Many mammals use adaptive heterothermy (e.g., torpor, hibernation) to reduce metabolic demands of maintaining high body temperature ( T b ). Torpor is typically characterized by coordinated declines in T b and metabolic rate (MR) followed by active rewarming. Most hibernators experience periods of euthermy between bouts of torpor during which homeostatic processes are restored. In contrast, the common tenrec, a basoendothermic Afrotherian mammal, hibernates without interbout arousals and displays extreme flexibility in T b and MR. We investigated the molecular basis of this plasticity in tenrecs by profiling the liver proteome of animals that were active or torpid with high and more stable T b (∼32°C) or lower T b (∼14°C). We identified 768 tenrec liver proteins, of which 50.9% were differentially abundant between torpid and active animals. Protein abundance was significantly more variable in active cold and torpid compared with active warm animals, suggesting poor control of proteostasis. Our data suggest that torpor in tenrecs may lead to mismatches in protein pools due to poor coordination of anabolic and catabolic processes. We propose that the evolution of endothermy leading to a more realized homeothermy of boreoeutherians likely led to greater coordination of homeostatic processes and reduced mismatches in thermal sensitivities of metabolic pathways.
more »
« less
Non-Torpid Heterothermy in Mammals: Another Category along the Homeothermy–Hibernation Continuum
Synopsis Variability in body temperature is now recognized to be widespread among whole-body endotherms with homeothermy being the exception rather than the norm. A wide range of body temperature patterns exists in extant endotherms, spanning from strict homeothermy, to occasional use of torpor, to deep seasonal hibernation with many points in between. What is often lost in discussions of heterothermy in endotherms are the benefits of variations in body temperature outside of torpor. Endotherms that do not use torpor can still obtain extensive energy and water savings from varying levels of flexibility in normothermic body temperature regulation. Flexibility at higher temperatures (heat storage or facultative hyperthermia) can provide significant water savings, while decreases at cooler temperatures, even outside of torpor, can lower the energetic costs of thermoregulation during rest. We discuss the varying uses of the terms heterothermy, thermolability, and torpor to describe differences in the amplitude of body temperature cycles and advocate for a broader use of the term “heterothermy” to include non-torpid variations in body temperature.
more »
« less
- PAR ID:
- 10479318
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- Volume:
- 63
- Issue:
- 5
- ISSN:
- 1540-7063
- Format(s):
- Medium: X Size: p. 1039-1048
- Size(s):
- p. 1039-1048
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Synopsis Torpor is an incredibly efficient energy-saving strategy that many endothermic birds and mammals use to save energy by lowering their metabolic rates, heart rates, and typically body temperatures. Over the last few decades, the study of daily torpor—in which torpor is used for <24 h per bout—has advanced rapidly. The papers in this issue cover the ecological and evolutionary drivers of torpor, as well as some of the mechanisms governing torpor use. We identified broad focus areas that need special attention: clearly defining the various parameters that indicate torpor use and identifying the genetic and neurological mechanisms regulating torpor. Recent studies on daily torpor and heterothermy, including the ones in this issue, have furthered the field immensely. We look forward to a period of immense growth in this field.more » « less
-
Synopsis Migration is a widespread and highly variable trait among animals. Population-level patterns arise from individual-level decisions, including physiological and energetic constraints. Many aspects of migration are influenced by behaviors and strategies employed during periods of stopover, where migrants may encounter variable or unpredictable conditions. Thermoregulation can be a major cost for homeotherms which largely encounter ambient temperatures below the lower critical temperature during migration, especially during the rest phase of the daily cycle. In this review we describe the empirical evidence, theoretical models, and potential implications of bats and birds that use heterothermy to reduce thermoregulatory costs during migration. Torpor-assisted migration is a strategy described for migrating temperate insectivorous bats, whereby torpor can be used during periods of inactivity to drastically reduce thermoregulatory costs and increase net refueling rate, leading to shorter stopover duration, reduced fuel load requirement, and potential consequences