Applied winter biology: threats, conservation and management of biological resources during winter in cold climate regions.

Winter at high latitudes is characterized by low temperatures, dampened light levels and short photoperiods which shape ecological and evolutionary outcomes from cells to populations to ecosystems. Advances in our understanding of winter biological processes (spanning physiology, behaviour and ecology) highlight that biodiversity threats (e.g. climate change driven shifts in reproductive windows) may interact with winter conditions, leading to greater ecological impacts. As such, conservation and management strategies that consider winter processes and their consequences on biological mechanisms may lead to greater resilience of high altitude and latitude ecosystems. Here, we use well-established threat and action taxonomies produced by the International Union of Conservation of Nature-Conservation Measures Partnership (IUCN-CMP) to synthesize current threats to biota that emerge during, or as the result of, winter processes then discuss targeted management approaches for winter-based conservation. We demonstrate the importance of considering winter when identifying threats to biodiversity and deciding on appropriate management strategies across species and ecosystems. We confirm our expectation that threats are prevalent during the winter and are especially important considering the physiologically challenging conditions that winter presents. Moreover, our findings emphasize that climate change and winter-related constraints on organisms will intersect with other stressors to potentially magnify threats and further complicate management. Though conservation and management practices are less commonly considered during the winter season, we identified several potential or already realized applications relevant to winter that could be beneficial. Many of the examples are quite recent, suggesting a potential turning point for applied winter biology. This growing body of literature is promising but we submit that more research is needed to identify and address threats to wintering biota for targeted and proactive conservation. We suggest that management decisions consider the importance of winter and incorporate winter specific strategies for holistic and mechanistic conservation and resource management.

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.

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.

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.

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.

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.

Behavioral classification of low-frequency acceleration and temperature data from a free-ranging small mammal.

The miniaturization and affordability of new technology is driving a biologging revolution in wildlife ecology with use of animal-borne data logging devices. Among many new biologging technologies, accelerometers are emerging as key tools for continuously recording animal behavior. Yet a critical, but under-acknowledged consideration in biologging is the trade-off between sampling rate and sampling duration, created by battery- (or memory-) related sampling constraints. This is especially acute among small animals, causing most researchers to sample at high rates for very limited durations. Here, we show that high accuracy in behavioral classification is achievable when pairing low-frequency acceleration recordings with temperature. We conducted 84 hr of direct behavioral observations on 67 free-ranging red squirrels (200-300 g) that were fitted with accelerometers (2 g) recording tri-axial acceleration and temperature at 1 Hz. We then used a random forest algorithm and a manually created decision tree, with variable sampling window lengths, to associate observed behavior with logger recorded acceleration and temperature. Finally, we assessed the accuracy of these different classifications using an additional 60 hr of behavioral observations, not used in the initial classification. The accuracy of the manually created decision tree classification using observational data varied from 70.6% to 91.6% depending on the complexity of the tree, with increasing accuracy as complexity decreased. Short duration behavior like running had lower accuracy than long-duration behavior like feeding. The random forest algorithm offered similarly high overall accuracy, but the manual decision tree afforded the flexibility to create a hierarchical tree, and to adjust sampling window length for behavioral states with varying durations. Low frequency biologging of acceleration and temperature allows accurate behavioral classification of small animals over multi-month sampling durations. Nevertheless, low sampling rates impose several important limitations, especially related to assessing the classification accuracy of short duration behavior.

To Everything There Is a Season: Summer-to-Winter Food Webs and the Functional Traits of Keystone Species.

From a trophic perspective, a seasonal increase in air temperature and photoperiod propagates as bottom-up pulse of primary production by plants, secondary production by herbivores, and tertiary production by carnivores. However, food web seasonality reflects not only abiotic variation in temperature and photoperiod, but also the composition of the biotic community and their functional responses to this variation. Some plants and animals-here referred to as seasonal specialists-decouple from food webs in winter through migration or various forms of metabolic arrest (e.g., senescence, diapause, and hibernation), whereas some plants and resident animals-here referred to as seasonal generalists-remain present and trophically coupled in winter. The co-occurrence of species with divergent responses to winter introduces seasonal variation in interaction strengths, resulting in summer-to-winter differences in trophic organization. Autumn cooling and shortening day length arrests primary productivity and cues seasonal herbivores to decouple, leaving generalist carnivores to concentrate their predation on the few generalist herbivores that remain resident, active, and vulnerable to predation in winter, which themselves feed on the few generalist plant structures available in winter. Thus, what was a bottom-up pulse, spread among many species in summer, including highly productive seasonal specialists, reverses into strong top-down regulation in winter that is top-heavy, and concentrated among a small number of generalist herbivores and their winter foods. Intermediate-sized, generalist herbivores that remain active and vulnerable to predation in winter are likely to be keystone species in seasonal food webs because they provide the essential ecosystem service of turning summer primary productivity into winter food for carnivores. Empirical examination of terrestrial mammals and their seasonal trophic status in the boreal forest and across an arctic-to-tropics seasonality gradient indicates seasonal specialization is more common among herbivores, small body sizes, and in regions with intermediate seasonality, than among carnivores, large body size, and regions where summers are very short or very long. Better understanding of food webs in seasonal environments, including their vulnerability and resilience to climate change, requires a multi-season perspective.

Predators, energetics and fitness drive neonatal reproductive failure in red squirrels.

Neonatal reproductive failure should occur when energetic costs of parental investment outweigh fitness benefits. However, little is known about the drivers of neonatal reproductive failure in free-ranging species experiencing continuous natural variation in predator abundance and in the energetic and fitness costs and benefits associated with parental investment. Long-term comprehensive studies are required to better understand how biotic, abiotic and life-history conditions interact to drive occurrences of reproductive failure in the wild. Using 24 years (1987-2011) of reproductive data from a northern boreal population of North American red squirrels in south-western Yukon, we examined the effects of predator abundance, energetics (resource availability, ambient temperature and litter size) and fitness benefits (probability of overwinter juvenile survival and maternal age) on occurrences of neonatal reproductive failure (494/2670 reproductive attempts; 18·5%). Neonatal reproductive failure was driven by a combination of predator abundance, and the energetic and fitness costs and benefits of parental investment. The abundance of mustelids and maternal age was positively related to the occurrence of neonatal reproductive failure. High energy costs associated with a combination of low resource availability and cold ambient temperatures or large litters, corresponded to increased occurrences of neonatal reproductive failure. However, the strength of these relationships was influenced by variation in juvenile overwinter survival (i.e. fitness benefits). We provide evidence that predation pressure is an important driver of neonatal reproductive failure. In addition, we found a trade-off occurs between resource-dependent energetic and fitness costs and benefits of raising the current litter to independence.