Polar bear energetic and behavioral strategies on land with implications for surviving the ice-free period.

Declining Arctic sea ice is increasing polar bear land use. Polar bears on land are thought to minimize activity to conserve energy. Here, we measure the daily energy expenditure (DEE), diet, behavior, movement, and body composition changes of 20 different polar bears on land over 19-23 days from August to September (2019-2022) in Manitoba, Canada. Polar bears on land exhibited a 5.2-fold range in DEE and 19-fold range in activity, from hibernation-like DEEs to levels approaching active bears on the sea ice, including three individuals that made energetically demanding swims totaling 54-175 km. Bears consumed berries, vegetation, birds, bones, antlers, seal, and beluga. Beyond compensating for elevated DEE, there was little benefit from terrestrial foraging toward prolonging the predicted time to starvation, as 19 of 20 bears lost mass (0.4-1.7 kg•day-1). Although polar bears on land exhibit remarkable behavioral plasticity, our findings reinforce the risk of starvation, particularly in subadults, with forecasted increases in the onshore period.

A body composition model with multiple storage compartments for polar bears (Ursus maritimus).

Climate warming is rapidly altering Arctic ecosystems. Polar bears (Ursus maritimus) need sea ice as a platform from which to hunt seals, but increased sea-ice loss is lengthening periods when bears are without access to primary hunting habitat. During periods of food scarcity, survival depends on the energy that a bear has stored in body reserves, termed storage energy, making this a key metric in predictive models assessing climate change impacts on polar bears. Here, we developed a body composition model for polar bears that estimates storage energy while accounting for changes in storage tissue composition. We used data of dissected polar bears (n = 31) to link routinely collected field measures of total body mass and straight-line body length to the body composition of individual bears, described in terms of structural mass and two storage compartments, adipose and muscle. We then estimated the masses of metabolizable proteins and lipids within these storage compartments, giving total storage energy. We tested this multi-storage model by using it to predict changes in the lipid stores from an independent dataset of wild polar bears (n = 36) that were recaptured 8-200 days later. Using length and mass measurements, our model successfully predicted direct measurements of lipid changes via isotopic dilutions (root mean squared error of 14.5 kg). Separating storage into two compartments, and allowing the molecular composition of storage to vary, provides new avenues for quantifying energy stores of individuals across their life cycle. The multi-storage body composition model thus provides a basis for further exploring energetic costs of physiological processes that contribute to individual survival and reproductive success. Given bioenergetic models are increasingly used as a tool to predict individual fitness and population dynamics, our approach for estimating individual energy stores could be applicable to a wide range of species.

The acute physiological response of polar bears to helicopter capture.

Many wildlife species are live captured, sampled, and released; for polar bears (Ursus maritimus) capture often requires chemical immobilization via helicopter darting. Polar bears reduce their activity for approximately 4 days after capture, likely reflecting stress recovery. To better understand this stress, we quantified polar bear activity (via collar-mounted accelerometers) and body temperature (via loggers in the body core [Tabd] and periphery [Tper]) during 2-6 months of natural behavior, and during helicopter recapture and immobilization. Recapture induced bouts of peak activity higher than those that occurred during natural behavior for 2 of 5 bears, greater peak Tper for 3 of 6 bears, and greater peak Tabd for 1 of 6 bears. High body temperature (>39.0°C) occurred in Tper for 3 of 6 individuals during recapture and 6 of 6 individuals during natural behavior, and in Tabd for 2 of 6 individuals during recapture and 3 of 6 individuals during natural behavior. Measurements of Tabd and Tper correlated with rectal temperatures measured after immobilization, supporting the use of rectal temperatures for monitoring bear response to capture. Using a larger dataset (n = 66 captures), modeling of blood biochemistry revealed that maximum ambient temperature during recapture was associated with a stress leukogram (7-26% decline in percent lymphocytes, 12-21% increase in percent neutrophils) and maximum duration of helicopter operations had a similar but smaller effect. We conclude that polar bear activity and body temperature during helicopter capture are similar to that which occurs during the most intense events of natural behavior; high body temperature, especially in warm capture conditions, is a key concern; additional study of stress leukograms in polar bears is needed; and additional data collection regarding capture operations would be useful.

Physiological consequences of Arctic sea ice loss on large marine carnivores: unique responses by polar bears and narwhals.

