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Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest

Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike... Revista Brasileira de Ornitologia, 23(4), 405-416 ARTICLE December 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest 1,3,5 2,3 1,4 Nelson Buainain , Michele Leocádio Gaspar and Claydson P. de Assis Departamento de Vertebrados, Setor de Ornitologia, Quinta da Boa Vista, São Cristóvão, CEP 20940-040, Rio de Janeiro, RJ, Brazil. Laboratório de Entomologia, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Ilha do Fundão, C.P. 68044, CEP 21941-971, Rio de Janeiro, RJ, Brazil. Programa de Pós-Graduação em Zoologia do Museu Nacional/UFRJ, Quinta da Boa Vista, São Cristóvão, CEP 20940-040, Rio de Janeiro, RJ, Brazil. Laboratório de Genética e Evolução Molecular de Aves, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, CEP 05508-090, São Paulo, SP, Brazil. Corresponding author. nnbuainain@gmail.com Received on 28 April 2015. Accepted on 15 February 2016. ABSTRACT: Despite being an important area for endemic species of birds, the Caatinga biome is highly fragmented due to anthropogenic influences and t here is a lack of study on many aspects of its birds’ biology. In this semiarid environment, rainfall is highly seasonal, with two different and we ll-defined periods: a long dry season, and a short rainy season. This study aimed to qualify and quantify the diet of Sakesphorus cristatus, an endemic thamnophilid bird of the Caatinga, as well as to determine whether there was temporal variation between two different seasons and between dry seasons of two consecutive years. Surprisingly, this was the first study to have focused on describing and quantifying items found of any bir d species’ diet in the Caatinga. We analyzed the stomach contents of 72 specimens collected in the municipality of São Felix do Coribe, Bahia, Brazil. Data analysis included relative abundance and occurrence, average consumption/sample and alimentary importance index of each food category. Sampling adequacy was assessed using cumulative curves constructed with diversity index and coefficient of variation. In general t here is a high predominance of ants and termites, with seasonal shifts in the proportion of each item, and a high contribution of caterpillars during the breeding season. During the dry season, the most predominant prey categories in the diet were Formicidae, Isoptera and Coleoptera (adult, A), while during the rainy season, there was an increase in the proportion of Isoptera, Coleoptera (A) and Lepidoptera (larvae) consumption and a decrease in Formicidae. There was no significant difference between consumption of prey items between the two dry seasons. The overall analysis suggests that S. cristatus feeds mainly on the aforementioned insects and is an opportunistic species, adjusting its diet according to their prey availability. KEY-WORDS: Caatinga, feeding biology, insectivory, stomach contents, temporal variation. INTRODUCTION 2005, Lopes et al. 2005, Lima et al. 2010), or place their focus on unusual food items found in the stomach of a small number of specimens (e.g., Andrade et al. 2001), Research on the feeding biology of Brazilian birds was mainly shaped by pioneers more than half a century while collecting data for other purposes (Pacheco & ago, such as Moojen et al. (1941), Hempel (1949) and Gonzaga 1995). Schubart et al. (1965), who analyzed stomach contents Other areas of interest, such as the detailed of various species based on few specimens. However, the description and quantification of items found in the diet of Neotropical bird species as well as their correlations interest of Brazilian ornithologists on the diets of birds was not revived until the 1990’s. Since then, publications with environmental variables, have been neglected about avian diets have seen a significant increase. In (but see Chapman & Rosenberg 1991, Biondi et al. general, more recent studies either focus on questions 2005, Zilio 2006, Cabral et al. 2006, Fernandes 2007). regarding herbivory/frugivory (Francisco & Galetti 2001, Especially significant aspects of avian diets, such as seasonality, often fail to be addressed. However, birds in Chatellenaz 2008, Silva & Melo 2011), community studies, especially in Atlantic Forest (Durães & Marini seasonally well–defined environments may change their Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis diet (Bucher et al. 2003) and/or foraging strategy (Hejl seasons are clearly distinct, but rainfall is irregular and & Verner 1990) according to changes in food availability. seasonal, leading to a complex dynamic environment. This theme is alrea dy well known for temperate birds, This biome is still poorly studied in many aspects, among where changes in environmental aspects are considered them, avian diet as well as feeding adaptations to survive to be more dramatic. Nevertheless, it is still poorly in those extreme conditions. discussed in Neotropical ornithology despite the diversity The analyzed bird specimens were collected in the of species and environments of this region. Most tropical municipality of São Félix do Coribe, Bahia State, not biomes have more stable conditions regarding changes specifically for the purpose of this study. The study site in the environment when compared to temperate ones. is located at 13°20'3.19"S 43°48'24.12"W, near the However, some suffer abrupt changes of conditions along Corrente River, a tributary of the São Francisco River the year especially related to rainfall, as it is the case of the (middle region of São Francisco). The local vegetation is Brazilian Cerrado and Caatinga dry forests. characteristic of the Caatinga morpho-climatic domain Within this framework, the Silvery-Cheeked (Veloso et al. 1991) and comprises a native secondary Antshrike, Sakesphorus cristatus (Wied, 1831), is a vegetation of shrubby dry forests in early stages of bird species endemic to the Brazilian driest biome, the development. (Figure 1B, C). Caatinga. It is locally common at the understory and mid-story stratum (Stotz et al. 1996) of lower growth and Collection of data edges of deciduous woodlands and arid scrubs (Ridgely For the study, the contents of 72 stomachs, which are & Tudor 2009) that typically compose the Caatinga. housed at the collection of Museu Nacional, Universidade These birds are usually seen in pairs in mixed flocks next Federal do Rio de Janeiro, were analyzed. Twenty nine of to Megaxenops parnaguae Reiser 1905, Myrmorchilus these were collected in April 2010, 29 in April 2011 at the strigilatus (Wied, 1831), Taraba major (Vieillot, 1816), beginning of the dry season, and 14 in November 2010 Herpsilochmus pileatus (Lichtenstein, 1823), Cantorchilus at the beginning of the rainy season. The complete list of longirostris (Vieillot, 1819) and Formicivora melanogaster specimens can be found in the Appendix. As a reference Pelzeln, 1868 (Sick 1985, Teixeira et al. 1991, Olmos for the rainfall index, the city of Correntina, Bahia, was 2010). The Silvery-Cheeked Antshrike is considered a chosen as the area closest to the data collection site. Data typical insectivorous bird, however, there is no research were collected from the INMET (Instituto Nacional de on its diet and foraging behavior. Available information Meterologia / National Institute of Meteorology) website. is deduced from research on diverse species within the The stomach contents of each specimen were genus Sakesphorus (Zimmer & Isler 2003) and therefore analyzed with a stereo microscope hund Wetzlar h 33/10x. based on speculation. In order to address this gap, the Prey items in each sample were identified, counted and present paper qualifies and quantifies food items found preserved in 70% alcohol. Some of the fragments were in the diet of the Sakesphorus cristatus during the rainy photographed in the Laboratório de Entomologia, as well as the dry season. Moreover, the paper aims to Universidade Federal do Rio de Janeiro, to support the outline a correlation between the findings and t he identification of arthropods in future works. extreme environmental conditions specifically found in Food items were identified to the lowest possible the Caatinga. Besides being the first recor d on S. cristatus’ taxonomic level and categorized to Order level for diet, the present paper is also the first to analyze the diet statistical analysis. Formicidae (within Hymenoptera) and and its seasonal variation based on stomach contents of a seeds had their own categories. The category Hymenoptera bird in the Caatinga biome. included the non-Formicidae and possible Formicidae that could not be accurately identified. The identification was done based on specialized literature (Borror et al. METHODS 1989, Costa et al. 2006, Rafael et al. 2012), visits to the entomological collection of the Universidade Federal do Study area Rio de Janeiro, as well as photographs and illustrations of The area of the Caatinga is estimated to cover 800,000 fragments presented in other works on the diet of birds km² (IBGE 1985), encompassing all northeastern states (Ralph et al. 1985, Chapman & Rosenberg 1991, Gomes of Brazil as well as the northern part of Minas Gerais et al. 