Individual Behaviors Dominate the Dynamics of an Urban Mountain Lion Population Isolated by Roads

SummaryLarge carnivores can be particularly sensitive to the effects of habitat fragmentation on genetic diversity [1, 2]. The Santa Monica Mountains (SMMs), a large natural area within Greater Los Angeles, is completely isolated by urban development and the 101 freeway to the north. Yet the SMMs support a population of mountain lions (Puma concolor), a very rare example of a large carnivore persisting within the boundaries of a megacity. GPS locations of radio-collared lions indicate that freeways are a near-absolute barrier to movement. We genotyped 42 lions using 54 microsatellite loci and found that genetic diversity in SMM lions, prior to 2009, was lower than that for any population in North America except in southern Florida, where inbreeding depression led to reproductive failure [3–5]. We document multiple instances of father-daughter inbreeding and high levels of intraspecific strife, including the unexpected behavior of a male killing two of his offspring and a mate and his son killing two of his brothers. Overall, no individuals from the SMMs have successfully dispersed. Gene flow is critical for this population, and we show that a single male immigrated in 2009, successfully mated, and substantially enhanced genetic diversity. Our results imply that individual behaviors, most likely caused by limited area and reduced opportunities to disperse, may dominate the fate of small, isolated populations of large carnivores. Consequently, comprehensive behavioral monitoring can suggest novel solutions for the persistence of small populations, such as the transfer of individuals across dispersal barriers

Efficient recovery of whole blood RNA - a comparison of commercial RNA extraction protocols for high-throughput applications in wildlife species

Conclusion: By carefully choosing the appropriate RNA extraction method, whole blood can become a valuable source for high-throughput applications like expression arrays or transcriptome sequencing from natural populations. Additionally, candidate genes showing signs of selection could subsequently be genotyped in large population samples using whole blood as a source for RNA without harming individuals from rare or endangered species

Data from: Genome-wide expression reveals multiple systemic effects associated with detection of anticoagulant poisons in bobcats (Lynx rufus)

Anticoagulant rodenticides (ARs) are indiscriminate toxicants that threaten non-target predatory and scavenger species through secondary poisoning. Accumulating evidence suggests that AR exposure may have disruptive sublethal consequences on individuals that can affect fitness. We evaluated AR-related effects on genome wide expression patterns in a population of bobcats in southern California. We identify differential expression of genes involved in xenobiotic metabolism, endoplasmic reticulum stress response, epithelial integrity, and both adaptive and innate immune function. Further, we find that differential expression of immune related genes may be attributable to AR-related effects on leukocyte differentiation. Collectively, our results provide an unprecedented understanding of the sublethal effects of AR exposure on a wild carnivore. These findings highlight potential detrimental effects of ARs on a wide variety of species worldwide that may consume poisoned rodents and indicate the need to investigate gene expression effects of other toxicants added to natural environments by humans

A heavy burden: Metal exposure across the land-ocean continuum in an adaptable carnivore

Urbanisation and associated anthropogenic activities release large quantities of toxic metals and metalloids into the environment, where they may bioaccumulate and threaten both wildlife and human health. In highly transformed landscapes, terrestrial carnivores may be at increased risk of exposure through biomagnification. We quantified metallic element and metalloid exposure in blood of caracals (Caracal caracal), an adaptable felid inhabiting the rapidly urbanising, coastal metropole of Cape Town, South Africa. Using redundancy analysis and mixed-effect models, we explored the influence of demography, landscape use, and diet on the concentration of 11 metals and metalloids. Although species-specific toxic thresholds are lacking, arsenic (As) and chromium (Cr) were present at potentially sublethal levels in several individuals. Increased use of human-transformed landscapes, particularly urban areas, roads, and vineyards, was significantly associated with increased exposure to aluminium (Al), cobalt (Co) and lead (Pb). Foraging closer to the coast and within aquatic food webs was associated with increased levels of mercury (Hg), selenium (Se) and arsenic, where regular predation on seabirds and waterbirds likely facilitates transfer of metals from aquatic to terrestrial food webs. Further, several elements were linked to lower haemoglobin levels (chromium, mercury, manganese, and zinc) and elevated levels of infection-fighting cells (mercury and selenium). Our results highlight the importance of anthropogenic activities as major environmental sources of metal contamination in terrestrial wildlife, including exposure across the land-ocean continuum. These findings contribute towards the growing evidence suggesting cities are particularly toxic areas for wildlife. Co-exposure to a suite of metal pollutants may threaten the long-term health and persistence of Cape Town's caracal population in unexpected ways, particularly when interacting with additional known pollutant and pathogen exposure. The caracal is a valuable sentinel for assessing metal exposure and can be used in pollution monitoring programmes to mitigate exposure and promote biodiversity conservation in human-dominated landscapes.We would like to thank the WWF Table Mountain Fund, Claude Leon Foundation, Cape Leopard Trust, University of Cape Town Faculty of Science, National Research Foundation (NRF), Institute for Communities and Wildlife in Africa (iCWild), Big Cat Rescue, Wildlife ACT, Experiment, Botanica Wines, and numerous private donors for their generous funding and support of this research. We would like to acknowledge I. Sánchez and C. M. Pérez for their laboratory support at the Instituto de Investigación en Recursos Cinegéticos (IREC).Peer reviewe

