ABSTRACT
Disuse osteoporosis results from physical inactivity. Reduced mechanical loading of bone stimulates bone resorption leading to bone loss, decreased mechanical properties, and increased fracture risk. Compensatory mechanisms evolved in hibernators to preserve skeletal muscle and bone during the prolonged physical inactivity that occurs during annual hibernation. This paper reports the preservation of bone properties in an exceptionally old black bear that was physically inactive for about 6 months annually for 31 years. The biological mechanisms that preserve bone during prolonged disuse during hibernation are also reviewed.
Subject(s)
Hibernation , Osteoporosis , Ursidae , Animals , Bone Density , Bone and Bones , Osteoporosis/prevention & controlABSTRACT
Ungulates are important to the diet of bears because they are high in protein, and the level of dietary protein strongly influences bear size. The size a bear obtains as an adult influences important life history characteristics, such as age of reproduction and reproductive success; therefore, it is important to know what foods are available to bears and how they are utilizing them. We tested hypotheses concerning the effect of age, sex, and location on black bear carnivory. We collected hair and vestigial premolar teeth from 49 Utah black bears, Ursus americanus according to the Utah Division of Wildlife Resources hunt unit. Hunt units differed in habitat quality and local ungulate density. We analyzed a vestigial premolar for the age of the bears and used analysis of the δ13C and δ15N values of the hairs of each bear to infer the degree of carnivory. δ15N of black bear hairs was positively correlated with increased availability of ungulates. There was a positive relationship between the δ15N of bear hairs and age in hunt units with the highest ungulate densities only. The δ15N and δ13C of black bear hairs were positively correlated, suggesting that bears are more carnivorous at higher altitudes. This study demonstrates the value of stable isotope analysis in understanding the feeding ecology of bears over broad geographic ranges. It demonstrates that ungulate availability is important to the feeding ecology of black bears in the Intermountain West.
Subject(s)
Carnivora , Ursidae , Animals , Carnivory , Diet , UtahABSTRACT
Periods of disuse or physical inactivity increases bone porosity and decreases bone mineral density, resulting in a loss of bone mechanical competence in many animals. Although large hibernators like bears and marmots prevent bone loss during hibernation, despite long periods of physical inactivity, some small hibernators do lose bone during hibernation. Little pocket mice (Perognathus longimembris) remain underground during winter hibernation and undergo bouts of torpor and interbout arousals, but the torpor bout duration is shorter than other rodent hibernators. Additionally, little pocket mice may enter torpor during summer estivation. In this study, cortical and trabecular bone architectural, mineral, and mechanical properties were analyzed for femurs from little pocket mice captured during 8 different months (March to October) to determine seasonal effects on bone. There were no differences in any bone properties between the pre-hibernation month of October and the post-hibernation month of March, suggesting winter hibernation did not adversely affect bone properties. However, cortical area was higher in March than April, May, and June. Bone mechanical and osteocyte lacunar properties were not different between any months. Trabecular bone in the distal femoral epiphysis showed no changes between months. The distal femoral metaphyseal region showed higher trabecular spacing and lower trabecular number in May than August, otherwise, there were no differences in trabecular parameters. The few monthly differences in bone properties may be due to physical inactivity from periodic summer estivation or from the timing of birth and growth in spring and summer months. Anat Rec, 300:2175-2183, 2017. © 2017 Wiley Periodicals, Inc.
Subject(s)
Bone Density/physiology , Femur/anatomy & histology , Femur/physiology , Hibernation/physiology , Osteogenesis/physiology , Seasons , Animals , Female , Male , MiceABSTRACT
Reduced skeletal loading typically results in decreased bone strength and increased fracture risk for humans and many other animals. Previous studies have shown bears are able to prevent bone loss during the disuse that occurs during hibernation. Studies with smaller hibernators, which arouse intermittently during hibernation, show that they may lose bone at the microstructural level. These small hibernators, like bats and squirrels, do not utilize intracortical remodeling. However, slightly larger mammals like marmots do. In this study we examined the effects of hibernation on bone structural, mineral, and mechanical properties in yellow-bellied marmots (Marmota flaviventris). This was done by comparing cortical bone properties in femurs and trabecular bone properties in tibias from marmots killed before hibernation (fall) and after hibernation (spring). Age data were not available for this study; however, based on femur length the post-hibernation marmots were larger than the pre-hibernation marmots. Thus, cross-sectional properties were normalized by allometric functions of bone length for comparisons between pre- and post-hibernation. Cortical thickness and normalized cortical area were higher in post-hibernation samples; no other normalized cross-sectional properties were different. No cortical bone microstructural loss was evident in osteocyte lacunar measurements, intracortical porosity, or intracortical remodeling cavity density. Osteocyte lacunar area, porosity, and density were surprisingly lower in post-hibernation samples. Trabecular bone volume fraction was not different between pre- and post-hibernation. Measures of both trabecular and cortical bone mineral content were higher in post-hibernation samples. Three-point bending failure load, failure energy, elastic energy, ultimate stress, and yield stress were all higher in post-hibernation samples. These results support the idea that, like bears, marmots are able to prevent disuse osteoporosis during hibernation, thus preventing increased fracture risk and promoting survival of the extreme environmental conditions that occur in hibernation.
