Limits to physical performance and metabolism across species

Turner, Nigel; Hulbert, A. J.; Else, Paul L.

doi:10.1097/01.mco.0000247474.56908.79

Cited by 12 publications

(7 citation statements)

References 73 publications

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“…Decapotoma lunata (Auerswald and Gade, 1995) and Locusta migratoria (van der Horst et al, 1978)]. Whilst oxygen availability is thought to be the primary limiting factor for peak metabolism, energy limitation is thought to be crucial in endurance metabolism (Turner et al, 2006). Our results are consistent with this hypothesis, because the relationship between flight metabolism and trehalose concentration after the flight was strongest when flight metabolism was measured as CO 2 production during the last 5 min of the experiment.…”

Section: Discussionsupporting

confidence: 81%

Oxygen and energy availability interact to determine flight performance in the Glanville fritillary butterfly

Fountain

Melvin

Ikonen

et al. 2016

Journal of Experimental Biology

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Flying insects have the highest known mass-specific demand for oxygen, which makes it likely that reduced availability of oxygen might limit sustained flight, either instead of or in addition to the limitation due to metabolite resources. The Glanville fritillary butterfly (Melitaea cinxia) occurs as a large metapopulation in which adult butterflies frequently disperse between small local populations. Here, we examine how the interaction between oxygen availability and fuel use affects flight performance in the Glanville fritillary. Individuals were flown under either normoxic (21 kPa O 2 ) or hypoxic (10 kPa O 2 ) conditions and their flight metabolism was measured. To determine resource use, levels of circulating glucose, trehalose and whole-body triglyceride were recorded after flight. Flight performance was significantly reduced in hypoxic conditions. When flown under normoxic conditions, we observed a positive correlation among individuals between post-flight circulating trehalose levels and flight metabolic rate, suggesting that low levels of circulating trehalose constrains flight metabolism. To test this hypothesis experimentally, we measured the flight metabolic rate of individuals injected with a trehalase inhibitor. In support of the hypothesis, experimental butterflies showed significantly reduced flight metabolic rate, but not resting metabolic rate, in comparison to control individuals. By contrast, under hypoxia there was no relationship between trehalose and flight metabolic rate. Additionally, in this case, flight metabolic rate was reduced in spite of circulating trehalose levels that were high enough to support high flight metabolic rate under normoxic conditions. These results demonstrate a significant interaction between oxygen and energy availability for the control of flight performance.

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Section: Discussionsupporting

confidence: 81%

Oxygen and energy availability interact to determine flight performance in the Glanville fritillary butterfly

Fountain

Melvin

Ikonen

et al. 2016

Journal of Experimental Biology

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“…The mechanisms that lead to differences in metabolic rate and aging are complex and multifaceted, with no one mechanism or hypothesis explaining all differences in metabolic rate or aging (Konarzewski and Książek, 2013;McKechnie and Swanson, 2010;Tosato et al, 2007;Turner et al, 2006b). Therefore, even with these changes, determining the validity of the membrane pacemaker hypotheses will be difficult, but instituting these changes will substantially aid us in detangling if one or both of these hypotheses are valid or if some element of fatty acyl composition besides number of double bonds, such as n-3/n-6 ratio or carbon length (Buttemer et al, 2010;Paula et al, 1996;Valencak and Ruf, 2007), is responsible for correlations among fatty acyl composition, metabolic rate, and longevity.…”

Section: Discussionmentioning

confidence: 98%

Perspectives on the membrane fatty acid unsaturation/pacemaker hypotheses of metabolism and aging

Calhoon

Williams

2015

Chemistry and Physics of Lipids

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“…With regard to the brain, regional metabolism in both humans and rats is either unchanged or decreased by acute sleep deprivation [16], [58], [59], [60]; therefore, the brain is an unlikely source of an excessive and progressive drain on energy reserves during chronic sleep restriction. Candidate cell functions that may drive the metabolic intensity of the vital organs during sleep restriction include anabolic processes and implicate mitochondrial reactions, substrate cycling, and membrane integrity [54], [61], [62].…”

Section: Discussionmentioning

confidence: 99%

Repeated Exposure to Severely Limited Sleep Results in Distinctive and Persistent Physiological Imbalances in Rats

Everson

Szabó

2011

PLoS ONE

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Chronic sleep disruption in laboratory rats leads to increased energy expenditure, connective tissue abnormalities, and increased weights of major organs relative to body weight. Here we report on expanded findings and the extent to which abnormalities become long-lasting, potentially permanent changes to health status after apparent recuperation from chronic sleep disruption. Rats were exposed 6 times to long periods of disrupted sleep or control conditions during 10 weeks to produce adaptations and then were permitted nearly 4 months of undisturbed sleep. Measurements were made in tissues from these groups and in preserved tissue from the experimental and control groups of an antecedent study that lacked a lengthy recuperation period. Cycles of sleep restriction resulted in energy deficiency marked by a progressive course of hyperphagia and major (15%) weight loss. Analyses of tissue composition in chronically sleep-restricted rats indicated that protein and lipid amounts in internal organs were largely spared, while adipose tissue depots appeared depleted. This suggests high metabolic demands may have preserved the size of the vital organs relative to expectations of severe energy deficiency alone. Low plasma corticosterone and leptin concentrations appear to reflect low substrate availability and diminished adiposity. After nearly 4 months of recuperation, sleep-restricted rats were consuming 20% more food and 35% more water than did comparison control rats, despite normalized weight, normalized adipocytes, and elevated plasma leptin concentrations. Plasma cholesterol levels in recuperated sleep-restricted rats were diminished relative to those of controls. The chronically increased intake of nutriments and water, along with altered negative feedback regulation and substrate use, indicate that internal processes are modified long after a severe period of prolonged and insufficient sleep has ended.

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Limits to physical performance and metabolism across species

Abstract: Animals display great diversity in physical and metabolic performance. The many factors that interact to set the upper limit of performance in different species are set by their evolutionary history and define the metabolic window in which they exist.

Cited by 12 publications

References 73 publications

Oxygen and energy availability interact to determine flight performance in the Glanville fritillary butterfly

Oxygen and energy availability interact to determine flight performance in the Glanville fritillary butterfly

Perspectives on the membrane fatty acid unsaturation/pacemaker hypotheses of metabolism and aging

Repeated Exposure to Severely Limited Sleep Results in Distinctive and Persistent Physiological Imbalances in Rats

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