Mastozoología Neotropical ISSN: 0327-9383 ISSN: 1666-0536 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

de Carvalho, Rone F.; Passos, Daniel C.; Lessa, Leonardo G. DIET VARIATIONS IN SHORT-TAILED Monodelphis domestica (DIDELPHIMORPHIA, DIDELPHIDAE) DUE TO SEASONAL AND INTERSEXUAL FACTORS Mastozoología Neotropical, vol. 26, núm. 2, 2019, Julio-, pp. 340-348 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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DIET VARIATIONS IN SHORT-TAILED OPOSSUM Monodelphis domestica (DIDELPHIMORPHIA, DIDELPHIDAE) DUE TO SEASONAL AND INTERSEXUAL FACTORS Rone F. de Carvalho1, Daniel C. Passos3 and Leonardo G. Lessa1,2

1Universidade Federal dos Vales do Jequitinhonha e Mucuri, Departamento de Ciências Biológicas, Laboratório de Ecologia. Diamantina, MG, Brasil. 2Universidade Federal dos Vales do Jequitinhonha e Mucuri, Programa de Pós-graduação em Biologia , Laboratório de Ecologia. Diamantina, MG, Brasil. [Correspondence: Leonardo G. Lessa ] 3Universidade Federal Rural do Semi-Árido, Programa de Pós-graduação em Ecologia e Conservação, Laboratório de Ecologia e Comportamento Animal. Mossoró, RN, Brasil.

ABSTRACT. We analyzed the diet composition of Monodelphis domestica (Wagner, 1842) distributed in a high-altitude rocky habitat (campo rupestre) in Southeastern Brazil, between October 2015 and December 2016. We also evaluated whether there are diet dierences depending on body mass, sex and seasons. We collected 70 fecal samples of 29 M. domestica specimens and recorded ve food categories (arthropods, vertebrates, seeds, owers and plant vegetative parts). Monodelphis domestica presented a specialized diet, the specimens mainly fed on invertebrates (founded in 100% of the samples). The samples also presented plant vegetative parts (leaves and stems), owers and small vertebrates (scales and fragmented bones of lizards, snakes and birds). The species showed seasonal diet variations and consumed large portions of arthropods, small portions of vertebrates and plant vegetative parts during the rainy season. Intersexual dierences inuenced the diet composition: the range of food items consumed by males was wider than that ate by females. Our ndings helped better understanding the food ecology of short-tailed , besides being the rst study about the diet of a didelphid species distributed in high-altitude rocky habitats.

RESUMO. Variações na dieta da cuíca-de-rabo-curto Monodelphis domestica (Didelphimorphia, Didelphidae) devido a fatores sazonais e intersexuais. Analisamos a composição da dieta de Monodelphis domestica (Wagner, 1842) em uma área de campos rupestres no sudeste brasileiro, entre outubro de 2015 e dezembro de 2016. Também avaliamos se existem diferenças na dieta de acordo com a massa corporal, sexos e estações do ano. Obtivemos 70 amostras fecais de 29 indivíduos e 5 categorias de itens alimentares foram identicadas (artrópodes, vertebrados, sementes, ores e partes vegetativas de plantas). Monodelphis domestica apresentou uma dieta especializada consumindo principalmente artrópodes (registrados em 100% das amostras). As amostras também apresentaram partes vegetativas (folhas e caules), ores e pequenos vertebrados (escamas e ossos fragmentados de lagartos, serpentes e aves). A espécie mostrou variação sazonal na dieta, consumindo uma alta proporção de artrópodes, pequenos vertebrados, e partes vegetativas de plantas durante os meses chuvosos. Houve também diferença intersexual na composição da dieta, com machos consumindo um espectro mais amplo de itens do que as fêmeas. Nossos resultados contribuem para a compreensão da ecologia alimentar

Recibido 14 junio 2018. Aceptado 7 enero 2019. Editor asociado: D. Astúa DIET OF Monodelphis domestica 341

das cuícas-de-cauda-curta, e representa o primeiro estudo especíco sobre a dieta de dideldeos em campos rupestres.

Key words: Campos rupestres, food habit, insectivorous, .

Palabras-chaves: Campos rupestres, hábito alimentar, insetívoros, marsupiais.

