Habitat alteration or climate: What drives the densities of an invading ungulate?

Anthropogenic habitat alteration and climate change are two well-known contributors to biodiversity loss through changes to species distribution and abundance; yet, disentangling the effects of these two factors is often hindered by their inherent confound across both space and time. We leveraged a contrast in habitat alteration associated with the jurisdictional boundary between two Canadian provinces to evaluate the relative effects of spatial variation in habitat alteration and climate on white-tailed deer (Odocoileus virginianus) densities. White-tailed deer are an invading ungulate across much of North America, whose expansion into Canada's boreal forest is implicated in the decline of boreal caribou (Rangifer tarandus caribou), a species listed as Threatened in Canada. We estimated white-tailed deer densities using 300 remote cameras across 12 replicated 50 km2 landscapes over 5 years. White-tailed deer densities were significantly lower in areas where winter severity was higher. For example, predicted deer densities declined from 1.83 to 0.35 deer/km2 when winter severity increased from the lowest value to the median value. There was a tendency for densities to increase with increasing habitat alteration; however, the magnitude of this effect was approximately half that of climate. Our findings suggest that climate is the primary driver of white-tailed deer populations; however, understanding the mechanisms underpinning this relationship requires further study of over-winter survival and fecundity. Long-term monitoring at the invasion front is needed to evaluate the drivers of abundance over time, particularly given the unpredictability of climate change and increasing prevalence of extreme weather events.

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.

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.

Trophic consequences of terrestrial eutrophication for a threatened ungulate.

Changes in primary productivity have the potential to substantially alter food webs, with positive outcomes for some species and negative outcomes for others. Understanding the environmental context and species traits that give rise to these divergent outcomes is a major challenge to the generality of both theoretical and applied ecology. In aquatic systems, nutrient-mediated eutrophication has led to major declines in species diversity, motivating us to seek terrestrial analogues using a large-mammal system across 598 000 km2 of the Canadian boreal forest. These forests are undergoing some of the most rapid rates of land-use change on Earth and are home to declining caribou (Rangifer tarandus caribou) populations. Using satellite-derived estimates of primary productivity, coupled with estimates of moose (Alces alces) and wolf (Canis lupus) abundance, we used path analyses to discriminate among hypotheses explaining how habitat alteration can affect caribou population growth. Hypotheses included food limitation, resource dominance by moose over caribou, and apparent competition with predators shared between moose and caribou. Results support apparent competition and yield estimates of wolf densities (1.8 individuals 1000 km-2) above which caribou populations decline. Our multi-trophic analysis provides insight into the cascading effects of habitat alteration from forest cutting that destabilize terrestrial predator-prey dynamics. Finally, the path analysis highlights why conservation actions directed at the proximate cause of caribou decline have been more successful in the near term than those directed further along the trophic chain.

Genomics, environment and balancing selection in behaviourally bimodal populations: The caribou case.

Selection forces that favour different phenotypes in different environments can change frequencies of genes between populations along environmental clines. Clines are also compatible with balancing forces, such as negative frequency-dependent selection (NFDS), which maintains phenotypic polymorphisms within populations. For example, NFDS is hypothesized to maintain partial migration, a dimorphic behavioural trait prominent in species where only a fraction of the population seasonally migrates. Overall, NFDS is believed to be a common phenomenon in nature, yet a scarcity of studies were published linking naturally occurring allelic variation with bimodal or multimodal phenotypes and balancing selection. We applied a Pool-seq approach and detected selection on alleles associated with environmental variables along a North-South gradient in western North American caribou, a species displaying partially migratory behaviour. On 51 loci, we found a signature of balancing selection, which could be related to NFDS and ultimately the maintenance of the phenotypic polymorphisms known within these populations. Yet, remarkably, we detected directional selection on a locus when our sample was divided into two behaviourally distinctive groups regardless of geographic provenance (a subset of GPS-collared migratory or sedentary individuals), indicating that, within populations, phenotypically homogeneous groups were genetically distinctive. Loci under selection were linked to functional genes involved in oxidative stress response, body development and taste perception. Overall, results indicated genetic differentiation along an environmental gradient of caribou populations, which we found characterized by genes potentially undergoing balancing selection. We suggest that the underlining balancing force, NFDS, plays a strong role within populations harbouring multiple haplotypes and phenotypes, as it is the norm in animals, plants and humans too.

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.

Conservation strategies for species affected by apparent competition.

Apparent competition is an indirect interaction between 2 or more prey species through a shared predator, and it is increasingly recognized as a mechanism of the decline and extinction of many species. Through case studies, we evaluated the effectiveness of 4 management strategies for species affected by apparent competition: predator control, reduction in the abundances of alternate prey, simultaneous control of predators and alternate prey, and no active management of predators or alternate prey. Solely reducing predator abundances rapidly increased abundances of alternate and rare prey, but observed increases are likely short-lived due to fast increases in predator abundance following the cessation of control efforts. Substantial reductions of an abundant alternate prey resulted in increased predation on endangered huemul (Hippocamelus bisulcus) deer in Chilean Patagonia, which highlights potential risks associated with solely reducing alternate prey species. Simultaneous removal of predators and alternate prey increased survival of island foxes (Urocyon littoralis) in California (U.S.A.) above a threshold required for population recovery. In the absence of active management, populations of rare woodland caribou (Rangifer tarandus caribou) continued to decline in British Columbia, Canada. On the basis of the cases we examined, we suggest the simultaneous control of predators and alternate prey is the management strategy most likely to increase abundances and probabilities of persistence of rare prey over the long term. Knowing the mechanisms driving changes in species' abundances before implementing any management intervention is critical. We suggest scientists can best contribute to the conservation of species affected by apparent competition by clearly communicating the biological and demographic forces at play to policy makers responsible for the implementation of proposed management actions.