Poisoned chalice: Use of transformed landscapes associated with increased persistent organic pollutant concentrations and potential immune effects for an adaptable carnivore

Wildlife around cities bioaccumulate multiple harmful environmental pollutants associated with human activities. Exposure severity can vary based on foraging behaviour and habitat use, which can be examined to elucidate exposure pathways. Carnivores can play vital roles in ecosystem stability but are particularly vulnerable to bioaccumulation of pollutants. Understanding the spatial and dietary predictors of these contaminants can inform pollutant control, and carnivores, at the top of food webs, can act as useful indicator species. We test for exposure to toxic organochlorines (OCs), including dichloro-diphenyl-trichloroethane (DDT) and polychlorinated biphenyls (PCBs), in a medium-sized felid, the caracal (Caracal caracal), across the peri-urban and agricultural landscapes of the city of Cape Town, South Africa. Concentrations in both blood (n = 69) and adipose tissue (n = 25) were analysed along with detailed spatial, dietary, demographic, and physiological data to assess OC sources and exposure risk. The analysis revealed widespread exposure of Cape Town's caracals to organochlorines: detection rate was 100% for PCBs and 83% for DDTs in blood, and 100% for both compounds in adipose. Caracals using human-transformed areas, such as vineyards and areas with higher human population and electrical transformer density, as well as wetland areas, had higher organochlorine burdens. These landscapes were also highly selected foraging areas, suggesting caracals are drawn into areas that co-incidentally increase their risk of exposure to these pollutants. Further, biomagnification potential was higher in individuals feeding on higher trophic level prey and on exotic prey. These findings point to bioaccumulation of OC toxicants and widespread exposure across local food webs. Additionally, we report possible physiological effects of exposure, including elevated white blood cell and platelet count, suggesting a degree of immunological response that may increase disease susceptibility. Cape Town's urban fringes likely represent a source of toxic chemicals for wildlife and require focused attention and action to ensure persistence of this adaptable mesocarnivore.This research was generously supported by the WWF Table Mountain Fund, Claude Leon Foundation, Cape Leopard Trust, University of Cape Town Faculty of Science, University of California Santa Cruz, Botanica Wines, Stellenbosch University, National Research Foundation (NRF), Institute for Communities and Wildlife in Africa (iCWild), Big Cat Rescue, Wildlife ACT, Experiment, and numerous private donors. We are thankful to J. Broadfield and numerous volunteers for assistance with fieldwork. We thank Eskom (K. Chetty) and the City of Cape Town (J. Traut) for sharing electrical transformer data. SANParks Scientific Services provided the TMNP shapefile. We are grateful to I. Sánchez and C. M. Moraga Pérez at the Instituto de Investigación en Recursos Cinegéticos for laboratory support.Peer reviewe

Data from: Genome-wide expression reveals multiple systemic effects associated with detection of anticoagulant poisons in bobcats (Lynx rufus)

