Corridor-based approach with spatial cross-validation reveals scale-dependent effects of geographic distance, human footprint and canopy cover on grizzly bear genetic connectivity.

Understanding how human infrastructure and other landscape attributes affect genetic differentiation in animals is an important step for identifying and maintaining dispersal corridors for these species. We built upon recent advances in the field of landscape genetics by using an individual-based and multiscale approach to predict landscape-level genetic connectivity for grizzly bears (Ursus arctos) across ~100,000 km2 in Canada's southern Rocky Mountains. We used a genetic dataset with 1156 unique individuals genotyped at nine microsatellite loci to identify landscape characteristics that influence grizzly bear gene flow at multiple spatial scales and map predicted genetic connectivity through a matrix of rugged terrain, large protected areas, highways and a growing human footprint. Our corridor-based modelling approach used a machine learning algorithm that objectively parameterized landscape resistance, incorporated spatial cross validation and variable selection and explicitly accounted for isolation by distance. This approach avoided overfitting, discarded variables that did not improve model performance across withheld test datasets and spatial predictive capacity compared to random cross-validation. We found that across all spatial scales, geographic distance explained more variation in genetic differentiation in grizzly bears than landscape variables. Human footprint inhibited connectivity across all spatial scales, while open canopies inhibited connectivity at the broadest spatial scale. Our results highlight the negative effect of human footprint on genetic connectivity, provide strong evidence for using spatial cross-validation in landscape genetics analyses and show that multiscale analyses provide additional information on how landscape variables affect genetic differentiation.

Diet and landscape characteristics drive spatial patterns of mercury accumulation in a high-latitude terrestrial carnivore.

Limited information exists on mercury concentrations and environmental drivers of mercury bioaccumulation in high latitude terrestrial carnivores. Spatial patterns of mercury concentrations in wolverine (Gulo gulo, n = 419) were assessed across a 1,600,000 km2 study area in relation to landscape, climate, diet and biological factors in Arctic and boreal biomes of western Canada. Hydrogen stable isotope ratios were measured in wolverine hair from a subset of 80 animals to assess the spatial scale for characterizing environmental conditions of their habitat. Habitat characteristics were determined using GIS methods and raster datasets at two scales, the collection location point and a 150 km radius buffer, which was selected based on results of a correlation analysis between hydrogen stable isotopes in precipitation and wolverine hair. Total mercury concentrations in wolverine muscle ranged >2 orders of magnitude from 0.01 to 5.72 µg/g dry weight and varied geographically, with the highest concentrations in the Northwest Territories followed by Nunavut and Yukon. Regression models at both spatial scales indicated diet (based on nitrogen stable isotope ratios) was the strongest explanatory variable of mercury concentrations in wolverine, with smaller though statistically significant contributions from landscape variables (soil organic carbon, percent cover of wet area, percent cover of perennial snow-ice) and distance to the Arctic Ocean coast. The carbon and nitrogen stable isotope ratios of wolverine muscle suggested greater mercury bioaccumulation could be associated with feeding on marine biota in coastal habitats. Landscape variables identified in the modelling may reflect habitat conditions which support enhanced methylmercury transfer to terrestrial biota. Spatially-explicit estimates of wet atmospheric deposition were positively correlated with wolverine mercury concentrations but this variable was not selected in the final regression models. These landscape patterns provide a basis for further research on underlying processes enhancing methylmercury uptake in high latitude terrestrial food webs.

Carnivore Contact: A Species Fracture Zone Delineated Amongst Genetically Structured North American Marten Populations (Martes americana and Martes caurina).

North American martens are forest dependent, influenced by human activity, and climate vulnerable. They have long been managed and harvested throughout their range as the American marten (Martes americana). Recent work has expanded evidence for the original description of two species in North America - M. americana and the Pacific Coast marten, M. caurina - but the geographic boundary between these groups has not been described in detail. From 2010 to 2016 we deployed 734 multi-taxa winter bait stations across a 53,474 km2 study area spanning seven mountain ranges within the anticipated contact zone along the border of Canada and the United States. We collected marten hair samples and developed genotypes for 15 polymorphic microsatellite loci for 235 individuals, and 493 base-pair sequences of the mtDNA gene COI for 175 of those individuals. Both nuclear and mitochondrial genetic structure identified a sharp break across the Clark Fork Valley, United States with M. americana and M. caurina occurring north and south of the break, respectively. We estimated global effective population size (N e ) for each mountain range, clinal genetic neighborhood sizes (NS), calculated observed (H o ) and expected (H e ) heterozygosity, fixation index (F ST ), and clinal measures of allelic richness (Ar), H o , and inbreeding coefficient (F IS ). Despite substantial genetic structure, we detected hybridization along the fracture zone with both contemporary (nuclear DNA) and historic (mtDNA) gene flow. Marten populations in our study area are highly structured and the break across the fracture zone being the largest documented in North America (F ST range 0.21-0.34, mean = 0.27). With the exception of the Coeur d'Alene Mountains, marten were well distributed across higher elevation portions of our sampling area. Clinal NS values were variable suggesting substantial heterogeneity in marten density and movement. For both M. americana and M. caurina, elevationaly dependent gene flow and high genetic population structure suggest that connectivity corridors will be important to ensuring long-term population persistence. Our study is an example of how a combination of global and clinal molecular data analyses can provide important information for natural resource management.

