Seasonal variations and population parameters explaining the use of space of neotropical rodents

Accepted Manuscript Title: Seasonal variations and population parameters explaining the use of space of Neotropical rodents Author: Clarisse R. Rocha Raquel Ribeiro Jader Marinho-Filho PII: DOI: Reference:

S1616-5047(16)30094-5 http://dx.doi.org/doi:10.1016/j.mambio.2016.07.043 MAMBIO 40845

To appear in: Received date: Accepted date:

27-2-2016 25-7-2016

Please cite this article as: Rocha, Clarisse R., Ribeiro, Raquel, Marinho-Filho, Jader, Seasonal variations and population parameters explaining the use of space of Neotropical rodents.Mammalian Biology http://dx.doi.org/10.1016/j.mambio.2016.07.043 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Seasonal variations and population parameters explaining the use of space of Neotropical rodents

Clarisse R. Rochaa*, Raquel Ribeirob & Jader Marinho-Filhoa

a

Lab. de Mamíferos, Dept. Zoologia, Instituto de Ciências Biológicas, Campus

Universitário Darcy Ribeiro, Universidade de Brasília, 70910-900, Brasília, Brazil. b

Instituto de Estudos em Saúde e Biológicas – IESB. Universidade Federal do Sul e

Sudeste do Pará. Folha 31, Lote 07. Nova Marabá. 68000-500. Marabá – PA, Brazil

*

Corresponding author: [email protected]. (55) 61 31073034

Headline – Space use by rodents in the cerrado

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Abstract Space use by animals has been studied for decades; however, gaps still exist in the understanding of how it is affected by biological and environmental factors. The aim of this study was to determine how biological traits, population parameters and seasonal variations affect the use of space by rodents in a tropical savannah environment. This study was performed in two grids in a grassland area at Aguas Emendadas Ecological Station between January 2004 and December 2013. The trapping sessions lasted six consecutive days and were performed monthly. Sherman traps, which were baited and reset daily, were used to capture the animals. The movement area was estimated using the minimum convex polygon method, and the mean movement distance was used to investigate the factors that affect the movement of the rodents. The hypothesis that a significant difference exists in the movement area size among species was corroborated; however, this difference was not related to body weight. As a general pattern for these rodents, males displayed larger movement areas than females. Movement area size showed an inverse relationship to population density. The understanding of the factors that affect the space use by rodents are complex and the interactions of these factors may also modulate space use by rodents. Our results suggest that space use is also affected by climatic variations.

Key-words: Calomys tener, Home range, Necromys lasiurus, Thalpomys lasiotis

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Introduction Several factors affect the use of space by an animal, including biological factors and environmental parameters (Burt, 1943; Fernandes et al., 2010; Getz et al., 2005; Loretto and Vieira, 2005; Perry and Garland, 2002; Schoener, 1968; Spencer, 2012). Social behaviour, such as mating systems and territories of species may affect morphological, physiological and ecological traits of the animals (Lindstedt et al., 1986; Schoener, 1968), directly influencing their use of space. Body size is one of the best predictors of life-history features, including homerange size. Many authors reported an allometric relationship between body size and home ranges (Milton and May, 1976; Harestad and Bunell, 1979; Swihart et al., 1987), which could be explained by a multitude of factors, including social organization and mating systems (Damuth, 1981). In promiscuous species, the space use of males is expected to be larger than that of females because males tend to increase their effective movement to access females, whereas the smaller amplitude of movement by females may reflect their territorial behaviour for offspring protection (Gaulin and FitzGerald, 1986; Gomez et al., 2011; Wolff, 1993; Wolff et al., 1994). In fact, previous studies showed females using smaller areas, whereas males increase their areas during reproduction (Getz et al., 2005; Magnusson et al., 1995). Climate effects on the use of space are complex and these effects are often indirectly associated with food resource availability or seasonality and predation risk (Börger et al., 2006; Moorcroft, 2012; Powell and Mitchell, 2012; Spencer, 2012). Seasonal variation in the use of space may be explained by seasonal changes in reproductive activity, population density or food availability. Studies conducted on rodent populations have shown that the space use size is inversely related to the population density (Ambrose, 1973; Erlinge et al., 1990; 3

Makarieva et al., 2005; Priotto et al., 2002). The presence of a member of the population affects the space used by another member because it imposes limits on its movements (Alho and Souza, 1982). The variables sex, seasonality, population density and body mass may interact in a complex manner to explain the variation in the movements of mammals (Getz et al., 2005). In the present study, three species of cricetid rodents were monitored over 10 years, with the aim of detecting how these important biological and environmental factors affect the space use of these animals. We evaluated the following hypotheses: (1) males use larger areas than females, (2) the use of space differs between dry and wet seasons, (3) the distance covered by animals differs between reproductive and non-reproductive periods and may show different responses between sexes, (4) the distance covered by an animal varies between the sampling areas, (5) the distance covered by an animal is directly related to its body weight, and (6) the distance covered by an animal is indirectly related to population density.

