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Variation in the food-niche width of Gracilinanus microtarsus (Didelphimorphia: Didelphidae) in a cerrado remnant in south-eastern Brazil
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Variation in the food-niche width of Gracilinanus microtarsus (Didelphimorphia: Didelphidae) in a cerrado remnant in south-eastern Brazil By E.G. Martins, V. Bonato, A. Pinheiro and S.F. dos Reis Programa de Po´s-graduac- a˜o em Ecologia, Universidade Estadual de Campinas, Campinas, Brazil; Instituto de Matema´tica, Estatı´stica e Computac- a˜o Cientı´fica, Universidade Estadual de Campinas, Campinas, Brazil; and Instituto de Cieˆncias Biolo´gicas, Centro Regional Universita´rio Espı´rito Santo do Pinhal, Espı´rito Santo do Pinhal, Brazil Receipt of Ms. 6.4.2005 Acceptance of Ms. 1.3.2006
Key words: gracile mouse opossum, feeding ecology, intrapopulation variation
The gracile mouse opossum Gracilinanus microtarsus is a small (20–45 g), sexually dimorphic (males 30–45 g; females 20–30 g), short-lived (1.0–1.5 years), solitary, arboreal, nocturnal didelphid marsupial (Emmons and Feer 1997; Eisenberg and Redford 2000; Martins et al. 2006a). This species occurs in a range of habitats including the cerrado (Emmons and Feer 1997; Gargaglioni et al. 1998; Eisenberg and Redford 2000), a complex of five vegetation physiognomies and one of the most important terrestrial hotspots of diversity in the world (Oliveira-Filho and Ratter 2002; Silva and Bates 2002). Climate in the cerrado is highly seasonal (Silva and Bates 2002) and affects the temporal and spatial dynamics of plant flowering and fruiting (Batalha and Martins 2004) and abundance of insects (Pinheiro et al. 2002; V. Bonato, unpubl. data); the latter represent the most frequent food resources in the diet of G. microtarsus (Martins and Bonato 2004; Martins et al. 2006b). In the cerrado, particularly in the physiognomy known as cerrada˜o, G. microtarsus occurs at high population densities and its reproduction occurs in the warm–wet season,
with males suffering high mortality rates afterwards (Martins et al. 2006a, c). These findings show that the life history of G. microtarsus is strongly influenced by seasonality and, therefore, we expect the consumption of food resources to be equally influenced. Additionally, we expect the consumption of food resources to be influenced by sex since sexual size dimorphism and its correlates, such as energetic requirements and foraging behaviours, may differentially affect food consumption by males and females (Shine 1989). Here, we ask if sex and seasonality are factors that contribute significantly for intrapopulation variation in the food-niche width of G. microtarsus. This study was done from January to December 2001 at the Clube Na´utico Araraquara (211430 S, 481010 W), located in Ame´rico Brasiliense, approximately 300 km northwest of Sa˜o Paulo city in south-eastern Brazil. The Clube Na´utico Araraquara has two remnants of cerrada˜o (ca. 73 and 307 ha), a physiognomy of the cerrado characterized by dense forest with tall trees and a completely closed canopy (Oliveira-Filho and Ratter 2002; Silva and Bates 2002). The climate of the
1616-5047/$ - see front matter r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2006.03.001 Mamm. biol. 71 (2006) 5 304–308
ARTICLE IN PRESS Variation in the food-niche width of Gracilinanus microtarsus
region has two well-defined seasons, namely, a warm–wet season from October to March and a cool–dry season from April to September (Tolentino 1967; Primavesi et al. 1999). Trapping was done on two consecutive nights every 15 days from January to December 2001, for a total of 23 sampling occasions and 46 days of fieldwork. The animals were captured in the smaller cerrada˜o remnant (ca. 73 ha) using a 7 7 trapping grid with 49 trapping stations located 10 m from each other. A single Sherman live-trap (dimensions 7.5 9.0 23.5 cm) was set on trees at each trapping station ca. 1.75 m above ground and baited with banana, peanut butter and cod-liver oil. Individuals captured were marked with a numbered leg-band and their sex and age were recorded. Age was determined based primarily on the sequence of tooth eruption and individuals were recorded as adults when all of the teeth had erupted (Costa et al. 2003). One hundred and forty-six faeces (100 from males and 46 from females) were sampled from 38 adult individuals of G. microtarsus (25 males and 13 females) and preserved in 70% ethanol. Of the total number of faeces, 51 were sampled in the warm–wet season and 95 were sampled in the cool–dry season. Description of the procedures of identification of food items detected in the faeces of G. microtarsus as well as detailed information on diet composition can be found in Martins et al. (2006b). Food-niche widths of males and females were measured for each trimester of the year 2001 (two corresponding to the warm–wet season: January–March and October–December; two corresponding to the cool–dry season: April–June and July–September) with the Shannon–Wiener index of diversity (Colwell and Futuyma 1971; Krebs 1989) X H ij ¼ pðij Þ;k log pðijÞ;k , k
