Aim‐then‐shoot anemotaxis involved in the hopping approach of potato tuberworm moth Phthorimaea operculella toward a sex pheromone source

Male moths locate conspecific females by pheromone‐induced upwind flight maintained by detecting a visual flow, termed optomotor anemotaxis. Their behavioural pattern is characterized by an upwind surge in response to a pheromone stimulus and crosswind casting after odour loss, which is considered to be reset and restarted on receipt of another pheromone pulse. However, pheromone‐stimulated males of the potato tuberworm moth Phthorimaea operculella exhibit a series of short and straight intermittent flights, or hops, when moving upwind. It is unclear whether they navigate by employing the same behavioural pattern and wind detection mechanism as that used by flying moths. To analyze odour‐modulated anemotaxis in male potato tuberworm moths, a flat wind tunnel is constructed to give regular odour stimuli to an insect regardless of its location. Moths are subjected to pheromone pulses of different frequencies to test whether they show a behavioural pattern that is reset and restarted by a pheromone pulse. Moths on the ground are also subjected to crosswind shear to examine their detection of wind direction. Path analyses reveal that males surge upwind when they receive a pheromone pulse and exhibit casting by successive hops when they lose odour. This behavioural pattern appears to be similar to that of flying moths. When the direction of the airflow is switched orthogonally, males adjust their course angle accordingly when they are on the ground. It is suggested that, instead of optomotor anemotaxis, this ‘aim‐then‐shoot’ system aids the detection of wind direction, possibly by mechanosensory means.     

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.     

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.     

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.     

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.     

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.     

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.     

Habitat cues synergize to elicit chemically mediated landing behavior in a specialist phytophagous insect,the grape berry moth

Many phytophagous insects locate their host plant using mixtures of volatile compounds produced by the plant. A key behavior in the host location process that has been the focus of decades of behavioral research is optomotor anemotaxis. Another key step in host location is landing on (or near) the odor source. In previous work, rubber septa emitting a synthetic blend of volatiles extracted from young shoots of grape plants, Vitus spp. (Vitaceae), elicited equivalent levels of oriented upwind flight by female grape berry moths (GBM), Paralobesia viteana (Clemens) (Lepidoptera: Tortricidae), as did actual (control) grape shoots. However, in contrast to the shoots, females did not land on the odor source. In this study, we used flight tunnel assays to investigate the landing response of GBM females with respect to chemical and visual stimuli, as well as differences in relative humidity. When stimuli were presented individually, only the synthetic blend of host plant volatiles elicited equivalent levels of oriented upwind flight compared to the plants. Interestingly, wet cotton strips elicited low but consistent levels of upwind flight. In paired assays, only the synthetic blend paired with wet cotton strips elicited landing, although at significantly lower levels than that elicited by grape shoots. To achieve landing rates equivalent to live grape shoots, grape berry moth females required all three stimuli we tested: host odor cues, moisture, and visual cues simulating a grape shoot. These results suggest the cues have a synergistic effect, and that landing behavior requires complex sensory processing using multiple sensory inputs. Furthermore, these results suggest that moisture plays an important role in the host plant location process.     

Visual ground pattern modulates flight speed of male Oriental fruit moth Grapholita molesta

Insects flying in a horizontal pheromone plume must attend to visual cues to ensure that they make upwind progress. Moreover, it is suggested that flying insects will also modulate their flight speed to maintain a constant retinal angular velocity of terrestrial contrast elements. Evidence from flies and honeybees supports such a hypothesis, although tests with male moths and beetles flying in pheromone plumes are not conclusive. These insects typically fly faster at higher elevations above a high‐contrast ground pattern, as predicted by the hypothesis, although the increase in speed is not sufficient to demonstrate quantitatively that they maintain constant visual angular velocity of the ground pattern. To test this hypothesis more rigorously, the flight speed of male oriental fruit moths (OFM) Grapholita molesta Busck (Lepidoptera: Tortricidae) flying in a sex pheromone plume in a laboratory wind tunnel is measured at various heights (5–40 cm) above patterns of different spatial wavelength (1.8–90°) in the direction of flight. The OFM modulate their flight speed three‐fold over different patterns. They fly fastest when there is no pattern in the tunnel or the contrast elements are too narrow to resolve. When the spatial wavelength of the pattern is sufficiently wide to resolve, moths fly at a speed that tends to maintain a visual contrast frequency of 3.5 ± 3.2 Hz rather than a constant angular velocity, which varies from 57 to 611° s^?1. In addition, for the first time, it is also demonstrated that the width of a contrast pattern perpendicular to the flight direction modulates flight speed.     

