Viscous effects and complex local flow behaviors dominate hemolymph circulation in the living wings of locusts

Abstract

An insects living systems - circulation, respiration, and a branching nervous system - extend from the body into the wing.1,2. Hemolypmh circulation in the wing is critical for hydrating tissues, such as the highly elastic resilin3 that enhances wing flexibility, and for supplying nutrients to living systems, including sensory organs such as scent-producing patches, sound-receiving tympana, and wind-sensing sensilla distributed across the wing.4-7During flight, the presence of hemolymph in the wings reduces aerodynamic instabilities like flutter8,9, and faster hemolymph flows are induced by flapping.10 Despite the critical role of hemolymph circulation in maintaining healthy wing function, wings are often considered "lifeless" cuticle, and most measurements remain qualitative or employ coarse, bulk-flow techniques. While pioneering work in the 1960s mapped hemolymph flow direction in 100 insect species,11 half a century later we still only have quantitative measurements of flow within the wings of a few insects. Here, we focused on the North American locust Schistocerca americana, a well-studied agricultural pest species, and performed a detailed, quantitative study of global and local hemolymph flows in the densely venated fore and hind wings, along with key regions in the body and pumping organs. Through high-speed fluorescent microscopy, we measured 800 individual trajectories of neutrally buoyant fluorescent particles that move in sync with hemolymph, in the wings and body of 8 live, resting locusts. Our data show that overall flow within the wings is circuitous, but local flow behavior is highly complex, with three distinct types of flow (pulsatile, continuous, and "leaky") occurring in various combinations in different areas of the wing. We provide the first quantitative measurements of "leaky" flow into wing regions that act as sinuses, where hemolymph flows out of tubular veins and pools within thin membranous regions. We also calculate Peclet, Reynolds, and Womersley numbers, and find that viscous effects dominate flow regimes throughout the wing. Pumping organs and wing regions closest to the body display significantly faster flows and higher Reynolds numbers, but remain within the viscous flow regime. Given the central role of wings in sustaining ecologically important insect behaviors such as pollination, migration, and mating, along with the vast diversity of insect wings seen in nature, this first detailed, quantitative map of hemolymph flows across a wing provides a template for future studies investigating the dynamics of hemolymph flows critical to sustaining wing health among insects.