Knowledge of resting sites’ types and pattern of use could help understand several aspects of an animal’s ecology (Smith et al. 2007). The choice of where to rest and the pattern of use of resting sites should be affected primarily by the availability of suitable sites, predation pressure, food resources distribution, or home range defense (e.g. Day and Elwood 1999, Smith et al. 2007). Mammals resting sites have been recorded mainly for large sized species such as primates (e.g. Smith et al. 2007) and carnivores (e.g. Baghli and Verhagen 2005). Non-volant small mammals – the most diverse group of mammals in the Neotropics – are nocturnal and thus difficult to locate visually, but some resting sites have been recorded using spool and line devices (e.g. Briani et al. 2001) and radiotelemetry (e.g. Moraes and Chiarello 2005). Here, we describe the type and pattern of use of resting sites by the opossums Caluromys philander (Linnaeus 1758), Marmosa paraguayana Tate, 1931 and Philander frenatus (Olfers 1818) in Atlantic Forest fragments.
This study was conducted in a fragmented landscape within Poço das Antas Biological Reserve (22°30′–22°33′ S, 42°15′–42°19′ W), Rio de Janeiro, Brazil, which consists of eight forest fragments surrounded by a matrix composed mostly of grasses and bracken. Adult individuals were captured and fitted with radio-collar transmitters at two of the fragments. Between May 2001 and September 2004, animal locations were obtained by a variation of the “homing-in on the animal” technique – locations were recorded when the signal was loud enough to be heard with the antenna disconnected from the receptor (Lira et al. 2007). The first location of each individual was obtained before it left its resting site (usually at sunset) and subsequent locations were obtained until the end of its activity when it entered the resting site (usually at sunrise). Occasionally, diurnal locations were obtained; all these were resting site locations.
Four Caluromys philander (Cp), eight Philander frenatus (Pf) and four Marmosa paraguayana (Mp) were fitted with transmitters and monitored for 2–8 months (Lira et al. 2007). Fifty resting sites used by 14 individuals were recorded. The number of resting sites used by an individual varied from two to six (Table 1) and was not influenced by its total number of locations (linear regression: R2=0.25; F=3.85; p=0.07).
Resting sites used by Philander frenatus individuals included underground burrows, tree cavities, tangles of lianas and palm crowns (Table 1, Figure 1). In the latter two nest types, dried leaves accumulated forming natural shelters. Unlike studies that described nest sharing, suggesting that opossums are more social than previously believed (Galliez et al. 2009, Astúa et al. 2015), simultaneous use of resting sites by radio-tracked individuals was not observed in this study. However, two P. frenatus individuals used the same tree cavity in different occasions – 7 months apart from each other – suggesting that resting sites with some specific characteristics are preferred by animals.
Additionally, we observed in eight different occasions two females, Pf-F02 and Pf-F04, resting inside spherical structures (~20 cm diameter) of interlaced dry leaves 1 m above the ground, which suggests that Philander frenatus individuals build their own resting sites (Table 1). Nest building has been already described for the brown four-eyed opossum Metachirus nudicaudatus Desmarest, 1817 (Moraes 2004, Loretto et al. 2005) and also for rodents (Briani et al. 2001, Shibata et al. 2004, Alvarenga and Talamoni 2005). Additionally, the behavior of gathering and carrying nesting material in curling tails was documented in captivity for Monodelphis domestica Wagner, 1842 (Unger 1982) and Didelphis virginiana Kerr, 1792 (McManus 1970) and in the field with camera traps for Caluromys philander (Dalloz et al. 2012), Didelphis marsupialis Linnaeus, 1758 and M. nudicaudatus (Delgado-V et al. 2014).
Our results suggest that individuals of Philander frenatus rest frequently in the understory; only Pf-M01 used underground burrows (Table 1). Indeed, Miles et al. (1981) have already described the preference of P. frenatus for resting in hollow trees and tree forks located at 8–10 m above ground. This is an interesting finding as this marsupial – despite its arboreal ability (Delciellos and Vieira 2006) – use preferentially the ground (Passamani 1995, Cunha and Vieira 2002) as has also been observed in our study area (Viveiros de Castro and Fernandez 2004). Cunha and Vieira (2002) suggested that the use of understory by P. frenatus could be related to competition with and occasional predation by Didelphis aurita Wied-Neuwied, 1826, a species that occurs in our studied forest fragments (Viveiros de Castro and Fernandez 2004).
As Caluromys philander and Marmosa paraguayana were always resting at the forest canopy or high in the understory, resting site types could not be identified in most cases. An exception was a female M. paraguayana (Mp-F01) that was located resting at the crown of an adult individual of the palm Astrocaryum aculeatissimum, approximately 3 m high (Table 1). A preference of M. paraguayana for nesting in A. aculeatissimum was described by Moraes and Chiarello (2005) who found 70.7% of the resting sites of M. paraguayana individuals in this palm species at an Atlantic Forest fragment (União Biological Reserve) which is 30 km away from our study area.
