Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats

  1. M Teague O'Mara  Is a corresponding author
  2. Martin Wikelski
  3. Christian C Voigt
  4. Andries Ter Maat
  5. Henry S Pollock
  6. Gary Burness
  7. Lanna M Desantis
  8. Dina KN Dechmann
  1. Max Planck Institute for Ornithology, Germany
  2. University of Konstanz, Germany
  3. Smithsonian Tropical Research Institute, Panama
  4. Leibniz Institute for Zoo and Wildlife Research, Germany
  5. University of Illinois at Urbana-Champaign, United States
  6. Trent University, Canada
5 figures and 3 additional files


Figure 1 with 4 supplements
Heart rate and energetic expenditure of U. bilobatum recorded across 350 hr of observation.

(A) 30 min examples of continuous heart rates of Uroderma bilobatum during daily activities and (B) the distribution of energetic costs estimated for these activities from heart rate.
Figure 1—figure supplement 1
Processing heart rate (fH) radio signals to extract heart rates of free-ranging bats.

Radio transmitters emit a continuous radio beacon that is interrupted by heart contractions. The signal is recorded to a digital recorder and the peak frequency is extracted using a finite impulse response filter. A timer function then counts transformed amplitude peaks that pass an adjustable threshold giving heart rate (bpm). Bat and radio tag graphic by Jorge Aleman, Smithsonian Tropical Research Institute.
Figure 1—figure supplement 2
Distribution of heart rates during flying and foraging, nightly non-flight activities, and in-roost rest during day light hours.
Figure 1—figure supplement 3
Flow through respironmetry calibration of non-exercising Uroderma bilobatum heart rate.

(A) Calibration of heart rate versus energy consumption and (B) of body temperature versus energy consumption.
Figure 1—figure supplement 4
Calibration of heart rate versus energy consumption measured in flow through respirometry of non-exercising bats (filled circles and dashed line) versus the energetic expenditure predicted by estimates for exercising animals that incorporate exercise-induced changes in stroke volume (open diamonds, solid line).

Respirometry calibrations did not capture the full range of heart rates measured in free-flying bats (173–1066 bpm).
Example heart rate recordings of one individual (bat 1) from 2014-12-07.

(A) Twenty-four hours of observation include periods of missing data when the bat was out of tracking range (grey boxes). Black and white bars above indicate night and day. Inset B shows more detail from the same time period (13–16 hr) to highlight the daily, cyclic bradycardia executed by these bats that save up to 10% of their daily energetic expenditure.
Mean field metabolic rate ±95% CI estimated by the number of hours spent in flight with (solid line) and without (dashed line) daily cyclic bradycardia.

A conservative estimate of two hours flight and a mean FMR of 45.79 kJ day−1 is based on our radio tracking observations of free-flying bats in their natural environment. This is within the estimates from the Speakman (2005) scaling relationship (grey box) for the range of body masses (16–19 g) measured in this population.
δ13C measured from exhaled CO2 post feeding on agave nectar (black circles) and Ficus insipida (blue squares).

(A) Uroderma fueled metabolism from ingested food immediately upon feeding on agave nectar (black) and fueled 50% (t50) of their metabolism within 8 min. There was no change in δ13C when bats were fed figs that comprise their natural diet. (B) When fed agave nectar over 72 hr bats reached a t50 for fat replacement after 13 hr and approached asymptotic values at 48 hr.
Baseline and restrained plasma cortisol values from female (n = 15) and male (n = 6) U. bilobatum.

There were no differences between sexes in baseline values, but females had higher circulating plasma cortisol values after one hour of restraint.

Additional files

Supplementary file 1

Mean ± sd per bat for heart rates (frequency in beats per minutes, fH) and energy consumption (kilojoules per hour, kJ h−1and Watts, W) used during flight, roosting at night, and resting during the day.

N gives the number of observations of heart rate observations used to calculate values.
Supplementary file 2

Individual fitted equations of a 1 pool exponential model for incorporation of ingested δ13C into breath carbon dioxide. 1 pool model: δ13C breath(t) = δ13C breath(∞) + [δ13Cbreath(0) – δ13C breath(∞)] e-t/k
Transparent reporting form

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. M Teague O'Mara
  2. Martin Wikelski
  3. Christian C Voigt
  4. Andries Ter Maat
  5. Henry S Pollock
  6. Gary Burness
  7. Lanna M Desantis
  8. Dina KN Dechmann
Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats
eLife 6:e26686.