skip to main content

Title: Walking Drosophila navigate complex plumes using stochastic decisions biased by the timing of odor encounters
When walking along a city street, you might encounter a range of scents and odors, from the smells of coffee and food to those of exhaust fumes and garbage. The odors are swept to your nose by air currents that move scents in two different ways. They carry them downwind in a process called advection, but they also mix them chaotically with clean air in a process called turbulence. What results is an odor plume: a complex ever-changing structure resembling the smoke rising from a chimney. Within a plume, areas of highly concentrated odor particles break up into smaller parcels as they travel further from the odor source. This means that the concentration of the odor does not vary along a smooth gradient. Instead, the odor arrives in brief and unpredictable bursts. Despite this complexity, insects are able to use odor plumes with remarkable ease to navigate towards food sources. But how do they do this? Answering this question has proved challenging because odor plumes are usually invisible. Over the years, scientists have come up with a number of creative solutions to this problem, including releasing soap bubbles together with odors, or using wind tunnels to generate simpler, straight plumes more » in known locations. These approaches have shown that when insects encounter an odor, they surge upwind towards its source. When they lose track of the odor, they cast themselves crosswind in an effort to regain contact. But this does not explain how insects are able to navigate irregular odor plumes, in which both the timing and location of the odor bursts are unpredictable. Demir, Kadakia et al. have now bridged this gap by showing how fruit flies are attracted to smoke, an odorant that is also visible. By injecting irregular smoke plumes into a custom-built wind tunnel, and then imaging flies as they walked through it, Demir, Kadakia et al. showed that flies make random halts when navigating the plume. Each time they stop, they use the timing of the odor bursts reaching them to decide when to start moving again. Rather than turning every time they detect an odor, flies initiate turns at random times. When several odor bursts arrive in a short time, the flies tend to orient these turns upwind rather than downwind. Flies therefore rely on a different strategy to navigate irregular odor plumes than the ‘surge and cast’ method they use for regular odor streams. Successful navigation through complex irregular plumes involves a degree of random behavior. This helps the flies gather information about an unpredictable environment as they search for the source of the odor. These findings may help to understand how other insects use odor to navigate in the real world, for example, how mosquitoes track down human hosts. « less
Authors:
; ; ; ;
Award ID(s):
1755494
Publication Date:
NSF-PAR ID:
10216468
Journal Name:
eLife
Volume:
9
ISSN:
2050-084X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Insects rely on their olfactory system to forage, prey, and mate. They can sense odorant plumes emitted from sources of their interests with their bilateral odorant antennae, and track down odor sources using their highly efficient flapping-wing mechanism. The odor-tracking process typically consists of two distinct behaviors: surging upwind and zigzagging crosswind. Despite the extensive numerical and experimental studies on the flying trajectories and wing flapping kinematics during odor tracking flight, we have limited understanding of how the flying trajectories and flapping wings modulate odor plume structures. In this study, a fully coupled three-way numerical solver is developed, which solves the 3D Navier-Stokes equations coupled with equations of motion for the passive flapping wings, and the odorant convection-diffusion equation. This numerical solver is applied to investigate the unsteady flow field and the odorant transport phenomena of a fruit fly model in both surging upwind and zigzagging crosswind cases. The unsteady flow generated by flapping wings perturbs the odor plume structure and significantly impacts the odor intensity at the olfactory receptors (i.e., antennae). During zigzagging crosswind flight, the differences in odor perception time and peak odor intensity at the receptors potentially help create stereo odorant mapping to track odor source.more »Our simulation results will provide new insights into the mechanism of how fruit flies perceive odor landscape and inspire the future design of odor-guided micro aerial vehicles (MAVs) for surveillance and detection missions.

    « less
  2. Despite the ecological importance of long-distance dispersal in insects, its mechanistic basis is poorly understood in genetic model species, in which advanced molecular tools are readily available. One critical question is how insects interact with the wind to detect attractive odor plumes and increase their travel distance as they disperse. To gain insight into dispersal, we conducted release-and-recapture experiments in the Mojave Desert using the fruit fly,Drosophila melanogaster. We deployed chemically baited traps in a 1 km radius ring around the release site, equipped with cameras that captured the arrival times of flies as they landed. In each experiment, we released between 30,000 and 200,000 flies. By repeating the experiments under a variety of conditions, we were able to quantify the influence of wind on flies’ dispersal behavior. Our results confirm that even tiny fruit flies could disperse ∼12 km in a single flight in still air and might travel many times that distance in a moderate wind. The dispersal behavior of the flies is well explained by an agent-based model in which animals maintain a fixed body orientation relative to celestial cues, actively regulate groundspeed along their body axis, and allow the wind to advect them sideways. The modelmore »accounts for the observation that flies actively fan out in all directions in still air but are increasingly advected downwind as winds intensify. Our results suggest that dispersing insects may strike a balance between the need to cover large distances while still maintaining the chance of intercepting odor plumes from upwind sources.

