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Diet of some species of Neotropical small mammals
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ORIGINAL INVESTIGATION
Diet of some species of Neotropical small mammals Soˆnia A. Talamoni, Denise Couto, Dirceu A. Cordeiro Ju´nior, Fernanda M. Diniz Conservation, Ecology and Behaviour Group, Post-graduate Programme in Vertebrate Zoology, Pontifical Catholic University of Minas Gerais, Pre´dio 41, Dom Jose´ Gaspar, 500, 30535-610 Belo Horizonte, MG , Brazil Received 13 April 2007; accepted 7 September 2007
Abstract Dietary analysis was performed to determine the variations in diet of some small neotropical species of mammals collected in seasonal areas of the cerrado (a savannah-like grassland) and semi-deciduous forest. Food items were determined based on the analysis of stomach contents of 126 animals (one didelphid and five sigmodontine rodent species). Most species presented herbivorous-omnivorous habits, with a preference for the vegetative parts of plants. Akodon montensis Thomas (1913) was the most abundant species in the forest area and demonstrated a uniform consumption of animal and vegetal items through the year, and contained 65.7% plant material in its diet. Necromys lasiurus (Lund, 1841) was the most abundant in the cerrado with 72.6% of vegetation in its diet, but showed a high consumption of animal items during the rainy season. Oligoryzomys nigripes (Olfers, 1818) contained 95.1% of plant material, while Oxymycterus delator (Thomas, 1903) consumed 61.6% invertebrates, mainly insects. The didelphid Philander frenatus (Olfers, 1818) consumed invertebrates (47.7%), small vertebrates (7.3%) and plant material (44.9%). r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. key words: Akodon; Necromys; herbivorous diet; stomach contents
Introduction The eating habits and availability of food resources are essential aspects to understanding populations and communities of mammals, life-history strategies, and ecological roles of animals (DeBlase and Martin 1980; Meserve et al. 1988; Galindo-Leal and Krebs 1998; Martinez et al. 1990). Information about the eating habits of small herbivorous mammals, mainly rodents, is scarce due to their efficient food mastication, which results in small fragments, which are difficult to identify (Hansson 1970). In the Neotropics, some work has been done on food availability as correlated with habitat Corresponding author.
E-mail address: [email protected] (S.A. Talamoni).
(Borchert and Hansen 1983; Martinez et al. 1990; Bergallo and Magnusson 1999), demographic population (Fleming 1971; Gonza´lez et al. 1989; Adler and Beatty 1997; Adler 1998; Bergallo and Magnusson 1999) and the reproductive cycle of those animals (Martino and Aguilera 1989; Bilenca et al. 1992; Suarez 1994). In Brazil, the details of the diet of small mammals is limited to some studies (Leite et al. 1996; Santori et al. 1996, 1997; Talamoni et al. 1999). One problem for diet analysis is that the diets of small mammals have often been studied by the analysis of faeces or stomach contents. Analysis of faeces is highly inaccurate because of differential digestion, and stomach contents analysis requires the sacrifice of large numbers of individuals and cannot be used for some species because of conservation considerations (Kronfeld and Dayan 1998). Thus, the
1616-5047/$ - see front matter r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2007.09.008 Mamm. biol. 73 (2008) 337–341
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S.A. Talamoni et al. / Mamm. biol. 73 (2008) 337–341
animals of this study were also sacrificed for a reproduction study (Couto 2000). The objective of the present work was to determine the diet of some species— Oligoryzomys nigripes (Olfers, 1818), Oryzomys subflavus (Wagner, 1842), Necromys lasiurus (Lund, 1841), Oxymycterus delator (Thomas, 1903), from cerrado (a savannah-like grassland), and Philander frenatus (Olfers, 1818) and Akodon montensis Thomas (1913), from semideciduous forest, both seasonal vegetation types of Brazil, and to contribute to the knowledge of the trophic ecology of Neotropical small mammals.
Material and methods Study site The collection of small mammals was carried out monthly from October 1998 to October 1999, in seasonal semideciduous forest and cerrado areas, in the Serra do Rola-Moc¸a State Park (PERM), in the state of Minas Gerais, Brazil (201030 S, 431570 W). The Park encompasses nearly 9500 ha, with elevations ranging from 1100 to 1400 m above sea level, and a mosaic of different plant communities include semideciduous forest, cerrado and open areas such as high-altitude fields. The cerrado is Brazil’s second largest vegetation formation, and is defined as a xeromorphic vegetation type. The semideciduous forest and cerrado are associated with the occurrence of a very predictable dry season (Eiten 1992). The climate is marked by a rainy summer (October–March) and a dry winter (April–September). Total precipitation in the study area during this work period was 1457 mm, whereas the maximum and minimum temperatures averaged 29.2 and 10.8 1C. December–March were the hottest months, with a mean temperature of 21.3 1C, while June–September were the coldest, with a mean of 16.9 1C.
