Effectiveness of population-based recovery actions for threatened southern mountain caribou.

Habitat loss is affecting many species, including the southern mountain caribou (Rangifer tarandus caribou) population in western North America. Over the last half century, this threatened caribou population's range and abundance have dramatically contracted. An integrated population model was used to analyze 51 years (1973-2023) of demographic data from 40 southern mountain caribou subpopulations to assess the effectiveness of population-based recovery actions at increasing population growth. Reducing potential limiting factors on threatened caribou populations offered a rare opportunity to identify the causes of decline and assess methods of recovery. Southern mountain caribou abundance declined by 51% between 1991 and 2023, and 37% of subpopulations were functionally extirpated. Wolf reduction was the only recovery action that consistently increased population growth when applied in isolation, and combinations of wolf reductions with maternal penning or supplemental feeding provided rapid growth but were applied to only four subpopulations. As of 2023, recovery actions have increased the abundance of southern mountain caribou by 52%, compared to a simulation with no interventions. When predation pressure was reduced, rapid population growth was observed, even under contemporary climate change and high levels of habitat loss. Unless predation is reduced, caribou subpopulations will continue to be extirpated well before habitat conservation and restoration can become effective.

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.

Saving endangered species using adaptive management.

Adaptive management is a powerful means of learning about complex ecosystems, but is rarely used for recovering endangered species. Here, we demonstrate how it can benefit woodland caribou, which became the first large mammal extirpated from the contiguous United States in recent history. The continental scale of forest alteration and extended time needed for forest recovery means that relying only on habitat protection and restoration will likely fail. Therefore, population management is also needed as an emergency measure to avoid further extirpation. Reductions of predators and overabundant prey, translocations, and creating safe havens have been applied in a design covering >90,000 km2 Combinations of treatments that increased multiple vital rates produced the highest population growth. Moreover, the degree of ecosystem alteration did not influence this pattern. By coordinating recovery involving scientists, governments, and First Nations, treatments were applied across vast scales to benefit this iconic species.

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.

Using predator-prey theory to predict outcomes of broadscale experiments to reduce apparent competition.

Apparent competition is an important process influencing many ecological communities. We used predator-prey theory to predict outcomes of ecosystem experiments aimed at mitigating apparent competition by reducing primary prey. Simulations predicted declines in secondary prey following reductions in primary prey because predators consumed more secondary prey until predator numbers responded to reduced prey densities. Losses were exacerbated by a higher carrying capacity of primary prey and a longer lag time of the predator's numerical response, but a gradual reduction in primary prey was less detrimental to the secondary prey. We compared predictions against two field experiments where endangered woodland caribou (Rangifer tarandus caribou) were victims of apparent competition. First, when deer (Odocoileus sp.) declined suddenly following a severe winter, cougar (Puma concolor) declined with a 1-2-year lag, yet in the interim more caribou were killed by cougars, and caribou populations declined by 40%. Second, when moose (Alces alces) were gradually reduced using a management experiment, wolf (Canis lupus) populations declined but did not shift consumption to caribou, and the largest caribou subpopulation stabilized. The observed contrasting outcomes of sudden versus gradual declines in primary prey supported theoretical predictions. Combining theory with field studies clarified how to manage communities to mitigate endangerment caused by apparent competition that affects many taxa.

Testing predator-prey theory using broad-scale manipulations and independent validation.

A robust test of ecological theory is to gauge the predictive accuracy of general relationships parameterized from multiple systems but applied to a new area. To address this goal, we used an ecosystem-level experiment to test predator-prey theory by manipulating prey abundance to determine whether predation was density dependent, density independent, compensatory or depensatory (inversely density dependent) on prey populations. Understanding the nature of predation is of primary importance in community ecology because it establishes whether predation has little effect on prey abundance (compensatory), whether it promotes coexistence (density dependent) and reduces the equilibrium of prey (density independent) or whether it can be destabilizing (depensatory). We used theoretical predictions consisting of functional and numerical equations parameterized independently from meta-analyses on wolves (Canis lupus) and moose (Alces alces), but applied to our specific wolf-moose system. Predictions were tested by experimentally reducing moose abundance across 6500 km(2) as a novel way of evaluating the nature of predation. Depensatory predation of wolves on moose was the best explanation of the population dynamic - a mechanism that has been hypothesized to occur but has rarely been evaluated. Adding locally obtained kill rates and numerical estimates to the independent data provided no benefit to model predictions, suggesting that the theory was robust to local variation. These findings have critical implications for any organism that is preyed upon but that also has, or will be, subject to increased human exploitation or perturbations from environmental change. If depensatory predation is not accounted for in harvest models, predicted yields will be excessive and lead to further population decline.

Population size and major valleys explain microsatellite variation better than taxonomic units for caribou in western Canada.

