Socio-Spatial Organization and Kin Structure in Ocelots from Integration of Camera Trapping and Noninvasive Genetics

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Socio-Spatial Organization and Kin Structure in Ocelots from Integration of Camera Trapping and Noninvasive Genetics Journal of Mammalogy, 96(1):120–128, 2015 DOI:10.1093/jmamma/gyu012 Socio-spatial organization and kin structure in ocelots from integration of camera trapping and noninvasive genetics Torrey W. Rodgers,* Jacalyn Giacalone, Edward J. Heske, Jan E. JaneČka, Patrick A. Jansen, Christopher A. Phillips, and Robert L. Schooley Department of Animal Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL 61801, USA (TWR, EJH) Smithsonian Tropical Research Institute, 0843-03092 Balboa, Ancon, Panama (TWR, JG, PAJ) Montclair State University, 1 Normal Avenue, Montclair, NJ 07043, USA (JG) Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801, USA (RLS) Department of Biological Sciences, Duquesne University, 600 Forbes Avenue, Pittsburgh, PA 15282, USA (JEJ) Department of Environmental Sciences, Wageningen University and Research Centre, PO Box 47, 6700 AA Wageningen, The Netherlands (PAJ) Illinois Natural History Survey, Prairie Research Institute, University of Illinois, 1816 S. Oak, Champaign, IL 61820, USA (EJH, CAP) * Correspondent: [email protected] Kin selection theory predicts that under certain conditions animals will tolerate related individuals in their home ranges. We examined the relationship between spatiotemporal overlap and genetic relatedness in ocelots (Leopardus pardalis) to determine if kin selection plays a role in structuring ocelot populations. We used 3 years of camera trapping to examine the spatial organization of an ocelot population on Barro Colorado Island in Panama. We also placed camera traps on ocelot latrines to match photographs of individual ocelots with microsatellite genotypes from feces. Strengths of spatiotemporal overlap between individual ocelots were calculated using a half-weight association index based on how often individuals were photographed at the same camera within 30 days of one another. We calculated relatedness between individuals based on 11 variable microsatellite loci. Male ocelots overlapped with ≤ 11 females, and females overlapped with ≤ 7 males. We detected no clear evidence of strict intersexual territoriality in either sex. Mean overlap among males was more than 5 times greater than overlap among females; however, spatiotemporal overlap was strong between some female pairs. Overall, overlapping individuals were more related to one another than was the sample population as a whole, consistent with the hypothesis that kin selection influences ocelot spatial organization. This finding was driven by relatedness among overlapping females, and by relatedness among overlapping individuals of opposite sex, but not by overlapping males. Key words: Barro Colorado Island, genetic relatedness, Leopardus pardalis, ocelot, space-use overlap, spatial organization © 2015 American Society of Mammalogists, www.mammalogy.org Space use by individual animals is dictated by the need to overlap in their use of space (Davies and Houston 1984). At acquire the resources necessary to maximize fitness such as low population density the cost of territoriality may be low food, mates, or den sites. Consequently, the spatial organization because there will be few competitors from which a home of individuals at the population level is determined by intraspe- range must be defended. At high population density, however, cific competition for these resources, as well as by the abundance the cost of defending a territory from many competitors may and dispersion of the resources themselves (Clutton-Brock be high, resulting in overlap in space use among individuals. and Harvey 1978; Macdonald 1983; Sandell 1989; Nicholson The amount of overlap may in turn be determined by the dis- et al. 2011; Lührs and Kappeler 2013). If the fitness benefits persion of resources in the environment. If resources are het- of defending these resources outweigh the costs, then animals erogeneously distributed in the environment as is common in will defend exclusive territories. Conversely, if the fitness costs most natural systems (Johnson et al. 2002), then when condi- of territory defense outweigh the benefits, individuals should tions are favorable, multiple individuals may share resources 120 RODGERS ET AL.