Food habits of sympatric opossums coexisting in small Atlantic Forest fragments in Brazil

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Original investigation

Food habits of sympatric opossums coexisting in small Atlantic Forest fragments in Brazil By F.M.V. Carvalho, F.A.S. Fernandez and J.L. Nessimian Departamento de Ecologia; and Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

Abstract The diets of sympatric species of opossums coexisting in small (o10 ha) Atlantic Forest fragments were studied at Poc- o das Antas Biological Reserve, southeastern Brazil. Food items consumed by Caluromys philander and Didelphis aurita were investigated through the analysis of faecal contents, and compared with the diet of Micoureus demerarae analysed in a previous study. The major diet components for all three species were arthropods and fruits, with a high richness of items of both feeding categories; feathers were also found in the diet of D. aurita. The most frequent insect orders overall were Hymenoptera and Coleoptera, and most seeds were from plants of secondary vegetation such as Cecropia and Piper. The diets showed little variation along time and space for all three species. Diets were also similar among species, except for a larger consumption of Arachnida and Diplopoda and a smaller consumption of Lepidoptera by D. aurita when compared to M. demerarae. Diversity of food items was lower for C. philander when compared with either other species. There was a high feeding niche overlap between species, suggesting that differentiation in diet composition would not be enough to allow coexistence of the three species in small fragments. Coexistence may rather be allowed by vertical segregation and/or by differences in prey size. r 2005 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Key words: Caluromys philander, Didelphis aurita, Micoureus demerarae, diet, fragmentation

Introduction Fragmentation is a widespread process that causes alterations in ecological processes – such as predation, competition, herbivory and seed dispersal (Murcia 1995) – that may affect resource availability for animal consumers. The fragmentation of the Brazilian Atlantic Forest, one of the World’s biodiversity hotspots (Myers et al. 2000) has already reached dramatic levels, and there is an urgent need for understanding the biology and ecology of species in its fragments

(Terborgh 1992). Neotropical marsupials are mostly forest-dwelling species and therefore studies about their feeding ecology are important for understanding how well the Atlantic Forest remnants can be suitable for a long-term persistence of their populations in the fragmented landscape. We studied the diets of three species of marsupials, Didelphis aurita, Micoureus demerarae and Caluromys philander (order Marsupialia, family Didelphidae), in very small

1616-5047/$ - see front matter r 2005 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2005.08.003 Mamm. biol. 70 (2005) 6
366–375

ARTICLE IN PRESS Food habits of opossums in Atlantic Forest fragments fragments (mostly o10 ha), where they coexist with other species of marsupials and rodents (Viveiros de Castro and Fernandez 2004). The objectives of this study were (1) to determine diet composition of the bare-tailed woolly opossum C. philander and the blackeared common opossum D. aurita; (2) to compare diets intraspecifically among different fragments, climatic seasons, sexes, age classes and breeding and non-breeding periods; and (3) to compare diets interspecifically between the two species and also with a third marsupial species, the woolly mouse opossum M. demerarae, previously studied in the same area (Pinheiro et al. 2002).

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temperatures of 24.61C and average annual precipitation of 2121 mm (Ribeiro de Mello and Fernandez 2000); most rain falls from September to April (Fig. 1). Within the reserve, the study area was a system of eight small Atlantic Forest fragments, known as Ilhas dos Barbados (‘‘Islands of the Howler Monkeys’’). The fragments vary in area from 1.2 to 13.3 ha and they are about 2 km away from the reserve’s main forest block (3500 ha). Fragments are separated from each other by a matrix of open vegetation, dominated by grasses (Imperata brasiliensis, Melinis minutiflora, Panicum maximum) and bracken (Pteridium aquilinum), with scattered pioneer trees, Cecropia spp. and Trema micrantha (Viveiros de Castro and Fernandez 2004).

Data recording

Material and methods Study site This study was carried out in Poc- o das Antas Biological Reserve (221300 –221330 S; 421150 421190 W), with 6300 ha, mostly covered with lowland Atlantic Forest. The climate of Poc- o das Antas is warm tropical, with average annual

The diets of the marsupials were studied by analysis of faecal samples. The samples were obtained from March 1995 to July 2002, during a demographic study in the Ilhas dos Barbados (Quental et al. 2001; Viveiros de Castro and Fernandez 2004). Traps used were Sherman (38  10  12 cm) and Tomahawk (48.3  15.2  15.3 cm), set at the ground, understory (1.5–2 m)

rainfall 250.0

75.0

100.0

50.0

50.0

25.0

0.0

0.0 sep/01

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mar/01

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sep/00

200.0

mar/00

125.0

sep/99

250.0

mar/99

150.0

sep/98

300.0

mar/98

175.0

sep/97

350.0

mar/97

200.0

sep/96

400.0

mar/96

225.0

sep/95

450.0

average temperature (°C)

average temperature

mar/95

rainfall (mm)

500.0

Fig. 1. Ombrothermic diagram for Poc- o das Antas Biological Reserve, from March 1995 to September 2001.

