What if it gets crowded? Density-dependent tortuosity in individual movements of a Neotropical mammal
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1 bs_bs_banner Austral Ecology (2015) 40, What if it gets crowded? Density-dependent tortuosity in individual movements of a Neotropical mammal PAULO JOSÉ A. L. ALMEIDA, 1 * MARCUS VINÍCIUS VIEIRA, 2,3 JAYME AUGUSTO PREVEDELLO, 4 MAJA KAJIN, 5 GERMAN FORERO-MEDINA 6 AND RUI CERQUEIRA 2,3 1 Laboratório Nacional de Computação Científica Coordenação de Matemática Aplicada, Petrópolis ( pjabreu@lncc.br), 2 Laboratório de Vertebrados, Departamento de Ecologia, 3 Programa de Pós-graduação em Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, 5 Departamento de Ecologia, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, 4 Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil, and 6 Wildlife Conservation Society, Cali, Colombia Abstract Effects of density dependence on animal movements have received much attention in ecology, but it is still debated to what extent dispersal and movements in general are density dependent, and their potential contribution to population regulation processes. Here, we determine the occurrence and nature of density dependence in the movements of a Neotropical marsupial, the black-eared opossum Didelphis aurita Wied-Neuwied Using spool-and-line tracking devices, we estimated the tortuosity of fine-scale movements of 149 individuals by their fractal dimension D. We evaluated the relative importance of population size, reproductive or climatic seasons and reproductive maturity of individuals as determinants of movement tortuosity, using a model selection approach. Population size was the most important determinant of movement tortuosity, with season (climatic seasons for females, reproductive seasons for males) and reproductive maturity as secondary but also important variables. We detected a positive density-dependent effect on movement tortuosity, resulting in more intensive use of areas by individuals during periods of high population size. This positive association between movement tortuosity and population size is more likely to result from intraspecific competition, which forces individuals to explore their environment more intensively during high-density periods. Therefore, despite being density dependent, movements in D. aurita apparently do not contribute to population regulation mechanisms. Key words: abundance, Atlantic forest, Didelphis, marsupial, fractals, reproductive season. *Corresponding author. Accepted for publication February Density dependence is a core concept in population ecology and has been the subject of much research (Forchhammer et al. 1998; Lima & Jaksic 1999; Berryman et al. 2002; Bonsall & Mangel 2009). Many studies have evaluated how vital rates such as survival and fecundity affect and are affected by population density (e.g. Fowler 1981; Reznick et al. 2002). Yet, changes in density are the result of changes not only in population size, but also in the area occupied by the individuals within a population. This area results mostly from the amplitude of movements made by individuals, but density dependence in movements has seldom been studied in invertebrates (but see Fourcassié et al. 2003; Fronhofer et al. 2015), while in vertebrates the focus is mainly on dispersal movements (e.g. Matthysen 2005). This represents a clear limitation to the understanding of density-dependent processes in populations, as animal movements may be important determinants of population structure and dynamics (Turchin 1998). Studies investigating the potential influence of population density on animal movements have focused mainly on dispersal (Aars & Ims 2000; Ims & Andreassen 2005; Delgado et al. 2010). However, dispersal is just one of the drivers of animal movement, which may also be related to factors such as habitat selection, the search for food and mates, and the physiological condition and sensorial abilities of individuals (Bell 1991; Zollner & Lima 1997; Prevedello et al. 2010). All these processes depend on individual choices (e.g. Morris 2003), which may result in different behaviour patterns, and may have a density-dependent component (Morris & MacEachern 2010). It is still unclear to what extent
2 DENSITY DEPENDENCE IN MOVEMENTS 759 dispersal and movements in general are density dependent, and what mechanisms regulate densitydependent movements (Matthysen 2005). Two factors known to affect animal movements are variation in resources and reproductive activity, which vary (Doerr & Doerr 2004; Garcia et al. 2005; Loretto & Vieira 2005), and may affect the amount of movement necessary to find food or to reproduce. In such cases, density dependence in movements would be detected, but only as an indirect effect. Direct effects of population density on tortuosity are a result of either an interaction between individuals, or immediate responses to local depletion of resources by a high-density population. If so, direct density dependence would result in a stronger signal of population density per se, whereas indirect effects would result in stronger effects of seasonal variation in resources or reproduction. Here we determine the occurrence and nature of density dependence in path tortuosity of a Neotropical marsupial, the black-eared opossum Didelphis aurita Wied-Neuwied This species is a suitable model to investigate the relative importance of density dependence on animal movements because its demography, reproduction and patterns of habitat preference are relatively well known (Gentile & Cerqueira 1995; Moura et al. 2005; Rademaker & Cerqueira 2006; Kajin et al. 2008) and because it may be a good representative of other opportunistic didelphid