Erin E. Boydston

Effects of urbanization on carnivore species distribution and richness

Abstract Urban development can have multiple effects on mammalian carnivore communities. We conducted a meta-analysis of 7,929 photographs from 217 localities in 11 camera-trap studies across coastal southern California to describe habitat use and determine the effects of urban proximity (distance to urban edge) and intensity (percentage of area urbanized) on carnivore occurrence and species richness in natural habitats close to the urban boundary. Coyotes (Canis latrans) and bobcats (Lynx rufus) were distributed widely across the region. Domestic dogs (Canis lupus familiaris), striped skunks (Mephitis mephitis), raccoons (Procyon lotor), gray foxes (Urocyon cinereoargenteus), mountain lions (Puma concolor), and Virginia opossums (Didelphis virginiana) were detected less frequently, and long-tailed weasels (Mustela frenata), American badgers (Taxidea taxus), western spotted skunks (Spilogale gracilis), and domestic cats (Felis catus) were detected rarely. Habitat use generally reflected availability for most species. Coyote and raccoon occurrence increased with both proximity to and intensity of urbanization, whereas bobcat, gray fox, and mountain lion occurrence decreased with urban proximity and intensity. Domestic dogs and Virginia opossums exhibited positive and weak negative relationships, respectively, with urban intensity but were unaffected by urban proximity. Striped skunk occurrence increased with urban proximity but decreased with urban intensity. Native species richness was negatively associated with urban intensity but not urban proximity, probably because of the stronger negative response of individual species to urban intensity.

Altered behaviour in spotted hyenas associated with increased human activity

To investigate how anthropogenic activity might affect large carnivores, we studied the behaviour of spotted hyenas (Crocuta crocuta) during two time periods. From 1996 to 1998, we documented the ecological correlates of space utilization patterns exhibited by adult female hyenas defending a territory at the edge of a wildlife reserve in Kenya. Hyenas preferred areas near dense vegetation but appeared to avoid areas containing the greatest abundance of prey, perhaps because these were also the areas of most intensive livestock grazing. We then compared hyena behaviour observed in 1996‐98 with that observed several years earlier and found many differences. Female hyenas in 1996‐98 were found farther from dens, but closer to dense vegetation and to the edges of their territory, than in 1988‐90. Recent females also had larger home ranges, travelled farther between consecutive sightings, and were more nocturnal than in 1988‐90. Finally, hyenas occurred in smaller groups in 1996‐98 than in 1988‐90. We also found several changes in hyena demography between periods. We next attempted to explain differences observed between time periods by testing predictions of hypotheses invoking prey abundance, climate, interactions with lions, tourism and livestock grazing. Our data were consistent with the hypothesis that increased reliance on the reserve for livestock grazing was responsible for observed changes. That behavioural changes were not associated with decreased hyena population density suggests the behavioural plasticity typical of this species may protect it from extinction.

Three Pathogens in Sympatric Populations of Pumas, Bobcats, and Domestic Cats: Implications for Infectious Disease Transmission

Anthropogenic landscape change can lead to increased opportunities for pathogen transmission between domestic and non-domestic animals. Pumas, bobcats, and domestic cats are sympatric in many areas of North America and share many of the same pathogens, some of which are zoonotic. We analyzed bobcat, puma, and feral domestic cat samples collected from targeted geographic areas. We examined exposure to three pathogens that are taxonomically diverse (bacterial, protozoal, viral), that incorporate multiple transmission strategies (vector-borne, environmental exposure/ingestion, and direct contact), and that vary in species-specificity. Bartonella spp., Feline Immunodeficiency Virus (FIV), and Toxoplasma gondii IgG were detected in all three species with mean respective prevalence as follows: puma 16%, 41% and 75%; bobcat 31%, 22% and 43%; domestic cat 45%, 10% and 1%. Bartonella spp. were highly prevalent among domestic cats in Southern California compared to other cohort groups. Feline Immunodeficiency Virus exposure was primarily associated with species and age, and was not influenced by geographic location. Pumas were more likely to be infected with FIV than bobcats, with domestic cats having the lowest infection rate. Toxoplasma gondii seroprevalence was high in both pumas and bobcats across all sites; in contrast, few domestic cats were seropositive, despite the fact that feral, free ranging domestic cats were targeted in this study. Interestingly, a directly transmitted species-specific disease (FIV) was not associated with geographic location, while exposure to indirectly transmitted diseases – vector-borne for Bartonella spp. and ingestion of oocysts via infected prey or environmental exposure for T. gondii – varied significantly by site. Pathogens transmitted by direct contact may be more dependent upon individual behaviors and intra-specific encounters. Future studies will integrate host density, as well as landscape features, to better understand the mechanisms driving disease exposure and to predict zones of cross-species pathogen transmission among wild and domestic felids.