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and canopy (5–15 m), baited with a mixture of banana, oat, peanut butter and bacon, placed on a manioc slice. Faeces were collected from the traps upon capture or directly from the animal during handling. For each sample the name of the species, capture date, capture point, plus sex, reproductive condition, age class and weight of the individual were recorded. Faecal samples were collected in fragments (as named in the previous studies quoted above) A (7.0 ha), D (8.7 ha) and E (11.0 ha). Samples were examined using binocular microscopes and their contents were separated in the following categories: arthropods, seeds, other plant matter, hair, and material of other sorts or non-identified. Arthropods were identified until at least the level of order, or family when possible. Seeds were separated in morphotypes and identified until family, or until genus, when possible. Since didelphid marsupials do not have incisive teeth specialized to crack seeds, these items in the faeces were assumed to represent frugivory rather than granivory. Data analyses used frequency of occurrence in faecal samples (number of samples where the item was present divided by the total number of samples) of each arthropod order and of each morphotype of seeds. Only the first sample collected of each individual was used, unless different samples of the same individual were obtained with an interval of more than 3 days. This procedure aimed to assure the statistical independence of the data, as an animal’s meal can last about 2 or 3 days until it is completely eliminated (R.T. Santori, personal communication). Diets of C. philander and D. aurita were compared among fragments, climatic seasons (dry and humid), breeding and non-breeding periods, sexes and age classes. For C. philander and for D. aurita, it was not possible to compare age classes and breeding and non-breeding periods, respectively, because the number of data in some of the categories involved was too small. Feeding habits of a third species, M. demerarae, were also studied previously in the same area by Pinheiro et al. (2002). Here, interspecific pairwise comparisons of diets of the three species were made, using the results for M. demerarae reported by Pinheiro et al. (2002) improved by applying the criterium described above for independence of data, and also by including additional samples for this species. In all analyses, we considered the dry season from September until April and the wet season from May until August, as defined by the ombrothermic diagram (Fig. 1). Reproductive season was from October until March, and age classes (juveniles, subadults and adults) defined using tooth eruption sequence, both following Quental et al. (2001).

Some samples were excluded from comparisons because of uncertainties in the determination of either age, class or sex. Presence of ants (Hymenoptera, Formicidae) in the diets was considered only when at least two species were found in the same sample. This procedure was adopted in order to avoid overestimating the frequency of ants in the diets, as it was very common to have baits attacked by ants during the study. In each occasion when a bait was attacked, the attackers nearly always belonged to a single ant species (although different ant species attacked the baits in different occasions). Therefore, we opted for a conservative approach, as the presence of only one species of ants could represent sample contamination.

Statistical analysis Diets of C. philander and D. aurita were analysed testing, for each species, the null hypothesis that the proportion of arthropods to seeds did not differ between different fragments, climatic seasons, sexes, age classes and breeding and non-breeding periods. The contingency G-test (log-likelihood ratio) with Yates correction (Zar 1999) was used for these comparisons. Arthropods were then separated by groups, which correspond to orders, except in two cases: arachnids, that were considered as a single group, because each of the orders (Araneae, Acari and Opiliones) had numbers too small to be considered separately; and class Diplopoda (superclass Myriapoda). Then it was tested, for each marsupial species, the null hypothesis that the distribution of frequencies of arthropods among these groups did not differ between different situations (the same comparisons as in the previous paragraph), using contingency G-tests. All samples for each species were then used to compare species’ diets pairwise (including M. demerarae), testing the two kinds of null hypotheses: (1) the proportion of arthropods to seeds and (2) the distribution of frequencies of arthropods among groups did not differ between fragments, climatic seasons, sexes, age classes and breeding and non-breeding periods. Again, comparisons were performed using contingency G-tests. Diversity of food items (using as categories arthropods, fruits and vertebrates) in the diet of the three marsupial species was compared among species, pairwise, considering all samples. Diversities were expressed by the Shannon index, followed by the Hutcheson t-test (Zar 1999) to test the null hypothesis that diet diversity was the same for both species of each pair. Feeding niche overlap among

