Avian red blood cell mitochondria produce more heat in winter than in autumn

Nord, Andreas; Metcalfe, Neil B.; Page, Jennifer L.; Huxtable, Anna; McCafferty, Dominic J.; Dawson, Neal J.

doi:10.1096/fj.202100107r

Cited by 36 publications

(54 citation statements)

References 50 publications

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“…Prenatal exposure to heat-calls induced a shift of nestling mitochondrial function towards higher ATP production ( OXPHOS ) and therefore lower FCR L/R and FCR L/ETS under undisturbed in-nest conditions. The prenatal acoustic signal, therefore, had similar impact on mitochondria to that of direct exposure to environmental temperatures in other species [ 26 , 28 , 31 ]. For example, in adults of three tit species, acclimatization to low winter temperatures increased LEAK respiration in RBCs [ 28 ].…”

Section: Discussionmentioning

confidence: 99%

“…LEAK can also reduce the oxidative damage associated with the production of reactive oxygen species (ROS) in mitochondria (‘uncoupling to survive hypothesis' [ 35 ]). This leads to trade-offs between energy production, heat generation and oxidative balance [ 36 ], with LEAK accounting for 20–70% of cellular respiration, or up to 25% of the organismal basal metabolic rate [ 28 , 34 , 37 ]. LEAK proportion and therefore mitochondrial efficiency (inverse to the ratio of LEAK over mitochondrial overall respiration under endogenous ( ROUTINE ) or stimulated ( ETS ) conditions) can differ between species [ 12 ], but also between individuals [ 13 ].…”

Section: Introductionmentioning

confidence: 99%

“…Notably, mitochondrial efficiency may underlie variation in individual quality, including growth performance, since high efficiency reduces the amount of food needed to sustain growth [ 13 ]. Alternatively, variations in mitochondrial efficiency may correspond to differential adaptive strategies [ 10 , 12 ], with, for example, thermal acclimation to cold in fish, mammals and birds [ 28 , 38 , 39 ] increasing the proportion of LEAK respiration. During development, the proportion of LEAK also varies, notably with stress exposure decreasing mitochondrial efficiency [ 11 , 15 ], although no anticipatory adaptive programming has so far been investigated.…”

Section: Introductionmentioning

confidence: 99%

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Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

et al. 2021

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Sound is an essential source of information in many taxa and can notably be used by embryos to programme their phenotypes for postnatal environments. While underlying mechanisms are mostly unknown, there is growing evidence for the involvement of mitochondria—main source of cellular energy (i.e. ATP)—in developmental programming processes. Here, we tested whether prenatal sound programmes mitochondrial metabolism. In the arid-adapted zebra finch, prenatal exposure to ‘heat-calls’—produced by parents incubating at high temperatures—adaptively alters nestling growth in the heat. We measured red blood cell mitochondrial function, in nestlings exposed prenatally to heat- or control-calls, and reared in contrasting thermal environments. Exposure to high temperatures always reduced mitochondrial ATP production efficiency. However, as expected to reduce heat production, prenatal exposure to heat-calls improved mitochondrial efficiency under mild heat conditions. In addition, when exposed to an acute heat-challenge, LEAK respiration was higher in heat-call nestlings, and mitochondrial efficiency low across temperatures. Consistent with its role in reducing oxidative damage, LEAK under extreme heat was also higher in fast growing nestlings. Our study therefore provides the first demonstration of mitochondrial acoustic sensitivity, and brings us closer to understanding the underpinning of acoustic developmental programming and avian strategies for heat adaptation.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

et al. 2021

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“…Even though blood volume represents ∼8-10% of the total volume in birds (Sturkie and Griminger, 1986), it is unknown what proportional contribution blood cells make to the total metabolic rate. Nord et al (2021) reported that coal tits (Periparus ater) and great tits (Parus major) increased their mitochondrial respiration rates and CS activity of RBCs in winter, which may be a response to changes in metabolic demands between seasons. In the following sections, we offer alternative explanations for the observed increases in mass-adjusted BMR and COX activity in RBCs and why it could be associated to the costs of osmotic stress.…”

