Reversal of the adipostat control of torpor during migration in hummingbirds.

Erich R Eberts,Christopher G Guglielmo,Kenneth C Welch

doi:10.7554/elife.70062

Erich R Eberts, Christopher G Guglielmo + Show 1 more

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https://doi.org/10.7554/elife.70062

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Abstract

Many small endotherms use torpor to reduce metabolic rate and manage daily energy balance. However, the physiological 'rules' that govern torpor use are unclear. We tracked torpor use and body composition in ruby-throated hummingbirds (Archilochus colubris), a long-distance migrant, throughout the summer using respirometry and quantitative magnetic resonance. During the mid-summer, birds entered torpor at consistently low fat stores (~5% of body mass), and torpor duration was negatively related to evening fat load. Remarkably, this energy emergency strategy was abandoned in the late summer when birds accumulated fat for migration. During the migration period, birds were more likely to enter torpor on nights when they had higher fat stores, and fat gain was positively correlated with the amount of torpor used. These findings demonstrate the versatility of torpor throughout the annual cycle and suggest a fundamental change in physiological feedback between adiposity and torpor during migration. Moreover, this study highlights the underappreciated importance of facultative heterothermy in migratory ecology.

Highlights

IntroductionFacultative hypothermia is an energy conservation strategy that allows many mammalian and some avian species to survive periods of resource unavailability or to optimize their energy budgets in certain environments or life stages (McKechnie and Lovegrove, 2002; Ruf and Geiser, 2015)
Torpor is sensitive to critically low endogenous energy reserves; when the birds fatten for migration, this rule is abandoned, and the birds enter torpor with high levels of fat
While it does not appear that torpor initiation in the migration period is sensitive to a high energy threshold, the abandonment of the emergency threshold indicates that the rules governing of torpor use are dependent on life history stage, and that hummingbirds may employ torpor as part of various energy management strategies throughout the annual cycle

Summary

Introduction

IntroductionFacultative hypothermia is an energy conservation strategy that allows many mammalian and some avian species to survive periods of resource unavailability or to optimize their energy budgets in certain environments or life stages (McKechnie and Lovegrove, 2002; Ruf and Geiser, 2015). Studies that have investigated the use of torpor in hummingbirds in relation to food availability and body mass suggest that torpor initiation is controlled by an endogenous mechanism sensitive to an energy-store threshold (Hainsworth et al, 1977; Hiebert, 1992; Powers et al, 2003). This model predicts that a bird will initiate torpor if its energy stores reach critically low levels with enough time remaining in the night to achieve net energy savings. Hummingbirds typically rewarm 1-2 hours before sunrise, so they rarely enter torpor after approximately 75% of the night has elapsed; even if critically low energy levels are reached late in the night, birds may avoid entering torpor at this point if the energetic benefits are outweighed by the potential costs

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