Anticoagulant rodenticides (ARs) are indiscriminate toxicants that threaten non-target predatory and scavenger species through secondary poisoning. Accumulating evidence suggests that AR exposure may have disruptive sublethal consequences on individuals that can affect fitness. We evaluated AR-related effects on genome wide expression patterns in a population of bobcats in southern California. We identify differential expression of genes involved in xenobiotic metabolism, endoplasmic reticulum stress response, epithelial integrity, and both adaptive and innate immune function. Further, we find that differential expression of immune related genes may be attributable to AR-related effects on leukocyte differentiation. Collectively, our results provide an unprecedented understanding of the sublethal effects of AR exposure on a wild carnivore. These findings highlight potential detrimental effects of ARs on a wide variety of species worldwide that may consume poisoned rodents and indicate the need to investigate gene expression effects of other toxicants added to natural environments by humans

Data from: Urbanization and anticoagulant poisons promote immune dysfunction in bobcats

Understanding how human activities influence immune response to environmental stressors can support biodiversity conservation across increasingly urbanizing landscapes. We studied a bobcat (Lynx rufus) population in urban southern California that experienced a rapid population decline from 2002–2005 due to notoedric mange. Because anticoagulant rodenticide (AR) exposure was an underlying complication in mange deaths, we aimed to understand sublethal contributions of urbanization and ARs on 65 biochemical markers of immune and organ function. Variance in immunological variables was primarily associated with AR exposure and secondarily with urbanization. Use of urban habitat and AR exposure has pervasive, complex and predictable effects on biochemical markers of immune and organ function in free-ranging bobcats that include impacts on neutrophil, lymphocyte and cytokine populations, total bilirubin and phosphorus. We find evidence of both inflammatory response and immune suppression associated with urban land use and rat poison exposure that could influence susceptibility to opportunistic infections. Consequently, AR exposure may influence mortality and has population-level effects, as previous work in the focal population has revealed substantial mortality caused by mange infection. The secondary effects of anticoagulant exposure may be a worldwide, largely unrecognized problem affecting a variety of vertebrate species in human-dominated environments

Anthropogenic activities and age class mediate carnivore habitat selection in a human-dominated landscape

Summary: Human activities increasingly challenge wild animal populations by disrupting ecological connectivity and population persistence. Yet, human-modified habitats can provide resources, resulting in selection of disturbed areas by generalist species. To investigate spatial and temporal responses of a generalist carnivore to human disturbance, we investigated habitat selection and diel activity patterns in caracals (Caracal caracal). We GPS-collared 25 adults and subadults in urban and wildland-dominated subregions in Cape Town, South Africa. Selection responses for landscape variables were dependent on subregion, animal age class, and diel period. Contrary to expectations, caracals did not become more nocturnal in urban areas. Caracals increased their selection for proximity to urban areas as the proportion of urban area increased. Differences in habitat selection between urban and wildland caracals suggest that individuals of this generalist species exhibit high behavioral flexibility in response to anthropogenic disturbances that emerge as a function of habitat context

Data from: Interactions between demography, genetics, and landscape connectivity increase extinction probability for a small population of large carnivores in a major metropolitan area

The extinction vortex is a theoretical model describing the process by which extinction risk is elevated in small, isolated populations owing to interactions between environmental, demographic, and genetic factors. However, empirical demonstrations of these interactions have been elusive. We modelled the dynamics of a small mountain lion population isolated by anthropogenic barriers in greater Los Angeles, California, to evaluate the influence of demographic, genetic, and landscape factors on extinction probability. The population exhibited strong survival and reproduction, and the model predicted stable median population growth and a 15% probability of extinction over 50 years in the absence of inbreeding depression. However, our model also predicted the population will lose 40–57% of its heterozygosity in 50 years. When we reduced demographic parameters proportional to reductions documented in another wild population of mountain lions that experienced inbreeding depression, extinction probability rose to 99.7%. Simulating greater landscape connectivity by increasing immigration to greater than or equal to one migrant per generation appears sufficient to largely maintain genetic diversity and reduce extinction probability. We provide empirical support for the central tenet of the extinction vortex as interactions between genetics and demography greatly increased extinction probability relative to the risk from demographic and environmental stochasticity alone. Our modelling approach realistically integrates demographic and genetic data to provide a comprehensive assessment of factors threatening small populations

ImmigrantPopulation

ImmigrantPopulatio