where H is the Shannon–Wiener index of diversity (niche width), pðij Þ;k is the frequency of occurrence of the food resource k found in the faeces of sex i in trimester j. The Shannon–Wiener index can assume values ranging from 0 to N. To standardize the index on a scale ranging from 0 to 1, the
305
observed Shannon–Wiener index, H, was divided by log k (Krebs 1989), where k was the total number of food resources detected in the faeces of G. microtarsus. Sampling error estimates for indices of niche width can be obtained using Taylor series expansions (Manly 1985), which hold for symmetrical indices and large sample sizes. Because of the asymmetric nature of the Shannon–Wiener index and the small sample size obtained in this study, 10,000 non-parametric bootstrap resamplings were used to calculate the confidence limits, i.e., 2.5 and 97.5 percentiles (Efron and Tibshirani 1993; Davison and Hinkley 1997). The non-parametric bootstrap resamplings were done in Matlab code. The average food-niche width of males was broader in the trimesters corresponding to the cool–dry season than in those corresponding to the warm–wet season. In contrast, the average food-niche width of females was narrower in the trimesters corresponding to the cool–dry season than in those corresponding to the warm–wet season. Within each sex, the average food-niche widths across trimesters were not significantly different. Between sexes, the average food-niche widths were similar in the trimesters corresponding to the warm–wet season, but were significantly different in the trimesters corresponding to the cool–dry season (Fig. 1). Our results showed that males and females of G. microtarsus had similar food-niche widths in the warm–wet season, when insects are abundant in the cerrado (Pinheiro et al. 2002; V. Bonato, unpubl. data). On the other hand, in the cool–dry season when insects are less abundant (Pinheiro et al. 2002; V. Bonato, unpubl. data), food-niche width between males and females diverged becoming broader in the former and narrower in the latter. This implies, as inferred from the Shannon– Wiener index (Krebs 1989), that food resource consumption in males becomes more even, i.e. more diverse, than that of females in the cool–dry season. A question that arises from these results is why the food-niche width increases in males and decreases in females in the cool–dry season, when insect abundance is low. A likely explanation may be the differences in the patterns of space use between sexes since
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Fig. 1. Shannon–Wiener indices of food-niche width in Gracilinanus microtarsus by sex and trimester. Upper and lower limits of the 95% confidence intervals are a bootstrapped estimate of the variability in the measure associated with sampling errors. Solid line and filled box: males; dashed line and open circle: females.
it is well established that available food is usually proportional to area traversed by individuals (McNab 1963; Schoener 1969, 1971). Males in G. microtarsus traverse large areas having home ranges on average twice as large as that of females (E. G. Martins, unpubl. data). It is, therefore, not unexpected that males have higher probabilities of finding more food and thus maintaining or increasing the diversity of food resources consumed in the cool–dry season. However, in spite of males traversing larger areas than do females, food-niche width was very similar between the sexes in the warm–wet season. This similarity may be attributable to the high abundance of food resources in this season in the cerrado (Pinheiro et al. 2002; V. Bonato, unpubl. data), providing the same diversity of food resources for both sexes, regardless of their relative movements. Finally, it is worth noticing that the observed pattern of variation in food-niche width of males but not that of females of G. microtarsus follows a classic tenet of optimal foraging theory, which predicts a broadening of food-niche width under conditions of food limitation (Stephens and Krebs 1986; Gray
1987). The fact that this prediction does not apply equally to males and females of G. microtarsus is not surprising because optimal foraging theory is based upon the assumption that individuals or classes of individuals within a population are ecologically equivalent (Stephens and Krebs 1986; Perry and Pianka 1997). Our results thus make evident that there is significant intrapopulation variation in the food-niche of G. microtarsus and that individuals of different sexes cannot be treated as ecologically equivalent.
