Pheromone binding protein shapes olfactory temporal resolution

Male moths are capable of orienting towards conspecific females using sex pheromones. Since pheromones are distributed as discontinuous plumes owing to air turbulence, tracking intermittent stimuli with high temporal resolution is suggested to be important for efficient localisation. Here, using a pheromone binding protein (BmPBP1) knockout silkmoth, we revealed that the loss of functional pheromone binding protein altered antennal response kinetics resulting in reduced temporal resolution to intermittent pheromone stimuli on the antennae. Behavioural analysis revealed that BmPBP1-knockout males exhibited significantly less straight walking, which occurs when detecting pheromone stimuli, especially to high frequency stimuli. Accordingly, BmPBP1-knockout males took a significantly longer time to locate pheromone sources and females than did wild-type males. Together, BmPBP1 plays a critical role in determining temporal antennal response kinetics and that an appropriate range of temporal sensory and behavioural resolutions is essential for tracking pheromone plumes for efficient pheromone source localisation in the silkmoth.

Path Meander of Male Codling Moths (Cydia pomonella) Foraging for Sex Pheromone Plumes: Field Validation of a Novel Method for Quantifying Path Meander of Random Movers Developed Using Computer Simulations

Measures of path meander are highly relevant to studies of optimal foraging by animals. However, directly recording paths of small animals such as insects can be difficult because of small size or crepuscular activity. Computer simulations of correlated random walkers demonstrated that the rates of decay in captures across a rectangular grid of traps when movers were released at its corner can be used to produce calibration curves for quantifying path meander indirectly. Simulations using spatial parameters matching those previously documented for male codling moths (Cydia pomonella (L.)) foraging for female pheromone plumes in the field predicted that meander, as measured in circular standard deviation (c.s.d.) of turn angles between track segments, should be ca. 50° and 30° when the target population density is high vs. low, respectively. Thus, if optimized, the mean value measured for C. pomonella populations encountering an unknown target density should fall between these limits. We recorded decay in C. pomonella catch across a 5 × 5 grid of pheromone-baited traps each separated by 15 m on 39 occasions where batches of ca. 800 males were released 10 m outside the corner of trapping grids arranged in five large Michigan apple orchards. This decay constant was translated into mean c.s.d value for path meander using the standard curve generated by the computer simulations. The measured decay constant for C. pomonella males was negative 0.99 ± 0.02 (S.E.M.), which translates to a path meander of 37 ± 2° c.s.d. Thus, the measured path meander of 37° fell between the 50° and 30° values optimal for dense and sparse populations, respectively. In addition to providing a rare documented example of optimal foraging for odor plumes, this research offers proof-of-concept for a novel approach to quantifying path meander of movers that could prove useful across diverse taxa.

Dynamic Properties of Antennal Responses to Pheromone in Two Moth Species

Dynamic properties of pheromone plumes are behaviorally important in some moths for inducing upwind flight, but little is known about the time-dependent properties of odor transduction or the mechanisms that limit receptor dynamic sensitivity. We stimulated male antennae of two moth species, Cadra cautella and Spodoptera exigua, with pheromone plumes in a wind tunnel while recording electroantennograms (EAG) and concentration of a surrogate plume (propylene, which mimics a pheromone plume) using a photoionization detector (PID). Turbulent plumes were produced by mechanical baffles, creating broad frequency range dynamic concentration changes at the antennae. Frequency response functions and coherence functions between PID and EAG signals were used to measure the dynamic responses of the two species to pheromone blends and individual components. A single time constant filter fitted the responses of both species, but S. exigua was about three times faster than C. cautella. Responses to individual pheromone components were significantly different in S. exigua but not in C. cautella. We also fitted the data with a simple block-structured nonlinear cascade. This supported the simple filter model but also suggested that the response saturates at an early stage of chemotransduction.