SciELO - Scientific Electronic Library Online

 
vol.17 número1Actualización sobre el estado del apostadero de lobo marino de un pelo sudamericano (Otaria Flavescens) en la Isla Trinidad, estuario de Bahía Blanca, ArgentinaHábitos alimenticios de Heteromys Australis (Rodentia: Heteromyidae) en el norte de la cordillera central de Colombia índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

  • No hay articulos citadosCitado por SciELO

Links relacionados

Compartir


Mastozoología neotropical

versión impresa ISSN 0327-9383versión On-line ISSN 1666-0536

Mastozool. neotrop. v.17 n.1 Mendoza ene./jun. 2010

 

ARTÍCULOS Y NOTAS

Young didelphid consumption by Micoureus paraguayanus (Didelphimorphia: Didelphidae) in southeastern Brazil

Mathias M. Pires1, Eduardo G. Martins2, Leonardo D. Cruz3, Fernanda R. Fernandes1, Rute B. G. Clemente-Carvalho4, Maria Nazareth F. Silva5, and Sérgio F. dos Reis6

1 Programa de pós-graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, Rua Bertrand Russell, s/n, Caixa Postal 6109, CEP 13083-970, Campinas, São Paulo, Brazil [Corresponding author: Mathias M. Pires <mathiasmpires@gmail.com>].
2 Department of Forest Sciences, University of British Columbia, 2424 Main Mall, V6T 1Z4, Vancouver, BC, Canada.
3 Programa de pós-graduação em Zoologia, Instituto de Biociências, Universidade Estadual Paulista, Av. 24-A, 1515, Bela Vista, CEP 13506-900, Rio Claro, São Paulo, Brazil.
4 Programa de pósgraduação em Genética, Instituto de Biologia, Universidade Estadual de Campinas, Rua Charles Darwin, s/n, Caixa Postal 6109, CEP 13083-970, Campinas, São Paulo, Brazil.
5 Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Aleixo, CEP 69060-001, Manaus, Amazonas, Brazil.
6 Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Rua Charles Darwin, s/n, Caixa Postal 6109, CEP 13083-970, São Paulo, Brazil.

ABSTRACT: In a study aiming to describe the diet of Micoureus paraguayanus in a southeastern Brazilian Cerrado (savannah-like) remnant, we found young didelphid remains in fecal samples from live-trapped adults. These findings uncovered either events of scavenging on dead young didelphids or infanticide adding to the knowledge on the dietary breadth and behavioral ecology of M. paraguayanus.

RESUMEN: Consumo de crías de didélfidos por Micoureus paraguayanus (Didelphimorphia: Didelphidae) en el sudeste de Brasil. En un estudio con el objetivo de describir la dieta de Micoureus paraguayanus en un remanente de Cerrado en el sudeste de Brasil, encontramos vestigios de didélfidos jóvenes en muestras de heces de adultos capturados. Estos resultados sugieren el consumo de individuos ya muertos o infanticidio. Nuestros hallazgos añaden un nuevo conocimiento acerca de la dieta y ecología conductual de M. paraguayanus.

Key words. Cannibalism; Cerrado; Didelphid; Infanticide.

Palabras clave. Canibalismo; Cerrado; Didélfidos; Infanticidio.

