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Charles T. Robbins

Publications and source records attributed to Charles T. Robbins.

At least 19 recordsLinked to original sources

The effects of carnivory and herbivory on the energy balance of Arctic grizzly bears

Omnivores often face tradeoffs between selecting for spatially dispersed energy-dense vertebrate prey versus densely distributed herbivorous resources that have limited energetic value per unit intake. Arctic grizzly bears ( Ursus arctos ) are large omnivores within a resource-limited ecosystem that are known to exhibit smaller body masses and occur at lower densities than grizzly bears in other regions of North America. We evaluated the energy balance of Arctic grizzly bears during a portion of the fall hyperphagic period in two ecologically differing regions on Alaska’s northern Arctic coast by monitoring mass change, food intake, activity, and energy expenditure of 12 individuals over 17–22 days. Bears in coastal areas were more carnivorous than bears in the foothills that were predominantly herbivorous and frugivorous. Carnivory was associated with greater movement, body fat, and energy expenditure and two of four carnivorous bears lost mass. Overall, the mean body fat of the bears in this study was 34% lower than other grizzly bear populations in North America in the fall. Furthermore, the bears in this study exhibited relatively small changes in body mass (x̄ = 3%, range =−2 to 11%) that were 60% lower than other grizzly bear populations which typically gain substantial mass in the fall in preparation for denning. Our results, while representing a snapshot from a small number of bears during the fall hyperphagic period, are consistent with previous studies and indicate limited availability of energy-dense food resources during this time for grizzly bears in this region of the Arctic.

Alaska

Ursids evolved dietary diversity without major alterations in metabolic rates

The diets of the eight species of ursids range from carnivory (e.g., polar bears, Ursus maritimus ) to insectivory (e.g., sloth bears, Melursus ursinus ), omnivory (e.g., brown bears, U. arctos ), and herbivory (e.g., giant pandas, Ailuropoda melanoleuca ). Dietary energy availability ranges from the high-fat, highly digestible, calorically dense diet of polar bears (~ 6.4 kcal digestible energy/g fresh weight) to the high-fiber, poorly digestible, calorically restricted diet (~ 0.7) of giant pandas. Thus, ursids provide the opportunity to examine the extent to which dietary energy drives evolution of energy metabolism in a closely related group of animals. We measured the daily energy expenditure (DEE) of captive brown bears in a relatively large, zoo-type enclosure and compared those values to previously published results on captive brown bears, captive and free-ranging polar bears, and captive and free-ranging giant pandas. We found that all three species have similar mass-specific DEE when travel distances and energy intake are normalized even though their diets differ dramatically and phylogenetic lineages are separated by millions of years. For giant pandas, the ability to engage in low-cost stationary foraging relative to more wide-ranging bears likely provided the necessary energy savings to become bamboo specialists without greatly altering their metabolic rate.

Scientific Reports

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.

Manitoba

New insights into dietary management of polar bears (Ursus maritimus) and brown bears (U. arctos)

Although polar bears ( Ursus maritimus ) and brown bears ( U. arctos ) have been exhibited in zoological gardens for centuries, little is known about their nutritional needs. Multiple recent studies on both wild and captive polar bears and brown bears have found that they voluntarily select dietary macronutrient proportions resulting in much lower dietary protein and higher fat or digestible carbohydrate concentrations than are currently fed in most zoos. These lower protein concentrations selected by both species maximized growth rates and efficiencies of energy utilization in brown bears and may play a role in reducing kidney, liver, and cardiovascular diseases in both species. Therefore, we propose the need for the development of new dietary regimens for both species in managed care that better reflect their macronutrient needs. We developed a new kibble that is higher in fat and lower in protein than typical diets that have been fed in managed care, has a fatty acid profile more consistent with wild bear diets, and has been readily consumed by both brown bears and polar bears. The kibble can be fed as the sole diet or as part of more complex diets with additional fruits, meats, or vegetables. Because many nutritional deficiencies and related diseases can take months or years to appear, we urge caution and continued long-term monitoring of bears and their diets to ensure their optimal health.