INTRODUCTION to mates searching, whereas females have a large energetic demand because they are pregnant or Trophic ecology is one of the outstanding features lactating (Martins et al. 2006; Camargo et al. 2014; of several organisms, including marsupials’ biology, Melo et al. 2018). and it has major implications in the understanding of their natural history and on the functional role In addition, seasonal environments, such as the played by these (Castilheiro & Dos Santos Cerrado (a savanna-like ecosystem), can also inu- Filho 2013; Camargo et al. 2014). Several didelphid ence the species diet because the food availability species participate in mutualistic relationships in the (specially insects and fruits) can change during the Neotropics, since they feed on and disperse intact year (Martins et al. 2006; Camargo et al. 2014; Lessa seeds of a wide variety of eshy fruits (Cáceres 2002; & Geise 2014a). Therefore, some didelphid species Lessa et al. 2013). Furthermore, evidences suggest can adapt their diet in order to consume resources that didelphids’ feeding habits can change depend- according to their availability in the environment ing on age, sex, reproductive activity and season (Lessa & Geise 2014a; Melo et al. 2018). (Martins et al. 2006; Casella & Cáceres 2006; Santori Monodelphis domestica, and Monodelphis species et al. 2012; Lessa & Geise 2014a). Nevertheless, the more generally, have traditionally been treated as in- knowledge about the diet and food strategies of most sectivores (Paglia et al. 2012), although information species belonging to the genus Monodelphis remains about its food habits also reports the consumption of poor: only 29% of the 60 Brazilian didelphid marsu- small vertebrates (rodents, lizards, frogs and snakes), pials had their diets investigated¬ in specic studies fruits and carrion (Streilein 1982; Emmons & Feer (Lessa & Geise 2010; Santori et al. 2012). 1997; Hume 1999; Neto & Dos Santos 2012). However, Short-tailed opossum (genus Monodelphis Burnett most detailed information about the diet of this 1830, Didelphidae) is the most speciose genus of species was reported by cafeteria experiments, in didelphid marsupials; it has 22 currently recog- which M. domestica individuals were fed in captivity nized species (Pavan & Voss 2016). Monodelphis (Daniels et al. 2005; Constantino 2015). Recent domestica (Wagner, 1842) is a terrestrial, diurnal studies on the diet of Monodelphis spp., based on and crepuscular didelphid and its representatives fecal analysis and on stomach contents, showed have the widest geographic distribution in the genus that insects were the most frequently consumed (Streilein 1982; Emmons & Feer 1997; Smith 2008). resource (Casella & Cáceres 2006; Pinotti et al. 2011; They are found in open dry and high-altitude rocky Castilheiro & Dos Santos Filho 2013). These ndings habitats (campos rupestres) in Central, Northeastern suggest that M. domestica may also be primarily and Eastern Brazil, mainly in seasonal savanna-like insectivorous, although the available data are very biomes (Cerrado and Caatinga) (Macrini 2004; Melo limited. So far, we found no systematized and de- & Sponchiado 2012). tailed studies about the composition of M. domestica Monodelphis domestica shows sexual size dimor- natural diet. phism with males being larger than adult females This article reports the feeding habits of (mean body mass 71.4 g; range, 55 - 95 g) (Eisenberg M. domestica specimens living in a seasonal high- & Redford 1999; Macrini 2004), this dierence in altitude rocky habitat in southeastern Brazil. The size can result in dierent energetic demands, inu- aims of our study were to describe the species encing the diet composition (Camargo et al. 2014; natural diet in the assessed area and to evaluate Melo et al. 2018). Like other Neotropical marsupials, whether there are diet changes due to individual M. domestica also shows a seasonal pattern of repro- body mass, sex (male vs. female) and sampling time duction occurring in the beginning of the warm-wet (dry vs. rainy season). We expect the following: season (Bergallo & Cerqueira 1994; Macrini 2004). (1) That M. domestica feeds more intensively on in- During this period, males feed more intensively on sects (mainly termites, ants and beetles) compared to insects because of higher energy demands related fruits (see Casella & Cáceres 2006; Castilheiro & Dos 342 Mastozoología Neotropical, 26(2):340-348 Mendoza, 2019 R. F. de Carvalho et al. hp://www.sarem.org.ar – hp://www.sbmz.org