Material and Methods

Study site

The cerrado is a savannah with two well-defined climatic seasons: a cold and dry winter (from April to September) and a hot and wet summer (from October to March) (Oliveira-Filho and Ratter, 2002; Ribeiro and Walter, 2001). According to the classification of Köppen-Geiger, the climate is type Aw, with 1500 mm of mean annual rainfall (Cardoso et al., 2015). The study was performed on the Aguas Emendadas Ecological Station (Estação Ecológica de Águas Emendadas, ESECAE), located in the north-eastern portion of the Federal District, Brazil, in open areas with the presence of 4

murundus, which consist of microrelief with trees and shrubs (Oliveira-Filho and Ratter, 2002; Sano and Almeida, 1998). See Ribeiro et al. (2011) for more detailed information on the study site.

Animal capture

Captures occurred between January 2004 and December 2013. Full moon periods were avoided because of the documented decline in rodent activity during these periods (O'Farrell, 1974; Price et al., 1984). Two capture stations were placed in open areas with murundus: Grid 1 (15º32′51′′S and 47º36′55′′W), with a scarce presence of woody vegetation (n = 18), and Grid 2 (15º32′14′′S and 47º36′46′′W), with a higher presence of woody species (n = 42) than Grid 1(Ribeiro and Marinho-Filho, 2005). Each of the grids, separated by 1 km, consisted of 100 points, separated from each other by 15 metres, in a total area of 1.82 ha (135 x 135 m). Fifty traps were simultaneously placed in each grid. Capture sessions were performed monthly. In each session, the traps remained in operation for 6 consecutive nights and were checked and baited daily at dawn. Baits consisted of banana, peanut butter, sardine and cornmeal. After 3 nights, the traps were removed from the odd points in each of the grids and transferred to the even points to allow alternate sampling of all 100 points in each grid. All captured individuals were marked with numbered earrings (1005-1, National Band and Tag, Co., Newport, KY) or phalange ablation. Animals were weighed, sexed and classified according to their developmental (juvenile or adult) and reproductive (reproductive or non-reproductive) stages.

The developmental stage was classified according to the relationship between body weight and reproductive stage. The lowest body weight recorded for individuals considered reproductive was used to determine the developmental stage of the rodents. 5

Animals with weight higher than this value were considered adults, whereas animals with weight lower than this value were considered juveniles. Females were considered reproductive when they had vaginal perforation, were pregnant or showed obvious teats. Males were considered reproductive when the testicles were in the scrotum. All capture, handling and marking procedures were approved by the University of Brasilia Animal Care and Use Committee (CEUA-UNBDOC 47208/2009) and followed the Guidelines of animal care and use by the American Society of Mammalogists (Sikes and Gannon, 2011). Captures and collections were performed with authorization from the Brazilian Institute for the Environment (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis - IBAMA No. 15151-1 to 10). More details about the capture method may be obtained in Rocha et al. (2011).

Data analysis

The movement area sizes of individuals of each of the three species captured were estimated with the Minimum Convex Polygon (MCP) method using the Ranges 8 v 2.8 software (Kenward et al., 2008). Although the areas enclosed by the Minimum Convex Polygon are not actual estimates of individual home ranges (sensu Burt, 1943) (sensu Burt, 1943), they allow to compare the movement areas of individuals and determine the effects of season, and trapping grids.

The movement areas were

calculated only for individuals with four or more captures to ensure a better estimate (Múrua et al., 1986; Pires et al., 2010). To estimate the movement areas with the MCP method, all captures recorded for each individual during a given season (dry or wet) were used, provided they complied with the required number of captures. The animals that had more than 25% of the edge of the perimeter of their movement areas adjacent to the edges of the study grids were excluded from the analysis. The movement areas of

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individuals who moved between the two study grids were not estimated. This movement occurred with only a few individuals and only once for each and therefore was considered a dispersal event.

To determine whether body weight differs between males and females, a t test was performed for each of the species analysed, with reproductive and non-reproductive animals being evaluated separately. To verify whether the movement areas calculated by MCP differ significantly among species, a covariance analysis (ANCOVA) was performed, using the number of recaptures as a covariable. Subsequently, a Tukey’s test was performed using the package HH of the R software to determine which species differed in terms of movement area size (Heiberger, 2015). Movement area estimates were log transformed before the analyses.