Sampling Animals were captured using 60 mesh-wire live-traps (30 15 15 cm). Thirty traps were placed in forest areas and 30 in cerrado. The traps were placed on the ground at 15 m intervals, along three lines 20 m apart. During four nights in each month the traps were baited with a mixture of banana and peanut butter and checked the following morning. The skins and skulls of the animals were deposited in the reference collection of the Museum of Natural Science of the Catholic University of Minas Gerais. From a total of 191 individuals captured, only 126 individuals (one didelphid and five rodents species) were studied because they gave sufficient sample sizes. Stomachs contents of Philander frenatus (n ¼ 10) and Akodon montensis (n ¼ 37) captured only in forest and Necromys lasiurus (n ¼ 27), Oryzomys subflavus (n ¼ 14), Oligoryzomys nigripes (n ¼ 22) and Oxymycterus delator (n ¼ 16) captured only in cerrado were analysed.
in ethanol 100%. Due to an initially proposed reproduction study (Couto 2000), the procedure for the capture of animals involved bait. Stomachs with a large amount of bait (up to 40%) and empty stomachs were rejected. For a total stomach contents analysis a small amount of bait may bias results; thus, to estimate the relative abundance of food items, half the stomach contents without bait was homogenised in 5 ml of distilled water and four samples of 1 ml from each stomach were removed and spread on Petri plates. Samples were examined under microscope at 30 magnification, on a grid of 7.5 7.0 cm, with 240 subdivisions of 0.5 cm. All items in intersections of the quadrates were counted and compared with material collected in the study area. Identification of vegetal fragments was facilitated through visualisation of samples under microscope at 100 magnification. These samples were placed on a microscope slide and cleared in Hertwig’s solution, as described in DeBlase and Martin (1980). The remains of chitins, larvae Coleoptera, larvae Lepidoptera, bones, hairs and other fragments were used to identify the animal items. Leaf tissue, unidentified vegetal tissue, root, seed were used to identify the vegetal items; fungi were also considered. The number of counted items, in each food category, was recorded for all stomachs and expressed as a proportion of the total items in all food categories, obtained from the sample of each species (Hyslop 1980). The following food categories were utilised: insects and Araneae (Arachnida), unidentified arthropod, small vertebrates, leaf tissue, unidentified vegetal tissue, root, seed and fungi. For species with continuous capture the w2 test (Zar 1999) was applied to test the hypothesis of no difference between the composition of the diet within the dry and rainy seasons.
Results A great consumption of the vegetative parts of plants was observed, except for P. frenatus and O. delator, where analysis indicated a larger proportion of animal origin (55% and 61.6%, respectively). The consumption of small vertebrates was also observed in P. frenatus (Table 1). Indefinable fungi consumption was observed for A. montensis and O. delator. Animal and vegetal diets of A. montensis, the most captured species in the forest, and N. lasiurus, the most captured in the cerrado (Table 1), are presented in Figure 1. For these species, there was no significant difference between the amount of animal and vegetal items within the rainy and dry seasons (A. montensis, n ¼ 23 in the rain and n ¼ 14 in the dry, w2 ¼ 1.51, p40.05; N. lasiurus, n ¼ 15 in the rain and n ¼ 12 in the dry, w2 ¼ 0.66, p40.05). It was found 65.7% of vegetal items on the diet of A. montensis and 72.6% on diet of N. lasiurus. O. nigripes presented 95.1% of vegetal items on its diet (Table 1).