Zoo Biology

Fatty acid profiles of feeding and fasting bears: Estimating calibration coefficients, the timeframe of diet estimates, and selective mobilization during hibernation

Accurate information on diet composition is central to understanding and conserving carnivore populations. Quantitative fatty acid signature analysis (QFASA) has emerged as a powerful tool for estimating the diets of predators, but ambiguities remain about the timeframe of QFASA estimates and the need to account for species-specific patterns of metabolism. We conducted a series of feeding experiments with four juvenile male brown bears ( Ursus arctos ) to (1) track the timing of changes in adipose tissue composition and QFASA diet estimates in response to a change in diet and (2) quantify the relationship between consumer and diet FA composition (i.e., determine “calibration coefficients”). Bears were fed three compositionally distinct diets for 90–120 days each. Two marine-based diets were intended to approximate the lipid content and composition of the wild diet of polar bears ( U. maritimus ). Bear adipose tissue composition changed quickly in the direction of the diet and showed evidence of stabilization after 60 days. During hibernation, FA profiles were initially stable but diet estimates after 10 weeks were sensitive to calibration coefficients. Calibration coefficients derived from the marine-based diets were broadly similar to each other and to published values from marine-fed mink ( Mustela vison ), which have been used as a model for free-ranging polar bears. For growing bears on a high-fat diet, the temporal window for QFASA estimates was 30–90 days. Although our results reinforce the importance of accurate calibration, the similarities across taxa and diets suggest it may be feasible to develop a generalized QFASA approach for mammalian carnivores.

Journal of Comparative Physiology B: Biochemical,

Energetic and health effects of protein overconsumption constrain dietary adaptation in an apex predator

Studies of predator feeding ecology commonly focus on energy intake. However, captive predators have been documented to selectively feed to optimize macronutrient intake. As many apex predators experience environmental changes that affect prey availability, limitations on selective feeding can affect energetics and health. We estimated the protein:fat ratio of diets consumed by wild polar bears using a novel isotope-based approach, measured protein:fat ratios selected by zoo polar bears offered dietary choice and examined potential energetic and health consequences of overconsuming protein. Dietary protein levels selected by wild and zoo polar bears were low and similar to selection observed in omnivorous brown bears, which reduced energy intake requirements by 70% compared with lean meat diets. Higher-protein diets fed to zoo polar bears during normal care were concurrent with high rates of mortality from kidney disease and liver cancer. Our results suggest that polar bears have low protein requirements and that limitations on selective consumption of marine mammal blubber consequent to climate change could meaningfully increase their energetic costs. Although bear protein requirements appear lower than those of other carnivores, the energetic and health consequences of protein overconsumption identified in this study have the potential to affect a wide range of taxa.

Scientific Reports

Quantifying energetic costs and defining energy landscapes experienced by grizzly bears

Animal movements are major determinants of energy expenditure and ultimately the cost–benefit of landscape use. Thus, we sought to understand those costs and how grizzly bears ( Ursus arctos ) move in mountainous landscapes. We trained captive grizzly bears to walk on a horizontal treadmill and up and down 10% and 20% slopes. The cost of moving upslope increased linearly with speed and slope angle, and this was more costly than moving horizontally. The cost of downslope travel at slower speeds was greater than the cost of traveling horizontally but appeared to decrease at higher speeds. The most efficient walking speed that minimized cost per unit distance was 1.19±0.11 m s −1 . However, grizzly bears fitted with GPS collars in the Greater Yellowstone Ecosystem moved at an average velocity of 0.61±0.28 m s −1 and preferred to travel on near-horizontal slopes at twice their occurrence. When traveling uphill or downhill, grizzly bears chose paths across all slopes that were ∼54% less steep and costly than the maximum available slope. The net costs (J kg −1 m −1 ) of moving horizontally and uphill were the same for grizzly bears, humans and digitigrade carnivores, but those costs were 46% higher than movement costs for ungulates. These movement costs and characteristics of landscape use determined using captive and wild grizzly bears were used to understand the strategies that grizzly bears use for preying on large ungulates and the similarities in travel between people and grizzly bears that might affect the risk of encountering each other on shared landscapes.