To verify whether a significant difference exists in the movement areas calculated by the MCP between sexes and between seasons, an ANCOVA was performed for each species, with the number of recaptures being used as a covariable (Crawley, 2007). For Hairy-tailed Bolo Mouse (Necromys lasiurus (Lund 1840)), the study area (grid) was also included in the model. For Delicate Vesper Mouse (Calomys tener (Winge 1887)) and Hairy-eared Cerrado Mouse (Thalpomys lasiotis (Thomas 1916)), this variable was not used because of the low number of movement area estimates in one of the grids. Subsequently, the normality and homoscedasticity of the residuals of the model were graphically verified (Crawley, 2007).

Several of the factors that may affect the space use by individuals, such as variations in the reproductive stage, body weight and species abundance, change during the period when the movement area is estimated. Therefore, a non-circular distance was calculated as a movement index, which has been used in studies on the space use by 7

small mammals (Jennrich and Turner, 1969; Slade and Russell, 1998). We chose the mean movement distance (MD) as an estimate of movement. This index is based on the mean of the distances covered by the animals among successive captures and was calculated with the data recorded only within each capture session (a maximum of 6 days). Juveniles were excluded from the analyses because of the low number of estimates for this group of animals.

To determine whether the MD differs among species, an ANOVA was performed, followed by a Tukey’s test. For this analysis, the MD estimates were log transformed. We used the generalized least squares (GLS) model selection to verify which factors affected the MD. The complete model of the model selection considered the following variables to be independent: sex (male or female), the reproductive stage of each sex (reproductive or non-reproductive), the study grid (grid 1 or grid 2), the body weight of the individual, the species abundance (in the month and in the sampling grid of each individual) and the climatic season (dry and wet). The GLS model selection was performed using the nlme package for R software (Pinheiro et al., 2011). The model selection and its validation were performed according to the protocol described by Zuur et al. (2009) for data with a normal distribution. Initially, we checked for patterns of temporal autocorrelation in the MDs by comparing the quality of the adjustment of the initial model adjusted for the models with fixed factors (GLS) and by linear mixed effects models (lme), which consider the collection period, month and year to be random variables. We also employed mixed linear models that used the individual as a random variable to avoid overestimating the number of independent samples. The best global model chosen to perform the analyses was ranked with the lowest values of the Akaike information criterion (AIC) (Table A.1, A.2 and A.3). Once the best global model was defined, all plausible models were created and subsequently selected from 8

the lowest values of the AIC. The final model was graphically evaluated to check the normality and homoscedasticity of the residuals.

Results

The effort of 72,000 traps*nights resulted in 6,772 captures, with a success rate of 9%. The three species most captured and evaluated were Necromys lasiurus (60.5%), Calomys tener (19.5%) and Thalpomys lasiotis (17%). Other six rodent species were captured, including Calomys expulsus (Lund 1841), Cerradomys scotti (Langguth and Bonvicino 2002), Clyomys laticeps (Thomas 1909), Mus musculus Muridae (Linnaeus 1758), Oligoryzomys fornesi (Massoia 1973), and Oligoryzomys nigripes (Olfers 1818). Gracilinanus agilis (Burmeister 1854) and Thylamys karimii (Petter, 1968) were the only marsupials captured.

Body weight differed between males and females for N. lasiurus (reproductive: t = - 4.711; df = 407; p < 0.001, non-reproductive: t = - 9.806; df = 413; p < 0.001) and T. lasiotis (reproductive: t = - 2.389; df = 158; p = 0.009, non-reproductive: t = - 4.435; df = 214; p < 0.001). Males (N. lasiurus - mean [𝑋̅] = 41 g, T. lasiotis - 𝑋̅ = 19.5 g) showed higher body weights than females (N. lasiurus – 𝑋̅ = 36 g, T. lasiotis 𝑋̅ = 18 g). However, C. tener (species mean – 13 g) did not show a difference in the body weights between the males and females (reproductive: t = 2.463; df = 275; p = 0.993, nonreproductive: t = -1.084; df = 175; p = 0.140) (Fig. 1). The movement area was calculated for 52 males (mean number of captures [𝑋̅] = 6, maximum [max] = 10) and 28 females of C. tener (𝑋̅ = 5.7; max = 9), 155 males (𝑋̅ = 7.3; max = 23) and 104 females (𝑋̅ = 8.4; max = 20) of N. lasiurus and 46 males (𝑋̅ = 9.4; max = 19) and 34 females (𝑋̅ = 9.1; max = 21) of T. lasiotis. Calomys tener was the 9

species with the largest movement area estimates (adjusted mean [m] ± SD = 0.320 ± 0.020 ha, followed by T. lasiotis (m ± SD = 0.274 ± 0.021 ha) and N. lasiurus (m ± SD = 0.173 ± 0.011 ha) (Fig. 2).