Santos Filho 2013); (2) that vertebrate consumption The collected material was washed in metal mesh would be positively inuenced by M. domestica body sieve (0.1 mm), separated and identied through stereomi- size. Body size could be more associated with preda- croscopy in laboratory. Items were identied at the lowest taxonomic level possible and separated into 5 categories: tion among didelphids than could be explained just i) seeds, ii) owers, iii) vegetative parts (leaves or stems), by chance (see Santori et al. 1997; Macedo et al. 2010); iv) arthropods, and v) vertebrates. The consumption fre- (3) there are seasonal variations in the pattern of food quency of each food category (expressed in percentage) was consumption by M. domestica related to sex. The based on the number of samples presenting the category sexual dimorphism in size, associated with dierent in question. Each fecal sample encompassed all feces produced by a single animal overnight. energetic demands over the year, may exert inuence Invertebrates in the samples were identied according on food consumption by M. domestica, reected in to the specialized literature (Triplehorn & Johnson 2011; dierential diets for males and females (as suggested Constantino 2012; 2015) and through the comparison to an by other studies with small Neotropical didelphids arthropod collection and to seeds collected in the same study site. Lizard and snake scales found in the feces in seasonal environments, see Martins et al. 2006; samples were morphologically (number and position of Camargo et al. 2014; Melo et al. 2018). mucros and sensorial holes) and morphometrically (total length, total width, mucro length and mucro-base width) MATERIALS AND METHODS evaluated. Next, they were compared to voucher specimens deposited in a scientic collection (Coleção Herpetológica Study site do Semiárido – CHSA) and to information available in the literature (Rodrigues 1986; Franco & Ferreira 2002; Franco We conducted the study in a high-altitude rocky habi- et al. 2017). We asked specialists to identify Isoptera and tat (campo rupestre) (18°14’S; 43°36’W; 1 387 m altitude) Hymenoptera fragments (Thiago Santos, Federal University in the northern portion of Espinhaço mountain range, of Vale do Jequitinhonha and Mucuri - UFVJM). Diamantina County, Minas Gerais State, Brazil. Campos The project was approved by the Committee on rupestres are ecotonal highland habitats, located between Ethics in the Use of Animals - CEUA\UFVJM (protocol the Cerrado and Atlantic Forest domains. These rocky n. 12\2016) and by Chico Mendes Institute for Biodiversity formations are inuenced by a whole diversity of factors, Conservation (Instituto Chico Mendes de Conservação da including water availability, sun exposure, topography, as Biodiversidade - ICMBIO), which issued permission to well as the type of soil. (Giulietti & Pirani 1988). capture and handle opossums (license n. 52836-1). The Based on Köppen classication, the climate in the site trapping and handling procedures complied to the guide- is of the Cwb type (mesothermal): mild and wet summers lines sanctioned by the American Society of Mammalogists (October to March) and dry and cold winters (April to (Sikes 2016). September) (Neves et al. 2005). However, rainfall rates throughout the sampling period did not match the expected Statistical analyses standard for the study site; thus, we adopted the accumu- lated rainfall and evapotranspiration values (recorded dur- We used the Relative Frequency of Occurrence (FO), ex- ing the sampling months) as the criterion to dene the dry pressed as the number of samples where an item was found and rainy periods. We took into account the months when (n) divided by the total number of samples and multiplied rainfall rates were higher than the evapotranspiration ones by 100, to determine the contribution of each item in the (November and December- 2015 and January, February, diet of M. domestica (Korschgen 1987). March, October, November and December – 2016) as rainy We used the Levins’s standardized index (Krebs 1998) periods. Dry months were those when rainfall rates were to calculate dietary niche breadth. This index ranges from lower than the evapotranspiration ones (October - 2015 0 to 1: lower values indicate diets dominated by few prey and April, May, June, July, August and September - 2016). items (specialist predators) and the higher ones appoint Rainfall rates are available in the National Institute of out more generalist diets (Hurlbert 1978). Meteorology – INMET (http://www.inmet.gov.br), data were B − 1 BA = collected in an automatic station in Diamantina County, n − 1 MG (Station 83538, Latitude: 18.23, Longitude: 43.64, alti- A tude: 1 296.12 m). Wherein, B = Levins’ standard measure (from 0 to 1); B = Levins’ Niche breadth measurement (estimated through B = 1/ P p2 p j Sampling design and data collection j ; j = proportion of food item in the diet; and n=number of consumed resources. Opossum specimens were captured during ve consecutive We used a Mann-Whitney test to evaluate possible nights in a monthly basis. We used 100 Tomahawk traps dierences in the body mass between individuals who (300 x 160 x 160 mm), which were set on the ground based had consumed or not vertebrate items. We tested the on the capture-mark-recapture method from October 2015 null hypothesis that medians body mass did not dier to December 2016. As bait we used a mixture of banana, between these groups. For these analyses we used the sardine oil, corn meal and oat grains. Captured opossums software BioEstat 5.3 (Ayres et al. 2007). Although the were identied, weighted, marked with numbered ear tags age of captured individuals was not identied through the (Zootech®) and released in the same location. Feces of each tooth eruption sequence (see Quental et al. 2001), median specimen were collected during manipulation procedures weight was the reference to dene the adult specimens, or inside the traps. Samples were stored in paper envelopes since adult females weigh from 80 to 110 g and males from and preserved at -10°C in order to avoid fungi infestation. 80 to 150 g (Fadem & Rayve 1985). DIET OF Monodelphis domestica 343