2001, Manhães et al. 2010). Most of the arthropods (Figure 1A). Historically, the area has been considered a were very fragmented, so body parts were associated by poor environment regarding species richness (compared morphological similarities and counted to estimate the to other Brazilian biomes), neglecting the significant minimum number of individuals of each category present number of endemic species. The C aatinga has an extreme in the sample. Seeds were counted individually. Each seed and irregular rainfall regime, with dry periods lasting up or individual prey was counted as one item. to eight months (Sick 1985, IBGE 2010). Dry and rainy A natural bias of diet studies based on stomach Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis FIGURE 1. Map showing the study site and the extension of the Caatinga Biome in Brazilian territory (A). Close up of Google Earth satellite view of the study site location (B). Picture of the shrubby Caatinga forest fragment at the study site (C). contents cannot be avoided, as the digestion of soft bodied are adequate when the coefficient of variation reaches arthropods, such as termites, is faster than the digestion 15%. The importance of each category in the diet was of hard bodied arthropods, such as beetles (Dillery 1965, estimated using a modified A limentary Importance Rosenberg & Cooper 1990). Nevertheless, sclerotized index (AI ) of Kawakami & Vazzoler (1980). This index parts, such as the jaws of termites and the chelicerae of considers the relative abundance and occurrence of each spiders, remain in the sample even after the rest of the category, thus reducing the bias caused by items that body was digested (Chapman & Rosenberg 1991). either occur frequently, but in small numbers or items that occur sporadically, but in great quantities. This index Statistical analyses was calculated by the equation stated below, in which RO is the relative occurrence and  the mean relative The method proposed by Durães & Marini (2005) was abundance of each category ( ). The RO was calculated by applied to verify if the sampling was properly representing dividing the number of samples occurring in one category the diet of the species. Using Estimates version 8.2, by the total sample number ( ). The relative abundance sampling adequacy of each season was assessed by building (RA ) was calculated by dividing the number of items of cumulative curves with two different parameters: diet a certain category by y the total of items of that sample. diversity (DD) (using Shannon index) and the associated In a next step, the  of each category was obtained by coefficient of variation (CV) (S hannon index standard adding the RA among the samples and dividing it by the deviation/DD). Firstly, a sample was selected randomly total sample number. and its diet diversity index was calculated. Secondly, a second sample was added and the index of both samples ൌ   Ȁ ሺ   ሻ was calculated. The procedure was repeated without replacements of samples until all samples were added. After 100 runs, the DD of each round was calculated The software PAST 2.17c (Hammer et al. 2001) based on their mean value. The CV was calculated from was used to verify the suspected existence of annual diet the DD mean values. Adequacy was inferred by visual variations between the dry seasons of 2010 and 2011, inspection of diet diversity curve and by the hypothesis and seasonal diet variations between dry and rainy season of Durães & Marini (2005), which states that samples of 2010. A multivariate Non-Parametric MANOVA Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis (PERMANOVA), which explores the power of a with the parameters of Durães & Marini (2005). In both multivariate analysis and Mann-Whitney’s U test of each periods the coefficient of variation was 10% or less when category, was used to assess the level of significance of the diversity curve stabilized, thus below the proposed variations. A P level of 0.05 was used for all statistical tests 15% threshold (Figure 2). Our results match the ones and Bonferroni correction was applied when multiple obtained by Durães & Marini (2005) for Atlantic Forest statistical comparisons were done. A Non-Parametric test birds and those by Chapman & Rosenberg (1991) for was used because data did not meet the homoscedastic Amazonian Woodcreepers. According to the method, and normality assumption. eight to ten samples were enough to statistically estimate Regarding the evaluation of sampling adequacy the diet of Silvery-Cheeked Antshrike in the shrubby methods, our coefficient of variation was in agreement Caatinga in both periods. FIGURE 2. Diet diversity (DV, black squares) and coefficient of variation (CV, white circles) of the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus) in the dry and wet seasons. The graphs show t hat both seasons had adequate minimum sampling to estimate the species diet during those periods. The greater index of diet diversity during the rainy season when compared to the dry season, shows a greater equitability between the different categories consumption rate in the diet during the rainy season. RESULTS during the dry season. It was present in all samples, which is an extremely significant result considering that A total of 6,244 items belonging to 16 categories were 58 stomachs were analyzed. The maximum number identified. In both seasons, there was a predominance of the recorded was 258 ants in a single specimen. Isoptera was following categories: Formicidae (ants), Isoptera (termites) the second most representative category; it also showed high numbers for all analyzed indexes and the maximum and Coleoptera (beetles: A, Adult). Relative abundance and occurrence, food importance index and average items number of individuals in a single sample was 181. per sample of the different categories are shown in Table 1. Coleoptera (A) had much lower index values compared to the previous two categories; nevertheless, beetles were Dry season present in 54 of 58 samples. The other categories had an AI equal or less than We recorded 5,630 items in the 58 dry season samples. 1% and were considered rare or sporadical items, The minimum number of items found in one sample was including the following: seeds, Coleoptera (L, larvae), 15, the maximum was 293, and the average was 95.03 Lepidoptera (adults, A, and larvae, L), Hemiptera, items/sample. Araneae, Pseudoscorpiones, Neuroptera (larvae), Diptera, Chilopoda, Thysanoptera, Acari and Hy menoptera. Five Formicidae had the highest rates for all indexes Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis TABLE 1. Arthropods in the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus). All parameters calculated for each season and category based on 72 stomach samples. (A) adult, (L) larvae. CategoryImportance Index Relative abundance Relative occurrence Average of consumption (%) (%) (%) (Items/sample) Dry Rainy Dry Rainy Dry Rainy Dry Rainy Season Season Season Season Season Season Season Season Formicidae 64.19 29.69 58.30 27.85 100 93 56.60 12.21 Isoptera 31.63 50.26 36.89 50 97 100 35.81 21.79 Coleoptera (A) 3.34 12.26 2.71 10 93 93 2.64 4.14 Hymenoptera 0.73 0.24 1.20 0.82 48 29 1.17 0.29 Lepidoptera (L) 0.06 6.05 0.24 7 24 64 0.24 3.07 Araneae 0.01 0.69 0.14 0.89 10 29 0.14 0.36 Pseudoscorpiones 0.01 0.19 0.09 0.82 7 21 0.09 29 Chilopoda 0.01 0.00 0.09 0 9 0 0.07 0 Coleoptera (L) 0 0.24 0.04 0.99 3 21 0.04 0.43 Lepidoptera (A) 0 0 0.02 0 2 0 0.02 0 Hemiptera 0 0.06 0.05 0.33 5 14 0.05 0.14 Neuroptera (L) 0 0.17 0.04 0.82 3 14 0.03 0.29 Diptera 0 0.16 0.04 0.33 3 0 0.04 0.14 Thysanoptera 0 0 0.02 0 2 0 0.02 0 Acari 0 0 0.04 0 3 0 0.04 0 seeds in four of 58 samples were found, all apparently variation by Mann-Whitney’s U test were Formicidae (U being of the same species considering the morphological = 42, Z= 4.98 , p <0.00), Coleoptera (A) (U = 250.5, Z= similarity. The diet diversity index was 0.87. -1.88, p <0.04), Lepidoptera (L) (U = 190, Z= -3.37, p The NP-MANOVA did not show significant <0.00) and Araneae (U = 293.5, Z= -2.15, p <0.03). The difference in consumption of prey between dry seasons on basic statistics can be found in Table 2. There was an abrupt different years (p<0.56), neither did Mann-Whitney’s U decrease of the total average consumption per specimen test for the categories individually. Consumption of items with fewer items being consumed during the rainy season was slightly higher in 2011 than in 2010. We recorded than the dry season. The two main categories (Formicidae 2,983 items in 2011 (mean = 102.86 individuals/sample) and Isoptera) had considerable reduction in the average versus 2,648 in 2010 (mean 91.31 individuals/sample). consumption, while Coleoptera (A) and Lepidoptera (L) increased significantly. Regar ding consumption of Rainy season ants, the relative abundance (from 58 to 28%) and the average consumption (from 56.60 to 13.15 individuals/ We identified 614 items in 14 samples. The minimum sample) reductions were dramatic. Despite the reduction number of items per sample was eight, the maximum of average consumption, the second most abundant and was 82, and the average was 39.74. Isoptera was the most important (AI ) category during dry season, Isoptera, had important category (AI ), occurring in all samples, followed one of the highest rates in the rainy season. Regarding by Formicidae and Coleoptera (A). Another important Lepidoptera (L), this increase is particularly striking: category was Lepidoptera (L, larvae) (Table 1), even though the AI increased from 0.06 to 6.05% and the average its indexes were not as significant as the latter categories. consumption from 0.24 to 3.07 individuals/sample. Their average consumption was 3.07 individuals/sample, There was also an increase in the importance index of nine a number similar to that of adult beetles. The other out of 16 prey categories, indicating a greater diversity categories summed up 6% of the items found. Chilopoda, of the diet during the rainy season. This increase in the Thysanoptera, Lepidoptera (A) and seeds were not recor ded diet diversity is also supported by the diet diversity index in this season. The diet diversity index was 1.33. variation (dry = 0.87; rainy = 1.33) (Figure 2A, B). Seasonal variation Sampling adequacy The NP-MANOVA showe d a significant difference in The curves of sampling adequacy showe d that both, the consumption of prey between seasons (p<0.00). The dry and the rainy season samplings, were stabilized and categories that had an acceptable significance level of thus properly estimated the diet of S. cristatus during Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis those periods (Figure 2A, B). In the dry season, the completely stabilized with nine samples (CV = 5%). curve began to stabilize with only three or four samples, For the rainy season, sampling was stabilized with nine when the coefficient of variation (CV) reached 10% and samples, when the CV was 5%. TABLE 2 (1). Basic statistics for each item in dry and rainy season in the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus).  Isoptera Formicidae Hymenoptera ColeopteraLepidopteraHemiptera Araneae            Dry season n 5858 58 585858 58 Min 07 0 000 0 Max 181 259 7 7 1 1 3 Sum 2069 3189 63 147 15 3 7 Mean 35.67 54.98 1.08 2.53 0.25 0.05 0.12 Standard error 4.89 4.77 0.22 0.22 0.05 0.02 0.06 Variance 1391.13 1324.47 2.95 2.81 0.19 0.04 0.21 Standard deviation 37.29 36.39 1.71 1.67 0.44 0.22 0.46 Coefficient of variation 104.55 66.19 158.32 66.19 170.79 431.91 382.62 Rainy season            n 1313 13 131313 13 Min 10 0 000 0 Max 56 48 1 981 2 Sum 248 156 4 54 38 2 5 Mean 19.07 12.00 0.30 4.15 2.92 0.15 0.38 Standard error 4.62 3.4 0.13 0.77 0.87 0.1 0.18 Variance 278.07 150.66 0.23 7.8 9.91 0.14 0.42 Standard deviation 16.67 12.27 0.48 2.79 3.14 0.37 0.65 Coefficient of variation 87.41 102.28 156.12 67.26 107.69 244.09 169.11 TABLE 2 (2). Basic statistics for each item in dry and rainy season in the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus).   Pseudoscorpiones NeuropteraDipteraChilopoda Thysanoptera Acari Seeds Dry season           n 58 5858585858 58 Min 0 00000 0 Max 2 11111 1 Sum 5 22412 3 Mean 0.08 0.03 0.03 0.06 0.01 0.03 0.05 Standard error 0.04 0.02 0.02 0.03 0.01 0.02 0.02 Variance 0.11 0.03 0.03 0.06 0.01 0.03 0.04 Standard deviation 0.33 0.18 0.18 0.25 0.13 0.18 0.22 Coefficient of variation 393.79 533.77 533.77 370.63 761.57 533.77 431.91 Rainy season           n 13 1313131313 13 Min 0 00000 0 Max 2 31000 0 Sum 4 42000 0 Mean 0.3 0.3 0.15 0.00 0.00 0.00 0.00 Standard error 0.17 0.23 0.1 0.00 0.00 0.00 0.00 Variance 0.39 0.73 0.14 0.00 0.00 0.00 0.00 Standard deviation 0.63 0.85 0.37 0.00 0.00 0.00 0.00 Coefficient of variation 204.88 277.82 244.09 0.00 0.00 0.00 0.00 Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis Arthropod composition the families of beetles, Curculionidae (Figures 3F and 4E), Chrysomelidae, Cerambycidae, Nitidulidae, We identified at least 13 ant morphotypes. Among Tenebrionidae and Scarabaeoidea (superfamily) were the identified genera, there were Cephalotes (Figure found. Among these taxa, Tenebrionidae, Scarabaeoidea 3A), Pheidole (Figure 3B) and Odontomachus (Figure and Nitidulidae are predominantly detritivores and 3C). At least three morphotypes of Cephalotes were the others are phytophagous. The most common identified, making it one of the most frequent and beetle taxa were Curculionidae, Chrysomelidae and abundant preys in the diet of S. cristatus. In contrast, Cerambycidae, and among these, two morphotypes winged ants were rare. Regarding termites, we found of the tribe Naupactini (Curculionidae) (Figure the castes of workers (Figure 3D) and soldiers (Figures 3F) were extremely common and identified in most 3E and 4D), with workers being the most frequent samples. Among the non-Formicidae Hymenoptera, and abundant. No winged termite was found. Among wasps (Vespidae) and bees (Apidae) were found. FIGURE 3. Arthropod fragments from the stomach contents of the Silvery-Cheeked Antshrike (Sakesphorus cristatus). A total of 72 stomachs were sampled. A: Cephalotes sp. (Formicidae); B: Pheidole sp. (Formicidae); C: Odontomachus sp. (Formicidae); D: Worker termite (Isoptera); E: Soldier termite (Isoptera); F: Weevil’s head (Curculionidae: Naupactini); G: Sorts of elytra (Coleoptera); H: Caterpillar (Lepidoptera, L); I: Chelicerae (Araneae); J: Seed; K: Caterpillar’s head (Lepidoptera, L). Scale bar = 1mm. Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis The identified spiders belong to Theraphosidae but the ones we could identify were either lace Tingidae (tarantulas) (Figure 4I), one of them remarkably large, as (bugs) or Auchenorrhyncha (cicadas), both typically sap- well as Salticidae (jumping-spiders) and Thomisidae (crab sucking phytophages. The only dipteran found was a spiders). The hemipterans were rare and very fragmented Brachycera (fly) (Figure 4H). FIGURE 4. Arthropod fragments from the stomach contents of the Silvery-Cheeked Antshrike (Sakesphorus cristatus). A total of 72 stomachs were sampled. A-C: Ants (Formicidae); D: Soldier termite (Isoptera); E: Weevil’s head (Curculionidae: Erodiscinae); F: Weevil’s abdomen and leg (Curculionidae); G: Coleoptera larva; H: Fly (Diptera: Brachycera); I: Tarantula (Araneae: Theraphosidae). Scale bar = 1mm. DISCUSSION these are reported as typical food for Thamnophilidae (Gomes et al. 2001, Durães & Marini 2005, Lopes et al. Our data confirmed t hat the Silvery-cheeked Antshrike is 2005, Aguiar & Coltro-Júnior 2008, Manhães & Dias 2008, Lima et al. 2010), while apterous termites, one of a predominantly insectivorous species. We found that the proportion and occurrence of consumption of the different the most important categories in our study, have not been categories of prey varies significantly between seasons. commonly mentioned in the literature so far, especially The taxa most commonly identified were For micidae, not in such great quantities/proportions. Isoptera, Coleoptera (A) and Lepidoptera (L). Three of Our results show that ants are one of the key Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis resources to the bird species under study and probably abundant. Beetles are either less important for the diet of to other birds in Caatinga. Their importance was alrea dy S. cristatus compared to other birds, or underestimated by suggested in previous studies on neotropical birds (Gomes the lack of a method concerning the mass of each category. et al. 2001, Aguiar & Coltro-Júnior 2008, Lopes et al. Caterpillars were the fourth most consumed 2005) and is attributed to their natural abundance (Poulin category during the rainy season, but still very relevant & Lefebvre 1997, Durães & Marini 2005). Nevertheless, in S. cristatus diet. Because they are energetically rich and they were the most consumed category during the dry soft bodied they are considered one of the most important season, when availability of insects and other arthropods food sources for nestlings (Yard et al. 2004), as well as for in Caatinga is extremely low. For nearly all arthropods the diet of many adult birds during rainy periods. The studied in this biome, there was much greater abundance importance in the consumption of lepidopteran larvae during rainy season (Vasconcellos et al. 2007, Santos during the breeding season has already been discussed by et al. 2009, Araújo et al. 2010a, Araújo et al. 2010b, several authors, including studies in arid regions (Holmes Vasconcellos et al. 2010, Oliveira et al. 2011) with strong 1990, Poulin et al. 1994, Yard et al. 2004, Biondi et al. positive correlation with rainfall and relative humidity. 