Diet analysis
Discussion
The stomachs were removed and fixed in ethanol 100%. After fixation, their contents were washed, filtered and fixed once again
Most rodents showed a herbivorous–omnivorous diet; however, O. delator was considered mainly
ARTICLE IN PRESS S.A. Talamoni et al. / Mamm. biol. 73 (2008) 337–341
339
Table 1. Number and percentage, in brackets, of animal and vegetal food items, considering total items observed in stomach contents of small mammals caught in seasonal semideciduous forest (Fo) and cerrado (Ce), from October 1998 through October 1999, in the PERM, Brazil Species (area, n)
P. frenatus (Fo, n ¼ 10) Ol. nigripes (Ce, n ¼ 22) Or. subflavus (Ce, n ¼ 14) A. montensis(Fo, n ¼ 37) N. lasiurus (Ce, n ¼ 27) Ox. delator (Ce, n ¼ 16) a
Animal items
Vegetal items
Invertebratea
Vertebrateb
Total animal
209 [47.7]
32 [7.3]
241 [55]
Unidentified vegetal tissue
Fungi
Total items
Leaf tissue
Root
Seed
Total vegetal
75 [17.1]
34 [7.7]
35 [7.9]
53 [12.1]
197 [44.9]
–
438
42 [17]
21 [8.5]
235 [95.1]
–
247
12 [4.9]
–
12 [4.9]
105 [42.5]
67 [27.1]
104 [36.4]
–
104 [36.4]
110 [38.4]
43 [15]
7 [2.4]
22 [7.6]
182 [63.6]
–
286
218 [34.3]
–
218 [34.3]
255 [40.1]
70 [11]
11 [1.7]
82 [12.9]
418 [65.7]
29[4.4]
636
96 [27.3]
–
96 [27.3]
126 [35.8]
34 [9.6]
24 [6.8]
71 [20.2]
255 [72.6]
–
351
180 [61.6]
–
180 [61.6]
58 [19.8]
27 [9.2]
10 [3.4]
17 [5.8]
112 [37.2]]
9[2.9]
301
Unidentified arthropod; insects; araneae. Small vertebrate (feather, muscle).
b
Vegetal diet
100
Animal diet 80
%
60 40 20 0 Oct/Nov Dec/Jan Feb/Mar Apr/May Jun/Jul 120 100
%
80 60 40 20 0 Oct/Nov
Dec/Jan
Apr/May
Jun/Jul
Aug/Sep
Oct
Months
Figure. 1. Proportion of animal and vegetal diet of Akodon montensis in semideciduous forest (A) and of Necromys lasiurus in cerrado (B) from October 1998 through October 1999, in the PERM, Brazil.
insectivorous–omnivorous. The consumption of invertebrates in a greater proportion (70%), besides seeds and vegetal tissue, was previously observed in Oxymycterus roberti (Thomas, 1901) (Borchert and Hansen 1983) and Oxymycterus rutilans (Olfers, 1818) (Suarez 1994). In relation to P. frenatus, despite its omnivorous diet, it was observed to have a greater consumption of animal items, including the consumption of small vertebrates. These results are in accordance with Santori et al.
(1997), who reported the consumption of small vertebrates and invertebrates as the main items. The carnivorous tendency of this species based on experimental analysis of assimilation and digestive efficiency was suggested by Santori et al. (1995). Among the species analysed in this work, O. nigripes showed a higher consumption of vegetal items, indicating a tendency to a strict herbivore diet, which is in concordance with Meserve et al. (1988), and with Ellis et al. (1998) for other species of the genus. Akodon montensis demonstrated a uniform consumption of animal and vegetal items throughout the year. This information characterises omnivorous animals, as observed in other species of Akodon, which tend to present different proportions of arthropods, seeds and fruits in their diet (Meserve et al. 1988; Martinez et al. 1990). The results for A. montensis suggested that the items of animal origin, especially insects, were important resources. In tropical areas insect abundance changes during the year, being greater during the rainy season (Smythe 1982); thus, the relatively high consumption of this item during the dry season may indicate an active search of this resource during this period. In Argentina, a relative entomophagous habit was also observed for Akodon azarae (J. Fischer, 1829), and this tendency was more pronounced in autumn and winter (dry seasons in Brazil) (Ellis et al. 1998). Akodon montensis showed a seasonal annual reproductive cycle, with the reproductive activity mainly occurring during the rainy season, while most individuals of A. montensis captured in the dry season were sub-adults (Couto and Talamoni 2005). In an agriculture area of the Argentine pampas a high insect consumption rate was registered by reproductively active individuals of A. azarae (Bilenca et al. 1992). Correlation between reproductive activity and
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ingestion of animal items was observed in Oryzomys capito (Olfers, 1818) and Proechimys cuvieri (Petter, 1978) in French Guiana (Henry 1997). Necromys lasiurus clearly showed a high consumption of animal items during the rainy season, decreasing during the dry period, when there was an increase in vegetal items, which indicates an opportunist feeding behaviour in relation to the abundance of food resource in the environment. This pattern is in concordance with the observations of Meserve et al. (1988) in species of small mammals in the Chilean temperate rainforest, where the animals widely used food resources in relation to their availability. Pronounced entomophagy in summer (December–February) was also observed for Bolomys ( ¼ Necromys) obscurus in Argentina (Ellis et al. 1998). In this study, all stomach contents analysed belong to reproductively active individuals (Couto and Talamoni 2005). The dietary variation observed can be attributed to different physiological requirements of the individuals and animal groups. Therefore, studies on populations associated with dietary analysis and food resources availability may facilitate the understanding of population changes, reproductive strategies as well as the dispersion pattern of these animals.