We used the G-test (Zar 2010) to evaluate possible diet and Tropidurus montanus Rodrigues 1987 and to a dierences between the dry and rainy months and between small snake belonging to genus Thamnody nastes males and females. These analyses were conducted in Wagler 1830. Monodelphis domestica samples also the BioEstat 5.3 software (Ayres et al. 2007). We used the Shannon-Wiener index (H’) to calculate food–item presented avian bones and egg fragments, which diversity in samples subjected to each treatment, i.e., dry could not be identied under low taxonomic level and rainy months, and sex (males versus females). The because fragments were broken into small pieces Hutcheson’s t-test (Zar 2010) was used to evaluate the that hampered identication. There was signicant signicance of dierences recorded through the Shannon- dierence between the median body-mass (U = 18.5; Wiener index. It tested the null hypothesis that diet diver- sity did not dier between treatments. These analyses were p = 0.023) of individuals who consumed vertebrates conducted in the PAST software version 2.17 c. Signicance (n = 6, median = 102 g, 5 males and 1 female) and level 5% was adopted for all analyses. Feces samples of that of the ones who did not consume them (n = 17, recaptured specimens were excluded from the analyses in median = 45 g, 8 males, 8 females and 1 individual order to avoid pseudo-replications (Hurlbert 1984). not sexed). Only 23 individuals who had their weight recorded were used in this analysis. RESULTS Diet signicantly changed between climatic peri- The 6,700 trap nights (900 trap nights in 2015 and ods (G = 96.9361; df = 26; p < 0.0001); animals fed 5800 in 2016) resulted in 1.33% capture success. on a wider diversity of food items during the rainy We collected 70 fecal samples of 29 M. domestica months (H’dry = 2.09; H’rainy = 2.32; specimens, 33 samples in the dry months and 37 mboxtextitt = -2.64; df = 651.94; p = 0.0085). Some in the rainy ones. Forty-one (41) samples belonged groups of items were only consumed during the to male specimens (23 collected in the dry months rainy season: Lepidoptera, Odonata, Orthoptera, and 18 in the rainy ones) and 28 belonged to females as well as some seeds such as Miconia sp. (10 collected in the dry months and 18 in the rainy (Melastomataceae) and Solanum buddleiaefolium ones), being one sample excluded because it had no (Solanaceae) (Fig. 1). Vertebrates were more fre- sex identication. Males (n = 12; average weight quent in the samples collected throughout the rainy ± sd = 89.33 ± 35.05 g) were heavier than females season (21.62%) than in samples from the dry months (n = 10; average weight ± sd = 48.70 ± 25.32 g) (6.06%). On the other hand, Asteraceae seeds were (t = -3.06; df = 20; p = 0.0062), being seven samples more frequent (27.27%) in the dry months (Table 1). excluded from this analysis from those individuals The species also showed dierences in the which body mass was not recorded. frequency of food items consumed by each sex Monodelphis domestica specimens presented spe- (G = 119.25; df = 26; p < 0.0001): males had cialized diet (BA= 0.24); they mainly fed on arthro- more diversied diet than females (H’males = 2.34; pods, which was the most frequent food category, H’females = 2.02; t = 3.85; df = 655.14; p = 0.0001). since they were founded in 100% of the collected Food items such as Solanum buddleiaefolium samples (Table 1). Hymenoptera (ants and bees), (Solanaceae), Blattodea, Hemiptera, Lepidoptera, Isoptera (termites belonging to genera Nasutitermes Odonata were consumed only by males, while and Neocapritermes) and Coleoptera (beetles) were Miconia sp. (Melastomataceae) and Orthoptera were the most frequent orders of arthropods. Diplopoda consumed only by females (Table 1). Vertebrates had an intermediate frequency, being followed by were more consumed by males (19.51%) than females Blattodea, Aranae, Hemiptera, Lepidoptera, Odonata (7.14%) (Fig. 2). and Orthoptera, which was recorded lower frequen- The diet of M. domestica also showed dier- cies (Table 1). Seeds from ve plant families were ences in diet composition (FO) between sexes recorded in 31.4% of the samples; among them, in dry (G =155.11; df =15; p < 0.0001) and rainy Asteraceae was the most frequent one (Table 1). The seasons (G =165.41; df = 24; p < 0.0001). Males samples also had plant vegetative parts (leaves and presented a more diverse diet than females stems) recorded in intermediate (22.9%) and ow- during the dry (H’males = 2.05; H’females = 1.82; ers recorded in low frequencies (7.1%), respectively t = 3.20;; p = 0.0015) and during the rainy season (Table 1). (H’males =2.49; H’females = 2.02; t = 6.45; df = 724.76; p < 0.0001). Vertebrates were found in 14% of the sam- ples. They were identied through the presence DISCUSSION of scales, fragmented bones and eggs in the col- lected feces (Table 1). Scales belonged to the lizard In our study, M. domestica specimens presented species Eurolophosaurus nanuzae Rodrigues 1981 a specialized diet feeding mainly on animal mat- 344 Mastozoología Neotropical, 26(2):340-348 Mendoza, 2019 R. F. de Carvalho et al. hp://www.sarem.org.ar – hp://www.sbmz.org