2005, Lopes et al. 2005). The higher consumption of The ant populations, however, have an abundance pattern lepidopterans during the rainy season was also observed opposite of other insects. Their peak of abundance and in stomach contents of other bird species from the same activity is during the dry season (Nunes et al. 2011, study area (NBN unpublished data). Based on these Medeiros et al. 2012), which makes them an extremely results we suggest that these insects are also important for important resource during this time of the year. the breeding biology of Caatinga birds. Although apterous termites are not commonly The other food categories consumed by Silvery- reported in diet studies of neotropical birds as important Cheeked Antshrike were much less numerous. prey, we found them in our study to be an essential food Nevertheless, special attention should be given to the resource. These insects play a very important role not presence of fruits. Poulin et al. 1994) observed a higher only in the diet of the Silvery-cheeked Antshrike but in consumption of fruits by many bird species in an arid the other Caatinga birds since many other bird species of region of Venezuela during the dry season, when the same area consume them widely (NBN unpublished arthropod abundance and water availability is critical. data). This matches the findings of other vertebrates Even though consumption was very low and probably previously studied in arid/semi-arid environments, not significant to S. cristatus diet, this may be an evidence including birds, reptiles, amphibians and bats (Advani of opportunism and plasticity in the feeding behavior 1982, Poulin et al. 1994, Griffiths & Christian 1996, of species that live in extreme conditions of survival, Gibson 2001, Cabral et al. 2006, Hardy & Crnkovic such as food or water scarcity (Wendelken & Martin 2006, Kolodiuk et al. 2010). Its absence in diet studies 1988, Poulin et al. 1994). Opportunistic and sporadic is probably due to the difficulty of identifying them, or consumption of fruits during the dry season in other perhaps the small number of studies made with semi-arid Sakesphorus as well as Thamnophilidae species has alrea dy environments’ species. Because their body is extremely been reported (Haverschmidt 1968, Poulin et al. 1994, soft and thin, body parts are quickly digested leaving only Lima et al. 2010). their mandibles, which may be confounded with the ones The diet of Silvery-Cheeked Antshrike seems to be of other insects. associated with availability of food, which in turn, is most Despite their low abundance, coleopterans were positively correlated with rainfall and relative humidity identified in 93% of all samples in both seasons. Their (except for Formicidae). During the dry season, its diet ubiquitousness in studies on the diet of thamnophilids relies mainly on resources that are able to maintain their shows that coleopterans are, indeed, essential resources population, as in the case of ants and termites. On the for these birds. Nevertheless, even though they were very other hand, during the rainy season, it consumes more frequent in this study, their relative abundance in the diet energy-rich food, such as caterpillars and beetles. Even of Silvery-cheeked Antshrike was very low compared to though we did not conduct an insect survey of the area, those obtained in studies of thamnophilid birds in other other studies on insect population fluctuation in the biomes such as the Amazon and Atlantic Forests (Lopes Caatinga support our results confirming that the insects et al. 2005, Vasconcelos et al. 2007, Aguiar & Coltro- consumed by S. cristatus are in fact quite abundant Júnior 2008). Their presence and predominance in diet during those periods of time (Vasconcellos et al. 2007, studies of birds is often attributed to their hard bodies Santos et al. 2009, Araújo et al. 2010a, Araújo et al. 2010, and the difficulty of digestion of the elytra, which would Vasconcellos et al. 2010, Oliveira et al. 2011, Nunes et al. facilitate the detection of this group (Willis & Oniki 2011, Medeiros et al. 2012). 1978). However, that did not happen in the case of S. Studies on feeding biology, along with others such as cristatus, where Formicidae and Isoptera were much more breeding biology, taxonomy, and distributional patterns, Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis Araújo, V. F. P.; Bandeira, A. G. & Vasconcellos, A. 2010b. provide the most basic knowledge about a bird’s natural Abundance and stratification of soil macroarthropods in a history. This, in turn, comprises the fundamental resource Caatinga Forest in Northeast Brazil. Brazilian Journal of Biology, for the conservation of species and environments. The 70: 737-746. fact that our results are the first information based on Biondi, L. M.; Bó, M. S. & Favero, M. 2005. Dieta del Chimango stomach contents of any bird in Caatinga, being the (Milvago chimango) durante el período reproductivo en El sudeste de La província de Buenos Aires, Argentina. Ornitologia species addressed one of the most common in the biome, Neotropical, 16: 31-42. draws attention to a bigger, problematic scenario. Even Borror, D. J.; Triplehorn, C. A. & Johnson, N. F. 1989. An though our scientific co llections and study methods have introduction to the study of insects. Orlando, FLA: Saunders College significantly improved since the work of Moojen e t al. Publishing. Bucher, E. H.; Tamburini, D.; Abril, A. & Torres, P. 2003. Folivory (1941), many species lack basic information about their in the white-tipped plantcutter Phytotoma rutila: seasonal natural history. Although this is especially true for birds in variations in the diet composition and quality. Journal of Avian Caatinga, there still remains a gap for many other species. Biolology, 34: 211-216. Thus, we emphasize the need to increase the number of Cabral, J. C.; Granzinolli, M. A. M. & Motta-Junior, J.C. 2006. Dieta do quiriquiri, Falco sparverius (Aves: Falconiformes), na studies focusing on the basic knowledge of Neotropical Estação Ecológica de Itirapina, SP. Revista Brasileira de Ornitologia, birds as well as the use of specimens housed in scientific 14: 393-399. collections. Chapman, A. & Rosenberg, K. 1991. Diet of four sympatric amazonian Wodcreepers (Dendrocolaptidae). Condor, 93: 904-915. Chatellenaz, M. L. 2008. Diet of the Grayish Saltator (Saltator coerulescens) in north-eastern Argentina. Ornitologia Neotropical, ACKNOWLEDGEMENTS 19: 617-625. Costa, C.; Ide, S. & Simioka, C. E. 2006. Insetos imaturos, metamorfose e identificação. Ribeirão Preto: Ed itora Holos. We thank Renata Durães for the assistance with Dillery, D. G. 1965. Post-mortem digestion of stomach contents in methods. Renner Baptista, José Ricardo Mermudes the Savannah Sparrow. The Auk, 58: 281. and all members of the Laboratório de Entomologia, Durães, R. & Marini, M. A. 2005. A quantitative assessment of bird Universidade Federal do Rio de Janeiro for the aid diets in the Brazilian Atlantic Forest, with recommendations for future diet studies. Ornitologia Neotropical, 16: 65-83. with identification of arthropods, the space and stereo Fernandes, F. R.; Cruz, L. D. & Rodrigues, A. A. F. 2007. Diet microscope camera provided. Marianna Simões, Laura of the Gray-Breasted Martin (Hirundinidae: Progne chalybea) in a Stransky and Magdalena Rodekirchen for the English wintering are in Maranhão, Brazil. Revista Brasileira de Ornitologia, review. Marcos André Raposo for the final review, and 15: 445-447. valuable textual advices. Fundação Carlos Chagas Filho Francisco, M. R. & Galetti, M. 2001. Frugivoria e dispersão de sementes de Rapanea lancifolia (Myrsinaceae) por aves numa área de Amparo à Pesquisa do Estado do Rio de Janeiro de cerrado do Estado de São Paulo, Sudeste do Brasil. Ararajuba, (FAPERJ) for the financial support to CPA (Process 9: 13-19. number E-26/101.489/2010) and NBN (Process Gibson, L.A. 2001. Seasonal changes in the diet and food availability number 100.682/2012). CPA also thank to Fundação of the greater bilby (Macrotis lagotis) in south-western Queensland. Wildlife Research, 28: 121-134. de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Griffiths, A. D. & Christian, K. A. 1996. Diet and habitat use of Process number 2014/10914-2) and A Coordenação de frillneck lizards in a seasonal tropical environment. Oecologia, Aperfeiçoamento de Pessoal de Nível Superior (CAPES) 106: 39-46. for financial support. Gomes, V. S. M.; Alves, V. S. & Ribeiro, J. R. I. 2001. Itens encontrados em amostras de regurgitação de Pyriglena leucoptera (Vieillot) (Aves, Thamnophilidae) em u ma floresta secundária no Estado do Rio de Janeiro. Revista Brasileira de Zoologia, 18: 1073-1079. REFERENCES Hammer, Ø.; Harper, D. A. T. & Ryan, P. D. 2001. PAST: Paleontological Statistics Software Package for Education and Advani, R. 1982. Seasonal fluctuations in the diet composition of Data Analysis. Palaeontologia Electronica, 4(1): 9pp. Rhinopoma hardwickei in the Rashastan desert. Proceedings of the Hardy, L. M. & Crnkovic, A. C. 2006. Diet of amphibians and Indian Academy of Science, 91: 563-568. reptiles from the Engare Ondare River region of central Kenya, Aguiar, K. M. 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Revista Brasileira de Entomologia, 56: 81-85. cyphergaster (Silvestri) (Isoptera: Termitidae) in the Dry Forest of Moojen, J.; Carvalho, J. & Lopes, H. S. 1941. Observações sobre Caatinga, Northeastern Brazil. Neotropical Entomology, 36: 693- o conteúdo gástrico de aves brasileiras. Memórias do Instituto 698. Oswaldo Cruz, 36: 405-444. Vasconcellos, A.; Andreazze, R.; Almeida, A. M.; Araujo, H. F. P.; Nunes, F. A.; Segundo, G. B. M.; Vasconcelos, Y. B.; Azevedo, Oliveira, E. S. & Oliveira, U. 2010. Seasonality of insects in the R. & Quinet, Y. 2011. Ground-foraging ants (Hymenoptera: semi-arid Caatinga of northeastern Brazil. Revista Brasileira de Formicidae) and rainfall effect on pitfall trapping in a deciduous Entomologia, 54: 471-476. thorn woodland (Caatinga), northeastern Brazil. Revista de Veloso, R. B.; Rangel Filho, A. L. R. & Lima, J. C. A. 1991. Biología Tropical, 59: 1637-1650. Classificação da vegetação brasileira, adaptada a um sistema universal. Oliveira, V. H. 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Analysis of droppings to describe diets of small birds. Journal Field Ornithology, 56: 165-174. Associate Editor: Marcos Pérsio Dantas Santos Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis APPENDIX Access numbers of specimens of the Silvery-Cheeked Antshrike (Sakesphorus cristatus) whose stomachs were analyzed in this study. Dry season - 2010: MNA 5169; MNA 5172; MNA 5195; MNA 5219; MNA 5228; MNA 5256; MNA 5266; MNA 5270; MNA 5279; MNA 5286; MNA 5309; MNA 5312; MNA 5319; MNA 5322; MNA 5332; MNA 5333; MNA 5336; MNA 6422; MNA 6445; MNA 6488; MNA 6519; MNA 6520; MNA 6713; MNA 6730; MNA 6742; MNA 6872; MNA 7043; MNA 7061. 2011: MNA 7065; MNA 5268; MNA 7067; MNA 7056; MNA 7055; MNA 7054; MNA 7045; MNA 6901; MNA 6898; MNA 6896; MNA 6735; MNA 6727; MNA 7060; MNA 7059; MNA 6909 ; MNA 6899; MNA 6893; MNA 6739; MNA 6738; MNA 7382; MNA 7258; MNA 7254; MNA 7066; MNA 7051; MNA 6921; MNA 6741; MNA 6733; MNA 6736. Rainy season - 2010: MNA 5272; MNA 7024; MNA 7025; MNA 7028; MNA 7030; MNA 7032; MNA 7035; MNA 7036; MNA 7039; MNA 7047; MNA 7048; MNA 7049; MNA 7057; MNA 7062. Revista Brasileira de Ornitologia, 23(4), 2015 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest

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Revista Brasileira de Ornitologia, 23(4), 405-416 ARTICLE December 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest 1,3,5 2,3 1,4 Nelson Buainain , Michele Leocádio Gaspar and Claydson P. de Assis Departamento de Vertebrados, Setor de Ornitologia, Quinta da Boa Vista, São Cristóvão, CEP 20940-040, Rio de Janeiro, RJ, Brazil. Laboratório de Entomologia, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Ilha do Fundão, C.P. 68044, CEP 21941-971, Rio de Janeiro, RJ, Brazil. Programa de Pós-Graduação em Zoologia do Museu Nacional/UFRJ, Quinta da Boa Vista, São Cristóvão, CEP 20940-040, Rio de Janeiro, RJ, Brazil. Laboratório de Genética e Evolução Molecular de Aves, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, CEP 05508-090, São Paulo, SP, Brazil. Corresponding author. nnbuainain@gmail.com Received on 28 April 2015. Accepted on 15 February 2016. ABSTRACT: Despite being an important area for endemic species of birds, the Caatinga biome is highly fragmented due to anthropogenic influences and t here is a lack of study on many aspects of its birds’ biology. In this semiarid environment, rainfall is highly seasonal, with two different and we ll-defined periods: a long dry season, and a short rainy season. This study aimed to qualify and quantify the diet of Sakesphorus cristatus, an endemic thamnophilid bird of the Caatinga, as well as to determine whether there was temporal variation between two different seasons and between dry seasons of two consecutive years. Surprisingly, this was the first study to have focused on describing and quantifying items found of any bir d species’ diet in the Caatinga. We analyzed the stomach contents of 72 specimens collected in the municipality of São Felix do Coribe, Bahia, Brazil. Data analysis included relative abundance and occurrence, average consumption/sample and alimentary importance index of each food category. Sampling adequacy was assessed using cumulative curves constructed with diversity index and coefficient of variation. In general t here is a high predominance of ants and termites, with seasonal shifts in the proportion of each item, and a high contribution of caterpillars during the breeding season. During the dry season, the most predominant prey categories in the diet were Formicidae, Isoptera and Coleoptera (adult, A), while during the rainy season, there was an increase in the proportion of Isoptera, Coleoptera (A) and Lepidoptera (larvae) consumption and a decrease in Formicidae. There was no significant difference between consumption of prey items between the two dry seasons. The overall analysis suggests that S. cristatus feeds mainly on the aforementioned insects and is an opportunistic species, adjusting its diet according to their prey availability. KEY-WORDS: Caatinga, feeding biology, insectivory, stomach contents, temporal variation. INTRODUCTION 2005, Lopes et al. 2005, Lima et al. 2010), or place their focus on unusual food items found in the stomach of a small number of specimens (e.g., Andrade et al. 2001), Research on the feeding biology of Brazilian birds was mainly shaped by pioneers more than half a century while collecting data for other purposes (Pacheco & ago, such as Moojen et al. (1941), Hempel (1949) and Gonzaga 1995). Schubart et al. (1965), who analyzed stomach contents Other areas of interest, such as the detailed of various species based on few specimens. However, the description and quantification of items found in the diet of Neotropical bird species as well as their correlations interest of Brazilian ornithologists on the diets of birds was not revived until the 1990’s. Since then, publications with environmental variables, have been neglected about avian diets have seen a significant increase. In (but see Chapman & Rosenberg 1991, Biondi et al. general, more recent studies either focus on questions 2005, Zilio 2006, Cabral et al. 2006, Fernandes 2007). regarding herbivory/frugivory (Francisco & Galetti 2001, Especially significant aspects of avian diets, such as seasonality, often fail to be addressed. However, birds in Chatellenaz 2008, Silva & Melo 2011), community studies, especially in Atlantic Forest (Durães & Marini seasonally well–defined environments may change their Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis diet (Bucher et al. 2003) and/or foraging strategy (Hejl seasons are clearly distinct, but rainfall is irregular and & Verner 1990) according to changes in food availability. seasonal, leading to a complex dynamic environment. This theme is alrea dy well known for temperate birds, This biome is still poorly studied in many aspects, among where changes in environmental aspects are considered them, avian diet as well as feeding adaptations to survive to be more dramatic. Nevertheless, it is still poorly in those extreme conditions. discussed in Neotropical ornithology despite the diversity The analyzed bird specimens were collected in the of species and environments of this region. Most tropical municipality of São Félix do Coribe, Bahia State, not biomes have more stable conditions regarding changes specifically for the purpose of this study. The study site in the environment when compared to temperate ones. is located at 13°20'3.19"S 43°48'24.12"W, near the However, some suffer abrupt changes of conditions along Corrente River, a tributary of the São Francisco River the year especially related to rainfall, as it is the case of the (middle region of São Francisco). The local vegetation is Brazilian Cerrado and Caatinga dry forests. characteristic of the Caatinga morpho-climatic domain Within this framework, the Silvery-Cheeked (Veloso et al. 1991) and comprises a native secondary Antshrike, Sakesphorus cristatus (Wied, 1831), is a vegetation of shrubby dry forests in early stages of bird species endemic to the Brazilian driest biome, the development. (Figure 1B, C). Caatinga. It is locally common at the understory and mid-story stratum (Stotz et al. 1996) of lower growth and Collection of data edges of deciduous woodlands and arid scrubs (Ridgely For the study, the contents of 72 stomachs, which are & Tudor 2009) that typically compose the Caatinga. housed at the collection of Museu Nacional, Universidade These birds are usually seen in pairs in mixed flocks next Federal do Rio de Janeiro, were analyzed. Twenty nine of to Megaxenops parnaguae Reiser 1905, Myrmorchilus these were collected in April 2010, 29 in April 2011 at the strigilatus (Wied, 1831), Taraba major (Vieillot, 1816), beginning of the dry season, and 14 in November 2010 Herpsilochmus pileatus (Lichtenstein, 1823), Cantorchilus at the beginning of the rainy season. The complete list of longirostris (Vieillot, 1819) and Formicivora melanogaster specimens can be found in the Appendix. As a reference Pelzeln, 1868 (Sick 1985, Teixeira et al. 1991, Olmos for the rainfall index, the city of Correntina, Bahia, was 2010). The Silvery-Cheeked Antshrike is considered a chosen as the area closest to the data collection site. Data typical insectivorous bird, however, there is no research were collected from the INMET (Instituto Nacional de on its diet and foraging behavior. Available information Meterologia / National Institute of Meteorology) website. is deduced from research on diverse species within the The stomach contents of each specimen were genus Sakesphorus (Zimmer & Isler 2003) and therefore analyzed with a stereo microscope hund Wetzlar h 33/10x. based on speculation. In order to address this gap, the Prey items in each sample were identified, counted and present paper qualifies and quantifies food items found preserved in 70% alcohol. Some of the fragments were in the diet of the Sakesphorus cristatus during the rainy photographed in the Laboratório de Entomologia, as well as the dry season. Moreover, the paper aims to Universidade Federal do Rio de