M. (1977): Stomach flushing: a technique for Chelonian dietary studies. Herpetologica 33: 281-284. Lindeman, P.V. (1996): Comparative life history of Paint- ed Turtles (Chrysemys picta) in two habitats in the inland Pacific Northwest. Copeia 1996: 114-130. 12 Elizângela Silva Brito et alii Lima, A.C., Magnusson, W.E., Costa, V.L. (1997): Diet of the turtle Phrynops rufipes in central Amazônia. Copeia 1997: 216-219. Luiselli, L., Akani, G.C., Politano, E., Odegbune, E., Bello, O. (2004): Dietary shifts of sympatric freshwater tur- tles in pristine and oil-polluted habitats of the Niger Delta, southern Nigeria. Herpetol. J. 14: 57-64. Marques, T.S., Lara, N.R.F., Bassettil, A.B., Ferronato, B.O., Malvásio, A., Verdade, L.M. (2013): Population structure of Mesoclemmys vanderhaegei (Testudines, Chelidae) in a silvicultural system in southeastern Brazil. Herpetol. Notes 6: 179-182. Marques, T.S., Böhm, S., Brito, E.S., Cabrera, M.R., Ver- dade, L.M. (2014): Mesoclemmys vanderhaegei (Bour 1973) - Vanderhaege’s Toad-headed Turtle, Karumbé- hy. In: Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/ SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs. Rhodin, A.G.J., Pritchard, P.C.H., vanDijk, P.P., Saumure, R.A., Buhl- mann, K.A., Iverson, J.B., Mittermeier, R.A., Eds. Che- lonian Res. Monogr. 5: 083.1-8. Marrero, C. (1994): Métodos para cuantificar contenidos estomacales en peces. Universidad Nacional Experi- mental de los Llanos Occidentales “Ezequiel Zamora”. Universidad de Los Llanos “Ezequiel Zamora”, Caracas. McTigue, T.A., Zimmerman, R.J. (1991): Carnivory vs. herbivory in juvenile Penaeus setiferus (Linnaeus) and Penaeus aztecus (Ives). J. Exp. Mar. Biol. Ecol. 151: 1-16. Martins, F.I., Souza, F.L., Costa, H.T.M. (2010): Feeding habits of Phrynops geoffroanus (Chelidae) in an urban river in central Brazil. Chelonian Conserv. Biol. 9: 294-297. Medem, M.F. (1960): Observaciones sobre la distribución geográfica y ecologia de la tortuga Phrynops geoffroa- na ssp. en Colombia. Informe sobre reptiles Colombi- anos (V). Novedades Colombianas 5: 291-300. Mittermeier, R.A., Rhodin, A.G.J., Medem, F., Soini, P., Hoogmoed, M.S., Espinoza, N.C. (1978): Distribution of the South American Chelid Turtle Phrynops gibbus, with observations on habitat and reproduction. Her- petologica 34: 94-100. Moll, D. (1976): Food and feeding strategies of the Ouachita map turtle (Graptemys pseudogeographica ouachitensis). Am. Midl. Nat. 96: 487-482. Moll, D. (1990): Population sizes and foraging ecology in a tropical freshwater stream turtle community. J. Her- petol. 24: 48-53. Moll, E.O., Moll D. (2000): Conservation of River Turtles. In: Turtle Conservation, pp. 127-155. Klemens, M.W., Ed, Smithsonian Institution Press, Washington. Moll, D., Moll, E.O. (2004): The Ecology, Exploitation, and Conservation of River Turtles. Oxford University Press, New York. Parmenter, R.R., Avery, H.W. (1990): The feeding ecology of the slider turtle In: Life History and Ecology of the Slider Turtle, pp. 257-266. Gibbons, J.W., Ed, Smithso- nian Institution Press, Washington. Pérez, G.R. (1988): Guia para el Estúdio de los Macroin- vertebrados Acuáticos del Departamento de Antio- quia. FEN Colombia/COLCIENCIAS/Universidad de Antioquia, Colombia. Polis, G.A. (1991): Complex trophic interactions in deserts: an empirical critique of food-web theory. Am. Midl. Nat. 138: 123-155. Polis, G.A., Strong, D.R. (1996): Food web complexity and community dynamics. Am. Midl. Nat. 147: 813-846. Rowe, J.W., Parsons, W. (2000): Diet of the Midland turtle (Chrysemys picta marginata) on Beaver Island, Michi- gan. Herpetol. Rev. 31: 16-17. Rueda-Almonacid, J.V., Carr, J.L., Mittermeier, R.A., Rod- ríguez-Mahecha, J.V., Mast, R.B., Vogt, R.C., Rhodin, A.G. J., Ossa-Velásquez, J., Rueda, J.N., Mittermeier, C.G. (2007). Las tortugas y los cocodrilianos de los países andinos del Trópico. Conservación Internac- ional, Bogotá. Sabino, J. (1999): Comportamento de peixes em riachos: métodos de estudo para uma abordagem naturalística. In: Ecologia de Peixes de Riachos, pp. 183-208. Cara- maschi, E.P., Mazzoni, R., Peres-Neto, P.R., Eds, Série Oecologia Brasiliensis, 6. PPGE-UFRJ, Rio de Janeiro. Sabino, J., Medina, Jr., Andrade, L.P. (2005): Visitantes mal-comportados e piraputangas obesas: a pressão da visitação pública sobre Brycon hilarii no Balneário Municipal de Bonito, Mato Grosso do Sul, Brasil. In: Anais do Encontro Nacional de Inovação Cientí- fica para o Homem do Século XXI, pp. 321-332. IV ENPIC, 19-21 October 2005. Editora da UNIDERP, Campo Grande. Schoener, T.W. (1971): Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2: 369-404. Souza, F.L., Abe, A.S. (1998): Resource partitioning by the Neotropical freshwater turtle, Hydromedusa maxi- miliani. J. Herpetol. 