Seasonal Metabolic Acclimatization Varies in Direction and Magnitude among Populations of an Afrotropical Passerine Bird

Noakes, Matthew J.; Wolf, Blair O.; McKechnie, Andrew E.

doi:10.1086/689030

Cited by 26 publications

(55 citation statements)

References 70 publications

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“…Here, we refer to any physiological adjustment of an organism in response to an environmental stimulus resulting in the improved ability of that organism to cope with its changing environment as physiological adaptation (Boratynski et al, 2017;Brinkmann et al, 2014;Rymer et al, 2016). However, physiological adaptation is also often called acclimatization (Noakes et al, 2017;Petit et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases

Rimbach

Pillay

Schradin

2016

Journal of Experimental Biology

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In response to variation in food availability and ambient temperature (T a ), many animals show seasonal adaptations in their physiology. Laboratory studies showed that thyroid hormones are involved in the regulation of metabolism, and their regulatory function is especially important when the energy balance of an individual is compromised. However, little is known about the relationship between thyroid hormones and metabolism in free-living animals and animals inhabiting seasonal environments. Here, we studied seasonal changes in triiodothyronine (T 3 ) levels, resting metabolic rate (RMR) and two physiological markers of energy balance (blood glucose and ketone bodies) in 61 free-living African striped mice (Rhabdomys pumilio) that live in an semi-arid environment with food shortage during the dry season. We predicted a positive relationship between T 3 levels and RMR. Further, we predicted higher T 3 levels, blood glucose levels and RMR, but lower ketone body concentrations, during the moist season when food availability is high compared with summer when food availability is low. RMR and T 3 levels were negatively related in the moist season but not in the dry season. Both RMR and T 3 levels were higher in the moist than in the dry season, and T 3 levels increased with increasing food availability. In the dry season, blood glucose levels were lower but ketone body concentrations were higher, indicating a change in substrate use. Seasonal adjustments in RMR and T 3 levels permit a reduction of energy expenditure when food is scarce, and reflect an adaptive response to reduced food availability in the dry season.

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Section: Introductionmentioning

confidence: 99%

Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases

Rimbach

Pillay

Schradin

2016

Journal of Experimental Biology

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“…Here we suggest that plasticity of thermal performance curves is an ancestral trait that has been maintained in endotherms to buffer physiological reaction rates from variation in core body or tissue temperatures. Note that there is an important distinction between acclimation of metabolic rates to increase heat production in response to cold environmental temperatures (e.g., Boratyński et al, 2017 ; Noakes et al, 2017 ), and the plasticity of performance curves we are suggesting (Figure 1A ). The former serves to maintain body temperatures in variable climates, and the latter optimizes reaction rates when tissue temperatures change despite adjustments of metabolic heat production.…”

Section: Introductionmentioning

confidence: 77%

Plasticity of Performance Curves Can Buffer Reaction Rates from Body Temperature Variation in Active Endotherms

Seebacher

Little

2017

Front. Physiol.

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Endotherms regulate their core body temperature by adjusting metabolic heat production and insulation. Endothermic body temperatures are therefore relatively stable compared to external temperatures. The thermal sensitivity of biochemical reaction rates is thought to have co-evolved with body temperature regulation so that optimal reaction rates occur at the regulated body temperature. However, recent data show that core body temperatures even of non-torpid endotherms fluctuate considerably. Additionally, peripheral temperatures can be considerably lower and more variable than core body temperatures. Here we discuss whether published data support the hypothesis that thermal performance curves of physiological reaction rates are plastic so that performance is maintained despite variable body temperatures within active (non-torpid) endotherms, and we explore mechanisms that confer plasticity. There is evidence that thermal performance curves in tissues that experience thermal fluctuations can be plastic, although this question remains relatively unexplored for endotherms. Mechanisms that alter thermal responses locally at the tissue level include transient potential receptor ion channels (TRPV and TRPM) and the AMP-activated protein kinase (AMPK) both of which can influence metabolism and energy expenditure. Additionally, the thermal sensitivity of processes that cause post-transcriptional RNA degradation can promote the relative expression of cold-responsive genes. Endotherms can respond to environmental fluctuations similarly to ectotherms, and thermal plasticity complements core body temperature regulation to increase whole-organism performance. Thermal plasticity is ancestral to endothermic thermoregulation, but it has not lost its selective advantage so that modern endotherms are a physiological composite of ancestral ectothermic and derived endothermic traits.

