Antennal mechanosensors mediate sex pheromone‐induced upwind orientation in the potato tuberworm moth

Males of the potato tuberworm moth Phthorimaea operculella (Lepidoptera: Gelechiidae) locate conspecific females by a series of short and straight flights, or ‘hops’. On the floor of a wind tunnel, P. operculella can change their heading angles in response to wind direction shift, suggesting that they detect wind direction and orient upwind when on the ground. It is unlikely that they navigate in wind by vision‐induced optomotor anemotaxis as in many flying moths. To investigate the mechanism of wind direction detection in this species, their orientation behaviour in response to pheromone pulses is observed in a wind tunnel. Intact male moths orient upwind even in complete darkness. After the flagellum of one antenna is amputated, male moths still successfully orient upwind. However, they fail to head upwind when the basal segments of both of their antennae are immobilized with glue. The ability to surge upwind is restored by removing the glue from the antennae. Thus, the results of the present study indicate that males of P. operculella orient upwind in response to mechanoreceptive cues from mechanosensory organs on their antennae. In Lepidoptera, two distinct anemotactic mechanisms of different sensory modalities appear to coexist: optomotor anemotaxis when airborne and the aim‐then‐shoot anemotactic system mediated by antennal mechanoreception when on the ground.     

Guidance of flying male moths by wind-borne sex pheromone

ABSTRACT. On passing from clean air into a homogeneous cloud of sex pheromone in a wind tunnel flying male Adoxophyes orana (F.v.R.) (Lepidoptera: Tortricidae) turned more or less upwind and reduced the time and distance between their switchings of track from one side of the wind line to the other. These responses became adapted under the constant pheromone stimulation in the cloud, thereby arresting upwind progress; but the adapted moths would now 'lock-on' to an added pheromone plume and advance upwind along it. Moths also locked-on to the border of a pheromone cloud, not by turning back on losing the scent as previously supposed but by initiating the above programme of small-amplitude, crosswind movements (reversing anemomenotaxis). The onset and cessation of the pheromone stimulus produced anemotactic responses that differed quantitatively within a continuum, not two distinct kinds of response as previously supposed. The behavioural mechanism whereby uniform permeation of an area with synthetic sex pheromone can prevent males from finding females is reconsidered.     

A non-anemotactic mechanism used in pheromone source location by flying moths

ABSTRACT. Male oriental fruit moths, Grapholitha molesta (Busck) (Tortricidae), continue to zigzag along a pheromone plume to the source in zero wind, if they have started flight with wind on. If the pheromone source is removed and the plume is hence truncated, moths flying in zero wind out of the end of the plume into clean air increase the width of their reversals and the angles of the straight legs of the tracks so they are more directly across the former wind line. Such moths reach the source less often than do those flying along a continuous plume. The males continue to zigzag up a plume in zero wind, apparently by a combination of sequential sampling of concentration along their path and the performance of an internal, self-steered programme of track reversals (zigzags) whose frequency increases with concentration. Visual feedback may aid in the still-air performance of the zigzags. We propose that both the sequential sampling (longitudinal klinotaxis) and self-steered counter-turning programme also are used in wind as well; anemotaxis apparently polarizes the direction of the zigzags to result in upwind displacement, and the narrow zigzags caused by the higher concentration in the plume keep the male 'locked on' to the odour.     

Pheromone-mediated optomotor anemotaxis and altitude control exhibited by male oriental fruit moths in the field