Table 1 Number and Frequency of Occurrence (%) of food items in fecal samples of Monodelphis domestica between October 2015 and December 2016 in a campo rupestre habitat in southeastern Brazil.

Males Females Dry months Rainy months Total Food items (n=41) (n=28) (n=33) (n=37) (n=70) Seeds Asteraceae 7(17.07) 7(25) 9(27.27) 5(13.51) 14(20) Cactaceae Cipocereus minensis 1(2.44) 1(3.57) - 2(5.41) 2(2.86) Melastomataceae Miconia sp. - 1(3.57) 1(3.03) - 1(1.43) Poaceae 4(9.76) 1(3.57) 4(12.12) 1(2.7) 5(7.14) Solanaceae Solanum buddleiaefolium 1(2.44) - - 1(2.7) 1(1.43) Unidentied morfotype 1 1(2.44) - - 1(2.7) 1(1.43) Total seeds 13(31.71) 9(32.14) 12(36.36) 10(27.03) 22(31.43) Flowers Poaceae 1(2.44) 2(7.14) - 3(8.11) 3(4.29) Unidentied owers 2(4.88) 1(3.57) 1(3.03) 2(5.41) 3(4.29) Total owers 2(4.88) 3(10.71) 1(3.03) 4(10.81) 5(7.14) Vegetative plant matter 8(19.51) 8(28.57) 3(9.09) 13(35.14) 16(22.86) Arthropoda Araneae 3(7.32) 4(14.29) 3(9.09) 4(10.81) 7(10) Blattodea 5(12.2) - 2(6.06) 3(8.11) 5(7.14) Coleoptera 14(34.15) 14(50) 9(27.27) 19(51.35) 28(40) Diplopoda 12(29.27) 1(3.57) 6(18.18) 7(18.92) 13(18.57) Hemiptera 2(4.88) - 1(3.03) 1(2.7) 2(2.86) Hymenoptera 37(90.24) 23(82.14) 29(87.88) 32(86.49) 61(87.14) Apoidea 19(46.34) 9(32.14) 18(54.55) 10(27.03) 28(40) Formicidae 35(85.37) 21(75) 28(84.85) 28(75.68) 56(80) Isoptera 29(70.73) 25(89.29) 25(75.76) 30(81.08) 55(78.57) Nasutitermes 18(43.9) 10(35.71) 16(48.48) 12(32.43) 28(40) Neocapritermes 11(26.83) 12(42.86) 12(36.36) 11(29.73) 23(32.86) Silvestretermes - 1(3.57) - 1(2.7) 1(1.43) Lepidoptera 1(2.44) - - 1(2.7) 1(1.43) Odonata 1(2.44) - - 1(2.7) 1(1.43) Orthoptera - 1(3.57) - 1(2.7) 1(1.43) Larvae 4(9.76) 2(7.14) 3(9.09) 3(8.11) 6(8.57) Unidentied Arthropoda 9(21.95) 9(32.14) 5(15.15) 14(37.84) 19(27.14) Total Arthropoda 41(100) 28(100) 33(100) 37(100) 70(100) Vertebrates Birds 2(4.88) - 1(3.03) 1(2.7) 2(2.86) Squamata - Tropiduridae Eurolophosaurus nanuzae 1(2.44) 1(3.57) 1(3.03) 1(2.7) 2(2.86) Tropidurus montanus 1(2.44) - 1(3.03) - 1(1.43) Squamata - Dipsadidae Thamnodynastes sp. - 1(3.57) - 1(2.7) 1(1.43) Unidentied Squamata 3(7.32) - - 3(8.11) 3(4.29) Egg 1(2.44) - - 1(2.7) 1(1.43) Unidentied Vertebrates 1(2.44) - - 1(2.7) 1(1.43) Total vertebrates 8(19.51) 2(7.14) 2(6.06) 8(21.62) 10(14.29) DIET OF Monodelphis domestica 345

