Charles T. Robbins's research while affiliated with Washington State University and other places
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Publications (163)
A male mutation bias is observed across vertebrates, and, where data are available, this bias is accompanied by increased per-generation mutation rates with parental age. While continuing mitotic cell division in the male germline post-puberty has been proposed as the major cellular mechanism underlying both patterns, little direct evidence for thi...
The eight species of bears world-wide consume a wide variety of diets. Some are specialists with extensive anatomical and physiological adaptations necessary to exploit specific foods or environments [e.g., polar bears ( Ursus maritimus ), giant pandas ( Ailuropoda melanoleuca ), and sloth bears ( Melursus ursinus )], while the rest are generalists...
Understanding how metabolic reprogramming happens in cells will aid the progress in the treatment of a variety of metabolic disorders. Brown bears undergo seasonal shifts in insulin sensitivity, including reversible insulin resistance in hibernation. We performed RNA-sequencing on brown bear adipocytes and proteomics on serum to identify changes po...
The brown bear (Ursus arctos) is the second largest and most widespread extant terrestrial carnivore on Earth and has recently emerged as a medical model for human metabolic diseases. Here, we report a fully phased chromosome-level assembly of a male North American brown bear built by combining Pacific Biosciences (PacBio) HiFi data and publicly av...
The brown bear ( Ursus arctos ) is the second largest and most widespread extant terrestrial carnivore on Earth and has recently emerged as a medical model for human metabolic diseases. Here, we report a fully-phased chromosome-level assembly of a male North American brown bear built by combining Pacific Biosciences (PacBio) HiFi data and publicly...
Hibernation in brown bears is an annual process involving multiple physiologically distinct seasons – hibernation, active, and hyperphagia. While recent studies have characterized broad patterns of differential gene regulation and isoform usage between hibernation and active seasons, patterns of gene and isoform expression during hyperphagia remain...
A male mutation bias is observed across vertebrates, and, where data are available, this bias is accompanied by increased per-generation mutation rates with parental age. While continuing mitotic cell division in the male germline post-puberty has been proposed as the major cellular mechanism underlying both patterns, little direct evidence for thi...
Obesity is among the most prevalent of health conditions in humans leading to a multitude of metabolic pathologies such as type 2 diabetes and hyperglycemia. However, there are many wild animals that have large seasonal cycles of fat accumulation and loss that do not result in the health consequences observed in obese humans. One example is the gri...
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 met...
Understanding hibernation in brown bears (Ursus arctos) can provide insight into some human diseases. During hibernation, brown bears experience periods of insulin resistance, physical inactivity, extreme bradycardia, obesity, and the absence of urine production. These states closely mimic aspects of human diseases such as type 2 diabetes, muscle a...
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 diet...
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:...
Understanding hibernation in brown bears ( Ursus arctos ) can provide insight into many human diseases. During hibernation, brown bears experience states of insulin resistance, physical inactivity, extreme bradycardia, obesity, and the absence of urine production. These states closely mimic human diseases such as type 2 diabetes, muscle atrophy, re...
Hibernation is characterized by depression of many physiological processes. To determine if this state is reversible in a non-food caching species, we fed hibernating grizzly bears (Ursus arctos horribilis) dextrose for 10 days to replace 53% or 100% of the estimated minimum daily energetic cost of hibernation. Feeding caused serum concentrations o...
Hair cortisol concentration (HCC) is being used increasingly to evaluate long‐term stress in many mammalian species. Most of the cortisol is assumed to passively diffuse from circulating blood into hair follicles and gradually accumulate in growing hair. However, our research with free‐ranging grizzly bears (Ursus arctos) suggests HCC increases sig...
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 ups...
Hibernation is characterized by suppression of many physiological processes. To determine if this state is reversible in a non-food caching species, we fed hibernating grizzly bears (Ursus arctos horribilis) glucose for 10 days to replace 53% or 100% of the estimated minimum daily energetic cost of hibernation. Feeding caused serum concentrations o...
