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Mammalian Biology Zeitschrift fuÈr SaÈugetierkunde www.elsevier.de/mammbiol Short communication Diet of three didelphid marsupials (Mammalia, Didelphimorphia) in southern Brazil By N. C. CAÂCERES Department of Biosciences, Mato Grosso do Sul Federal University, Brazil Receipt of Ms. 30. 06. 2003 Acceptance of Ms. 18. 03. 2004 Key words: Neotropical marsupials, frugivory, seed dispersal Didelphid marsupials are nocturnal and solitary small mammals. Some species, such as Metachirus nudicaudatus (Desmarest, 1817), are more terrestrial than others, like Philander frenata (Olfers, 1818), which sometimes uses the vertical forest stratum. The weights of these two taxa are comparable averaging 280 to 350 g, but Didelphis aurita Wied-Neuwied, 1826 is averaging 985 g (Fonseca et al. 1996). Despite their wide neotropical distribution, little is known about their diet and role on seed dispersal, mainly for smaller species. In this study, M. nudicaudatus, P. frenata and D. aurita were compared in order to characterize their respective diets and roles in seed dispersal. The three species were trapped systematically in two Atlantic forest sites in southern Brazil, 250 km apart. One site is located in lowland secondary forest at Itapoa (Volta Velha Reserve, 26°05' S 48°40' W); the other is in primary submontane forest at Piraquara in the Serra do Mar (1 000 m a. s. l., 25°28' S and 48°50' W). Average annual temperature and rainfall are higher in the lowland Atlantic Forest area (21 °C, 2 000 mm vs. 17 °C, 1 400 mm) (Maack 1981). Two 2.5 ha-grids of 40 traps ( 40 ´ 20 ´ 20 cm) each were used to capture marsu1616-5047/04/69/06-430 $ 30.00/0. pials in each study area. Single traps were set at 8 stations along 5 parallel lines, with 30 m spacing between trap stations and lines, and trapping took place on four consecutive nights monthly from October 1997 to September 1998. Traps were baited with banana and codfish liver oil. Each animal was aged (following Tyndale-Biscoe and Mackenzie 1976) and marked by punching a unique pattern of holes in the ears before releasing them. Diet was determined by investigation of faeces (collected from traps) washed over a 1 mm-mesh. Any seed found were placed on moist paper in Petri dishes for germination. The dry mass of litter invertebrate prey was also estimated each month at both study areas by drying all individuals in a 57 °C oven for 3 days after removal from 7 pit traps (10 cm in diameter) on each grid. Trap success and species composition were different between the two sites, as I captured only D. aurita (3 individuals on 5 occasions) and M. nudicaudatus (14 individuals, 44 total captures) at Itapoa and D. aurita (1 individual, captured one time but evidenced only through hair and faeces left in the trap) and P. frenata (9 individuals, 14 captures) at Piraquara. Mamm. biol. 69 (2004) 6 ´ 430±433 Diet of three didelphid marsupials (Mammalia, Didelphimorphia) in southern Brazil The diet of all three species and at both sites consisted primarily of invertebrates (Tab. 1). Invertebrates of the leaf litter were readily available for opossums during certain months (January in the lowland, and December and March in the submontane area) of the rainy season. The diet of P. frenata included much more vertebrate prey than that of M. nudicaudatus, which was preponderantly insectivorous. Despite the small sample size, D. aurita was more frugivorous than the other two species (Tab. 1), with many more seeds in faeces (350 vs. 76 and 2086, respectively). 