Surviving winter: Physiological regulation of energy balance in a temperate ectotherm entering and exiting brumation

Holden, Kaitlyn G.; Gangloff, Eric J.; Gomez-Mancillas, Evangelina; Hagerty, Kelsi; Bronikowski, Anne M.

doi:10.1016/j.ygcen.2021.113758

Cited by 23 publications

(12 citation statements)

References 85 publications

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“…However, higher RMRs also increase energetic demands, which might expose organisms to energetic stress at times of resource scarcity (Auer, Bassar, et al, 2020; Williams et al, 2015). The mechanisms behind elevated RMR in cooler habitats include increases in mitochondrial density and enzyme activity, as well as hormonal modulation (Baldwin & Hochachka, 1970; Holden et al, 2021; Norin & Malte, 2012). Whether or not the costs of having high RMR are offset by maintaining activity at lower temperatures warrants further investigation.…”

Section: Discussionmentioning

confidence: 99%

Environmental temperature predicts resting metabolic rates in tropidurinae lizards

et al. 2022

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Interspecific variation in metabolic rates may be associated with climate, habitat structure, and resource availability. Despite a strong link between ecology and physiology, there is a dearth in the understanding of how the costs of body maintenance change during ecological transitions. We focused on an ecologically diverse group of neotropical lizards (Tropidurinae) to investigate whether and how resting metabolic rate (RMR) evolved under divergent micro‐ and macrohabitat conditions. Using a phylogenetic framework, we tested whether species from hot and dry habitats had lower RMRs in relation to those from cooler and mesic habitats, and investigated whether microhabitat usage had an effect over body mass‐adjusted RMRs. Our results suggest that RMRs are not phylogenetically structured in Tropidurinae. We found no correlation between metabolism, precipitation, and microhabitat usage. Species from warmer habitats had lower RMR compared to those from cooler habitats, supporting a mechanism of negative compensation in metabolic responses to temperature. Ectotherms from warmer habitats can limit energetic demand and expenditure through reduced RMR, whereas those from cooler habitats may sustain activity despite thermal constraints via increased RMR. Our work highlights the role of temperature in shaping metabolic responses in lizards, giving additional support to the notion that physiology and ecological contexts are intertwined.

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Section: Discussionmentioning

confidence: 99%

Environmental temperature predicts resting metabolic rates in tropidurinae lizards

et al. 2022

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“…The spermatogenic activity, for example, reached its peak after the end of brumation in snakes since it stops or slows down under low environmental temperature (Saint Girons, 1982). During brumation, snakes exhibit a slowing down of all metabolic and physiological activities to maintain an energy balance (Holden et al, 2021). The suitable environmental temperature might also be an important factor for successful incubation of eggs (Cunnington and Cebek, 2005).…”

Section: Discussionmentioning

confidence: 99%

The reproductive cycle of the flowered racer (Platyceps florulentus) from a rural area to the east of the Nile Delta, Egypt.

al.¹

2022

Egypt. J. of Aquatic Biolo. and Fish.

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“…We have previously shown that increasing temperatures affect energy processing and regulation pathways (e.g., glucose, insulin, corticosterone) and that individuals adjust their physiology to deliver O 2 to tissues to maintain metabolic competence (Gangloff et al, 2016). Given this, it is possible that under normal temperatures (within preferred activity range),

{\dot{V}}_{{normalO}_{2}}

is driven by kinetics, but at thermal extremes, rates of respiration are modulated by intrinsic mechanisms, such as hormonal control (Holden et al, 2021). Significant variation in mitochondrial properties and performance (e.g., oxidation, phosphorylation, reactive oxygen species production) may occur across tissue types (Brown et al, 2012; Hulbert et al, 2006; Salin, Auer, Anderson, et al, 2016), which in turn has consequences for organismal metabolic rate.…”

Section: Discussionmentioning

confidence: 99%

“…Measures of the stable carbon isotope composition of breath (reported as δ 13 C of carbon dioxide, CO 2 ) can be used to test for the thermal dependence of fuel selection, as respired CO 2 is a direct byproduct of metabolism, and because the organic compounds from which CO 2 is derived differ characteristically in their δ 13 C values (Hatch et al, 2002; McCue & Welch, 2015; Welch et al, 2016). While relevant to all life, ectotherms that experience long periods of dormancy (e.g., brumation, aestivation) in response to environmental conditions must be capable of physiologically accommodating a broad range of temperatures to maintain organismal functionality (Holden et al, 2021; Williams et al, 2012; Wilsterman et al, 2020). Thus, animals may experience increased mortality if variability in their thermal conditions accelerates the pace of energy usage (Williams et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Temperature‐dependence of metabolism and fuel selection from cells to whole organisms

et al. 2021

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Temperature affects nearly every aspect of how organisms interact with and are constrained by their environment. Measures of organismal energetics, such as metabolic rate, are highly temperature‐dependent and governed through temperature effects on rates of biochemical reactions. Characterizing the relationships among levels of biological organization can lend insight into how temperature affects whole‐organism function. We tested the temperature dependence of cellular oxygen consumption and its relationship to whole‐animal metabolic rate in garter snakes (Thamnophis elegans). Additionally, we tested whether thermal responses were linked to shifts in the fuel source oxidized to support metabolism with the use of carbon stable isotopes. Our results demonstrate temperature dependence of metabolic rates across levels of biological organization. Cellular (basal, adenosine triphosphate‐linked) and whole‐animal rates of respiration increased with temperature but were not correlated within or among individuals, suggesting that variation in whole‐animal metabolic rates is not due simply to variation at the cellular level, but rather other interacting factors across scales of biological organization. Counter to trends observed during fasting, elevated temperature did not alter fuel selection (i.e., natural‐abundance stable carbon isotope composition in breath, δ13Cbreath). This consistency suggests the maintenance and oxidation of a single fuel source supporting metabolism across a broad range of metabolic demands.

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Surviving winter: Physiological regulation of energy balance in a temperate ectotherm entering and exiting brumation

Cited by 23 publications

References 85 publications

Environmental temperature predicts resting metabolic rates in tropidurinae lizards

Environmental temperature predicts resting metabolic rates in tropidurinae lizards

The reproductive cycle of the flowered racer (Platyceps florulentus) from a rural area to the east of the Nile Delta, Egypt.

Temperature‐dependence of metabolism and fuel selection from cells to whole organisms

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