Oscillations for active sensing in olfaction: bioinspiration from insect antennal movements.

Crustacean and insect antennal scanning movements have been postulated to increase odorant capture but the exact mechanisms as well as measures of efficiency are wanting. The aim of this work is to test the hypothesis that an increase in oscillation frequency of a simplified insect antenna model translates to an increase of odorant capture, and to quantify by how much and through which mechanism. We approximate the antennal movements of bumblebees, quantified in a previous study, by a vertical oscillatory movement of a cylinder in a homogeneous horizontal flow with odorants. We test our multiphysics flow and mass transfer numerical model with dedicated experiments using particle image velocimetry. A new entire translating experimental measurement setup containing an oil tank enables us to work at appropriate Strouhal and Reynolds numbers. Increasing antennal oscillating frequency does increase the odorant capture rate, up to 200%, proving this behavior being active sensing. This result holds however only up to a critical frequency. A decrease of efficiency characterizes higher frequencies, due to molecules depletion within oversampled regions, themselves defined by overlaying boundary layers. Despite decades of work on thermal and mass transfer studies on oscillating cylinders, no analogy with published cases was found. This is due to the unique flow regimes studied here, resulting from the combination of organ small size and low frequencies of oscillations. A theory for such flow regimes is thus to be developed, with applications to fundamental research on animal perception up to bioinspired olfaction.

Insect pectinate antennae maximize odor capture efficiency at intermediate flight speeds.

Flying insects are known to orient themselves over large distances using minute amounts of odors. Some bear pectinate antennae of remarkable architecture thought to improve olfactory performance. The semiporous, multiscale nature of these antennae influences how odor molecules reach their surface. We focus here on the repeating structural building blocks of these antennae in Saturniid moths. This microstructure consists of one ramus or branch and its many hair-like sensilla, responsible for chemical detection. We experimentally determined leakiness, defined as the proportion of air going through the microstructure rather than flowing around it, by particle image velocimetry visualization of the flow around three-dimensional printed scaled-up mock-ups. The combination of these results with a model of mass transfer showed that most pheromone molecules are deflected around the microstructure at low flow velocities, keeping them out of reach. Capture is thus determined by leakiness. By contrast, at high velocities, molecular diffusion is too slow to be effective, and the molecules pass through the structure without being captured. The sensory structure displays maximal odor capture efficiency at intermediate flow speeds, as encountered by the animal during flight. These findings also provide a rationale for the previously described "olfactory lens," an increase in pheromone reception at the proximal end of the sensors. We posit that it is based on passive mass transfer rather than on physicochemical surface processes.

Leakiness and flow capture ratio of insect pectinate antennae.

The assumption that insect pectinate antennae, which are multi-scale organs spanning over four orders of magnitude in size among their different elements, are efficient at capturing sexual pheromones is commonly made but rarely thoroughly tested. Leakiness, i.e. the proportion of air that flows within the antenna and not around it, is a key parameter which depends on both the macro- and the microstructure of the antenna as well as on the flow velocity. The effectiveness of a structure to capture flow and hence molecules is a trade-off between promoting large leakiness in order to have a large portion of the flow going through it and a large effective surface area to capture as much from the flow as possible, therefore leading to reduced leakiness. The aim of this work is to measure leakiness in 3D-printed structures representing the higher order structure of an antenna, i.e. the flagellum and the rami, with varying densities of rami and under different flow conditions. The male antennae of the moth Samia cynthia (Lepidoptera: Saturniidae) were used as templates. Particle image velocimetry in water and oil using 3D-printed scaled-up surrogates enabled us to measure leakiness over a wide range of equivalent air velocities, from 0.01 m s-1 to 5 m s-1, corresponding to those experienced by the moth. We observed the presence of a separated vortex ring behind our surrogate structures at some velocities. Variations in the densities of rami enabled us to explore the role of the effective surface area, which we assume to permit equivalent changes in the number of sensilla that host the chemical sensors. Leakiness increased with flow velocity in a sigmoidal fashion and decreased with rami density. The flow capture ratio, i.e. the leakiness multiplied by the effective surface area divided by the total surface area, embodies the above trade-off. For each velocity, a specific structure leads to a maximum flow capture ratio. There is thus not a single pectinate architecture which is optimal at all flow velocities. By contrast, the natural design seems to be robustly functioning for the velocity range likely to be encountered in nature.

The morphological heterogeneity of cricket flow-sensing hairs conveys the complex flow signature of predator attacks.