The ecology of human-carnivore coexistence.

With a shrinking supply of wilderness and growing recognition that top predators can have a profound influence on ecosystems, the persistence of large carnivores in human-dominated landscapes has emerged as one of the greatest conservation challenges of our time. Carnivores fascinate society, yet these animals pose threats to people living near them, resulting in high rates of carnivore death near human settlements. We used 41 y of demographic data for more than 2,500 brown bears-one of the world's most widely distributed and conflict-prone carnivores-to understand the behavioral and demographic mechanisms promoting carnivore coexistence in human-dominated landscapes. Bear mortality was high and unsustainable near people, but a human-induced shift to nocturnality facilitated lower risks of bear mortality and rates of conflict with people. Despite these behavioral shifts, projected population growth rates for bears in human-dominated areas revealed a source-sink dynamic. Despite some female bears successfully reproducing in the sink areas, bear persistence was reliant on a supply of immigrants from areas with minimal human influence (i.e., wilderness). Such mechanisms of coexistence reveal a striking paradox: Connectivity to wilderness areas supplies bears that likely will die from people, but these bears are essential to avert local extirpation. These insights suggest carnivores contribute to human-carnivore coexistence through behavioral and demographic mechanisms, and that connected wilderness is critical to sustain coexistence landscapes.

Genetic tagging in the Anthropocene: scaling ecology from alleles to ecosystems.

The Anthropocene is an era of marked human impact on the world. Quantifying these impacts has become central to understanding the dynamics of coupled human-natural systems, resource-dependent livelihoods, and biodiversity conservation. Ecologists are facing growing pressure to quantify the size, distribution, and trajectory of wild populations in a cost-effective and socially acceptable manner. Genetic tagging, combined with modern computational and genetic analyses, is an under-utilized tool to meet this demand, especially for wide-ranging, elusive, sensitive, and low-density species. Genetic tagging studies are now revealing unprecedented insight into the mechanisms that control the density, trajectory, connectivity, and patterns of human-wildlife interaction for populations over vast spatial extents. Here, we outline the application of, and ecological inferences from, new analytical techniques applied to genetically tagged individuals, contrast this approach with conventional methods, and describe how genetic tagging can be better applied to address outstanding questions in ecology. We provide example analyses using a long-term genetic tagging dataset of grizzly bears in the Canadian Rockies. The genetic tagging toolbox is a powerful and overlooked ensemble that ecologists and conservation biologists can leverage to generate evidence and meet the challenges of the Anthropocene.

Estimating unrecorded human-caused mortalities of grizzly bears in the Flathead Valley, British Columbia, Canada.

Managing the number of grizzly bear (Ursus arctos) mortalities to a sustainable level is fundamental to bear conservation. All known grizzly bear deaths are recorded by management agencies but the number of human-caused grizzly bear deaths that are not recorded is generally unknown, causing considerable uncertainty in the total number of mortalities. Here, we compare the number of bears killed legally by hunters to the number killed by people for all other reasons, for bears wearing functioning radiocollars and for uncollared bears recorded in the British Columbia (BC) government mortality database for the Flathead Valley in southeast BC. Between 1980 and 2016, permitted hunters killed 10 collared bears and 12 (9 known, 3 suspected) were killed by people for other reasons. This ratio differed (p < 0.0001) from the uncollared bears in the government database where 71 were killed by hunters while only 10 were killed for other reasons. We estimate that 88% (95% CI; 67-96%) of the human-caused mortalities that were not by permitted hunters were unreported. The study area may have low reporting rates because it is >40 km on a gravel road from a Conservation Officer office, so reporting is difficult and there are no human residences so there is little concern of a neighbor contacting an officer. Our results are likely indicative of other places that are road-accessed but far from settlements. We discuss the implications of sampling individuals for collaring and the possible implications of wearing a collar on the animal's fate.

