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

Abstract

Active flight requires the ability to efficiently fuel bursts of costly locomotion while maximizing energy conservation during non-flying times. We took a multi-faceted approach to estimate how fruit-eating bats (Uroderma bilobatum) manage a high-energy lifestyle fueled primarily by fig juice. Miniaturized heart rate telemetry shows that they use a novel, cyclic, bradycardic state that reduces daily energetic expenditure by 10% and counteracts heart rates as high as 900 bpm during flight. Uroderma bilobatum support flight with some of the fastest metabolic incorporation rates and dynamic circulating cortisol in vertebrates. These bats will exchange fat reserves within 24 hr, meaning that they must survive on the food of the day and are at daily risk of starvation. Energetic flexibly in U. bilobatum highlights the fundamental role of ecological pressures on integrative energetic networks and the still poorly understood energetic strategies of animals in the tropics.

Keywords: Uroderma bilobatum; ecological physiology; ecology; energetics; flight; heart rate; torpor.

Figure 1.. 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 (f_H) 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).

Figure 2.. 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.

Figure 3.. 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.

Figure 4.. 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.

Figure 5.. 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.