Optomotor regulation of ground velocity in moths during flight to sex pheromone at different heights

ABSTRACT. Males of two species of moths ( Grapholitha molesta (Busck) and Heliothis virescens (F.)) were flown in a sustained-flight tunnel in horizontal pheromone plumes. The up-tunnel velocity of the moths increased with increasing height of flight and for G.molesta was independent of tunnel wind velocities. Use of moving ground patterns verified that the height of flight above the ground was the factor related to the changes in up-tunnel velocity. Even though up-tunnel velocity increased with increased flight height, angular velocity of image motion did not. Males appeared to use visual cues from the ground pattern and from other sources to determine their up-tunnel velocities. The relationship of preferred retinal velocities to optomotor anemotaxis is discussed.     

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.     

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.     

Migration to and dispersal from oilseed rape by the pollen beetle,Meligethes aeneus,in relation to wind direction

1 Host‐plant‐odour‐induced upwind anemotaxis is accepted as the main mechanism by which herbivorous insects find their host plant within an heterogenous environment, but field data supporting this hypothesis are scarce. 2 The flight directions of the pollen beetle Meligethes aeneus to and from a plot of winter oilseed rape and the direction of the wind were recorded concurrently. The beetles were sampled by eight double‐sided window traps encircling the plot. Distal sides of the traps, relative to the plot, sampled the beetles as they flew towards the plot, whereas the proximal sides of the traps sampled them as they flew away from the plot. Paired data on daily catch of beetles in distal or proximal traps and the volume of air impacting each trap were compared. 3 Correlations between daily catch of M. aeneus into distal traps and trap wind volume were negative, indicating that flights by both overwintered‐ and new‐generation insects towards the plot were upwind. 4 Correlations between daily catch of M. aeneus into proximal traps and trap wind volume varied with generation. Catch of overwintered‐generation M. aeneus was negatively correlated with trap wind volume, indicating that flight was upwind. Proximal trap catch of the new‐generation M. aeneus was weakly/modestly positively correlated with trap wind volume, indicating that flights were downwind or crosswind. 5 Understanding the effect of wind direction on flight of M. aeneus holds potential for improving the forecasting of their arrival and spatial distribution on the crop for integrated pest management.     

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.     

Factors influencing the landing of maleEpiphyas postvittana (Walker) exhibiting pheromone-mediated flight (Lepidoptera: Tortricidae)

The effects of changes in various visual and olfactory properties of a white card surface on the landing position of male Epiphyas postvittanaexhibiting pheromone-mediated flight were studied in a wind tunnel. Males landed predominantly at the most downwind position of a surface in line with the pheromone source, regardless of the strength of the source. The position on the surface that males landed was strongly influenced by visual factors. The landing position of males appeared to be influenced by visual cues along all three axes of the surface. Decreases in either the dimension horizontally perpendicular to the wind direction or the vertical dimension resulted in greater numbers of males landing farther upwind on the surface than the downwind edge. Visual changes in the axis along the wind direction also affected the position at which males landed. For example, when presented with two white card surfaces with a 4- cm gap between them, males tended to land on the downwind edge of the upwind surface (on which the source was located). When the gap was bridged with clear Mylar, the landing pattern was significantly different, with the greater proportion of males landing on the downwind surface. However, when Mylar was placed on the plexiglass floor of the tunnel (in addition to bridging the gap), the landing pattern on the surface was not significantly different from that on the two surfaces without the Mylar bridge. It is suggested that during the prelanding and landing phases of pheromone-mediated flight, male moths orient to visual features of the surface containing the pheromone source rather than to visual features of the source (conspecific female moth) itself.     