Repeated use of resting sites was observed for all three species (Table 1). More than half of the resting site locations of nine out of the 14 radio-tracked individuals were in a single resting site. According with Aquino and Encarnación (1986) and Smith et al. (2007), the repeated use of resting sites could be a strategy to stay close to resources, protection against adverse weather conditions, predators and/or competitors, territorial defense or caring of young. In our study, the repeated use of resting sites was observed not only in females but also in males and this behavior occurred throughout the year, not only during the reproductive period – which, for opossums, normally coincide with the period of higher food availability, the warm-wet season (Barros et al. 2015). Additionally, although there is evidence for site fidelity in opossums, as far as we know there is no evidence of opossums actively defending an area and we have also not observed any agonistic encounter during our study. Therefore, we believe that the repeated use of resting sites in our study area might be a strategy to stay close to resources and a protection against adverse weather conditions, predators and/or competitors.
We thank the colleagues from Laboratório de Ecologia e Conservação de Populações (UFRJ) for their help in the fieldwork. This study was funded by Fundação Grupo Boticário de Proteção à Natureza, MacArthur Foundation, The Nature Conservancy and Idea Wild. We also thank Dr. Christiane Denys and two anonymous referees for their constructive comments on the manuscript. Personal grants were given by FAPERJ, CAPES and CNPq.
Alvarenga, C.A. and S.A. Talamoni. 2005. Nests of the Brazilian squirrel Sciurus ingrami Thomas (Rodentia, sciuridae). Zoologia 22: 816–818. Google Scholar
Astúa, D., R.A. Carvalho, P.F. Maia, A.R. Magalhães and D. Loretto. 2015. First evidence of gregarious denning in opossums (Didelphimorphia, Didelphidae), with notes on their social behaviour. Biol. Lett. 11: 20150307. PubMedCrossrefWeb of ScienceGoogle Scholar
Baghli, A. and R. Verhagen. 2005. Activity patterns and use of resting sites by polecats in an endangered population. Mammalia 69: 211–222. Google Scholar
Barros, C.S., T. Püttker and R. Pardini. 2015. Timing and environmental cues associated with triggering of reproductive activity in Atlantic forest marsupials. Mamm. Biol. 80: 141–147. CrossrefWeb of ScienceGoogle Scholar
Briani, D.C., E.M. Vieira and A.M.V. Vieira. 2001. Nests and nesting sites of Brazilian forest rodents (Nectomys squamipes and Oryzomys intermedius) as revealed by a spool-and-line device. Acta Theriol. 46: 331–334. Google Scholar
Dalloz, M.F., D. Loretto, B. Papi, P. Cobra and M.V. Vieira. 2012. Positional behaviour and tail use by the bare-tailed woolly opossum Caluromys philander (Didelphimorphia, Didelphidae). Mamm. Biol. 77: 307–313. CrossrefWeb of ScienceGoogle Scholar
Day, R.T. and R.W. Elwood. 1999. Sleeping site selection by the golden-handed tamarin Saguinus midas: the role of predation risk, proximity to feeding sites, and territorial defence. Ethology 105: 1035–1051. CrossrefGoogle Scholar
Delgado-V, C.A., A. Arias-Alzate, S. Aristizábal-Arango and J.D. Sánchez-Londoño. 2014. Uso de la cola y el marsúpio em Didelphis marsupialis y Metachirus nudicaudatus (Didelphimorphia: Didelphidae) para transportar material de anidación. Mastozool. Neotrop. 21: 129–134. Google Scholar
Galliez, M., M. Leite, T.L. Queiroz and F.A.S. Fernandez. 2009. Ecology of the water opossum Chironectes minimus in Atlantic Forest streams of southeastern Brazil. J. Mammal. 90: 93–103. Web of ScienceCrossrefGoogle Scholar
Lira, P.K., F.A.S. Fernandez, H.S.A. Carlos and P.L. Curzio. 2007. Use of a fragmented landscape by three species of opossum in south-eastern Brazil. J. Trop. Ecol. 23: 427–435. Web of ScienceCrossrefGoogle Scholar
Loretto, D., E. Ramalho and M.V. Vieira. 2005. Defense behavior and nest architecture of Metachirus nudicaudatus Desmarest, 1817 (Marsupialia, Didelphidae). Mammalia 69: 417–419. Google Scholar
Miles, M.A., A.A. Souza and M.M. Póvoa. 1981. Mammal tracking and nest location in Brazilian forest with an improved spool-and-line device. J. Zool. 195: 331–347. Google Scholar
Moraes, E.A. 2004. Radio tracking of one Metachirus nudicaudatus (Desmarest, 1817) individual in Atlantic Forest of southeastern Brazil. Boletim do Museu de Biologia Mello Leitão 17: 57–64. Google Scholar
Moraes, E.A. and A. Chiarello. 2005. Sleeping sites of the wolly mouse opossum Micoureus demerarae (Thomas) (Didelphimorphia, Didelphidae) in the Atlantic Forest of south-eastern Brazil. Zoologia 22: 839–843. Google Scholar
Passamani, M. 1995. Vertical stratification of small mammals in Atlantic Hill forest. Mammalia 59: 276–279. Google Scholar
Smith, A.C., C. Knogge, M. Huck, P. Löttker, H.M. Buchanan-Smith and E.W. Heymann. 2007. Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): effects of foraging, thermoregulation, predation, and resource defense constraints. Am. J. Phys. Anthropol. 134: 340–353. CrossrefPubMedWeb of ScienceGoogle Scholar
Viveiros de Castro, E.B. and F.A.S. Fernandez. 2004. Determinants of differential extinction vulnerabilities of small mammals in Atlantic Forest fragments in Brazil. Biol. Conserv. 119: 73–80. CrossrefGoogle Scholar
About the article
Published Online: 2017-04-27
Published in Print: 2017-12-20