Mark A. Willis

Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta

We performed field experiments to measure the relative importance of olfactory and visual cues in nectar foraging by wild tobacco hornworm moths, Manduca sexta (Lepidoptera, Sphingidae) in the Sonoran Desert of Arizona, U.S.A. We manipulated flowers of sacred Datura (Datura wrightii; Solanaceae) to experimentally decouple floral scent from visual display and presented these cues to free-flying moths in mixed and homogeneous arrays. Moths did not feed from cloth-bagged fragrant flowers lacking strong visual contrast, nor did they feed from paper model flowers lacking plant odours. Unexpectedly, moths fed from paper model flowers that were associated solely with vegetative odours, albeit at lower levels than when floral scent was present. Subsequent experiments revealed that the combination of floral and vegetative odours did not incrementally increase nectar feeding and that floral scent without vegetation was sufficient to elicit feeding when paper flowers were present. Thus, wild M. sexta in our study did not show generalized feeding responses to natural or artificial flowers with single sensory stimuli; like naive laboratory-reared moths, they required a combination of visual and olfactory cues. However, given the prior foraging experience of our study population on Datura flowers, their lack of generalized feeding responses may reflect a learned preference for the full complement of floral cues, rather than the persistence of innate sensory constraints. Future efforts to distinguish between these hypotheses should focus on whether M. sexta can be conditioned to associate nectar with visual cues alone, and whether moths that feed ad libitum from nectar-rich plants learn floral attributes as a search image or generalize to single-modality stimuli.

Navigational Strategies Used by Insects to Find Distant, Wind-Borne Sources of Odor

Insects locate many resources important to survival by tracking along wind-borne odor plumes to their source. It is well known that plumes are patchy distributions of high concentration packets of odor interspersed with clean air, not smooth Gaussian distributions of odor intensity. This realization has been crucial to our understanding of plume-tracking behavior, because insect locomotory movements and sensory processing typically take place in the range of tens to hundreds of milliseconds, permitting them to respond to the rapid changes in odor concentration they experience in plumes. Because odor plumes are not comprised of smooth concentration gradients, they cannot provide the directional information necessary to allow plume-tracking insects to steer toward the source. Many experiments have shown that, in the species examined, successful source location requires two sensory inputs: the presence of the attractive odor and the detection of the direction of the wind bearing that odor. All plume-tracking insects use the wind direction as the primary directional cue that enables them to steer their movements toward the odor source. Experimental manipulations of the presence and absence of the odor, and the presence, absence, or direction of the wind during plume tracking, have begun to resolve the relationship between these two sensory inputs and how they shape the maneuvers we observe. Experiments, especially those undertaken in the natural wind and odor environments of the organisms in question and those directed at understanding the neural processing that underlie plume tracking, promise to enhance our understanding of this remarkable behavior.

Odor-modulated upwind flight of the sphinx moth, Manduca sexta L.

Summary1.Male and female Manduca sexta flew upwind in response to the odor of female sex-pheromone gland extract or fresh tobacco leaf respectively, and generated very similar zigzagging tracks along the odor plume.2.After loss of odor during flight, males and females alike: (1) first flew slower and steered their flight more across the wind, then (2) stopped moving upwind, and finally (3) regressed downwind.3.Males flying upwind in a pheromone plume in wind of different velocities maintained their ground speed near a relatively constant ‘preferred’ value by increasing their air speed as the velocity of the wind increased, and also maintained the average angle of their resultant flight tracks with respect to the wind at a preferred value by steering a course more precisely due upwind.4.The inter-turn duration and turn rate, two measures of the temporal aspects of the flight track, were maintained, on average, with remarkable consistency across all wind velocities and in both sexes. The inter-turn durations also decreased significantly as moths approached the odor source, suggesting modulation of the temporal pattern of turning by some feature of the odor plume. This temporal regularity of turning appears to be one of the most stereotyped features of odor-modulated flight in M. sexta.

