When death comes: linking predator-prey activity patterns to timing of mortality to understand predation risk.

The assumption that activity and foraging are risky for prey underlies many predator-prey theories and has led to the use of predator-prey activity overlap as a proxy of predation risk. However, the simultaneous measures of prey and predator activity along with timing of predation required to test this assumption have not been available. Here, we used accelerometry data on snowshoe hares (Lepus americanus) and Canada lynx (Lynx canadensis) to determine activity patterns of prey and predators and match these to precise timing of predation. Surprisingly we found that lynx kills of hares were as likely to occur during the day when hares were inactive as at night when hares were active. We also found that activity rates of hares were not related to the chance of predation at daily and weekly scales, whereas lynx activity rates positively affected the diel pattern of lynx predation on hares and their weekly kill rates of hares. Our findings suggest that predator-prey diel activity overlap may not always be a good proxy of predation risk, and highlight a need for examining the link between predation and spatio-temporal behaviour of predator and prey to improve our understanding of how predator-prey behavioural interactions drive predation risk.

Balancing food acquisition and predation risk drives demographic changes in snowshoe hare population cycles.

Snowshoe hare cycles are one of the most prominent phenomena in ecology. Experimental studies point to predation as the dominant driving factor, but previous experiments combining food supplementation and predator removal produced unexplained multiplicative effects on density. We examined the potential interactive effects of food limitation and predation in causing hare cycles using an individual-based food-supplementation experiment over-winter across three cycle phases that naturally varied in predation risk. Supplementation doubled over-winter survival with the largest effects occurring in the late increase phase. Although the proximate cause of mortality was predation, supplemented hares significantly decreased foraging time and selected for conifer habitat, potentially reducing their predation risk. Supplemented hares also lost less body mass which resulted in the production of larger leverets. Our results establish a mechanistic link between how foraging time, mass loss and predation risk affect survival and reproduction, potentially driving demographic changes associated with hare cycles.

Contribution of late-litter juveniles to the population dynamics of snowshoe hares.

Determining the factors driving cyclic dynamics in species has been a primary focus of ecology. For snowshoe hares (Lepus americanus), explanations of their 10-year population cycles most commonly feature direct predation during the peak and decline, in combination with their curtailment in reproduction. Hares are thought to stop producing third and fourth litters during the cyclic decline and do not recover reproductive output for several years. The demographic effects of these reproductive changes depend on the consistency of this pattern across cycles, and the relative contribution to population change of late-litter versus early litter juveniles. We used monitoring data on snowshoe hares in Yukon, Canada, to examine the contribution of late-litter juveniles to the demography of their cycles, by assigning litter group for individuals caught in autumn based on body size and capture date. We found that fourth-litter juveniles occur consistently during the increase phase of each cycle, but are rare and have low over-winter survival (0.05) suggesting that population increase is unlikely to be caused by their occurrence. The proportion of third-litter juveniles captured in the autumn remains relatively constant across cycle phases, while over-winter survival rates varies particularly for earlier-litter juveniles (0.14-0.39). Juvenile survival from all litters is higher during the population increase and peak, relative to the low and decline. Overall, these results suggest that the transition from low phase to population growth may stem in large part from changes in juvenile survival as opposed to increased reproductive output through the presence of a 4th litter.

Prey availability and ambient temperature influence carrion persistence in the boreal forest.

Scavenging by vertebrates can have important impacts on food web stability and persistence, and can alter the distribution of nutrients throughout the landscape. However, scavenging communities have been understudied in most regions around the globe, and we lack understanding of the biotic drivers of vertebrate scavenging dynamics. In this paper, we examined how changes in prey density and carrion biomass caused by population cycles of a primary prey species, the snowshoe hare Lepus americanus, influence scavenging communities in the northern boreal forest. We further examined the impact of habitat and temperature on scavenging dynamics. We monitored the persistence time, time until first scavenger, and number of species scavenging experimentally-placed hare carcasses over four consecutive years in the southwestern Yukon. We simultaneously monitored hare density and carrion biomass to examine their influence relative to temperature, habitat, and seasonal effects. For the primary scavengers, we developed species-specific scavenging models to determine variation on the effects of these factors across species, and determine which species may be driving temporal patterns in the entire community. We found that the efficiency of the scavenging community was affected by hare density, with carcass persistence decreasing when snowshoe hare densities declined, mainly due to increased scavenging rates by Canada lynx Lynx canadensis. However, prey density did not influence the number of species scavenging a given carcass, suggesting prey abundance affects carrion recycling but not necessarily the number of connections in the food web. In addition, scavenging rates increased in warmer temperatures, and there were strong seasonal effects on the richness of the vertebrate scavenging community. Our results demonstrate that vertebrate scavenging communities are sensitive to changes in species' demography and environmental change, and that future assessments of food web dynamics should consider links established through scavenging.

Hair cortisol as a reliable indicator of stress physiology in the snowshoe hare: Influence of body region, sex, season, and predator-prey population dynamics.

