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

Abstract

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.

Acoustic developmental programming: a mechanistic and evolutionary framework

“…Notably, the father and siblings can provide vibro-acoustic information to embryos directly [7][8][9]46] rather than through differential allocation by the mother [10], and this has implications for sexual conflict and sibling competition (Figure I) [106]. Furthermore, embryos cueing directly on environmental sounds may affect parentoffspring conflict [9,106], even though embryonic eavesdropping may sometimes be key to the evolution of parent-to-embryo signals for acoustic developmental programming [84].…”

“…Alternatively, developmental vibro-acoustic cues can originate directly from behavioral or physiological processes, such as eggshell opening in stinkbugs [39], embryonic heart-beat in reptiles, and breathingassociated clicking sounds in birds (also indicative of developmental stage [44,45,75]). Likewise, zebra finch parental heat-calls are in fact produced by a specialized thermoregulatory mechanism -'vocal panting'which increases emitter tolerance to high temperature extremes [84]. However, Box 3.…”

“…Notably, developmental programming by heat-calls in zebra finches is to date the only known mechanism for transgenerational adaptation to high temperatures in endotherms [7]. If this phenomenon occurs in other passerine species [84], it might reduce the impact of climate change on avian population persistence [88]. Furthermore, anthropogenic noise pollutionthat is typically associated with high levels of vibrationsis well known for impairing acoustic communication in adults [89].…”

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

“…Here, we tested whether adaptive programming of mitochondrial function for high temperatures occurs, through prenatal acoustic signals. In the zebra finch ( Taeniopygia guttata ), parents emit ‘heat-calls’ during incubation at high temperatures [ 40 , 41 ], which improves the caller's thermoregulation capacity [ 42 ]. Embryonic exposure to such heat-calls adaptively alters nestling development, with nestlings being smaller in hot nests, but larger in milder shady conditions, which then improves reproductive success throughout adulthood [ 40 ].…”

How to Stay Cool: Early Acoustic and Thermal Experience Alters Individual Behavioural Thermoregulation in the Heat

“…For inter-individual variation, however, we are aware of only two studies on behavioural thermoregulation. The onset of panting behaviour in zebra finches (Taeniopygia guttata) exposed to a standard increase in air temperature (T air ) in a metabolic chamber is repeatable within individuals, but varies considerably between individuals, with some individuals starting panting at 27 • C, while others do not pant until air temperature reaches 40 • C (Pessato et al, 2020). This suggests that individuals may consistently vary in their thermoregulation strategies.…”