Rapid environmental changes in the Arctic are threatening the survival of marine species that rely on the predictable presence of the sea ice. Two Arctic marine mammal specialists, the polar bear (Ursus maritimus) and narwhal (Monodon monoceros), appear especially vulnerable to the speed and capriciousness of sea ice deterioration as a consequence of their unique hunting behaviors and diet, as well as their physiological adaptations for slow-aerobic exercise. These intrinsic characteristics limit the ability of these species to respond to extrinsic threats associated with environmental change and increased industrial activity in a warming Arctic. In assessing how sea ice loss may differentially affect polar bears that hunt on the ice surface and narwhals that hunt at extreme depths below, we found that major ice loss translated into elevated locomotor costs that range from 3- to 4-fold greater than expected for both species. For polar bears this instigates an energy imbalance from the combined effects of reduced caloric intake and increased energy expenditure. For narwhals, high locomotor costs during diving increase the risk of ice entrapment due to the unreliability of breathing holes. These species-specific physiological constraints and extreme reliance on the polar sea ice conspire to make these two marine mammal specialists sentinels of climate change within the Arctic marine ecosystem that may foreshadow rapid changes to the marine ecosystem.

Identifying reliable indicators of fitness in polar bears.

Animal structural body size and condition are often measured to evaluate individual health, identify responses to environmental change and food availability, and relate food availability to effects on reproduction and survival. A variety of condition metrics have been developed but relationships between these metrics and vital rates are rarely validated. Identifying an optimal approach to estimate the body condition of polar bears is needed to improve monitoring of their response to decline in sea ice habitat. Therefore, we examined relationships between several commonly used condition indices (CI), body mass, and size with female reproductive success and cub survival among polar bears (Ursus maritimus) measured in two subpopulations over three decades. To improve measurement and application of morphometrics and CIs, we also examined whether CIs are independent of age and structural size-an important assumption for monitoring temporal trends-and factors affecting measurement precision and accuracy. Maternal CIs and mass measured the fall prior to denning were related to cub production. Similarly, maternal CIs, mass, and length were related to the mass of cubs or yearlings that accompanied her. However, maternal body mass, but not CIs, measured in the spring was related to cub production and only maternal mass and length were related to the probability of cub survival. These results suggest that CIs may not be better indicators of fitness than body mass in part because CIs remove variation associated with body size that is important in affecting fitness. Further, CIs exhibited variable relationships with age for growing bears and were lower for longer bears despite body length being related to cub survival and female reproductive success. These results are consistent with findings from other species indicating that body mass is a useful metric to link environmental conditions and population dynamics.

The seasonal energetic landscape of an apex marine carnivore, the polar bear.

Divergent movement strategies have enabled wildlife populations to adapt to environmental change. In recent decades, the Southern Beaufort Sea subpopulation of polar bears (Ursus maritimus) has developed a divergent movement strategy in response to diminishing sea ice where the majority of the subpopulation (73-85%) stays on the sea ice in summer and the remaining bears move to land. Although declines in sea ice are generally considered a challenge to energy balance in polar bears residing in some regions of the Arctic, little quantitative data exists concerning the seasonal energy expenditures of this apex marine carnivore. We used GPS satellite collars with tri-axial accelerometers and conductivity sensors to measure the location, behavior, and energy expenditure of five adult female polar bears in the southern Beaufort Sea across seasons of sea ice breakup and minimum extent. Using a Bayesian mixed-effects model, we found that energy expenditure was influenced by month, ocean depth, and habitat type (sea ice or land). Total energy expenditure from May through September ranged from 37.7 to 47.2 mJ/kg for individual bears. Bears that moved to land expended 7% more energy on average from May through September than bears that remained on the receding sea ice. In August, when bears were moving from the sea ice to land or moving north with the receding pack ice, bears that moved to land spent 7% more time swimming and expended 22% more energy. This means the immediate cost of moving to land exceeded the cost of remaining on the receding summer pack ice. These findings suggest a physiological reason why the majority of the Southern Beaufort Sea subpopulation continues to inhabit a diminishing summer ice platform. However, bears that moved to land spent 29% more time in preferred hunting habitats over the continental shelf than bears that remained on the sea ice. Bears on land also had access to subsistence-harvested bowhead whale carcasses. Hence, our findings indicate there may be a greater overall energetic benefit to move to land in this region, which suggests that the use of the diminishing summer sea ice may be functioning as an ecological trap.

Estimating the energy expenditure of free-ranging polar bears using tri-axial accelerometers: A validation with doubly labeled water.

Measures of energy expenditure can be used to inform animal conservation and management, but methods for measuring the energy expenditure of free-ranging animals have a variety of limitations. Advancements in biologging technologies have enabled the use of dynamic body acceleration derived from accelerometers as a proxy for energy expenditure. Although dynamic body acceleration has been shown to strongly correlate with oxygen consumption in captive animals, it has been validated in only a few studies on free-ranging animals. Here, we use relationships between oxygen consumption and overall dynamic body acceleration in resting and walking polar bears Ursus maritimus and published values for the costs of swimming in polar bears to estimate the total energy expenditure of 6 free-ranging polar bears that were primarily using the sea ice of the Beaufort Sea. Energetic models based on accelerometry were compared to models of energy expenditure on the same individuals derived from doubly labeled water methods. Accelerometer-based estimates of energy expenditure on average predicted total energy expenditure to be 30% less than estimates derived from doubly labeled water. Nevertheless, accelerometer-based measures of energy expenditure strongly correlated (r 2 = 0.70) with measures derived from doubly labeled water. Our findings highlight the strengths and limitations in dynamic body acceleration as a measure of total energy expenditure while also further supporting its use as a proxy for instantaneous, detailed energy expenditure in free-ranging animals.