Acknowledgements We thank IBAMA for the licence to capture animals (098/99-NUFAS MG); the Sanitation Company of Minas Gerais (COPASA) for their permission to collect in the APE Mutuca; Joa˜o A. de Oliveira, from the Museu Nacional do Rio de Janeiro, for the identification of Oxymycterus delator, and to A. Linghorn for English revision. FIP-PUC Minas provided financial support.
Zusammenfassung Nahrungsanalysen einiger kleiner neotropischer Sa¨ugetiere Zum Studium der Variation der Erna¨hrung wurden neotropische Kleinsa¨uger untersucht, die im Cerrado (Savannen-a¨hnliche Landschaft) und halb-immergru¨nen Waldzonen leben. Der Mageninhalt von 126 Tieren (eine Beutelratte und fu¨nf Nagetierarten der Unterfamilie Sigmodontinae) wurde untersucht und identifiziert. Die Arten waren teilweise als Herbivore, teils als Omnivore zu bezeichnen, doch zogen sie vegetative Pflanzenteile als Nahrung vor. Im Wald war Akodon montensis Thomas (1913) die ha¨ufigste Art. Sie konsumierte im Laufes des Jahres tierisches und pflanzliches Futter recht gleichma¨ssig, doch machten Pflanzenteile
etwa 65,7% der Nahrung aus. Necromys lasiurus (Lund, 1841) war die ha¨ufigste Art im Cerrado, mit 72,6% pflanzlichen Bestandteilen der Nahrung. Wa¨hrend der Regenzeit nahm sie aber einen grossen Anteil tierischer Nahrung auf. Die Nahrung von Oligoryzomys nigripes (Olfers, 1818) umfasste 95,1% pflanzliches Material, wa¨hrend die Nahrung von Oxymycterus delator (Thomas, 1903) 61,6% wirbellose Tiere beinhaltete, wobei Insekten u¨berwogen. Die Beutelratte Philander frenatus (Olfers, 1818) konsumierte Wirbellose (47,7%), kleine Wirbeltiere (7,3%) und Pflanzen (44,9%).
References Adler, G.H., 1998. Impacts of resource abundance on populations of a tropical forest rodent. Ecology 79, 242–254. Adler, G.H., Beatty, R.P., 1997. Changing reproductive rates in a Neotropical forest rodent, Proechimys semispinosus. J. Anim. Ecol. 66, 472–480. Bergallo, H.G., Magnusson, W.E., 1999. Effects of climate and food availability on four species in southeastern Brazil. J. Mammal. 80, 472–486. Bilenca, D.N., Kravetz, F.O., Zuleta, G.A., 1992. Food habits of Akodon azarae and Calomys laucha (Cricetidae, Rodentia) in agroecosystems of Central Argentina. Mammalia 56, 371–383. Borchert, M., Hansen, R.L., 1983. Effects of flooding and wildfire on valley side wet campo rodents in Central Brazil. Rev. Brasil. Biol. 43, 229–240. Couto, D., 2000. Reproduction condition of small mammals of cerrado and forest in a special protection area in the southeastern Brazil. Master Thesis, Pontificia Universidade Cato´lica de Minas Gerais, Belo Horizonte. Couto, D., Talamoni, S.A., 2005. Reproductive condition of Akodon montensis Thomas and Bolomys lasiurus (Lund) (Rodentia, Muridae) based on histological and histometric analyses of testes and external characteristics of gonads. Acta Zool. 86, 111–118. DeBlase, A.F., Martin, R.E., 1980. A Manual of Mammalogy With Keys to Families of the World. Wm. C. Brown Company Publishers, Dubuque, IA. Eiten, G., 1992. Natural Brazilian vegetation types and their causes. An. Acad. Bras. Cieˆn. 64, 35–65. Ellis, B.A., Mills, J.N., Glass, G.E., McKee Jr., K.T., Enria, D.A., Childs, J.E., 1998. Dietary habits of the common rodents in an agroecosystem in Argentina. J. Mammal. 79, 1203–1220. Fleming, T.H., 1971. Population Ecology of Three Species of Neotropical Rodents, vol.143. University of Michigan. Miscellaneous Publications of Museum of Zoology, pp. 1–77. Galindo-Leal, C., Krebs, C.J., 1998. Effects of food abundance on individuals and populations of the rock mouse (Peromyscus difficilis). J. Mammal. 79, 1131–1142. Gonza´lez, L., Muru´a, R., Jofre´, C., 1989. The effect of seed availability on population density of Oryzomys in Southern Chile. J. Mammal. 70, 401–403.
