NOTA

Food habits and carnivory by a small size opossum, Gracilinanus agilis (Didelphimorphia: Didelphidae)

 

Leonardo G. Lessa¹ and Lena Geise²

¹ Universidade Federal dos Vales do Jequitinhonha e Mucuri, Departamento de Ciências Biológicas, Laboratório de Ecologia, CEP 39100-000 Diamantina, Minas Gerais, Brasil [correspondence: <leoglessa@gmail.com>].
² Universidade do Estado do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, Laboratório de Mastozoologia, Rua São Francisco Xavier 524, CEP 20550-011, Rio de Janeiro, Brasil.

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ABSTRACT.

We investigated the diet of gracile mouse opossum, Gracilinanus agilis (Burmeister, 1854), from the analysis of 144 fecal samples collected between November 2009 and October 2011 in an area of savanna riparian forest in the Brazilian Cerrado. Invertebrates were the most frequently consumed food items (96.5%) followed by fruits of pioneer species (29.8%) and flowers (6%). We also observed the presence of fragments of bird vertebrae and downs in samples from 2 adult males, this being the first record of predation on small vertebrates by G. agilis. The presence of fragments of birds in the feces of the gracile mouse opossum suggests that despite the small size of this species and its primarily insectivorous habits, small vertebrates may be included in its diet.

RESUMO.

Registro de carnivoria pelo pequeno marsupial Gracilinanus agilis (Didelphimorphia: Didelphidae).

Investigamos a dieta do marsupial Gracilinanus agilis (Burmeister, 1854) a partir da análise de 144 amostras fecais coletadas entre novembro de 2009 e outubro de 2011 em uma área de mata ciliar savânica no Cerrado brasileiro. Invertebrados constituíram o item alimentar consumido com maior frequência (96.5%) seguido por frutos de espécies pioneiras (29.8%) e flores (6%). Também observamos a presença de fragmentos de vértebras de aves e plúmulas em amostras de dois machos adultos, este é o primeiro registro da predação de vertebrados pelo G. agilis. A presença de fragmentos de aves nas fezes de G. agilis sugerem que, apesar de seu pequeno tamanho e de seu hábito alimentar primariamente insetívoro, vertebrados de pequeno porte, podem ser incluídos em sua dieta.

Key words: Cerrado; Didelphimorphia; Diet; Feeding ecology; Marsupials.

Palavras chave: Cerrado; Didelphimorphia; Dieta; Ecologia alimentar; Marsupiais.

Recibido 9 abril 2014.
Aceptado 19 mayo 2014.
Editor asociado: A Chemisquy

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Gracile mouse opossum, Gracilinanus agilis (Burmeister, 1854), is a small didelphid marsupial with preferably arboreal habits (Paglia et al., 2012) that is occasionally caught on the ground (Eisenberg and Redford, 1999). Adults weigh from 13 to 40 g and males are generally heavier than females (Costa et al., 2003; Paglia et al., 2012). This species has the widest geographic distribution in the genus, occurring in forest formations of Brazilian Cerrado (riparian forests and dry forests), but also in isolated areas in the Caatinga (Costa et al., 2003; Reis et al., 2010; Geise et al., 2010).

Gracilinanus agilis has been regarded as insectivore-omnivore (Paglia et al., 2012) and its natural diet includes primarily a wide variety of insects (Coleoptera, Hymenoptera and Isoptera), but may also include fruits and even flowers (Bocchiglieri et al., 2010; Lessa et al., 2010; Camargo et al., 2011; Lessa et al., 2013). On the other hand, laboratory feeding preference experiments suggest that small didelphids such as G. agilis incorporate into their diet a higher proportion of fruits than indicated by field studies (Astúa de Moraes et al., 2003; Santori et al., 2012). To date, detailed information on the dietary habits of this species is still scarce (Lessa and Geise, 2010; Santori et al., 2012). Didelphids with wide geographic distribution in different biomes or habitats may differ in their diet in response to exogenous factors such as the local variation in resource availability (Ceotto et al., 2009; Lessa and Geise, 2010; Lessa and Geise, 2014). Therefore, it is reasonable to assume that, throughout its wide geographical distribution, G. agilis could present a more varied diet than is currently known. In this study, we report the first record of carnivory by this small didelphid marsupial aiming to extend the existing knowledge on its feeding habits and, consequently, on its ecology.

We conducted the study in an area of savanna riparian forest in Parque Estadual do Rio Preto (PERP: 18°05'20" S; 43°20'25" W), located in the municipality of São Gonçalo do Rio Preto, in the state of Minas Gerais, Brazil. With an area of 12 000 hectares, the PERP is located in the southern portion of the Espinhaço range with a mosaic of vegetation physiognomies, which includes campos rupestres (dry, rocky grasslands), cerrado (stricto sensu), cerradão (woodland savanna) and riparian woodlands along the banks of the Rio Preto River. The climate is type Cwb (mesothermal) according to the Köppen climatic classification, with mild and wet summers (October to March) and dry winters (April to September; Lessa et al., 2013).