Spatial and temporal structures of pheromone plumes in fields and forests

Wind‐borne odour stimuli from a small point‐source of pheromone are intermittent owing to the effects of atmospheric turbulence on the odour plume. The work reported here measures the characteristics of the intermittent stimulus in open fields and forests during typical daytime atmospheric conditions. To model the pheromone plume, negatively charged atmospheric ions were used as a tracer. They were released from an ion generator, and ion detectors measured the fluctuating flux of ions at positions up to 20 m downwind in the open field case and 10 m in the forest. In both the open field and in the forest, ion signals were highly intermittent, with a signal present only 20% of the time. Ion signals recorded in the forest consisted of bursts with gaps between them of at least three‐fold greater duration than those from the open field. In both environments, bursts generally each comprised a series of ‘spikes’, on average three in the field and seven in the forest. To validate the use of ionized air plumes as models of pheromone plumes, the antennae of male Lymantria dispar (gypsy moth) were used as detectors to quantify the plume of synthetic (+)‐disparlure emanating from a 2000 ng point source placed ≈ 10 cm from the ion source. A comparison of ion signals and EAGs (electronantennograms) suggests that the antennae respond to the main spikes within a burst, but no consistent relationship between the strength of the spikes and the magnitude of the EAG response was found. The average strengths of bursts in the ion detector signal decreased systematically as the distance from the ion generator to the ion detector increased. A similar trend, however, was not detected in the EAG response.

Odor-modulated orientation in walking male cockroaches Periplaneta americana, and the effects of odor plumes of different structure

SUMMARY The location of distant resources using odor information usually also requires information on the flow of air (or water) through the environment together with the expression of internally programmed steering responses. The orientation responses of virgin male Periplaneta americana L. to wind and the female sex-pheromone component (-)-periplanone-B were video-recorded in a laboratory wind tunnel and quantified. P. americana males showed no preferred walking orientation when released in zero wind in the absence of pheromone. When introduced into 25 cm s-1 wind in the absence of pheromone, 79% of males walked downwind. Upon introduction to a plume of (-)-periplanone-B in wind, 100% of males walked upwind in the pheromone plume to the source. Males were then challenged with wind-borne plumes of (-)-periplanone-B of four different temporal/spatial structures. In nearly all cases, the only statistically significant changes in behavioral parameters measured from their walking tracks were observed from males tracking the treatment consisting of the most turbulent plume. The plume-tracking performances of males challenged with the other three less turbulent plumes were visually and quantitatively similar, regardless of the width. Males tracking all four plumes showed evidence of turns resulting from multiple mechanisms. Some of the observed maneuvers were temporally regular counterturns, suggesting steering according to an ongoing internal program, while others could have been triggered by encountering the change in odor concentration between pheromone and clean air at the lateral boundary of the plume or chemotactically upon the detection of changes in odor concentration.

Effects of altering flow and odor information on plume tracking behavior in walking cockroaches, Periplaneta americana (L.).

SUMMARY Animals using odor plumes to locate resources are activated to track these plumes by the presence of an attractive odor, and typically steer toward the source using directional cues from the flowing air or water bearing the odor. We challenged freely walking virgin male cockroaches, Periplaneta americana, to track plumes of airborne female pheromone and then video-recorded and analyzed their responses as the odor plume and wind were independently manipulated. Plume tracking males that experienced the total loss of directional air flow halfway to the odor source showed little change in their performance, and 100% were able to quickly locate the pheromone source. By contrast, males experiencing a sudden loss of odor while tracking a plume rapidly changed their behavior; often turning downwind and retracing their steps to the release point, or walking in loops, but rarely moving upwind to the previous location of the source. In a subsequent experiment, in order to determine whether a memory of the previously experienced wind direction could provide the directional information necessary to locate an odor source, we challenged males to track plumes in zero wind after pre-exposing them to: (1) wind and pheromone, (2) wind only, and (3) neither wind nor pheromone. These were compared to males tracking a wind-borne pheromone plume, in which case, all males were able to locate the pheromone source. Our results show that males require the detection of wind and pheromone simultaneously during plume tracking in order to quickly and efficiently locate the odor source. These results are consistent with those reported from flying moths tracking wind-borne pheromone plumes, and suggest that the control system underlying this behavior requires ongoing simultaneous experience with wind and odor information during the performance of the behavior to operate efficiently.