ARTICLE IN PRESS Food habits of opossums in Atlantic Forest fragments

M. demerarae, C. philander and D. aurita was estimated pairwise using the Simplified Morisita Index (Krebs 1989).

Results Caluromys philander A total of 21 faecal samples of C. philander were analysed, belonging to 14 individuals. Arthropods were found in all samples. The most frequent of the seven orders found were Coleoptera and Hymenoptera. Arachnida and Diptera were found in three samples, and Orthoptera, Lepidoptera and Corrodentia were observed in one sample each (Table 1). Seeds were found in 15 samples (71% of the total). They were separated in

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seven morphotypes, six of which were identified. These types are from the families Piperaceae, Moraceae, Melastomataceae and Cecropiaceae (Table 1). Among the identified seeds, Ficus sp. 2 (Moraceae) was the most frequent, and Cecropia sp. and Ficus sp. 1 were the most abundant ones. Proportions of arthropods to seeds did not differ significantly between fragments (G= 0.0389, 1 df, P40.75), climatic seasons (Go0.00001, 1 df, P40.975), sexes (G= 0.4204, 1 df, P40.50) or breeding and nonbreeding periods (G=0.0129, 1 df, P40.90). Frequency distributions of arthropods among groups also did not differ significantly between fragments (G=4.4328, 6 df, P40.50), climatic seasons (G=4.8761, 6 df, P40.50), sexes (G=9.0988, 6 df, P40.10) or breeding and

Table 1. Frequency of occurence (in %) of food itens found in the diets of Micoureus demerarae, Caluromys philander and Didelphis aurita at Ilhas dos Barbados, Poc- o das Antas Biological Reserve, Brazil. Frequencies are expressed as the number of samples containing each item (in parenthesis), divided by the total number of collected samples and multiplied by 100. Numbers of samples with arthropods coincides with the total number of samples. Numbers of samples with seeds: M. demerarae, 64; C. philander, 15; D. aurita, 14. M. demerarae n=100 Aves Hymenoptera Coleoptera Arachnida Hemiptera Diptera Lepidoptera Corrodentia Orthoptera Blattodea Isoptera Copepoda Isopoda Diplopoda Odonata Mantodea Piper sp. Ficus sp.1 Cecropia sp. Piper mollicomum Miconia sp. Solanaceae Passiflora sp. Ficus sp.2 Cecropia aff. hololeuca Cucurbitaceae

59.0 59.0 27.0 15.0 11.0 15.0 1.0 13.0 1.0 1.0 1.0 1.0

17.2 1.6 12.5 6.3 3.1 1.6

— (59) (59) (27) (15) (11) (15) (1) (13) (1) — (1) (1) (1) — — (11) (1) (8) (4) — (2) (1) — — —

C. philander n=21

D. aurita n=16

— 38.1 (8) 57.1 (12) 14.3 (3) — 14.3 (3) 4.8 (1) 4.8 (1) 4.8 (1) — — — — — — — 6.7 (1) 13.3 (2) 13.3 (2) 6.7 (1) 6.7 (1) — — 20.0 (3) — —

12.5 81.3 75.0 81.3 12.5 12.5 6.3 25.0 6.3 18.8

12.5 6.3 6.3 21.4 21.4 7.1

14.2 14.2 5.8

(2) (13) (12) (13) (2) (2) (1) — (4) (1) (3) — — (2) (1) (1) (3) — (3) (1) — — — (2) (2) (1)

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non-breeding P40.25).