32: 106-112. Souza, F.L., Abe, A.S. (2000): Feeding ecology, density and biomass of the freshwater turtle, Phrynops geof- froanus, inhabiting a polluted urban river in South- eastern Brazil. J. Zool. 252: 437-446. Souza, F.L. (2004): Uma revisão sobre padrões de ativi- dade, reprodução e alimentação de cágados brasileiros (Testudines, Chelidae). Phyllomedusa 31: 15-27. Souza, F.L. (2005): Geographical distribution patterns of South American side-necked turtles (Chelidae), with 13Diet of Mesoclemmys vanderhaegei emphasis on Brazilian species. Rev. Esp. Herpetol. 19: 33-46. Spencer R., Thompson, M.B., Hume, I.D. (1998): The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii. Comp. Biochem. Physiol. 121A: 341-349. Suzuki, F.M., Orsi, M.L. (2008): Formação de cardumes por Astyanax altiparanae (Teleostei: Characidae) no Rio Congonhas, Paraná, Brasil. Rev. Bras. Zool. 25: 566-569. Vinke, T., Vinke, S., Köhler, G. (2013): What is known about Mesoclemmys vanderhaegei (Bour 1973): A sys- tematic review of the available literature. Paraquaria Nat. 1: 21-31. Vogt, R.C. (1980): Food partitioning in three sympatric species of Map Turtle, genus Graptemys (Testudinata, Emydidae). Am. Midl. Nat. 105: 102-111. Vogt, R.C., Villareal, J. L.B. (1993): Species abundance and biomass distribution in freshwater turtles. In: Proceedings of the Conservation, Restoration and Management of Tortoises and Turtles, pp. 210-218. Abbema, J.V., Ed, An International Conference. State University of New York, Purchase, New York. Wilkinson, L. (1990): Systat: the System for Statistics. Sys- tat Inc., Evanston. Zar, J.H. (1996): Biostatistical Analisys. Prentice Hall, New Jersey. Acta Herpetologica Vol. 11, n. 1 - June 2016 Firenze University Press Feeding Habits of Mesoclemmys vanderhaegei (Testudines: Chelidae) Elizângela Silva Brito1,*, Franco Leandro Souza2, Christine Strüssmann3 Morphology, ecology, and behaviour of Hylarana intermedia, a Western Ghats frog Ambika Kamath1, Rachakonda Sreekar2,3 A new account for the endangered Cerrado Rocket Frog Allobates goianus (Bokermann, 1975) (Anura: Aromobatidae), with comments on taxonomy and conservation Thiago Ribeiro de Carvalho1,2,*, Lucas Borges Martins1,2, Ariovaldo Antonio Giaretta1 Molecular phylogenetics of the Pristimantis lacrimosus species group (Anura: Craugastoridae) with the description of a new species from Colombia Mauricio Rivera-Correa, Juan M. Daza* Population structure and activity pattern of one species of Adenomera Steindachner, 1867 (Anura: Leptodactylidae) in northeastern Brazil Maria Juliana Borges-Leite1,*, João Fabrício Mota Rodrigues2, Patrícia De Menezes Gondim1, Diva Maria Borges-Nojosa1 Vocal repertoire of Scinax v-signatus (Lutz 1968) (Anura, Hylidae) and comments on bioacoustical synapomorphies for Scinax perpusillus species group Marco Antônio Peixoto1,*, Carla Silva Guimarães1, João Victor A. Lacerda2, Fernando Leal2, Pedro C. Rocha2, Renato Neves Feio1 Amendment of the type locality of the endemic Sicilian pond turtle Emys trinacris Fritz et al. 2005, with some notes on the highest altitude reached by the species (Testudines, Emydidae) Federico Marrone*, Francesco Sacco, Vincenzo Arizza, Marco Arculeo Photo-identification in amphibian studies: a test of I3S Pattern Marco Sannolo1,*, Francesca Gatti2, Marco Mangiacotti3,4, Stefano Scali3, Roberto Sacchi4 No evidence for the ‘expensive-tissue hypothesis’ in the dark-spotted frog, Pelophylax nigromaculatus Li Zhao, Min Mao, Wen Bo Liao* No short term effect of Clinostomum complanatum (Trematoda: Digenea: Clinostomatidae) on survival of Triturus carnifex (Amphibia: Urodela: Salamandridae) Giacomo Bruni1,*, Claudio Angelini2 Yeasts in amphibians are common: isolation and the first molecular characterization from Thailand Srisupaph Poonlaphdecha, Alexis Ribas* Introduction of Eleutherodactylus planirostris (Amphibia, Anura, Eleutherodactylidae) to Hong Kong Wing Ho Lee1, Michael Wai-Neng Lau2, Anthony Lau3, Ding-qi Rao4, Yik-Hei Sung5,* Correlation between endoscopic sex determination and gonad histology in pond sliders, Trachemys scripta (Reptilia: Testudines: Emydidae) David Perpiñán1, Albert Martínez-Silvestre2,3, Ferran Bargalló3, Marco Di Giuseppe4, Jorge Orós5, Taiana Costa6,* Book Review: John W. Wilkinson. Amphibian Survey and Monitoring Handbook. Pelagic Publishing Franco Andreone Book Review: Susan Newman. Frogs amphibians and their threatened environment. Discovery and expression through Art K-3. Frogs are green Franco Andreone