A hierarchical modeling approach to predict the distribution and density of Sierra Nevada Red Fox (Vulpes vulpes necator).

Carnivores play critical roles in ecosystems, yet many species are declining worldwide. The Sierra Nevada Red Fox (Vulpes vulpes necator; SNRF) is a rare and endangered subspecies of red fox limited to upper montane forests, subalpine, and alpine environments of California and Oregon, United States. Having experienced significant distribution contractions and population declines in the last century, the subspecies is listed as at-risk by relevant federal and state agencies. Updated information on its contemporary distribution and density is needed to guide and evaluate conservation and management actions. We combined 12 years (2009-2020) of detection and nondetection data collected throughout California and Oregon to model the potential distribution and density of SNRFs throughout their historical and contemporary ranges. We used an integrated species distribution and density modeling approach, which predicted SNRF density in sampled locations based on observed relationships between environmental covariates and detection frequencies, and then projected those predictions to unsampled locations based on the estimated correlations with environmental covariates. This approach provided predictions that serve as density estimates in sampled regions and projections in unsampled areas. Our model predicted a density of 1.06 (95% credible interval = 0.8-1.36) foxes per 100 km2 distributed throughout 22,926 km2 in three distinct regions of California and Oregon-Sierra Nevada, Lassen Peak, and Oregon Cascades. SNRFs were most likely to be found in areas with low minimum temperatures and high snow water equivalent. Our results provide a contemporary baseline to inform the development and evaluation of conservation and management actions, and guide future survey efforts.

The ecology of human-caused mortality for a protected large carnivore.

Mitigating human-caused mortality for large carnivores is a pressing global challenge for wildlife conservation. However, mortality is almost exclusively studied at local (within-population) scales creating a mismatch between our understanding of risk and the spatial extent most relevant to conservation and management of wide-ranging species. Here, we quantified mortality for 590 radio-collared mountain lions statewide across their distribution in California to identify drivers of human-caused mortality and investigate whether human-caused mortality is additive or compensatory. Human-caused mortality, primarily from conflict management and vehicles, exceeded natural mortality despite mountain lions being protected from hunting. Our data indicate that human-caused mortality is additive to natural mortality as population-level survival decreased as a function of increasing human-caused mortality and natural mortality did not decrease with increased human-caused mortality. Mortality risk increased for mountain lions closer to rural development and decreased in areas with higher proportions of citizens voting to support environmental initiatives. Thus, the presence of human infrastructure and variation in the mindset of humans sharing landscapes with mountain lions appear to be primary drivers of risk. We show that human-caused mortality can reduce population-level survival of large carnivores across large spatial scales, even when they are protected from hunting.

Linking population performance to nutritional condition in an alpine ungulate.

Bighorn sheep (Ovis canadensis) can live in extremely harsh environments and subsist on submaintenance diets for much of the year. Under these conditions, energy stored as body fat serves as an essential reserve for supplementing dietary intake to meet metabolic demands of survival and reproduction. We developed equations to predict ingesta-free body fat in bighorn sheep using ultrasonography and condition scores in vivo and carcass measurements postmortem. We then used in vivo equations to investigate the relationships between body fat, pregnancy, overwinter survival, and population growth in free-ranging bighorn sheep in California and Nevada. Among 11 subpopulations that included alpine winter residents and migrants, mean ingesta-free body fat of lactating adult females during autumn ranged between 8.8% and 15.0%; mean body fat for nonlactating females ranged from 16.4% to 20.9%. In adult females, ingesta-free body fat > 7.7% during January (early in the second trimester) corresponded with a > 90% probability of pregnancy and ingesta-free body fat > 13.5% during autumn yielded a probability of overwinter survival > 90%. Mean ingesta-free body fat of lactating females in autumn was positively associated with finite rate of population increase (λ) over the subsequent year in bighorn sheep subpopulations that wintered in alpine landscapes. Bighorn sheep with ingesta-free body fat of 26% in autumn and living in alpine environments possess energy reserves sufficient to meet resting metabolism for 83 days on fat reserves alone. We demonstrated that nutritional condition can be a pervasive mechanism underlying demography in bighorn sheep and characterizes the nutritional value of their occupied ranges. Mountain sheep are capital survivors in addition to being capital breeders, and because they inhabit landscapes with extreme seasonal forage scarcity, they also can be fat reserve obligates. Quantifying nutritional condition is essential for understanding the quality of habitats, how it underpins demography, and the proximity of a population to a nutritional threshold.

Evaluating wildlife translocations using genomics: A bighorn sheep case study.