periods

(G=7.4326,

6

df,

Didelphis aurita For D. aurita, 16 samples were analysed, every one from a different individual. Arthropods were found in all samples. The most frequent among 12 different arthropod groups were Hymenoptera, Arachnida and Coleoptera. Orthoptera were found in four samples, Isoptera in three, and Diplopoda, Diptera and Hemiptera in two samples. The remaining orders found were Lepidoptera, Blattodea, Odonata and Mantodea, in only one sample each (Table 1). Seeds were found in 14 samples (87.5% of the total). Seeds were separated in 11 morphotypes, six of which were identified, belonging to the families Piperaceae, Cecropiaceae, Moraceae and Cucurbitaceae (Table 1). Piper sp. (Piperaceae) and Cecropia sp. were the most frequent seeds, and Cecropia sp. was the most abundant one, representing 92% of the total abundance of seeds. Besides arthropods and seeds, feathers were also found in two samples of D. aurita. There were no significant differences in the proportions of arthropods to seeds in any comparison: between fragments (G=0.0128, 1 df, P40.90), climatic seasons (G=0.0374, 1 df, P40.75), sexes (G=0.0573, 1 df, P40.75) and age classes (G=0.2597, 2 df, P40.75). There were also no significant differences in the distribution of frequencies of arthropod groups in the diet, either between fragments (G=6.7477, 10 df, P40.50), climatic seasons (G=6.2202, 11 df, P40.75), sexes (G=9.8956, 11 df, P40.25) or age classes (G=22.3526, 22 gl, P40.25). Interspecific Comparisons Interspecific comparisons among the diets of the three marsupials showed no significant differences in proportions of arthropods to seeds, either between M. demerarae and C. philander (G=0.0111, P40.90), M. demerarae and D. aurita (G=0.3361 P40.50), or C. philander and D. aurita (G=0.0251, P40.75). The distribution of arthropods among groups was significantly different between

M. demerarae and D. aurita (G=27.9734, 14 df, Po0.025). The differences were due mainly to a greater proportion of Arachnida and Diplopoda in faecal samples of D. aurita and of Lepidoptera in M. demerarae. Moreover, some arthropod groups were found in samples of a single species: Corrodentia, Copepoda and Isopoda for M. demerarae; Odonata and Mantodea for D. aurita. However, the distribution of arthropods among groups was not significantly different in the comparisons between M. demerarae and C. philander (G=9.6632, 11 df, P40.50) and between C. philander and D. aurita (G=15.7557, 12 df, P40.10) (Fig. 2). The diversity of items in the diet was significantly higher for M. demerarae (H0 = 2.523) than for C. philander (H0 =2.240) (t=2.083, 93 df, Po0.05). The diversity of items in the diet of D. aurita (H0 =2.699) was also significantly higher than C. philander (t=2.934, 119 df, Po0.005). Between M. demerarae and D. aurita there was no significant difference (t=1.394, 164 gl, P40.10). According to Morisita’s index, M. demerarae showed similar niche overlaps with C. philander (0.91) and D. aurita (0.92). Both values were higher than the overlap estimated between C. philander and D. aurita (0.84).

Discussion Arthropods were the main item in the diets of C. philander, D. aurita and M. demerarae, followed by fruits. Coleoptera and Hymenoptera (mainly Formicidae) were the two most frequent orders; this is unsurprising, as Formicidae is often the animal family with greatest biomass in tropical forests and Coleoptera is the most diverse order in nature. Moreover, beetles can be overestimated in the diet in relation to other groups of arthropods, because their resistant elytra are more difficult to digest while passing by the digestive tract. Presence of Lepidoptera and Diptera was more frequent as larvae and pupae; these are more nutritious than adult forms (Redford and Dorea 1984). Dipteran larvae may indicate consumption of carrion by the marsupials, as a way of obtaining animal protein with low energy cost (Santori

ARTICLE IN PRESS Food habits of opossums in Atlantic Forest fragments

90.0

M . demerarae

C. philander

371

D. aurita

80.0

frequency (%)

70.0 60.0 50.0 40.0 30.0 20.0 10.0 Mantodea

Odonata

Diplopoda

Isopoda

Copepoda

Isoptera

Blattodea

Orthoptera

Corrodentia

Lepidoptera

Diptera

Hemiptera

Arachnida

Coleoptera

Hymenoptera

0.0

arthropods

Fig. 2. Frequencies of the arthropod groups found in the faecal samples of the marsupials M. demerarae, C. philander and D. aurita in small forest fragments at Ilhas dos Barbados, Poc- o das Antas Biological Reserve, southeastern Brazil.

et al. 1997). Feathers and hair were found in samples from D. aurita and from all three species respectively, but feathers and hair were not analysed and it is difficult to ascertain whether they came from live prey or from carrion; the hair may also come from the marsupial itself. Nowak (1991) reported the use of small vertebrates and carrion by Caluromys spp. The consumption of vertebrates by M. demerarae and by Didelphis spp. has also been observed in other studies (Cordero and Nicolas 1987; Ca´ceres and Monteiro-Filho 2001; Ca´ceres et al. 2002). In the intraspecific analyses, both for C. philander and D. aurita, no significant difference was found either in the proportions of arthropod to seeds, or the frequencies of arthropod groups. A similar pattern was found for M. demerarae by Pinheiro et al. (2002), who proposed four hypotheses for explaining it: high constancy of diet; lack of variation in spatio-temporal patterns of resource availability; complex interactions among factors; and the categories used in the analysis (e.g. orders) being quite wide, while the diet may still differ within categories. The same hypotheses, plus the addi-