Density-dependent signaling: An alternative hypothesis on the function of chemical signaling in a non-territorial solitary carnivore.

Brown bears are known to use rubbing behavior as a means of chemical communication, but the function of this signaling is unclear. One hypothesis that has gained support is that male bears rub to communicate dominance to other males. We tested the communication of dominance hypothesis in a low-density brown bear population in southeast British Columbia. We contrasted rubbing rates for male and female bears during and after the breeding season using ten years of DNA-mark-recapture data for 643 individuals. Here we demonstrate that male brown bears rub 60% more during the breeding than the non-breeding season, while female rubbing had no seasonal trends. Per capita rub rates by males were, on average, 2.7 times higher than females. Our results suggest that the function of rubbing in the Rocky Mountains may not only be to communicate dominance, but also to self-advertise for mate attraction. We propose that the role of chemical communication in this species may be density-dependent, where the need to self-advertise for mating is inversely related to population density and communicating for dominance increases with population density. We suggest that future endeavors to elucidate the function of rubbing should sample the behavior across a range of population densities using camera trap and genotypic data.

Experimental moose reduction lowers wolf density and stops decline of endangered caribou.

The expansion of moose into southern British Columbia caused the decline and extirpation of woodland caribou due to their shared predators, a process commonly referred to as apparent competition. Using an adaptive management experiment, we tested the hypothesis that reducing moose to historic levels would reduce apparent competition and therefor recover caribou populations. Nested within this broad hypothesis were three specific hypotheses: (1) sport hunting could be used to substantially reduce moose numbers to an ecological target; (2) wolves in this ecosystem were primarily limited by moose abundance; and (3) caribou were limited by wolf predation. These hypotheses were evaluated with a before-after control-impact (BACI) design that included response metrics such as population trends and vital rates of caribou, moose, and wolves. Three caribou subpopulations were subject to the moose reduction treatment and two were in a reference area where moose were not reduced. When the moose harvest was increased, the moose population declined substantially in the treatment area (by 70%) but not the reference area, suggesting that the policy had the desired effect and was not caused by a broader climatic process. Wolf numbers subsequently declined in the treatment area, with wolf dispersal rates 2.5× greater, meaning that dispersal was the likely mechanism behind the wolf numerical response, though reduced recruitment and starvation was also documented in the treatment area. Caribou adult survival increased from 0.78 to 0.88 in the treatment area, but declined in the reference. Caribou recruitment was unaffected by the treatment. The largest caribou subpopulation stabilized in the treatment area, but declined in the reference area. The observed population stability is comparable to other studies that used intensive wolf control, but is insufficient to achieve recovery, suggesting that multiple limiting factors and corresponding management tools must be addressed simultaneously to achieve population growth.

The influence of sulfur and hair growth on stable isotope diet estimates for grizzly bears.

Stable isotope ratios of grizzly bear (Ursus arctos) guard hair collected from bears on the lower Stikine River, British Columbia (BC) were analyzed to: 1) test whether measuring δ34S values improved the precision of the salmon (Oncorhynchus spp.) diet fraction estimate relative to δ15N as is conventionally done, 2) investigate whether measuring δ34S values improves the separation of diet contributions of moose (Alces alces), marmot (Marmota caligata), and mountain goat (Oreamnos americanus) and, 3) examine the relationship between collection date and length of hair and stable isotope values. Variation in isotope signatures among hair samples from the same bear and year were not trivial. The addition of δ34S values to mixing models used to estimate diet fractions generated small improvement in the precision of salmon and terrestrial prey diet fractions. Although the δ34S value for salmon is precise and appears general among species and areas, sulfur ratios were strongly correlated with nitrogen ratios and therefore added little new information to the mixing model regarding the consumption of salmon. Mean δ34S values for the three terrestrial herbivores of interest were similar and imprecise, so these data also added little new information to the mixing model. The addition of sulfur data did confirm that at least some bears in this system ate marmots during summer and fall. We show that there are bears with short hair that assimilate >20% salmon in their diet and bears with longer hair that eat no salmon living within a few kilometers of one another in a coastal ecosystem. Grizzly bears are thought to re-grow hair between June and October however our analysis of sectioned hair suggested at least some hairs begin growing in July or August, not June and, that hair of wild bears may grow faster than observed in captive bears. Our hair samples may have been from the year of sampling or the previous year because samples were collected in summer when bears were growing new hair. The salmon diet fraction increased with later hair collection dates, as expected if samples were from the year of sampling because salmon began to arrive in mid-summer. Bears that ate salmon had shorter hair and δ15N and δ34S values declined with hair length, also suggesting some hair samples were grown the year of sampling. To be sure to capture an entire hair growth period, samples must be collected in late fall. Early spring samples are also likely to be from the previous year but the date when hair begins to grow appears to vary. Choosing the longest hair available should increase the chance the hair was grown during the previous year and, maximize the period for which diet is measured.

