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Torpor energetics are related to the interaction between body mass and climate in bats of the family Vespertilionidae

Jorge Ayala-Berdon, Kevin I. Medina-Bello

Posted on: 7 December 2023 , updated on: 28 October 2024

Preprint posted on 2 October 2023

Article now published in Journal of Experimental Biology at http://dx.doi.org/10.1242/jeb.246824

Smarter bats take better naps! New study finds that, by entering a state of “mini hibernation”, bats inhabiting warm climates save more energy than cold climate bats, and the reason may be linked to brain size!

Selected by Sarah Young-Veenstra

Categories: physiology, zoology

Updated 28 October 2024 with a postLight by Sarah Young-Veenstra

Jorge Ayala-Berdon and Kevin Medina-Bello’s bioRxiv preprint was recently republished in the esteemed Journal of Experimental Biology! This well written preprint did not require major revisions for publication, however, the study’s background and application is conveyed with more clarity in the published version, such that some of the questions I initially raised in my preLight were answered.

 

This study empirically explores, for the first time, how torpor is related to body mass and habitat climate. Although this relationship has been theoretically modelled, Ayala-Berdon and Medina-Bello were the first to pragmatically test the assumptions. Ultimately, the study found that both body size and climate impact torpor, such that smaller bats and bats from colder climates benefit the most from torpor-induced energy savings. I wondered in my preLight whether the climate-specific pattern might be based on acclimatory differences or evolutionary differences between populations. The published version of this study suggests the differences are evolutionary adaptations to the local conditions, where warmer climates may not be as energetically demanding as colder climates. Thus, colder climates may impose selection for bats who save energy more efficiently, while warmer climates may favour other traits, such as larger brains.

 

I also wondered how the authors might expect the climate pattern to scale across populations in the Northern-most ranges of the bats’ distribution, where winter temperatures drop below 0°C. Although this question is not directly addressed in the publication, the predicted application of this study to other temperature habitats is intuitive. Every species has an ambient temperature range in which they do not need to expend energy to thermoregulate (termed the thermoneutral zone). Below the lower limit of the thermoneutral zone is a threshold temperature that triggers torpor as an energy saving strategy (rather than expending more energy to maintain body heat). The authors discuss how the thermoneutral zone shifts in species living in different habitats. Thus, the thermoneutral zone may shift to lower temperatures in colder habitats, but the torpor strategy and size/climate-specific torpor energy savings are likely consistent.

 

Overall, this is a fascinating, novel, and important study that helps researchers better understand torpor – a prevalent physiological phenomenon – which may have important implications for further understanding the greater biology, ecology, and geographical distribution of animals who utilize torpor strageties.

Background

Many species across the animal kingdom deal with difficult times by sleeping through them. You might think this an appealing option, and bats would agree with you. Bats, like all living things, have a limited range of what conditions they can tolerate. For instance, species have an optimal temperature range, above which is too hot to handle and below which is too cold to function. When the ambient temperature becomes too cold to function, an animal struggles because it is unable to create enough energy to maintain basic life functions. Bats, however, can cope with these cold temperatures by entering a state of torpor. Torpor is akin to a temporary hibernation, where an animal essentially powers down for a few hours within a day. This allows bats to decrease the amount of energy necessary for survival, which is reflected by a depression of the rate at which their body creates energy (metabolic rate).

 

Torpor is an effective strategy because it allows an animal to enter a state of complete inactivity, which consists of slower bodily functions, a slower heart rate, and a lower body temperature to maintain. Suffice to say, torpor is characterized by extremely low energetic expenditure, and the metabolic rate needed to sustain this state can be as little as 10% of the metabolic rate that sustains an animal’s awake state.

 

An animal’s body temperature serves as an indication of how much energy their body is demanding. The higher the body temperature, the higher the metabolic rate. When a bat enters torpor, their body temperature drops. Interestingly, most animals from warm climates who utilize torpor maintain a higher body temperature during torpor relative to those who inhabit cold climates. This indicates that warm climate animals consume more energy during torpor than cold climate animals. Furthermore, small animals appear to be able to reach a relatively low minimum body temperature during torpor compared to large animals, indicating that small animals can maximize energetic savings to a greater extent during torpor than large animals. The preprint I will discuss here explores an interesting new avenue: how the energetic dynamics of torpor are impacted by the interaction of body mass and climate in different bat species.

 

Key Findings

The research team collected 11 different species of bats, who vary widely in body mass, from four locations in central Mexico: two warm climate sites and two cold climate sites. They acclimated bats to 28°C, then gradually decreased the temperature to 8°C. The researchers measured the metabolic rate before entering torpor (basal metabolic rate), the temperature at which the bats entered torpor, and the metabolic rate during torpor. Furthermore, from these measurements, the research team calculated the metabolic reduction (%) during torpor to estimate the energetic savings that torpor facilitates. Using a phylogenetic model, the researchers compared bat species across warm and cold habitats and detected several interesting patterns in torpor energetics.