Fig. 1. Relative Frequency of Occurrence (RFO) of food items recorded in fecal samples of Monodelphis domestica during the rainy (black bars) and dry seasons (white bars). Asterisks (*) denotes food items consumed in a sole sea- son. Database collected between October 2015 and December 2016 in a campo rupestre habitat in southeastern Brazil. ter, including a wide variety of arthropods (e.g. et al. 2010; Santori et al. 2012), which would be Hymenoptera, Isoptera and Coleoptera), and small expected since young individuals would not be able vertebrates such as lizards (e.g. E. nanuzae, to subdue lizards or snakes bigger than themselves. T. montanus Thamnodynastes ), snakes ( sp.) and Food availability can explain the variations in birds (unidentied). Overall, Neotropical didelphid the diet composition of some didelphids (Cáceres marsupials have been classied as omnivorous and 2002; Lessa & Geise 2010; 2014a; Melo et al. 2018), generalists, since they consume a wide variety of which are mainly opportunistic preferring items food items (Paglia et al. 2012). However, recent that are available over time and accessible in space studies have shown that small-bodied open-habitat (Santori et al. 2012). According to our results, Gracilinanus agilis macrurus species (e.g. , Monodelphis domestica presented seasonal changes M. domestica and ) tend to have more insectivorous in diet, feeding more on arthropods, small verte- and/or carnivorous diets (Camargo et al. 2014; Lessa brates and on plant vegetative parts during the & Geise 2014b; Melo et al. 2018, this study). rainy months. Seasonal shift in diet were found Monodelphis domestica inhabits seasonal savanna- in studies with other primarily insectivorous didel- like biomes (Caatinga and Cerrado) presenting irreg- phid species distributed in savanna-like environ- ular rainfall in arid and semi-arid regions (Eisenberg ments, such as Metachirus nudicaudatus (Lessa & & Redford 1999; Macrini 2004). In this sense, Geise 2014a), Gracilinanus agilis (Camargo et al. M. domestica appears to be ecologically comparable 2014; Lessa & Geise 2010; 2014b), and Thylamys to equivalent insectivorous/carnivorous species from macrurus (Melo et al. 2018). Hymenoptera (ants), Australia’s xeric areas (Morton 1980) in its ability Isoptera (termites) and Coleoptera (beetles) are the to maintain water balance in the production of most common insect orders distributed in Cerrado metabolic water from a high-protein animal-matter (Pinheiro et al. 2002), and these orders were also the diet (Christian 1983). most frequent found in M. domestica fecal samples The presence in the diet of scales that be- throughout the year. This evidence suggests that M. domestica campos rupestres longed to small vertebrates such as the lizards diet of in depends, at (E. nanuzae and T. montanus) as well the snake least partially, on the environmental availability of Thamnodynastes sp., suggest their predation by invertebrate preys. In fact, many other didelphids, larger-bodied M. domestica individuals, probably known by their opportunistic feeding strategies, adults. In this sense, small vertebrates would presented similar behavior (Streilein 1982; Cáceres only be accessible to adult short-tailed opossums, 2002; Albanese et al. 2012; Lessa & Geise 2014a; since according to Streilein (1982), captive and wild Martins et al. 2006; Melo et al. 2018). M. domestica can only capture preys who are almost During reproduction, male usually face similar to their size and their own body mass. Such high energetic costs in searching for a mate, while result corroborates other studies, which reported females usually face high energetic costs during that small vertebrates are more often eaten by adult pregnancy and lactation (Martins et al. 2006). In than younger marsupials (Santori et al. 1997; Macedo M. domestica, males usually are heavier than females 346 Mastozoología Neotropical, 26(2):340-348 Mendoza, 2019 R. F. de Carvalho et al. hp://www.sarem.org.ar – hp://www.sbmz.org

