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Austral Ecology (2015) 40, 758–764
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-MEDINA6 AND RUI CERQUEIRA2,3 1 Laboratório Nacional de Computação Científica – Coordenação de Matemática Aplicada, Petrópolis (Email:
[email protected]), 2Laboratório de Vertebrados, Departamento de Ecologia, 3Programa 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, 4Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil, and 6Wildlife 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 1826. 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 2015.
ments (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
© 2015 Ecological Society of Australia
doi:10.1111/aec.12250
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 move-
D E N S I T Y D E P E N D E N C E I N M OV E M E N T S
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 1826. 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 © 2015 Ecological Society of Australia
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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 (22°28′28″S, 42°59′86″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 (
