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1 SHORT COMMUNICATION 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? Camila S. Barros a,b,, Renato Crouzeilles a, Fernando A.S. Fernandez a,b a Laboratório de Ecologia e Conservação de Populações, Departamento de Ecologia, Universidade Federal do Rio de Janeiro, CP 680, Ilha do Fundão, Rio de Janeiro, RJ , Brazil b Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro. Rio de Janeiro, Brazil Received 7 March 07; accepted 14 August 07 Keywords: Micoureus; Philander; Atlantic Forest; Breeding seasons; Conservation Reproductive seasonality is one of the most important ways by which an animal adapts to temporal changes in its environment, for example, allowing it to deal with seasonal fluctuations in resource availability. Since Davis (194) seminal work, the seasonal cycle of reproduction of marsupials in Neotropical forests has been well established; reproduction usually falls within the wet season. Marsupials main food resources are insects and fruits (Emmons and Feer 1997), which usually have a higher availability in the wet period (Bergallo and Magnusson 1999). As the lactation is the period with highest energy demands in marsupials (Atramentrowicz 1992), its synchronization with the wet season allows lactating females to have more energy available. In fact, many studies with Neotropical marsupials link the beginning of the reproductive period with the increase in precipitation and the resulting enhancement of food resources (Fleming 1973; Tyndale- Biscoe and Mackenzie 1976; O Connell 1979; Fonseca and Kierulff 1989). Corresponding author. Laboratório de Ecologia e Conservação de Populaço es, Departamento de Ecologia, Universidade Federal do Rio de Janeiro, CP 680, Ilha do Fundão, Rio de Janeiro, RJ , Brazil. address: cbarros@biologia.ufrj.br (C.S. Barros). The species studied were Micoureus paraguayanus (Tate, 1931) and Philander frenata Olfers, The woolly mouse opossum M. paraguayanus (previously Marmosa cinerea, Micoureus cinereus and Micoureus demerarae) is endemic to Atlantic Forest in Brazil. It is a medium sized ( g adult weight) solitary didelphid marsupial, with nocturnal and arboreal habits. Its diet consists of insects and fruits (Pinheiro et al. 02). At Ilhas dos Barbados M. paraguayanus is represented by small populations in each fragment, forming a metapopulation (Pires and Fernandez 1999; Pires et al. 02). The grey four-eyed opossum P. frenata is the Atlantic Forest form of what had been previously regarded as a widely distributed species, P. opossum (Patton and Da Silva 1997). It is a medium sized opossum ( g adult weight). It is solitary, nocturnal and mostly terrestrial (Emmons and Feer 1997). At Ilhas dos Barbados P. frenata may be represented by a single population using the whole landscape, as each individual establishes a home range with both fragments and matrix as parts of its range, being able to move among more than one fragment in a night (Pires et al. 02; Lira et al. 07). It eats mostly insects and small vertebrates (Cáceres 04). In the present study, populations of these two marsupials were monitored in a fragmented landscape for 11 years. The seasonality of their reproduction in this changed environment was /$ - see front matter r 07 Deutsche Gesellschaft fu r Säugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:.16/j.mambio Mamm. biol. 73 (08)

2 464 ARTICLE IN PRESS C.S. Barros et al. / Mamm. biol. 73 (08) compared with the patterns shown by the same species in previous studies. The study was carried out from 199 to 0, in a set of eight Atlantic Forest fragments (named from A to H) called Ilhas dos Barbados within Poc o das Antas Biological Reserve ( S; W), one of the largest lowland Atlantic Coastal Forest Reserves in the Rio de Janeiro State, Brazil. The weather is wet tropical. Annual average temperature was 2.7 1C and annual average rainfall was 2309 mm over the 11 study years (measured at meteorological station from Programa Mata Atlaˆntica/JBRJ within the Reserve). There is a moderate seasonality, as less than one-third of the rainfall occurs in the dry season, which occurred regularly from April to September (Fig. 1). The fragment areas range from approximately 1.2 to 13.3 ha, and distances among them range from 60 and 1180 m. The fragments are separated by a matrix of exotic grasses, such as Imperata brasilensis, Melinis minutiflora and Panicum maximum, intermingled with bracken (Pteridium aquinum) and sparse pioneer trees (Trema micrantha and Cecropia spp.). The data were obtained from capture mark recapture studies carried out in three fragments, A from March 199 to September 1998, D from April 1996 to November 01 and E from January 00 to November 0. Each sampling session comprised five consecutive trapping nights. Up to 1999, and in 04 0, sampling was performed every second month. From 00 to 03, sample sessions were spaced by 3 months. The grids had parallel lines every 0 m, with trapping points set m apart. Two traps were set at each trapping point, one on the ground and one at a tree, either