Wyoming

The clock keeps ticking: Circadian rhythms of free-ranging polar bears

Life in the Arctic presents organisms with multiple challenges, including extreme photic conditions, cold temperatures, and annual loss and daily movement of sea ice. Polar bears ( Ursus maritimus ) evolved under these unique conditions, where they rely on ice to hunt their main prey, seals. However, very little is known about the dynamics of their daily and seasonal activity patterns. For many organisms, activity is synchronized (entrained) to the earth’s day/night cycle, in part via an endogenous (circadian) timekeeping mechanism. The present study used collar-mounted accelerometer and global positioning system data from 122 female polar bears in the Chukchi and Southern Beaufort Seas collected over an 8-year period to characterize activity patterns over the calendar year and to determine if circadian rhythms are expressed under the constant conditions found in the Arctic. We reveal that the majority of polar bears (80%) exhibited rhythmic activity for the duration of their recordings. Collectively within the rhythmic bear cohort, circadian rhythms were detected during periods of constant daylight (June-August; 24.40 ± 1.39 h, mean ± SD) and constant darkness (23.89 ± 1.72 h). Exclusive of denning periods (November-April), the time of peak activity remained relatively stable (acrophases: ~1200-1400 h) for most of the year, suggesting either entrainment or masking. However, activity patterns shifted during the spring feeding and seal pupping season, as evidenced by an acrophase inversion to ~2400 h in April, followed by highly variable timing of activity across bears in May. Intriguingly, despite the dynamic environmental photoperiodic conditions, unpredictable daily timing of prey availability, and high between-animal variability, the average duration of activity (alpha) remained stable (11.2 ± 2.9 h) for most of the year. Together, these results reveal a high degree of behavioral plasticity in polar bears while also retaining circadian rhythmicity. Whether this degree of plasticity will benefit polar bears faced with a loss of sea ice remains to be determined.

Alaska

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.

Journal of Experimental Biology

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.

Oecologia

Isotopic incorporation and the effects of fasting and dietary lipid content on isotopic discrimination in large carnivorous mammals

There has been considerable emphasis on understanding isotopic discrimination for diet estimation in omnivores. However, discrimination may differ for carnivores, particularly species that consume lipid-rich diets. Here, we examined the potential implications of several factors when using stable isotopes to estimate the diets of bears, which can consume lipid-rich diets and, alternatively, fast for weeks to months. We conducted feeding trials with captive brown bears ( Ursus arctos ) and polar bears ( Ursus maritimus ). As dietary lipid content increased to ∼90%, we observed increasing differences between blood plasma and diets that had not been lipid extracted (∆ 13 C tissue-bulk diet ) and slightly decreasing differences between plasma δ 13 C and lipid-extracted diet. Plasma Δ 15 N tissue-bulk diet increased with increasing protein content for the four polar bears in this study and data for other mammals from previous studies that were fed purely carnivorous diets. Four adult and four yearling brown bears that fasted 120 d had plasma δ 15 N values that changed by <±2‰. Fasting bears exhibited no trend in plasma δ 13 C. Isotopic incorporation in red blood cells and whole blood was ≥6 mo in subadult and adult bears, which is considerably longer than previously measured in younger and smaller black bears ( Ursus americanus ). Our results suggest that short-term fasting in carnivores has minimal effects on δ 13 C and δ 15 N discrimination between predators and their prey but that dietary lipid content is an important factor directly affecting δ 13 C discrimination and indirectly affecting δ 15 N discrimination via the inverse relationship with dietary protein content.

Physiological and Biochemical Zoology

Can polar bears use terrestrial foods to offset lost ice-based hunting opportunities?

Increased land use by polar bears ( Ursus maritimus ) due to climate-change-induced reduction of their sea-ice habitat illustrates the impact of climate change on species distributions and the difficulty of conserving a large, highly specialized carnivore in the face of this global threat. Some authors have suggested that terrestrial food consumption by polar bears will help them withstand sea-ice loss as they are forced to spend increasing amounts of time on land. Here, we evaluate the nutritional needs of polar bears as well as the physiological and environmental constraints that shape their use of terrestrial ecosystems. Only small numbers of polar bears have been documented consuming terrestrial foods even in modest quantities. Over much of the polar bear's range, limited terrestrial food availability supports only low densities of much smaller, resident brown bears ( Ursus arctos ), which use low-quality resources more efficiently and may compete with polar bears in these areas. Where consumption of terrestrial foods has been documented, polar bear body condition and survival rates have declined even as land use has increased. Thus far, observed consumption of terrestrial food by polar bears has been insufficient to offset lost ice-based hunting opportunities but can have ecological consequences for other species. Warming-induced loss of sea ice remains the primary threat faced by polar bears.