Energetic costs of locomotion in bears: is plantigrade locomotion energetically economical?

Ursids are the largest mammals to retain a plantigrade posture. This primitive posture has been proposed to result in reduced locomotor speed and economy relative to digitigrade and unguligrade species, particularly at high speeds. Previous energetics research on polar bears (Ursus maritimus) found locomotor costs were more than double predictions for similarly sized quadrupedal mammals, which could be a result of their plantigrade posture or due to adaptations to their Arctic marine existence. To evaluate whether polar bears are representative of terrestrial ursids or distinctly uneconomical walkers, this study measured the mass-specific metabolism, overall dynamic body acceleration, and gait kinematics of polar bears and grizzly bears (Ursus arctos) trained to rest and walk on a treadmill. At routine walking speeds, we found polar bears and grizzly bears exhibited similar costs of locomotion and gait kinematics, but differing measures of overall dynamic body acceleration. Minimum cost of transport while walking in the two species (2.21 J kg-1 m-1) was comparable to predictions for similarly sized quadrupedal mammals, but these costs doubled (4.42 J kg-1 m-1) at speeds ≥5.4 km h-1 Similar to humans, another large plantigrade mammal, bears appear to exhibit a greater economy while moving at slow speeds.

Spring fasting behavior in a marine apex predator provides an index of ecosystem productivity.

The effects of declining Arctic sea ice on local ecosystem productivity are not well understood but have been shown to vary inter-specifically, spatially, and temporally. Because marine mammals occupy upper trophic levels in Arctic food webs, they may be useful indicators for understanding variation in ecosystem productivity. Polar bears (Ursus maritimus) are apex predators that primarily consume benthic and pelagic-feeding ice-associated seals. As such, their productivity integrates sea ice conditions and the ecosystem supporting them. Declining sea ice availability has been linked to negative population effects for polar bears but does not fully explain observed population changes. We examined relationships between spring foraging success of polar bears and sea ice conditions, prey productivity, and general patterns of ecosystem productivity in the Beaufort and Chukchi Seas (CSs). Fasting status (≥7 days) was estimated using serum urea and creatinine levels of 1,448 samples collected from 1,177 adult and subadult bears across three subpopulations. Fasting increased in the Beaufort Sea between 1983-1999 and 2000-2016 and was related to an index of ringed seal body condition. This change was concurrent with declines in body condition of polar bears and observed changes in the diet, condition and/or reproduction of four other vertebrate consumers within the food chain. In contrast, fasting declined in CS polar bears between periods and was less common than in the two Beaufort Sea subpopulations consistent with studies demonstrating higher primary productivity and maintenance or improved body condition in polar bears, ringed seals, and bearded seals despite recent sea ice loss in this region. Consistency between regional and temporal variation in spring polar bear fasting and food web productivity suggests that polar bears may be a useful indicator species. Furthermore, our results suggest that spatial and temporal ecological variation is important in affecting upper trophic-level productivity in these marine ecosystems.

Habitat degradation affects the summer activity of polar bears.

Understanding behavioral responses of species to environmental change is critical to forecasting population-level effects. Although climate change is significantly impacting species' distributions, few studies have examined associated changes in behavior. Polar bear (Ursus maritimus) subpopulations have varied in their near-term responses to sea ice decline. We examined behavioral responses of two adjacent subpopulations to changes in habitat availability during the annual sea ice minimum using activity data. Location and activity sensor data collected from 1989 to 2014 for 202 adult female polar bears in the Southern Beaufort Sea (SB) and Chukchi Sea (CS) subpopulations were used to compare activity in three habitat types varying in prey availability: (1) land; (2) ice over shallow, biologically productive waters; and (3) ice over deeper, less productive waters. Bears varied activity across and within habitats with the highest activity at 50-75% sea ice concentration over shallow waters. On land, SB bears exhibited variable but relatively high activity associated with the use of subsistence-harvested bowhead whale carcasses, whereas CS bears exhibited low activity consistent with minimal feeding. Both subpopulations had fewer observations in their preferred shallow-water sea ice habitats in recent years, corresponding with declines in availability of this substrate. The substantially higher use of marginal habitats by SB bears is an additional mechanism potentially explaining why this subpopulation has experienced negative effects of sea ice loss compared to the still-productive CS subpopulation. Variability in activity among, and within, habitats suggests that bears alter their behavior in response to habitat conditions, presumably in an attempt to balance prey availability with energy costs.