for broad-scale movement patterns and survival. Hummingbirds can adopt a similar strategy, but most birds are not capable of torpor. However, there is an increasing recognition of the use of more shallow heterothermic strategies by diverse bird species during migration, with similarly important implications for migration energetics. A growing body of published literature and preliminary data from ongoing research indicate that heterothermic migration strategies in birds may be more common than traditionally appreciated. We further take a broad evolutionary perspective to consider heterothermy as an alternative to migration in some species, or as a conceptual link to consider alternatives to seasonal resource limitations. There is a growing body of evidence related to heterothermic migration strategies in bats and birds, but many important questions related to the broader implications of this strategy remain.more » « less
-
Abstract Mechanistic approaches for predicting the ranges of endotherms are needed to forecast their responses to environmental change. We test whether physiological constraints on maximum metabolic rate and the factor by which endotherms can elevate their metabolism (metabolic expansibility) influence cold range limits for mammal and bird species. We examine metabolic expansibility at the cold range boundary (MECRB) and whether species’ traits can predict variability in MECRBand then use MECRBas an initial approach to project range shifts for 210 mammal and 61 bird species. We find evidence for metabolic constraints: the distributions of metabolic expansibility at the cold range boundary peak at similar values for birds (2.7) and mammals (3.2). The right skewed distributions suggest some species have adapted to elevate or evade metabolic constraints. Mammals exhibit greater skew than birds, consistent with their diverse thermoregulatory adaptations and behaviors. Mammal and bird species that are small and occupy low trophic levels exhibit high levels of MECRB. Mammals with high MECRBtend to hibernate or use torpor. Predicted metabolic rates at the cold range boundaries represent large energetic expenditures (>50% of maximum metabolic rates). We project species to shift their cold range boundaries poleward by an average of 3.9° latitude by 2070 if metabolic constraints remain constant. Our analysis suggests that metabolic constraints provide a viable mechanism for initial projections of the cold range boundaries for endotherms. However, errors and approximations in estimating metabolic constraints (e.g., acclimation responses) and evasion of these constraints (e.g., torpor/hibernation, microclimate selection) highlight the need for more detailed, taxa‐specific mechanistic models. Even coarse considerations of metabolism will likely lead to improved predictions over exclusively considering thermal tolerance for endotherms.more » « less
-
Cooke, Steven (Ed.)Abstract In the mid-continental grasslands of North America, climate change is increasing the intensity and frequency of extreme weather events. Increasingly severe storms and prolonged periods of elevated temperatures can impose challenges that adversely affect an individual's condition and, ultimately, survival. However, despite mounting evidence that extreme weather events, such as heavy rain storms, can impose short-term physiological challenges, we know little regarding the putative costs of such weather events. To determine the consequences of extreme weather for small endotherms, we tested predictions of the relationships between both severe precipitation events and wet bulb temperatures (an index that combines temperature and humidity) prior to capture with body composition and hematocrit of grasshopper sparrows (Ammodramus savannarum) caught during the breeding season at the Konza Prairie Biological Station, Kansas, USA, between 2014 and 2016. We measured each individual's fat mass, lean mass and total body water using quantitative magnetic resonance in addition to their hematocrit. Individuals exposed to storms in the 24 hours prior to capture had less fat reserves, more lean mass, more water and higher hematocrit than those exposed to moderate weather conditions. Furthermore, individuals stored more fat if they experienced high wet bulb temperatures in the week prior to capture. Overall, the analysis of these data indicate that extreme weather events take a physiological toll on small endotherms, and individuals may be forced to deplete fat stores and increase erythropoiesis to meet the physiological demands associated with surviving a storm. Elucidating the potential strategies used to cope with severe weather may enable us to understand the energetic consequences of increasingly severe weather in a changing world.more » « less
An official website of the United States government
