Baby in the bathwater: Should we abandon the use of body temperature thresholds to quantify expression of torpor?

doi:10.1016/j.jtherbio.2011.08.001

Journal of Thermal Biology

Volume 36, Issue 7, October 2011, Pages 376-379

https://doi.org/10.1016/j.jtherbio.2011.08.001 Get rights and content

Abstract

Boyles et al. (this issue) argue against the use of body temperature (T_b) thresholds to quantify the expression of torpor in endotherms and our purpose is to provide a counterpoint argument. We contend that T_b thresholds provide valuable information about ecological factors influencing the evolution of thermoregulation. We also point out shortcomings of the so-called heterothermy index proposed as an alternative. However, to be clear, we do agree with Boyles et al. (this issue) that the use of torpor thresholds can limit some aspects of the study of thermoregulation and applaud the more widespread incorporation of theoretical underpinnings proposed by Boyles et al. (this issue) and others.

Highlights

► We address use of the torpor cut-off method to analyze body temperature patterns. ► In point–counterpoint format, we discuss the pros and cons of the method. ► The method may have limited advances in our understanding of thermoregulation. ► Conversely, huge gains in knowledge have been achieved with the method.

Introduction

Boyles et al. (this issue) argue against the method of distinguishing between torpid and non-torpid states in endotherms based on body temperature (T_b) thresholds. They argue that T_b thresholds eliminate the potential for ecophysiologists to place thermoregulation by endotherms in an adaptive context because they exclude endotherms traditionally classified as homeotherms and encourage a “stamp collecting” mentality, where the expression (or not) of torpor is simply cataloged in species after species without considering its adaptive significance. We wholeheartedly agree with Boyles et al. (this issue) that the evolutionary physiology literature on hibernation and daily torpor (see e.g., Geiser and Ruf, 1995) will benefit from stronger theoretical underpinning based on evolutionary biology and we applaud their efforts, and those of others, to further develop this framework (Angilletta et al., 2010, Boyles et al., 2011). We also agree that our understanding of thermoregulation by endotherms would benefit from greater inclusion of homeotherms in comparative analyses and that use of arbitrary T_b thresholds (e.g., 30 °C) may limit the inference to be gained from inter-specific comparisons. However, we argue that Boyles et al. (this issue) dismissal of T_b thresholds amounts to throwing out the baby with the thermal biology bathwater. While acknowledging the beneficial aspects of their proposed approach, our purpose is to play devil's advocate and highlight both theoretical and practical objections.

Section snippets

What is torpor?

First, it is critical to define what we actually mean when we use the word torpor. Boyles et al. (this issue) refer to T_b thresholds for torpor as being inconsistent with IUPS (2003), which defines torpor on the basis of “behavioral responsiveness to stimuli”. However, in our view and as pointed out elsewhere (Willis, 2007), this definition is misleading and outdated, has led to considerable confusion in the literature and, in practice, is not what the vast majority of ecophysiologists mean

Do torpor and homeothermy represent distinct physiological states?

Boyles et al. (this issue) suggest there is little evidence to conclude that heterothermic and homeothermic endotherms are representative of distinct physiological states and that T_b flexibility is better represented as a continuum from perfect homeothermy to pronounced heterothermy. On the contrary, we argue that there is evidence to support a non-arbitrary distinction between species based on their ability to adjust the T_b setpoint as a behavioral or physiological response to energy

Do T_b thresholds dismiss homeothermy as “ecologically and evolutionarily inconsequential”?

Boyles et al. (this issue) suggest that little can be learned about the adaptive significance of thermoregulatory strategies based on T_b thresholds in part because studies dependent on T_b thresholds treat homeotherms as “ecologically and energetically inconsequential” and implicitly assume that homeotherms do not maximize fitness. Boyles et al. (this issue) seem to misunderstand what most studies of torpor in endotherms aim to do: understand ecological, behavioral and/or physiological factors

Are we just “stamp collecting”?

Boyles et al. (this issue) also appear dismissive of collecting measurements of similar variables from multiple species (i.e., what they term “stamp collecting”) when it comes to depth and duration of torpor. We argue (and expect Boyles et al. (this issue) would agree) that, in general, this kind of study repetition is actually critical to the comparative method, which forms the basis of evolutionary physiology. For example hundreds of studies have “stamp collected” measurements of basal or

Heterothermy index: an alternative?

Although we differ on the points above, we agree with much of Boyles et al. (this issue) nicely explained rationale for not using arbitrary T_b thresholds. Inconsistency among threshold values for different species can limit the inference to be drawn from comparative studies and the concern that many analyses might omit energetically and ecologically important shallow torpor bouts is a legitimate one. While the absolute value for a T_b threshold may appear arbitrary, it is often picked in

Acknowledgments

Our research on thermal responses by animals has been supported by the Natural Sciences and Engineering Research Council (Canada), and Australian Research Council and National Research Foundation (South Africa). We are grateful to J.G. Boyles, B. Smit and A.E. McKechnie for the opportunity to respond.

