Lisa M. Lyren

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.

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.

Frequent Transmission of Immunodeficiency Viruses among Bobcats and Pumas

ABSTRACT With the exception of human immunodeficiency virus (HIV), which emerged in humans after cross-species transmissions of simian immunodeficiency viruses from nonhuman primates, immunodeficiency viruses of the family Lentiviridae represent species-specific viruses that rarely cross species barriers to infect new hosts. Among the Felidae, numerous immunodeficiency-like lentiviruses have been documented, but only a few cross-species transmissions have been recorded, and these have not been perpetuated in the recipient species. Lentivirus seroprevalence was determined for 79 bobcats (Lynx rufus) and 31 pumas (Puma concolor) from well-defined populations in Southern California. Partial genomic sequences were subsequently obtained from 18 and 12 seropositive bobcats and pumas, respectively. Genotypes were analyzed for phylogenic relatedness and genotypic composition among the study set and archived feline lentivirus sequences. This investigation of feline immunodeficiency virus infection in bobcats and pumas of Southern California provides evidence that cross-species infection has occurred frequently among these animals. The data suggest that transmission has occurred in multiple locations and are most consistent with the spread of the virus from bobcats to pumas. Although the ultimate causes remain unknown, these transmission events may occur as a result of puma predation on bobcats, a situation similar to that which fostered transmission of HIV to humans, and likely represent the emergence of a lentivirus with relaxed barriers to cross-species transmission. This unusual observation provides a valuable opportunity to evaluate the ecological, behavioral, and molecular conditions that favor repeated transmissions and persistence of lentivirus between species.

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 ...

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.

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.

Urban Habitat Fragmentation and Genetic Population Structure of Bobcats in Coastal Southern California

Abstract Although habitat fragmentation is recognized as a primary threat to biodiversity, the effects of urban development on genetic population structure vary among species and landscapes and are not yet well understood. Here we use non-invasive genetic sampling to compare the effects of fragmentation by major roads and urban development on levels of dispersal, genetic diversity, and relatedness between paired bobcat populations in replicate landscapes in coastal southern California. We hypothesized that bobcat populations in sites surrounded by urbanization would experience reduced functional connectivity relative to less isolated nearby populations. Our results show that bobcat genetic population structure is affected by roads and development but not always as predicted by the degree that these landscape features surround fragments. Instead, we suggest that urban development may affect functional connectivity between bobcat populations more by limiting the number and genetic diversity of source populations of migrants than by creating impermeable barriers to dispersal.

Pathogen exposure varies widely among sympatric populations of wild and domestic felids across the United States

Understanding how landscape, host, and pathogen traits contribute to disease exposure requires systematic evaluations of pathogens within and among host species and geographic regions. The relative importance of these attributes is critical for management of wildlife and mitigating domestic animal and human disease, particularly given rapid ecological changes, such as urbanization. We screened > 1000 samples from sympatric populations of puma (Puma concolor), bobcat (Lynx rufus), and domestic cat (Felis catus) across urban gradients in six sites, representing three regions, in North America for exposure to a representative suite of bacterial, protozoal, and viral pathogens (Bartonella sp., Toxoplasma gondii, feline herpesvirus-1, feline panleukopenea virus, feline calicivirus, and feline immunodeficiency virus). We evaluated prevalence within each species, and examined host trait and land cover determinants of exposure; providing an unprecedented analysis of factors relating to potential for infections in domesticated and wild felids. Prevalence differed among host species (highest for puma and lowest for domestic cat) and was greater for indirectly transmitted pathogens. Sex was inconsistently predictive of exposure to directly transmitted pathogens only, and age infrequently predictive of both direct and indirectly transmitted pathogens. Determinants of pathogen exposure were widely divergent between the wild felid species. For puma, suburban land use predicted increased exposure to Bartonella sp. in southern California, and FHV-1 exposure increased near urban edges in Florida. This may suggest interspecific transmission with domestic cats via flea vectors (California) and direct contact (Florida) around urban boundaries. Bobcats captured near urban areas had increased exposure to T. gondii in Florida, suggesting an urban source of prey Bobcats captured near urban areas in Colorado and Florida had higher FIV exposure, possibly suggesting increased intraspecific interactions through pile-up of home ranges. Beyond these regional and pathogen specific relationships, proximity to the wildland-urban interface did not generally increase the probability of disease exposure in wild or domestic felids, empha- sizing the importance of local ecological determinants. Indeed, pathogen exposure was often negatively associated with the wildland-urban interface for all felids. Our analyses suggest cross-species pathogen transmission events around this interface may be infrequent, but followed by self-sustaining propagation within the new host species. virus; puma (Puma concolor); Toxoplasma gondii; urbanization.

Variability in assays used for detection of lentiviral infection in bobcats (Lynx rufus), pumas (Puma concolor), and ocelots (Leopardus pardalis).

Although lentiviruses similar to feline immunodeficiency virus (FIV) are known to infect numerous felid species, the relative utility of assays used for detecting lentiviral infection has not been compared for many of these hosts. We tested bobcats (Lynx rufus), pumas (Felis concolor), and ocelots (Leopardus pardalis) for exposure to lentivirus using five different assays: puma lentivirus (PLV), African lion lentivirus (LLV), and domestic cat FIV-based immunoblots, a commercially available enzyme-linked immunosorbent assay (ELISA) kit, and nested polymerase chain reaction (PCR). Puma lentivirus immunoblots identified more seropositive individuals than the other antibody-detection assays. The commercial ELISA provided a fair ability to recognize seropositive samples when compared with PLV immunoblot for screening bobcats and ocelots, but not pumas. Polymerase chain reaction identified fewer positive samples than PLV immunoblot for all three species. Immunoblot results were equivalent whether the sample tested was serum, plasma, or whole blood. The results from this study and previous investigations suggest that the PLV immunoblot has the greatest ability to detect reactive samples when screening wild felids of North America and is unlikely to produce false positive results. However, the commercial ELISA kit may provide an adequate alternative for screening of some species and is more easily adapted to field conditions.

Mapping behavioral landscapes for animal movement: a finite mixture modeling approach

Because of its role in many ecological processes, movement of animals in response to landscape features is an important subject in ecology and conservation biology. In this paper, we develop models of animal movement in relation to objects or fields in a landscape. We took a finite mixture modeling approach in which the component densities are conceptually related to different choices for movement in response to a landscape feature, and the mixing proportions are related to the probability of selecting each response as a function of one or more covariates. We combined particle swarm optimization and an expectation-maximization (EM) algorithm to obtain maximum-likelihood estimates of the model parameters. We used this approach to analyze data for movement of three bobcats in relation to urban areas in southern California, USA. A behavioral interpretation of the models revealed similarities and differences in bobcat movement response to urbanization. All three bobcats avoided urbanization by moving either parallel to urban boundaries or toward less urban areas as the proportion of urban land cover in the surrounding area increased. However, one bobcat, a male with a dispersal-like large-scale movement pattern, avoided urbanization at lower densities and responded strictly by moving parallel to the urban edge. The other two bobcats, which were both residents and occupied similar geographic areas, avoided urban areas using a combination of movements parallel to the urban edge and movement toward areas of less urbanization. However, the resident female appeared to exhibit greater repulsion at lower levels of urbanization than the resident male, consistent with empirical observations of bobcats in southern California. Using the parameterized finite mixture models, we mapped behavioral states to geographic space, creating a representation of a behavioral landscape. This approach can provide guidance for conservation planning based on analysis of animal movement data using statistical models, thereby linking connectivity evaluations to empirical data.