Seasonal Expression of Avian and Mammalian Daily Torpor and Hibernation: Not a Simple Summer-Winter Affair‚Ä?1
Authors: Fritz Geiser
Journal: Frontiers in Physiology (2020)
Discipline: BIOLOGY & BIOCHEMISTRY
Keywords: daily torpor; energy expenditure; heterothermy; hibernation; reproduction
Affiliations: Centre for Behavioural and Physiological Ecology, Zoology CO2, University of New England, Armidale, NSW, Australia.

Abstract:  Daily torpor and hibernation (multiday torpor) are the most efficient means for energy conservation in endothermic birds and mammals and are used by many small species to deal with a number of challenges. These include seasonal adverse environmental conditions and low food/water availability, periods of high energetic demands, but also reduced foraging options because of high predation pressure. Because such challenges differ among regions, habitats and food consumed by animals, the seasonal expression of torpor also varies, but the seasonality of torpor is often not as clear-cut as is commonly assumed and differs between hibernators and daily heterotherms expressing daily torpor exclusively. Hibernation is found in mammals from all three subclasses from the arctic to the tropics, but is known for only one bird. Several hibernators can hibernate for an entire year or express torpor throughout the year (8% of species) and more hibernate from late summer to spring (14%). The most typical hibernation season is the cold season from fall to spring (48%), whereas hibernation is rarely restricted to winter (6%). In hibernators, torpor expression changes significantly with season, with strong seasonality mainly found in the sciurid and cricetid rodents, but seasonality is less pronounced in the marsupials, bats and dormice. Daily torpor is diverse in both mammals and birds, typically is not as seasonal as hibernation and torpor expression does not change significantly with season. Torpor in spring/summer has several selective advantages including: energy and water conservation, facilitation of reproduction or growth during development with limited resources, or minimisation of foraging and thus exposure to predators. When torpor is expressed in spring/summer it is usually not as deep and long as in winter, because of higher ambient temperatures, but also due to seasonal functional plasticity. Unlike many other species, subtropical nectarivorous blossom-bats and desert spiny mice use more frequent and pronounced torpor in summer than in winter, which is related to seasonal availability of nectar or water. Thus, seasonal use of torpor is complex and differs among species and habitats. 

Retracted: No

PubPeer comments:
 While not the main topic of the paper, Geiser (2020) includes an aside that reasserts a long-misplaced critique of a simple metric for describing variation in body temperature of endothermic mammals and birds: the Heterothermy Index (HI). The critique represents an obvious misunderstanding of the HI, and has potential to discourage future use of HI, even though it has proven quite useful when implemented and interpreted correctly (e.g., Dammhahn et al. 2017). The Heterothermy Index is little more than a modified standard deviation (it is calculated around a modal body temperature instead of a mean body temperature). The main criticism of HI is that it is possible to obtain the same HI value for two individuals with different thermoregulatory patterns, which my colleagues and I were the first to point out when we originally proposed HI (Boyles et al. 2011). After nearly a decade of using HI, it has become clear that cases of identical HI values describing different patterns are the exception, not the rule. For this to even be possible in a biologically meaningful way, one would need to directly compare an individual or species with a long, shallow torpor bout to one with a short, deep torpor bout. However, the traditional paradigm postulates that animals which use torpor fall into one of two categories: those that use deep, long torpor bouts (i.e. hibernators) and those that use short, shallow torpor bouts (i.e. daily heterotherms)(e.g., Geiser Ruf 1995, Geiser 2004, Ruf Geiser 2014, Geiser 2020). Species demonstrating the body temperature patterns that might be problematic for interpretations of HI are labeled intermediate and considered worthy of papers specifically focused on their uniqueness (e.g., Geiser Mzilikazi 2011, Geiser Martin 2013). As only a few mammals and birds studied to date display these u201cproblematicu201d body temperature patterns, HI can be applied with little controversy as an intra- or interspecific comparative metric for all but a small number of the roughly 15,000 endothermic species. The same cannot be said for other metrics commonly used to describe body temperature of endotherms (e.g., torpor cut-offs are only applicable to facultative heterotherms). Ironically, the concern about identical HI values for different thermoregulatory patterns would stand to be far more substantive if one took the position that mammals and birds represent a continuum and species demonstrating a wide diversity of thermoregulatory patterns are likely more common than long thought (sensu Boyles et al. 2013). It also speaks volumes that Geiser (2020) relied on hypothetical body temperature data representing vastly different sampling conditions instead of using real data for animals in his dismissal of HI. I have calculated HI values for dozens if not hundreds of species and can confirm that it is exceedingly difficult to find a biologically meaningful example of this issue using real data. All potential examples I have seen could easily be overcome with appropriate sampling and a healthy dose of common sense. To achieve identical HI values for the two hypothetical body temperature patterns, Geiser (2020) calculates HI in a manner my colleagues and I have explicitly and repeatedly warned against. In the original paper on HI (Boyles et al. 2011), we stated u201cu2026like the equation for standard deviation on which it is based, HI is sensitive to sample size in very small samplesu201d. In a recent paper (Boyles 2019), I argued u201cshort sampling durations can lead to misleading interpretationsu201d and u201cHI is not intended for, and not useful for, describing specific changes in different parts of the thermoregulatory cycle within speciesu201d. Geiser (2020) disregarded these warnings to an extreme degree by calculating HI for less than one full daily cycle in one of the hypothetical individuals with the goal of describing a single torpor bout. If one were to recalculate HI values for the individual using short, deep torpor and assuming it remained euthermic over the rest of the period measured for the individual using the shallow, long torpor bout, the HI value of the first individual would drop to ~11. If the first individual repeated the same torpor bout again during the second day, HI would be ~15. In either case, the first individual would clearly be less heterothermic than the second individual in a predictable way and easily differentiated by HI. The comparison being made in Figure 1 of Geiser (2020) demonstrates a fundamental misunderstanding and misuse of HI values. If it is my past writing on the subject that has been unnecessarily obtuse, I take this opportunity to categorically state that such use of HI is completely inappropriate. HI values calculated on less than a single daily cycle are nonsensical and interpretations of HI values calculated from even a few days of data require care and common sense (although they are not necessarily unreliable). It is unfortunate that such a misconception made it through the peer-review process, and I implore researchers to avoid using HI values in this manner with empirical data. Geiser (2020) demonstrates that if you attempt to use HI to describe a single torpor bout in isolation, you stand to be confused. I concur. This is the philosophical equivalent of analyzing categorical data in a t-test, misinterpreting the (unreliable) results, and then concluding the t-test is a flawed analytical tool. In summary, as my colleagues and I warned nearly a decade ago, it is theoretically possible to confuse thermoregulatory patterns based on HI values, especially if one misuses the metric and then misinterprets the results. As I have repeatedly argued elsewhere (Boyles 2019), the Heterothermy Index has a specific use, as does every metric currently available to describe body temperature of endotherms. The argument against using HI because of the possibility of two patterns resulting in the same value is a straw man. Every metric can lead to questionable results when misused, and I hope researchers using any metric will make the effort to understand the implications of their analytical choices and to use metrics applicable to the question at hand (Boyles 2019). Boyles, J. G. (2019) A brief introduction to methods for describing body temperature in endotherms. Physiol. Biochem. Zool., 92, 365. Boyles, J. G., B. Smit A. E. 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