Hair cortisol concentration is increasingly used as a convenient, non-invasive, and integrative measure of physiology and health in natural populations of mammals. However, the use of this index is potentially confounded by individual variation in body region-specific differences in cortisol deposition rates. Here we examine correlations in cortisol concentrations in hair collected from the ear, shoulder, and thigh of wild snowshoe hares, Lepus americanus, as well as the influence of sex on cortisol measurements. We further evaluated this technique's ability to capture seasonal and cyclical patterns of snowshoe hare glucocorticoid secretion from 2013 to 2015 in the southwestern Yukon (Canada). We found positive correlations (R2 = 0.20-0.32) in all pairwise comparisons among body regions, and differences among individuals accounted for the greatest proportion of variance (47.3%) in measurements. From 2013 to 2015 the hares' primary predator - Canada lynx - approximately doubled in population abundance. We found a significant increase in hare hair cortisol concentrations across this time period. Cortisol indices were higher in summer than winter pelage, reflecting predicted physiological responses to seasonal variation in food availability and individual risk. Variation in hair cortisol concentrations was more similar to long-term (weeks-months) integrative indices of adrenal capacity than point samples of fecal glucocorticoid metabolite concentrations. Overall, we find that hair cortisol analysis is a simple and useful tool for estimations of population-level stress physiology in wild mammals, and sampling of core body regions with consistent moulting patterns produced the most robust results in this species.

Quantifying fear effects on prey demography in nature.

In recent years, it has been argued that the effect of predator fear exacts a greater demographic toll on prey populations than the direct killing of prey. However, efforts to quantify the effects of fear have primarily relied on experiments that replace predators with predator cues. Interpretation of these experiments must consider two important caveats: (1) the magnitude of experimenter-induced predator cues may not be realistically comparable to those of the prey's natural sensory environment, and (2) given functional predators are removed from the treatments, the fear effect is measured in the absence of any consumptive effects, a situation which never occurs in nature. We contend that demographic consequences of fear in natural populations may have been overestimated because the intensity of predator cues applied by experimenters in the majority of studies has been unnaturally high, in some instances rarely occurring in nature without consumption. Furthermore, the removal of consumption from the treatments creates the potential situation that individual prey in poor condition (those most likely to contribute strongly to the observed fear effects via starvation or reduced reproductive output) may have been consumed by predators in nature prior to the expression of fear effects, thus confounding consumptive and fear effects. Here, we describe an alternative treatment design that does not utilize predator cues, and in so doing, better quantifies the demographic effect of fear on wild populations. This treatment substitutes the traditional cue experiment where consumptive effects are eliminated and fear is simulated with a design where fear is removed and consumptive effects are simulated through the experimental removal of prey. Comparison to a natural population would give a more robust estimate of the effect of fear in the presence of consumption on the demographic variable of interest. This approach represents a critical advance in quantifying the mechanistic pathways through which predation structures ecological communities. Discussing the merits of both treatments will motivate researchers to go beyond simply describing the existence of fear effects and focus on testing their true magnitude in wild populations and natural communities.

Use of salivary cortisol to evaluate the influence of rides in dromedary camels.

Animals in captivity and in the wild face numerous challenges, including the risk of enduring acute or chronic stress. In captivity, facilities attempt to alleviate the risk of chronic stress by providing environmental enrichment, shown to minimize behavioral disorders and stress in several species. One potential form of enrichment in zoos is training animals to provide rides for guests, however, the effect of this activity on the welfare of individual animals has never been examined. We validated the use of saliva for assessing stress in dromedary camels (Camelus dromedarius), an animal commonly used for rides. We then measured variation in salivary cortisol in four male camels while providing rides of differing frequency for guests at the Toronto Zoo. The camels were sampled during the ride season (June to September) using four treatments: (1) in their pasture, (2) at the ride area when not performing rides, (3) while providing a low number of rides (n=50/day) and (4) while providing a high number of rides (n=150/day). Furthermore, samples were taken before and after the ride season for comparison. There was a significant difference between the post-ride season treatment and the three treatments involving guest presence during the ride season (ride area, low rides, high rides). In general, cortisol concentrations were lower during the ride season and higher during the non-ride season. Based on the metrics we used, performing rides is not a stressful experience for these dromedary camels and suggests that rides may be a form of enrichment.

Coat color mismatch improves survival of a keystone boreal herbivore: Energetic advantages exceed lost camouflage.

Climate warming is causing asynchronies between animal phenology and environments. Mismatched traits, such as coat color change mismatched with snow, can decrease survival. However, coat change does not serve a singular adaptive benefit of camouflage, and alternate coat change functions may confer advantages that supersede mismatch costs. We found that mismatch reduced, rather than increased, autumn mortality risk of snowshoe hares in Yukon by 86.5% when mismatch occurred. We suggest that the increased coat insulation and lower metabolic rates of winter-acclimatized hares confer energetic advantages to white mismatched hares that reduce their mortality risk. We found that white mismatched hares forage 17-77 min less per day than matched brown hares between 0°C and -10°C, thus lowering their predation risk and increasing survival. We found no effect of mismatch on spring mortality risk, during which mismatch occurred at warmer temperatures, suggesting a potential temperature limit at which the costs of conspicuousness outweigh energetic benefits.

