Reversal of the adipostat control of torpor during migration in hummingbirds

  1. Erich R Eberts
  2. Christopher G Guglielmo
  3. Kenneth C Welch

  • Curated by eLife

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    Evaluation Summary:

    This study substantially advances our understanding of why, when, and how wild birds use daily torpor as an energetic strategy. A technically challenging combination of carefully controlled experiments on temporarily captive wild birds along with frequent respiratory measurements and whole-body composition measurements was key to making this advance.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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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.

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  1. Version published to 10.7554/elife.70062 on eLife
  2. eLife

    Evaluation Summary:

    This study substantially advances our understanding of why, when, and how wild birds use daily torpor as an energetic strategy. A technically challenging combination of carefully controlled experiments on temporarily captive wild birds along with frequent respiratory measurements and whole-body composition measurements was key to making this advance.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    This study aimed to determine the rules governing the use of torpor and whether these rules differed between the breeding, fattening and migration periods of the annual cycle of the ruby-throated hummingbird. The authors evaluated changes in the relationships between evening body fat content and the torpor occurrence, torpor duration, time of torpor entry, and amount of energy expended before torpor entry during the breeding, fattening and migration periods. Authors showed that birds shift the rules on when to enter torpor depending on whether they are in a life-history stage where a lean body composition is advantageous such as during breeding or during times when accumulating energy stores is advantageous such as during migration: during breeding, ruby-throated hummingbirds go into torpor when body fat stores drop to 5% of body mass and are unlikely to enter torpor above this threshold within 75% of the night, whereas during migration they are more likely to enter torpor at high body fat content. Authors conclude that their findings demonstrate the versatility of torpor as an energy management mechanism throughout the annual cycle. They also suggest that torpor plays a role in driving pre-migratory increases in body mass during the fattening period.

    This is a detailed and interesting study, however, it is not clear that this study has repeatedly and accurately defined a consistent rule governing torpor use in hummingbirds. Its findings, nonetheless, has implications for our understanding of the physiology of torpor.

  4. eLife

    Reviewer #2 (Public Review):

    This study quantifies body composition, energy expenditure and torpor use in breeding and migrating Ruby-throated hummingbirds. The authors quantify body composition using QMR providing direct high-resolution measurements of fat storage. They additionally use flow through respirometry to measure energy expenditure allowing for accurate estimates of torpor use and night-time energy savings. Serial measurements across the breeding, fattening and migration seasons show how birds seasonally adjust their body fat threshold for torpor use (the adipostat) to support potential energy emergencies (e. g. cold snaps, storms that prevent foraging) during breeding season to a new higher fat setpoint during migration to support rapid fat accumulation to fuel migration.

    A key strength of the paper is that the authors directly quantify body composition using QMR which provides rapid, repeatable, noninvasive measurements of body composition. Combined with the night-time respirometry measurements the study provides a really exciting and convincing picture of the changing context for torpor use with differing life history stages in hummingbirds.

    This work also importantly provides insight into how climate change induced reductions in floral nectar with increased drought and higher temperatures during migration may be buffered by the increased use of torpor.

  5. eLife

    Reviewer #3 (Public Review):

    This is an excellent study overall. It pushes frontiers with respect to our understanding of torpor. The design and methods are rigorous and well suited to some key questions in bird torpor biology: what determines the use, timing, and duration of torpor? The use of respirometry and QMR was a major strength of the study. The study convincingly uncovers an interaction between seasonal cycles and body fat in determining torpor use and bout length.

    The study uses 16 wild Ruby-throated Hummingbirds that were each held in captivity during the course of a summer. The controlled conditions were necessary, but present both a strength and a weakness. The weakness is that environmental cues that may effect torpor - variation in temperature, precipitation, food availability, etc. - were not in effect (note: daylight cycles were varied in a semi-natural way, but that needed to be described in more detail). Body mass and composition was convincingly important for torpor initiation and length, but it was difficult to tell what factors caused variation in body mass and composition because all of the birds had ad libitum food; was it just individual variation? Were some birds more stressed than others by captivity? For this and other reasons, looking forward, I hope these investigators thought to collect genetic samples from each individual.

  6. Version published to 10.1101/2021.05.13.443997v1 on bioRxiv