The three species showed differences in the movement area estimates (F(2,415) = 36.8; r2 = 0.210; p < 0.001), but only N. lasiurus differed significantly from C. tener (Z = - 6.794; p < 0.001) and T. lasiotis (Z = 4.137; p < 0.001). The movement areas of Calomys tener and T. lasiotis were similar (Z = - 2.125; p = 0.082). The three species also showed different MD means (F(2,1294) = 67.91; r2 = 0.094; p < 0.001). The MD covered by C. tener was significantly larger than the MD covered by T. lasiotis (p < 0.001) and MD covered by T. lasiotis was significantly larger than the MD covered by N. lasiurus (p < 0.001) (Fig. 3). The movement areas of C. tener (F(2,81) = 5.813; r2 = 0.125; p = 0.004) and T. lasiotis (F(2,77) = 36.31; r2 = 0.485; p < 0.001) varied between sexes. Males showed larger movement areas than females (Fig. 4). For N. lasiurus, the movement areas varied between sex and areas (F(3,255) = 14.43; r2 = 0.145; p < 0.001). The movement areas varied between areas and males showed larger movement areas than females (Fig. 5).

The MD estimates were calculated for 180 males (37 non reproductive) and 97 females (31 non reproductive) of C. tener, 436 males (190 non reproductive) and 362 females (183 non reproductive) of N. lasiurus and 148 males (73 non reproductive) and 116 females (66 non reproductive) of T. lasiotis. The best ranked model indicates that the variables of sex and abundance were the most important for explaining the variations in the movement estimates for C. tener (Table 1; Table A.4 and A.5). The MD estimates were inversely proportional to the species abundance; therefore, the 10

males showed a larger MD than females (Fig. 6). The best model selected to explain the variation in MD for N. lasiurus included the variables of abundance, sex and body weight (Table 2; Table A.6 and A.7). The MD of N. lasiurus was inversely related to abundance and was significantly larger for males than for females (Fig. 7a). These estimates were also directly proportional to the body weight increases in these animals (Fig. 7b). For T. lasiotis, the variables that best explained the variation in MD were abundance, sex and climatic season (Table 3; Table A.8 and A.9). For this species, the MD covered by males was significantly larger than the MD covered by females and inversely proportional to the abundance and larger in the wet season (Fig. 8). The variable ‘reproductive stage’ was not select for any species. No relationship was found between the distance traveled by reproductive and non-reproductive individuals.

Discussion Differences between males and females and population density were the most important factors to explain the variation in space use by rodents. The results also suggest that space use may vary between dry and wet seasons, as found for T. lasiotis. Conversely, the movement of these rodents in open areas did not vary with the reproductive condition, as would be expected. In the present study, as a general pattern for the three species, males showed significantly larger MD and movement areas than females, regardless of how the data were analysed. These results corroborate other studies performed with N. lasiurus in savannah areas in central Brazil (Alho and Souza, 1982), savannah patches within the Amazon forest (Magnusson et al., 1995) and the Atlantic forest (Pires et al., 2010). Studies performed with other mammal species (Belcher and Darrant, 2004; Ostfeld,

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1985) and with other vertebrate groups, such as lizards (Perry and Garland, 2002), also reported differences in the size pattern of the home range between males and females. The body mass showed little influence in patterns of movement of these rodents. In the present study, only one species, N. lasiurus, showed an increase in movement that was directly proportional to the increase in body weight. For the remaining species, movement and body weight were inversely related. The species with the lowest body weight, C. tener, showed the largest space-use estimates, whereas the species with the highest body weight (N. lasiurus) showed smaller space-use estimates. The small range of body mass between the three studied species can be one of the explanations. And so, the factors that determine the extent and the quality of the movement areas of vertebrates, as foraging mode, feeding regime and intra and inter-specific relationships (Cáceres et al., 2010; Lindstedt et al., 1986; Perry and Garland, 2002) may be more important to explain the differences showed between species. No variation was detected in the area covered by individuals of C. tener and N. lasiurus between the dry and rainy seasons. Despite the great availability of fruits and insects in the wet season in the cerrado (Oliveira and Frizzas, 2008; Pinheiro et al., 2002; Proença et al., 2000; Silva et al., 2011), the study site provides great availability of grass seeds (unpublished data) in the dry season, and these species can benefit from this food resource. The movements performed by the males and females of T. lasiotis were greater in the wet season than dry seasons. The abundance of T. lasiotis significantly reduces in the wet season (Ribeiro et al., 2011) and can be related to higher distances performed by this species. The increase in the movement areas of the three species was also negatively related to the increase in population abundance. For T. lasiotis, in the last 2 years, when the abundance of this species was much lower, the space used by these animals was