The effect of wind speed on the flight responses of tsetse flies to CO2: a wind-tunnel study

Abstract. Female Glossina morsitans morsitans Westwood were video-recorded in a wind-tunnel as they entered, in cross-wind flight, a broad plume of CO₂ (a component of host odour). At a wind speed that corresponds with peak catches in the field (c. 0.6 ms-¹) odour produced both significant upwind turning responses (in-flight anemotaxis) and kinetic responses (reduced flight speed and increased sinuosity (m-¹). At a wind speed of c. 0.2 ms-¹ flies displayed anemotactic, but not kinetic, responses to odour. At very low wind speeds (0.1ms-¹) neither upwind turning responses nor kinetic responses to odour were detected. The results are discussed with regard to current theory of host-location by tsetse.     

Importance of the experimental setup in research on attractiveness of odours in moths: an example with Busseola fusca

Wind tunnel and Y‐tube olfactometer studies are useful for demonstrating the responsiveness of male moths to sex pheromones. However, in the cereal stem borer, Busseola fusca (Fuller) (Lepidoptera: Noctuidae), wind tunnel bioassays yielded poor results when the behavioural responses of females to plant odours were tested. We demonstrated that for B. fusca females, the Y‐tube olfactometer was better suited for measuring the attractiveness of plant odours, compared with the wind tunnel. In particular, we showed B. fusca preference for odours of a host over a non‐host plant species using this apparatus. Behavioural responses for B. fusca after host finding are also discussed.     

风洞内粘虫飞翔行为与气流的关系

利用自制的昆虫飞翔实验风洞 ,系统观测了在风洞条件下粘虫在不同流速实验气流中的起飞行为与飞翔行为。结果表明 ,微风能刺激粘虫起飞 ,试虫表现明显的偏爱迎风 (或稍偏一点角度 )起飞的习性 ,飞翔时亦多采取迎风 (或稍偏一点角度 )的姿势。试虫在气流中的实际位移是昆虫飞翔位移与气流位移的矢量和。当气流速度小于 2 m/ s时 ,逆风向位移占多数 ;而气流速度为 3～ 4 m/ s时 ,94 .8%的试虫为顺风向位移。     

Anemotactic responses of the predatory mite,Phytoseiulus persimilis Athias-Henriot,and their role in prey finding

Although it is well established that the predatory mite Phytoseiulus persimilis Athias-Henriot responds to odour emanating from leaves infested by its phytophagous prey, the two-spotted spider mite Tetranychus urticae Koch, little is known of the behavioural mechanisms elicited by odour perception and how they contribute to finding the prey. In this paper the influence of prey-related odour on orientation to wind direction is discussed. It was analysed by observing the predator's walking paths in still air and in an air stream uniformly permeated either with or without prey-related odour stimuli. The results show that well-fed predator females move upwind in presence of these stimuli, but downwind otherwise. Starved predators always move upwind. The anemotactic responses observed are therefore both odour-conditioned and (feeding) state-dependent.In an attempt to explain these responses it is argued that the anemotactic responses of well-fed predators may contribute to arrestment within the area marked by a cluster of prey-colonized leaves. The anemotactic responses of starved predators may help them to find clusters of spider mite colonies located upwind. Why predatory mites also move upwind in absence of prey-related odour stimuli, is a question that remains to be answered.     

Responses of male Mediterranean fruit flies, Ceratitis capitata, to trimediure in a wind tunnel of novel design

ABSTRACT. The responses of male Ceratitis capitata (Wiedemann) (Diptera; Tephritidae) to trimediure were investigated in a wind tunnel of novel design with disposable plastic walls. Trimediure was presented to the flies either in the form of a discrete 'plume' or uniformly dispersed in the air passing through the tunnel. The flies showed an increase in flight activity in response to the two forms of stimulation and performed a zig-zag anemotactic flight in response to the plume, reminiscent of the behaviour of moths responding to a sex pheromone. They performed a straight, upwind, anemotactic response to the uniformly dispersed odour. The design of wind tunnel used in these tests was found to have several advantages: air flow and turbulence can be easily varied and the plastic walls can be changed to eliminate contamination problems.