Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

Abstract

Mammalian heterotherms, species that employ short or long periods of torpor, are found in many different climatic regions. Although the underlying physiological mechanisms of heterothermy in species from lower latitudes (i.e., the tropics and southern hemisphere) appear analogous to those of temperate and arctic heterotherms, the ultimate triggers and resulting patterns of energy expenditure and body temperature are often noticeably different. Phenotypic flexibility in the patterns of thermoregulation in non-Holarctic species can be extensive (depending on body condition, environmental parameters and species competition) and the factors responsible for inducing heterothermy are more variable in non-Holarctic species. As well as being a regular adaptation to seasonality, heterothermy can also be employed as a response to unpredictability in environmental parameters and as a response to emergency situations. Non-Holarctic heterotherms also challenge the notion that regular inter-bout arousals during hibernation are obligatory and suggest all that is necessary to maintain proper functioning during hibernation is an occasional passive return to-or maintenance of-a relatively high body temperature. The study of non-Holarctic heterotherms has led to the conclusion that heterothermy must be defined on the basis of mechanistic, physiological parameters, and not solely by body temperature; yet we are still limited in our abilities to record such mechanistic parameters in the field. It is now believed that homeothermy in mammals evolved in hot climates via an ancestral heterothermic state. Similar to extant warm-climate heterotherms, early mammals could have relied mainly on passive body temperature regulation with a capacity for short-to longer-term up-regulation of metabolism when needed. Hibernation, as seen in temperate and arctic species may then be a derived state of this ancestral heterothermy, and the study of torpor in warm climates can provide potential models for the energetics of early mammals.

Integrating Mortality Risk and the Adaptiveness of Hibernation

“…Hibernation is considered an adaptation to seasonal, hence predictable decreases in food resources and ambient temperatures. However, hibernation is also observed in mild climates and when ambient conditions are still favorable for activity (Nowack et al, 2020). If remarkable physiological aspects of hibernation have been widely studied, fewer studies have focused on its ecological and evolutionary significance.…”

“…A surprisingly large proportion of mammals, including a monotreme, several marsupials, and placental species regularly enter daily torpor and seasonal hibernation in the southern hemisphere (Grigg and Beard, 2000). For some species in these regions, the use of torpor may not be related to low environmental temperatures or limited food availability (Nowack et al, 2020). For example, the short-beaked echidna hibernates (Grigg et al, 1989) while ants and termites, which constitute the main part of its diet, remain available throughout the year (Grigg and Beard, 2000).…”

A unifying, eco‐physiological framework for animal dormancy

“…In the mammalian literature, metabolic flexibility in protoendothermic species (e.g. tenrecs or tropical and sub‐tropical bats) that use a mix of daily torpor‐ and hibernation‐like strategies across the heterothemic period have been difficult to integrate with the broader daily torpor‐hibernation dichotomy (Nowack et al., 2020; Treat et al., 2018; van Breukelen & Martin, 2015). We need a flexible concept of dormancy that transcends phylogenetic divisions and captures ecologically relevant axes of dormancy to facilitate phylogenetically broad comparative dormancy research.…”

Prolonged Torpor in Goodman’s Mouse Lemur (Microcebus lehilahytsara) from the High-Altitude Forest of Tsinjoarivo, Central-Eastern Madagascar

“…Climatic unpredictability has been linked to unique energy-conserving traits present in endemic fauna, including torpor [Wright, 1999]. The expression of heterothermy in the tropics is not limited to Madagascar, and species using this strategy range from Afrotropical mammals, such as elephant shrews, to Australasian species such as sugar gliders [Geiser and Körtner, 2010;McKechnie and Mzilikazi, 2011;Nowack et al, 2020].…”