The family Didelphidae includes 95 species widely distributed throughout the Neotropical region (Gardner, 2007). Dietary studies have revealed a wide variety of food resources consumed by didelphids, such as fruits, nectar, small vertebrates and arthropods (Vieira and Astúa de Moraes, 2003; Carvalho et al., 2005). Fruits and arthropods, for example, are frequent in the diets of Gracilinanus, Micoureus, Metachirus, Marmosa and Caluromys, whereas small vertebrates are frequently consumed by Didelphis, Chironectes, Philander, Monodelphis and Lutreolina (Santori et al., 1997; Cáceres et al., 2002; Vieira and Astúa de Moraes, 2003; Casella and Cáceres, 2006; Ceotto et al., 2009). The frequency and relative proportions with which different food resources are consumed vary widely among didelphid species and have led to their placement along a continuum from frugivory to carnivory (Astúa de Moraes et al., 2003; Vieira and Astúa de Moraes, 2003). The woolly mouse opossum Micoureus paraguayanus Tate, 1931, falls in the middle of this continuum, consuming a wide variety of arthropods such as hymenopterans, coleopterans, and hemipterans, and fruits from different taxa such as Cecropiaceae, Piperaceae and Moraceae (Leite et al., 1996; Carvalho et al., 1999; Cáceres et al., 2002; Casella and Cáceres, 2006). The consumption of birds was also reported for M. paraguayanus, suggesting that vertebrates may play an important role in the diet of some populations (Cáceres et al., 2002; Casella and Cáceres, 2006). Despite the dietary diversity uncovered for M. paraguayanus, the consumption of any mammal species has not been reported so far. In this note we communicate the first record of the consumption of didelphid marsupials by M. paraguayanus. This information is relevant not only because it contributes towards the goal of a more complete specification of the dietary breadth of M. paraguayanus, but also as a way of probing into the behavior of such secretive mammals as didelphids.
Our data was gathered during a study aiming to evaluate the endogenous and exogenous factors influencing the diet of two small marsupials, M. paraguayanus and Gracilinanus microtarsus, which coexist in a south-eastern Brazilian Cerrado (savannah-like) remnant (Reserva Biológica de Mogi Guaçu, São Paulo, 22º 15'/22º 18' S; 47º 08'/47º 13' W). Feces were collected from individuals captured in an 11 x 11 trapping grid with 121 trappingstations located 15 m from each other. We captured 20 adult individuals of which seven were females and 13 were males. This strongly male-biased sampling is expected since there is evidence for male biased dispersion in M. paraguayanus (Pires and Fernandez, 1999). We collected 165 fecal samples (mean number of fecal samples and range: males 5.15, 1-23; females 14.0, 1-41) and analyzed each sample in the laboratory with a stereoscope. Four of those samples contained vertebrate remains. Vertebrate items collected from the feces of M. paraguayanus, were air dried, mounted in metal stubs, coated with gold in a Sputter Coater Balzers SCD050, and examined in a Jeol JSM 5800LV scanning electron microscope (SEM).
None of the males had evidence of vertebrate consumption, whereas the four samples containing vertebrate remains were found in feces from three of the seven captured females. One sample of one female contained a fragmented toothrow and bone fragments not completely ossified, a second sample from another female contained only a fragmented bone, and two samples from a third female contained one vertebrate claw each. The toothrow (Fig. 1) contained only three teeth, a long and curved canine and two premolars differing in size, with P2 being larger than P1; a dental morphology which unambiguously refers to a didelphid upper toothrow (Gardner and Creighton, 2007). Although the claws and the bone found in other fecal samples clearly represent vertebrate consumption events, their morphology is not enough to reliably identify the species consumed; therefore we focused on the toothrow and bones found in the same sample for the discussion below. Hair could not help in the identification of fragments since all fecal samples contained a large amount of hair most likely from the sampled individuals themselves. The comparison of the toothrow and bones found in the feces with those of museum specimens of M. paraguayanus and G. microtarsus, established that the toothrow and bones were much smaller in size than those of adults of both species. Moreover the sample which contained the toothrow dates from December, when we expect only adults and newborns of M. paraguayanus compose the population, since juveniles seem to appear only after January (Barros et al., 2008). This observation, coupled with the fact that the bones and maxilla detected were not completely ossified and the feces containing vertebrate remains were collected during the reproductive season (December and March) of both species (Quental et al., 2001; Martins et al., 2006; Barros et al., 2008), suggests that our finding uncovered either an event of scavenging on a dead young didelphid, or infanticide (intra or interspecific).


Fig. 1. Scanning electron microscope photograph of a fragmented young didelphid upper toothrow, containing one canine and two premolars found in a female M. paraguayanus fecal sample.