Acknowledgements We are deeply indebted to E. L. A. Monteiro Filho, G. Machado, C. A. Magalha˜es, J. Semir, J. Y. Tamashiro, S. U. Neto, V. E. Molina, N. E. Oliveira and A. P. P. Gouveia for helping at different stages of this work and to P. R. Guimara˜es Jr., M. S. Arau´jo, J. A. F. Diniz Filho and S. Hyslop for their comments on the manuscript. This work was funded by the Fundac- a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo, FAPESP, Brazil.
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307
References Batalha, M. A.; Martins, F. R. (2004): Reproductive phenology of the cerrado plant community in Emas National Park (central Brazil). Aust. J. Bot. 52, 149–161. Colwell, R. K.; Futuyma, D. J. (1971): On the measurement of niche breadth and overlap. Ecology 52, 567–576. Costa, L. P.; Leite, Y. L. R.; Patton, J. L. (2003): Phylogeography and systematic notes on two species of gracile mouse opossums, genus Gracilinanus (Marsupialia: Didelphidae) from Brazil. P. Biol. Soc. Washington 116, 275–292. Davison, A. C.; Hinkley, D. V. (1997): Bootstrap Methods and their Application. Cambridge: Cambridge University Press. Efron, B.; Tibshirani, R. J. (1993): An Introduction to Bootstrap. New York: Chapman & Hall. Eisenberg, J. F.; Redford, K. H. (2000): . Mammals of the Neotropics: The Central Neotropics. Vol. 3. Chicago: University of Chicago Press. Emmons, L. H.; Feer, F. (1997): Neotropical Rainforest Mammals: A Field Guide. Chicago: University of Chicago Press. Gargaglioni, L. H.; Batalha˜o, M. E.; Lapenta, M. J.; Carvalho, M. F.; Rossi, R. V.; Veruli, V. P. (1998): Mamı´ feros da Estac- a˜o Ecolo´gica de Jataı´ , Luiz Antoˆnio, Sa˜o Paulo. P. Avul. Zool. 40, 267–287. Gray, R. D. (1987): Faith and foraging: a critique of the ‘paradigm argument from design’. In: Foraging Behavior. Ed. by A. C. Kamil, J. R. Krebs and H. R. Pulliam. New York: Plenum Press. Pp. 59–140. Krebs, C. J. (1989): Ecological Methodology. New York: Harper Collins Publishers. Manly, B. F. J. (1985): The Statistics of Natural Selection. New York: Chapman & Hall. Martins, E. G.; Bonato, V. (2004): On the diet of Gracilinanus microtarsus (Marsupialia, Didelphidae) in an Atlantic Rainforest fragment in southeastern Brazil. Mamm. Biol. 69, 58–60. Martins, E. G., Bonato, V., da-Silva, C. Q., dos Reis, S. F., (2006a): Seasonality in reproduction, age structure and density of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia: Didelphidae) in a Brazilian cerrado. J. Trop. Ecol. (in press). Martins, E. G.; Bonato, V.; Pinheiro, H. P.; dos Reis, S. F. (2006b): Diet of the gracile mouse opossum (Gracilinanus microtarsus) (Didelphimorphia: Didelphidae) in a Brazilian cerrado: patterns of food consumption
and intrapopulation variation. J. Zool. 269, 21–28. Martins, E. G., Bonato, V., da-Silva, C. Q., dos Reis, S. F. (2006c): Partial semelparity in the Neotropical didelphid marsupial Gracilinanus microtarsus. J. Mammal. (in press). McNab, B. K. (1963): Bioenergetics and the determinants of home range size. Am. Nat. 97, 133–140. Oliveira-Filho, A. T., Ratter, J. (2002): Vegetation physiognomies and woody flora of the cerrado biome. In: The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Ed. by P. S. Oliveira and R. J. Marquis. New York: Columbia University Press. Pp. 91–120. Perry, G.; Pianka, E. R. (1997): Animal foraging: past, present and future. Trends Ecol. Evol. 12, 360–364. Pinheiro, F.; Diniz, I. R.; Coelho, D.; Bandeira, M. P. S. (2002): Seasonal pattern of insect abundance in the Brazilian cerrado. Austral. Ecol. 27, 132–136. Primavesi, O., Primavesi, A. C. P. A., Pedroso, A. F., Camargo, A. C., Rassini, J. B., RochaFilho, J., Oliveira, G. P., Correa, L. A., Armelin, M. J .A., Vieira, S. R., Dechen, S. C. F. (1999): Microbacia Hidrogra´fica do Ribeira˜o Canchim: Um Modelo Real de Laborato´rio Ambiental. Sa˜o Carlos: Embrapa Pecua´ria Sudeste. Schoener, T. W. (1969): Sizes of feeding territories among birds. Ecology 49, 123–141. Schoener, T. W. (1971): Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2, 369–404. Shine, R. (1989): Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q. Rev. Biol. 64, 419–461. Silva, J. M. C.; Bates, J. M. (2002): Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52, 225–233. Stephens, D. W.; Krebs, J. R. (1986): Foraging Theory. Princeton: Princeton University Press. Tolentino, M. (1967): Estudo Crı´ tico sobre o Clima da Regia˜o de Sa˜o Carlos. Sa˜o Carlos: Prefeitura Municipal de Sa˜o Carlos.