431 The main invertebrate prey consumed by all three species of opossums were Opiliones, Coleoptera and Diplopoda (in order of importance), but also predominantly Pulmonata for P. frenata. Birds were the most common vertebrates consumed, particularly for P. frenata (Tab. 1). Seeds ingested ranged from ~ 1 to 6 mm in length. Larger seed quantities were seen for D. aurita (Philodendron cf. imbe: n = 2 042 seeds) and for P. frenata (Monstera adansonii: n = 296 seeds). Germination occurred at moderate to high frequencies (Tab. 1). Juvenile individuals belonging to age classes 2 (M. nudi- Table 1. Frequencies of occurrence (in %) of food items found in faeces of didelphid marsupials from two Atlantic forest sites of southern Brazil, and respective germination of seeds found in scats. Seed germination in % is in parenthesis. N is the total number of seeds placed for germination. Food items Metachirus nudicaudatus (44 faeces) Fruits Araceae Anthurium sp. Monstera adansonii Schott Philodendron cf. imbe Schott Bromeliaceae cf. Nidularium Cecropiaceae Coussapoa microcarpa (Sch.) Rizz Moraceae Ficus luschnatiana (Miq.) Miq. Solanaceae Solanum swartzianum Roem. and Schult. Non-identified 7 Vertebrates Aves Mammalia Reptilia Invertebrates Decapoda Blattariae Coleoptera Hymenoptera (ants) Lepidoptera (larvae) Orthoptera Diplopoda Opiliones Pulmonata Philander frenata (14 faeces) 29 Didelphis aurita (6 faeces) N 83 2 (88) ± 2 (29) ± 7 (97) ± ± ± 50 (58) 2 (77) ± ± ± ± 7 (100) ± ± ± 7 9 5 2 2 57 36 21 14 33 33 17 ± 100 14 23 68 39 7 23 50 64 5 100 21 36 57 29 ± 21 36 50 21 100 50 ± 50 17 ± 67 83 67 17 ± 20 (67) ± 20 (67) 20 8 25 14 and 60 22 15 43 03 432 N. C. CAÂCERES caudatus) and 3 (M. nudicaudatus, P. frenata) were confirmed to be fruit eaters (not damaging seed cover and embryos). Coexistence of these three species of opossums might be facilitated by adequate food supplies and food diversity, particularly insects (Fonseca and Kierulff 1989) as well as habitat selection and body size relationships (Leite et al. 1996). In particular, P. frenata is omnivorous but frequently consumes vertebrate prey (Santori et al. 1997). Its major consumption of Pulmonata can be related to a preference for stream-side habitats (Charles-Dominique 1983). On the other hand, M. nudicaudatus is highly insectivorous but only occasionally consumes vertebrates or fruits (Santori et al. 1995). However, D. aurita has been reported to be frugivorous-omnivorous (e. g. Fonseca et al. 1996; Leite et al. 1996), which is supported by data presented here. The similarly sized marsupials, M. nudicaudatus and P. frenata, are never found at similar population levels in a given locality of the Atlantic forest (Cerqueira et al. 1993; Bergallo 1994), reflecting different adaptabilities. Insects are more abundant during the wet season in neotropical rainforests (e. g. Bergallo and Magnusson 1999), as was seen here. Insects are also important in the diet of young opossums (CaÂceres 2002; Santori et al. 1997). Importantly, there appears to be a close relation between insect availability and seasonal reproduction of opossums (Julien-LaferrieÁre and Atramentowicz 1990). Based on the frequency, amount, and viability of seeds found in faecal samples, each of the 3 species of marsupials studied can be classified as occasional seed dispersers (P. frenata and M. nudicaudatus) and potential seed dispersers (D. aurita; e. g., CaÂceres et al. 1999). Consumption of fruits by juvenile didelphid marsupials is also important to forest succession, particularly since the occurrence of juveniles is seasonal (Cerqueira