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Maintaining a high and stable body temperature as observed in most endothermic mammals and birds is energetically costly and many heterothermic species reduce their metabolic demands during energetic bottlenecks through the use of torpor. With the increasing number of heterotherms revealed in a diversity of habitats, it becomes apparent that triggers and patterns of torpor use are more variable than previously thought. Here, we report the previously overlooked use of, shallow rest-time torpor (body temperature >30 °C) in African lesser bushbabies, Galago moholi. Body core temperature of three adult male bushbabies recorded over five months showed a clear bimodal distribution with an average active modal temperature of 39.2 °C and a resting modal body temperature of 36.7 °C. Shallow torpor was observed in two out of three males (n = 29 torpor bouts) between June and August (austral winter), with body temperatures dropping to an overall minimum of 30.7 °C and calculated energy savings of up to 10%. We suggest that shallow torpor may be an ecologically important, yet mostly overlooked energy-saving strategy employed by heterothermic mammals. Our data emphasise that torpor threshold temperatures need to be used with care if we aim to fully understand the level of physiological plasticity displayed by heterothermic species.
Determining the different phases of torpor from skin- or body temperature data in heterotherms
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Unfortunately, the lack of a common definition in this case has led to a diversity of different body temperature thresholds being used, from the use of “active” temperatures (the Tb recorded immediately prior to departure from roost; Barclay et al., 2001) to torpor onset values calculated using lab-derived equations (Willis, 2007), and in many cases various seemingly “arbitrary” cut-off values appear to have been applied (reviewed by Barclay et al., 2001). Nevertheless, it remains one of the easiest metrics to apply, and although this may not be an optimal metric for direct comparisons of torpor use between species (see Boyles, 2019) it still provides good estimates within populations or species if the cut-off values are chosen sensibly (Brigham et al., 2011). An overlooked aspect with this method, however, is that torpor bouts themselves consist of different phases as individuals (i) gradually ‘enter’ torpor with declining body temperatures, (ii) remain for a period at ‘stable’ torpid body temperature, and (iii) ‘arouse’ out of torpor with increasing body temperatures, each of which will differ greatly in their energetic characteristics (see Utz et al., 2007; Geiser et al., 2014; Menzies et al., 2016).
Technological innovations have made heat-sensitive data-loggers smaller, more efficient and less expensive, which has led to a growing body of literature that measures the skin- or body temperatures of small animals in their natural environments. Studies of this type on heterothermic endotherms have prompted much debate regarding how to best define ‘torpor’ expressions from skin- or body temperature data alone. We propose a new quantitative method for defining torpor ‘entries’, ‘arousals’ and ‘stable torpor periods’ whilst comparing the results to ‘torpor bout’ durations identified using only the torpor cut-off method. By decomposing a torpor bout into ‘entries’, ‘stable torpor periods’, and ‘active arousals’, we avoid biases introduced by using strict threshold temperature values for the onset of torpor, thereby allowing better insight into individual use of torpor. We present our method as an easy-to-use function written in R-code, offering an un-biased and consistent methodology to be applied on skin- or body temperature measurements across datasets and research groups. When testing the function on a large dataset of skin temperature data collected on three bat species in Norway (Plecotus auritus: N_ind = 39; Eptesicus nilssonii: N_ind = 11; Myotis brandtii: N_ind = 10), we identified 461 complete torpor bouts across species. More than 40% of the torpor bouts (N_bouts = 192) did not contain stable torpor periods, because the bats aroused before they had reached a stable skin temperature level. Furthermore, only considering ‘torpid’ and ‘euthermic’ temperature values by applying strict cut-off thresholds led to potentially large underestimations of torpor bout durations compared to our quantitative determination of the onset and termination of each torpor bout. We highlight the importance of differentiating between torpor phases, especially for active arousals that can be very energetically expensive and may alter our evaluation of the actual energetic savings gained by an individual employing torpor.
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Birds regulate body temperature (T_b) around setpoint values through changes in metabolic heat production and evaporative heat dissipation, accompanied by behavioral adjustments of heat transfer via radiation, convection, and conduction. Although the active-phase T_bs of 38–42°C maintained during normothermy are broadly similar across taxa, there is substantial phylogenetic variation in heat tolerance and evaporative cooling capacity. There are also pronounced differences among orders in the capacity for hypometabolic states such as torpor, during which T_b may decrease to below 5°C. In terms of heat dissipation pathways, the last decade has seen the avian beak emerge as an important site of radiative and convective heat loss. The role of developmental plasticity in the ontogeny of thermoregulation, particularly as a determinant of heat tolerance later in life, is a field of enquiry with considerable relevance for predicting the performance of both domesticated and nondomesticated species under hotter future climates.
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Citation Excerpt :
To ensure that any differences in total daily activity between the control and charcoal/ash substrate was not caused by changing from old to new substrate, total daily activity was measured before (1749.0 ± 810.8 counts/day, n = 7, N = 14) and after (1885.3 ± 923.4 counts/day, n = 7, N = 14) changing the control substrate from old to new and no difference was found (t20 = 0.4, p = 0.7). As this formula provides a threshold estimate that detects shallow torpor bouts it was preferred over the widely used threshold of 30.0 °C [2], which may overlook decreases in Tb that are energetically important [5]. Therefore, torpor bout entry and arousal were calculated from times that Tb decreased below and above 32.5 °C.
The predicted increase of the frequency and intensity of wildfires as a result of climate change could have a devastating impact on many species and ecosystems. However, the particular physiological and behavioural adaptions of animals to survive fires are poorly understood. We aimed to provide the first quantitative data on physiological and behavioural mechanisms used by a small heterothermic marsupial mammal, the fat-tailed dunnart (Sminthopsis crassicaudata), that may be crucial for survival during and immediately after a fire. Specifically, we aimed to determine (i) whether captive torpid animals are able to respond to fire stimuli and (ii) which energy saving mechanisms are used in response to fires. The initial response of torpid dunnarts to smoke exposure was to arouse immediately and therefore express shorter and shallower torpor bouts. Dunnarts also increased activity after smoke exposure when food was provided, but not when food was withheld. A charcoal/ash substrate, imitating post-fire conditions, resulted in a decrease in torpor use and activity, but only when food was available. Our novel data suggests that heterothermic mammals are able to respond to fire stimuli, such as smoke, to arouse from torpor as an initial response to fire and adjust torpor use and activity levels according to food availability modulated by fire cues.
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Both tissue samples were frozen in liquid nitrogen and then stored at −80 °C. Since analyzing heterothermy use with a fixed threshold of body temperature has methodological drawbacks (Boyles et al., 2011; Brigham et al., 2011; Canale et al., 2012), daily shallow hypothermia depth and bout duration were determined on individual Tb profiles. Hypothermia depth corresponded to daily minimal body temperature (Tb min, °C).
Optimal levels of unsaturated fatty acids have positive impacts on the use of prolonged bouts of hypothermia in mammalian hibernators, which generally have to face low winter ambient temperatures. Unsaturated fatty acids can maintain the fluidity of fat and membrane phospholipids at low body temperatures. However, less attention has been paid to their role in the regulation of shallow hypothermia, and in tropical species, which may be challenged more by seasonal energetic and/or water shortages than by low temperatures. The present study assessed the relationship between the fatty acids content of white adipose and liver tissues and the expression of shallow hypothermia in a tropical heterothermic primate, the gray mouse lemur (Microcebus murinus). The adipose tissue is the main tissue for fat storage and the liver is involved in lipid metabolism, so both tissues were expected to influence hypothermia dependence on fatty acids. As mouse lemurs largely avoid deep hypothermia (i.e. torpor) use under standard captive conditions, the expression of hypothermia was triggered by food-restricting experimental animals. Hypothermia depth increased with time, with a stronger increase for individuals that exhibited higher contents of unsaturated fatty acids suggesting that they were more flexible in their use of hypothermia. However these same animals delayed the use of long hypothermia bouts relative to individuals with a higher level of saturated fatty acids. This study evidences for the first time that body fatty acids unsaturation levels influence the regulation of body temperature not only in cold-exposed hibernators but also in tropical, facultative heterotherms.
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Baby in the bathwater: Should we abandon the use of body temperature thresholds to quantify expression of torpor?