Identifying conservation units below the species level is becoming increasingly important, particularly when limited resources necessitate prioritization for conservation among such units. This problem is exemplified with caribou, a mammal with a circum-Arctic distribution that is exposed to a broad spectrum of ecological conditions, but is also declining in many parts of its range. We used microsatellite markers to evaluate the suitability of existing intra-specific taxonomic designations to act as population units for conservation and contrasted this with landscape features that were independent of taxonomy. We also quantified the relationship between genetic differentiation and subpopulation size, a factor that has been under-represented in landscape genetic research. Our data set included three subspecies and three ecotypes of caribou that varied in population size by five orders of magnitude. Our results indicated that genetic structure did not correspond to existing taxonomic designation, particularly at the level of ecotype. Instead, we found that major valleys and population size were the strongest factors associated with substructure. There was a negative exponential relationship between population size and F(ST) between pairs of adjacent subpopulations, suggesting that genetic drift was the mechanism causing the structure among the smallest subpopulations. A genetic assignment test revealed that movement among subpopulations was a fraction of the level needed to stabilize smaller subpopulations, indicating little chance for demographic rescue. Such results may be broadly applicable to landscape genetic studies, because population size and corresponding rates of drift have the potential to confound interpretations of landscape effects on population structure.

Implications of body condition on the unsustainable predation rates of endangered mountain caribou.

Both top-down and bottom-up processes influence herbivore populations, and identifying dominant limiting factors is essential for applying effective conservation actions. Mountain caribou are an endangered ecotype of woodland caribou (Rangifer tarandus caribou) that have been declining, and unsustainable predation has been identified as the proximate cause. To investigate the role of poor nutrition, we examined the influence of sex, season, age class, and available suitable habitat (i.e., old-growth forest>140 years) per caribou on bone marrow fat content of caribou that died (n = 79). Sex was the only strong predictor of marrow fat. Males that died during and post rut had lower marrow fat than females or males at other times of year. Old-growth abundance per caribou, season, and age class did not predict marrow fat. Caribou killed by predators did not have less marrow fat than those that died in accidents, suggesting that nutritionally stressed caribou were not foraging in less secure habitats or that predators selected nutritionally stressed individuals. Marrow fat in endangered and declining populations of mountain caribou was similar to caribou in other, more viable populations. Our results support previous research suggesting that observed population declines of mountain caribou are due to excessive predation that is not linked to body condition.

Vital rates of two small populations of brown bears in Canada and range-wide relationship between population size and trend.

Identifying mechanisms of population change is fundamental for conserving small and declining populations and determining effective management strategies. Few studies, however, have measured the demographic components of population change for small populations of mammals (<50 individuals). We estimated vital rates and trends in two adjacent but genetically distinct, threatened brown bear (Ursus arctos) populations in British Columbia, Canada, following the cessation of hunting. One population had approximately 45 resident bears but had some genetic and geographic connectivity to neighboring populations, while the other population had <25 individuals and was isolated. We estimated population-specific vital rates by monitoring survival and reproduction of telemetered female bears and their dependent offspring from 2005 to 2018. In the larger, connected population, independent female survival was 1.00 (95% CI: 0.96-1.00) and the survival of cubs in their first year was 0.85 (95% CI: 0.62-0.95). In the smaller, isolated population, independent female survival was 0.81 (95% CI: 0.64-0.93) and first-year cub survival was 0.33 (95% CI: 0.11-0.67). Reproductive rates did not differ between populations. The large differences in age-specific survival estimates resulted in a projected population increase in the larger population (λ = 1.09; 95% CI: 1.04-1.13) and population decrease in the smaller population (λ = 0.84; 95% CI: 0.72-0.95). Low female survival in the smaller population was the result of both continued human-caused mortality and an unusually high rate of natural mortality. Low cub survival may have been due to inbreeding and the loss of genetic diversity common in small populations, or to limited resources. In a systematic literature review, we compared our population trend estimates with those reported for other small populations (<300 individuals) of brown bears. Results suggest that once brown bear populations become small and isolated, populations rarely increase and, even with intensive management, recovery remains challenging.

Predator-mediated allee effects in multi-prey systems.

Allee effects can have significant consequences for small populations and understanding the causal mechanisms for such effects is important for guiding conservation actions. One proposed mechanism is through predation, in which a type II functional response leads to increasing predation rates as prey numbers decline. However, models to support this mechanism have incorporated only a single declining prey species in the functional response, which is probably an oversimplification. We reevaluated the potential for predator-mediated Allee effects in a multi-prey system using Holling's disc equation. We also used empirical data on a large herbivore to examine how grouping behavior may influence the potential for predation-mediated Allee effects. Results based on a multi-prey expression of the functional response predict that Allee effects caused by predation on relatively rare secondary prey may not occur because handling time of the abundant prey dominates the functional response such that secondary prey are largely "bycatch". However, a predator-mediated Allee effect can occur if secondary prey live in groups and if, as the population declines, their average group size declines (a relationship seen in several species). In such a case, the rate at which the number of groups declines is less than the rate at which the population declines. Thus the rate at which a predator encounters a group remains relatively stable, but when a predator kills one animal from smaller groups, the predation rate increases. These results highlight the need to evaluate risks associated with potential changes in group size as populations decline.

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.

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.

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.

Genetic analysis reveals demographic fragmentation of grizzly bears yielding vulnerably small populations.