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larger than in previous years. Space use by an individual will modify the distribution of resources available for the remaining individuals (Mitchell and Powell, 2004), affecting how each individual within the population moves in relationship to the remaining individuals. In the present study, no variation was detected in the area covered by individuals with regard to the reproductive stage of the males and females for any of the species studied. However, the differences found in the space use between sexes and climatic seasons suggest differences in the reproductive or feeding behaviour. Therefore, an evaluation of the diet of those animals would be necessary to better understand the relationship between space use, seasonality and reproduction. The species analysed in the present study showed differences in diet composition and possibly also in their predation rates, as they display different activity patterns: C. tener and T. lasiotis are nocturnal, and N. lasiurus is diurnal (Vieira et al., 2010; Vieira and Baumgarten, 1995). These results emphasize that several factors are simultaneously responsible for the variations found in the space use between animals of different sexes or different species. In the grid with higher plant richness, males and females of N. lasiurus moved across longer distances. These results suggest that the environment/habitat quality may also affect the space use by this species, possibly associated to differences in food and shelter availability between the grids. In a study performed in Illinois, United States, where the climate is temperate, the difference in the space use of Blarina brevicauda between seasons varied according to the two types of habitat studied (Getz and McGuire, 2008), indicating that environmental factors (e.g., habitat) may affect the size of the movement areas/home ranges between the seasons. The factors that affect the space use of small mammals may vary temporally; that is, a given parameter may be significant in a given moment and of no importance in

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another moment. Individuals may change their behaviour in periods of food scarcity or availability, and this may affect their use of space. Individual variation also affects the space use (Mares et al., 1980). The size and shape of the home range, as well as the spatial and temporal activity, vary considerably among individuals. Such plasticity allows the animal to modulate its behaviour according to local environmental conditions (Ambrose, 1973). Short-term studies observe momentary responses to variations in the pressures from the physical and biotic environment. Only long-term studies, with a higher number of individuals analysed and a combination of different analytical methods, may detect more general patterns. The most important patterns that we could observe in the present study were the following: 1) the males of the three rodent species studied showed larger movement areas than females, and 2) the species abundance was inversely related to the movement distances of these rodents. Climatic seasonality was associated to differences in space use by species; however, reproduction, although apparently concentrated in the wet season, did not show any relationship to the variation observed in the movement areas.

Acknowledgements We thank the University of Brasília and the Programa de Pós-graduação em Ecologia, the

National

Post-Doctoral

Program/CAPES/

Ministry

of

Education

(PNPD/CAPES/MEC); Fundação de Empreendimentos Científicos e Tecnológicos (FINATEC)

and

Fundação

de

Amparo

à

Pesquisa

do

Distrito

Federal

(FAPDF/PRONEX) for material and financial support. We also thank the National Council for Scientific and Technological Development (CNPq) for financial support to JMF (Proc. 309182/2013-1) and for the Master’s fellowship to Ingrid Mattos, as well as 14

for the scholarships to people who helped in the field. We also thank the staff of Aguas Emendadas Ecological Station (ESECAE), the Animal Care and Use Committee of the UnB (CEUA-UNBDOC 47208) and Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (Number 15151-1 to 10) for providing the authorizations to conduct this research. The manuscript was translated to English from Portuguese by Wiley.

