Baby in the bathwater: Should we abandon the use of body temperature thresholds to quantify expression of torpor?
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 (Tb) thresholds. They argue that Tb 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 Tb 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 Tb 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 Tb 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 However, in our view and as pointed out elsewhere (Willis, 2007), this definition is misleading and outdated, has led to considerable confusion in the literature and, in practice, is not what the vast majority of ecophysiologists mean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 Tb 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 Tb setpoint as a behavioral or physiological response to energy
Do Tb 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 Tb thresholds in part because studies dependent on Tb 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 Tb 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 Tb 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.
References (28)
- et al.
Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction
Comp. Biochem. Physiol. B
(2003) - et al.
The evolution of thermal physiology in endotherms
Front. Biosci.
(2010) - et al.
What's hot and what's not: defining torpor in free-ranging birds and mammals
Can. J. Zool.
(2001) - et al.
A new comparative metric for estimating heterothermy in endotherms
Physiol. Biochem. Zool.
(2011) - Boyles, J.G., Smit, B., McKechnie, A.E.. Does use of the torpor cut-off method to analyze variation in body temperature...
Metabolic rate and body temperature reduction during hibernation and daily torpor
Ann. Rev. Physiol.
(2004)- et al.
Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns
Physiol. Zool.
(1995) - et al.
Does torpor of elephant shrews differ from that of other heterothermic mammals?
J. Mamm.
(2011) Glossary of terms for thermal physiology
J. Therm. Biol.
(2003)- et al.
Activity and torpor in two sympatric Australian desert marsupials
J. Zool. London
(2011)
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.
Cited by (35)
Saving energy via short and shallow torpor bouts
2023, Journal of Thermal BiologyDetermining the different phases of torpor from skin- or body temperature data in heterotherms
2023, Journal of Thermal BiologyCitation Excerpt :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).
Regulation of body temperature
2022, Sturkie's Avian PhysiologyPhysiological and behavioural responses of a small heterothermic mammal to fire stimuli
2015, Physiology and BehaviorCitation 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.
Shallow hypothermia depends on the level of fatty acid unsaturation in adipose and liver tissues in a tropical heterothermic primate
2014, Journal of Thermal BiologyCitation Excerpt :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).
Non-Torpid Heterothermy in Mammals: Another Category along the Homeothermy–Hibernation Continuum
2023, Integrative and Comparative Biology