1. Heat dissipation limit theory posits that energy available for growth and reproduction in endotherms is limited by their ability to dissipate heat. In mammals, endogenous heat production increases markedly during gestation and lactation, and thus female mammals may be subject to greater thermal constraints on energy expenditure than males. Such...
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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...
The purpose of this study was to investigate changes in expression of known cellular regulators of metabolism during hyperphagia (Sept) and hibernation (Jan) in skeletal muscle and adipose tissue of brown bears and determine whether signaling molecules and transcription factors known to respond to changes in cellular energy state are involved in th...
Revealing the mechanisms underlying the reversible physiology of hibernation could have applications to both human and animal health as hibernation is often associated with disease-like states. The present study uses RNA-sequencing to reveal the tissue and seasonal transcriptional changes occurring in grizzly bears (Ursus arctos horribilis). Compar...
There is growing interest in the ecological significance of phenological diversity, particularly in how spatially variable resource phenologies (i.e. resource waves) prolong foraging opportunities for mobile consumers. While there is accumulating evidence of consumers moving across landscapes to surf resource waves, there is little data quantifying...
Wildlife restoration programs depend on having animals that have evolved to handle the constraints, including disease, posed by the new environment. Grizzly bears (Ursus arctos horribilis) once thrived while feeding on salmon (Onchorhynchus spp.) and other foods in California, Oregon, Washington, and Idaho, USA. Unlike Canadian and Alaskan salmon,...
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...
Knowledge of density-dependent responses in grizzly bears is largely circumstantial yet critical to managing populations near carrying capacity. We studied grizzly bear (Ursus arctos) body condition and demographics in Denali National Park, Alaska, USA, 1991–1998, and compared our results with data from a nearby heavily hunted population to better...
Food sources for North America’s grizzly bear (Ursus arctos horribilis Ord, 1815) population have changed as habitats have fragmented, altering available resources and putting bears in contact with unnatural foods. Bears have evolved mechanisms to tolerate obesity, and do not develop adverse health consequences despite storing massive amounts of bo...
Significance
Climate change is altering the seasonal timing of biological events, effectively rescheduling the potential interactions among species. We know specialist consumers suffer when they fail to synchronize with their prey; however, little is known about how generalist consumers respond to phenological shifts across multiple food resources....
Adiponectin is the most abundant plasma adipokine, and is well known for its role in energy homeostasis and cardiac protection. In humans with dilated cardiomyopathy, myocardial adiponectin protein expression is reduced compared to normal hearts and has been implicated in the pathology of cardiomyopathy. Serum adiponectin levels are often conflicti...
Recognizing the potential value of steroid hormone measurements to augment non-invasive genetic sampling, we developed procedures based on enzyme-linked immunoassays to quantify reproductive steroid hormone concentrations in brown bear (Ursus arctos) hair. Then, using 94 hair samples collected from eight captive adult bears over a 2-year period, we...
Grizzly bears (Ursus arctos horribilis) have evolved remarkable metabolic adaptations including enormous fat accumulation during the active season followed by fasting during hibernation. However, these fluctuations in body mass do not cause the same harmful effects associated with obesity in humans. To better understand these seasonal transitions,...
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 ic...
The majority of terrestrial locomotion studies have focused on parasagittal motion and paid less attention to forces or movement in the frontal plane. Our previous research has shown that grizzly bears produce higher medial ground reaction forces (lateral pushing from the animal) than would be expected for an upright mammal, suggesting frontal plan...
Tri-axial accelerometers have been used to remotely identify the behaviors of a wide range of taxa. Assigning behaviors to accelerometer data often involves the use of captive animals or surrogate species, as accelerometer signatures are generally assumed to be similar to those of their wild counterparts. However, this has rarely been tested. Valid...
Recent studies suggest that bears have relatively high cognitive capabilities. However, cognitive processes and problem solving abilities remain relatively unexplored in bear species. We studied the capacity for eight captive brown bears (Ursus arctos) to move and use inanimate objects in order to obtain a food reward. We recorded their behaviors d...