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References Alho, C.J.R., Souza, M.J., 1982. Home range and use of space in Zygodontomys lasiurus (Cricetidae, Rodentia) in the central Brazil. Ann Carnegie Mus 51, 127-132. Ambrose, H.W., 1973. An experimental study of some factors affecting the spatial and temporal activity of Microtus pennsylvanicus. J Mammal 54, 79-110. Belcher, C.A., Darrant, J.P., 2004. Home range and spatial organization of the marsupial carnivore, Dasyurus maculatus maculatus (Marsupialia: Dasyuridae) in south-eastern Australia. J Zool 262, 271-280. Börger, L., Franconi, N., Ferretti, F., Meschi, F., De Michele, G., Gantz, A., Coulson, T., 2006. An integrated approach to identify spatiotemporal and individual-level determinants of animal home range size. Am Nat 168, 471-485. Burt, W.H., 1943. Territoriality and Home Range Concepts as Applied to Mammals. J Mammal 24, 346-352. Cáceres, N.C., Graipel, M.E., Monteiro-Filho, E.L.A., 2010. Técnicas de observação e amostragem de marsupiais, in: Reis, N.R., Peracchi, A.L., Rossaneis, B.K., Fregonezi, M.N. (Eds.), Técnicas de estudos aplicadas aos mamíferos silvestres brasileiros. Technical Books Editora, Rio de Janeiro, pp. 21-36. Cardoso, M.R.D., Marcuzzo, F.F.N., Barros, J.R., 2015. Classificação Climática de Köppen-Geiger para o Estado de Goiás e o Distrito Federal. Acta Geográfica 8, 40-55. Crawley, M.J., 2007. The R book. Chichester. UK: Wiley. Erlinge, S., Hoogenboom, I., Agrell, J., Nelson, J., Sandell, M., 1990. Density-related home-range size and overlap in adult field voles (Microtus agrestis) in Southern Sweden. J Mammal 71, 597-603. Fernandes, F.R., Cruz, L.D., Martins, E.G., dos Reis, S.F., 2010. Growth and home range size of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia: Didelphidae) in Brazilian cerrado. J Trop Ecol 26, 185-192. Gaulin, S.J., FitzGerald, R.W., 1986. Sex differences in spatial ability: an evolutionary hypothesis and test. Am Nat, 74-88. Getz, L.L., McGuire, B., 2008. Factors influencing movement distances and home ranges of the short-tailed shrew (Blarina brevicauda). Northeastern Naturalist, 293-302. Getz, L.L., Oli, M.K., Hofmann, J.E., McGuire, B., Ozgul, A., 2005. Factors influencing movement distances of two species of sympatric voles. J Mammal 86, 647654. Gomez, D., Sommaro, L., Steinmann, A., Chiappero, M., Priotto, J., 2011. Movement distances of two species of sympatric rodents in linear habitats of Central Argentine agro-ecosystems. Mamm Biol 76, 58-63. Heiberger, R.M., 2015. Statistical analysis and data display: Heiberger and Holland. , R package version 2.1-32 ed. Jennrich, R., Turner, F., 1969. Measurement of non-circular home range. J Theor Biol 22, 227-237. Kenward, R.E., Walls, S.S., South, A.B., Casey, N.M., 2008. Ranges8: For the analysis of tracking and location data. Anatrack Ltd., Wareham, UK. Lindstedt, S.L., Miller, B.J., Buskirk, S.W., 1986. Home range, time, and body size in mammals. Ecology 67, 413-418. Loretto, D., Vieira, M.V., 2005. The effects of reproductive and climatic seasons on movements in the black-eared opossum (Didelphis aurita wied-neuwied, 1826). J Mammal 86, 287-293. 16