Janeiro, to support the outline a correlation between the findings and t he identification of arthropods in future works. extreme environmental conditions specifically found in Food items were identified to the lowest possible the Caatinga. Besides being the first recor d on S. cristatus’ taxonomic level and categorized to Order level for diet, the present paper is also the first to analyze the diet statistical analysis. Formicidae (within Hymenoptera) and and its seasonal variation based on stomach contents of a seeds had their own categories. The category Hymenoptera bird in the Caatinga biome. included the non-Formicidae and possible Formicidae that could not be accurately identified. The identification was done based on specialized literature (Borror et al. METHODS 1989, Costa et al. 2006, Rafael et al. 2012), visits to the entomological collection of the Universidade Federal do Study area Rio de Janeiro, as well as photographs and illustrations of The area of the Caatinga is estimated to cover 800,000 fragments presented in other works on the diet of birds km² (IBGE 1985), encompassing all northeastern states (Ralph et al. 1985, Chapman & Rosenberg 1991, Gomes of Brazil as well as the northern part of Minas Gerais et al. 2001, Manhães et al. 2010). Most of the arthropods (Figure 1A). Historically, the area has been considered a were very fragmented, so body parts were associated by poor environment regarding species richness (compared morphological similarities and counted to estimate the to other Brazilian biomes), neglecting the significant minimum number of individuals of each category present number of endemic species. The C aatinga has an extreme in the sample. Seeds were counted individually. Each seed and irregular rainfall regime, with dry periods lasting up or individual prey was counted as one item. to eight months (Sick 1985, IBGE 2010). Dry and rainy A natural bias of diet studies based on stomach Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis FIGURE 1. Map showing the study site and the extension of the Caatinga Biome in Brazilian territory (A). Close up of Google Earth satellite view of the study site location (B). Picture of the shrubby Caatinga forest fragment at the study site (C). contents cannot be avoided, as the digestion of soft bodied are adequate when the coefficient of variation reaches arthropods, such as termites, is faster than the digestion 15%. The importance of each category in the diet was of hard bodied arthropods, such as beetles (Dillery 1965, estimated using a modified A limentary Importance Rosenberg & Cooper 1990). Nevertheless, sclerotized index (AI ) of Kawakami & Vazzoler (1980). This index parts, such as the jaws of termites and the chelicerae of considers the relative abundance and occurrence of each spiders, remain in the sample even after the rest of the category, thus reducing the bias caused by items that body was digested (Chapman & Rosenberg 1991). either occur frequently, but in small numbers or items that occur sporadically, but in great quantities. This index Statistical analyses was calculated by the equation stated below, in which RO is the relative occurrence and  the mean relative The method proposed by Durães & Marini (2005) was abundance of each category ( ). The RO was calculated by applied to verify if the sampling was properly representing dividing the number of samples occurring in one category the diet of the species. Using Estimates version 8.2, by the total sample number ( ). The relative abundance sampling adequacy of each season was assessed by building (RA ) was calculated by dividing the number of items of cumulative curves with two different parameters: diet a certain category by y the total of items of that sample. diversity (DD) (using Shannon index) and the associated In a next step, the  of each category was obtained by coefficient of variation (CV) (S hannon index standard adding the RA among the samples and dividing it by the deviation/DD). Firstly, a sample was selected randomly total sample number. and its diet diversity index was calculated. Secondly, a second sample was added and the index of both samples ൌ   Ȁ ሺ   ሻ was calculated. The procedure was repeated without replacements of samples until all samples were added. After 100 runs, the DD of each round was calculated The software PAST 2.17c (Hammer et al. 2001) based on their mean value. The CV was calculated from was used to verify the suspected existence of annual diet the DD mean values. Adequacy was inferred by visual variations between the dry seasons of 2010 and 2011, inspection of diet diversity curve and by the hypothesis and seasonal diet variations between dry and rainy season of Durães & Marini (2005), which states that samples of 2010. A multivariate Non-Parametric MANOVA Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis (PERMANOVA), which explores the power of a with the parameters of Durães & Marini (2005). In both multivariate analysis and Mann-Whitney’s U test of each periods the coefficient of variation was 10% or less when category, was used to assess the level of significance of the diversity curve stabilized, thus below the proposed variations. A P level of 0.05 was used for all statistical tests 15% threshold (Figure 2). Our results match the ones and Bonferroni correction was applied when multiple obtained by Durães & Marini (2005) for Atlantic Forest statistical comparisons were done. A Non-Parametric test birds and those by Chapman & Rosenberg (1991) for was used because data did not meet the homoscedastic Amazonian Woodcreepers. According to the method, and normality assumption. eight to ten samples were enough to statistically estimate Regarding the evaluation of sampling adequacy the diet of Silvery-Cheeked Antshrike in the shrubby methods, our coefficient of variation was in agreement Caatinga in both periods. FIGURE 2. Diet diversity (DV, black squares) and coefficient of variation (CV, white circles) of the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus) in the dry and wet seasons. The graphs show t hat both seasons had adequate minimum sampling to estimate the species diet during those periods. The greater index of diet diversity during the rainy season when compared to the dry season, shows a greater equitability between the different categories consumption rate in the diet during the rainy season. RESULTS during the dry season. It was present in all samples, which is an extremely significant result considering that A total of 6,244 items belonging to 16 categories were 58 stomachs were analyzed. The maximum number identified. In both seasons, there was a predominance of the recorded was 258 ants in a single specimen. Isoptera was following categories: Formicidae (ants), Isoptera (termites) the second most representative category; it also showed high numbers for all analyzed indexes and the maximum and Coleoptera (beetles: A, Adult). Relative abundance and occurrence, food importance index and average items number of individuals in a single sample was 181. per sample of the different categories are shown in Table 1. Coleoptera (A) had much lower index values compared to the previous two categories; nevertheless, beetles were Dry season present in 54 of 58 samples. The other categories had an AI equal or less than We recorded 5,630 items in the 58 dry season samples. 1% and were considered rare or sporadical items, The minimum number of items found in one sample was including the following: seeds, Coleoptera (L, larvae), 15, the maximum was 293, and the average was 95.03 Lepidoptera (adults, A, and larvae, L), Hemiptera, items/sample. Araneae, Pseudoscorpiones, Neuroptera (larvae), Diptera, Chilopoda, Thysanoptera, Acari and Hy menoptera. Five Formicidae had the highest rates for all indexes Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis TABLE 1. Arthropods in the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus). All parameters calculated for each season and category based on 72 stomach samples. (A) adult, (L) larvae. CategoryImportance Index Relative abundance Relative occurrence Average of consumption (%) (%) (%) (Items/sample) Dry Rainy Dry Rainy Dry Rainy Dry Rainy Season Season Season Season Season Season Season Season Formicidae 64.19 29.69 58.30 27.85 100 93 56.60 12.21 Isoptera 31.63 50.26 36.89 50 97 100 35.81 21.79 Coleoptera (A) 3.34 12.26 2.71 10 93 93 2.64 4.14 Hymenoptera 0.73 0.24 1.20 0.82 48 29 1.17 0.29 Lepidoptera (L) 0.06 6.05 0.24 7 24 64 0.24 3.07 Araneae 0.01 0.69 0.14 0.89 10 29 0.14 0.36 Pseudoscorpiones 0.01 0.19 0.09 0.82 7 21 0.09 29 Chilopoda 0.01 0.00 0.09 0 9 0 0.07 0 Coleoptera (L) 0 0.24 0.04 0.99 3 21 0.04 0.43 Lepidoptera (A) 0 0 0.02 0 2 0 0.02 0 Hemiptera 0 0.06 0.05 0.33 5 14 0.05 0.14 Neuroptera (L) 0 0.17 0.04 0.82 3 14 0.03 0.29 Diptera 0 0.16 0.04 0.33 3 0 0.04 0.14 Thysanoptera 0 0 0.02 0 2 0 0.02 0 Acari 0 0 0.04 0 3 0 0.04 0 seeds in four of 58 samples were found, all apparently variation by Mann-Whitney’s U test were Formicidae (U being of the same species considering the morphological = 42, Z= 4.98 , p <0.00), Coleoptera (A) (U = 250.5, Z= similarity. The diet diversity index was 0.87. -1.88, p <0.04), Lepidoptera (L) (U = 190, Z= -3.37, p The NP-MANOVA did not show significant <0.00) and