Authors’ addresses: E. G. Martins, Programa de Po´s-graduac- a˜o em Ecologia, Universidade Estadual de Campinas, CP 6109, 13083-970 Campinas, SP, Brazil V. Bonato,
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Instituto de Cieˆncias Biolo´gicas, Centro Regional Universita´rio Espı´ rito Santo do Pinhal, Av. He´lio Vergueiro Leite, s/n, 13990-000 Espı´ rito Santo do Pinhal SP, Brazil A. Pinheiro, Departamento de Estatı´ stica, Instituto de Matema´tica, Estatı´ stica e Computac- a˜o Cientı´ fica,
Universidade Estadual de Campinas, CP 6065, 13083-859 Campinas, SP, Brazil S. F. dos Reis, Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas, CP 6109, 13083-970 Campinas, SP, Brazil (e-mail: [email protected])
www.elsevier.de/mambio
Short communication
Variation in the food-niche width of Gracilinanus microtarsus (Didelphimorphia: Didelphidae) in a cerrado remnant in south-eastern Brazil By E.G. Martins, V. Bonato, A. Pinheiro and S.F. dos Reis Programa de Po´s-graduac- a˜o em Ecologia, Universidade Estadual de Campinas, Campinas, Brazil; Instituto de Matema´tica, Estatı´stica e Computac- a˜o Cientı´fica, Universidade Estadual de Campinas, Campinas, Brazil; and Instituto de Cieˆncias Biolo´gicas, Centro Regional Universita´rio Espı´rito Santo do Pinhal, Espı´rito Santo do Pinhal, Brazil Receipt of Ms. 6.4.2005 Acceptance of Ms. 1.3.2006
Key words: gracile mouse opossum, feeding ecology, intrapopulation variation
The gracile mouse opossum Gracilinanus microtarsus is a small (20–45 g), sexually dimorphic (males 30–45 g; females 20–30 g), short-lived (1.0–1.5 years), solitary, arboreal, nocturnal didelphid marsupial (Emmons and Feer 1997; Eisenberg and Redford 2000; Martins et al. 2006a). This species occurs in a range of habitats including the cerrado (Emmons and Feer 1997; Gargaglioni et al. 1998; Eisenberg and Redford 2000), a complex of five vegetation physiognomies and one of the most important terrestrial hotspots of diversity in the world (Oliveira-Filho and Ratter 2002; Silva and Bates 2002). Climate in the cerrado is highly seasonal (Silva and Bates 2002) and affects the temporal and spatial dynamics of plant flowering and fruiting (Batalha and Martins 2004) and abundance of insects (Pinheiro et al. 2002; V. Bonato, unpubl. data); the latter represent the most frequent food resources in the diet of G. microtarsus (Martins and Bonato 2004; Martins et al. 2006b). In the cerrado, particularly in the physiognomy known as cerrada˜o, G. microtarsus occurs at high population densities and its reproduction occurs in the warm–wet season,
with males suffering high mortality rates afterwards (Martins et al. 2006a, c). These findings show that the life history of G. microtarsus is strongly influenced by seasonality and, therefore, we expect the consumption of food resources to be equally influenced. Additionally, we expect the consumption of food resources to be influenced by sex since sexual size dimorphism and its correlates, such as energetic requirements and foraging behaviours, may differentially affect food consumption by males and females (Shine 1989). Here, we ask if sex and seasonality are factors that contribute significantly for intrapopulation variation in the food-niche width of G. microtarsus. This study was done from January to December 2001 at the Clube Na´utico Araraquara (211430 S, 481010 W), located in Ame´rico Brasiliense, approximately 300 km northwest of Sa˜o Paulo city in south-eastern Brazil. The Clube Na´utico Araraquara has two remnants of cerrada˜o (ca. 73 and 307 ha), a physiognomy of the cerrado characterized by dense forest with tall trees and a completely closed canopy (Oliveira-Filho and Ratter 2002; Silva and Bates 2002). The climate of the
1616-5047/$ - see front matter r 2006 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2006.03.001 Mamm. biol. 71 (2006) 5 304–308
ARTICLE IN PRESS Variation in the food-niche width of Gracilinanus microtarsus