Abstract. In the field over short grass, pheromone-stimulated oriental fruit moth males, Grapholita molesta (Busck), flying under high windspeeds tended to steer courses more into the wind and to increase their airspeeds compared with those flying in low windspeeds.Thus, optomotor anemotaxis enabled the males to steer relatively consistent upwind track angles and to maintain an upwind progress of between c. 50–100 cm/s despite variable wind velocities.Zigzagging flight tracks were observed at both 10 m and 3 m from the source, as were tracks with no apparent zigzags.Transitions from casting to upwind flight or vice-versa were observed.The durations of the intervals between reversals during both upwind zigzagging flight and casting were consistent with those observed in previous wind-tunnel experiments.The control of altitude was more precise during upwind zigzagging flight than during casting.In general, the side-to-side deviations in the tracks were greater than the up-and-down deviations, with both the side-to-side and vertical distances and their ratios being consistent with previous wind-tunnel studies of pheromone-mediated flight.One difference between the field and laboratory flight tracks was that males in the field exhibited much higher airspeeds than in the wind tunnel.Males occasionally were observed to progress downwind faster than the wind itself, and further analysis showed that they were steering a downwind course in pheromone-free air following exposure to pheromone, which is the first time this has been recorded in moths.We propose that such downwind flight may aid in the relocation of a pheromone plume that has been lost due to a wind-shift, by enabling the moth to catch up to the pheromone as it recedes straight downwind away from the source.     

Detection of short pure-tone stimuli in the noctuid ear: what are temporal integration and integration time all about?

The interception of a pheromone filament induces flying moths to surge briefly nearly straight upwind; in the absence of pheromone moths cease upwind progress and zigzag crosswind. We tested males of the almond moth, Cadra cautella (Lepidoptera, Pyralidae), in a low-turbulence wind tunnel in wind velocities of 20, 40 and 80 cm s⁻¹. A mechanical pulse generator was set to produce plumes either with same pheromone pulse frequency (pulse generation frequency of 2.9 Hz, interpulse distances from 7 cm to 28 cm) or plumes with same interpulse distance across the three wind velocities (interpulse distance of 14 ± 2 cm, pulse generation frequency of 1.7–5.0 Hz). In plumes of similar pulse frequency, the faster the speed of the wind the slower the ground speed of flight. However, in plumes of similar interpulse distance, ground speed remained relatively constant independent of the wind speed. A `realized' frequency of pulse interception for males flying along the various combinations of pulse frequencies and wind velocities was calculated using the males' average airspeed and the spatial distribution of pheromone pulses in the plume. Realized frequency of pulse interception ranged from 1.3- to 3.0-fold higher than the frequency of pulse generation. The flight tracks of males reflected the regime of realized pulse interception. These results suggest that upwind flight orientation of male C. cautella to pheromone in different wind velocities is determined by the flux of filament encounter. Accepted: 3 September 1997     

Appetitive flight patterns of male Agrotis segetum moths over landscape scales

An analysis is presented of the first harmonic radar studies of pheromone-plume locating flights of male Agrotis segetum moths over distances of up to 500 m. Upon release most moths flew in a direction having a downwind component. The first significant changes in flight orientations occur in the immediate vicinity of a pheromone source. Moths that were initially flying downwind change course and start flying crosswind whilst those that initially flew crosswind change course and start flying upwind. It is shown that such behaviour is consistent with the adoption of an effective plume-location strategy, and conditions are identified when downwind flights would be more advantageous than crosswind ones. Additionally, some of the complex flight patterns that can arise at later times are shown to be compatible with the adoption of an optimal biased scale-free (Lévy-flight) searching strategy. It is found that disruptive doses of sex pheromone can have a marked influence upon male moth flight patterns.     

Manoeuvres used by flying male oriental fruit moths to relocate a sex pheromone plume in an experimentally shifted wind-field