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Hansson, L., 1970. Methods of morphological diet microanalysis in rodents. Oikos 21, 255–266. Henry, O., 1997. The influence of sex and reproductive state on diet preference in four terrestrial mammals of the French Guianan rain forest. Can. J. Zool. 75, 929–935. Hyslop, E.J., 1980. Stomach contents analysis – a review of methods and their application. J. Fish Biol. 17, 411–429. Kronfeld, N., Dayan, T., 1998. A new method of determining diets of rodents. J. Mammal. 79, 1198–1202. Leite, Y.L.R., Costa, L.P., Stallings, J.R., 1996. Diet and vertical space use of three sympatric opossums in a Brazilian Atlantic forest reserve. J. Trop. Ecol. 12, 435–440. Martinez, R.L., Bocco, M.E., Mo´naco, N., Polop, J., 1990. Winter diet in Akodon dolores Thomas, 1916. Mammalia 54, 197–205. Martino, A.M.G., Aguilera, M., 1989. Food habits of Holochilus venezuelae in rice fields. Mammalia 53, 545–561. Meserve, P.L., Lang, B.K., Patterson, B.D., 1988. Trophic relationships of small mammals in a Chilean temperate rainforest. J. Mammal. 69, 721–730. Santori, R.T., Cerqueira, R., Kleske, C.C., 1995. Digestive anatomy and efficiency of Dedelphis aurita and Philander
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www.elsevier.de/mambio
ORIGINAL INVESTIGATION
Diet of some species of Neotropical small mammals Soˆnia A. Talamoni, Denise Couto, Dirceu A. Cordeiro Ju´nior, Fernanda M. Diniz Conservation, Ecology and Behaviour Group, Post-graduate Programme in Vertebrate Zoology, Pontifical Catholic University of Minas Gerais, Pre´dio 41, Dom Jose´ Gaspar, 500, 30535-610 Belo Horizonte, MG , Brazil Received 13 April 2007; accepted 7 September 2007
Abstract Dietary analysis was performed to determine the variations in diet of some small neotropical species of mammals collected in seasonal areas of the cerrado (a savannah-like grassland) and semi-deciduous forest. Food items were determined based on the analysis of stomach contents of 126 animals (one didelphid and five sigmodontine rodent species). Most species presented herbivorous-omnivorous habits, with a preference for the vegetative parts of plants. Akodon montensis Thomas (1913) was the most abundant species in the forest area and demonstrated a uniform consumption of animal and vegetal items through the year, and contained 65.7% plant material in its diet. Necromys lasiurus (Lund, 1841) was the most abundant in the cerrado with 72.6% of vegetation in its diet, but showed a high consumption of animal items during the rainy season. Oligoryzomys nigripes (Olfers, 1818) contained 95.1% of plant material, while Oxymycterus delator (Thomas, 1903) consumed 61.6% invertebrates, mainly insects. The didelphid Philander frenatus (Olfers, 1818) consumed invertebrates (47.7%), small vertebrates (7.3%) and plant material (44.9%). r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. key words: Akodon; Necromys; herbivorous diet; stomach contents
Introduction The eating habits and availability of food resources are essential aspects to understanding populations and communities of mammals, life-history strategies, and ecological roles of animals (DeBlase and Martin 1980; Meserve et al. 1988; Galindo-Leal and Krebs 1998; Martinez et al. 1990). Information about the eating habits of small herbivorous mammals, mainly rodents, is scarce due to their efficient food mastication, which results in small fragments, which are difficult to identify (Hansson 1970). In the Neotropics, some work has been done on food availability as correlated with habitat Corresponding author.
E-mail address: [email protected] (S.A. Talamoni).