region has two well-defined seasons, namely, a warm–wet season from October to March and a cool–dry season from April to September (Tolentino 1967; Primavesi et al. 1999). Trapping was done on two consecutive nights every 15 days from January to December 2001, for a total of 23 sampling occasions and 46 days of fieldwork. The animals were captured in the smaller cerrada˜o remnant (ca. 73 ha) using a 7 7 trapping grid with 49 trapping stations located 10 m from each other. A single Sherman live-trap (dimensions 7.5 9.0 23.5 cm) was set on trees at each trapping station ca. 1.75 m above ground and baited with banana, peanut butter and cod-liver oil. Individuals captured were marked with a numbered leg-band and their sex and age were recorded. Age was determined based primarily on the sequence of tooth eruption and individuals were recorded as adults when all of the teeth had erupted (Costa et al. 2003). One hundred and forty-six faeces (100 from males and 46 from females) were sampled from 38 adult individuals of G. microtarsus (25 males and 13 females) and preserved in 70% ethanol. Of the total number of faeces, 51 were sampled in the warm–wet season and 95 were sampled in the cool–dry season. Description of the procedures of identification of food items detected in the faeces of G. microtarsus as well as detailed information on diet composition can be found in Martins et al. (2006b). Food-niche widths of males and females were measured for each trimester of the year 2001 (two corresponding to the warm–wet season: January–March and October–December; two corresponding to the cool–dry season: April–June and July–September) with the Shannon–Wiener index of diversity (Colwell and Futuyma 1971; Krebs 1989) X H ij ¼ pðij Þ;k log pðijÞ;k , k
where H is the Shannon–Wiener index of diversity (niche width), pðij Þ;k is the frequency of occurrence of the food resource k found in the faeces of sex i in trimester j. The Shannon–Wiener index can assume values ranging from 0 to N. To standardize the index on a scale ranging from 0 to 1, the
305
observed Shannon–Wiener index, H, was divided by log k (Krebs 1989), where k was the total number of food resources detected in the faeces of G. microtarsus. Sampling error estimates for indices of niche width can be obtained using Taylor series expansions (Manly 1985), which hold for symmetrical indices and large sample sizes. Because of the asymmetric nature of the Shannon–Wiener index and the small sample size obtained in this study, 10,000 non-parametric bootstrap resamplings were used to calculate the confidence limits, i.e., 2.5 and 97.5 percentiles (Efron and Tibshirani 1993; Davison and Hinkley 1997). The non-parametric bootstrap resamplings were done in Matlab code. The average food-niche width of males was broader in the trimesters corresponding to the cool–dry season than in those corresponding to the warm–wet season. In contrast, the average food-niche width of females was narrower in the trimesters corresponding to the cool–dry season than in those corresponding to the warm–wet season. Within each sex, the average food-niche widths across trimesters were not significantly different. Between sexes, the average food-niche widths were similar in the trimesters corresponding to the warm–wet season, but were significantly different in the trimesters corresponding to the cool–dry season (Fig. 1). Our results showed that males and females of G. microtarsus had similar food-niche widths in the warm–wet season, when insects are abundant in the cerrado (Pinheiro et al. 2002; V. Bonato, unpubl. data). On the other hand, in the cool–dry season when insects are less abundant (Pinheiro et al. 2002; V. Bonato, unpubl. data), food-niche width between males and females diverged becoming broader in the former and narrower in the latter. This implies, as inferred from the Shannon– Wiener index (Krebs 1989), that food resource consumption in males becomes more even, i.e. more diverse, than that of females in the cool–dry season. A question that arises from these results is why the food-niche width increases in males and decreases in females in the cool–dry season, when insect abundance is low. A likely explanation may be the differences in the patterns of space use between sexes since
ARTICLE IN PRESS 306
E.G. Martins et al.
