Introduction

Climate change is causing the sea ice in arctic regions to melt earlier in spring (e.g., [1,2]), leading to a trophic mismatch between polar bears and their primary spring prey, the pups of ringed seals (Phoca hispida) [3]. The bears acquire the majority of their annual energy reserves from hunting seals on the ice, especially during the spring when they capture pups in their snow lairs [4]. In western Hudson Bay, polar bears have historically relied on the energy from hunting these seal pups to sustain them through the ice-free period on land until the ice reforms in fall [5,6]. Assuming that polar bear survival is dependent on access to seals during this critical period, many predict declines in polar bear survival and abundance coincident with the advance of sea ice breakup as polar bears will be forced ashore with smaller fat reserves for longer periods (e.g., [3,7,8]).

Molnár et al. [8] used a mechanistic approach to predict polar bear survival that involved establishing a relationship between physical measures (size and structure) and body composition to determine how energy stores are incrementally depleted as polar bears spend longer periods on land during the ice-free season. The model was parameterized with measurements of captured polar bears in western Hudson Bay and daily maintenance costs that are based on past patterns of average daily weight loss experienced by the bears until they returned to the ice [9,10]. Molnár et al. [8] used the model to predict the proportions of adult males that would starve to death as the ice-free season expands to 180 days, a scenario predicted as ice conditions worsen in response to climate change. The model takes into account somatic maintenance costs and the effects of limited movements (2 km d^-1) but does not allow for energy influx into the system from consuming additional food on land.

Molnár et al. [8] justified not including a food intake parameter with the assertion that there is no “energetically meaningful” food available for polar bears to eat. They cite Hobson et al. [11] who found that polar bears only utilize fat accumulated from hunting seals prior to coming ashore for energy based on “marine” (as opposed to “terrestrial”) stable carbon isotope signatures in exhaled CO₂ of polar bears captured on land. Because energy utilization pathways can change under conditions of extreme stress (which polar bears may experience when captured [12]) and since land-based foods, such as geese and marine algae, can possess a marine signature [13,14,15] their assertions may not be valid.

Polar bears are opportunists (e.g., [16,17]) and have been documented consuming various types and combinations of land-based food since the earliest natural history records (e.g., [18,19, 20,21]). While subadults and family groups have been most often observed pursuing terrestrial animal prey [22,23] and eating plants such as berries [16], the spatial distribution of polar bear scats and personal observations (L.J. Gormezano and R.F. Rockwell), suggest that at least some adult males currently consume plants and animals during the ice-free period [21]. In the absence of genetic analyses, the proportion of adult males using land-based resources is not yet known, but it is reasonably assumed that if such foraging occurs and yields some energetic benefit it will increase in frequency (e.g., through social learning) as the needs intensify [24,25].

In this paper, we reconstruct Molnár et al.’s [8] model to predict future survival of adult male polar bears as the ice-free season expands to 180 days, but consider a scenario in which nutritionally stressed bears seek additional terrestrial food when available. Because polar bears have always consumed food on land and such feeding is already incorporated into daily weight loss patterns used to build the original model, we only include novel animal foods (caribou, Rangifer tarandus, eggs and Lesser snow geese, hereafter snow geese or LSGO, Chen caerulescens caerulescens) that have more recently been identified in the land-based diet [13]. The recent population increases of snow geese and caribou (i.e., 1980s, 1990s) have made them more available to arriving bears, which coincides with the onset of advance in spring ice-breakup [13]. Arriving polar bears now spatially overlap nesting snow goose colonies (see Figure 1 in [26]) as well as local caribou herds which extend across the Cape Churchill Peninsula, south to the Nelson River [13]. Furthermore, as polar bears come ashore earlier they will overlap more of both the incubation periods of snow geese and calving of caribou, potentially creating a new trophic match on land to compensate for the growing mismatch with seals on the earlier disappearing ice.