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“…Only relatively recently have workers investigated seasonal adjustments in BMR and M sum of birds inhabiting lower latitudes with milder winters and hotter summers, but the limited available data suggest more variability in the magnitude and direction of metabolic adjustments compared with that of their high-latitude counterparts (reviewed by McKechnie et al, 2015). Intraspecific variation in seasonal metabolic acclimatization has also been reported among populations of two subtropical species, Euplectes orix (van de Ven et al, 2013) and Plocepasser mahali (Noakes et al, 2017;Smit and McKechnie, 2010). A continuum between selection for cold tolerance or energy conservation has been suggested to drive patterns of avian metabolic adjustments in response to fluctuations in minimum T a and food availability, respectively (Smit and McKechnie, 2010), and it is possible that the milder winters at lower latitudes permit greater flexibility in the direction and magnitude of seasonal metabolic acclimatization (McKechnie et al, 2015;Noakes et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…A continuum between selection for cold tolerance or energy conservation has been suggested to drive patterns of avian metabolic adjustments in response to fluctuations in minimum T a and food availability, respectively (Smit and McKechnie, 2010), and it is possible that the milder winters at lower latitudes permit greater flexibility in the direction and magnitude of seasonal metabolic acclimatization (McKechnie et al, 2015;Noakes et al, 2017). This does not necessarily mean subtropical and tropical birds have an inherently greater physiological flexibility than their temperate-zone counterparts, but rather that very low winter T a at high latitudes results in demands for enhanced cold tolerance that simply overwhelm other factors affecting metabolic adjustments (Noakes et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Phenotypic flexibility of metabolic rate and evaporative water loss does not vary across a climatic gradient in an Afrotropical passerine bird

Noakes

McKechnie

2020

Journal of Experimental Biology

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Small birds inhabiting northern temperate and boreal latitudes typically increase metabolic rates during cold winters or acclimation to low air temperatures (Taccl). Recent studies suggest considerable variation in patterns of seasonal metabolic acclimatization in birds from subtropical and tropical regions with milder winters, but there remains a dearth of acclimation studies investigating metabolic flexibility among lower-latitude birds. We used short-term thermal acclimation experiments to investigate phenotypic flexibility in basal metabolic rate (BMR), thermoneutral evaporative water loss (EWL) and summit metabolism (Msum) in three populations of white-browed sparrow-weavers (Plocepasser mahali) along a climatic and aridity gradient. We allocated individuals to one of three Taccl treatments (5 °C, 20 °C and 35 °C; n=11 per population per Taccl) for 28 days, and measured post-acclimation BMR, EWL and Msum using flow-through respirometry. Our data reveal the expected pattern of lower BMR and EWL (∼ 12 % and 25 % lower respectively) in birds at Taccl=35 °C compared to cooler Taccl treatments, as observed in previous acclimation studies on subtropical birds. We found no variation in the reaction norms of BMR and EWL among populations in response to acclimation, suggesting previously documented differences in seasonal BMR acclimatization are the result of phenotypic flexibility. In contrast to higher-latitude species, Msum did not significantly vary in response to thermal acclimation. These findings support the idea that factors other than enhancing cold tolerance may be driving patterns of metabolic variation in subtropical birds.

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Seasonal Metabolic Acclimatization Varies in Direction and Magnitude among Populations of an Afrotropical Passerine Bird

Cited by 26 publications

References 70 publications

Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases

Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases

Plasticity of Performance Curves Can Buffer Reaction Rates from Body Temperature Variation in Active Endotherms

Phenotypic flexibility of metabolic rate and evaporative water loss does not vary across a climatic gradient in an Afrotropical passerine bird

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