ABSTRACT. In a wind-field experimentally shifted in direction by 35d?, flying male Grapholita molesta (Busck) zigzagging upwind either maintained contact with a pheromone plume and followed it across during the shift or lost it and commenced casting at c. 90d? across the shifting windline to locate it eventually in its new position. Males accomplished both of these results by integrating the previously described systems of optomotor anemotaxis and self-steered counterturning, but with faster reaction-times to pheromone on and off than heretofore calculated for this species. We found no evidence that males following the plume across used chemotaxis as proposed for another species, Rather, the sawtoothed-shaped tracks were a result of the anemotactic and counterturning systems responding rapidly and reiteratively to each loss and gain of pheromone along the plume in the shifting wind. The response to an increase or decrease in pheromone concentration by males was to change their course angle to more upwind or more crosswind, respectively, on the very first reversal (within c. 0.15 s) after the concentration changed. Because males adjusted their airspeeds more slowly to changes in concentration, the groundspeeds along the more upwind-orientated legs were lower than those along cross-wind legs, contributing to the sawtoothed shape of tracks of plume-followers. The self-steered counterturning programme also reacted quickly to concentration changes, the reversal intervals tending to be shorter following each contact with pheromone than after each excursion into cleaner wind. Following casting after losing the plume, males relocating the pheromone plume exhibited an upwind ‘surge’ of narrow zigzagging flight because on the first leg in the plume they steered a course more directly upwind than on the previous leg and increased the frequency of counterturning to its highest value while maintaining the relatively high airspeed acquired while casting.     

An analysis of anemotactic zigzagging flight in male moths stimulated by pheromone

ABSTRACT. The zigzagging behaviour of male Plodia interpunctella flying up a plume of sex pheromone was investigated in a horizontal wind tunnel by detailed analysis of the moths' ground tracks, groundspeeds, orientations and airspeeds. The moths ‘homed in’ on the source of the pheromone plume by progressively reducing airspeed and turning more into wind, thereby reducing groundspeed and the distance between track reversals and so narrowing down their zigzags (Fig. 16). Track angles and times between reversals were unaffected. Removing the wind-borne pheromone plume while a moth was flying along it confirmed that zigzagging can be an anemotactic response to losing the scent rather than a chemotactic response to the plume. For the first 1–2 s after the moth entered pheromone-free air the zigzagging was indistinguishable from that shown when the plume remained; thereafter it widened progressively until the moths were flying to and fro at c. 90° to the wind. The after-effect of odour stimulation persisted for many zigs and zags and many seconds (Figs. 4 and 5). Moths flying along pheromone plumes compensated efficiently for differences of wind speed, showing similar distributions of track angles to wind, and of ground-speeds, in winds of 0.1, 0.2 and 0.3 ms^-1 (Figs. 12 and 13). Groundspeed varied with track angle to wind and this relationship was also similar in the three wind speeds (Fig. 14). This constancy of track angles and groundspeeds was due to the moths both increasing their airspeeds and turning more into wind at the higher wind speeds (Fig. 17). Thus the direction of the apparent movement of the ground pattern beneath the moths varied with wind speed. It is inferred that the moths, although unable to sense the wind directly, are able to compensate for changes in wind speed by integrating the wind-dependent optomotor input with information about their own airspeed, or with information about their own turning movements. Maintaining some ‘preferred’ relationship between these inputs by adjustments of orientation and airspeed, would then serve to maintain a given combination of track angle and groundspeed independently of wind speed. The preferred relationship is repeatedly re-set by the changing olfactory input from the pheromone plume, which also controls the switching between left and right of the upwind direction.     

Flight behaviour of Cadra cautella males in rapidly pulsed pheromone plumes

Abstract Airborne pheromone plumes in wind comprise filaments of odour interspersed with gaps of clean air. When flying moths intercept a filament, they have a tendency to surge upwind momentarily, and then fly crosswind until another filament is intercepted. Thus, the moment-to-moment contact with pheromone mediates the shape of a flight track along the plume. Within some range of favourable interception rates, flight tracks become straighter and are headed more due upwind. However, as the rate of interception increases, there comes a point at which the moth should not be able to discern discreet filaments but, rather, should perceive a 'fused signal'. At the extreme, homogeneous clouds of pheromone inhibit upwind progress by representative tortricids. In a wind tunnel, Cadra cautella (Walker) (Lepidoptera: Pyralidae) were presented with 10 ms pulses of pheromone at a repetition rate of 5, 10, 17 and 25/s and a continuous, internally turbulent plume. Pulse size and concentrations were verified with a miniature photoionization detector sampling surrogate odour, propylene, at 100 Hz. Male moths maintain upwind progress even at plumes of 25 filaments/s. Furthermore, moths exhibited greater velocities and headings more due upwind at 17 and 25 Hz than at the lower frequencies or with the continuous plume. It is hypothesized that either C. cautella possesses a versatile sensory system that allows the resolution of these rapidly pulsed pheromone plumes, or that this species does not require a 'flickering' signal to fly upwind.     