Food availability and long-term predation risk interactively affect antipredator response.

Food availability and temporal variation in predation risk are both important determinants of the magnitude of antipredator responses, but their effects have rarely been examined simultaneously, particularly in wild prey. Here, we determine how food availability and long-term predation risk affect antipredator responses to acute predation risk by monitoring the foraging response of free-ranging snowshoe hares (Lepus americanus) to an encounter with a Canada lynx (Lynx canadensis) in Yukon, Canada, over four winters (2015-2016 to 2018-2019). We examined how this response was influenced by natural variation in long-term predation risk (2-month mortality rate of hares) while providing some individuals with supplemental food. On average, snowshoe hares reduced foraging time up to 10 h after coming into close proximity (≤75 m) with lynx, and reduced foraging time an average of 15.28 ± 7.08 min per lynx encounter. Hares tended to respond more strongly when the distance to lynx was shorter. More importantly, the magnitude of hares' antipredator response to a lynx encounter was affected by the interaction between food-supplementation and long-term predation risk. Food-supplemented hares reduced foraging time more than control hares after a lynx encounter under low long-term risk, but decreased the magnitude of the response as long-term risk increased. In contrast, control hares increased the magnitude of their response as long-term risk increased. Our findings show that food availability and long-term predation risk interactively drive the magnitude of reactive antipredator response to acute predation risk. Determining the factors driving the magnitude of antipredator responses would contribute to a better understanding of the indirect effects of predators on prey populations.

There's a storm a-coming: Ecological resilience and resistance to extreme weather events.

Extreme weather events (EWEs) are expected to increase in stochasticity, frequency, and intensity due to climate change. Documented effects of EWEs, such as droughts, hurricanes, and temperature extremes, range from shifting community stable states to species extirpations. To date, little attention has been paid to how populations resist and/or recover from EWEs through compensatory (behavioral, demographic, or physiological) mechanisms; limiting the capacity to predict species responses to future changes in EWEs. Here, we systematically reviewed the global variation in species' demographic responses, resistance to, and recovery from EWEs across weather types, species, and biogeographic regions. Through a literature review and meta-analysis, we tested the prediction that population abundance and probability of persistence will decrease in populations after an EWE and how compensation affects that probability. Across 524 species population responses to EWEs reviewed (27 articles), we noted large variation in responses, such that, on average, the effect of EWEs on population demographics was not negative as predicted. The majority of species populations (80.4%) demonstrated compensatory mechanisms during events to reduce their deleterious effects. However, for populations that were negatively impacted, the demographic consequences were severe. Nearly 20% of the populations monitored experienced declines of over 50% after an EWE, and 6.8% of populations were extirpated. Population declines were reflected in a reduction in survival. Further, resilience was not common, as 80.0% of populations that declined did not recover to before EWE levels while monitored. However, average monitoring time was only two years with over a quarter of studies tracking recovery for less than the study species generation time. We conclude that EWEs have positive and negative impacts on species demography, and this varies by taxa. Species population recovery over short-time intervals is rare, but long-term studies are required to accurately assess species resilience to current and future events.

Continental divide: Predicting climate-mediated fragmentation and biodiversity loss in the boreal forest.

Climate change threatens natural landscapes through shifting distribution and abundance of species and attendant change in the structure and function of ecosystems. However, it remains unclear how climate-mediated variation in species' environmental niche space may lead to large-scale fragmentation of species distributions, altered meta-population dynamics and gene flow, and disrupted ecosystem integrity. Such change may be especially relevant when species distributions are restricted either spatially or to a narrow environmental niche, or when environments are rapidly changing. Here, we use range-wide environmental niche models to posit that climate-mediated range fragmentation aggravates the direct effects of climate change on species in the boreal forest of North America. We show that climate change will directly alter environmental niche suitability for boreal-obligate species of trees, birds and mammals (n = 12), with most species ranges becoming smaller and shifting northward through time. Importantly, species distributions will become increasingly fragmented, as characterized by smaller mean size and greater isolation of environmentally-suitable landscape patches. This loss is especially pronounced along the Ontario-Québec border, where the boreal forest is narrowest and roughly 78% of suitable niche space could disappear by 2080. Despite the diversity of taxa surveyed, patterns of range fragmentation are remarkably consistent, with our models predicting that spruce grouse (Dendragapus canadensis), boreal chickadee (Poecile hudsonicus), moose (Alces americanus) and caribou (Rangifer tarandus) could have entirely disjunct east-west population segments in North America. These findings reveal potentially dire consequences of climate change on population continuity and species diversity in the boreal forest, highlighting the need to better understand: 1) extent and primary drivers of anticipated climate-mediated range loss and fragmentation; 2) diversity of species to be affected by such change; 3) potential for rapid adaptation in the most strongly-affected areas; and 4) potential for invasion by replacement species.