Salcedo, M. K. | bioRxiv Science

bioRxiv2021

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

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.

physiology↗

bioRxiv2018

Size, shape and structure of insect wings

The size, shape and structure of insect wings are intimately linked to their ability to fly. However, there are few systematic studies of the variability of the natural patterns in wing morphology across insects. We assemble a comprehensive dataset of insect wings and analyze their morphology using topological and geometric notions in terms of i) wing size and contour shape, ii) vein geometry and topology, and iii) shape and distribution of wing membrane domains. These morphospaces are a first-step in defining the diversity of wing patterns across insect orders and set the stage for investigating their functional consequences.

evolutionary biology↗

bioRxiv2017

Collective mechanical adaptation of honeybee swarms

Honeybee Apis mellifera swarms form clusters made solely of bees attached to each other, forming pendant structures on tree branches (1). These clusters can be hundreds of times the size of a single organism. How these structures are stably maintained under the influence of static gravity and dynamic stimuli (e.g. wind) is unknown. To address this, we created pendant conical clusters attached to a board that was shaken with varying amplitude, frequency and total duration. Our observations show that horizontally shaken clusters spread out to form wider, flatter cones, i.e. the cluster adapts to the dynamic loading conditions, but in a reversible manner - when the loading is removed, the cluster recovers its original shape, slowly. Measuring the response of a cluster to a sharp pendular excitation before and after it adapted shows that the flattened cones deform less and relax faster than the elongated ones, i.e. they are more stable mechanically. We use particle-based simulations of a passive assemblage to suggest a behavioral hypothesis that individual bees respond to local variations in strain. This behavioral response improves the collective stability of the cluster as a whole at the expense of increasing the average mechanical burden experienced by the individual. Simulations using this rule explain our observations of adaptation to horizontal shaking. The simulations also suggest that vertical shaking will not lead to significant differential strains and thus no adaptation. To test this, we shake the cluster vertically and find that indeed there is no response to this stimulus. Altogether, our results show how an active, functional super-organism structure can respond adaptively to dynamic mechanical loading by changing its morphology to achieve better load sharing.

animal behavior and cognition↗