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1 December 2012 Notes on Food Habits of Armadillos (Cingulata, Dasypodidae) and Anteaters (Pilosa, Myrmecophagidae) at Serra Da Capivara National Park (PiauÍ State, Brazil)
Vanderson Corrêa Vaz, Ricardo Tadeu Santori, Ana Maria Jansen, Ana Cláudia Delciellos, Paulo Sérgio D'Andrea
Author Affiliations +
Abstract

This is one of the few studies on food habits of armadillos and anteaters in the Caatinga, Brazil. Our aim was to describe food items found in fecal and stomach samples of six species (Dasypus novemcinctus, D. septemcinctus, Euphractus sexcinctus, Myrmecophaga tridactyla, Tamandua tetradactyla, Tolypeutes tricinctus) at the Serra da Capivara National Park, Piauí State, Brazil. For most species, invertebrates — especially Isoptera and Hymenoptera — were the main food source. Seeds were found in samples of most species studied, including M. tridactyla and T. tetradactyla.

The orders Cingulata and Pilosa include 31 species in 14 genera and five families (Wilson & Reeder, 2005). These orders are distributed from the southern United States of America to the southernmost tip of Argentina (Gardner, 2008). Most species occur in South America, five in Central America and only one whose distribution extends to North America (Wetzel, 1982; Eisenberg & Redford, 1999; Gardner, 2008). The large overlap in the range of these taxa is possible due to the great diversity of habits, ranging from fossorial to arboreal species and from carnivorous-omnivorous to insectivorous food habits (Redford, 1985a). Also, they are able to occupy a wide range of habitats, from dryland to tropical rainforest (Wetzel, 1982; Bonato et al., 2008). Data on the biology and ecology of these taxa, mostly on their foods habits, are yet scarce (McDonough & Loughry, 2008). Furthermore, studies on the diet of species are essential to understanding their ecological role in the ecosystem and their geographic distribution (McDonough & Loughry, 2008).

Acording to Redford (1985a), armadillos can be divided into four groups following food habits of the species: I) the carnivore-omnivores, including the genera Zaedyus, Euphractus, and Chaetophractus; II) the generalist fossorial insectivores, represented by the genera Chlamyphorus and Calyptophractus; III) the terrestrial generalist insectivores, mainly the species of Dasypus; and IV) the specialist insectivores (specialized in ants and termites), which include the genera Cabassous, Tolypeutes, and Priodontes. Food preference of armadillos is for termites and ants, but when these items are scarce, armadillos are able to feed on some other arthropods, or even fruits, tubers and small vertebrates, depending on their availability (Greegor, 1985; Redford, 1985a, b; Wirtz et al., 1985; Smith & Redford, 1990; Bolkovic et al., 1995; Anacleto & Marinho-Filho, 2001; Anacleto, 2007).

Anteaters were described as the only truly myrmecophagous Xenarthra species and, according to Montgomery (1985a, b), the main difference among the four extant species is the ratio of ingested ants to termites. His studies suggest Cyclopes is strictly arboreal and feeds exclusively on ants. Furthermore, he observed that Tamandua has terrestrial and arboreal habits and feeds on termites and ants. The ratio of ants to termites in its diet varies according to prey availability. Recently, the consumption of fruits in wild Tamandua mexicana was described by Brown (2011). The terrestrial Myrmecophaga feeds mainly on ants, but does not exclude termites from its diet while actively searching for its preferred food item (Montgomery, 1985a; Redford, 1986; Medri et al., 2003).

Located in the Caatinga biome in the semi-arid northeastern Brazilian region, the Serra da Capivara National Park (SCNP) has a high species richness of armadillos and anteaters: Cabassous unicinctus (Linnaeus, 1758), Dasypus novemcinctus Linnaeus, 1758, D. septemcinctus Linnaeus, 1758, Euphractus sexcinctus (Linnaeus, 1758), Tolypeutes tricinctus (Linnaeus, 1758), Myrmecophaga tridactyla Linnaeus, 1758, and Tamandua tetradactyla (Linnaeus, 1758) (Olmos, 1995; Superina & Abba, 2010). Roadkills and hunting are among the principal causes of death of these species in SCNP (Miranda & Alencar, 2007). Our aim in this study was to describe the food habits of armadillos and anteaters through examination of dead specimens found at the SCNP, thereby increasing the knowledge of the ecology of these species at the Caatinga.

The SCNP (08°26′50″ – 08°54′23″S, 42°19′47″ – 42°45′51″W) is located in southeastern Piauí State, Brazil, at the western limit of the semi-arid Caatinga biome. At approximately 130,000 ha in size, it is the largest protected area located in the Caatinga domain. It is also one of the most important archaeological sites in South America (Emperaire, 1989). Annual average precipitation is 645.7 mm (±248.3 mm) (meteorological stations of São Raimundo Nonato and São João do Piauí municipalities), with the rainy period occurring from November to April. Annual average temperature is 28.02 °C (±1.0 °C) (INMET Instituto Nacional de Meteorologia).