at a height of about 1. m or on platforms hanging at heights ranging from to 12 m. Traps used were Sherman XLF (38 cm 19 cm 12 cm) and Tomahawk 603 (48. cm 17 cm 17 cm). Total trapping effort was 48,080 trapnights. The bait used was a mixture of banana, oat, peanut butter and minced bacon, placed on top of a manioc slice. The individuals captured were marked with an aluminum ear tag with an individual alphanumerical code. Sex, reproductive condition and age (based on tooth eruption pattern; Tyndale-Biscoe and Mackenzie 1976; Vidigal 1997) were recorded for each capture. Only females were used in the determination of reproductive activity, as the external characteristics that indicate reproductive activity are easily and precisely detectable for females only. Females that had pouch young or swollen mammae were considered as reproductively active. Population densities were estimated by the ratio between the population size (estimated by Burnham and Overton s (1979) Jackknife estimator) and the fragment size, as capture grid covers almost the whole fragment. Circular statistics (Zar 1999; Program ORIANA) was used to describe the breeding seasonality. Each month corresponds to a 301 sector in the circular histograms. In each sector a vector is drawn, whose length is given by the frequency of reproductive events recorded in each calendar month during the whole study. From these vectors one calculates an average vector, r. Its length ranges from 0 to 1, a larger value indicates that the observations are clustered more closely around the mean. To test if the data are distributed in a uniform manner, Rayleigh s Uniformity Test (Zar 1999) was used. Logistic regression (Gotelli and Ellison 04) was used to test if the presence of reproductive females was related with precipitation. Only months when females were captured were used. Precipitation was tested in three ways, without time lag and with time lags of 1 and 2 months. These lags take in account the likely time before high precipitation is Jan Feb Mar Apr Jun Jul Aug Sep Oct Nov Dec Precipitation (mm) Temperature ( C) 0 Fig. 1. Ombrothermic diagram with the mean monthly precipitation from 199 to 0 at Poço das Antas Biological Reserve.

3 C.S. Barros et al. / Mamm. biol. 73 (08) converted into actual availability of resources for the animals. Square-root transformations were applied to the precipitation data, in order to fulfill the normality assumption of logistic regression. During the whole study, 166 individuals (116 captures) of M. paraguayanus were caught, from these 94 (684) were females. For P. frenata 79 individuals (243 captures) were caught, from these 37 (129) were females. For M. paraguayanus there was no evidence that mean densities differed among populations (A: 1.1 ind/ha (70.99); D: 1. ind/ha (70.71); E: 1.01 ind/ha (70.4); ANOVA F ¼ 2.30; p ¼ 0.11; n ¼ 73). Timing of breeding was similar across the three populations of M. paraguayanus and therefore they were analyzed together. There were reproductive females only within the wet season, from October to (Fig. 2). The distribution of females in reproductive activity was different from a uniform distribution along the year (length of mean vector ¼ 0.63; Rayleigh s Z ¼ 29.04, po0.001, n ¼ 74). Presence of breeding females was significantly related with rainfall at the same month (Logistic regression L ¼ 74.21, w 2 ¼ 26.98, df ¼ 1, po0.001), a month before (L ¼ 60.18, w 2 ¼ 41.00, df ¼ 1, po0.001), and 2 months before (L ¼ 88.76, w 2 ¼ 12.42, df ¼ 1, po0.001; all n presences ¼ 36, n absences ¼ 37). Juveniles appear only from January through. At least two litters were recorded within each breeding season, one in October/November and another in January/February. The median litter size was 11 young (min ¼ 6; max ¼ 11; n ¼ 24). P. frenata was abundant at the study area from 1997 to 04. The presence of reproductive females of P. frenata showed no evidence of seasonality (length of the mean vector ¼ 0.07; Rayleigh s Z ¼ 0.137; po0.874; n ¼ 27). Reproductively active females were found throughout the year, except for June and September (Fig. 2). There was no significant relationship between the presence of breeding females and the precipitation at the same month (Logistic regression L ¼ 39., w 2 ¼ 0., df ¼ 1, p ¼ 0.6), a month before (L ¼ 39.4, w 2 ¼ 0.21, df ¼ 1, p ¼ 0.6) or 2 months before (L ¼ 39.66, w 2 ¼ 0.09, df ¼ 1, p ¼ 0.76, all n presences ¼, n absences ¼ 22). Unlike M. paraguayanus, for P. frenata juveniles were detected almost throughout the year. The median litter size was five young (min ¼ 1; max ¼ 8; n ¼ 21). As expected for Neotropical marsupials, M. paraguayanus breeding was markedly seasonal and fell within the wet period, when resource availability is high. Although reproductive data on Micoureus are scarce in the literature, seasonal reproduction linked with the wet season seems to be common for this species (Fonseca and Kierulff 1989) and its congeneric M. demerarae (O Connell 1979). The reproductive period was quite regular among years, starting in October and ending in March. The