marsupials and small mammals. Didelphis aurita is predominantly terrestrial but occasionally uses the arboreal strata (Cunha & Vieira 2005), and is a diet generalist (Astúa de Moraes et al. 2003). Population peaks of D. aurita tend to occur every year, more frequently during the reproductive season, but not consistently associated with a particular climatic season (Mendel et al. 2008). As other congeneric species, D. aurita appears to have a promiscuous mating system (Ryser 1992; Cáceres 2003). The range of individual movements vary among seasons, but for females, this variation is associated with climatic seasons, with larger movement areas in the dry season, whereas for males movements are more affected by reproductive seasons, with larger movement areas during the reproductive season (Loretto & Vieira 2005). Density dependence in movements of this marsupial has never been investigated. Using a model selection approach, we determined the relative importance of population size on movement tortuosity, considering the potential effects of climatic and reproductive seasonality, sex and reproductive status of individuals, all likely determinants of movement tortuosity. Path tortuosity may be (i) inversely related to population sizes, contributing to a negative feedback and regulatory process of abundance; (ii) directly related to population size, indicating that population sizes and tortuosity are both responses to common environmental factors; or (iii) unrelated to direct changes in population size, reflecting only changes in seasonal resource availability or reproductive activity. METHODS Individuals of D. aurita were sampled in bimonthly trapping sessions of 5 days from 1997 to 2006, as part of a large capture recapture program performed by Laboratório de Vertebrados, Universidade Federal do Rio de Janeiro. The study area is within a protected area of the Brazilian Atlantic Forest inside the Parque Nacional da Serra dos Órgãos, state of Rio de Janeiro ( S, W). The studied area harbours a diverse community of small mammals composed of at least seven species of small rodents and eight species of marsupials (Olifiers et al. 2007). Three 0.64 ha grids were sampled, each with 25 trap stations (each station with two traps) spaced 20 m apart in a 5 5 design (details in Gentile et al. 2004). Some captured individuals were equipped with a spooland-line device that consisted of a bobbinless cocoon of nylon thread (Cansew Inc., Montreal), wrapped in polyvinyl chloride (PVC) film (Boonstra & Craine 1986; Miles et al. 2009). Spools weighed either 1.7 g (175 m of thread) or 4.5 g (480 m of thread), with the small spool only deployed on young D. aurita. The spool was attached between the shoulder blades of individuals using an estercyanoacrylate-based glue. Anaesthetics were not necessary because animals were handled quickly and without injury. Marks of the attached spools had disappeared from individuals recaptured in the following trapping sessions, confirming that the procedure was harmless to the animals (as in Steinwald et al. 2006). All animals were treated carefully following the guidelines of the American Society of Mammalogists (Sikes et al. 2011) and were released at the point of their capture. Animal paths were tracked at least 4 h after animal release. Paths were mapped by taking polar coordinates (azimuth and distance) between points of change in movement direction ( 5 ). The first 20 m of movement were discarded from analysis, to avoid the potential influence of escaping behaviour on movement tortuosity. Arboreal movements were infrequent, corresponding to less than 3% of the paths of the individuals on average (Cunha & Vieira 2005), and therefore were not considered in the analyses. For short arboreal movements (<5 m), we assumed a straight line between the two consecutive ground movements, whereas longer arboreal movements ( 5 m) were not recorded, the tracking being interrupted when they occurred. Data analysis To quantify path tortuosity, we calculated the fractal mean index, D (Dicke & Burrough 1988; Nams 2005), using the software Fractal v (Villis O. Nams. Department of Environmental Sciences, Nova Scotia Agricultural College, Canada).This index represents a measure of tortuosity and is
3 760 P. J. A. L. ALMEIDA ET AL. based on the theoretical framework of fractal geometry (Mandelbrot 1983). It is easy to interpret, has a clear theoretical background and is little affected by location errors or spatial scale (Almeida et al. 2010; Prevedello et al. 2010). In general, an increase in D is related to a more intensive use of areas by individuals (Fig. 1; Almeida et al. 2010). To better characterize movement patterns, we used only paths longer than 30 m in the analyses, which accounted for 94.9% of all paths recorded. We adopted a model selection approach to determine the relative importance of population size on tortuosity. The models considered population size as a predictor variable, but also season (reproductive/non-reproductive for males, humid/super-humid for females), sex and reproductive status (young/adult), all likely determinants of movement tortuosity. Because density dependence in tortuosity may occur only in particular seasons or only for individuals with a particular reproductive status, interaction terms between population size and these variables were also included in the models. The a priori chosen model set thus comprised the possible additive combinations of these previously selected variables, including these two interaction terms. These models summarize pre-existing information on factors likely affecting movements in this species and population, and should allow isolation of density-dependent effects on tortuosity. Population