INDIVIDUAL VARIATION IN SPACE USE BY FEMALE SPOTTED HYENAS

Abstract Large carnivores range more widely than many other terrestrial mammals, and this behavior tends to bring them into frequent conflict with humans. Within any carnivore population, individual variation in patterns of space use should be expected to make some animals more vulnerable than others to risks of mortality from humans and other sources. In this study, our goal was to document variation among individuals in space use by female spotted hyenas (Crocuta crocuta). We examined predictions of hypotheses suggesting that space use by female hyenas is affected by reproductive state, social rank, and local prey abundance. Home-range size, distance at which females were found from the current communal den, and distance at which they were found from the nearest territorial boundary all varied significantly with the 3 independent variables. Females with den-dwelling cubs had smaller home ranges, were found closer to the communal den, and were found farther from the territorial boundary than were females with no den-dwelling cubs. Neither social rank nor prey availability significantly influenced the space-use patterns of females with den-dwelling cubs. Among females with no den-dwelling cubs, high-ranking females had smaller home ranges, were closer to the communal den, and were farther from the territorial boundary than were low-ranking females. The females ranging most widely were low-ranking individuals with no den-dwelling cubs when they were observed during periods of prey scarcity.

Interfacing models of wildlife habitat and human development to predict the future distribution of puma habitat.

The impact of human land uses on ecological systems typically differ relative to how extensively natural conditions are modified. Exurban development is intermediate-intensity residential development that often occurs in natural landscapes. Most species-habitat models do not evaluate the effects of such intermediate levels of human development and even fewer predict how future development patterns might affect the amount and configuration of habitat. We addressed these deficiencies by interfacing a habitat model with a spatially-explicit housing-density model to study the effect of human land uses on the habitat of pumas (Puma concolor) in southern California. We studied the response of pumas to natural and anthropogenic features within their home ranges and how mortality risk varied across a gradient of human development. We also used our housing-density model to estimate past and future housing densities and model the distribution of puma habitat in 1970, 2000, and 2030. The natural landscape for pumas ...

Taphonomic and zooarchaeological implications of spotted hyena (Crocuta crocuta) bone accumulations in Kenya: a modern behavioral ecological approach

Abstract The significant impact of extant carnivores, particularly spotted hyenas, on the depositional history and physical characteristics of archaeofaunal and paleontological assemblages is well recognized. We focus on the behavioral ecology of extant spotted hyenas (Crocuta crocuta) in relation to bone accumulations produced by one East African clan at communal dens. Limbs and skulls of prey animals more frequently appear at dens than do other carcass portions. These items reflect the relative abundance of prey species near dens; carnivore remains are poorly represented. Comparative analysis reveals that bones are deposited far more slowly (<7 carcass portions per month) and accumulations tend to be smaller at Crocuta dens than at dens of either brown (Parahyaena brunnea) or striped (Hyaena hyaena) hyenas. We propose that extant Crocuta bone accumulation rates and sizes are likely affected by prey species abundance, clan size, social interactions within the clan, and the type and availability of den sites. We also suggest that the potential for intraspecific behavioral variability in bone accumulation patterns is important when comparisons are made among spotted hyena populations and across hyena species. For example, accumulation patterns may be dramatically influenced by the temporal span, potentially ranging from days to hundreds or thousands of years, in which bones are collected, depending on the species-specific history of occupation at a given site. Understanding the behavioral and ecological variability likely to influence bone accumulation patterns at dens used by different hyaenids will allow taphonomists and zooarchaeologists to refine their knowledge of mechanisms underlying site formation processes and potential causes of variability in deeper-time den assemblages.

Gene flow and pathogen transmission among bobcats (Lynx rufus) in a fragmented urban landscape.

Urbanization can result in the fragmentation of once contiguous natural landscapes into a patchy habitat interspersed within a growing urban matrix. Animals living in fragmented landscapes often have reduced movement among habitat patches because of avoidance of intervening human development, which potentially leads to both reduced gene flow and pathogen transmission between patches. Mammalian carnivores with large home ranges, such as bobcats (Lynx rufus), may be particularly sensitive to habitat fragmentation. We performed genetic analyses on bobcats and their directly transmitted viral pathogen, feline immunodeficiency virus (FIV), to investigate the effects of urbanization on bobcat movement. We predicted that urban development, including major freeways, would limit bobcat movement and result in genetically structured host and pathogen populations. We analysed molecular markers from 106 bobcats and 19 FIV isolates from seropositive animals in urban southern California. Our findings indicate that reduced gene flow between two primary habitat patches has resulted in genetically distinct bobcat subpopulations separated by urban development including a major highway. However, the distribution of genetic diversity among FIV isolates determined through phylogenetic analyses indicates that pathogen genotypes are less spatially structured—exhibiting a more even distribution between habitat fragments. We conclude that the types of movement and contact sufficient for disease transmission occur with enough frequency to preclude structuring among the viral population, but that the bobcat population is structured owing to low levels of effective bobcat migration resulting in gene flow. We illustrate the utility in using multiple molecular markers that differentially detect movement and gene flow between subpopulations when assessing connectivity.

Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta)

Observational and telemetry data were used in a geographic information system database to document the ontogenetic development of sexually dimorphic patterns of space use among free-living spotted hyenas Crocuta crocuta in Kenya. No measures of space use were sexually dimorphic among den-dwelling cubs, nor were sex differences apparent among hyenas that had ceased using dens for shelter until these animals were c. 30 months of age. Significant sex differences emerged late in the third year of life, and persisted throughout the remainder of the life span; males were found farther from the geographic centre of the natal territory than were females, and the mean size of individual 95 % utility distributions was larger for males than females. Most dispersal events by radio-collared males were preceded by a series of exploratory excursions outside the natal territory. All collared males dispersed, but no collared females did so. Most dispersing males moved only one or two home ranges away at dispersal, roughly 8–10 km distant from the natal territory, before settling in a new social group.

Courtship and mating in free-living spotted hyenas

Summary Female spotted hyenas (Crocuta crocuta) are larger and more aggressive than males, and their genitalia are heavily ‘masculinized’. These odd traits in females pose unusual challenges for males during courtship and copulation. Here our goals were to describe and quantify the behavior patterns involved in courtship and copulation in Crocuta, and determine whether rates of affiliative behavior directed toward females by males vary with female age, social rank, or time to conception. We also inquired whether consort formation with a particular female was necessary for a male to sire that female’s cubs. Behavioral observations and paternity data based on 12 microsatellite loci were collected over 11 years from free-ranging hyenas in Kenya. Several of the courtship displays exhibited by male hyenas differed from those found in other carnivores, and appeared to reflect intense motivational conflict between tendencies to approach and flee from females. Most male advances were either ignored by females or elicited aggression from females toward males. Rates of male affiliative behavior toward females peaked around the time of conception. Although males behaved similarly toward young and old females in the highest social rank category, males directed more affiliative behavior toward older than younger females that were mid- and low-ranking. Multiple short mounts usually preceded a long mount, but intromission and ejaculation appeared to occur only during long mounts. Female receptivity was indicated by inhibited aggression toward the male and assumption of a distinctive receptive stance. The only behavior indicative of female proceptivity was following of the male by the female in mating contexts. Some males who sired cubs formed consortships with females whereas others did not, suggesting that individual male hyenas may adopt alternative reproductive tactics to attract and acquire mates. Our results also suggest that low fertility may be an important cost of female virilization in this species.

Evolution of Puma Lentivirus in Bobcats (Lynx rufus) and Mountain Lions (Puma concolor) in North America

ABSTRACT Mountain lions (Puma concolor) throughout North and South America are infected with puma lentivirus clade B (PLVB). A second, highly divergent lentiviral clade, PLVA, infects mountain lions in southern California and Florida. Bobcats (Lynx rufus) in these two geographic regions are also infected with PLVA, and to date, this is the only strain of lentivirus identified in bobcats. We sequenced full-length PLV genomes in order to characterize the molecular evolution of PLV in bobcats and mountain lions. Low sequence homology (88% average pairwise identity) and frequent recombination (1 recombination breakpoint per 3 isolates analyzed) were observed in both clades. Viral proteins have markedly different patterns of evolution; sequence homology and negative selection were highest in Gag and Pol and lowest in Vif and Env. A total of 1.7% of sites across the PLV genome evolve under positive selection, indicating that host-imposed selection pressure is an important force shaping PLV evolution. PLVA strains are highly spatially structured, reflecting the population dynamics of their primary host, the bobcat. In contrast, the phylogeography of PLVB reflects the highly mobile mountain lion, with diverse PLVB isolates cocirculating in some areas and genetically related viruses being present in populations separated by thousands of kilometers. We conclude that PLVA and PLVB are two different viral species with distinct feline hosts and evolutionary histories. IMPORTANCE An understanding of viral evolution in natural host populations is a fundamental goal of virology, molecular biology, and disease ecology. Here we provide a detailed analysis of puma lentivirus (PLV) evolution in two natural carnivore hosts, the bobcat and mountain lion. Our results illustrate that PLV evolution is a dynamic process that results from high rates of viral mutation/recombination and host-imposed selection pressure.