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

Anaïs Pessato,Katherine L Buchanan,Andrew E Mckechnie,Mylene M Mariette

doi:10.1038/s41598-020-75909-6

Anaïs Pessato, Katherine L Buchanan + Show 2 more

Open Access

https://doi.org/10.1038/s41598-020-75909-6

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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.

Highlights

Animals thriving in hot deserts rely on extraordinary adaptations and thermoregulatory capacities to cope with heat
Changes in resting metabolic rate (RMR) differed between calling and panting, likely because most individuals had not reached their lowest RMR values by the time they started silent panting, whereas calling onset occurred after RMR had stabilised. Consistent with this interpretation, we found that when restricting analyses to trials where individuals started silent panting at Ta = 40 °C (n = 8 trials for 6 birds), RMR did not change at the onset of panting (LMM: est < 0.01, se = 0.01, p = 0.704)
Our results suggest that vocal panting may correspond to such change in thermoregulation strategy predicted by that study[41], to increase evaporative water loss when individuals are no longer able to maintain a viable Tb via silent panting

Summary

Introduction

Animals thriving in hot deserts rely on extraordinary adaptations and thermoregulatory capacities to cope with heat. Passerines are an evolutionary puzzle: despite being one of the most successful avian evolutionary radiations including in arid environments[20,21], their performance in the heat is constrained by the absence of gular flutter or the capacity for large increases in cutaneous e vaporation[12,22] The reasons why these efficient evaporative cooling pathways are absent in some avian orders, including passerines and parrots, are unclear. In a desert-adapted passerine species, adults were found to emit an unusual vocalisation, triggered by high air temperatures[26,27,28] This “heat-call” occurs both in wild and captive populations of the Zebra finch (Taeniopygia guttata), a common iconic species of the Australian arid interior[29]. We hypothesise that heat-calls may indicate the use of a so-far undescribed thermoregulation mechanism—or “vocal panting”—which may in turn increase individuals’ thermoregulation capacities in the heat

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