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The thermal performance curve for aerobic metabolism of a flying endotherm.

ABSTRACT: Performance benefits of stable, warm muscles are believed to be important for the evolution of endothermy in mammals, birds and flying insects. However, thermal performance curves have never been measured for a free-flying endotherm, as it is challenging to vary body temperatures of these animals, and maximal flight performance is difficult to elicit. We varied air temperatures and gas densities to manipulate thoracic temperatures of flying honeybees from 29°C to 44°C, with low air densities used to increase flight metabolic rates to maximal values. Honeybees showed a clear thermal performance curve with an optimal temperature of 39°C. Maximal flight metabolic rates increased by approximately 2% per 1°C increase in thoracic temperature at suboptimal thoracic temperatures, but decreased approximately 5% per 1°C increase as the bees continued to heat up. This study provides the first quantification of the maximal metabolic performance benefit of thermoregulation in an endotherm. These data directly support aerobic capacity models for benefits of thermoregulation in honeybees, and suggest that improved aerobic capacity probably contributes to the multiple origins of endothermic heterothermy in bees and other insects.

SUBMITTER: Glass JR

PROVIDER: S-EPMC9382204 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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The thermal performance curve for aerobic metabolism of a flying endotherm.

Glass Jordan R JR Harrison Jon F JF

Proceedings. Biological sciences 20220817 1981

Performance benefits of stable, warm muscles are believed to be important for the evolution of endothermy in mammals, birds and flying insects. However, thermal performance curves have never been measured for a free-flying endotherm, as it is challenging to vary body temperatures of these animals, and maximal flight performance is difficult to elicit. We varied air temperatures and gas densities to manipulate thoracic temperatures of flying honeybees from 29°C to 44°C, with low air densities use ...[more]

PMID: 35975442

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Project description:According to the "aerobic capacity model," endothermy in birds and mammals evolved as a result of natural selection favoring increased persistent locomotor activity, fuelled by aerobic metabolism. However, this also increased energy expenditure even during rest, with the lowest metabolic rates occurring in the thermoneutral zone (TNZ) and increasing at ambient temperatures (Ta) below and above this range, depicted by the thermoregulatory curve. In our experimental evolution system, four lines of bank voles (Myodes glareolus) have been selected for high swim-induced aerobic metabolism and four unselected lines have been maintained as a control. In addition to a 50% higher rate of oxygen consumption during swimming, the selected lines have also evolved a 7.3% higher mass-adjusted basal metabolic rate. Therefore, we asked whether voles from selected lines would also display a shift in the thermoregulatory curve and an increased body temperature (Tb) during exposure to high Ta. To test these hypotheses we measured the RMR and Tb of selected and control voles at Ta from 10 to 34°C. As expected, RMR within and around the TNZ was higher in selected lines. Further, the Tb of selected lines within the TNZ was greater than the Tb of control lines, particularly at the maximum measured Ta of 34°C, suggesting that selected voles are more prone to hyperthermia. Interestingly, our results revealed that while the slope of the thermoregulatory curve below the lower critical temperature (LCT) is significantly lower in the selected lines, the LCT (26.1°C) does not differ. Importantly, selected voles also evolved a higher maximum thermogenesis, but thermal conductance did not increase. As a consequence, the minimum tolerated temperature, calculated from an extrapolation of the thermoregulatory curve, is 8.4°C lower in selected (-28.6°C) than in control lines (-20.2°C). Thus, selection for high aerobic exercise performance, even though operating under thermally neutral conditions, has resulted in the evolution of increased cold tolerance, which, under natural conditions, could allow voles to inhabit colder environments. Further, the results of the current experiment support the assumptions of the aerobic capacity model of the evolution of endothermy.

Project description:Equatorial fishes, and the critically important fisheries based on them, are thought to be at-risk from climate warming because the fishes have evolved in a relatively aseasonal environment and possess narrow thermal tolerance windows that are close to upper thermal limits. We assessed survival, growth, aerobic performance and critical thermal maxima (CTmax) following acute and 21 d exposures to temperatures up to 4°C higher than current maxima for six species of freshwater fishes indigenous to tropical countries and of importance for human consumption. All six species showed 1.3-1.7°C increases in CTmax with a 4°C rise in acclimation temperature, values which match up well with fishes from other climatic regions, and five species had survival >87% at all temperatures over the treatment period. Specific growth rates varied among and within each species in response to temperature treatments. For all species, the response of resting metabolic rate (RMR) was consistently more dynamic than for maximum metabolic rate, but in general both acute temperature exposure and thermal acclimation had only modest effects on aerobic scope (AS). However, RMR increased after warm acclimation in 5 of 6 species, suggesting incomplete metabolic compensation. Taken in total, our results show that each species had some ability to perform at temperatures up to 4°C above current maxima, yet also displayed certain areas of concern for their long-term welfare. We therefore suggest caution against the overly broad generalization that all tropical freshwater fish species will face severe challenges from warming temperatures in the coming decades and that future vulnerability assessments should integrate multiple performance metrics as opposed to relying on a single response metric. Given the societal significance of inland fisheries in many parts of the tropics, our results clearly demonstrate the need for more species-specific studies of adaptive capacity to climate change-related challenges.

Dataset Information

The thermal performance curve for aerobic metabolism of a flying endotherm.

Publications

The thermal performance curve for aerobic metabolism of a flying endotherm.

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