To evaluate the potential effectiveness of each food toward fulfilling daily energy requirements of adult males projected to starve while on land for 180 days according to Molnár et al. [8], we address these questions:

1. How many individual or combined units of each animal sex and age class (e.g., clutch of eggs, caribou calves) would need to be consumed to prevent starvation in each adult male polar bear?
2. What is the total energy potentially available to polar bears each day from snow geese, eggs and caribou?
3. How many starving adult male polar bears could be supported by each food source?

We discuss the limitations of our derived energy calculations in light of the absence of rigorous data on certain aspects of polar bear foraging behavior such as locomotive costs associated with different foraging techniques.

Methods

Results

Of the 97 adult male polar bears sampled, Molnár et al. [8] predicted that 28% (27) and 48% (47) would starve if resting or walking before energy depletion, respectively. Of those bears that were resting before starving, we found that many (10) experienced energy deficits of less than 50,000 kcal. Of those bears that were walking before starving, most (28) experienced deficits less than 100,000 kcal, with most falling between 50,000 and 100,000 kcal based on our analyses (Fig 1).

Discussion

As the ice-free season expands with earlier spring breakup, polar bears are expected to come ashore in western Hudson Bay with smaller energy stores [3] causing them to rely on terrestrial food sources to compensate for energy deficits and avoid starvation. Molnár et al. [8] predicted that, depending upon their activity while ashore, between 28 and 48% of adult male polar bears would starve to death unless supplemental food was consumed. By evaluating the energy value of novel foods that polar bears currently consume on land, caribou, snow geese and their eggs, we found that there are sufficient calories to compensate for daily accrued energy deficits of adult male polar bears expected to starve as the ice-free season expands to 180 days. The veracity of relying on these land-based resources, however, likely depends on a number of factors including future prey availability, polar bear foraging behavior, energy costs associated with prey procurement and physiological utilization of different macronutrients.

Although local populations of both snow geese and caribou have grown substantially since the 1960s [13], future availability is difficult to predict. Both species have displayed weak phenological shifts in response to climate change, as reproductive cycles are cued more by day length than air temperature [34,35]. As a result, mismatches with emergent vegetation at the peak of goose brood rearing and peak caribou calving as well as habitat changes have impacted both species [57,67]. Snow geese in the CCP have responded to changes in food availability (mostly due to destructive foraging) by inhabiting new areas, moving further inland from the coast and consuming alternative plant species [67]. Further, there is evidence to suggest that deficiencies from mismatches with emergent vegetation at the onset of brood rearing may, in part, be compensated for by earlier access to berries later in the season (C.P. Mulder, unpublished data). Behavioral changes, such as range shifts, are possible with heavy predation, however, the lack of such responses from other nesting geese experiencing arctic fox and polar bear predation suggests that local snow goose populations would likely not alter their behavior substantially (see [26] and references therein). Such adaptive responses to environmental stresses and resilience in the face of rigorous management control attempts [38,68] suggests that snow geese may remain a viable future food source for polar bears on the CCP.

The resiliency of caribou in the face of progressive environmental change is less certain [57]. Although the Churchill herd is currently stable, studies in other regions have suggested that increases in variability and advances in emergence of commonly consumed plants with warming temperatures have negatively impacted calf survival [35]. Other threats have included replacement of preferred winter forage (i.e., lichen and herbaceous plants) with shrubs and grasses from forest fires, grazing and warmer temperatures [69,70,71]. Also, projected increases in precipitation would give predators, such as wolves, an advantage potentially increasing mortality [72]. These changes, however, can affect populations adapted to harsh conditions in different ways [73], so that some populations are experiencing growth while others decline [57]. Given the small number of animals required to satisfy the energetic requirements of starving polar bears, it is unclear whether even modest future declines in the Churchill herd would hinder polar bear predation efforts as long as caribou maintain their current distribution (i.e., along the coast). Caribou may occupy the coast of western Hudson Bay (where polar bears occur in high densities) for a variety of reasons including to avoid harassment by insects (e.g., [74]) so whether the increased threat of predation would cause them to shift their distribution further inland is unknown. Encounter rates between polar bears and caribou may decrease with declines in abundance and shifts in distribution, but the method of capture (e.g., ambush versus chase) may be more important in determining predation success [75,76].