(Borchert and Hansen 1983; Martinez et al. 1990; Bergallo and Magnusson 1999), demographic population (Fleming 1971; Gonza´lez et al. 1989; Adler and Beatty 1997; Adler 1998; Bergallo and Magnusson 1999) and the reproductive cycle of those animals (Martino and Aguilera 1989; Bilenca et al. 1992; Suarez 1994). In Brazil, the details of the diet of small mammals is limited to some studies (Leite et al. 1996; Santori et al. 1996, 1997; Talamoni et al. 1999). One problem for diet analysis is that the diets of small mammals have often been studied by the analysis of faeces or stomach contents. Analysis of faeces is highly inaccurate because of differential digestion, and stomach contents analysis requires the sacrifice of large numbers of individuals and cannot be used for some species because of conservation considerations (Kronfeld and Dayan 1998). Thus, the
1616-5047/$ - see front matter r 2007 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2007.09.008 Mamm. biol. 73 (2008) 337–341
ARTICLE IN PRESS 338
S.A. Talamoni et al. / Mamm. biol. 73 (2008) 337–341
animals of this study were also sacrificed for a reproduction study (Couto 2000). The objective of the present work was to determine the diet of some species— Oligoryzomys nigripes (Olfers, 1818), Oryzomys subflavus (Wagner, 1842), Necromys lasiurus (Lund, 1841), Oxymycterus delator (Thomas, 1903), from cerrado (a savannah-like grassland), and Philander frenatus (Olfers, 1818) and Akodon montensis Thomas (1913), from semideciduous forest, both seasonal vegetation types of Brazil, and to contribute to the knowledge of the trophic ecology of Neotropical small mammals.
Material and methods Study site The collection of small mammals was carried out monthly from October 1998 to October 1999, in seasonal semideciduous forest and cerrado areas, in the Serra do Rola-Moc¸a State Park (PERM), in the state of Minas Gerais, Brazil (201030 S, 431570 W). The Park encompasses nearly 9500 ha, with elevations ranging from 1100 to 1400 m above sea level, and a mosaic of different plant communities include semideciduous forest, cerrado and open areas such as high-altitude fields. The cerrado is Brazil’s second largest vegetation formation, and is defined as a xeromorphic vegetation type. The semideciduous forest and cerrado are associated with the occurrence of a very predictable dry season (Eiten 1992). The climate is marked by a rainy summer (October–March) and a dry winter (April–September). Total precipitation in the study area during this work period was 1457 mm, whereas the maximum and minimum temperatures averaged 29.2 and 10.8 1C. December–March were the hottest months, with a mean temperature of 21.3 1C, while June–September were the coldest, with a mean of 16.9 1C.
Sampling Animals were captured using 60 mesh-wire live-traps (30 15 15 cm). Thirty traps were placed in forest areas and 30 in cerrado. The traps were placed on the ground at 15 m intervals, along three lines 20 m apart. During four nights in each month the traps were baited with a mixture of banana and peanut butter and checked the following morning. The skins and skulls of the animals were deposited in the reference collection of the Museum of Natural Science of the Catholic University of Minas Gerais. From a total of 191 individuals captured, only 126 individuals (one didelphid and five rodents species) were studied because they gave sufficient sample sizes. Stomachs contents of Philander frenatus (n ¼ 10) and Akodon montensis (n ¼ 37) captured only in forest and Necromys lasiurus (n ¼ 27), Oryzomys subflavus (n ¼ 14), Oligoryzomys nigripes (n ¼ 22) and Oxymycterus delator (n ¼ 16) captured only in cerrado were analysed.
in ethanol 100%. Due to an initially proposed reproduction study (Couto 2000), the procedure for the capture of animals involved bait. Stomachs with a large amount of bait (up to 40%) and empty stomachs were rejected. For a total stomach contents analysis a small amount of bait may bias results; thus, to estimate the relative abundance of food items, half the stomach contents without bait was homogenised in 5 ml of distilled water and four samples of 1 ml from each stomach were removed and spread on Petri plates. Samples were examined under microscope at 30 magnification, on a grid of 7.5 7.0 cm, with 240 subdivisions of 0.5 cm. All items in intersections of the quadrates were counted and compared with material collected in the study area. Identification of vegetal fragments was facilitated through visualisation of samples under microscope at 100 magnification. These samples were placed on a microscope slide and cleared in Hertwig’s solution, as described in DeBlase and Martin (1980). The remains of chitins, larvae Coleoptera, larvae Lepidoptera, bones, hairs and other fragments were used to identify the animal items. Leaf tissue, unidentified vegetal tissue, root, seed were used to identify the vegetal items; fungi were also considered. The number of counted items, in each food category, was recorded for all stomachs and expressed as a proportion of the total items in all food categories, obtained from the sample of each species (Hyslop 1980). The following food categories were utilised: insects and Araneae (Arachnida), unidentified arthropod, small vertebrates, leaf tissue, unidentified vegetal tissue, root, seed and fungi. For species with continuous capture the w2 test (Zar 1999) was applied to test the hypothesis of no difference between the composition of the diet within the dry and rainy seasons.