 

Smaller bats save more energy with torpor

By virtue of having less body mass, small bats have less tissue available to metabolize into energy than large bats do. As a result, larger bats tend to exhibit higher basal metabolic rates than smaller bats. This study found that during torpor, when the metabolic rate drops to the minimum rate capable of sustaining life, larger bats maintained a higher metabolic rate than smaller bats. This pattern was consistent within both warm climates and cold climates (preprint Figure 4f). Furthermore, smaller bats decreased their metabolic rate to a greater extent during torpor, thereby conserving more energy than larger bats when engaging torpor strategies. While this pattern was observed within each climate, the trend was steeper within the warm climate (preprint Figure 4c).

 

Smaller bats enter torpor at higher temperatures

In nature, an animal’s surface-area to volume ratio (SA:V) is an important factor that plays a major role in determining an individual’s ecological niche. Indeed, SA:V determines how significant evaporation will be to an animal’s thermoregulatory capacity. When surface area is much greater than volume, evaporation can heavily interfere with an animal’s ability to maintain their body temperature. Whereas when the SA:V is smaller, evaporation is less harmful to thermoregulatory efforts. As a general rule, the smaller the organism, the greater the SA:V. In fact, their high SA:V is largely the reason that small animals tend not to inhabit cold climates: a high SA:V makes them vulnerable to heat loss in cold temperatures. When their endogenously produced heat inevitably evaporates, cold climates steal small animals’ body heat at a higher rate than they can replenish it, thereby demanding a metabolic rate that is impossible to maintain.

 

Owing to their high SA:V, smaller bats are less cold tolerant than larger bats. Unsurprisingly, this is reflected in the temperature that triggers torpor. This study found that smaller bats enter torpor at higher temperatures than large bats. This pattern was present in both climates but displayed a more dramatic trend in cold climates (preprint Figure 4d).

 

Climate Overrules Mass in Energetic Patterns!

Conceptually consistent with SA:V determined thermoregulation, the researchers noticed that their warm climate sites were dominated by small bats while their cold climate sites were dominated by large bats. However, contrary to mass-determined energetics, warm climate bats had ~23% higher metabolic rates than cold climate bats, despite being ~53% smaller (preprint Figure 4a & Figure 4f). Additionally, warm climate bats reduced their metabolic rate to a greater extent during torpor, allowing them to save more energy than cold climate bats (preprint Figure 4c).

 

The reason why climate-induced metabolic rates can rival the mass-determined effect may be related to brain size. Bats inhabiting warm climates live in more diverse, intricate environments than bats in cold climates do, and habitat complexity has been linked to brain size. Bats who navigate more complex environments possess larger brains than those who inhabit simple environments. Such differences in organ size correlates with energetics, where larger brained individuals have higher metabolic rates than smaller brained individuals. Additionally, prey abundance is higher in warmer climates, which allows bats in these areas to fuel a consistently high metabolic rate.

 

Conclusions

This study is the first to highlight how torpor is affected by body mass and climate as interacting factors. The authors not only found body mass-dependent traits that are consistent with thermoregulatory principles, but also discovered a significant interaction between body mass and climate. Climate proves to be a major factor in controlling torpor energetics, so much so that it can overpower the effect of body size. The mechanism(s) underlying the significance of climate is unknown, although the researchers assert that the environmental complexity associated with different climates mandate different brain sizes, which, in turn, mediate different metabolic demands. However, this hypothesis requires testing, and this study suggests a need for more comprehensive research into the effects of body mass and climate on torpor and hibernation, not only in bats, but also in other species who employ these energy saving strategies.

 

Summary figure. A generalized map of bat collection locations in central Mexico. Southern sites, coded red, are the warm climate sites (24°C – 40°C) and northern sites, coded blue, are the cold climate sites (10°C-22°C). Comparing bats collected in each climate, warm climate bats displayed smaller body mass (g), higher basal metabolic rates (mLO2g-1), lower minimum sustainable metabolic rates during torpor (mLO2hr-1), and a greater reduction of their metabolic rate during torpor (%) relative to cold climate bats

 

Why I Chose this Preprint:

This study presents a novel physiological interaction that determines the effectiveness of torpor in bats. Ayala-Berdon and Medina-Bello shed new light on how torpor’s effectiveness as a coping mechanism varies within species and across habitats and highlight new avenues for further research into the deeper biology that underlies the existence of these patterns. The results of this study, and potential further work on the topic, may have direct implications for current natural phenomena as we see populations range-shift northward.

 

Questions for the Authors:

  1. It is very interesting to see the differences in torpor energetics of bats between warm and cold climates within central Mexico, where the cold climate is, at the most, ~30°C colder than the warm climate. How do you think this pattern might scale into the Northern-most ranges of bats’ distribution where temperatures drop below 0°C?
  2. You discuss the evolutionary link between evaporative cooling and roosting choice, which is intriguing! Do you expect that the choice to roost in areas that are effectively buffered against the elements, as opposed to poorly isolated areas, is a conscious choice or instinctual? Further, if you were to conduct your study again but include an element of roosting choice, how do you think it might have affected the body mass and climate dependent patterns in your results?
  3. Do you think that the climate-specific patterns you observed were based on adaptational differences or evolutionary differences between populations? If one was to take a bat from a warm climate and acclimatize it to cold temperatures, or acclimatize a cold climate bat to warm temperatures, would their torpor energetics match your study’s results?

Tags: behaviour, hibernation, metabolism, physiology, range shift, temperature, tolerance

doi: https://doi.org/10.1242/prelights.36138

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