Effects of light levels and plume structure on the orientation manoeuvres of male gypsy moths flying along pheromone plumes

The upwind zigzag flights of male gypsy moths (Lymantria dispar L.; Lepidoptera: Lymantriidae) along narrow, ribbon‐like and wide, turbulent plumes of pheromone were examined in a wind tunnel at light levels of 450 and 4 lux. Under all conditions tested males flew upwind zigzag paths. In 450 lux, males flying along turbulent plumes had the highest ground speeds and the widest crosswind excursions between counterturns, compared to slow flight and a narrow zigzag of males along a ribbon plume. In a turbulent plume, males flew more slowly and had narrower zigzags in 4 than in 450 lux. Across most treatments of plume structure and light level, the rate of transverse image flow and the frequency of counterturning remained relatively constant. The effects of light levels on orientation are not readily reconcilable with a model in which moths in low light levels would head more towards crosswind, thereby enhancing the rate of transverse image flow and the perception of wind‐induced drift.     

An analysis of anemotactic flight in female moths stimulated by host odour and comparison with the males' response to sex pheromone

ABSTRACT. The flight pattern of mated female navel orangeworm moths, Amyelois transitella (Walker), responding to odour from potential larval hosts is zigzagging upwind flight. However, at times these moths are capable of flying nearly directly upwind towards the odour source (track angles near 0). This response indicates that these females are capable of very accurate anemotactic control of their heading or course angle, since small angular errors in this measure would translate into larger deviations from direct upwind flight. Males of this species exhibit flight patterns similar to those of females, including track angles clustered about 0 when flying upwind to a source of the female-produced pheromone, but under these experimental conditions they flew with a higher average airspeed than the females. When females lose contact with an odour plume they initiate a well-defined programme of cross-wind counterturning or casting, which may normally increase their chances of retrieving contact with that plume when the wind direction shifts. The resultant track angles of females increase significantly by 0.8 s after plume loss, indicating that the female has initiated changes in both her course angle and airspeed. By 1 s after plume loss the females' track angles are no longer unimodally distributed about 0, but are bimodally distributed about -90 and +90. Males responded more rapidly to the loss of a pheromone plume, demonstrating a significant change in track angle 0.4 s after plume loss. Overall, female and male A.transitella exhibited remarkably similar anemotactic flight manoeuvres during upwind flight to odour sources as well as after plume loss.     

Visually-guided, upwind turning behaviour of free-flying tsetse flies in odour-laden wind: a wind-tunnel study

Abstract. To test the hypothesis that tsetse flies use visual input from the apparent movement of the ground to assess wind direction while in flight, Glossina morsitans morsitans Westwood females were video- recorded in a wind-tunnel as they entered, in cross-wind flight, a broad plume of simulated host odour (C0₂ at c. 0.05%). The tunnel (2.3 times 1.2 m wide) generated winds up to 0.25 m s^-1 and had a strongly patterned floor that could be moved upwind or downwind to increase or decrease the visual input due to wind drift. Flight tracks were analysed for speed, direction relative to the wind, and angle of turn. Mean groundspeeds were c. 1.8 m s^-1. In control measurements in still air (with or without odour) flies turned 50:50 'upwind': 'downwind'. With a 0.25 m s^-1 odour-perme- ated wind, 79% turned upwind, and c. 70% left view flying upwind. When the floor was moved at 0.25 m s^-1 upwind (to mimic the visual input from the ground due to a 0.5 m s_^-1 wind), the strength of this response increased. If instead the floor was moved downwind, faster than the wind speed (to mimic the visual input due to a wind from the opposite direction), 59% turned downwind and c. 70% left view flying downwind, and thus away from the source (though progressing 'upwind' in terms of the visual input from apparent ground pattern movement). Upwind turns were on average significantly larger than downwind turns. It is concluded that tsetse navigate up host odour plumes in flight by responding to the visual flow fields due to their movement over the ground (optomotor anemotaxis), even in weak winds blowing at a fraction of their groundspeed.     