Results A great consumption of the vegetative parts of plants was observed, except for P. frenatus and O. delator, where analysis indicated a larger proportion of animal origin (55% and 61.6%, respectively). The consumption of small vertebrates was also observed in P. frenatus (Table 1). Indefinable fungi consumption was observed for A. montensis and O. delator. Animal and vegetal diets of A. montensis, the most captured species in the forest, and N. lasiurus, the most captured in the cerrado (Table 1), are presented in Figure 1. For these species, there was no significant difference between the amount of animal and vegetal items within the rainy and dry seasons (A. montensis, n ¼ 23 in the rain and n ¼ 14 in the dry, w2 ¼ 1.51, p40.05; N. lasiurus, n ¼ 15 in the rain and n ¼ 12 in the dry, w2 ¼ 0.66, p40.05). It was found 65.7% of vegetal items on the diet of A. montensis and 72.6% on diet of N. lasiurus. O. nigripes presented 95.1% of vegetal items on its diet (Table 1).
Diet analysis
Discussion
The stomachs were removed and fixed in ethanol 100%. After fixation, their contents were washed, filtered and fixed once again
Most rodents showed a herbivorous–omnivorous diet; however, O. delator was considered mainly
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339
Table 1. Number and percentage, in brackets, of animal and vegetal food items, considering total items observed in stomach contents of small mammals caught in seasonal semideciduous forest (Fo) and cerrado (Ce), from October 1998 through October 1999, in the PERM, Brazil Species (area, n)
P. frenatus (Fo, n ¼ 10) Ol. nigripes (Ce, n ¼ 22) Or. subflavus (Ce, n ¼ 14) A. montensis(Fo, n ¼ 37) N. lasiurus (Ce, n ¼ 27) Ox. delator (Ce, n ¼ 16) a
Animal items
Vegetal items
Invertebratea
Vertebrateb
Total animal
209 [47.7]
32 [7.3]
241 [55]
Unidentified vegetal tissue
Fungi
Total items
Leaf tissue
Root
Seed
Total vegetal
75 [17.1]
34 [7.7]
35 [7.9]
53 [12.1]
197 [44.9]
–
438
42 [17]
21 [8.5]
235 [95.1]
–
247
12 [4.9]
–
12 [4.9]
105 [42.5]
67 [27.1]
104 [36.4]
–
104 [36.4]
110 [38.4]
43 [15]
7 [2.4]
22 [7.6]
182 [63.6]
–
286
218 [34.3]
–
218 [34.3]
255 [40.1]
70 [11]
11 [1.7]
82 [12.9]
418 [65.7]
29[4.4]
636
96 [27.3]
–
96 [27.3]
126 [35.8]
34 [9.6]
24 [6.8]
71 [20.2]
255 [72.6]
–
351
180 [61.6]
–
180 [61.6]
58 [19.8]
27 [9.2]
10 [3.4]
17 [5.8]
112 [37.2]]
9[2.9]
301
Unidentified arthropod; insects; araneae. Small vertebrate (feather, muscle).
b
Vegetal diet
100
Animal diet 80
%
60 40 20 0 Oct/Nov Dec/Jan Feb/Mar Apr/May Jun/Jul 120 100
%
80 60 40 20 0 Oct/Nov
Dec/Jan
Apr/May
Jun/Jul
Aug/Sep
Oct
Months
Figure. 1. Proportion of animal and vegetal diet of Akodon montensis in semideciduous forest (A) and of Necromys lasiurus in cerrado (B) from October 1998 through October 1999, in the PERM, Brazil.
insectivorous–omnivorous. The consumption of invertebrates in a greater proportion (70%), besides seeds and vegetal tissue, was previously observed in Oxymycterus roberti (Thomas, 1901) (Borchert and Hansen 1983) and Oxymycterus rutilans (Olfers, 1818) (Suarez 1994). In relation to P. frenatus, despite its omnivorous diet, it was observed to have a greater consumption of animal items, including the consumption of small vertebrates. These results are in accordance with Santori et al.
