Olfactory navigation in arthropods

Abstract

Using odors to find food and mates is one of the most ancient and highly conserved behaviors. Arthropods from flies to moths to crabs use broadly similar strategies to navigate toward odor sources—such as integrating flow information with odor information, comparing odor concentration across sensors, and integrating odor information over time. Because arthropods share many homologous brain structures—antennal lobes for processing olfactory information, mechanosensors for processing flow, mushroom bodies (or hemi-ellipsoid bodies) for associative learning, and central complexes for navigation, it is likely that these closely related behaviors are mediated by conserved neural circuits. However, differences in the types of odors they seek, the physics of odor dispersal, and the physics of locomotion in water, air, and on substrates mean that these circuits must have adapted to generate a wide diversity of odor-seeking behaviors. In this review, we discuss common strategies and specializations observed in olfactory navigation behavior across arthropods, and review our current knowledge about the neural circuits subserving this behavior. We propose that a comparative study of arthropod nervous systems may provide insight into how a set of basic circuit structures has diversified to generate behavior adapted to different environments.

Unraveling the neural basis of spatial orientation in arthropods

“…Signals are fed directly to descending pathways, allowing to maintain flight balance or initiate escape responses. In addition, several other brain areas receive optic flow input, among them the central complex, likely combining distance and directional information for path integration as suggested by Stone et al ( 2017 ) for sweat bees.…”

Gain control in olfactory receptor neurons and the detection of temporal fluctuations in odor concentration

“…While recent studies on the ON and OFF ORNs have clearly shown that the slower the rate of concentration change, the higher is their precision in differentiating small concentration changes ( Tichy et al, 2016 ), their capacity to encode variations in temporally discontinuous concentration pulses was not examined in closer detail. The significance of intermittent odor signals in plume tracking and the role of the rate of filament or pulse encounter in anemotactic orientation for both flying and walking insects are well known ( Willis and Baker, 1984 ; Murlis et al, 1992 ; Cardé and Willis, 2008 ; Lei et al, 2009 ; Cardè, 2021 ; Jayaram et al, 2022 ; Steele et al, 2023 ). Results from studies in moths and other insects indicate a nearly universal strategy for odor-source location that was framed as a surge upwind in the odor plume and a tendency toward cross-wind casting upon loss of the odor.…”

“…The temporal response characteristics of the ON and OFF ORNs are consistent with the idea that plume trackers walking on a smooth surface in a stationary or slowly expanding odor plume may use the change in shape and size of the encountered concentration pulses including their gradients in space and time to localize the odor source. Walking and in-flight plume tracking in turbulent flows, where odor concentration is patchily distributed resulting in temporally intermittent stimulation, requires measuring the timing of odor on and off and representing the intermittent plume as a spatiotemporal entity of the constituent odor filaments, but not filament concentration or its rate of changes ( Martin et al, 2011 ; Steele et al, 2023 ; Talley et al, 2023 ). Wind tunnel studies suggest that two temporal features—odor intermittency and encounter frequency—can enhance the navigation of turbulent odor plumes in many moth species and Drosophila , which run or fly faster and straighter upwind when receiving odor hits at higher frequency than lower ones ( Mafra-Neto and Cardè, 1994 ; Vickers and Baker, 1994 ; Keller and Weissburg, 2004 ; Jayaram et al, 2022 ).…”

A new leaf sensing organ in a predatory insect group, the praying mantises

“…Insects possess sophisticated chemosensory capabilities (Hallem et al ., 2006; Sato & Touhara, 2008, Martin et al . 2011, Steele et al 2023) and much of their behavioral ecology is tied to the detection and discrimination of chemicals (de Boer and Dicke 2006, Xu and Turlings, 2018; Felton and Tumlinson, 2008; Kannan et al 2022). Perceiving chemical stimuli provides critical information for identifying habitat and oviposition sites, food sources, mates, and predators over short and long distances (Engsontia et al ., 2008; Iacovone et al ., 2016).…”