Fig. 1. Shannon–Wiener indices of food-niche width in Gracilinanus microtarsus by sex and trimester. Upper and lower limits of the 95% confidence intervals are a bootstrapped estimate of the variability in the measure associated with sampling errors. Solid line and filled box: males; dashed line and open circle: females.
it is well established that available food is usually proportional to area traversed by individuals (McNab 1963; Schoener 1969, 1971). Males in G. microtarsus traverse large areas having home ranges on average twice as large as that of females (E. G. Martins, unpubl. data). It is, therefore, not unexpected that males have higher probabilities of finding more food and thus maintaining or increasing the diversity of food resources consumed in the cool–dry season. However, in spite of males traversing larger areas than do females, food-niche width was very similar between the sexes in the warm–wet season. This similarity may be attributable to the high abundance of food resources in this season in the cerrado (Pinheiro et al. 2002; V. Bonato, unpubl. data), providing the same diversity of food resources for both sexes, regardless of their relative movements. Finally, it is worth noticing that the observed pattern of variation in food-niche width of males but not that of females of G. microtarsus follows a classic tenet of optimal foraging theory, which predicts a broadening of food-niche width under conditions of food limitation (Stephens and Krebs 1986; Gray
1987). The fact that this prediction does not apply equally to males and females of G. microtarsus is not surprising because optimal foraging theory is based upon the assumption that individuals or classes of individuals within a population are ecologically equivalent (Stephens and Krebs 1986; Perry and Pianka 1997). Our results thus make evident that there is significant intrapopulation variation in the food-niche of G. microtarsus and that individuals of different sexes cannot be treated as ecologically equivalent.
Acknowledgements We are deeply indebted to E. L. A. Monteiro Filho, G. Machado, C. A. Magalha˜es, J. Semir, J. Y. Tamashiro, S. U. Neto, V. E. Molina, N. E. Oliveira and A. P. P. Gouveia for helping at different stages of this work and to P. R. Guimara˜es Jr., M. S. Arau´jo, J. A. F. Diniz Filho and S. Hyslop for their comments on the manuscript. This work was funded by the Fundac- a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo, FAPESP, Brazil.
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References Batalha, M. A.; Martins, F. R. (2004): Reproductive phenology of the cerrado plant community in Emas National Park (central Brazil). Aust. J. Bot. 52, 149–161. Colwell, R. K.; Futuyma, D. J. (1971): On the measurement of niche breadth and overlap. Ecology 52, 567–576. Costa, L. P.; Leite, Y. L. R.; Patton, J. L. (2003): Phylogeography and systematic notes on two species of gracile mouse opossums, genus Gracilinanus (Marsupialia: Didelphidae) from Brazil. P. Biol. Soc. Washington 116, 275–292. Davison, A. C.; Hinkley, D. V. (1997): Bootstrap Methods and their Application. Cambridge: Cambridge University Press. Efron, B.; Tibshirani, R. J. (1993): An Introduction to Bootstrap. New York: Chapman & Hall. Eisenberg, J. F.; Redford, K. H. (2000): . Mammals of the Neotropics: The Central Neotropics. Vol. 3. Chicago: University of Chicago Press. Emmons, L. H.; Feer, F. (1997): Neotropical Rainforest Mammals: A Field Guide. Chicago: University of Chicago Press. Gargaglioni, L. H.; Batalha˜o, M. E.; Lapenta, M. J.; Carvalho, M. F.; Rossi, R. V.; Veruli, V. P. (1998): Mamı´ feros da Estac- a˜o Ecolo´gica de Jataı´ , Luiz Antoˆnio, Sa˜o Paulo. P. Avul. Zool. 40, 267–287. Gray, R. D. (1987): Faith and foraging: a critique of the ‘paradigm argument from design’. In: Foraging Behavior. Ed. by A. C. Kamil, J. R. Krebs and H. R. Pulliam. New York: Plenum Press. Pp. 59–140. Krebs, C. J. (1989): Ecological Methodology. New York: Harper Collins Publishers. Manly, B. F. J. (1985): The Statistics of Natural Selection. New York: Chapman & Hall. Martins, E. G.; Bonato, V. (2004): On the diet of Gracilinanus microtarsus (Marsupialia, Didelphidae) in an Atlantic Rainforest fragment in southeastern Brazil. Mamm. Biol. 69, 58–60. Martins, E. G., Bonato, V., da-Silva, C. Q., dos Reis, S. F., (2006a): Seasonality in reproduction, age structure and density of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia: Didelphidae) in a Brazilian cerrado. J. Trop. Ecol. (in press). Martins, E. G.; Bonato, V.; Pinheiro, H. P.; dos Reis, S. F. (2006b): Diet of the gracile mouse opossum (Gracilinanus microtarsus) (Didelphimorphia: Didelphidae) in a Brazilian cerrado: patterns of food consumption
and intrapopulation variation. J. Zool. 269, 21–28. Martins, E. G., Bonato, V., da-Silva, C. Q., dos Reis, S. F. (2006c): Partial semelparity in the Neotropical didelphid marsupial Gracilinanus microtarsus. J. Mammal. (in press). McNab, B. K. (1963): Bioenergetics and the determinants of home range size. Am. Nat. 97, 133–140. Oliveira-Filho, A. T., Ratter, J. (2002): Vegetation physiognomies and woody flora of the cerrado biome. In: The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Ed. by P. S. Oliveira and R. J. Marquis. New York: Columbia University Press. Pp. 91–120. Perry, G.; Pianka, E. R. (1997): Animal foraging: past, present and future. Trends Ecol. Evol. 12, 360–364. Pinheiro, F.; Diniz, I. R.; Coelho, D.; Bandeira, M. P. S. (2002): Seasonal pattern of insect abundance in the Brazilian cerrado. Austral. Ecol. 27, 132–136. Primavesi, O., Primavesi, A. C. P. A., Pedroso, A. F., Camargo, A. C., Rassini, J. B., RochaFilho, J., Oliveira, G. P., Correa, L. A., Armelin, M. J .A., Vieira, S. R., Dechen, S. C. F. (1999): Microbacia Hidrogra´fica do Ribeira˜o Canchim: Um Modelo Real de Laborato´rio Ambiental. Sa˜o Carlos: Embrapa Pecua´ria Sudeste. Schoener, T. W. (1969): Sizes of feeding territories among birds. Ecology 49, 123–141. Schoener, T. W. (1971): Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2, 369–404. Shine, R. (1989): Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q. Rev. Biol. 64, 419–461. Silva, J. M. C.; Bates, J. M. (2002): Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52, 225–233. Stephens, D. W.; Krebs, J. R. (1986): Foraging Theory. Princeton: Princeton University Press. Tolentino, M. (1967): Estudo Crı´ tico sobre o Clima da Regia˜o de Sa˜o Carlos. Sa˜o Carlos: Prefeitura Municipal de Sa˜o Carlos.
Authors’ addresses: E. G. Martins, Programa de Po´s-graduac- a˜o em Ecologia, Universidade Estadual de Campinas, CP 6109, 13083-970 Campinas, SP, Brazil V. Bonato,
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E.G. Martins et al.
Instituto de Cieˆncias Biolo´gicas, Centro Regional Universita´rio Espı´ rito Santo do Pinhal, Av. He´lio Vergueiro Leite, s/n, 13990-000 Espı´ rito Santo do Pinhal SP, Brazil A. Pinheiro, Departamento de Estatı´ stica, Instituto de Matema´tica, Estatı´ stica e Computac- a˜o Cientı´ fica,
Universidade Estadual de Campinas, CP 6065, 13083-859 Campinas, SP, Brazil S. F. dos Reis, Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas, CP 6109, 13083-970 Campinas, SP, Brazil (e-mail: [email protected])