“…We predicted that (i) if prenatal programming of mitochondrial function by heat-calls is aimed at reducing heat production, mitochondrial efficiency would be higher in heat-call exposed birds. Indeed, in addition to reducing leak-related heat production, high mitochondrial efficiency, by lowering food requirements [ 13 ], would decrease the amount of heat generated by food digestion (heat-increment of feeding [ 43 , 44 ]). Alternatively, or in addition, (ii) if the adaptive benefits of heat-call exposure stem from reducing the detrimental physiological impact of heat, heat-call individuals may increase LEAK at very high temperatures to decrease oxidative damage.…”
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.
“…We predicted that (i) if prenatal programming of mitochondrial function by heat-calls is aimed at reducing heat production, mitochondrial efficiency would be higher in heat-call exposed birds. Indeed, in addition to reducing leak-related heat production, high mitochondrial efficiency, by lowering food requirements [ 13 ], would decrease the amount of heat generated by food digestion (heat-increment of feeding [ 43 , 44 ]). Alternatively, or in addition, (ii) if the adaptive benefits of heat-call exposure stem from reducing the detrimental physiological impact of heat, heat-call individuals may increase LEAK at very high temperatures to decrease oxidative damage.…”
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.
“…The average linear decrease in potential greater glider population density from decreasing climatic suitability was unrelated to the initial amount and spatial arrangement of the high-quality feeding landscapes we used to test these effects. The observed population decline related to climate and independent of habitat availability has been observed on worldwide biodiversity (Mantyka-Pringle, Martin, & Rhodes, 2012) and was for example reported for greater gliders (Smith & Smith, 2020;Wagner et al, 2020), butterflies (Parmesan et al, 1999) Continuous unsuitable climatic conditions in the form of high ambient temperatures and low water availability will negatively affect the greater glider's ability to forage, reproduce, and persist in the landscape (Foley, Kehl, Nagy, Kaplan, & Borsboom, 1990;Kavanagh & Lambert, 1990;Rübsamen et al, 1984;Youngentob, Lindenmayer, Marsh, Krockenberger, & Foley, 2021).…”
Wildlife can persist in a range of landscape configurations, but population densities can vary due to resource availability. Resources and environmental conditions shaping habitat suitability may be spatially dispersed or clumped, which can drive habitat availability. We explored how spatial configuration and aggregation of favorable feeding resources and climatic conditions affect populations of the greater glider (Petauroides volans), an arboreal marsupial in
“…Foraging behavior. To test the hypothesis that foraging behavior will decline with increasing heat load (Youngentob et al, 2021), we constructed two separate models, with rate of prey capture attempts and distance flown to obtain prey as response variables. In each model we included the following fixed effects: air temperature and solar radiation (contributors to heat load; Mitchell et al, 2018), wind speed (because wind reduces heat load due to enhanced cooling; Wolf and Walsberg, 1996) and two-way interactions between these weather variables.…”
Section: Statistical Modelsmentioning
confidence: 99%
“…Air temperatures that exceed body temperature also result in heat gain, which endotherms avoid by using cooler microhabitats (Williams et al, 1999;Walde et al, 2009;Carroll et al, 2015;Ruth et al, 2020) but this strategy relies upon thermal heterogeneity within the organism's environment. Behaviors that curtail metabolic heat production, such as inactivity and fasting, also reduce heat gain (Beale et al, 2018) but may adversely impact energy balance (Youngentob et al, 2021).…”
Section: Introductionmentioning
confidence: 99%
“…Many thermoregulatory behaviors cannot simply be "scaled up" in response to increasing temperature because behaviors that facilitate dry heat loss in moderate heat are maladaptive (promoting heat gain) once environmental temperatures become extreme. Additionally, the costs associated with thermoregulatory behaviors, such as dehydration risk from panting or sweating, or loss of body condition from changed foraging patterns, may become untenable with greater heat exposure (Albright et al, 2017;Cunningham et al, 2021;Youngentob et al, 2021). Finally, many thermoregulatory behaviors are dependent upon the thermal heterogeneity of an organism's environment, yet anthropogenic environmental change can alter the thermal profile of habitat, reducing the availability of critical thermally buffered microsites (Chen et al, 1999;Neel and McBrayer, 2018).…”
Anthropogenic climate change is increasing the frequency and intensity of heat waves, thereby threatening biodiversity, particularly in hot, arid regions. Although free-ranging endotherms can use behavioral thermoregulation to contend with heat, it remains unclear to what degree behavior can buffer organisms from unprecedented temperatures. Thermoregulatory behaviors that facilitate dry heat loss during moderate heat become maladaptive once environmental temperatures exceed body temperature. Additionally, the costs associated with behavioral thermoregulation may become untenable with greater heat exposure, and effective cooling may be dependent upon the availability of specific microhabitats. Only by understanding the interplay of these three elements (responses, costs and habitat) can we hope to accurately predict how heat waves will impact wild endotherms. We quantified the thermoregulatory behaviors and microhabitat use of a small passerine, the Jacky Winter (Microeca fascinans), in the mallee woodland of SE Australia. At this location, the annual number of days ≥ 42°C has doubled over the last 25 years. The birds’ broad repertoire of behavioral responses to heat was nuanced and responsive to environmental conditions, but was associated with reduced foraging effort and increased foraging costs, accounting for the loss of body condition that occurs at high temperatures. By measuring microsite surface temperatures, which varied by up to 35°C at air temperatures > 44°C, we found that leaf-litter coverage and tree size were positively correlated with thermal buffering. Large mallee eucalypts were critical to the birds’ response to very high temperatures, providing high perches that facilitated convective cooling, the coolest tree-base temperatures and the greatest prevalence of tree-base crevices or hollows that were used as refuges at air temperatures > 38°C. Tree-base hollows, found only in large mallees, were cooler than all other microsites, averaging 2°C cooler than air temperature. Despite the plasticity of the birds’ response to heat, 29% of our habituated study population died when air temperatures reached a record-breaking 49°C, demonstrating the limits of behavioral thermoregulation and the potential vulnerability of organisms to climate change.
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