Abstract

Highlights

Introduction

Section snippets

What is torpor?

Do torpor and homeothermy represent distinct physiological states?

Do Tb thresholds dismiss homeothermy as “ecologically and evolutionarily inconsequential”?

Are we just “stamp collecting”?

Heterothermy index: an alternative?

Acknowledgments

Comp. Biochem. Physiol. B

The evolution of thermal physiology in endotherms

Front. Biosci.

What's hot and what's not: defining torpor in free-ranging birds and mammals

Can. J. Zool.

A new comparative metric for estimating heterothermy in endotherms

Physiol. Biochem. Zool.

Metabolic rate and body temperature reduction during hibernation and daily torpor

Ann. Rev. Physiol.

Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns

Physiol. Zool.

Does torpor of elephant shrews differ from that of other heterothermic mammals?

J. Mamm.

Glossary of terms for thermal physiology

J. Therm. Biol.

Activity and torpor in two sympatric Australian desert marsupials

J. Zool. London

The zoogeography of mammalian basal metabolic rate

Am. Nat.

Heterothermy in elephant shrews, Elephantulus spp. (Macroscelidea): daily torpor or hibernation?

J. Comp. Physiol. B

The allometry of avian basal metabolic rate: good predictions need good data

Physiol. Biochem. Zool.

Torpor in an African caprimulgid, the freckled nightjar Caprimulgus tristigma

J. Avian Biol.

Do T_b thresholds dismiss homeothermy as “ecologically and evolutionarily inconsequential”?