Wildlife restoration often involves translocation efforts to reintroduce species and supplement small, fragmented populations. We examined the genomic consequences of bighorn sheep (Ovis canadensis) translocations and population isolation to enhance understanding of evolutionary processes that affect population genetics and inform future restoration strategies. We conducted a population genomic analysis of 511 bighorn sheep from 17 areas, including native and reintroduced populations that received 0-10 translocations. Using the Illumina High Density Ovine array, we generated datasets of 6,155 to 33,289 single nucleotide polymorphisms and completed clustering, population tree, and kinship analyses. Our analyses determined that natural gene flow did not occur between most populations, including two pairs of native herds that had past connectivity. We synthesized genomic evidence across analyses to evaluate 24 different translocation events and detected eight successful reintroductions (i.e., lack of signal for recolonization from nearby populations) and five successful augmentations (i.e., reproductive success of translocated individuals) based on genetic similarity with the source populations. A single native population founded six of the reintroduced herds, suggesting that environmental conditions did not need to match for populations to persist following reintroduction. Augmentations consisting of 18-57 animals including males and females succeeded, whereas augmentations of two males did not result in a detectable genetic signature. Our results provide insight on genomic distinctiveness of native and reintroduced herds, information on the relative success of reintroduction and augmentation efforts and their associated attributes, and guidance to enhance genetic contribution of augmentations and reintroductions to aid in bighorn sheep restoration.

Habitat predicts local prevalence of migratory behaviour in an alpine ungulate.

The resource hierarchy hypothesis predicts that the most important factors limiting a species' distribution act at the coarsest spatial scales. However, resource selection behaviour affords mobile organisms the opportunity to adopt a range of tactics for navigating spatial trade-offs between competing biotic and abiotic constraints. Throughout the animal kingdom, partial migration (where some individuals migrate, and others remain resident year round) offers a pervasive example of such behavioural polymorphism. Identifying the differences between these behaviours is therefore central to understanding the conditions (habitat) needed to sustain migrant and resident populations. Here we test an extension of the resource hierarchy hypothesis. We hypothesized that rather than responding to a single limiting factor, migration and residency represent contrasting scale-specific approaches to managing trade-offs between forage, predation risk and severe winter conditions. Furthermore, we predicted that the distribution of habitat selected by migrants and residents is predictive of the local prevalence of migratory behaviour. To test these hypotheses, we quantified migratory status- (resident/migrant) and season-specific (winter/summer) differences in resource selection by eight populations of federally endangered Sierra Nevada bighorn sheep Ovis canadensis sierrae across three spatial scales: population range, individual range and within individual range. We then integrated these spatial predictions to produce separate spatial predictions of migrant and resident winter habitat. As predicted, model selection provided strong evidence for the importance of status-specific differences in resource selection. Residents showed stronger coarse-scale selection for terrain associated with predator avoidance and stronger fine-scale selection for greenness, while in migrants this pattern was reversed. Availability of migrant habitat predicted the local prevalence of migration (top model pseudo R2 of .87). Our ability to respond to global declines of migratory species depends on improving our understanding of the conditions required to maintain migratory behaviour. Through explicitly contrasting migrant and resident behaviour, our results illustrate seasonal differences in migrant and resident habitat and how these two behaviours represent responses to different limiting conditions. Our analyses provides a novel empirical basis for assessing the local prevalence of migratory behaviour across large landscapes.

Risk-sensitive allocation in seasonal dynamics of fat and protein reserves in a long-lived mammal.

Body reserves of numerous taxa follow seasonal rhythms that are a function of temporal patterns in food availability and life-history events; however, tests of the theory underlying the allocation of somatic reserves for long-lived organisms are rare, especially for free-ranging mammals. We evaluated the hypothesis that allocation of somatic reserves to survival (i.e., metabolic processes) and reproduction should be sensitive to current nutritional state relative to seasonal thresholds in those reserves. Our goal was to reveal the linkages between nutrition and life-history traits to understand how long-lived, iteroparous organisms balance the allocation of somatic reserves to reproduction, while retaining reserves as insurance for survival in unpredictable environments. Our evaluation was based on seasonal dynamics in fat (measured as ingesta-free body fat; IFBFat) and protein reserves (measured as ingesta-free, fat-free body mass; IFFFBMass) of 136 female mule deer (Odocoileus hemionus) over 8 years. Although mean changes in fat and protein reserves were positive over summer and negative over winter, accretion and catabolism of those reserves was not consistent among individuals. Over winter, both lipid and protein stores available in autumn were catabolized in proportion to their availability above a post-winter threshold (5·8% IFBFat, 33 kg IFFFBMass); however, lean body tissue was spared at the expense of lipid reserves. Female deer mostly synthesized lean body tissue over summer and committed post-winter fat reserves to reproduction relative to their availability above an autumn threshold (>8·6% IFBFat), which was lowered by 2·8 percentage points (pp) for each additional young recruited. Mothers reduced their autumn fat threshold to secure current reproductive investment and, thereby, endured a cost of reproduction at the expense of fat accumulation. Allocation of somatic reserves occurred in a risk-sensitive framework; females allocated reserves relative to their availability above seasonal thresholds. In contrast to current notions of summer accretion and winter catabolism of body reserves, some individuals deposited reserves over winter and catabolized reserves over summer, mainly because regulation of individual condition was state-dependent. Consequently, behaviour and life-history strategies may be as much a function of nutritional contributions of the previous season as of the current one.