Subject(s)
Bone and Bones/chemistry , Bone and Bones/physiology , Bone and Bones/ultrastructure , Hibernation/physiology , Marmota/anatomy & histology , Animals , Bone Density , Bone Remodeling/physiology , Humans , Marmota/physiology , Stress, Mechanical , Tensile StrengthABSTRACT
Disuse typically causes an imbalance in bone formation and bone resorption, leading to losses of cortical and trabecular bone. In contrast, bears maintain balanced intracortical remodeling and prevent cortical bone loss during disuse (hibernation). Trabecular bone, however, is more detrimentally affected than cortical bone in other animal models of disuse. Here we investigated the effects of hibernation on bone remodeling, architectural properties, and mineral density of grizzly bear (Ursus arctos horribilis) and black bear (Ursus americanus) trabecular bone in several skeletal locations. There were no differences in bone volume fraction or tissue mineral density between hibernating and active bears or between pre- and post-hibernation bears in the ilium, distal femur, or calcaneus. Though indices of cellular activity level (mineral apposition rate, osteoid thickness) decreased, trabecular bone resorption and formation indices remained balanced in hibernating grizzly bears. These data suggest that bears prevent bone loss during disuse by maintaining a balance between bone formation and bone resorption, which consequently preserves bone structure and strength. Further investigation of bone metabolism in hibernating bears may lead to the translation of mechanisms preventing disuse-induced bone loss in bears into novel treatments for osteoporosis.
Subject(s)
Bone Resorption/veterinary , Hibernation/physiology , Ursidae/physiology , Animals , Bone Density/physiology , Bone Resorption/diagnostic imaging , Bone Resorption/pathology , Bone Resorption/physiopathology , Female , Femur/diagnostic imaging , Femur/pathology , Femur/physiopathology , Male , Models, Biological , Motor Activity/physiology , Osteogenesis/physiology , Sheep , X-Ray MicrotomographyABSTRACT
Disuse typically uncouples bone formation from resorption, leading to bone loss which compromises bone mechanical properties and increases the risk of bone fracture. Previous studies suggest that bears can prevent bone loss during long periods of disuse (hibernation), but small sample sizes have limited the conclusions that can be drawn regarding the effects of hibernation on bone structure and strength in bears. Here we quantified the effects of hibernation on structural, mineral, and mechanical properties of black bear (Ursus americanus) cortical bone by studying femurs from large groups of male and female bears (with wide age ranges) killed during pre-hibernation (fall) and post-hibernation (spring) periods. Bone properties that are affected by body mass (e.g. bone geometrical properties) tended to be larger in male compared to female bears. There were no differences (p>0.226) in bone structure, mineral content, or mechanical properties between fall and spring bears. Bone geometrical properties differed by less than 5% and bone mechanical properties differed by less than 10% between fall and spring bears. Porosity (fall: 5.5+/-2.2%; spring: 4.8+/-1.6%) and ash fraction (fall: 0.694+/-0.011; spring: 0.696+/-0.010) also showed no change (p>0.304) between seasons. Statistical power was high (>72%) for these analyses. Furthermore, bone geometrical properties and ash fraction (a measure of mineral content) increased with age and porosity decreased with age. These results support the idea that bears possess a biological mechanism to prevent disuse and age-related osteoporoses.
Subject(s)
Hibernation/physiology , Ursidae/anatomy & histology , Ursidae/physiology , Aging/pathology , Aging/physiology , Animals , Awards and Prizes , Biomechanical Phenomena , Bone Density , Bone Remodeling/physiology , Female , Femur/anatomy & histology , Femur/physiology , Male , Societies, Scientific , Stress, Mechanical , Time FactorsABSTRACT
Disuse (i.e. inactivity) causes bone loss, and a recovery period that is 2-3 times longer than the inactive period is usually required to recover lost bone. However, black bears experience annual disuse (hibernation) and remobilization periods that are approximately equal in length, yet bears maintain or increase cortical bone material properties and whole bone mechanical properties with age. In this study, we investigated the architectural properties of bear femurs to determine whether cortical structure is preserved with age in bears. We showed that cross-sectional geometric properties increase with age, but porosity and resorption cavity density do not change with age in skeletally immature male and female bears. These findings suggest that structural properties substantially contribute to increasing whole bone strength with age in bears, particularly during skeletal maturation. Porosity was not different between skeletally immature and mature bears, and showed minimal regional variations between anatomical quadrants and radial positions that were similar in pattern and magnitude between skeletally immature and mature bears. We also found gender dimorphisms in bear cortical bone properties: females have smaller, less porous bones than males. Our results provide further support for the idea that black bears possess a biological mechanism to prevent disuse osteoporosis.