et al. 1993; CaÂceres 2002) and correlated with the time of appearance of fleshy fruits in many neotropical forests (e. g., Smithe 1970; Julien-LaferrieÁre and Atramentowicz 1990; CaÂceres et al. 1999). Acknowledgements The author thanks J. Quadros for hair identification, A. M. Brito-Filho, C. C. Baskin and J. L. Patton for help with the English translation, S. M. Silva for help with seed identifications, and E. L. A. Monteiro-Filho, H. G. Bergallo and J. L. Patton for help in improving drafts of the manuscript. CAPES/MEC/Brazil provided a fellowship and CPG-Zoo/UFPR supported this study. References Bergallo, H. G. (1994): Ecology of a small mammal community in an Atlantic Forest area in southeastern Brazil. Stud. Neotrop. Fauna and Environm. 29, 197±217. Bergallo, H. G.; Magnusson, W. E. (1999): Effects of climate and food availability on four rodent species in southeastern Brazil. J. Mammalogy 80, 472±486. CaÂceres, N. C. (2002): Food habits and seed dispersal by the white-eared opossum, Didelphis albiventris, in southern Brazil. Stud. Neotrop. Fauna and Environm. 37, 97±104. CaÂceres, N. C.; Dittrich, V. A. O.; MonteiroFilho, E. L. A. (1999): Fruit consumption, distance of seed dispersal and germination of solanaceous plants ingested by the common opossum (Didelphis aurita) in southern Brazil. Rev. Ecol. Terre Vie 54, 225±234. Cerqueira, R.; Gentile, R.; Fernandez, F. A. S.; D'andrea, P. S. (1993): A five-year population study of an assemblage of small mammals in southeastern Brazil. Mammalia 57, 507±517. Charles-Dominique, P. (1983): Ecology and social adaptations in didelphid marsupials: comparison with eutherians of similar ecology. In: Advances in the Study of Mammalian Behavior. Ed. by J. F. Eisenberg and D. G. Kleiman. Shippensburg: Spec. Publ. American Soc. Mammalogist. Vol. 7, 395±422. Fonseca, G. A. B.; Kierulff, M. C. M. (1989): Biology and natural history of Brazilian Atlantic forest mammals. Bull. Florida Stat. Mus. Biol. Sci. 34, 99±152. Fonseca, G. A. B.; Herrmann, G.; Leite, Y. L. R.; Mittermeier R. A.; Rylands, A. B.; Patton, J. L. (1996): Lista anotada dos mamõÂferos do Brasil. Occas. Pap. Conserv. Biol. 4, 1±38. Julien-LaferrieÁre, D.; Atramentowicz, M. (1990): Feeding and reproduction of three didelphid marsupials in two neotropical forests (French Guiana). Biotropica 22, 404±415. Diet of three didelphid marsupials (Mammalia, Didelphimorphia) in southern Brazil Leite, Y. L. R.; Stallings, J. R.; Costa, L. P. (1996): Diet and vertical space use of three sympatric opossums in a Brazilian Atlantic forest reserve. J. Trop. Ecol. 12, 435±440. Maack, R. (1981): Geografia fõÂsica do Estado do ParanaÂ. Rio de Janeiro: J. Olympio. Santori, R. T.; AstuÂa De Moraes, D.; Cerqueira, R. (1995): Diet composition of Metachirus nudicaudatus and Didelphis aurita (Marsupialia, Didelphoidea) in Southeastern Brazil. Mammalia 59, 511±516. Santori, R. T.; AstuÂa de Moraes, D.; Grelle, C. E. V.; Cerqueira, R. (1997): Natural diet at a restinga forest and laboratory food preferences of the opossum Philander frenata in 433 Brazil. Stud. Neotrop. Fauna and Environm. 32, 12±16. Smithe, N. (1970): Relationships between fruiting seasons and seed dispersal methods in a neotropical forest. Am. Nat. 104, 25±35. Tyndale-Biscoe, C. H.; Mackenzie, R. B. (1976): Reproduction in Didelphis marsupialis and D. albiventris in Colombia. J. Mammalogy 57, 249±265. Author's address: Nilton C. CaÂceres, Departamento de BiocieÃncias, Cx.P. 051, Universidade Federal do Mato Grosso do Sul, Aquidauana, MS, 79.200-000, Brazil (e-mail: [email protected])