Arthropod flow-sensing hair length ranges over more than an order of magnitude, from 0.1 to 5 mm. Previous studies repeatedly identified the longest hairs as the most sensitive, but recent studies identified the shortest hairs as the most responsive. We resolved this apparent conflict by proposing a new model, taking into account both the initial and long-term aspects of the flow pattern produced by a lunging predator. After the estimation of the mechanical parameters of hairs, we measured the flow produced by predator mimics and compared the predicted and observed values of hair displacements in this flow. Short and long hairs respond over different time scales during the course of an attack. By harbouring a canopy of hairs of different lengths, forming a continuum, the insect can fractionize these moments. Short hairs are more agile, but are less able to harvest energy from the air. This may result in longer hairs firing their neurons earlier, despite their slower deflection. The complex interplay between hair agility and sensitivity is also modulated by the predator distance and the attack speed, characteristics defining flow properties. We conclude that the morphological heterogeneity of the hair canopy mirrors the flow complexity of an entire attack, from launch to grasp.

Predator-induced flow disturbances alert prey, from the onset of an attack.

Many prey species, from soil arthropods to fish, perceive the approach of predators, allowing them to escape just in time. Thus, prey capture is as important to predators as prey finding. We extend an existing framework for understanding the conjoint trajectories of predator and prey after encounters, by estimating the ratio of predator attack and prey danger perception distances, and apply it to wolf spiders attacking wood crickets. Disturbances to air flow upstream from running spiders, which are sensed by crickets, were assessed by computational fluid dynamics with the finite-elements method for a much simplified spider model: body size, speed and ground effect were all required to obtain a faithful representation of the aerodynamic signature of the spider, with the legs making only a minor contribution. The relationship between attack speed and the maximal distance at which the cricket can perceive the danger is parabolic; it splits the space defined by these two variables into regions differing in their values for this ratio. For this biological interaction, the ratio is no greater than one, implying immediate perception of the danger, from the onset of attack. Particular attention should be paid to the ecomechanical aspects of interactions with such small ratio, because of the high degree of bidirectional coupling of the behaviour of the two protagonists. This conclusion applies to several other predator-prey systems with sensory ecologies based on flow sensing, in air and water.

Responses of cricket cercal interneurons to realistic naturalistic stimuli in the field.

The ability of the insect cercal system to detect approaching predators has been studied extensively in the laboratory and in the field. Some previous studies have assessed the extent to which sensory noise affects the operational characteristics of the cercal system, but these studies have only been carried out in laboratory settings using white noise stimuli of unrealistic nature. Using a piston mimicking the natural airflow of an approaching predator, we recorded the neural activity through the abdominal connectives from the terminal abdominal ganglion of freely moving wood crickets (Nemobius sylvestris) in a semi-field situation. A cluster analysis of spike amplitudes revealed six clusters, or 'units', corresponding to six different subsets of cercal interneurons. No spontaneous activity was recorded for the units of larger amplitude, reinforcing the idea they correspond to the largest giant interneurons. Many of the cercal units are already activated by background noise, sometimes only weakly, and the approach of a predator is signaled by an increase in their activity, in particular for the larger-amplitude units. A scaling law predicts that the cumulative number of spikes is a function of the velocity of the flow perceived at the rear of the cricket, including a multiplicative factor that increases linearly with piston velocity. We discuss the implications of this finding in terms of how the cricket might infer the imminence and nature of a predatory attack.

Directional cues in Drosophila melanogaster audition: structure of acoustic flow and inter-antennal velocity differences.

Drosophila melanogaster have bilateral antisymmetric antennae that receive the particle velocity component of an acoustic stimulus. Acoustic communication is important in their courtship, which takes place in the acoustic near-field. Here, the small size of the dipole sound source (the male wing) and the rapid attenuation rate of particle velocity produce a spatially divergent sound field with highly variable magnitude. Also, male and female D. melanogaster are not usually stationary during courtship, resulting in a variable directionality of the acoustic stimulus. Using both particle image velocimetry and laser Doppler vibrometry, we examined the stimulus flow around the head of D. melanogaster to identify the actual geometry of the acoustic input to the antennae and its directional response. We reveal that the stimulus changes in both magnitude and direction as a function of its angle of incidence. Remarkably, directionality is substantial, with inter-antennal velocity differences of 25 dB at 140 Hz. For an organism whose auditory receivers are separated by only 660 ± 51 µm (mean ± s.d.), this inter-antennal velocity difference is far greater than differences in intensity observed between tympanal ears for organisms of similar scale. Further, the mechanical sensitivity of the antennae changes as a function of the angle of incidence of the acoustic stimulus, with peak responses along axes at 45 and 315 deg relative to the longitudinal body axis. This work indicates not only that the flies are able to detect differential cues in signal direction, but also that the male song structure may not be the sole determinant of mating success; his spatial positioning is also crucial to female sound reception and therefore also perhaps to her decision making.