size was estimated using the software CAPTURE V (Rexstad & Burnham 1991), implemented inside program MARK (White & Burnham 1999). We used the Mh model and the Jackknife estimator in order to account for possible heterogeneity inside the population, either due to gender or age-class differences. Climatic seasons were defined using an ombrothermic diagram (Bagnouls & Gaussen 1957) and the climatological normals for Teresópolis, the closest meteorological station (Instituto Nacional de Meteorologia 1992). There was no evidence of real hydric deficit during the studied months in the area of study (Walter 1986). The climatic series indicated a superhumid period from October to May, when monthly averaged precipitation exceeded 75 mm, and a humid period from June to September (previously classified as wet and dry seasons in Loretto & Vieira 2005). The reproductive season was defined as the period when females had newborns or lactation activity, which occurred from the end of May until the end of January, during the humid season and the beginning of the super-humid season. Therefore, the super-humid and reproductive seasons overlap to a large degree, but the reproductive season is longer. Individuals were considered reproductively mature if they had the third molar present, based on Macedo et al. (2006). Tortuosity was analysed separately for males and females because range and concentration of movements varies seasonally, but in males according to reproductive/nonreproductive seasons, whereas in females according to humid/super-humid seasons (Loretto & Vieira 2005). To determine if tortuosity followed the same pattern for males and females, initially two possible full models for males and females were compared, both containing all predictor variables differing only in the classification of seasons: by reproductive or climatic season. For each model, we calculated the Akaike information criterion corrected for small sizes (AICc), Δ i and Akaike doi: /aec weights (w i, the weight of evidence that model i is the best model in the set). The relative importance of each predictor variable was obtained by summing the w i of all models containing the variable (Burnham & Anderson 1998). Parameter estimates for each explanatory variable were calculated by averaging across all models. RESULTS We successfully tracked the movements of 149 individuals, comprising 75 males and 74 females. Examples of typical female tracks in different seasons are shown in Figure 1. The full model for females using climatic seasons had more support from the data (AICc = ) than the full model using reproductive/non-reproductive seasons (AICc = , Δ=3.282). The opposite occurred for males as expected, even though the difference between the full model with climatic seasons (AICc = ) and the one with reproduction seasons (AICc = ) was small (Δ =0.441). Therefore, the subsequent analyses were based on a full model with climatic seasons for females, but with reproductive seasons for males. The most plausible models for both males and females included population size as a determinant of movement tortuosity, but also reproductive or climatic season, and reproductive maturity (Table 1). (a) (b) Fig. 1. Adult female path in the humid season Total path lenght = 364 m D Fractal =1.19 Adult female path in the super-humid season Total path lenght = 379 m D Fractal =1.49 Examples of movement paths of Didelphis aurita Ecological Society of Australia
4 DENSITY DEPENDENCE IN MOVEMENTS 761 Table 1. Performance of the most plausible models explaining movement tortuosity of females and males of D. aurita Model K Log-likelihood AICc Δi w i a) Females Clim.seas + Maturity + Population size Clim.seas + Pop.size Pop.size Maturity + Pop.size Clim.seas + Maturity + Pop.size + Pop.size*Maturity Clim.seas + Maturity + Pop.size + Pop.size*Climatic season Clim.seas + Maturity Clim.seas + Pop.size + Pop.size*Clim.seas Clim.seas Maturity + Pop.size + Pop.size*Maturity Null b) Males Maturity + Pop.size Repr.seas Repr.seas + Pop.size Repr.seas + Pop.size Repr.seas + Maturity + Pop.size Repr.seas + Maturity Repr.seas + Pop.size + Pop.size*Maturity Null All models included one parameter for the intercept and one for residual variation. Only models with Δ i Δ null model are shown. *, interaction terms; Δi, AICc minimum AICc; AICc, Akaike information criteria corrected; Clim.seas, climatic season; Repr.seas, reproductive season; w i, Akaike weights. Table 2. Average model explaining movement tortuosity of females and males of D. aurita Variable ˆβ SE Importance (Σ wi) a) Females Population size Season: humid (compared with super-humid) Maturity: immature (compared with mature individuals) Interaction: population size*maturity Interaction: population size*season b) Males Population size Season: reproductive (compared with non-reproductive) Maturity: immature (compared with mature individuals) Interaction: population size*maturity Interaction: population size*season The average model was based on all models in the set. ˆβ, standardized coefficient; Σwi, sum of Akaike weights of the models including the variable; SE, standard error. Accordingly, population size had high support from the data, but also seasonality and reproductive maturity, as inferred from the sum of w i values (Table 2). In both males and females, the effect of population size on tortuosity was positive, as revealed by the positive (and almost identical) regression coefficients (Table 2). Tortuosity was higher in young individuals compared with adults, also with almost identical coefficients for males and females (Table 2). For males, tortuosity was higher in the reproductive compared with the nonreproductive season, whereas for females tortuosity was higher in the humid compared with the superhumid season (Table 2). DISCUSSION We confirmed the hypothesis that movements in D. aurita are direct density dependent: population size
