A radiographic and histologic study of bone in the active and hibernating bat (Myotis lucifugus)

Abstract

A radiographic and histologic study of bat bones showed that there is a progressive loss of bone tissue during hibernation and abrupt reversal at arousal. Enhanced osteolysis accounted for the bone loss; osteoclasia was not observed.Increasing evidence strongly indicates that the parafollicular cells (light cells, C cells) of the thyroid gland synthesize calcitonin, the bone resorption inhibiting hormone (Pearse, '66; Matsuzawa and Kurosumi, '67; Ericson, '68). Although the importance of calcitonin in mammalian physiology is still enigmatic (Hirsch and Munson, '69), strong evidence that calcitonin may be physiologically important in the hibernator has been found. Parafollicular cells are sparse in the thyroid glands of most mammals (Stux, Thompson, Isler and Leblond, '63; Young, Duncan and Care, '68; Klinck, Oertel and Winship, '70), but they are widespread and abundant in the thyroid glands of hibernators (Azzali, '66; Azzali, '67; Nunez, Gould, Hamilton, Hayward and Holt, '67; Pearse and Welsch, '68; Gabe and Martoja, '69; Olivereau, '70).In the bat, parafollicular cells show rather striking seasonal variations in fine structure. During the first half of hibernation, the amount of granular endoplasmic reticulum is greatly reduced and the calcitonin-secretion granules lose their solid dense core (Nunez et al., '67; Nunez, Gould and Holt, '70) suggesting that calcitonin may be functionally inactive during the hibernation period. Cessation of calcitonin secretion during hibernation should result in increased bone resorption. However, the few reports on bone changes in hibernation are incomplete and conflict (Mayer and Bernick, '63; Bruce and Wiebers, '69). Therefore, in an effort to determine the effects of hibernation on ANAT. REC., 172: 97-108.bone and the mechanisms involved, and to establish possible interrelationships between bone changes and parafollicular cell activity, a histologic and radiographic study of the femur of active, prehibernating and hibernating bats was carried out. The results of the study are reported herein. MATERIAL AND METHODSThe bats used in this study were adult 'Myotis lucifugus, were of either sex, and were obtained from caves in Central Illinois before (September), during (November, December, January, and February) and after hibernation (late April) and are illustrated in figure 1. Bones were dissected and cleaned of soft tissues and pIaced in 10% fonnalin until they were radiographed and processed for histological examination.The bones were radiographed in a Faxitron 804 self-contained unit having a tungsten target and a 40 mil. Beryllium window. The nominal focal spot size was 0.5 mm. The tube was operated at 10 K.V.P., 3 MA, for exposure times of three minutes at a 24" focus-film distance. Kodak RPM film (having a speed value, grain size and contrast characteristics between industrial type M and industrial type A film) was used and processed through a medical X-Omat using a 90 second cycle. The radiographs were examined by light microscopy and were photographed a...

Effect of aestivation on long bone mechanical properties in the green-striped burrowing frog,Cyclorana alboguttata

“…This contrasts with both clinical systems of unloading and, more intriguingly, with the other natural disuse systems examined to date (hibernating mammals) in which bone remodelling is evident. For example, bone loss has been described in hibernating bats (Myotis lucifugus; Whalen et al, 1971), ground squirrels (Spermophilus undulatus; Mayer and Bernick, 1959) and hamsters (Cricetus cricetus; Kayser and Frank, 1963). In bats, much of the bone loss has been attributed to enhanced osteolysis (Whalen et al, 1971).…”

“…Although overall locomotor performance has never been measured in a hibernator, it is likely to parallel the deficit in isolated muscle performance and thereby reduce the demands on the skeletal system until the muscle regains its prehibernation performance. Hibernation also induces loss of bone in bats (Whalen et al, 1971), hamsters (Kayser and Frank 1963) and squirrels (Mayer and Bernick, 1959). In light of the empirically determined difference in muscle performance between emerging hibernators and aestivators, it seems possible that, in contrast to hibernators, aestivating frogs may preserve long bone size and strength in order to withstand the forces associated with jumping upon emergence.…”

“…The mechanical data were supplemented by histological analysis to assess osteocyte activity, as it is known that in hibernating bats osteocytic osteolysis accounts for much of the associated bone loss (Whalen et al, 1971).…”

“…The green-striped burrowing frog, Cyclorana alboguttata, survives droughts through the excavation of an underground chamber, the formation of a waterproof cocoon and the storage of water in the bladder (Flanigan et al, 1993;Withers, 1993). The inactivity of hibernation is known to be correlated with decreases in bone size and strength (Doty and Nunez, 1985;Whalen et al, 1971) although the response varies between species. However, whether aestivation also induces such changes in bone properties is unknown.…”

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

“…It is feasible that the metabolic depression and associated metabolic recycling that is fundamental to dormancy may help defend skeletal tissues from the effects of disuse. Early studies suggested that small hibernating mammals such as bats, ground squirrels and hamsters might experience bone loss during hibernation (Kayser and Frank, 1963;Mayer and Bernick, 1959;Whalen et al, 1972). However, more recent data from hibernating S. lateralis squirrels indicate that bone strength and stiffness are unaffected by winter inactivity (Utz et al, 2009).…”