Thermal acclimatisation to heatwave conditions is rapid but sex-specific in wild zebra finches.

Under climate change, increasing air temperature average and variability pose substantial thermal challenges to animals. While plasticity in thermoregulatory traits could potentially attenuate this impact, whether thermal acclimatisation can occur quickly enough to track weather variability in hot climates is unknown in any endotherm, and sex differences have never been tested. We investigated acclimatisation responsiveness of male and female wild zebra finches to short-term (< 2 weeks) summer temperature fluctuations in the Australian desert. Hotter weather before respirometry trials triggered a typical acclimatisation response (especially at chamber temperature Tchamb ≥ 40). However, acclimatisation occurred remarkably rapidly: metabolic rate responded within just one day, while body temperature (Tb) and evaporative cooling capacity (EHL/MHP) were best predicted by weather on the trial day; whereas evaporative water loss responded more slowly (1 week). Nonetheless, rapid acclimatisation only occurred in males, and females had higher Tb and lower EHL/MHP than males, potentially increasing hyperthermia risk. Furthermore, acclimatisation did not translate into greater acute heat tolerance (i.e. ability to tolerate Tchamb = 46 °C). Our results therefore reveal surprisingly rapid acclimatisation and even anticipatory adjustments to heat. However, with no changes in acute heat tolerance, and in females, phenotypic flexibility may provide only limited buffering against the detrimental impact of heatwaves.

A prenatal acoustic signal of heat affects thermoregulation capacities at adulthood in an arid-adapted bird.

Understanding animal physiological adaptations for tolerating heat, and the causes of inter-individual variation, is key for predicting climate change impacts on biodiversity. Recently, a novel mechanism for transgenerational heat adaptation was identified in a desert-adapted bird, where parents acoustically signal hot conditions to embryos. Prenatal exposure to "heat-calls" adaptively alters zebra finch development and their thermal preferences in adulthood, suggesting a long-term shift towards a heat-adapted phenotype. However, whether such acoustic experience improves long-term thermoregulatory capacities is unknown. We measured metabolic rate (MR), evaporative water loss (EWL) and body temperature in adults exposed to a stepped profile of progressively higher air temperatures (Ta) between 27 and 44 °C. Remarkably, prenatal acoustic experience affected heat tolerance at adulthood, with heat-call exposed individuals more likely to reach the highest Ta in morning trials. This was despite MR and EWL reaching higher levels at the highest Ta in heat-call individuals, partly driven by a stronger metabolic effect of moderate activity. At lower Ta, however, heat-call exposed individuals had greater relative water economy, as expected. They also better recovered mass lost during morning trials. We therefore provide the first evidence that prenatal acoustic signals have long-term consequences for heat tolerance and physiological adaptation to heat.

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

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.

Vocal panting: a novel thermoregulatory mechanism for enhancing heat tolerance in a desert-adapted bird.

Animals thriving in hot deserts rely on extraordinary adaptations and thermoregulatory capacities to cope with heat. Uncovering such adaptations, and how they may be favoured by selection, is essential for predicting climate change impacts. Recently, the arid-adapted zebra finch was discovered to program their offspring's development for heat, by producing 'heat-calls' during incubation in hot conditions. Intriguingly, heat-calls always occur during panting; and, strikingly, avian evaporative cooling mechanisms typically involve vibrating an element of the respiratory tract, which could conceivably produce sound. Therefore, we tested whether heat-call emission results from a particular thermoregulatory mechanism increasing the parent's heat tolerance. We repeatedly measured resting metabolic rate, evaporative water loss (EWL) and heat tolerance in adult wild-derived captive zebra finches (n = 44) at increasing air temperatures up to 44 °C. We found high within-individual repeatability in thermoregulatory patterns, with heat-calling triggered at an individual-specific stage of panting. As expected for thermoregulatory mechanisms, both silent panting and heat-calling significantly increased EWL. However, only heat-calling resulted in greater heat tolerance, demonstrating that "vocal panting" brings a thermoregulatory benefit to the emitter. Our findings therefore not only improve our understanding of the evolution of passerine thermal adaptations, but also highlight a novel evolutionary precursor for acoustic signals.

