Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator

Buck, C. Loren; Barnes, Brian M.

doi:10.1152/ajpregu.2000.279.1.r255

Cited by 243 publications

(272 citation statements)

References 49 publications

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“…It has been suggested that, similar to ground squirrels hibernating in freezing conditions (6), hibernating bears primarily use fat as a source of energy (27), and this is supported by our observed respiratory quotient values near 0.7. We detected no coordinated transcriptional changes for genes involved in lipid catabolism, however, although this may be due to a limited representation of lipid metabolism genes on the array.…”

Section: Differential Gene Expression In Hibernating Black Bearssupporting

confidence: 84%

Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus)

Fedorov

Goropashnaya

Tøien

et al. 2009

Physiological Genomics

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125

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We conducted a large-scale gene expression screen using the 3,200 cDNA probe microarray developed specifically for Ursus americanus to detect expression differences in liver and skeletal muscle that occur during winter hibernation compared with animals sampled during summer. The expression of 12 genes, including RNA binding protein motif 3 (Rbm3), that are mostly involved in protein biosynthesis, was induced during hibernation in both liver and muscle. The Gene Ontology and Gene Set Enrichment analysis consistently showed a highly significant enrichment of the protein biosynthesis category by overexpressed genes in both liver and skeletal muscle during hibernation. Coordinated induction in transcriptional level of genes involved in protein biosynthesis is a distinctive feature of the transcriptome in hibernating black bears. This finding implies induction of translation and suggests an adaptive mechanism that contributes to a unique ability to reduce muscle atrophy over prolonged periods of immobility during hibernation. Comparing expression profiles in bears to small mammalian hibernators shows a general trend during hibernation of transcriptional changes that include induction of genes involved in lipid metabolism and carbohydrate synthesis as well as depression of genes involved in the urea cycle and detoxification function in liver. gene expression; hibernation; translation; RNA binding protein motif 3 MAMMALIAN HIBERNATION IS a physiological and behavioral adaptation involving a coordinated suppression of heat production and body temperature wherein whole body metabolism and energy demand are significantly reduced over several days to several months. During hibernation, heart and respiration rates, blood flow, and oxygen consumption decrease dramatically to Ͻ10% of normal or basal rates (2, 4). These physiological changes do not represent a loss of homeostasis but instead are precisely controlled and spontaneously reversible, and they allow individual animals to survive highly seasonal or unpredictable environments where food availability becomes lacking (7, 12). The molecular and genetic basis of hibernation in small mammals has only recently begun to be described, and little is known about its evolutionary history. Hibernating species have been found in diverse families among seven orders of mammals (26), however, and the interspersed phylogenetic distribution of hibernating and nonhibernating species has led to the hypothesis that rather than requiring the creation of novel gene products, hibernation results from the differential expression of genes that exist widely among mammals (35).Microarray technology provides powerful means for the unbiased detection of differences in expression of thousands of genes in a single hybridization experiment (14). In contrast to single-gene expression analysis, the genome-wide approach also allows for identification of coordinated transcriptional changes in functional groups of regulatory genes within metabolic and signaling pathways. Recent studies of differential gen...

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Section: Differential Gene Expression In Hibernating Black Bearssupporting

confidence: 84%

Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus)

Fedorov

Goropashnaya

Tøien

et al. 2009

Physiological Genomics

Self Cite

125

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“…This is also accompanied by a progressive reduction in thermal sensitivity (Q 10 ) from summer to winter such that the metabolic rate of dormant lizards becomes relatively temperature independent (Abe 1983(Abe , 1993(Abe , 1995de Souza et al 2004). This suggests that metabolism is suppressed to the same minimum level in winter, regardless of the temperature, an observation that has also been made on some species of hibernating mammals (echidna: Nicol et al 1992; arctic ground squirrel: Buck and Barnes 2000;marmot: Ortmann and Heldmaier 2000). This has been proposed to have the selective advantage of maintaining extremely low metabolic rates even when burrow temperatures rise slightly.…”

Section: Perspectivementioning

confidence: 66%

Seasonal Changes in Daily Metabolic Patterns of Tegu Lizards (Tupinambis merianae) Placed in the Cold (17°C) and Dark