Evaluating apparent competition in limiting the recovery of an endangered ungulate.

Predation can disproportionately affect endangered prey populations when generalist predators are numerically linked to more abundant primary prey. Apparent competition, the term for this phenomenon, has been increasingly implicated in the declines of endangered prey populations. We examined the potential for apparent competition to limit the recovery of Sierra Nevada bighorn sheep (Ovis canadensis sierrae), an endangered subspecies under the US Endangered Species Act. Using a combination of location, demographic, and habitat data, we assessed whether cougar (Puma concolor) predation on endangered bighorn sheep was a consequence of their winter range overlap with abundant mule deer (Odocoileus hemionus). Consistent with the apparent competition hypothesis, bighorn sheep populations with higher spatial overlap with deer exhibited higher rates of cougar predation which had additive effects on adult survival. Bighorn sheep killed by cougars were primarily located within deer winter ranges, even though those areas constituted only a portion of the bighorn sheep winter ranges. We suspect that variation in sympatry between bighorn sheep and deer populations was largely driven by differences in habitat selection among bighorn sheep herds. Indeed, bighorn sheep herds that experienced the highest rates of predation and the greatest spatial overlap with deer also exhibited the strongest selection for low elevation habitat. Although predator-mediated apparent competition may limit some populations of bighorn sheep, it is not the primary factor limiting all populations, suggesting that the dynamics of different herds are highly idiosyncratic. Management plans for endangered species should consider the spatial distributions of key competitors and predators to reduce the potential for apparent competition to hijack conservation success.

Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep.

Evidence of inbreeding depression is commonly detected from the fitness traits of animals, yet its effects on population growth rates of endangered species are rarely assessed. We examined whether inbreeding depression was affecting Sierra Nevada bighorn sheep (Ovis canadensis sierrae), a subspecies listed as endangered under the U.S. Endangered Species Act. Our objectives were to characterize genetic variation in this subspecies; test whether inbreeding depression affects bighorn sheep vital rates (adult survival and female fecundity); evaluate whether inbreeding depression may limit subspecies recovery; and examine the potential for genetic management to increase population growth rates. Genetic variation in 4 populations of Sierra Nevada bighorn sheep was among the lowest reported for any wild bighorn sheep population, and our results suggest that inbreeding depression has reduced adult female fecundity. Despite this population sizes and growth rates predicted from matrix-based projection models demonstrated that inbreeding depression would not substantially inhibit the recovery of Sierra Nevada bighorn sheep populations in the next approximately 8 bighorn sheep generations (48 years). Furthermore, simulations of genetic rescue within the subspecies did not suggest that such activities would appreciably increase population sizes or growth rates during the period we modeled (10 bighorn sheep generations, 60 years). Only simulations that augmented the Mono Basin population with genetic variation from other subspecies, which is not currently a management option, predicted significant increases in population size. Although we recommend that recovery activities should minimize future losses of genetic variation, genetic effects within these endangered populations-either negative (inbreeding depression) or positive (within subspecies genetic rescue)-appear unlikely to dramatically compromise or stimulate short-term conservation efforts. The distinction between detecting the effects of inbreeding depression on a component vital rate (e.g., fecundity) and the effects of inbreeding depression on population growth underscores the importance of quantifying inbreeding costs relative to population dynamics to effectively manage endangered populations.