Visual cues collimate the trajectories of almond moth Cadra cautella males flying in wind and still air within a wind‐formed plume of pheromone

Male Cadra cautella (Walker) moths are videotaped in three dimensions in a 3‐m long wind tunnel as they fly within a 65‐cm wide plume of pheromone. Moths are presented two floor patterns, either ‘aligned’, a 25‐cm wide ‘trail’ of solid red circles along the tunnel's midline, or ‘offset’, in which the trail veers 25 cm to the left at the tunnel's midpoint. These visual patterns are presented either in a continuous airflow or airflow that is stopped before moths reach the tunnel's halfway point. Moths fly relatively straight paths over the aligned pattern in still air after the wind is stopped. With the offset pattern in wind and when the wind is stopped, moths swerve towards the offset pattern before again progressing along the plume. Prominent visual cues appear to ‘collimate’ (i.e. align with a directional cue) the moth's course as long as the moth remains in contact with pheromone. In wind, these moths appear to favour trajectories that enhance visual feedback, even if the path taken is not directly upwind. During wind lulls, this manoeuvre may enable moths to continue progress towards calling females along a visually set course. The centring of trajectory over prominent visual cues suggests that these moths favour a route that enhances visual feedback.     

Flight speed of male spruce bud worm moths in a wind tunnel at different wind speeds and at different distances from a pheromone source

ABSTRACT. Flying male spruce budworm ( Choristoneura fumiferana [Clem.]) moths responding to virgin females and to synthetic pheromone in a wind tunnel maintained a constant rate of upwind progress when held by moving optomotor cues at a constant distance from the pheromone source. When allowed to progress upwind to the source, however, they slowed their upwind speed progressively as they approached it. They also adjusted their flight speed to maintain similar rates of upwind progress at different wind speeds.     

Zigzagging and casting as a programmed response to wind-borne odour: a review

ABSTRACT. 'Counterturning' (meaning here the execution of a succession of alternating left and right turns) is the common feature in upwind zigzagging and cross-wind casting by flying insects manoeuvring towards a small source of wind-borne odour. Recent progress in understanding its control and function is discussed. Counterturning is internally controlled ('self-steered') in the limited sense that, once initiated by a chemical stimulus, it continues without further changes in the chemical input both in clean air and in a homogeneous cloud of odour. As a reaction it appears to be the kind of chemotaxis distinguished as longitudinal klinotaxis, for which the stimulus is a difference of chemical concentration detected over time along the insect's path, not across it. The new directions taken in response to the stimulus, being self-steered in the above sense, have no necessary relation to the direction of the chemical gradient that provided the stimulus but are influenced by the visual cues generated by wind drift. In wind, the counterturning programme is modulated by changes in the chemical input and simultaneously integrated with anemotaxis, but it can then continue in similar form after the wind has ceased. Unambiguous evidence for these conclusions is so far available only for certain flying male moths responding to sex pheromone. The primary function of counterturning, of all amplitudes and in both zigzagging and casting, appears to be the regaining of contact with an elusive scent.     