Forbidden fruit: human settlement and abundant fruit create an ecological trap for an apex omnivore.

Habitat choice is an evolutionary product of animals experiencing increased fitness when preferentially occupying high-quality habitat. However, an ecological trap (ET) can occur when an animal is presented with novel conditions and the animal's assessment of habitat quality is poorly matched to its resulting fitness. We tested for an ET for grizzly (brown) bears using demographic and movement data collected in an area with rich food resources and concentrated human settlement. We derived measures of habitat attractiveness from occurrence models of bear food resources and estimated demographic parameters using DNA mark-recapture information collected over 8 years (2006-2013). We then paired this information with grizzly bear mortality records to investigate kill and movement rates. Our results demonstrate that a valley high in both berry resources and human density was more attractive than surrounding areas, and bears occupying this region faced 17% lower apparent survival. Despite lower fitness, we detected a net flow of bears into the ET, which contributed to a study-wide population decline. This work highlights the presence and pervasiveness of an ET for an apex omnivore that lacks the evolutionary cues, under human-induced rapid ecological change, to assess trade-offs between food resources and human-caused mortality, which results in maladaptive habitat selection.

Sex, Diet, and the Social Environment: Factors Influencing Hair Cortisol Concentration in Free-Ranging Black Bears (Ursus americanus).

Increasingly, measures of glucocorticoid levels (e.g., cortisol), key components of the neuroendocrine stress axis, are being used to measure past hypothalamic-pituitary-adrenal (HPA) activity to index psychological and physiological stress exhibited by wildlife for assessing individual and population-level well-being. However, many intrinsic and extrinsic factors affect HPA activity in animals. Using American black bears (Ursus americanus; n = 116) as an ecological model and hair cortisol concentration (HCC) as an integrative measure of past HPA activity, we evaluated the influence of diet, sex and the social environment on black bear HCC in a free-ranging population that spanned adjoining ecoregions with differing densities of potential conspecific and heterospecific competitors. HCC varied by sex, with female HCC ranging from 0.6 to 10.7 pg/mg (median = 4.5 ± 1.2 mean absolute deviation [MAD]) and male HCC ranging from 0.5 to 35.1 pg/mg (median = 6.2 ± 2.6 MAD). We also observed a three-way interaction among sex, δ14C and ecoregion, which may indicate that some differences in HCC between female and male black bears results from variability in the nutritional needs of larger-bodied males relative to smaller-bodied females, slight differences in food resources use between ecoregions as well as sex-based differences regarding the social environment. Once we understand what drives sex-specific differences in HCC, HCC may aid our understanding of the physiological responses by bears and other wildlife to diverse environmental challenges.

Predicting grizzly bear density in western North America.

Conservation of grizzly bears (Ursus arctos) is often controversial and the disagreement often is focused on the estimates of density used to calculate allowable kill. Many recent estimates of grizzly bear density are now available but field-based estimates will never be available for more than a small portion of hunted populations. Current methods of predicting density in areas of management interest are subjective and untested. Objective methods have been proposed, but these statistical models are so dependent on results from individual study areas that the models do not generalize well. We built regression models to relate grizzly bear density to ultimate measures of ecosystem productivity and mortality for interior and coastal ecosystems in North America. We used 90 measures of grizzly bear density in interior ecosystems, of which 14 were currently known to be unoccupied by grizzly bears. In coastal areas, we used 17 measures of density including 2 unoccupied areas. Our best model for coastal areas included a negative relationship with tree cover and positive relationships with the proportion of salmon in the diet and topographic ruggedness, which was correlated with precipitation. Our best interior model included 3 variables that indexed terrestrial productivity, 1 describing vegetation cover, 2 indices of human use of the landscape and, an index of topographic ruggedness. We used our models to predict current population sizes across Canada and present these as alternatives to current population estimates. Our models predict fewer grizzly bears in British Columbia but more bears in Canada than in the latest status review. These predictions can be used to assess population status, set limits for total human-caused mortality, and for conservation planning, but because our predictions are static, they cannot be used to assess population trend.