frequency of females in reproductive activity was positively related with the precipitation of the same month, a month before and 2 months before. As is to be expected a delay between peaks in precipitation and their effect on the resource availability, the relationships, especially the lagged ones, indicate that M. paraguayanus reproduction is linked with resource availability. The age structure of the population also reflects its breeding seasonality. Young individuals were captured only from January to June, which corresponds to a 3 months delay from the reproductive season. This delay in the recruitment probably reflects the time lag between the period when are young still attached to the nipples until they become independent and thus available to be trapped. P. frenata, on the other hand, showed no breeding seasonality. Reproductive activity was found all year long, except for June and September. The presence of Micoureus paraguayanus Philander frenata December January December January November February November February October March October March September April September April August July June August July June Fig. 2. Circular histograms showing the seasonal variation in the proportion of reproductive females for two opossum species. Bars are the numbers of reproductive females recorded in each month (summed across years, 199 0). Arrows indicate the position and size of the mean vector.

4 466 ARTICLE IN PRESS C.S. Barros et al. / Mamm. biol. 73 (08) females in reproductive activity was not related with the precipitation, either with or without time lags. Therefore, there is no evidence for the influence of precipitation, either directly or indirectly through resource availability, on the reproductive activity of P. frenata. Young individuals were found almost along the whole year, except for June, October and November. For P. frenata, Cerqueira et al. (1993), in Restinga (coastal shrubland) and Gentile et al. (00), in Atlantic Forest, found seasonal patterns, with no females in reproductive activity from March to June and from to June, respectively. At Ilhas dos Barbados it was possible to detect plenty of reproductive activity in this same period. For example, three out of four females captured in April were reproducing, whereas Cerqueira et al. (1993) captured a total of 16 females in April of different years, yet none were reproductive. Those studies were relatively close to our study site, but they were carried out in different vegetation types. Besides the differences in the vegetation type, the landscape we studied is composed of very small fragments (1 13 ha), whereas the former studies were made in larger pieces of habitat. Such tiny fragments are highly exposed to edge effects (Pessoa and Oliveira 06), which can alter the food resource availability, for example, by enhancing the availability of insects (Lambert et al. 06). This change in resource availability may allow P. frenata to reproduce in the months when it would not be able to do so in continuous forests or larger fragments. Our results show that breeding seasonality was not as fixed as expected among marsupial species: M. paraguayanus followed the expected pattern for Neotropical marsupials, but P. frenata in the same area did not. Besides, and perhaps more interesting, they varied within a species (P. frenata), as compared with previous studies in different situations. At this point, it seems important to recall a distinctive feature of our study site, as compared to the sites of most previous studies: it is a highly fragmented landscape, with the original forest reduced to a set of tiny forest remnants. However, studies which addressed this question have assumed that breeding parameters obtained in continuous populations would remain basically unchanged in fragments (Laurance 1991; Viveiros de Castro and Fernandez 04). Our findings highlight that this is likely to be an unwarranted assumption. Acknowledgements We thank friends from LECP/UFRJ for helping in the field and for discussions; A. Pires for suggesting circular statistics; A. Sanseverino for translating the title; Programa Mata Atlaˆntica/JBRJ for rainfall data; Frank Zachos and two anonymous referees for their suggestions; Fundac a o O Botica rio de Protec a o a` Natureza, PROBIO/PRONABIO-MMA (BIRD/GEF), Critical Ecosystems Partnership Funding, CNPq, FAPERJ and FUJB for funding; IBAMA Poc o das Antas and the Golden Lion Tamarin Association for logistic support. Personal grants were given by CNPq, CAPES and FAPERJ. References Atramentrowicz, M., Optimal litter size: does it cost more to raise a large litter in Caluromys philander? Can. J. Zool. 70, 11. Bergallo, H.G., Magnusson, W.E., Effects of climate and food availability on four rodent species in southeastern Brazil. J. Mammal. 80, Burham, K.P., Overton, W.S., Robust estimation of population size when capture probabilities vary among animals. Ecology 60, Ca ceres, N.C., 04. Diet of three didelphid marsupials (Mammalian, Didelphimorphia) in southern Brazil. Mamm. 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