Fig. 2. Relative Frequency of Occurrence (RFO) of food items recorded in fecal samples of Monodelphis domestica males (black bars) and females (white bars). Asterisks (*) means food items consumed by a sole sex. Database collected between October 2015 and December 2016 in a campo rupestre habitat in southeastern Brazil.

(Macrini 2004) and increases home range during the their inuence on energetic demand between males breeding season in order to maximize the chances and females of M. domestica. of nding and obtaining mates and food (Bergallo The herein assessed M. domestica population, & Cerqueira 1994; Smith 2008). In turn, females are which was distributed in Brazilian mountain rocky pregnant/lactating during the wet season (Bergallo grasslands, presented primarily insectivorous/car- & Cerqueira 1994; Cáceres & Graipel 2012), fact nivorous diet. Our results demonstrated that body that increases their energetic demand during this size may inuenced diet composition (larger indi- time. According to Martins et al. (2006), is expected viduals were more likely to eat vertebrates than the that males increased their food consumption at the smaller ones), diet changed throughout the year (it end of the cool-dry season to store reserves to be was more diverse in the rainy season), and feeding used in searching for females and in mating. In habits changed depending on sex (males had more Females of small mammals, higher energetic demand generalist diets than females). This is the rst study are associated with lactation (Thompson 1992 apud addressing the diet of didelphid species living in Martins et al. 2006), so that, females of M. domestica high-altitude rocky habitats, and our ndings con- are expected to have an increased food consumption tribute to a better understanding about the food in the warm-wet season. However, our results do not ecology of free-ranging short-tailed opossums. support this pattern, since the diversity of food items detected in the diet of females was smaller than that ACKNOWLEDGMENTS detected in the diet of males in both seasons. We thank the sta of Laboratory of Conservation Biology (LabEco), Universidade dos Vales do Jequitinhonha e A possible explanation for this dierence in diet Mucuri, for help with the eld work and T. Santos for between males and females could be explained by his assistance on arthropods identication. We are grate- three hypotheses. First, it may be related to dif- ful for scholarship granted by Conselho Nacional de ferences in energy demand over the year due to Desenvolvimento Cientíco e Tecnológico (CNPq) to the rst author. We are also indebted to two anonymous intrinsic reproductive cycle of each sex. Second, reviewers for their comments and suggestions that greatly M. domestica is an opportunistic predator, so the improved the clarity of the manuscript. spatial and temporal availability of food items in the environmental may reect this variation in the diet. LITERATURE CITED Third, as some food items were identied into wide Albanese, S., M. A. Dacar, & R. A. Ojeda. 2012. Unvarying diet of a taxonomic categories (mostly orders or families), it is Neotropical desert inhabiting a variable environment: possible that subtle dierences in diet between sexes the case of Thylamys pallidior. Acta Theriologica 57:185-188. have been masked by the taxonomic categories used. https://doi.org/10.1007/s13364-011-0057-6 Ayres, M., M. Ayres Júnior, D. L. Ayres, A. A. S. Santos. 2007. Although we corroborate our hypothesis that diet BioEstat 5.0: Aplicacões Estatísticas nas áreas das Ciências diers between sexes, an analysis that measure the Biológicas. Belém: Sociedade Civil Mamirauá, MCT-CNPq. availability of food items in the environment at each Bergallo, H. G., & R. Cereira. 1994. Reproduction and growth of Monodelphis domestica in Northeastern Brazil. Journal of season as well as the caloric content of the food Zoology 232:551-563. https://doi.org/10.1111/j.1469-7998.1994. resources consumed, would be needed to conrm tb00003.x DIET OF Monodelphis domestica 347

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