Magnusson, W.E., De Lima Francisco, A., Sanaiotti, T.M., 1995. Home-range size and territoriality in Bolomys lasiurus (Rodentia: Muridae) in an Amazonian savanna. J Trop Ecol 11, 179-188. Makarieva, A.M., Gorshkov, V.G., Li, B.-L., 2005. Why do population density and inverse home range scale differently with body size?: Implications for ecosystem stability. Ecol Complex 2, 259-271. Mares, M.A., Adams, R., Lacher, T.E., Jr.; Willig, M.R., 1980. Home range dynamics in chipmunks: responses to experimental manipulation of population density and distribution. Ann Carnegie Mus 4913, 193-201. Mitchell, M.S., Powell, R.A., 2004. A mechanistic home range model for optimal use of spatially distributed resources. Ecol Model 177, 209-232. Moorcroft, P.R., 2012. Mechanistic approaches to understanding and predicting mammalian space use: recent advances, future directions. J Mammal 93, 903-916. Múrua, R., Gonzales, L.A., Meserve, P.L., 1986. Population ecology of Oryzomys longicaudatus philippii (Rodentia: Cricetidae) in southern Chile. J Anim Ecol 55, 281293. O'Farrell, M.J., 1974. Seasonal activity patterns of rodents in a Sagebrush Community. J Mammal 55, 809-823. Oliveira-Filho, A.T., Ratter, J.A., 2002. Vegetation physiognomies and woody flora of the Cerrado biome., in: Oliveira, P.S., Marquis, R.J. (Eds.), The Cerrado of Brazil Editora Columbia University, Nova Iorque, USA, pp. 91-119. Oliveira, C.M., Frizzas, M.R., 2008. Insetos do Cerrado: distribuição estacional e abundância. Boletim de Pesquisa e Desenvolvimento. Embrapa – CPAC, Planaltina, Brasil. Ostfeld, R.S., 1985. Limiting resources and territoriality in microtine rodents. Am Nat 126, 1-15. Perry, G., Garland, T., 2002. Lizard home ranges revisited: Effects of sex, body size, diet, habitat, and phylogeny. Ecology 83, 1870-1885. Pinheiro, F., Diniz, I., Coelho, D., Bandeira, M., 2002. Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecol 27, 132-136. Pinheiro, J., Bates, D., Debroy, S., 2011. R package. nlme: Linear and Nonlinear Mixed Effects Models. , 3 ed. Deepayan Sarkar and R Development Core Team. Pires, A.d.S., Fernandez, F.A.d.S., Feliciano, B.R., Freitas, D.d., 2010. Use of space by Necromys lasiurus (Rodentia, Sigmodontinae) in a grassland among Atlantic Forest fragments. Mamm Biol 75, 270-276. Powell, R.A., Mitchell, M.S., 2012. What is a home range? J Mammal 93, 948-958. Price, M.V., Waser, N.M., Bass, T.A., 1984. Effects of moonlight on microhabitat use by desert rodents. J Mammal 65, 353-356. Priotto, J., Steinmann, A., Polop, J., 2002. Factors affecting home range size and overlap in Calomys venustus (Muridae: Sigmodontinae) in Argentine agroecosystems. Mamm Biol 67, 97-104. Proença, C., Oliveira, R.S., Silva, A.P., 2000. Flores e frutos do Cerrado. Universidade de Brasília, São Paulo, Brasil. Ribeiro, J.F., Walter, B.M.T., 2001. As matas de galeria no contexto do bioma Cerrado., in: Ribeiro, J.F., Fonseca, C.E.L., Sousa-Silva, J.C. (Eds.), Cerrado: caracterização e recuperação de matas de galeria. EMBRAPA, Planaltina, Brasil, pp. 29-47. Ribeiro, R., Marinho-Filho, J., 2005. Estrutura da comunidade de pequenos mamíferos (Mammalia, Rodentia) da Estação Ecológica de Águas Emendadas, Planaltina, Distrito Federal, Brasil. Rev Bras Zool 22, 898-907.

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Ribeiro, R., Rocha, C., Marinho-Filho, J., 2011. Natural history and demography of Thalpomys lasiotis (Thomas, 1916), a rare and endemic species from the Brazilian savanna. Acta Theriol 56, 275-282. Rocha, C.R., Ribeiro, R., Takahashi, F.S.C., Marinho-Filho, J., 2011. Microhabitat use by rodent species in a central Brazilian cerrado. Mamm Biol 76, 651-653. Sano, S.M., Almeida, S.P., 1998. Cerrado: ambiente e flora. EMBRAPA-CPAC, Planaltina, Brasil. Schoener, T.W., 1968. Sizes of Feeding Territories among Birds. Ecology 49, 123-&. Sikes, R.S., Gannon, W.L., 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92, 235-253. Silva, N.A.P.d., Frizzas, M.R., Oliveira, C.M.d., 2011. Seasonality in insect abundance in the "Cerrado" of Goiás State, Brazil. Rev Bras Entomol 55, 79-87. Slade, N.A., Russell, L.A., 1998. Distances as indices to movements and home-range size from trapping records of small mammals. J Mammal 79, 346-351. Spencer, W.D., 2012. Home ranges and the value of spatial information. J Mammal 93, 929-947. Vieira, E., Baumgarten, L., Paise, G., Becker, R., 2010. Seasonal patterns and influence of temperature on the daily activity of the diurnal neotropical rodent Necromys lasiurus. Can J Zoolog 88, 259-265. Vieira, E.M., Baumgarten, L.C., 1995. Daily activity patterns of small mammals in a cerrado area from central Brazil. J Trop Ecol 11, 255-262. Wolff, J.O., 1993. Why area female small mammals territorial? . Oikos 68, 6. Wolff, J.O., Edge, W.D., Bentley, R., 1994. Reproductive and behavioral biology of the gray-tailed vole. J Mammal 75, 873-879. Zuur, A., Ieno, E., Walker, N., Saveliev, A., Smith, G., 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York, USA.