Pre-exposure modulates attraction to sex pheromone in a moth

In behavioural experiments we investigated the influence of previous short exposure to sex pheromone on subsequent response of male Spodoptera littoralis moths to sex pheromone. We found that pre-exposed males showed increased sensitivity to female sex pheromone after a single exposure to a pheromone plume compared to that found in na?ve males. The increased responsiveness lasted for at least 27 h after the exposure, showing that it was not just a short-term sensitization of the males. Exposure to the odour source without upwind movement towards the source was enough to increase the responsiveness. Physical activation without exposure to odour did not affect responsiveness. The increase in responsiveness after exposure was higher when the males were pre-exposed to natural female pheromone gland extract than when they were exposed to a higher dose of the main component, even though both odour sources elicited similar upwind attraction in na?ve males. Thus, the quality of the pheromone mixture to which males were exposed influenced the subsequent response.     

Flight of male Cadra cautella along plumes of air and pheromone superimposed on backgrounds of pheromone

Male Cadra cautella were presented with five heterogeneous pheromone clouds (created from source doses of 0, 0.01, 1, 100, and 10 000 ng) with and without superimposed plumes of either clean air or sex pheromone in a wind tunnel. Moths provided with the lowest doses of background clouds without a superimposed plume did not fly upwind. Moths provided with higher doses of background clouds, with or without superimposed air plumes, increased their track, course, and drift angles (i.e., their zigzags headed more towards crosswind) with increased dose, but slowed their velocity. No differences in flight track parameters were observed for moths provided with a superimposed pheromone plume, regardless of the background cloud dose. Moreover, moths were able to locate the source of superimposed air plumes in the highest background dose, and of superimposed pheromone plumes in any background dose. The significance of these results is discussed in the context of mating disruption.     

Cowpea weevil flights to a point source of female sex pheromone: analyses of flight tracks at three wind speeds

Abstract.  Two-day-old male cowpea weevils, Callosobruchus maculatus, fly upwind to a point source of female sex pheromone at three wind speeds. All beetles initiating flight along the pheromone plume make contact with the pheromone source. Analysis of digitized flight tracks indicates that C. maculatus males respond similarly to moths tested at several wind speeds. Beetles' mean net upwind speeds and speeds along their track are similar ( P  > 0.05) across wind speeds, whereas airspeeds increase ( P <  0.01) with increasing wind speed. Beetles adjust their course angles to fly more directly upwind in higher wind speeds, whereas track angles are almost identical at each wind speed. The zigzag flight paths are generally narrow compared with most moth flight tracks and interturn distances are similar ( P  > 0.05) at the wind speeds employed. The frequency of these counterturns across the wind line is almost constant regardless of wind speed, and there is little variation between individuals. The upwind flight tracks are more directly upwind than those typically seen for male moths flying upwind toward sex pheromone sources. Male moths typically produce a bimodal distribution of track angles to the left and right of the windline, whereas C. maculatus males' track angles are centred about 0°. Preliminary examination of two other beetle species indicates that they fly upwind in a similar fashion.     

Responses of male Helicoverpa zea to single pulses of sex pheromone and behavioural antagonist

Male Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) flying in a pheromone plume respond to the loss of pheromone when they fly into a large pocket of clean air by going into crosswind casting flight in a mean of 0.48 s; 0.62 s after re‐contacting pheromone presented as a single pulse, they surge upwind in a kind of narrow zigzagging flight. After 0.36 s of surging, they lapse into casting flight once again in the clean air following the pulse. The addition of a known behavioural antagonist (Z)‐11‐hexadecenyl acetate (Z11–16:Ac), to the pheromone significantly increases the mean latency of the response to a single pulse to 0.85 s. No other aspects of the surge were significantly changed by the presence of antagonist in the single pulse of pheromone. Thus, unlike males of the related species, Heliothis virescens, which show significant changes in track and course angles when antagonist is present in single pulses, only an increased latency of response to a filament containing antagonist occurred in H. zea males. The increased latency could act cumulatively when the male is exposed rapidly and repeatedly to filaments in a natural plume and explain the profound arrestment effect of the antagonist in such plumes. The latencies to casting and surging in response to a pulse of pheromone blend are longer than those of the smaller species, H. virescens, and may be due to size‐related differences in manoeuverability of H. zea vs. H. virescens.