Frontiers in Ecology and the Environment

Validation of mercury tip-switch and accelerometer activity sensors for identifying resting and active behavior in bears

Activity sensors are often included in wildlife transmitters and can provide information on the behavior and activity patterns of animals remotely. However, interpreting activity-sensor data relative to animal behavior can be difficult if animals cannot be continuously observed. In this study, we examined the performance of a mercury tip-switch and a tri-axial accelerometer housed in collars to determine whether sensor data can be accurately classified as resting and active behaviors and whether data are comparable for the 2 sensor types. Five captive bears (3 polar [ Ursus maritimus ] and 2 brown [ U. arctos horribilis ]) were fitted with a collar specially designed to internally house the sensors. The bears&rsquo; behaviors were recorded, classified, and then compared with sensor readings. A separate tri-axial accelerometer that sampled continuously at a higher frequency and provided raw acceleration values from 3 axes was also mounted on the collar to compare with the lower resolution sensors. Both accelerometers more accurately identified resting and active behaviors at time intervals ranging from 1 minute to 1 hour (&ge;91.1% accuracy) compared with the mercury tip-switch (range = 75.5&ndash;86.3%). However, mercury tip-switch accuracy improved when sampled at longer intervals (e.g., 30&ndash;60 min). Data from the lower resolution accelerometer, but not the mercury tip-switch, accurately predicted the percentage of time spent resting during an hour. Although the number of bears available for this study was small, our results suggest that these activity sensors can remotely identify resting versus active behaviors across most time intervals. We recommend that investigators consider both study objectives and the variation in accuracy of classifying resting and active behaviors reported here when determining sampling interval.

Ursus

Contrasting past and current numbers of bears visiting Yellowstone cutthroat trout streams

Spawning cutthroat trout ( Oncorhynchus clarkii bouvieri ) were historically abundant within tributary streams of Yellowstone Lake within Yellowstone National Park and were a highly digestible source of energy and protein for Yellowstone&rsquo;s grizzly bears ( Ursus arctos ) and black bears ( U. americanus ). The cutthroat trout population has subsequently declined since the introduction of non-native lake trout (Salvelinus namaycush), and in response to effects of drought and whirling disease ( Myxobolus cerebralis ). The trout population, duration of spawning runs, and indices of bear use of spawning streams had declined in some regions of the lake by 1997&ndash;2000. We initiated a 3-year study in 2007 to assess whether numbers of spawning fish, black bears, and grizzly bears within and alongside stream corridors had changed since 1997&ndash; 2000. We estimated numbers of grizzly bears and black bears by first compiling encounter histories of individual bears visiting 48 hair-snag sites along 35 historically fished streams.We analyzed DNA encounter histories with Pradel-recruitment and Jolly-Seber (POPAN) capture-mark-recapture models. When compared to 1997&ndash;2000, the current number of spawning cutthroat trout per stream and the number of streams with cutthroat trout has decreased. We estimated that 48 (95% CI&frac14;42&ndash;56) male and 23 (95% CI&frac14;21&ndash;27) female grizzly bears visited the historically fished tributary streams during our study. In any 1- year, 46 to 59 independent grizzly bears (8&ndash;10% of estimated Greater Yellowstone Ecosystem population) visited these streams. When compared with estimates from the 1997 to 2000 study and adjusted for equal effort, the number of grizzly bears using the stream corridors decreased by 63%. Additionally, the number of black bears decreased between 64% and 84%. We also document an increased proportion of bears of both species visiting front-country (i.e., near human development) streams. With the recovery of cutthroat trout, we suggest bears that still reside within the Lake basin will readily use this high-quality food resource.

