Abstract
The wings of Lepidoptera contain a matrix of living cells whose function requires appropriate temperatures. However, given their small thermal capacity, wings can overheat rapidly in the sun. Here we analyze butterfly wings across a wide range of simulated environmental conditions, and find that regions containing living cells are maintained at cooler temperatures. Diverse scale nanostructures and non-uniform cuticle thicknesses create a heterogeneous distribution of radiative cooling that selectively reduces the temperature of structures such as wing veins and androconial organs. These tissues are supplied by circulatory, neural and tracheal systems throughout the adult lifetime, indicating that the insect wing is a dynamic, living structure. Behavioral assays show that butterflies use wings to sense visible and infrared radiation, responding with specialized behaviors to prevent overheating of their wings. Our work highlights the physiological importance of wing temperature and how it is exquisitely regulated by structural and behavioral adaptations.
Highlights
The wings of Lepidoptera contain a matrix of living cells whose function requires appropriate temperatures
Butterfly wings are largely semitransparent in the mid-infrared spectrum, meaning that infrared radiation detected by the camera is only partially contributed by the wings, leading to errors in estimating the temperature over the entire wing
Using a robust ecological model species, Vanessa cardui[38,39], we show that circulatory and tracheal systems remain active in the wing veins throughout the entire adult stage
Summary
The wings of Lepidoptera contain a matrix of living cells whose function requires appropriate temperatures. In a pioneering early work, Wasserthal and Schmitz[36] implanted thermistors into wings and other parts of butterflies and heated the insects with a calibrated light beam This technique demonstrated that antennae, wings and thorax heat up at different rates and reach specific excess temperatures. We find that wings are extremely heterogeneous in their thermodynamic properties, with wing veins and other living parts of the wing being cooler than inter-vein regions under solar radiation This is achieved via elevated thermal emissivity due to a thickened chitinous layer and specialized nanostructuring of their scales such that they more efficiently dissipate heat through thermal radiation. Even heating by a small localized laser spot is sufficient to elicit displacement behaviors, and there is a tight window of trigger temperatures across families
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