Among didelphids, scavenging behavior has been deduced based on the detection of dipteran pupae remains in feces of species of the genera Monodelphis, Philander, Caluromys and also Micoureus, but no further information on the identity and quantity of the carrion consumed has been obtained (Santori et al., 1997; Vieira and Astúa de Moraes, 2003; Carvalho et al., 2005). Scavenging on carrion, including conspecific, has been shown to be an important food source to the diet of species of the genus Didelphis (Hopkins and Forbes, 1980). In particular, Hopkins and Forbes (1980) results show that especially on winter, in an urban environment, the most frequent mammal on the diet of Didelphis virginiana were conspecifics.
Intraspecific infanticide is the killing of immature by parents (also defined as filial cannibalism; Klug and Bonsall, 2007) or nonparental conspecifics. Among didelphids, filial cannibalism has been reported for captive opossums (genus Didelphis) in response to stress (Raven, 1929), but also seems to occur under the absence of stressors (Hopkins and Forbes, 1980). Similarly to filial cannibalism, nonparental infanticide behavior may provide individuals with nutritional benefits. In addition to that, territorial females that perform infanticide benefit from the abandonment of nest sites and territories by those mothers that had lost their offspring (Wolff, 1993, 1997). Since female M. paraguayanus seem to be territorial, because their home ranges show little overlap (Pires and Fernandez, 1999; Quental et al., 2001; Moraes and Chiarello 2005), and M. paraguayanus offspring pass through a nidiculous life, in which they may be vulnerable (Delciellos et al., 2006), nonparental infanticide behavior could also be included in this catalogue of possibilities.
Another possibility to be considered is that the maxilla and bones found in the samples are remains of a young of another didelphid species occurring in the study area such as G. microtarsus. Preying upon other marsupials is not unusual among didelphid species (Vieira and Astúa de Moraes, 2003). Interspecific predation on young could have an important role if sympatric didelphid species compete for nesting sites and would also provide an alternative source of food. Finally, we cannot exclude the possibility that young carried around by the female M. paraguayanus could have been consumed while inside the trap as a response to capture stress. Such a female could have been captured soon after we had set the traps and stayed there all night long, so that feces could contain remains of young consumed while inside the traps. This catalogue of possibilities reveals the potential behavioral complexity of the species and other didelphids. Detailed studies are needed to investigate the occurrence, prevalence, and ecological relevance of scavenging and infanticide behavior in M. paraguayanus and in other tropical mammalian species. Such information is important for us to better understand the unique ways in which each species experiences the environment and interfaces with the community and the implications of these behaviors for population and community dynamics.

ACKNOWLEDGMENTS

M. M. Pinto allowed access and provided logistic support at Reserva Biológica de Mogi Guaçu. This work was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo, FAPESP, Brazil. M. M. Pires is supported by a FAPESP scholarship (07/57299-7). E. G. Martins was supported by FAPESP scholarships (01/00092-5 and 03/10639-7). L. D. Cruz and F. R. Fernandes were supported by scholarships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil: 131806/2006-8 and 135028/2005-1). S. F. dos Reis is partially supported by a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil). We thank two anonymous reviewers for their comments and suggestions which improved the manuscript

LITERATURE CITED

1. ASTÚA DE MORAES D, RT SANTORI, R FINOTTI, and R CERQUEIRA. 2003. Nutritional and fibre contents of laboratory-established diets of Neotropical opossums (Didelphidae). Pp. 229-237, in: Predators with pouches: the biology of carnivorous marsupials (M Jones, C Dickman, and M Archer, eds.).CSIRO Publishing, Melbourne, Australia.         [ Links ]

2. BARROS CS, R CROUZEILLES, and FAS FERNANDEZ. 2008. Reproduction of the opossums Micoureus paraguayanus and Philander frenata in a fragmented Atlantic Forest landscape in Brazil: is seasonal reproduction a general rule for Neotropical marsupials? Mammalian Biology 73:463-467.         [ Links ]

3. CÁCERES NC, IR GHIZONI, JR, and ME GRAIPEL. 2002. Diet of two marsupials, Lutreolina crassicaudata and Micoureus demerarae, in a coastal Atlantic Forest island of Brazil. Mammalia 66:331-340.         [ Links ]

4. CARVALHO FMV, PS PINHEIRO, FAS FERNANDEZ, and JL NESSIMIAN. 1999. Diet of small mammals in Atlantic Forest fragments in southeastern Brazil. Revista Brasileira de Zoociências 1:91-101.         [ Links ]

5. CARVALHO FMV, FAS FERNANDEZ, and JL NESSIMIAN. 2005. Food habits of sympatric opossums coexisting in small Atlantic Forest fragments in Brazil. Mammalian Biology 70:366-375.         [ Links ]