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Figure 1 – Body weight of females (F) and males (M), reproductive (REP) and nonreproductive (NREP), of (a) Calomys tener, (b) Necromys lasiurus and (c) Thalpomys lasiotis captured in the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil, from January 2004 to December 2013. Figure 2 – Adjusted least square means and standard error of the home range calculated by the Minimum Convex Polygon method (in hectares) for Calomys tener, Necromys lasiurus and Thalpomys lasiotis, captured from January 2004 to December 2013 in the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil. Figure 3 – Mean and confidence interval of the mean movement distance, in metres, for the species Calomys tener, Necromys lasiurus and Thalpomys lasiotis captured from January 2004 to December 2013 in the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil. Figure 4 – Adjusted least square means and standard error of the home range calculated by the Minimum Convex Polygon method in hectares for Calomys tener and Thalpomys lasiotis, captured from January 2004 to December 2013 in the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil. Squares represent males, and circles represent females. Figure 5 – Adjusted least square means and Standard error of the home range calculated by the Minimum Convex Polygon method in hectares for Necromys lasiurus, captured in two areas (grids 1 and 2) from January 2004 to December 2013 in the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil. Squares represent males, and circles represent females. Figure 6 – Mean movement distance estimates (in metres) of the observed data (obs) and generated from the models selected (pred) for Calomys tener, with regard to the abundance and variation between the sexes, calculated during a study performed from January 2004 to December 2013 on the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil. Figure 7 – Mean movement distance estimates (in metres) of the observed data (obs) and generated from the models selected (pred) for Necromys lasiurus, (a) with regard to the abundance and variation between the sexes, and (b) with regard to the body weight and variation between the sexes, calculated during a study performed from January

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2004 to December 2013 on the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil. Figure 8 – Mean movement distance estimates (in metres) of the observed data (obs) and generated from the models selected (pred) for Thalpomys lasiotis, with regard to the abundance and variation between the sexes in (a) wet seasons and (b) dry seasons, calculated during a study performed from January 2004 to December 2013 on the Aguas Emendadas Ecological Station, Brasília, Federal District, Brazil.

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Fig.1

21

Fig.2

22

Fig.3

23

Fig.4

24

Fig.5

25

Fig.6

26

Fig.7

27

Fig.8

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Table 1 – Models ranked from the lowest Akaike Information Criterion (AIC) values, with their respective ∆AIC values, and degrees of freedom (df), generated from the global model {MD ~ sex * rep + weight + abund + grid + season} to determine the influence of these variables on the variations found in the distance covered by individuals of Calomys tener captured from 2004 to 2013 on the Aguas Emendadas Ecological Station, Federal District, Brazil. Models

AIC

†

MD ~ sex + abund

2655.375

0.000

4

MD ~ abund

2655.834

0.459

3

MD ~ sex + rep + abund

2656.413

1.038

5

MD ~ sex + weight + abund

2656.894

1.519

5

MD ~ sex + abund + grid

2657.221

1.846

5

†

∆AIC

df

∆AIC = AIC – minimum (AIC), sex = sex (male or female), rep = reproductive stage,

abund = number of individuals, grid = study grid (grid 1 or grid 2), weight = body weight, season = climatic season (dry and wet)

29

Table 2 – Models ranked from the lowest Akaike Information Criterion (AIC) values, with their respective ∆AIC values, and degrees of freedom (df), generated from the global model {MD ~ sex * rep + weight + abund + grid + season} to determine the influence of these variables on the variations found in the distance covered by individuals of Necromys lasiurus captured from 2004 to 2013 on the Aguas Emendadas Ecological Station, Federal District, Brazil. Models

AIC

†

MD ~ sex + weight + abund

6750.671

0.000

6

MD ~ weight + abund

6750.857

0.186

5

MD ~ sex + weight + abund + season

6751.377

0.706

7

MD ~ weight + abund + season

6751.793

1.122

6

MD ~ sex + rep + weight + abund

6752.662

1.991

7

†

∆AIC

df

∆AIC = AIC – minimum (AIC), sex = sex (male or female), rep = reproductive stage,

abund = number of individuals, grid = study grid (grid 1 or grid 2), weight = body weight, season = climatic season (dry and wet).

30

Table 3 – Models ranked from the lowest Akaike Information Criterion (AIC) values, with their respective ∆AIC values, and degrees of freedom (df), generated from the global model {MD ~ sex * rep + weight + abund + grid + season} to verify the influence of these variables on the variations found in the distance covered by individuals of Thalpomys lasiotis captured from 2004 to 2013 on the Aguas Emendadas Ecological Station, Federal District, Brazil. Model

AIC

†

MD ~ sex + abund + season

2190.25

0.00

6

MD ~ sex + abund + grid + season

2192.05

1.80

7

MD ~ sex + weight + abund + season

2192.07

1.82

7

MD ~ sex + rep + abund + season

2192.25

2.00

7

MD ~ sex + season

2192.81

2.56

5

†

∆AIC

df

∆AIC = AIC – minimum (AIC), sex = sex (male or female), rep = reproductive stage,

abund = number of individuals, grid = study grid (grid 1 or grid 2), weight = body weight, season = climatic season (dry and wet)

31