With the paucity of knowledge regarding energy consumption rates at varying speeds of travel, especially for adult males (i.e., > 235 kg), it is difficult to fully evaluate the feasibility of the foraging scenarios suggested. However, based on past and current behavior, it is clear that polar bears are capable of successfully capturing land-based ungulates, such as caribou (R.F. Rockwell, pers. obs., [77]) and muskoxen [78] and actively pursuing them in western Hudson Bay and other regions (L.J. Gormezano, pers. obs., [23,56]). The mean digestible energy content of a seal, pooled across age classes, is 69,047 kcal [79], which is roughly equivalent to the average worth of an adult female caribou during June and July, although most of the energy is from protein rather than fat. Using surprise hunting techniques, such as stalking and ambushing, whereby landscape features (i.e., ice, water) are used to mask their approach, polar bears are able to successfully capture seals without engaging in potentially costly pursuits [80,81]. Polar bears have employed these same techniques on land, using shrubs and physiographic features as cover to surprise caribou (R.F. Rockwell, pers. obs., [56]) suggesting equivalent (seal) calories could be obtained on land without drastic changes in energy output. Further, caribou capture rates (1 every 8.7–31.1 days) required to sustain starving walking polar bears coming ashore in the worst condition, are comparable to capture rates (1 seal every 5.6–24.4 days) [4] of different aged seals by polar bears in spring and summer.

Consumption rates of snow goose eggs and goslings that would compensate starving walking bears ranged from 3 to 26 clutches of eggs and 2 to 19 goslings per day depending on daily energy deficits. High daily depredation rates of goose nests have been reported in populations around the Arctic (e.g., 108 barnacle goose nests) [82] but can vary depending on nest density and total availability [83,84]. Based on camera footage of an common eider colony in western Hudson Bay, some polar bears were consuming between 19 and 38 nests per day (D. Iles, unpublished data) suggesting that the maximum consumption rates required to support starving bears (26 clutches) is not unrealistic. Also, polar bears coming ashore 60 days earlier (as would be projected for 2068), they would overlap the entire incubation period, which would provide substantially more calories to arriving bears than are currently available [34].

Capture rates of goslings and adults are rarely reported [85,86] but observations of polar bears capturing and consuming up to 3 individuals per day (of various ages) have been reported for snow geese [22]. The extra skill and effort required to obtain birds (as opposed to eggs) might pose limitations on meeting daily energy requirements from birds alone, however, maximum rates suggested in the combination diet (0.2 to 1.2 goslings d^-1, for example) are quite reasonable. Further, anecdotal observations of flightless goslings and adult snow geese being consumed consecutively by the same bear [22] and remains of adult snow geese and eggs recorded in the same scat (25% of scats with eggs) further suggests a combination diet (Fig 5a and 5b) would be a more realistic means to satisfy daily energy requirements.

The large numbers of starving polar bears that can be supported by each food resource suggest that surpluses would be available for other age and sex classes coming ashore with energy deficits. It is important to note, however, that the actual number of bears that will come ashore with energy deficits is unknown and may increase over time as marine food resources become limited. Further, the only costs associated with procurement of prey are a 2 km d^-1 movement cost above somatic maintenance. Similar to lions (Panthera leo), polar bears are considered inefficient walkers so extended pursuits could reduce energetic returns [87]. Pursuits of geese on land rarely exceed 30 seconds (R.F. Rockwell, pers. obs., [22]), however, pursuits of caribou (running, walking and swimming) have lasted up to an hour (L.J. Gormezano, pers. obs., [23,56]) suggesting that costs associated with each capture (including failed attempts) could be substantial.

Williams and Yeates [88] calculated an efficiency ratio (benefits/costs) of 3.8 for African lions pursuing ungulates on land. Given the comparable locomotive inefficiencies between lions and polar bears (Gormezano and Rockwell, unpublished data, [87,89]) it is possible that when polar bears engage in longer distance pursuits, as opposed to more energy conserving surprise techniques, a similar efficiency ratio could apply. In a hypothetical example, we applied this ratio to the energetic returns for caribou and found that it increased capture costs (i.e., above somatic and movement) 1.7, 3.0, 5.3 and 6.3 times their previous value of approximately 4,450 kcal for calves, yearlings, adult females and adult males, respectively. Applying these increased costs to the calculation of the number of starving walking polar bears supported by the total calories from adult male caribou, for example, would reduce the number supported by 84% from 28,464 to 4,543 bears. Although the exact energetic costs of polar bears pursuing caribou using different hunting strategies remain unknown, the data presented here provide a basis to estimate them once the appropriate behavioral and energetic studies have been performed.