Section: Energy and Osmoregulatory Adjustmentsmentioning

confidence: 99%

“…One of the unique characteristics of birds and often overlooked by ecological and evolutionary physiologists is the presence of nucleated RBCs with functional mitochondria. This key feature has recently caught the attention of physiologists and the existence of intra and interspecific variation in its function has been observed in a few species (Stier et al, 2013(Stier et al, , 2015(Stier et al, , 2017Nord et al, 2021). Decades ago, some suggested that ATP production in erythrocytes is involved in the maintenance of ion balance (Na and K) between erythrocytes and plasma (Hunter and Hunter, 1957).…”

Section: Changes In Erythrocyte Metabolic Activitymentioning

confidence: 99%

Integrative Physiological Responses to Acute Dehydration in the Rufous-Collared Sparrow: Metabolic, Enzymatic, and Oxidative Traits

et al. 2021

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Predictions indicate that birds worldwide will be affected by global warming and extreme climatic events which is especially relevant for passerines because the diurnal habits, small body size, and high mass-adjusted metabolic rates of this group make it particularly susceptible to increases in temperature and aridity. Some bird species respond to conditions that stress osmoregulation by increasing their rates of energy expenditure, nevertheless, the effect of dehydration on metabolic rates in birds has produced contrasting results. It also remains unknown whether hydration state may cause shifts in tissue-specific metabolic rates or modify tissue oxidative status. We used the rufous-collared sparrow (Zonotrichia capensis), to experimentally test the effect of dehydration on metabolic enzymes in erythrocytes, tissue oxidative status, basal metabolic rate (BMR), and total evaporative water loss. We found a significant increase in mass-adjusted BMR in water restricted (WR) birds compared to control birds (CT). Activity of cytochrome-c-oxidase (COX) in red blood cells (RBCs) was also significantly higher in the WR group relative to the CT group and this activity was positively correlated with mass-adjusted BMR. We found a moderate effect of water restriction on membrane damage of skeletal muscle. In a second set of individuals subjected to the same experimental conditions, lean mass and total water were tightly correlated and decreased by 10 and 12%, respectively, in birds in the WR group relative to the CT group. Decreases in total water and lean mass leads to an increase in mass-adjusted BMR in WR Z. capensis, suggesting that birds may simultaneously increase protein catabolism and production of metabolic water through oxidation. The significant positive relationship between BMR and COX in RBCs is a finding that requires additional research to determine whether erythrocyte metabolism is affected by dehydration per se and or it more generally reflects rates of energy expenditure in birds.

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Metabolic adjustments to winter severity in two geographically separated great tit (Parus major) populations

Pacioni,

Bushuev,

Sentís

et al. 2024

J Exp Zool Pt A

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Understanding the potential limits placed on organisms by their ecophysiology is crucial for predicting their responses to varying environmental conditions. A main hypothesis for explaining avian thermoregulatory mechanisms is the aerobic capacity model, which posits a positive correlation between basal (basal metabolic rate [BMR]) and summit (Msum) metabolism. Most evidence for this hypothesis, however, comes from interspecific comparisons, and the ecophysiological underpinnings of avian thermoregulatory capacities hence remain controversial. Indeed, studies have traditionally relied on between‐species comparisons, although, recently, there has been a growing recognition of the importance of intraspecific variation in ecophysiological responses. Therefore, here, we focused on great tits (Parus major), measuring BMR and Msum during winter in two populations from two different climates: maritime‐temperate (Gontrode, Belgium) and continental (Zvenigorod, Russia). We tested for the presence of intraspecific geographical variation in metabolic rates and assessed the predictions following the aerobic capacity model. We found that birds from the maritime‐temperate climate (Gontrode) showed higher BMR, whereas conversely, great tits from Zvenigorod showed higher levels of Msum. Within each population, our data did not fully support the aerobic capacity model's predictions. We argued that the decoupling of BMR and Msum observed may be caused by different selective forces acting on these metabolic rates, with birds from the continental‐climate Zvenigorod population facing the need to conserve energy for surviving long winter nights (by keeping their BMR at low levels) while simultaneously being able to generate more heat (i.e., a high Msum) to withstand cold spells.

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Avian red blood cell mitochondria produce more heat in winter than in autumn

Cited by 36 publications

References 50 publications

Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

Integrative Physiological Responses to Acute Dehydration in the Rufous-Collared Sparrow: Metabolic, Enzymatic, and Oxidative Traits

Metabolic adjustments to winter severity in two geographically separated great tit (Parus major) populations

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