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.

Resource exploitation efficiency collapses the home range of an apex predator.

Optimizing energy acquisition and expenditure is a fundamental trade-off for consumers, strikingly reflected in how mobile organisms use space. Several studies have established that home range size decreases as resource density increases, but the balance of costs and benefits associated with exploiting a given resource density is unclear. We evaluate how the ability of consumers to exploit their resources through movement (termed "resource exploitation") interacts with resource density to influence home range size. We then contrast two hypotheses to evaluate how resource exploitation influences home range size across a vast gradient of productivity and density of human-created linear features (roads and seismic lines) that are known to facilitate animal movements. Under the Diffusion Facilitation Hypothesis, linear features are predicted to lead to more diffuse space use and larger home ranges. Under the Exploitation Efficiency Hypothesis, linear features are predicted to increase foraging efficiency, resulting in less space being required to meet energetic demands and therefore smaller home ranges. Using GPS telemetry data from 142 wolves (Canis lupus) distributed over more than 500,000 km2 , we found that wolf home range size was influenced by the interaction between resource density and exploitation efficiency. Home range size decreased as linear feature density increased, supporting the Exploitation Efficiency Hypothesis. However, the effect of linear features on home range size diminished in more productive areas, suggesting that exploitation efficiency is of greater importance when resource density is low. These results suggest that smaller home ranges will occur where both linear feature density and primary productivity are higher, thereby increasing regional wolf density.

Demographic responses of a threatened, low-density ungulate to annual variation in meteorological and phenological conditions.

As global climate change progresses, wildlife management will benefit from knowledge of demographic responses to climatic variation, particularly for species already endangered by other stressors. In Canada, climate change is expected to increasingly impact populations of threatened woodland caribou (Rangifer tarandus caribou) and much focus has been placed on how a warming climate has potentially facilitated the northward expansion of apparent competitors and novel predators. Climate change, however, may also exert more direct effects on caribou populations that are not mediated by predation. These effects include meteorological changes that influence resource availability and energy expenditure. Research on other ungulates suggests that climatic variation may have minimal impact on low-density populations such as woodland caribou because per-capita resources may remain sufficient even in "bad" years. We evaluated this prediction using demographic data from 21 populations in western Canada that were monitored for various intervals between 1994 and 2015. We specifically assessed whether juvenile recruitment and adult female survival were correlated with annual variation in meteorological metrics and plant phenology. Against expectations, we found that both vital rates appeared to be influenced by annual climatic variation. Juvenile recruitment was primarily correlated with variation in phenological conditions in the year prior to birth. Adult female survival was more strongly correlated with meteorological conditions and declined during colder, more variable winters. These responses may be influenced by the life history of woodland caribou, which reside in low-productivity refugia where small climatic changes may result in changes to resources that are sufficient to elicit strong demographic effects. Across all models, explained variation in vital rates was low, suggesting that other factors had greater influence on caribou demography. Nonetheless, given the declining trajectories of many woodland caribou populations, our results highlight the increased relevance of recovery actions when adverse climatic conditions are likely to negatively affect caribou demography.

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.

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.

Influence of In-Situ Oil Sands Development on Caribou (Rangifer tarandus) Movement.

In-situ oil sands development (ISD) involves a network of facilities, wells, roads and pipelines to extract and transport subsurface bitumen. This technology is rapidly expanding and there is uncertainty whether ISDs restrict animal movement, leading to increased extinction probabilities for some wide-ranging species. Here we test for effects of simulated future (i.e., 50 years from now) and current ISDs on simulated movements of woodland caribou (Rangifer tarandus), a threatened species across North America. In simulations of future scenarios, we varied the spacing and permeability of ISDs and the presence/absence of protected areas. Permeability was measured as the number of times simulated caribou crossed ISDs with different levels of modelled permeability. We estimated the effects of these factors on caribou step length and annual home range size, key metrics of small and large spatiotemporal scales of movement, respectively. Current caribou crossings of above-ground pipeline features of ISDs were measured using camera traps and compared to expected caribou crossing rates based on present-day caribou movement simulations. Current crossing rates were evaluated within the context of predicted future crossing success rates necessary to maintain caribou step lengths and home ranges. With few exceptions, permeability across ISDs was the main factor affecting caribou movement, more so than spacing between developments or the presence of protected areas. However, minimal permeability (crossing rates of c. 15% to 60%, relative to an undisturbed site was needed to maintain existing home range size and step lengths. The effect of permeability on home range size and step length was non-linear, suggesting that small increases in permeability would provide a disproportionately greater benefit to caribou movement. Our predictions demonstrate that maintaining permeability across ISDs is more important than spacing between leases or including protected areas, and thus provides clear direction for mitigation efforts for features that will exist on the landscape for decades to come.

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.