The SCNP is situated at the southern limit of the sedimentary basin of the Parnaíba river, and there are no perennial rivers in the area. Water sources are concentrated in the “boqueirões” (moist areas). The flora of the SCNP is characterized by physiological and morphological adaptations to the xeric conditions typical of deciduous dry vegetation. In one of the few existing studies on the flora of the SCNP, 210 species were recorded (Lemos, 2004). The families Caesalpiniaceae, Fabaceae, Mimosaceae, Bignoniaceae, Euphorbiaceae, and Myrtaceae made up 46% of the recorded species (Lemos, 2004).

Carcasses of armadillos and anteaters were obtained from roadkills and poached animals confiscated in SCNP by rangers of the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), between March 1998 and March 2001. We collected data from carcasses of D. novemcinctus (N = 14), D. septemcinctus (N = 2), E. sexcinctus (N = 3), T. tricinctus (N = 3), M. tridactyla (N = 1), and T. tetradactyla (N = 8). Carcasses were kept frozen at -20 °C until analysis.

From the available carcasses, we analyzed sixteen fecal and six stomach samples of armadillos, and four stomach contents and five feces of anteaters (TABLE 1). Stomach contents and feces were kept in bottles with water to dissolve the material and prevent their contamination by fungi. Samples were washed under running tap water through a sieve with mesh screen of 1.0 mm2. The material retained on the sieve was placed in a glass container filled with a solution of water and detergent, to separate soil particles from plant and animal material. Afterwards, the contents were air dried and analyzed under a binocular magnifying glass (ZEISS Stemi SV6). Observed items were grouped into the following categories: vertebrates (scales, hairs, and bones), invertebrates (exoskeleton), fruits (seeds), soil, and not identified (NJ.). Food items were identified at family level when possible.

Considering all species in each family, a total of 14 types of food items were identified in the fecal samples of armadillos, while in stomach samples the number of food items identified was ten. For anteaters, the number of food items identified was six and three in fecal and stomach samples, respectively (TABLE 1).

Beetles and ants were found in all stomach and fecal samples of all armadillo species. Vertebrates (lizards) were found in samples of D. novemcinctus and E. sexcinctus. Remains of lizards of Sincidae and Tropiduridae families were found in samples of E. sexcinctus. Fruits were found in samples of these two species and also in D. septemcinctus samples. Plant parts (leaves and kindling wood) were present in 68% of the total samples (N = 22) for Dasypodidae and 86% contained soil particles (TABLE 1). Arachnids, Millipedes and seeds of Vitaceae were observed only in stomach contents, while seeds of Asteraceae and Cyperaceae, and insects of the order Dermaptera, occurred only in fecal samples of armadillos.

Ants and termites were the most frequent food items in stomach and fecal samples of anteaters. Beetles were found only in the fecal samples of T. tetradactyla. Among seeds, the Poaceae was the only family occurring in both types of samples, while seeds of Cyperaceae and Euphorbiaceae were found only in fecal contents. Although we have collected only one fecal sample for M. tridactyla, this sample contained more different types of seeds than those of T. tetradactyla. Unidentified plant parts were present in 55% of nine samples, and soil in 44% (TABLE 1).

This is one of the few studies on food habits of armadillos and anteaters of the Caatinga, contributing to the understanding of the biology and current status of this group in its northeastern distribution in Brazil. Our results corroborate the findings of previous studies in which armadillos in general were characterized as opportunistic feeders, while anteaters, as expected by their specialized morphology, behave as specialist insectivores (Redford, 1986). However, apart from insects, we also found seeds of Poaceae, Cyperaceae, and Euphorbiaceae in the samples from anteaters.

TABLE 1.

Number of samples containing food items found in fecal and stomach contents of armadillos and anteaters studied at Serra da Capivara National Park, Piauí State, Brazil. Fee = fecal content; N.I. = not identified; Sto = stomach content.

t01_84.gif

Among the recorded food items, invertebrates especially ants, termites, and beetles — were the main food source. Previous studies suggested that these arthropods provide water, fat, and nitrogen sources for the myrmecophagous species (Redford & Dorea, 1984; Redford, 1987). Moreover, this type of prey is an advantage in tropical regions due to its constant availability and the ease with which it can be found (Pulliam, 1974; Montgomery, 1985b).