    « less
  3. Abstract

    Insects rely on their olfactory system to forage, prey, and mate. They can sense odorant plumes emitted from sources of their interests with their bilateral odorant antennae, and track down odor sources using their highly efficient flapping-wing mechanism. The odor-tracking process typically consists of two distinct behaviors: surging upwind at higher velocity and zigzagging crosswind at lower velocity. Despite extensive numerical and experimental studies on odor guided flight in insects, we have limited understandings on the effects of flight velocity on odor plume structure and its associated odor perception. In this study, a fully coupled three-way numerical solver is developed, which solves the 3D Navier-Stokes equations coupled with equations of motion for the passive flapping wings, and the odorant convection-diffusion equation. This numerical solver is applied to resolve the unsteady flow field and the odor plume transport for a fruit fly model at different flight velocities in terms of reduced frequency. Our results show that the odor plume structure and intensity are strong related to reduced frequency. At smaller reduced frequency (larger forward velocity), odor plume is pushed up during downstroke and draw back during upstroke. At larger reduced frequency (smaller forward velocity), the flapping wings induce a shield-likemore »air flow around the antennae which may greatly increase the odor sampling range. Our finding may explain why flight velocity is important in odor guided flight.

    « less
  4. Insects rely on their olfactory system to forage, prey, and mate. They can sense odor emitted from sources of their interest, use their highly efficient flapping-wing mechanism to follow odor trails, and track down odor sources. During such an odor-guided navigation, flapping wings not only serve as propulsors for generating lift and maneuvering, but also actively draw odors to the antennae via wing-induced flow. This helps enhance olfactory detection by mimicking “sniffing” in mammals. However, due to a lack of quantitative measuring tools and empirical evidence, we have a poor understanding of how the induced flow generated by flapping kinematics affects the odor landscape. In the current study, we designed a canonical simulation to investigate the impact of flapping motion on the odor plume structures. A sphere was placed in the upstream and releases odor at the Schmidt number of 0.71 and Reynolds number of 200. In the downstream, an ellipsoidal airfoil underwent a pitch-plunge motion. Both two- and three-dimensional cases are simulated with Strouhal number of 0.9. An in-house immersed-boundary-method-based CFD solver was applied to investigate the effects of flapping locomotion on the wake topology and odor distribution. From our simulation results, remarkable resemblances were observed between the wakemore »topology and odor landscape. For the 2D case, an inverse von Kármán vortex street was formed in the downstream. For the 3D case, the wake bifurcates and forms two branches of horseshoe-like vortices. The results revealed in this study have the potential to advance our understanding of the odor-tracking capability of insects navigation and lead to transformative advancements in unmanned aerial devices that will have the potential to greatly impact national security equipment and industrial applications for chemical disaster, drug trafficking detection, and GPS-denied indoor environment.« less
  5. Olfactory systems in animals play a major role in finding food and mates, avoiding predators, and communication. Chemical tracking in odorant plumes has typically been considered a spatial information problem where individuals navigate towards higher concentration. Recent research involving chemosensory neurons in the spiny lobster, Panulirus argus, show they possess rhythmically active or ‘bursting’ olfactory receptor neurons that respond to the intermittency in the odor signal. This suggests a possible, previously unexplored olfactory search strategy that enables lobsters to utilize the temporal variability within a turbulent plume to track the source. This study utilized computational fluid dynamics to simulate the turbulent dispersal of odorants and assess a number of search strategies thought to aid lobsters. These strategies include quantification of concentration magnitude using chemosensory antennules and leg chemosensors, simultaneous sampling of water velocities using antennule mechanosensors, and utilization of antennules to quantify intermittency of the odorant plume. Results show that lobsters can utilize intermittency in the odorant signal to track an odorant plume faster and with greater success in finding the source than utilizing concentration alone. However, the additional use of lobster leg chemosensors reduced search time compared to both antennule intermittency and concentration strategies alone by providing spatially separatedmore »odorant sensors along the body.« less