Ecosystem conservation requires the presence of native carnivores, yet in North America, the distributions of many larger carnivores have contracted. Large carnivores live at low densities and require large areas to thrive at the population level. Therefore, if human-dominated landscapes fragment remaining carnivore populations, small and demographically vulnerable populations may result. Grizzly bear range contraction in the conterminous USA has left four fragmented populations, three of which remain along the Canada-USA border. A tenet of grizzly bear conservation is that the viability of these populations requires demographic linkage (i.e. inter-population movement of both sexes) to Canadian bears. Using individual-based genetic analysis, our results suggest this demographic connection has been severed across their entire range in southern Canada by a highway and associated settlements, limiting female and reducing male movement. Two resulting populations are vulnerably small (< or =100 animals) and one of these is completely isolated. Our results suggest that these trans-border bear populations may be more threatened than previously thought and that conservation efforts must expand to include international connectivity management. They also demonstrate the ability of genetic analysis to detect gender-specific demographic population fragmentation in recently disturbed systems, a traditionally intractable yet increasingly important ecological measurement worldwide.

Effect of season and high ambient temperature on activity levels and patterns of grizzly bears (Ursus arctos).

Understanding factors that influence daily and annual activity patterns of a species provides insights to challenges facing individuals, particularly when climate shifts, and thus is important in conservation. Using GPS collars with dual-axis motion sensors that recorded the number of switches every 5 minutes we tested the hypotheses: 1. Grizzly bears (Ursus arctos) increase daily activity levels and active bout lengths when they forage on berries, the major high-energy food in this ecosystem, and 2. Grizzly bears become less active and more nocturnal when ambient temperature exceeds 20°C. We found support for hypothesis 1 with both male and female bears being active from 0.7 to 2.8 h longer in the berry season than in other seasons. Our prediction under hypothesis 2 was not supported. When bears foraged on berries on a dry, open mountainside, there was no relationship between daily maximum temperature (which varied from 20.4 to 40.1°C) and the total amount of time bears were active, and no difference in activity levels during day or night between warm (20.4-27.3°C) and hot (27.9-40.1°C) days. Our results highlight the strong influence that food acquisition has on activity levels and patterns of grizzly bears and is a challenge to the heat dissipation limitation theory.

Changes in landscape composition influence the decline of a threatened woodland caribou population.

1. Large-scale habitat loss is frequently identified with loss of biodiversity, but examples of the direct effect of habitat alterations on changes in vital rates remain rare. Quantifying and understanding the relationship between habitat composition and changes in vital rates, however, is essential for the development of effective conservation strategies. 2. It has been suggested that the decline of woodland caribou Rangifer tarandus caribou populations in North America is precipitated by timber harvesting that creates landscapes of early seral forests. Such habitat changes have altered the predator-prey system resulting in asymmetric predation, where predators are maintained by alternative prey (i.e. apparent competition). However, a direct link between habitat condition and caribou population declines has not been documented. 3. We estimated survival probabilities for the threatened arboreal lichen-feeding ecotype of woodland caribou in British Columbia, Canada, at two different spatial scales. At the broader scale, observed variation in adult female survival rates among 10 distinct populations (range = 0.67-0.93) was best explained by variation in the amount of early seral stands within population ranges and population density. At the finer scale, home ranges of caribou killed by predators had lower proportions of old forest and more mid-aged forest as compared with multi-annual home ranges where caribou were alive. 4. These results are consistent with predictions from the apparent competition hypothesis and quantify direct fitness consequences for caribou following habitat alterations. We conclude that apparent competition can cause rapid population declines and even extinction where changes in species composition occur following large scale habitat change.

The role of predation in the decline and extirpation of woodland caribou.

To select appropriate recovery strategies for endangered populations, we must understand the dynamics of small populations and distinguish between the possible causes that drive such populations to low numbers. It has been suggested that the pattern of population decline may be inversely density-dependent with population growth rates decreasing as populations become very small; however, empirical evidence of such accelerated declines at low densities is rare. Here we analyzed the pattern of decline of a threatened population of woodland caribou (Rangifer tarandus caribou) in British Columbia, Canada. Using information on the instantaneous rate of increase relative to caribou density in suitable winter foraging habitat, as well as on pregnancy rates and on causes and temporal distribution of mortalities from a sample of 349 radiocollared animals from 15 subpopulations, we tested 3 hypothesized causes of decline: (a) food regulation caused by loss of suitable winter foraging habitat, (b) predation-sensitive foraging caused by loss of suitable winter foraging habitat and (c) predation with caribou being secondary prey. Population sizes of caribou subpopulations ranged from < 5 to > 500 individuals. Our results showed that the rates of increase of these subpopulations varied from -0.1871 to 0.0496 with smaller subpopulations declining faster than larger subpopulations. Rates of increase were positively related to the density of caribou in suitable winter foraging habitat. Pregnancy rates averaged 92.4% +/-2.24 and did not differ among subpopulations. In addition, we found predation to be the primary cause of mortality in 11 of 13 subpopulations with known causes of mortality and predation predominantly occurred during summer. These results are consistent with predictions that caribou subpopulations are declining as a consequence of increased predation. Recovery of these woodland caribou will thus require a multispecies perspective and an appreciation for the influence of inverse density dependence on population trajectories.