Air motion sensing hairs of arthropods detect high frequencies at near-maximal mechanical efficiency.

Using measurements based on particle image velocimetry in combination with a novel compact theoretical framework to describe hair mechanics, we found that spider and cricket air motion sensing hairs work close to the physical limit of sensitivity and energy transmission in a broad range of relatively high frequencies. In this range, the hairs closely follow the motion of the incoming flow because a minimum of energy is dissipated by forces acting in their basal articulation. This frequency band is located beyond the frequency at which the angular displacement of the hair is maximum which is between about 40 and 600 Hz, depending on hair length (Barth et al. [1] Phil. Trans. R. Soc. Lond. B 340, 445-461 (doi:10.1098/rstb.1993.0084)). Given that the magnitude of natural airborne signals is known to decrease with frequency, our results point towards the possible existence of spectral signatures in the higher frequency range that may be weak but of biological significance.

Why do insects have such a high density of flow-sensing hairs? Insights from the hydromechanics of biomimetic MEMS sensors.

Insects and arachnids are often quite hairy. The reasons for this high density of sensory hairs are unknown. Previous studies have predicted strong hydrodynamic coupling between densely packed airflow-sensitive hairs. Flow perturbation owing to single hairs and between tandem hairs, however, has never been experimentally measured. This paper aims to quantify the extent of flow perturbation by single and tandem hairs directly, using biomimetic microelectromechanical system (MEMS) hairs as physical models and particle image velocimetry (PIV) for flow visualization. Single and tandem MEMS hairs of varying interhair distances were subjected to oscillatory flows of varying frequency. Decreasing hair-to-hair distance markedly reduced flow velocity amplitude and increased the phase shift between the far-field flow and the flow between hairs. These effects were stronger for lower flow frequencies. We predict strong hydrodynamic coupling within whole natural hair canopies exposed to natural stimuli, depending on arthropod and hair sizes, and hair density. Thus, rather than asking why arthropods have so many hairs, it may be useful to address why hairs are packed together at such high densities, particularly given the exquisite sensitivity of a single hair.

Relative contributions of organ shape and receptor arrangement to the design of cricket's cercal system.

Understanding the relative contributions of the shape of a sensory organ and the arrangement of receptors to the overall performance of the organ has long been a challenge for sensory biologists. We tackled this issue using the wind-sensing system of crickets, the cerci, two conical abdominal appendages covered with arrays of filiform hairs. Scanning electron microscopy coupled with 3D reconstruction methods were used for mapping of all cercal filiform hairs. The hairs are arranged according to their diameter in a way that avoids collisions with neighbours during hair deflection: long hairs are regularly spaced, whereas short hairs are both randomly and densely distributed. Particle image velocimetry showed that the variation in diameter of the cercus along its length modifies the pattern of fluid velocities. Hairs are subject to higher air flow amplitudes at the base than at the apex of the cercus. The relative importance of interactions between receptors and the air flow around the organ may explain the performance of the cricket's cercal system: it is characterised by a high density of statistically non-interacting short hairs located at the base of the cercus where sensitivity to air currents is the highest.

The aerodynamic signature of running spiders.

Many predators display two foraging modes, an ambush strategy and a cruising mode. These foraging strategies have been classically studied in energetic, biomechanical and ecological terms, without considering the role of signals produced by predators and perceived by prey. Wolf spiders are a typical example; they hunt in leaf litter either using an ambush strategy or by moving at high speed, taking over unwary prey. Air flow upstream of running spiders is a source of information for escaping prey, such as crickets and cockroaches. However, air displacement by running arthropods has not been previously examined. Here we show, using digital particle image velocimetry, that running spiders are highly conspicuous aerodynamically, due to substantial air displacement detectable up to several centimetres in front of them. This study explains the bimodal distribution of spider's foraging modes in terms of sensory ecology and is consistent with the escape distances and speeds of cricket prey. These findings may be relevant to the large and diverse array of arthropod prey-predator interactions in leaf litter.