Reversal of the adipostat control of torpor during migration in hummingbirds

  1. Erich R Eberts  Is a corresponding author
  2. Christopher G Guglielmo
  3. Kenneth C Welch Jr
  1. University of Toronto, Canada
  2. University of Western Ontario, Canada

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.

Data availability

All data is available in the main text or the supplementary materials. Analyses reported in this article can be reproduced using the data and code provided by Eberts et al., (2021).

The following data sets were generated

Article and author information

Author details

  1. Erich R Eberts

    Department of Biological Sciences, University of Toronto, Toronto, Canada
    For correspondence
    erich.eberts@mail.utoronto.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4259-8752
  2. Christopher G Guglielmo

    University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Kenneth C Welch Jr

    Department of Biological Sciences, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3283-6510

Funding

Natural Sciences and Engineering Research Council of Canada (06129-2015 RGPIN)

  • Kenneth C Welch Jr

Human Frontier Science Program (RGP0062/2016)

  • Kenneth C Welch Jr

Natural Sciences and Engineering Research Council of Canada Discovery Grant (05245-2015 RGPIN)

  • Christopher G Guglielmo

Canada Foundation for Innovation, Ontario Research Fund

  • Christopher G Guglielmo

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Chima Nwaogu, University of Cape Town, South Africa

Ethics

Animal experimentation: Details of animal husbandry and all experiments were approved by the University of Toronto (protocol # 20011649) and the University of Western Ontario Animal Care Committees (protocol #2018-092). Hummingbirds were captured under Ontario Collecting Permit SC-00041.

Version history

  1. Received: May 5, 2021
  2. Preprint posted: May 15, 2021 (view preprint)
  3. Accepted: November 19, 2021
  4. Accepted Manuscript published: December 6, 2021 (version 1)
  5. Accepted Manuscript updated: December 7, 2021 (version 2)
  6. Version of Record published: December 31, 2021 (version 3)
  7. Version of Record updated: January 10, 2022 (version 4)
  8. Version of Record updated: January 11, 2023 (version 5)

Copyright

© 2021, Eberts et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,896
    views
  • 241
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Erich R Eberts
  2. Christopher G Guglielmo
  3. Kenneth C Welch Jr
(2021)
Reversal of the adipostat control of torpor during migration in hummingbirds
eLife 10:e70062.
https://doi.org/10.7554/eLife.70062

Share this article

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

Further reading

    1. Ecology
    2. Epidemiology and Global Health
    Emilia Johnson, Reuben Sunil Kumar Sharma ... Kimberly Fornace
    Research Article

    Zoonotic disease dynamics in wildlife hosts are rarely quantified at macroecological scales due to the lack of systematic surveys. Non-human primates (NHPs) host Plasmodium knowlesi, a zoonotic malaria of public health concern and the main barrier to malaria elimination in Southeast Asia. Understanding of regional P. knowlesi infection dynamics in wildlife is limited. Here, we systematically assemble reports of NHP P. knowlesi and investigate geographic determinants of prevalence in reservoir species. Meta-analysis of 6322 NHPs from 148 sites reveals that prevalence is heterogeneous across Southeast Asia, with low overall prevalence and high estimates for Malaysian Borneo. We find that regions exhibiting higher prevalence in NHPs overlap with human infection hotspots. In wildlife and humans, parasite transmission is linked to land conversion and fragmentation. By assembling remote sensing data and fitting statistical models to prevalence at multiple spatial scales, we identify novel relationships between P. knowlesi in NHPs and forest fragmentation. This suggests that higher prevalence may be contingent on habitat complexity, which would begin to explain observed geographic variation in parasite burden. These findings address critical gaps in understanding regional P. knowlesi epidemiology and indicate that prevalence in simian reservoirs may be a key spatial driver of human spillover risk.