MODULATION OF WHITEFLY TAKE-OFF AND FLIGHT ORIENTATION BY WIND SPEED AND VISUAL CUES

The effect of different wind speeds on take‐off and flight orientation of the sweetpotato whitefly, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae), was studied in the presence of a green visual stimulus which reflected 550 ± 10 nm light, or a white stimulus of the same intensity. When the white light was present, take‐off was negatively correlated with wind speed. Analysis of the flight tracks of whiteflies in 0, 15 and 30 cm/s wind with the white light present showed that flight was not directed toward the stimulus in zero wind, and that insects were carried downwind as the wind increased. Net displacement downwind was significantly slower than the wind speed, indicating that B. tabaci can control its rate of displacement relative to its surroundings, and is not always passively transported by the wind. In the presence of the green visual stimulus, take‐off and flight behaviour of B. tabaci was markedly different to that observed in the presence of the white light. Taking off was more likely and whiteflies made upwind orientated flights, landing on the illuminated section of the screen when it reflected green light. At all wind speeds tested, the mean ground speeds of B. tabaci were approximately 20 cm/s whether the insects were flying upwind or downwind. This uniformity of ground speed regardless of the changing effects of wind‐induced drift in different directions strongly suggests that whiteflies actively control their ground speed using visual flow fields in a manner similar to all other flying insects examined thus far.

Moth-Inspired Plume Tracking Strategies In Three-Dimensions

Two simple three-dimensional moth inspired odor tracking algorithms, Counter-turner and Modified counter-turner, were tested on a robotic platform. The Counter-turner uses the plume edge to modify the timing of the crosswind movements, while the Modified counter-turner uses the plume centerline. Both algorithms shows some success in tracking the plume to it’s source. In addition, flight tracks show promise in mimicking the flight tracks observed in biological experiments with the moth Manduca. Sexta.

A robotic platform for testing moth-inspired plume tracking strategies

A mobile autonomous robot capable of tracking an odor plume to its source can be used to locate hazardous material spills or leaks. To test plume tracking strategies in a laboratory environment, a robotic platform consisting of a linear Cartesian robotic gantry mounted inside a wind tunnel with a mobile floor has been designed. A plume of ionized air is created by an ion detector installed in the wind tunnel. A two-dimensional plume tracking strategy based on the behavior of the tobacco hornworm moth Manduca sexta is implemented and tested. It is discovered that a plume tracking algorithm can be implemented with the robotic platform almost as easily as in simulation.

Biologically-inspired search algorithms for locating unseen odor sources

Many animals use air- or water-borne plumes of odor molecules to locate distant unseen resources. They offer excellent models for the development of robotic systems capable of orientation to chemical plumes. The best studied example of this behavior in biology is that of male moths tracking plumes of the female sex-attractant pheromone upwind to their source, a sexually receptive female. To more fully understand the complex interaction between the odor stimulus, sensory processing, interacting control systems, and ongoing centrally organized behavior, we have implemented a simulation organized around what is known about the sensory systems, behavior and control systems of real moths. The simulation environment is flexible and can reflect the stochastic nature of real environments. Within the biologically relevant parameter space, simple reflexive models are sometimes able to locate the odor source, but even the most successful models (comprising layered control systems and centrally generated behavior) fall far short of the performance of real moths. To try to understand why, we have employed a genetic algorithm to optimize the performance of the models. This approach has identified unique combinations of parameters that yield similar success rates, but display behaviors that look very different.