tional one of limitations of our statistical power due to smaller sample sizes, may apply here. At present, we cannot decide conclusively on which of the above hypotheses may be correct. Diversity of items was significantly greater for M. demerarae and D. aurita when compared with C. philander. The result for M. demerarae was a consequence of this species’ diet being more evenly distributed among many items when compared to C. philander. For D. aurita, on the other hand, the high diversity was a consequence of the large number of different items. Caluromys philander had arthropods as the main item of its diet in fragments of Poc- o das Antas, present in all samples. This result contrasts with this species being regarded as a frugivore–omnivore (Robinson and Redford 1986). Leite et al. (1994, 1996), working in the main forest block of Poc- o das Antas, found fruits in 94.1% of samples and arthropods in 26.5% of them. Our results may reflect an ability of C. philander to change its diet, which can be important for its survival in small forest fragments, where fruiting trees are often scarce due to the open canopy and

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to the scarcity of seed-dispersing vertebrates, whereas arthropods are often abundant due to the high productivity of the edge vegetation. The diet of D. aurita was omnivore, including invertebrates, fruits and vertebrates. Opossums of the genus Didelphis are regarded as the most generalists among the didelphids (Vieira and Astu´a de Moraes 2003) and other studies also describe D. aurita as omnivore (Cordero and Nicolas 1987; Santori et al. 1995; Freitas et al. 1997). Leite et al. (1994) did not find differences in consumption of arthropods and seeds for D. aurita in the main forest block of Poc- o das Antas. In the present study, D. aurita was the species with the greatest frequency of fruits in the diet and had a high richness of items, despite having the smallest sample size. Didelphis aurita is also the species with the largest home range within the marsupials studied (Pires et al. 2002), which allows it to use a great variety of resources. These features of D. aurita’s ecology may contribute to explain its resistance to the fragmentation, as it is able to survive in very small fragments such as the ones we studied. The marsupials studied showed a high degree of dietary overlap; thus, their coexistence in the fragments is not well explained by differences in their diet composition. It is likely that differences in prey sizes, rather than categories, provide some differentiation. We could not evaluate prey size because arthropod orders were usually identified from tiny pieces of maxillae, elytra, legs and so on, from which it is often difficult to find out the size of the insect. However, there is often a correlation between body sizes and prey sizes, as found by Fisher and Dickman (1993a, b) in Australian dasyurid marsupials. Didelphis aurita is our largest species, followed by C. philander and M. demerarae; the ratios among their weights are approximately 10:5:1. Such differences could result in prey size differences large enough to allow coexistence, as suggested by Leite et al. (1994, 1996). However, coexistence of species can be possible even if overlap in some niche dimension is high, provided that there is segregation in other dimensions. In the

present case, coexistence among the three species may indeed be facilitated by vertical differences in habitat use, through preferences for different strata of vegetation. Micoureus demerarae is mostly arboreal, preferring upper and medium strata (Passamani 1995; Grelle 2003; Table 2). Caluromys philander is also an arboreal species, but it uses more the canopy (Charles-Dominique et al. 1981; Stallings 1989; Malcolm 1991; Leite et al. 1994; Julien-Laferrie`re 1995; Grelle 2003; Table 2). Didelphis aurita is classified as a terrestrial or scansorial species (Leite et al. 1994; Grelle 2003;Table 2). Overall, C. philander seems to be mostly arboreal, with M. demerarae intermediate and D. aurita the most terrestrial of the three, a pattern consistent with vertical stratification helping to explain their coexistence. As regards the possible role as seed dispersers, most of the seeds found in the diets of the marsupials studied are of pioneer plants, such as Cecropia spp. and Piper spp. Several studies report the role of didelphid marsupials in seed dispersal (Medellı´ n 1994; Grelle and Garcia 1999; Ca´ceres et al. 1999; Vieira and Izar 1999; Ca´ceres 2002). According to Pires et al. (2002), M. demerarae forms a metapopulation in the Ilhas dos Barbados, and movements of individuals of the other species among fragments have already been detected. As seeds ingested by these marsupials often pass through the digestive tract without damage, these animals can be efficient agents of seed dispersal among fragments and also play an important role

Table 2. Numbers of captures (percentages in parentheses) of Micoureus demerarae, Caluromys philander and Didelphis aurita at traps set at three different heights at Ilhas dos Barbados, Poc- o das Antas Biological Reserve, Brazil, 1995–2003. ‘‘Understory’’ refers to traps set at breast height and ‘‘canopy’’, to traps raised in platforms to the highest foliage stratum (heights 5–15 m).