Journal of Wildlife Management

Use of isotopic sulfur to determine whitebark pine consumption by Yellowstone bears: a reassessment

Use of naturally occurring stable isotopes to estimate assimilated diet of bears is one of the single greatest breakthroughs in nutritional ecology during the past 20 years. Previous research in the Greater Yellowstone Ecosystem (GYE), USA, established a positive relationship between the stable isotope of sulfur (&delta; 34 S) and consumption of whitebark pine (Pinus albicaulis) seeds. That work combined a limited sample of hair, blood clots, and serum. Here we use a much larger sample to reassess those findings. We contrasted &delta; 34 S values in spring hair and serum with abundance of seeds of whitebark pine in samples collected from grizzly (Ursus arctos) and American black bears (U. americanus) in the GYE during 2000&ndash;2010. Although we found a positive relationship between &delta; 34 S values in spring hair and pine seed abundance for grizzly bears, the coefficients of determination were small ( R 2 &thinsp;&le;&thinsp;0.097); we failed to find a similar relationship with black bears. Values of &delta; 34 S in spring hair were larger in black bears and &delta; 34 S values in serum of grizzly bears were lowest in September and October, a time when we expect &delta; 34 S to peak if whitebark pine seeds were the sole source of high &delta; 34 S. The relationship between &delta; 34 S in bear tissue and the consumption of whitebark pine seeds, as originally reported, may not be as clean a method as proposed. Data we present here suggest other foods have high values of &delta; 34 S, and there is spatial heterogeneity affecting the &delta; 34 S values in whitebark pine, which must be addressed.

Yellowstone National Park

Body and diet composition of sympatric black and grizzly bears in the Greater Yellowstone Ecosystem

The Greater Yellowstone Ecosystem (GYE) has experienced changes in the distribution and availability of grizzly bear (Ursus arctos) food resources in recent decades. The decline of ungulates, fish, and whitebark pine seeds (Pinus albicaulis) has prompted questions regarding their ability to adapt. We examined body composition and diet of grizzly bears using bioelectrical impedance and stable isotopes to determine if 1) we can detect a change in diet quality associated with the decline in either ungulates or whitebark pine, and 2) the combined decline in ungulates, fish, and pine seeds resulted in a change in grizzly bear carrying capacity in the GYE. We contrasted body fat and mass in grizzly bears with a potential competitor, the American black bear (Ursus americanus), to address these questions. Grizzly bears assimilated more meat into their diet and were in better body condition than black bears throughout the study period, indicating the decline in ungulate resources did not affect grizzly bears more than black bears. We also found no difference in autumn fat levels in grizzly bears in years of good or poor pine seed production, and stable isotope analyses revealed this was primarily a function of switching to meat resources during poor seed-producing years. This dietary plasticity was consistent over the course of our study. We did not detect an overall downward trend in either body mass or the fraction of meat assimilated into the diet by grizzly bears over the past decade, but we did detect a downward trend in percent body fat in adult female grizzly bears after 2006. Whether this decline is an artifact of small sample size or due to the population reaching the ecological carrying capacity of the Yellowstone ecosystem warrants further investigation.

Idaho, Montana, Wyoming

Grizzly bear predation links the loss of native trout to the demography of migratory elk in Yellowstone

The loss of aquatic subsidies such as spawning salmonids is known to threaten a number of terrestrial predators, but the effects on alternative prey species are poorly understood. At the heart of the Greater Yellowstone ecosystem, an invasion of lake trout has driven a dramatic decline of native cutthroat trout that migrate up the shallow tributaries of Yellowstone Lake to spawn each spring. We explore whether this decline has amplified the effect of a generalist consumer, the grizzly bear, on populations of migratory elk that summer inside Yellowstone National Park (YNP). Recent studies of bear diets and elk populations indicate that the decline in cutthroat trout has contributed to increased predation by grizzly bears on the calves of migratory elk. Additionally, a demographic model that incorporates the increase in predation suggests that the magnitude of this diet shift has been sufficient to reduce elk calf recruitment (4&ndash;16%) and population growth (2&ndash;11%). The disruption of this aquatic&ndash;terrestrial linkage could permanently alter native species interactions in YNP. Although many recent ecological changes in YNP have been attributed to the recovery of large carnivores&mdash;particularly wolves&mdash;our work highlights a growing role of human impacts on the foraging behaviour of grizzly bears.

Yellowstone National Park