Avian mortality risk during heat waves will increase greatly in arid Australia during the 21st century.

Intense heat waves are occurring more frequently, with concomitant increases in the risk of catastrophic avian mortality events via lethal dehydration or hyperthermia. We quantified the risks of lethal hyperthermia and dehydration for 10 Australian arid-zone avifauna species during the 21st century, by synthesizing thermal physiology data on evaporative water losses and heat tolerance limits. We evaluated risks of lethal hyperthermia or exceedance of dehydration tolerance limits in the absence of drinking during the hottest part of the day under recent climatic conditions, compared to those predicted for the end of this century across Australia. Increases in mortality risk via lethal dehydration and hyperthermia vary among the species modelled here but will generally increase greatly, particularly in smaller species (~10-42 g) and those inhabiting the far western parts of the continent. By 2100 CE, zebra finches' potential exposure to acute lethal dehydration risk will reach ~ 100 d y-1 in the far northwest of Australia and will exceed 20 d y-1 over > 50% of this species' current range. Risks of dehydration and hyperthermia will remain much lower for large non-passerines such as crested pigeons. Risks of lethal hyperthermia will also increase substantially for smaller species, particularly if they are forced to visit exposed water sources at very high air temperatures to avoid dehydration. An analysis of atlas data for zebra finches suggests that population declines associated with very hot conditions are already occurring in the hottest areas. Our findings suggest that the likelihood of persistence within current species ranges, and the potential for range shifts, will become increasingly constrained by temperature and access to drinking water. Our model adds to an increasing body of literature suggesting that arid environments globally will experience considerable losses of avifauna and biodiversity under unmitigated climate change scenarios.

Pigeon odor varies with experimental exposure to trace metal pollution.

Trace metals are chemical pollutants that have well-known noxious effects on wildlife and that are current major environmental issues in urban habitats. Previous studies have demonstrated their negative (e.g. lead) or positive (e.g. zinc) effects on body condition, immunity and reproductive success. Because of their effects on condition, trace metals are likely to influence the production of condition-dependent ornaments. The last decade has revealed that bird odors, like mammal odors, can convey information on individual quality and might be used as secondary sexual ornaments. Here, we used solid-phase microextraction headspace sampling with gas chromatography-mass spectrometry to investigate whether plumage scent varied with experimental supplementation in lead and/or zinc in feral pigeons. Zinc supplementation (alone or in combination with lead) changed the proportion of several volatiles, including an increase in the proportion of hydroxy-esters. The production of these esters, that most likely originate from preen gland secretions, may be costly and might thus be reduced by stress induced by zinc deficiency. Although lead is known to negatively impact pigeon condition, it did not statistically affect feather scent, despite most of the volatiles that increased with zinc exposure tended to be decreased in lead-supplemented pigeons. Further studies should evaluate the functions of plumage volatiles to predict how trace metals can impact bird fitness.

Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping.

Sound is arguably the external cue most accessible to embryos of many species, and as such may constitute an unrivalled source of early information. Recent evidence shows that prenatal sounds, similarly to maternal effects, may shape developmental trajectories. Establishing whether parental vocalisations are signals directed at embryos, or parental cues on which embryos eavesdrop, can elucidate whether parents or embryos control developmental outcomes. Prenatal exposure to a characteristic heat-related parental call was recently shown to alter zebra finch growth and fitness. Here, we test the ecological context of this behaviour in the wild, and assess the information value and specificity of this vocalisation for an embryonic audience. We show that wild zebra finches also produce this characteristic call, only at high temperatures. In addition, in the lab, we demonstrate experimentally that calling is specifically triggered by high air temperatures, can occur without an embryonic audience, and importantly, is predicted by individuals' body mass. Overall, our findings reveal a specialised heat vocalisation that enables embryonic eavesdropping, by indicating high ambient temperatures, and parents' capacity to cope with such conditions. This challenges the traditional view of embryos as passive agents of their development, and opens exciting research avenues on avian adaptation to extreme heat.