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.

eLife digest

To survive, all animals have to balance how much energy they take in and how much they use. They must find enough food to fuel the chemical processes that keep them alive – known as their metabolism – and store leftover fuel to use when food is not available. Bats, for example, have a fast metabolism and powerful flight muscles, which require a lot of energy. Some bat species, such as the tent-making bats, survive on fruit juice, and their food sources are often far apart and difficult to find. These bats are likely to starve if they go without food for more than 24 hours, and therefore need to conserve energy while they are resting.

To deal with potential food shortages, bats and other animals can enter a low-energy resting state called torpor. In this state, animals lower their body temperature and slow down their heart rate and metabolism so that they need less energy to stay alive. However, many animals that live in tropical regions, including tent-making bats, cannot enter a state of torpor, as it is too hot to sufficiently lower their body temperature. Until now, scientists did not fully understand how these bats control how much energy they use.

Now, O’Mara et al. studied tent-making bats in the wild by attaching small heart rate transmitters to four wild bats, and measured their heartbeats over several days. Since each heartbeat delivers oxygen and fuel to the rest of the body, measuring the bats’ heart rate indicates how much energy they are using. The experiments revealed for the first time that tent-making bats periodically lower their heart rates while resting (to around 200 beats per minute). This reduces the amount of energy they use each day by up to 10%, and helps counteract heart rates that can reach 900 beats per minute when the bats are flying.

Overall, these findings show that animals have evolved in various ways to control their use of energy. Future research should use similar technology to continue uncovering how wild animals have adapted to survive in different conditions. This knowledge will help us to understand how life has become so diverse in the tropics and the strategies that animals may use as climates change.