(1997), who reported the consumption of small vertebrates and invertebrates as the main items. The carnivorous tendency of this species based on experimental analysis of assimilation and digestive efficiency was suggested by Santori et al. (1995). Among the species analysed in this work, O. nigripes showed a higher consumption of vegetal items, indicating a tendency to a strict herbivore diet, which is in concordance with Meserve et al. (1988), and with Ellis et al. (1998) for other species of the genus. Akodon montensis demonstrated a uniform consumption of animal and vegetal items throughout the year. This information characterises omnivorous animals, as observed in other species of Akodon, which tend to present different proportions of arthropods, seeds and fruits in their diet (Meserve et al. 1988; Martinez et al. 1990). The results for A. montensis suggested that the items of animal origin, especially insects, were important resources. In tropical areas insect abundance changes during the year, being greater during the rainy season (Smythe 1982); thus, the relatively high consumption of this item during the dry season may indicate an active search of this resource during this period. In Argentina, a relative entomophagous habit was also observed for Akodon azarae (J. Fischer, 1829), and this tendency was more pronounced in autumn and winter (dry seasons in Brazil) (Ellis et al. 1998). Akodon montensis showed a seasonal annual reproductive cycle, with the reproductive activity mainly occurring during the rainy season, while most individuals of A. montensis captured in the dry season were sub-adults (Couto and Talamoni 2005). In an agriculture area of the Argentine pampas a high insect consumption rate was registered by reproductively active individuals of A. azarae (Bilenca et al. 1992). Correlation between reproductive activity and
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ingestion of animal items was observed in Oryzomys capito (Olfers, 1818) and Proechimys cuvieri (Petter, 1978) in French Guiana (Henry 1997). Necromys lasiurus clearly showed a high consumption of animal items during the rainy season, decreasing during the dry period, when there was an increase in vegetal items, which indicates an opportunist feeding behaviour in relation to the abundance of food resource in the environment. This pattern is in concordance with the observations of Meserve et al. (1988) in species of small mammals in the Chilean temperate rainforest, where the animals widely used food resources in relation to their availability. Pronounced entomophagy in summer (December–February) was also observed for Bolomys ( ¼ Necromys) obscurus in Argentina (Ellis et al. 1998). In this study, all stomach contents analysed belong to reproductively active individuals (Couto and Talamoni 2005). The dietary variation observed can be attributed to different physiological requirements of the individuals and animal groups. Therefore, studies on populations associated with dietary analysis and food resources availability may facilitate the understanding of population changes, reproductive strategies as well as the dispersion pattern of these animals.
Acknowledgements We thank IBAMA for the licence to capture animals (098/99-NUFAS MG); the Sanitation Company of Minas Gerais (COPASA) for their permission to collect in the APE Mutuca; Joa˜o A. de Oliveira, from the Museu Nacional do Rio de Janeiro, for the identification of Oxymycterus delator, and to A. Linghorn for English revision. FIP-PUC Minas provided financial support.
Zusammenfassung Nahrungsanalysen einiger kleiner neotropischer Sa¨ugetiere Zum Studium der Variation der Erna¨hrung wurden neotropische Kleinsa¨uger untersucht, die im Cerrado (Savannen-a¨hnliche Landschaft) und halb-immergru¨nen Waldzonen leben. Der Mageninhalt von 126 Tieren (eine Beutelratte und fu¨nf Nagetierarten der Unterfamilie Sigmodontinae) wurde untersucht und identifiziert. Die Arten waren teilweise als Herbivore, teils als Omnivore zu bezeichnen, doch zogen sie vegetative Pflanzenteile als Nahrung vor. Im Wald war Akodon montensis Thomas (1913) die ha¨ufigste Art. Sie konsumierte im Laufes des Jahres tierisches und pflanzliches Futter recht gleichma¨ssig, doch machten Pflanzenteile
etwa 65,7% der Nahrung aus. Necromys lasiurus (Lund, 1841) war die ha¨ufigste Art im Cerrado, mit 72,6% pflanzlichen Bestandteilen der Nahrung. Wa¨hrend der Regenzeit nahm sie aber einen grossen Anteil tierischer Nahrung auf. Die Nahrung von Oligoryzomys nigripes (Olfers, 1818) umfasste 95,1% pflanzliches Material, wa¨hrend die Nahrung von Oxymycterus delator (Thomas, 1903) 61,6% wirbellose Tiere beinhaltete, wobei Insekten u¨berwogen. Die Beutelratte Philander frenatus (Olfers, 1818) konsumierte Wirbellose (47,7%), kleine Wirbeltiere (7,3%) und Pflanzen (44,9%).
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