5 762 P. J. A. L. ALMEIDA ET AL. was the most important determinant of movement tortuosity, with season and reproductive maturity as secondary but also important variables. The nature of density dependence, however, was positive: path tortuosity increased with population size, independent of the effects of seasonality and reproductive maturity of individuals. Therefore, movement tortuosity is not contributing to a potential feedback or regulatory process of population size (sensu Royama 1992; Berryman 1999). Assuming that a higher tortuosity is related to a more intensive exploitation of the environment at every step of the path, more intensive exploitation was directly related to population size. Therefore, either (i) higher population sizes force individuals to explore the environment more intensively, or (ii) the opposite, by exploring their environments more intensively, individuals have more concentrated movements, which allow higher concentration of individuals, higher density and population size. In the first hypothesis, intraspecific competition must be the driving force: when density is low, individuals may explore larger areas of habitat in a less intensive pattern, thus resulting in more linear paths; when density is high, individuals may be forced to concentrate their activities in smaller areas, exploring them more intensively in an attempt to obtain the necessary resources. In the second hypothesis, causality is reversed and density dependence is indirect: higher resource availability would make individuals explore the environment more intensively, which would result in higher concentration of individuals, higher density and population size. Intraspecific competition seems more intense in high-density periods, as average body mass is lower in these periods (Mendel et al. 2008), which supports the first hypothesis of higher tortuosity resulting from more intense intraspecific competition in high-density periods. These contrasting hypotheses must be further tested in studies combining estimates of tortuosity of movement paths with estimates of movement areas, population size and resource availability. The effects of population size on movement tortuosity were only appropriately detected and quantified when taking into account the other important sources of variation: seasonality in resources (climatic seasons) or in reproduction, and reproductive maturity of individuals. The evidence provided by the data supports both as similarly important in models. In the humid season movements of females were less tortuous than in the super-humid season, which matches large movement areas and lower intensity of use (amount of thread per square root of movement area) in the humid season observed previously for females in the same population (Loretto & Vieira 2005). For males, however, movements in the reproductive season were more tortuous than in the non-reproductive doi: /aec season, but movement areas were larger as well, and intensity of use was lower in the same season (Loretto & Vieira 2005).The more tortuous movement of males over larger areas during the reproductive season may allow a more efficient search for females, considering that habitat scanning is more thorough. This higher tortuosity was apparently not captured by the intensity of use index (Loretto & Vieira 2005), probably because for a given amount of tracked thread, larger movement areas are always related to lower intensity of use values. The more tortuous paths of reproductively immature individuals are to be expected considering that young and immature individuals have less experience searching for resources and moving in yet unfamiliar areas. In addition, reproductively immature individuals usually have a smaller body size, thus facing more obstacles in their way, which could lead to increased movement tortuosity. The negative relationship between body size and movement tortuosity has been shown for individuals of D. aurita in translocation experiments (Prevedello et al. 2010). Young D. aurita also use the arboreal strata slightly more frequently than adults (Cunha & Vieira 2005), which is also likely to contribute to keeping them concentrated in smaller horizontal areas. Movements of D. aurita were density dependent, with more intensive use of smaller areas by individuals during periods of high population size. The positive nature of this density dependence probably results from higher intraspecific competition at higher population sizes, forcing individuals to explore their environment more intensively. Therefore, movements apparently do not contribute to population regulation in this species, which may represent a general pattern for other opportunistic didelphid marsupials and small mammals. ACKNOWLEDGEMENTS We thank A. M. Marcondes, Nélio Barros and Reginaldo Honorato for administrative and laboratory help, and the consecutive generations of undergraduate and graduate students of Laboratório de Vertebrados, UFRJ, for the indispensable help at collecting the data. Financial support was provided by grants from Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ/CNE to R. Cerqueira and M. V. Vieira, and FAPERJ/APQ1 to M. Kajin), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/PQ, PPBio and PELD to R. Cerqueira and M.V.Vieira), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES to Rui Cerqueira and a scholarship to P. Almeida for his M.Sc. Degree), PROBIOII/MCT/ MMS/GEF (to R. Cerqueira) and FAPESP 2015 Ecological Society of Australia
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