D. aurita M. demerarae C. philander

Ground

Understory

Canopy

125 (94.0) 460 (39.8) 14 (24.1)

8 (6.0) 629 (54.4) 35 (60.4)

0 67 (5.8) 9 (15.5)

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in forest regeneration in the matrix and fragment edges, where pioneer trees can establish successfully. Besides, marsupials can be pollinators, including the genera Caluromys and Didelphis (Janson et al. 1981; Gribel 1988; Vieira et al. 1991). The pollination and seed dispersal performed by mammals have an important positive effect in the reproductive success of plants (Fleming and Sosa 1994). These processes become especially important in small forest fragments, because many pollinators and seed dispersers are particularly vulnerable to the effects of fragmentation (Murcia 1996). Thus, a better knowledge of dietary ecology of small mammals in fragments may be important to understand not only the ecology of the marsupials themselves but also the processes that contribute to shape the biotic communities in forest fragments.

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Acknowledgements We thank IBAMA for allowing us to work in Poc- o das Antas and providing facilities there. The study also had support from GoldenLion-Tamarin Association. We are deeply indebted to our colleagues from Laboratory of Ecology and Conservation of Populations, UFRJ, for their help in fieldwork and for discussions. P. S. Pinheiro and J. L. Nascimento helped in many aspects of the work with M. demerarae. B. Costa helped identifying the seeds. We thank E. M. Vieira, R. T. Santori and two anonymous referees for their useful criticisms and suggestions. Nils Okun and Sara Beier wrote the abstract in German. The study was funded by Fundac- a˜o O Botica´rio de Protec- a˜o a` Natureza, FAPERJ, CNPq, CAPES and PROBIO (PRONABIO/ MMA).

Zusammenfassung Nahrungsgewohnheiten sympatrischer Opossum-Arten, die in kleinen Waldstu¨cken des atlantischen Regenwaldes in Brasilien vorkommen

Die Nahrungen sympatrischer Opossum-Arten wurde in kleinen atlantischen Waldstu¨cken des Biologischen Reservoirs Poc- o das Antas, Su¨dost Brasilien untersucht. Die von Caluromys philander und Didelphis aurita konsumierten Nahrungsgruppen wurden durch Kot-Analysen untersucht und anschliessend mit der in einer vorhergehenden Studie untersuchten Nahrung von Micoureus demerarae verglichen. Die Hauptnahrungstypen waren bei allen drei Arten athropoden und Fru¨chte, mit einer hohen Diversita¨t innerhalb beider Gruppen. Bei D. aurita fanden sich zudem feine Haare. Die dominierenden Insektenordnungen waren Hymenoptera und Coleoptera. Samen geho¨rten meist zu Pflanzen der Sekunda¨rvegetation, wie Cecropia und Piper. Die Nahrungszusammensetzungen zeigten nur geringe zeitliche und ra¨umliche Variation. Die Arten hatten ein u¨bereinstimmendes Nahrungsspektrum (Ausnahmen: die erho¨hten Anteile der Arachnida und Diplopoda bei D. aurita im Vergleich zu M. demerarae). Die Nahrungsdiversita¨t war bei C. philander geringer als bei den anderen beiden Arten. Die hohe Nahrungsu¨berlappung zwischen den Arten besta¨tigt, dass diese nur geringe Differenzierung in der Nahrung nicht fu¨r eine Koexistenz der drei Arten ausreicht. Eine Koexistenz wird vielmehr mo¨glich durch die vertikale Segregation und/oder durch Unterschiede in der Beutegro¨sse. r 2005 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved.

References Ca´ceres, N. C. (2002): Food habits and seed dispersal by the white-eared opossum, Didelphis albiventris, in southern Brazil. Stud. Neotrop. Fauna Environ. 37, 97–104.

Ca´ceres, N. C.; Dittrich, V. A. O.; Monteiro-Filho, E. L. A. (1999): Fruit consumption, distance of seed dipersal and germination of solanaceous plants ingested by the common opossum

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Authors’ addresses: Fa´bio Martins Vilar de Carvalho and Fernando Antonio dos Santos Fernandez, Departamento de Ecologia, Instituto de Biologia, CxP 68020, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ 21941-590, Brazil (e-mail: [email protected]) Jorge Luiz Nessimian, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ CEP 21941-590, Brazil