Brown bears (Ursus arctos) exhibit hyperphagia each fall and can become obese in preparation for hibernation. They do this without displaying the physiological problems typically seen in obese humans, such as Type 2 diabetes and heart disease. The study of brown bear hibernation biology could therefore aid in the development of novel methods for co...
Background
Most biological functions are synchronized to the environmental light:dark cycle via a circadian timekeeping system. Bears exhibit shallow torpor combined with metabolic suppression during winter dormancy. We sought to confirm that free-running circadian rhythms of body temperature (Tb) and activity were expressed in torpid grizzly (brow...
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 co...
Training nonhuman animals in captivity for participation in routine husbandry procedures is believed to produce a lower stress environment compared with undergoing a general anesthetic event for the same procedure. This hypothesis rests largely on anecdotal evidence that the captive subjects appear more relaxed with the trained event. Blood markers...
The majority of locomotion studies have focused on parasagittal motion and all but ignored any forces or movement in the frontal plane. Our previous research has shown that grizzly bears produce higher medial ground reaction forces (lateral pushing from the animal) than would be expected for an upright mammal, suggesting frontal plane movement is a...
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...
Locomotion of plantigrade generalists has been relatively little studied compared to more specialised postures even though plantigrady is ancestral among quadrupeds. Bears (Ursidae) are a representative family for plantigrade carnivorans, they have the majority of the morphological characteristics identified for plantigrade species, and they have t...
Food habit studies are among the first steps used to understand wildlife-habitat relationships. However, these studies are in themselves insufficient to understand differences in population productivity and life histories, because they do not provide a direct measure of the energetic value or nutritional composition of the complete diet. Here, we d...
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...
This is a Forum article in response to: Barber-Meyer, S. (2015) Trophic cascades from wolves to grizzly bears or changing abundance of bears and alternate foods? Journal of Animal Ecology, 83, doi: 10.1111/1365-2656.12338. We used multiple data sets and study areas as well as several lines of evidence to investigate potential trophic linkages in Ye...
Mammalian hibernation has intrigued scientists due to extreme variations in normal seasonal physiological homeostasis. Numerous species manifest a hibernation phenotype although the characteristics of the hypometabolic state can be quite different. Ground squirrels (e.g., Sciuridae) are often considered the prototypical hibernator as individuals in...
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 (δ34S) and consumption of whitebark...
The confluence of obesity and diabetes as a worldwide epidemic necessitates the discovery of new therapies. Success in this endeavor requires translatable preclinical studies, which traditionally employ rodent models. As an alternative approach, we explored hibernation where obesity is a natural adaptation to survive months of fasting. Here we repo...
It is as yet unknown how large plantigrade quadrupeds move in their surroundings. Bears are the only group of such mammals in the world. However, they are relatively understudied in the areas of biomechanics and locomotion. This study represents one of the first to investigate the gait mechanics of grizzly bears (Ursus arctos horribilis). We used t...
Mercury obtained from the diet accumulates in mammalian hair as it grows thus preserving a record of mercury intake over the growth period of a given hair segment. We adapted a micro-analysis approach, using laser ablation inductively coupled plasma mass spectrometry, to characterize temporal changes in mercury exposure and uptake in wild and capti...
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's grizzly bears (Ursus arctos) and black bears (U. americanus). The cutthroat trout population has subsequently de...
Many animals consume mixed diets that maximize their fitness by optimizing macronutrient intake. We tested whether brown bears (Ursus arctos), generalist omnivores that hibernate, regulated their diet to a common nutrient target, achieved a nutrient target related to fitness, and selected a nutrient target that differed between seasons and from oth...
Bears are the only group of large, plantigrade, quadrupedal mammals in the world. However, they are relatively understudied in the areas of biomechanics and locomotion. This study represents one of the first to investigate the gaits mechanics used by grizzly bears (Ursus arctos horribilis). We used three high speed cameras and a custom built forcep...