Araneae (U = 293.5, Z= -2.15, p <0.03). The difference in consumption of prey between dry seasons on basic statistics can be found in Table 2. There was an abrupt different years (p<0.56), neither did Mann-Whitney’s U decrease of the total average consumption per specimen test for the categories individually. Consumption of items with fewer items being consumed during the rainy season was slightly higher in 2011 than in 2010. We recorded than the dry season. The two main categories (Formicidae 2,983 items in 2011 (mean = 102.86 individuals/sample) and Isoptera) had considerable reduction in the average versus 2,648 in 2010 (mean 91.31 individuals/sample). consumption, while Coleoptera (A) and Lepidoptera (L) increased significantly. Regar ding consumption of Rainy season ants, the relative abundance (from 58 to 28%) and the average consumption (from 56.60 to 13.15 individuals/ We identified 614 items in 14 samples. The minimum sample) reductions were dramatic. Despite the reduction number of items per sample was eight, the maximum of average consumption, the second most abundant and was 82, and the average was 39.74. Isoptera was the most important (AI ) category during dry season, Isoptera, had important category (AI ), occurring in all samples, followed one of the highest rates in the rainy season. Regarding by Formicidae and Coleoptera (A). Another important Lepidoptera (L), this increase is particularly striking: category was Lepidoptera (L, larvae) (Table 1), even though the AI increased from 0.06 to 6.05% and the average its indexes were not as significant as the latter categories. consumption from 0.24 to 3.07 individuals/sample. Their average consumption was 3.07 individuals/sample, There was also an increase in the importance index of nine a number similar to that of adult beetles. The other out of 16 prey categories, indicating a greater diversity categories summed up 6% of the items found. Chilopoda, of the diet during the rainy season. This increase in the Thysanoptera, Lepidoptera (A) and seeds were not recor ded diet diversity is also supported by the diet diversity index in this season. The diet diversity index was 1.33. variation (dry = 0.87; rainy = 1.33) (Figure 2A, B). Seasonal variation Sampling adequacy The NP-MANOVA showe d a significant difference in The curves of sampling adequacy showe d that both, the consumption of prey between seasons (p<0.00). The dry and the rainy season samplings, were stabilized and categories that had an acceptable significance level of thus properly estimated the diet of S. cristatus during Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis those periods (Figure 2A, B). In the dry season, the completely stabilized with nine samples (CV = 5%). curve began to stabilize with only three or four samples, For the rainy season, sampling was stabilized with nine when the coefficient of variation (CV) reached 10% and samples, when the CV was 5%. TABLE 2 (1). Basic statistics for each item in dry and rainy season in the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus).  Isoptera Formicidae Hymenoptera ColeopteraLepidopteraHemiptera Araneae            Dry season n 5858 58 585858 58 Min 07 0 000 0 Max 181 259 7 7 1 1 3 Sum 2069 3189 63 147 15 3 7 Mean 35.67 54.98 1.08 2.53 0.25 0.05 0.12 Standard error 4.89 4.77 0.22 0.22 0.05 0.02 0.06 Variance 1391.13 1324.47 2.95 2.81 0.19 0.04 0.21 Standard deviation 37.29 36.39 1.71 1.67 0.44 0.22 0.46 Coefficient of variation 104.55 66.19 158.32 66.19 170.79 431.91 382.62 Rainy season            n 1313 13 131313 13 Min 10 0 000 0 Max 56 48 1 981 2 Sum 248 156 4 54 38 2 5 Mean 19.07 12.00 0.30 4.15 2.92 0.15 0.38 Standard error 4.62 3.4 0.13 0.77 0.87 0.1 0.18 Variance 278.07 150.66 0.23 7.8 9.91 0.14 0.42 Standard deviation 16.67 12.27 0.48 2.79 3.14 0.37 0.65 Coefficient of variation 87.41 102.28 156.12 67.26 107.69 244.09 169.11 TABLE 2 (2). Basic statistics for each item in dry and rainy season in the diet of the Silvery-Cheeked Antshrike (Sakesphorus cristatus).   Pseudoscorpiones NeuropteraDipteraChilopoda Thysanoptera Acari Seeds Dry season           n 58 5858585858 58 Min 0 00000 0 Max 2 11111 1 Sum 5 22412 3 Mean 0.08 0.03 0.03 0.06 0.01 0.03 0.05 Standard error 0.04 0.02 0.02 0.03 0.01 0.02 0.02 Variance 0.11 0.03 0.03 0.06 0.01 0.03 0.04 Standard deviation 0.33 0.18 0.18 0.25 0.13 0.18 0.22 Coefficient of variation 393.79 533.77 533.77 370.63 761.57 533.77 431.91 Rainy season           n 13 1313131313 13 Min 0 00000 0 Max 2 31000 0 Sum 4 42000 0 Mean 0.3 0.3 0.15 0.00 0.00 0.00 0.00 Standard error 0.17 0.23 0.1 0.00 0.00 0.00 0.00 Variance 0.39 0.73 0.14 0.00 0.00 0.00 0.00 Standard deviation 0.63 0.85 0.37 0.00 0.00 0.00 0.00 Coefficient of variation 204.88 277.82 244.09 0.00 0.00 0.00 0.00 Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis Arthropod composition the families of beetles, Curculionidae (Figures 3F and 4E), Chrysomelidae, Cerambycidae, Nitidulidae, We identified at least 13 ant morphotypes. Among Tenebrionidae and Scarabaeoidea (superfamily) were the identified genera, there were Cephalotes (Figure found. Among these taxa, Tenebrionidae, Scarabaeoidea 3A), Pheidole (Figure 3B) and Odontomachus (Figure and Nitidulidae are predominantly detritivores and 3C). At least three morphotypes of Cephalotes were the others are phytophagous. The most common identified, making it one of the most frequent and beetle taxa were Curculionidae, Chrysomelidae and abundant preys in the diet of S. cristatus. In contrast, Cerambycidae, and among these, two morphotypes winged ants were rare. Regarding termites, we found of the tribe Naupactini (Curculionidae) (Figure the castes of workers (Figure 3D) and soldiers (Figures 3F) were extremely common and identified in most 3E and 4D), with workers being the most frequent samples. Among the non-Formicidae Hymenoptera, and abundant. No winged termite was found. Among wasps (Vespidae) and bees (Apidae) were found. FIGURE 3. Arthropod fragments from the stomach contents of the Silvery-Cheeked Antshrike (Sakesphorus cristatus). A total of 72 stomachs were sampled. A: Cephalotes sp. (Formicidae); B: Pheidole sp. (Formicidae); C: Odontomachus sp. (Formicidae); D: Worker termite (Isoptera); E: Soldier termite (Isoptera); F: Weevil’s head (Curculionidae: Naupactini); G: Sorts of elytra (Coleoptera); H: Caterpillar (Lepidoptera, L); I: Chelicerae (Araneae); J: Seed; K: Caterpillar’s head (Lepidoptera, L). Scale bar = 1mm. Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis The identified spiders belong to Theraphosidae but the ones we could identify were either lace Tingidae (tarantulas) (Figure 4I), one of them remarkably large, as (bugs) or Auchenorrhyncha (cicadas), both typically sap- well as Salticidae (jumping-spiders) and Thomisidae (crab sucking phytophages. The only dipteran found was a spiders). The hemipterans were rare and very fragmented Brachycera (fly) (Figure 4H). FIGURE 4. Arthropod fragments from the stomach contents of the Silvery-Cheeked Antshrike (Sakesphorus cristatus). A total of 72 stomachs were sampled. A-C: Ants (Formicidae); D: Soldier termite (Isoptera); E: Weevil’s head (Curculionidae: Erodiscinae); F: Weevil’s abdomen and leg (Curculionidae); G: Coleoptera larva; H: Fly (Diptera: Brachycera); I: Tarantula (Araneae: Theraphosidae). Scale bar = 1mm. DISCUSSION these are reported as typical food for Thamnophilidae (Gomes et al. 2001, Durães & Marini 2005, Lopes et al. Our data confirmed t hat the Silvery-cheeked Antshrike is 2005, Aguiar & Coltro-Júnior 2008, Manhães & Dias 2008, Lima et al. 2010), while apterous termites, one of a predominantly insectivorous species. We found that the proportion and occurrence of consumption of the different the most important categories in our study, have not been categories of prey varies significantly between seasons. commonly mentioned in the literature so far, especially The taxa most commonly identified were For micidae, not in such great quantities/proportions. Isoptera, Coleoptera (A) and Lepidoptera (L). Three of Our results show that ants are one of the key Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis resources to the bird species under study and probably abundant. Beetles are either less important for the diet of to other birds in Caatinga. Their importance was alrea dy S. cristatus compared to other birds, or underestimated by suggested in previous studies on neotropical birds (Gomes the lack of a method concerning the mass of each category. et al. 2001, Aguiar & Coltro-Júnior 2008, Lopes et al. Caterpillars were the fourth most consumed 2005) and is attributed to their natural abundance (Poulin category during the rainy season, but still very relevant & Lefebvre 1997, Durães & Marini 2005). Nevertheless, in S. cristatus diet. Because they are energetically rich and they were the most consumed category during the dry soft bodied they are considered one of the most important season, when availability of insects and other arthropods food sources for nestlings (Yard et al. 2004), as well as for in Caatinga is extremely low. For nearly all arthropods the diet of many adult birds during rainy periods. The studied in this biome, there was much greater abundance importance in the consumption of lepidopteran larvae during rainy season (Vasconcellos et al. 2007, Santos during the breeding season has already been discussed by et al. 2009, Araújo et al. 2010a, Araújo et al. 2010b, several authors, including studies in arid regions (Holmes Vasconcellos et al. 2010, Oliveira et al. 2011) with strong 1990, Poulin et al. 1994, Yard et al. 2004, Biondi et al. positive correlation with rainfall and relative humidity. 