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We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020) and the intermittency of the odor signal, which we define to be the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here, we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments - achieving maximal performance when gains are near those inferred from experiment - but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep trade-off when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes. Finally, we show that the circuitry of the Drosophila olfactory periphery naturally enables simultaneous intermittency and frequency sensing, enhancing robust navigation through a diversity of odor environments. Together, our results suggest that the first stage of olfactory processing selects and encodes temporal features of odor signals critical to real-world navigation tasks.

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One of the biggest global challenges for our societies is to provide natural resources to the rapidly expanding population while maintaining sustainable and ecologically friendly products. The increasing public concern about toxic insecticides has resulted in the rapid development of alternative techniques based on natural infochemicals (ICs). ICs (e.g., pheromones, allelochemicals, volatile organic compounds) are secondary metabolites produced by plants and animals and used as information vectors governing their interactions. Such chemical language is the primary focus of chemical ecology, where behavior-modifying chemicals are used as tools for green pest management. The success of ecological programs highly depends on several factors, including the amount of ICs that enclose the crop, the range of their diffusion, and the uniformity of their application, which makes precise detection and quantification of ICs essential for efficient and profitable pest control. However, the sensing of such molecules remains challenging, and the number of devices able to detect ICs in air is so far limited. In this review, we will present the advances in sensing of ICs including biochemical sensors mimicking the olfactory system, chemical sensors, and sensor arrays (e-noses). We will also present several mathematical models used in integrated pest management to describe how ICs diffuse in the ambient air and how the structure of the odor plume affects the pest dynamics.

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Walking flies find the source of attractive odors by changing how frequently they stop and turn in response to the smell.

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How insects navigate complex odor plumes, where the location and timing of odor packets are uncertain, remains unclear. Here we imaged complex odor plumes simultaneously with freely-walking flies, quantifying how behavior is shaped by encounters with individual odor packets. We found that navigation was stochastic and did not rely on the continuous modulation of speed or orientation. Instead, flies turned stochastically with stereotyped saccades, whose direction was biased upwind by the timing of prior odor encounters, while the magnitude and rate of saccades remained constant. Further, flies used the timing of odor encounters to modulate the transition rates between walks and stops. In more regular environments, flies continuously modulate speed and orientation, even though encounters can still occur randomly due to animal motion. We find that in less predictable environments, where encounters are random in both space and time, walking flies navigate with random walks biased by encounter timing.

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 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.

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Chemical signals are primarily distributed throughout aquatic environments by processes that are affected by turbulence. Turbulence continually stirs and mixes chemical odorants into complex, filamentous structures that are sampled by organisms. These odorant signals are critical for survival and/or reproductive success of most aquatic animals, and the time varying spatial structure of velocity and concentration offers valuable guidance cues while navigating in a plume. Two separate techniques are described to simultaneously measure a turbulent odor plume on a scale relevant to the chemosensors and mechanosensors located along the antennules of aquatic organisms. The first, planar laser induced fluorescence (PLIF), is used to quantify odorant concentrations, while the second, particle image velocimetry (PIV), is used to measure turbulent fluid velocities.

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