6. CASELLA J and NC CÁCERES. 2006. Diet of four small mammal species from Atlantic forest patches in South Brazil. Neotropical Biology and Conservation 1:5-11.         [ Links ]

7. CEOTTO P, R FINOTTI, R SANTORI, and R CERQUEIRA. 2009. Diet variation of the marsupial Didelphis aurita and Philander frenatus (Didelphimorphia, Didelphidae) in a rural area of Rio de Janeiro state, Brazil. Mastozoología Neotropical 16:49-58.         [ Links ]

8. DELCIELLOS AC, D LORETTO, and MV VIEIRA. 2006. New methods for the study of vertical stratification of Neotropical oppossums. Oecologia Brasiliensis 10:135-153.         [ Links ]

9. GARDNER AL. 2007. Mammals of South America, volume 1: marsupials, xenarthrans, shrews, and bats. University of Chicago Press, Chicago, Illinois.         [ Links ]

10. GARDNER AL and GK CREIGHTON. 2007. Genus Micoureus Lesson, 1842. Pp. 74-82, in: Mammals of South America, volume 1: marsupials, xenarthrans, shrews, and bats (AL Gardner, ed.). University of Chicago Press, Chicago, Illinois.         [ Links ]

11. HOPKINS DD and RB FORBES. 1980. Dietary patterns of the Virginia opossum in an urban environment. The Murrelet 61:20-30.         [ Links ]

12. KLUG H and MB BONSALL. 2007. When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. The American Naturalist 170:886-901.         [ Links ]

13. LEITE YLR, LP COSTA, and JR STALLINGS. 1996. Diet and vertical space use of three sympatric opossums in a Brazilian Atlantic forest reserve. Journal of Tropical Ecology 12:435-440.         [ Links ]

14. MARTINS EG, V BONATO, CQ DA-SILVA, and SF REIS. 2006. Seasonality in reproduction, age structure and density of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia: Didelphidae) in a Brazilian cerrado. Journal of Tropical Ecology 22:461-468.         [ Links ]

15. MORAES EA, JR and AG CHIARELLO. 2005. A radio tracking study of home range and movements of the marsupial Micoureus demerarae (Thomas) (Mammalia Didelphidae) in the Atlantic forest of southeastern Brazil. Revista Brasileira de Zoologia 22:85-91.         [ Links ]

16. PIRES AS and FAS FERNANDEZ. 1999. Use of space by the marsupial Micoureus demerarae in small Atlantic Forest fragments in south-eastern Brazil. Journal of Tropical Ecology 15:279-290.         [ Links ]

17. QUENTAL TB, FAS FERNANDEZ, ATC DIAS, and FS ROCHA. 2001. Population dynamics of the marsupial Micoureus demerarae in small fragments of Atlantic Coastal Forest in Brazil. Journal of Animal Ecology 17:339-352.         [ Links ]

18. RAVEN HC. 1929. A case of matricide in the opossum. Journal of Mammalogy 10:168.         [ Links ]

19. SANTORI RT, D ASTÚA DE MORAES, CEV GRELLE, and R CERQUEIRA. 1997. Natural diet at a restinga forest and laboratory food preferences of the opossum Philander frenata in Brazil. Studies of Neotropical Fauna & Environment 32:12-16.         [ Links ]

20. VIEIRA EM and D ASTÚA DE MORAES. 2003. Carnivory and insectivory in Neotropical marsupials. Pp. 267-280, in: Predators with pouches: the biology of carnivorous marsupials (M Jones, C Dickman, and M Archer, eds.). CSIRO Publishing, Melbourne, Australia.         [ Links ]

21. WOLFF JO. 1993. Why are female small mammals territorial? Oikos 68:364-370.         [ Links ]

22. WOLFF JO. 1997. Population regulation in mammals: an evolutionary perspective. Journal of Animal Ecology 66:1-13.         [ Links ]

Recibido 24 junio 2009.
Aceptado 15 febrero 2010.

Editor asociado: D Flores

Creative Commons License Todo el contenido de esta revista, excepto dónde está identificado, está bajo una Licencia Creative Commons