2005, Lopes et al. 2005). The higher consumption of The ant populations, however, have an abundance pattern lepidopterans during the rainy season was also observed opposite of other insects. Their peak of abundance and in stomach contents of other bird species from the same activity is during the dry season (Nunes et al. 2011, study area (NBN unpublished data). Based on these Medeiros et al. 2012), which makes them an extremely results we suggest that these insects are also important for important resource during this time of the year. the breeding biology of Caatinga birds. Although apterous termites are not commonly The other food categories consumed by Silvery- reported in diet studies of neotropical birds as important Cheeked Antshrike were much less numerous. prey, we found them in our study to be an essential food Nevertheless, special attention should be given to the resource. These insects play a very important role not presence of fruits. Poulin et al. 1994) observed a higher only in the diet of the Silvery-cheeked Antshrike but in consumption of fruits by many bird species in an arid the other Caatinga birds since many other bird species of region of Venezuela during the dry season, when the same area consume them widely (NBN unpublished arthropod abundance and water availability is critical. data). This matches the findings of other vertebrates Even though consumption was very low and probably previously studied in arid/semi-arid environments, not significant to S. cristatus diet, this may be an evidence including birds, reptiles, amphibians and bats (Advani of opportunism and plasticity in the feeding behavior 1982, Poulin et al. 1994, Griffiths & Christian 1996, of species that live in extreme conditions of survival, Gibson 2001, Cabral et al. 2006, Hardy & Crnkovic such as food or water scarcity (Wendelken & Martin 2006, Kolodiuk et al. 2010). Its absence in diet studies 1988, Poulin et al. 1994). Opportunistic and sporadic is probably due to the difficulty of identifying them, or consumption of fruits during the dry season in other perhaps the small number of studies made with semi-arid Sakesphorus as well as Thamnophilidae species has alrea dy environments’ species. Because their body is extremely been reported (Haverschmidt 1968, Poulin et al. 1994, soft and thin, body parts are quickly digested leaving only Lima et al. 2010). their mandibles, which may be confounded with the ones The diet of Silvery-Cheeked Antshrike seems to be of other insects. associated with availability of food, which in turn, is most Despite their low abundance, coleopterans were positively correlated with rainfall and relative humidity identified in 93% of all samples in both seasons. Their (except for Formicidae). During the dry season, its diet ubiquitousness in studies on the diet of thamnophilids relies mainly on resources that are able to maintain their shows that coleopterans are, indeed, essential resources population, as in the case of ants and termites. On the for these birds. Nevertheless, even though they were very other hand, during the rainy season, it consumes more frequent in this study, their relative abundance in the diet energy-rich food, such as caterpillars and beetles. Even of Silvery-cheeked Antshrike was very low compared to though we did not conduct an insect survey of the area, those obtained in studies of thamnophilid birds in other other studies on insect population fluctuation in the biomes such as the Amazon and Atlantic Forests (Lopes Caatinga support our results confirming that the insects et al. 2005, Vasconcelos et al. 2007, Aguiar & Coltro- consumed by S. cristatus are in fact quite abundant Júnior 2008). Their presence and predominance in diet during those periods of time (Vasconcellos et al. 2007, studies of birds is often attributed to their hard bodies Santos et al. 2009, Araújo et al. 2010a, Araújo et al. 2010, and the difficulty of digestion of the elytra, which would Vasconcellos et al. 2010, Oliveira et al. 2011, Nunes et al. facilitate the detection of this group (Willis & Oniki 2011, Medeiros et al. 2012). 1978). However, that did not happen in the case of S. Studies on feeding biology, along with others such as cristatus, where Formicidae and Isoptera were much more breeding biology, taxonomy, and distributional patterns, Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis Araújo, V. F. P.; Bandeira, A. G. & Vasconcellos, A. 2010b. provide the most basic knowledge about a bird’s natural Abundance and stratification of soil macroarthropods in a history. This, in turn, comprises the fundamental resource Caatinga Forest in Northeast Brazil. Brazilian Journal of Biology, for the conservation of species and environments. The 70: 737-746. fact that our results are the first information based on Biondi, L. M.; Bó, M. S. & Favero, M. 2005. Dieta del Chimango stomach contents of any bird in Caatinga, being the (Milvago chimango) durante el período reproductivo en El sudeste de La província de Buenos Aires, Argentina. Ornitologia species addressed one of the most common in the biome, Neotropical, 16: 31-42. draws attention to a bigger, problematic scenario. Even Borror, D. J.; Triplehorn, C. A. & Johnson, N. F. 1989. An though our scientific co llections and study methods have introduction to the study of insects. Orlando, FLA: Saunders College significantly improved since the work of Moojen e t al. Publishing. Bucher, E. H.; Tamburini, D.; Abril, A. & Torres, P. 2003. Folivory (1941), many species lack basic information about their in the white-tipped plantcutter Phytotoma rutila: seasonal natural history. Although this is especially true for birds in variations in the diet composition and quality. Journal of Avian Caatinga, there still remains a gap for many other species. Biolology, 34: 211-216. Thus, we emphasize the need to increase the number of Cabral, J. C.; Granzinolli, M. A. M. & Motta-Junior, J.C. 2006. Dieta do quiriquiri, Falco sparverius (Aves: Falconiformes), na studies focusing on the basic knowledge of Neotropical Estação Ecológica de Itirapina, SP. Revista Brasileira de Ornitologia, birds as well as the use of specimens housed in scientific 14: 393-399. collections. Chapman, A. & Rosenberg, K. 1991. Diet of four sympatric amazonian Wodcreepers (Dendrocolaptidae). Condor, 93: 904-915. Chatellenaz, M. L. 2008. Diet of the Grayish Saltator (Saltator coerulescens) in north-eastern Argentina. Ornitologia Neotropical, ACKNOWLEDGEMENTS 19: 617-625. Costa, C.; Ide, S. & Simioka, C. E. 2006. Insetos imaturos, metamorfose e identificação. Ribeirão Preto: Ed itora Holos. We thank Renata Durães for the assistance with Dillery, D. G. 1965. Post-mortem digestion of stomach contents in methods. Renner Baptista, José Ricardo Mermudes the Savannah Sparrow. The Auk, 58: 281. and all members of the Laboratório de Entomologia, Durães, R. & Marini, M. A. 2005. A quantitative assessment of bird Universidade Federal do Rio de Janeiro for the aid diets in the Brazilian Atlantic Forest, with recommendations for future diet studies. Ornitologia Neotropical, 16: 65-83. with identification of arthropods, the space and stereo Fernandes, F. R.; Cruz, L. D. & Rodrigues, A. A. F. 2007. Diet microscope camera provided. 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Analysis of droppings to describe diets of small birds. Journal Field Ornithology, 56: 165-174. Associate Editor: Marcos Pérsio Dantas Santos Revista Brasileira de Ornitologia, 23(4), 2015 Detailed description and seasonal variation in the diet of the Silvery-Cheeked Antshrike Sakesphorus cristatus (Wied, 1831) (Aves: Thamnophilidae) in a Brazilian semi-arid forest Nelson Buainain, Michele Leocádio Gaspar and Claydson P. de Assis APPENDIX Access numbers of specimens of the Silvery-Cheeked Antshrike (Sakesphorus cristatus) whose stomachs were analyzed in this study. Dry season - 2010: MNA 5169; MNA 5172; MNA 5195; MNA 5219; MNA 5228; MNA 5256; MNA 5266; MNA 5270; MNA 5279; MNA 5286; MNA 5309; MNA 5312; MNA 5319; MNA 5322; MNA 5332; MNA 5333; MNA 5336; MNA 6422; MNA 6445; MNA 6488; MNA 6519; MNA 6520; MNA 6713; MNA 6730; MNA 6742; MNA 6872; MNA 7043; MNA 7061. 2011: MNA 7065; MNA 5268; MNA 7067; MNA 7056; MNA 7055; MNA 7054; MNA 7045; MNA 6901; MNA 6898; MNA 6896; MNA 6735; MNA 6727; MNA 7060; MNA 7059; MNA 6909 ; MNA 6899; MNA 6893; MNA 6739; MNA 6738; MNA 7382; MNA 7258; MNA 7254; MNA 7066; MNA 7051; MNA 6921; MNA 6741; MNA 6733; MNA 6736. Rainy season - 2010: MNA 5272; MNA 7024; MNA 7025; MNA 7028; MNA 7030; MNA 7032; MNA 7035; MNA 7036; MNA 7039; MNA 7047; MNA 7048; MNA 7049; MNA 7057; MNA 7062. Revista Brasileira de Ornitologia, 23(4), 2015

Journal

Ornithology Research – Springer Journals

Published: Dec 1, 2015

Keywords: Caatinga; feeding biology; insectivory; stomach contents; temporal variation

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