Previous studies have questioned the use of land-based foods to satisfy daily energy requirements while polar bears are on land [90,91]. Hobson et al. [11], for example, tested carbon dioxide exhaled by anesthetized polar bears in summer to evaluate whether a marine (seal) or terrestrial (berry) stable-carbon signature would be obtained and thus, which was supplying energy for current metabolic processes. Finding signatures that were almost identical to seals (and different from berries), they concluded that all bears were persisting solely on energy derived from oxidized fat reserves accumulated while on the ice [11].

It is possible, however, that the metabolic states of the bears in the Hobson et al. [11] study were altered due to the biochemical effects of being captured [92]. Using the same drugs and capture protocol, Cattet [12] found that the plasma cortisol levels of polar bears after capture were extremely elevated and although they decreased 40–50% after 1 hour, he noted that the physiological effects would continue well after the plasma cortisol levels decreased. He also observed sustained concentrations of plasma glucose correlated with the cortisol surge and suggested the bears may be exhibiting insulin resistance [12]. One of the many effects of cortisol is to sensitize adipose tissue to the action of lipolytic hormones and to cause insulin resistance by decreasing the rate at which insulin activates the glucose uptake system [93]. As a result, insulin resistance leads to the disinhibition of lipolysis in humans [94]. If similar processes occur in polar bears, the use of fat as a metabolic fuel that Hobson et al. [11] observed may not represent the prevalent process, but instead, may have been temporary and triggered by the stress of capture [92].

Furthermore, certain foods that polar bears consume on land can complicate results of biochemical studies to distinguish ‘marine’ versus ‘terrestrial’ sources of expended energy using stable carbon isotopes (δ13C) [14,95,96]. For example, marine algae (Laminaria spp. and Fucus spp.), typical C4 plants that polar bears commonly consume from land, are more enriched with carbon and have higher δ13C values (-24 to -12‰) compared to most C3 (terrestrial) plants, although values range widely depending on plant part and time period sampled [14,95].

Similarly, waterfowl, such as snow geese, Canada geese (Branta canadensis) and common eiders, summering on land in western Hudson Bay can exhibit ‘marine’ signatures from foraging on plants and animals in brackish marshes and marine habitats [97,98]. Muscle δ13C values for the aforementioned and other seabirds that polar bears consume can range from (-22.0 to -15.5‰) [15,97,98], which clearly overlap δ13C values for ringed seal muscle (-19.4 to -18.1‰) [90,97] and could, therefore, lead to erroneous conclusions regarding the sources of energy used on land. Without specifically including these terrestrial foods (i.e., marine algae, birds) a priori in carbon isotope mixing models, their proportional contribution can not be accurately assessed [99], especially given the range of food combinations observed in the summer diet from scat analysis [21].

Earlier arriving bears may come ashore with greater nutritional deficits from lost seal hunting opportunities as the ice-free season expands [7] but calories necessary to prevent starvation will likely be available from land-based resources, such as caribou, snow geese and eggs. The projected earlier 60-day arrival would allow polar bears to overlap both the entire incubation and calving periods of snow geese and caribou, respectively, creating new phenological matches to compensate for the growing mismatch with seals. Using the same energy-saving, surprise hunting methods (e.g., ambush, stalk) to hunt geese and caribou that they typically use to capture seals [80,81], would provide polar bears energy compensation similar to the maximum values reported here. Until further behavioral and oxygen consumption studies are performed, however, the true costs associated with different foraging strategies and thus the total energy returns can only be approximated.

Acknowledgments

We thank K. Abraham, D. Hedman and V. Trim for providing information on caribou in the Churchill region.