—OCELOT SPATIAL ORGANIZATION 121 within a given area at little cost to each other (i.e., the resource We had 2 goals in this study. First, we investigated patterns dispersion hypothesis—Macdonald 1983; Carr and Macdonald of intersexual and intrasexual overlap between individuals to 1986). This outcome does not negate all competition between gain insight into spatial organization of ocelots in a high-den- individuals that overlap however, especially during times of sity population. We hypothesized that ocelots would overlap in resource shortage (Johnson et al. 2002). their use of space both between and within each sex and would If individuals overlap in their space use and are competing not defend territories because of the high cost of defending a for shared resources, one mechanism that could minimize fit- home range from many competitors at high population density. ness costs due to competition is kin selection. Kin selection the- To test this hypothesis, we conducted a camera-trap study of ory predicts that organisms will be more tolerant of competition the ocelot population on Barro Colorado Island for 3 years. from relatives than from unrelated individuals because when Camera trapping enabled us to sample the entire adult popula- relatives share limited resources, inclusive fitness benefits off- tion in our study area throughout the study period, which would set the individual fitness costs of competition (Hamilton 1964; have been logistically unfeasible with radiotelemetry. To our Wade and Breden 1987). Female philopatry and male disper- knowledge, this is the 1st study to examine overlap in space use sal are typical among mammals (Greenwood 1980) including in a carnivore species with camera trapping. solitary carnivores (Waser and Jones 1983), thus relatedness Second, we evaluated whether kin structure was evident among individuals sharing space is often higher among females within the population to determine if genetic relatedness plays than among males. Relationships between spatial overlap and a role in structuring ocelot spatial organization. Space use for genetic relatedness have been investigated for many mammals females is most strongly tied to allocation of resources neces- including carnivores (Kitchen et al. 2005; Moyer et al. 2006; sary for rearing offspring, whereas for males, the most impor- Nicholson et al. 2011); however, such relationships for small tant resource is likely access to females (Clutton-Brock and solitary felids are poorly understood and seldom investigated Harvey 1978; Sandell 1989). We hypothesized that for both (but see Janečka et al. 2006) because solitary carnivores are sexes inclusive fitness benefits can reduce costs of sharing these generally elusive, and are thus difficult to study in the wild. resources with overlapping individuals. As a result, individuals By integrating 2 noninvasive techniques, we developed a should be more tolerant of sharing space and resources with novel approach to gain new insight into this relationship for a relatives than with nonrelatives. Therefore, we predicted that solitary felid. individuals of the same sex that overlap in their use of space We examined the relationship between spatiotemporal over- would be more closely related than individuals of the same sex lap and genetic relatedness in an ocelot (Leopardus pardalis) in the population as a whole. Finally, we hypothesized that indi- population to determine if spatial structure was consistent with viduals would avoid overlapping with relatives of the opposite predictions arising from kin selection theory. We worked on sex to avoid inbreeding (Pusey 1987). Therefore, we predicted Barro Colorado Island, an island in the Panama Canal that offers that relatedness between males and females that overlap with a unique opportunity to investigate this relationship because it one another would be low. To test these predictions, we used a has the highest ocelot density ever reported (> 1.5 individuals/ novel approach that integrated camera trapping with noninva- km2—Rodgers et al. 2014), likely due to an abundant prey base, sive genetics. and release from competition from larger predators (Moreno et al. 2006). Studying such a population is particularly interest- ing because it provides insight into the dynamics and flexibility Materials and Methods of socio-spatial organization at one extreme of the popula- Study site.—Field work was conducted on Barro Colorado tion density spectrum. Ocelots, like most felids, are typically Island, a 1,543-ha island in the Panama Canal waterway, at a described as solitary and territorial (Sunquist and Sunquist research station operated by the Smithsonian Tropical Research 2002); however, reported patterns of spatial overlap between Institute (Fig. 1). Barro Colorado Island (9°10′N, 79°51′W) sits individuals vary. As is the norm for most carnivore species within Gatun Lake, an artificial body of water created in 1912 by (Sandell 1989), all ocelot studies report intersexual overlap in the damming of the Chagres River to create the Panama Canal, which males overlap with several females. As for intrasexual and is part of the protected 54-km2 Barro Colorado Nature overlap, studies have reported that both female and male oce- Monument. Vegetation is tropical moist forest, and topography lots maintain exclusive
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