Yellow-bellied Marmots (Marmota flaviventris) preserve bone strength and microstructure during hibernation

Abstract

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.

Effects of hibernation on bone marrow transcriptome in thirteen-lined ground squirrels

“…Hibernators face the risk of losing bone strength during prolonged periods of inactivity. Recent studies in thirteen-lined and golden-mantled ground squirrels, marmots, and woodchucks have shown that some microstructural bone loss occurs during hibernation but macrostructural strength is maintained (24,55,92,100). During hibernation, the osteocyte lacunar porosity increases, indicating a decrease in cell number.…”

Prevention of muscle wasting and osteoporosis: the value of examining novel animal models

“…This applies to many species, such as bears, squirrels, woodchucks, bats, hamsters, prairie dogs and marmots (Cotton, 2016;Cotton and Harlow, 2010;Doherty et al, 2012;James et al, 2011;McGee-Lawrence et al, 2015Utz et al, 2009;Wojda et al, 2012). However, some small hibernators, such as the 13-lined ground squirrel (Ictidomys tridecemlineatus) have been reported to exhibit microstructural bone loss (osteocytic osteolysis) during hibernation bouts, which has not been observed in larger hibernating animals (McGeeLawrence et al, 2011).…”

“…Although these studies lacked thorough quantification of a wide array of bone properties, for small mammalian hibernators there is still conflicting evidence as to whether bone loss regularly occurs during dormancy. Whereas both arctic and golden-mantled ground squirrels retain cortical bone properties and strength following hibernation (Utz et al, 2009;Wojda et al, 2012), data indicate that hibernating I. tridecemlineatus might be unable to avoid microstructural losses of cortical and trabecular bone (McGee-Lawrence et al, 2011). Nevertheless, because bone geometrical and mechanical properties do not differ significantly between hibernating and active squirrels, these animals can still perhaps activate the appropriate physiological mechanisms to maintain bone macrostructure and strength throughout hibernation in preparation for normal skeletal function during arousal.…”

Exploring the Bone Proteome to Help Explain Altered Bone Remodeling and Preservation of Bone Architecture and Strength in Hibernating Marmots

“…Like bears, marmots do not lose bone mass and strength during hibernation periods lasting 5-6 mo (Wojda et al 2012). Marmots decrease their basal metabolic rate during hibernation to 5.5% of the levels observed during periods of physical activity (Hock 1969).…”

“…Animals that hibernate (e.g., marmots and bears) are naturally physically inactive for extended periods (6 mo or longer) annually. However, bears, marmots, woodchucks, and ground squirrels maintain bone properties, despite these long bouts of physical inactivity (McGee et al 2007bMcGee-Lawrence et al 2009aUtz et al 2009;Doherty et al 2012;Wojda et al 2012). Hibernating mammals demonstrate remarkable resilience by having evolved physiological mechanisms that allow them to survive extreme physiological and environmental conditions for prolonged periods of time (Carey et al 2003).…”