Seeds were found in samples of most studied species, except for T. tricinctus. A greater richness of seeds was recorded for D. novemcinctus (TABLE 1). The fruit consumption by armadillos is better described in the literature for E. sexcinctus, which feeds on native and also on cultivated species (Dalponte & Tavares-Filho, 2004) and is considered a seed disperser of imbuzeiro (Spondias tuberosa) in an area of Caatinga (Cavalcanti et al., 2009). For anteaters, there are some previous records of fruit eating in the wild only for Tamandua mexicana (Brown, 2011). Brown (2011) suggested that fruit consumption by anteaters may be common, although its mouth morphology can make the ingestion of seeds difficult, causing the rarity of this food item in its feces. Apparently, this is the first record of seeds in fecal samples of M. tridactyla, the diet of which was often described as based mainly on ants and termites (Medri et al., 2003; Braga, 2010), and in fecal and stomach samples of T. tetradactyla. Although these records may be considered an indication of fruit consumption by these species, it cannot be determined whether the ingestion of seeds was on purpose, by fruit consumption, or incidentally while feeding on insects.

Dasypus novemcinctus and E. sexcinctus were the only studied species that had ingested vertebrates. Lizards as a food item of these species may be associated with their great availability and /or the ease of capture of these animals in the study area, or even with the habit of feeding on carrion, as described by Redford (1985a). Vertebrate predation is well described in the literature mainly for the armadillos of the genera Dasypus, Chaetophractus, Euphractus, and Zaedyus (Barreto et al., 1985; Greegor, 1985; Wirtz et al., 1985; Redford, 1986; Dalponte & Tavares-Filho, 2004; Anacleto, 2007; Soibelzon et al., 2007; Superina et al., 2009; Abba et al., 2011a, b). The ingestion of soil and plant parts may be accidental, associated with the foraging behavior of the species, or intentional, for nutritional purposes (Bolkovic et al., 1995). Their ingestion may occur for distinct reasons: i) use of these items to facilitate digestion of prey; ii) as defense mechanism against the release of chemical substances by the prey, acting as absorbent material; or iii) as nutritional complements (Redford & Dorea, 1984; Montgomery, 1985b; Wirtz et al., 1985; Beyer et al., 1994; Bolkovic et al., 1995).

The total of different food items registered in this study, particularly for armadillos, was lower than the previously recorded by other authors in others biomes, mainly in the Cerrado (Bolkovic et al., 1995; Dalponte & Tavares-Filho, 2004; Anacleto, 2007). However, we recorded new food items for M. tridactyla: seeds of three different plant families. The present study also reveals the importance of analyzing stomach and fecal samples together, providing complementary data in investigations on food habits, because some items were only recorded in feces and others only in stomach contents. The difference in the items recorded in the two sample types may be caused by variations in digestibility or mechanical resistance of the item, time of passage through the digestive tract or order of ingestion of each item (Kunz & Whitaker, 1983; Dickman & Huang, 1988; Kronfeld & Dayan, 1998). Besides contributing to the knowledge on the ecology of these species in the Caatinga, this work is one of the few existing studies on the feeding habits of D. septemcinctus and T. tricinctus (Silva, 2006). Despite the fact that their food habits are mainly insectivorous, the species studied, mainly armadillos, may play a role in seed dispersion at SCNP, zoochory being considered the main form of seed dispersion in the Caatinga (Griz & Machado, 2001).

ACKNOWLEDGEMENTS

Thanks to the staff of the Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, and specially to Dr. João Alves de Oliveira, Dr. Ulisses Caramashi, MSc. Ricardo Loyola de Moura, BSc. Stella Franco and Carlos Augusto Caetano (Museu Nacional-Universidade Federal do Rio de Janeiro); Dra. Laure Emperaire (Institut de Recherche pour le Développement); and MSc. Danielle da Silva Fernandes (Jardim Botânico do Rio de Janeiro). BSc. Aline Tavares Siciliano (Universidade Federal do Estado do Rio de Janeiro) for the identification of food items. Rosemery Lodi (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) and the staff of Fundação Museu do Homen Americano for the assistance during this work. Dr. Claudio Bidau, Dra. Vera Bongertz (Instituto Oswaldo Cruz / Fundação Oswaldo Cruz) and two anonymous reviewers for insightful comments and English revision. Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) provided financial support to the authors.

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Vanderson Corrêa Vaz, Ricardo Tadeu Santori, Ana Maria Jansen, Ana Cláudia Delciellos, and Paulo Sérgio D'Andrea "Notes on Food Habits of Armadillos (Cingulata, Dasypodidae) and Anteaters (Pilosa, Myrmecophagidae) at Serra Da Capivara National Park (PiauÍ State, Brazil)," Edentata 13(1), 84-89, (1 December 2012). https://doi.org/10.5537/020.013.0107
Received: 17 September 2012; Accepted: 4 December 2012; Published: 1 December 2012
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KEYWORDS
Caatinga
comportamento alimentar
diet
Dieta
feeding behavior
xenarthrans
xenartros
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