Milsom

Andrade²,

Brito³

et al. 2008

Physiological and Biochemical Zoology

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. ABSTRACTOxygen consumption rate was measured continuously in young tegu lizards Tupinambis merianae exposed to 4 d at 25ЊC followed by 7-10 d at 17ЊC in constant dark at five different times of the year. Under these conditions, circadian rhythms in the rate of oxygen consumption persisted for anywhere from 1 d to the entire 2 wk in different individuals in all seasons except the winter. We also saw a progressive decline in standard oxygen consumption rate (at highly variable rates in different individuals) to a very low rate that was seasonally independent (ranging from to mL kg Ϫ1 h Ϫ1 across seasons). 19.1 ‫ע‬ 6.2 27.7 ‫ע‬ 0.2 Although this degree of reduction appeared to take longer to invoke when starting from higher metabolic rates, tegu lizards reduced their metabolism to the low rates seen in winter dormancy at all times of the year when given sufficient time in the cold and dark. In the spring and summer, tegus reduced their standard metabolic rate (SMR) by 80%-90% over the experimental run, but only roughly 20%-30% of the total fall was due to the reduction in temperature; 70%-80% of the total fall occurred at constant temperature. By autumn, when the starting SMR on the first night at 25ЊC was already reduced by 59%-81% (early and late autumn, respectively) from peak summer values, virtually all of the fall (63%-83%) in metabolism was due to the reduction in temperature. This suggests that the temperature-independent reduction of metabolism was already in place by autumn before the tegus had entered winter dormancy.

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“…Minimum body temperature, in turn, determines many physiological and behavioral parameters, including torpor bout length (Buck and Barnes, 2000), neural activity during torpor (Krilowicz et al, 1988), and electroencephalographic (EEG) power spectrum on return to euthermia (Larkin and Heller, 1996). However, it was previously unknown whether ambient temperature also influences the extent of neural plasticity during torpor.…”

Section: Neural Microstructure Retracts Linearly With Minimum Torpor mentioning

confidence: 99%

“…During torpor, both core and brain temperatures drop to within 0.5Ϫ3°C of ambient temperature (Strumwasser, 1959), often reaching near-freezing and even below-freezing temperatures in the wild (Barnes, 1989). Concomitant with this periodic drop in core body temperature, there is a virtual cessation of neural activity (Strumwasser, 1959;Walker et al, 1977), a dramatic drop in metabolic rate (Buck and Barnes, 2000), and a halting of many cell maintenance processes, including transcription and translation (Frerichs et al, 1998;van Breukelen and Martin, 2002). In between torpor bouts, hibernators briefly arouse to euthermic temperatures, during which time measurable neural activity resumes.…”

Section: Introductionmentioning

confidence: 99%

Ubiquitous and Temperature-Dependent Neural Plasticity in Hibernators

Ohe¹,

Darian‐Smith²,

Garner³

et al. 2006

J. Neurosci.

140

100

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Hibernating mammals are remarkable for surviving near-freezing brain temperatures and near cessation of neural activity for a week or more at a time. This extreme physiological state is associated with dendritic and synaptic changes in hippocampal neurons. Here, we investigate whether these changes are a ubiquitous phenomenon throughout the brain that is driven by temperature. We iontophoretically injected Lucifer yellow into several types of neurons in fixed slices from hibernating ground squirrels. We analyzed neuronal microstructure from animals at several stages of torpor at two different ambient temperatures, and during the summer. We show that neuronal cell bodies, dendrites, and spines from several cell types in hibernating ground squirrels retract on entry into torpor, change little over the course of several days, and then regrow during the 2 h return to euthermia. Similar structural changes take place in neurons from the hippocampus, cortex, and thalamus, suggesting a global phenomenon. Investigation of neural microstructure from groups of animals hibernating at different ambient temperatures revealed that there is a linear relationship between neural retraction and minimum body temperature. Despite significant temperature-dependent differences in extent of retraction during torpor, recovery reaches the same final values of cell body area, dendritic arbor complexity, and spine density. This study demonstrates large-scale and seemingly ubiquitous neural plasticity in the ground squirrel brain during torpor. It also defines a temperature-driven model of dramatic neural plasticity, which provides a unique opportunity to explore mechanisms of large-scale regrowth in adult mammals, and the effects of remodeling on learning and memory.

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Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator

Cited by 243 publications

References 49 publications

Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus)

Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus)

Seasonal Changes in Daily Metabolic Patterns of Tegu Lizards (Tupinambis merianae) Placed in the Cold (17°C) and Dark

Ubiquitous and Temperature-Dependent Neural Plasticity in Hibernators

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