Opossums were monthly captured from November 2009 to October 2011, through the capture-mark-recapture method. A total of 96 galvanized wire traps (300 x 160 x 160 mm) arranged in 180 m-long parallel transects separated by 50 m were used. In each transect, 12 capture stations were installed and spaced apart by 15 m. Orange or pineapple pieces, cotton wool soaked in Scotch^® emulsion and bacon bits were used as baits. Captured animals were identified, marked with numbered ear tags (Zootech^®) and released at the same location. Feces were collected directly from each specimen during manipulation or inside the trap. The samples were stored in paper envelopes and preserved at -10°C to avoid fungi infestation. One fecal sample was considered as being all feces produced by a single captured animal in a nighttime period. In laboratory, feces were examined under a stereoscopic microscope and food items were identified to the lowest taxonomic level. We used the relative frequency of occurrence expressed as the number of samples where an item was found (n), divided by the total number of samples and multiplied by 100, in order to determine the contribution of each item in the diet of G. agilis (Korschgen, 1987).

During 9216 trap nights and a capture success of 3.9%, we obtained 144 fecal samples. The diet of G. agilis showed a high frequency of arthropods (mainly Isoptera, Hymenoptera and Blattodea) present in 96.5% of the samples. Fruits were identified in 29.8% of the samples and flowers in 6% of the samples, indicating a diversified diet, but marked by a high frequency of insects throughout the year (Table 1). A predominantly insectivorous diet had been already recorded for G. agilis (Bocchiglieri et al., 2010; Lessa and Costa, 2010) and the same trend was observed for the congener G. microtarsus (Martins and Bonato, 2004). Patterns of prey selection by mammals appear to be related to both consumption preferences and prey availability in the environment (Leiner and Silva, 2007; Pinotti et al., 2011). The high frequency of arthropods in the samples of G. agilis was mainly related to the high consumption of Isoptera and Hymenoptera (Formicidae), abundant resources in the study area (Lessa, 2012) and in the Cerrado biome, even in the driest periods (Pinheiro et al., 2002). Furthermore, the high frequency of litter arthropods in the diet of G. agilis, especially Blattodea, indicates a foraging tendency on the ground, as suggested by Eisenberg and Redford (1999).

Table 1 Food items found in 144 samples o Gracilinanus agilis at Parque Estadual do Rio Preto, Minas Gerais, Brazil.

In the study area, in addition to the high frequency of arthropods in the diet of G. agilis, we also recorded the consumption of small vertebrates (birds) by this small sized marsupial, which was confirmed by the identification of fragments of heterocelic vertebral bodies (characteristic of birds; Hildebrand and Goslow, 2006) and downs in two samples from adult males. Small vertebrates can be preyed alive or consumed as carrion, a distinction hard to make when dealing with fecal content (Ceotto et al., 2009). The consumption of carrion is usually associated with the presence of dipteran pupae in the feces (Santori et al., 1997) and it has been already observed in studies on the diet of larger didelphids such as Philander frenatus, Lutreolina crassicaudata and Didelphis spp. (Santori et al., 1997; Ceotto et al., 2009; Macedo et al., 2010; Facure and Ramos, 2011; Santori et al., 2012). The consumption of carrion by didelphids can be an important source for the attainment of animal protein with a low energy cost (Santori et al., 1997; Macedo et al., 2010). However, we did not record the presence of dipteran pupae in the analyzed samples suggesting the predation, possibly of nestlings, by adult males of G. agilis. A similar pattern, with the consumption of small vertebrates (birds and small mammals) at low frequencies was also observed for other small didelphids such as Marmosops paulensis (Leiner and Silva, 2007) and Micoureus para­guayanus (Pires et al., 2010).

In Brazil, Didelphidae includes at least 56 spe­cies (Rossi et al., 2012); among them, there are many with different degrees of specializations towards carnivory/insectivory (see Vieira and Astúa de Moraes, 2003). Although no species of Neotropical marsupial feeds exclusively on plant matter, the relative importance of animals (vertebrates and invertebrates) in the composition of their diet may vary (Vieira and Astúa de Moraes, 2003). This is the first study to provide evidence of predation on vertebrates (birds) by G. agilis expanding the knowledge on the diet of this small sized didelphid marsupial. The record of birds in the diet shows that, although G. agilis has an opportunistic behavior primarily preying on arthropods, an abundant resource in the Cerrado biome (Pinheiro et al., 2002; Lessa and Costa, 2010), small vertebrates may be included in their diet. Thus, this study included G. agilis as a potential didelphid predator of small vertebrates.

Acknowledgments.

We thank Ricardo T. Santori for the valuable suggestions to the manuscript. The State Forest Institute (Instituto Estadual de Florestas - IEF) for allowing the access to PERP, and Chico Mendes Institute for Biodiversity Conservation (Instituto Chico Mendes de Conservação da Biodiversidade - ICMBIO) for issuing the license to capture the animals (license number 19790-1). Financial support was provided by the Research Support Foundation of the State of Minas Gerais (FAPEMIG: process number APQ 01034-09).

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