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 be...
Brown bears give birth and nurture their young for the first 3-5 months while fasting in hibernation. During this period, bears use body reserves to support the energy and protein costs of reproduction. Limited reserves may restrict reproductive investment. We developed a model to assess the energetic costs of reproduction during hibernation and to...
abstract : Safe and effective immobilization of grizzly bears (Ursus arctos) is essential for research and management. Fast induction of anesthesia, maintenance of healthy vital rates, and predictable recoveries are priorities. From September 2010 to May 2012, we investigated these attributes in captive and wild grizzly bears anesthetized with a co...
Cognitive bias tasks purport to assess affective states via responses to ambiguous stimuli. We hypothesized that a novel cognitive bias task based on positive reinforcement using quantity differences would detect changes in affect in captive grizzly bears (Ursus arctos horribilis). We trained bears (n = 8) to respond differently (nose or paw touch)...
Grizzly bears (Ursus arctos) have been reported as either nocturnal or diurnal in various studies, but have not been known to switch between the 2 times unless disturbed by humans. Black bears (Ursus americanus) are almost solely diurnal in studies unless human influences occur. Because human disturbance is often difficult to control, the relative...
Many temperate zone animals adapt to seasonal changes by altering their physiology. This is mediated in large part by endocrine signals that encode day length and regulate energy balance and metabolism. The objectives of this study were to determine if the daily patterns of two important hormones, melatonin and cortisol, varied with day length in c...
We explored multiple linkages among grey wolves (Canis lupus), elk (Cervus elaphus), berry-producing shrubs and grizzly bears (Ursus arctos) in Yellowstone National Park. We hypothesized competition between elk and grizzly bears whereby, in the absence of wolves, increases in elk numbers would increase browsing on berry-producing shrubs and decreas...
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 tributari...
The proposed dietary pattern of extinct Late Pleistocene cave bears (Ursus spelaeus Rosenmüller, 1794) has become controversial, as some authors have suggested that they were strictly vegetarian, whereas others maintain they were omnivores that at times ate large amounts of animal protein. We evaluated these alternatives by compiling stable isotope...
The ecological role of large predators in North America continues to spark heated public debate. Although brown bears (Ursus arctos L., 1758) and the salmon (genus Oncorhynchus Suckley, 1861) they feed on have declined in many areas, the Kodiak archipelago is famous for large brown bears and abundant salmon. Salmon have generally been managed for m...
Grizzly bears (Ursus arctos) and American black bears (U. americanus) are sympatric in much of Yellowstone National Park. Three primary bear foods, cutthroat trout (Oncorhynchus clarki), whitebark pine (Pinus albicaulis) nuts, and elk (Cervus elaphus), have declined in recent years. Because park managers and the public are concerned about the impac...
Global warming has the potential to reduce arctic sea ice and thereby increase the length of summer fall fasting when polar bears (Ursus maritimus) lose access to most marine mammals. To evaluate the consequences of such changes, we compared the cost of fasting by polar bears with hibernation by brown bears (U. arctos), American black bears (U. ame...
Seasonal cycles of reproduction, migration and hibernation are often synchronized to changes in daylength (photoperiod). Ecological and evolutionary pressures have resulted in physiological specializations enabling animals to occupy a particular temporal niche within the diel cycle leading to characteristic activity patterns. In this study, we char...
Hibernating bears retain most of their skeletal muscle strength despite drastically reduced weight-bearing activity. Regular neural activation of muscles is a potential mechanism by which muscle atrophy could be limited. However, both mechanical loading and neural activity are usually necessary to maintain muscle size. An alternative mechanism is t...
The number, size, and survival of bear cubs emerging from winter dens depend on maternal condition prior to entering the den. We hypothesized that delayed implantation provides flexibility in timing of birth such that pregnant females are able to track environmental or body conditions long after conception to optimize reproductive output in a chang...