Mammalia 2016; aop Alfredo H. Zúñiga*, Jaime E. Jiménez and Pablo Ramírez de Arellano Activity patterns in sympatric carnivores in the Nahuelbuta Mountain Range, southern-central Chile DOI 10.1515/mammalia-2015-0090 Received June 24, 2015; accepted August 26, 2016 Introduction Abstract: Species interactions determine the structure of Species interactions are one of the most studied topics in biological communities. In particular, interference behav- community ecology, as interspecific behavior can largely ior is critical as dominant species can displace subordi- determine the composition and structure of community nate species depending on local ecological conditions. In assemblages (Case and Gilpin 1974). For carnivores, inter- carnivores, the outcome of interference may have impor- specific interactions are particularly relevant because of tant consequences from the point of view of conservation, their role in top-down control in terrestrial ecosystems especially when vulnerable species are the ones suffering (Terborgh and Winter 1980). Nevertheless, given the key displacement. Using 24 baited camera traps and a sam- role of consumers and through trophic cascades, changes pling effort of 2821 trap nights, we examined the activ- in the environment could promote an increase of medium- ity patterns and spatial overlap of an assemblage of five sized carnivores or mesopredators, due to top predator sympatric carnivores in the Nahuelbuta Mountain Range, removal (Prange and Gehrt 2007) which can cause sub- in southern-central Chile. In this forested landscape we stantial changes in the dynamics of interaction among found predominantly nocturnal activity in all species, but sympatric species (Kamler et al. 2013), with adverse not for the puma (Puma concolor) and to a lesser extent, effects on subordinate species. Thus, to minimize risks, for the guigna (Leopardus guigna). In terms of spatial subordinate species tend to avoid encounters with domi- overlap, there was a non-significant negative relationship nant species (Berger and Gese 2007). between the puma and the culpeo (Lycalopex culpaeus), Coexistence among competitors can occur by minimiz- and a positive relationship among the three smaller spe- ing resource use overlap through niche segregation and cies of the assemblage, the guigna, the hog-nosed skunk complementarity (Jiménez et al. 1996). To avoid interfer- (Conepatus chinga), and the Darwin’s fox (Lycalopex fulvi- ence, subordinate species could modify their activity pat- pes). Culpeo displayed a negative spatial relationship with terns according to that of the dominant species (Carothers the three later species appearing to be a product of inter- and Jaksic 1984). Therefore, subordinate species should ference behavior. Species-specific ecological differences, avoid direct encounters among potential competitors including prey types and spatio-temporal partitioning and prevent interspecific competition (Kronfeld-Schor among the carnivores appear to allow their coexistence. and Dayan 2003). Shifting activity patterns, however, would require flexibility to cope with other environmen- Keywords: assemblage; camera traps; circadian cycle; tal requirements and ecological contexts (Di Bitetti et al. coexistence; interference. 2009, Hayward and Slotow 2009). Further, species’ eco- logical and morphological characteristics and resource use can increase the complexity of interference and the dynamics of the interactions. Donadio and Buskirk (2006) *Corresponding author: Alfredo H. Zúñiga, Laboratorio de Vida proposed that taxonomic and spatial similarities among Silvestre, Departamento de Ciencias Biológicas y Diversidad, Universidad de Los Lagos, Avenida Fuchslocher 1305, Casilla 933, species, as well as their size and respective prey, will Osorno, Chile, e-mail: [email protected] determine the interaction outcome. Jaime E. Jiménez: Department of Biological Sciences and Philosophy Although studies describing activity patterns in car- and Religion Studies, University of North Texas, TX, USA; Estación nivores have recently increased in the Neotropics, they de Campo Parque Etnobotánico Omora, Universidad de Magallanes, mainly focus on pair-wise species interactions (Jácomo Puerto Williams, Chile; and Institute of Ecology and Biodiversity, Chile et al. 2004, Lucherini et al. 2009), which limits the knowl- Pablo Ramírez de Arellano: División de Manejo Ecosistémico, edge about relationships in ecological communities. In Bioforest S. A., Coronel, Chile this sense, in most assemblages, the spatio-temporal Brought to you by | provisional account Authenticated | [email protected] author's copy Download Date | 10/26/16 4:59 PM 2 A.H. Zúñiga et al.: Activity patterns in carnivores dynamics of interactions among syntopic (sensu Rivas Lower elevation