Resumen: La evidencia de la depresión por endogamia comúnmente es detectada a partir de atributos de la adaptabilidad de animales, sin embargo sus efectos sobre las tasas de crecimiento poblacional raramente son evaluados. Examinamos si la depresión por endogamia estaba afectando a Ovis canadensis sierrae, una subespecie enlistada como en peligro en el Acta de Especies en Peligro de E.U.A. Nuestros objetivos fueron caracterizar la variación genética de esta subespecie; probar si la depresión por endogamia afecta las tasas vitales (supervivencia de adultos y fecundidad de hembras); evaluar si la depresión por endogamia puede limitar la recuperación dela subespecie y examinar el potencial para el manejo genético para incrementar las tasas de crecimiento poblacional. La variación genética en 4 subpoblaciones O. c. sierrae fue la más baja entre las reportadas para cualquier otra población silvestre de O. c. sierrae y nuestros resultados sugieren que la depresión por endogamia ha reducido la fecundidad de hembras adultas. Sin embargo, los tamaños poblacionales y tasas de crecimiento predichos por modelos de proyección matriciales demostraron que la depresión por endogamia no inhibiría sustancialmente la recuperación de O. c. sierrae en las próximas 8 generaciones (48 años). Más aun, simulaciones del rescate genético no sugirieron que tales actividades incrementarían los tamaños poblacionales o tasas de crecimiento durante el período modelado (10 generaciones, 60 años). Solo las simulaciones que aumentaron la población de Mono Basin con variación genética de otras subespecies, lo cual no es una opción de manejo actual, predijeron incrementos significativos en el tamaño poblacional. Aunque recomendamos que las actividades de recuperación deberían minimizar pérdidas futuras en la variación genética, parece poco probable que los efectos genéticos en estas poblaciones en peligro-ya sea negativas (depresión por endogamia) o positivas (rescate genético de la subespecie)-comprometan o estimulen dramáticamente los esfuerzos de conservación a corto plazo. La distinción entre la detección de los efectos de la depresión por endogamia sobre una tasa vital componente (e.g., fecundidad) y los efectos de la depresión por endogamia sobre el crecimiento poblacional resalta la importancia de cuantificar, mediante datos recolectados en campo, los costos de la endogamia en relación con la dinámica poblacional para el manejo efectivo de poblaciones en peligro.

Population-specific vital rate contributions influence management of an endangered ungulate.

To develop effective management strategies for the recovery of threatened and endangered species, it is critical to identify those vital rates (survival and reproductive parameters) responsible for poor population performance and those whose increase will most efficiently change a population's trajectory. In actual application, however, approaches identifying key vital rates are often limited by inadequate demographic data, by unrealistic assumptions of asymptotic population dynamics, and of equal, infinitesimal changes in mean vital rates. We evaluated the consequences of these limitations in an analysis of vital rates most important in the dynamics of federally endangered Sierra Nevada bighorn sheep (Ovis canadensis sierrae). Based on data collected from 1980 to 2007, we estimated vital rates in three isolated populations, accounting for sampling error, variance, and covariance. We used analytical sensitivity analysis, life-stage simulation analysis, and a novel non-asymptotic simulation approach to (1) identify vital rates that should be targeted for subspecies recovery; (2) assess vital rate patterns of endangered bighorn sheep relative to other ungulate populations; (3) evaluate the performance of asymptotic vs. non-asymptotic models for meeting short-term management objectives; and (4) simulate management scenarios for boosting bighorn sheep population growth rates. We found wide spatial and temporal variation in bighorn sheep vital rates, causing rates to vary in their importance to different populations. As a result, Sierra Nevada bighorn sheep exhibited population-specific dynamics that did not follow theoretical expectations or those observed in other ungulates. Our study suggests that vital rate inferences from large, increasing, or healthy populations may not be applicable to those that are small, declining, or endangered. We also found that, while asymptotic approaches were generally applicable to bighorn sheep conservation planning; our non-asymptotic population models yielded unexpected results of importance to managers. Finally, extreme differences in the dynamics of individual bighorn sheep populations imply that effective management strategies for endangered species recovery may often need to be population-specific.

Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring.

Stable isotope signatures of lactating females and their nursing offspring were measured on 11 species, including herbivores, carnivores, hibernators, and non-hibernators. We hypothesized that: (1) nursing offspring would have stable isotope signatures that were a trophic level higher than their mothers, and (2) this pattern would be species-independent. The plasma of adult females had a δ15N enrichment over their diets of 4.1±0.7‰, but offspring plasma had a mean δ15N enrichment over maternal plasma of 0.9±0.8‰ and no C enrichment (0.0±0.6‰). The trophic level enrichment did not occur between mother and offspring because milk was depleted in both δ15N (1.0±0.5‰) and δ13C (2.1±0.9‰) relative to maternal plasma. Milk to offspring plasma enrichment was relatively small (δ15N enrichment of 1.9±0.7‰ and δ13C enrichment of 1.9±0.8‰) compared to the trophic level enrichment between the adults and their diets. While some species did have significant differences between the isotope signatures of mother and offspring, the differences were not related to whether they were hibernators or non-hibernators, carnivores or herbivores. Investigators wanting to use stable isotopes to quantify weaning or other lactation processes or diets of predators when both adults and nursing offspring are consumed must first establish the parameters that apply to a particular species/environment/diet combination.