areas generally lack native forests and 1964) carnivore species is largely unknown. In the Nahuel- are heavily impacted and eroded with extensive planta- buta Mountain Range of southern Chile, mammals, espe- tions of Pinus radiata and Eucalyptus globulus. Few open cially carnivores, form an assemblage of interest given the areas with herbaceous vegetation and shrubs in various biogeographical isolation of this region (Armesto et al. stages of recovery remain due to past agricultural prac- 1996a) and because this is the only known location where tices and current livestock grazing. Caramávida contains a a diversity of carnivores that otherwise do not co-exist, are high number of endemic fauna (32 species; Armesto et al. syntopic (Murúa 1996). Thus, although only one species 1996b) and has high risks related to human activities, in this area has been studied (Jiménez 2000), time parti- such as logging. Due to this, the area has been considered tioning has not been addressed. Here, we hypothesize that a priority site in need of urgent conservation (Muñoz et al. the small scale co-occurrence of carnivores in Nahuelbuta 1996). can be explained by species’ spatial and temporal segre- gation as a mechanism to avoid interspecific interference through direct encounters. Assessment of activity patterns in carnivores To detect carnivores, we operated 24 Bushnell Trophy Cam camera traps (Bushnell Corporation, Overland Park, KS, Materials and methods USA) between September 2010 and February 2011. We obtained images that allowed unequivocal species identi- Study area fication (Kays and Slauson 2008), with recorded date and time on each image. Four transects of six cameras each Caramávida is a private 10,097-ha area located on the were arranged throughout the study area so that they western slope of the Nahuelbuta Mountain Range covered all the vegetation formations of the area (Luebert (37°41′S, 73°14′W) in south-central Chile (Figure 1). The and Pliscoff 2004). Cameras were spaced 500 m apart climate is Mediterranean-humid (Di Castri and Hajek one from one another (Rovero and Marshall 2009), and 1976), with main precipitation falling during the austral installed 1 m above the ground, fixed to tree trunks and winter months. The terrain is relatively rugged and eleva- baited with canned mackerel (Trachurus murphy, Zielinski tions range from 700 to 1000 m above sea level. The land- and Kucera 1995). Lines of cameras were arranged, on scape presents a combination of pristine and disturbed average, 2 km in distance one from the other (Figure 1). southern beech (Nothofagus spp.) and monkey-puzzle Cameras were active 24 h per day along the whole survey (Araucaria araucana) forests (Luebert and Pliscoff 2004). period. Figure 1: Study area and habitat types present. Dots indicate the locations of cameras. Brought to you by | provisional account Authenticated | [email protected] author's copy Download Date | 10/26/16 4:59 PM A.H. Zúñiga et al.: Activity patterns in carnivores 3 Activity patterns for each species were estimated as 100 the average number of images obtained per hour across ) 80 Night all the daily records. To ensure temporal independence, 60 Dawn species captured in each camera were counted once during 40 Day a single-hour interval. Daytime was grouped into four Dusk discrete periods (Fedriani 1997): dawn (06:01–08:00 h, Percentage (% 20 8.3% of the daily cycle), day (08:01–18:00 h, 41.7%), dusk 0 (18:01–20:00 h, 8.3%), and night (20:01–06:00 h, 41.7%). P. c. L. cu. L. f. L. g. C. ch. Co-use of activity time was assessed through Pianka’s Species overlap index (Pianka 1973). To determine whether Figure 2: Percent activity patterns of carnivores in Caramávida species pair-wise differences were statistically signifi- according to light availability periods. cant, values should fall outside confidence intervals of P. c., Puma concolor; L. cu., Lycalopex culpaeus; L. f., Lycalopex an expected random pattern. We obtained these intervals fulvipes; C. ch., Conepatus chinga; L. g., Leopardus guigna. Periods: through stochastic reallocations with 10,000 iterations, night (20:01–06:00 h), dawn (06:01–08:00 h), day (08:01–18:00 h), using the statistical package Spaa (Zhang et al. 2010) in and dusk (18:01–20:00 h). R statistical software version 0.2.0. The alpha level was set at 5%. Carnivores’ daily activity patterns differed in their variability (Coefficient of variation, puma: 73.7, culpeo: Spatial overlap among species 105.1, Darwin’s fox: 120.2, hog-nosed skunk: 104.8, and guigna: 104.7; Figure 3). However, differences in peaks We log-transformed the frequency of recordings of species among species were not statistically significant (Kruskal- to meet normality assumptions (Zar 1984), applied Bon-
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