Effects of pheromone plume structure and visual stimuli on the pheromone-modulated upwind flight of male gypsy moths (Lymantria dispar) in a Forest (Lepidoptera: Lymantriidae)

The pheromone-modulated upwind flight ofLymantria dispar males responding to different pheromone plume structures and visual stimuli designed to mimic trees was video recorded in a forest. Males flying upwind along pheromone plumes of similar structure generated tracks that were similar in appearance and quantitatively similar in almost all parameters measured, regardless of the experimentally manipulated visual stimuli associated with the pheromone source. Net velocities, ground speeds, and airspeeds of males flying in point-source plumes were slower than those of males flying in the wider, more diffuse plumes issuing from a cylindrical baffle. The mean track angle of males flying in plumes issuing from a point source was greater (oriented more across the wind) than that of males flying in plumes issuing from a transparent cylindrical baffle. Males flying in point-source plumes also turned more frequently and had narrower tracks overall than males responding to plumes from a cylindrical baffle. These data suggest thatL. dispar males orienting to pheromone sources (i.e., calling females) associated with visible vertical cylinders (i.e., trees) use predominantly olfactory cues to locate the source and that the structure of the pheromone plume markedly affects the flight orientation and the resultant track.     

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.     

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.     

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.     

Influence of plume structure and pheromone concentration on upwind flight of Cadra cautella males

Abstract. The effects of pheromone plume structure and its concentration on the pheromone-mediated flight of male Cadra cautella (Lepidoptera: Phycitinae) were investigated in a laminar-flow wind tunnel. When two C. caurella males flew simultaneously along a ribbon plume of mixed smoke and pheromone, their inflight behaviour was dependent on the instantaneous structure of the plume they encountered. When a male intercepted an intact ribbon filament, he sustained a crosswind course, whereas when he intercepted a turbulent filament (created by an upwind male fragmenting the ribbon plume), he adopted a flight course more due upwind. These results indicate that C. cautella males altered their in-flight manoeuvres in response to instantaneous changes in the fine structure of the pheromone plume. We also demonstrated that differences in the fine structure of the plume had more influence on the flight pattern of C. cautella males than a 1000-fold range in pheromone dose. The size of the plume was increased by adding wind deflectors upwind of the pheromone source, independent of source dosage, males following ribbon plumes flew slow zigzag tracks, whereas males following large, turbulent plumes flew directly to the source in fast, straight tracks with less counterturning.     

The effects of unilateral antennectomy on the flight behaviour of male Heliothis virescens in a pheromone plume

Abstract .Unilaterally antennectomized Heliothis virescens (F.) males flying close to the central axis of a plume of sex pheromone display no significant differences in behaviour compared to sham-operated males in course angles, track angles, airspeed and groundspeed. This demonstrates that right/left antennal information is not necessary for normal orientation movements in response to pheromone, but rather that it is 'blended' within the moth's central nervous system before pheromone-mediated manoeuvres are made. However, some unilaterally antennectomized moths (36%) make repetitive, asymmetrical, saw-tooth-shaped tracks during pheromone-mediated upwind progress, whereas control moths never make such tracks. Unilaterally antennectomized moths made such tracks on the side of the plume contralateral to the missing antenna. We hypothesize that these occasional asymmetrical tracks in unilaterally ablated males are the result of reiterative asymmetrical pheromone stimulation of a higher probability on track legs going toward rather than away from the long axis of the plume on males with a single antenna remaining on the 'away from axis' side. Combined with a greater propensity for treated moths to lock onto the plume away from the central axis on one side rather than the other, repetitive successive asymmetrical track legs (resulting in a saw-tooth-shaped track) are commonly observed in these moths. Control moths do also make asymmetric successive track legs but they rarely are repeated and thus are not readily observed.     

Effect of a vertical object on the sex pheromone-mediated flight and landing behaviors of the male lightbrown apple moth,Epiphyas postvittana (walker) (Lepidoptera: Tortricidae)

A small (2.5-cm-wide) vertical (10-cm-high) white object influenced the sex pheromone-mediated flight and landing behaviors of maleEpiphyas postvittana. When the vertical object was positioned on a horizontal surface to the side (3–5 cm) and upwind of a pheromone source (in the middle of the surface), the distribution of landing positions of males on the surface was different from that when the object was not present; males tended to land in positions skewed toward the side of the source that the object was on. The closer the object was positioned to the source, the greater the number of males that landed on the object (rather than on the horizontal surface). This difference in landing positions (when the object was present) corresponded with changes in the flight tracks; the tracks of males flying to the surface with an object were skewed toward the object and had higher amplitude intertrack reversal distances than the tracks of males flying to a surface without a vertical object. Positioning of a vertical object progressively upwind of the source resulted, apparently, in decreased effects on the landing (and presumably flight) behavior of males. The effect of the vertical object on the flight and landing behaviors of males corresponded largely with changes in pheromone plume structure (visualized with smoke) induced by the extra turbulence in the airflow over the source. Thus it appears that the vertical object influences the behavior of maleE. postvittana largely through the olfactory sensory modality. However, when a clear, Mylar object, in place of the white object, was placed on the surface, more males landed on the Mylar object (than did on the white object), suggesting that the vertical object may also influence the behavior of males through the visual modality.     

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     

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.     

Odor tracking flight of male Manduca sexta moths along plumes of different cross-sectional area

Males of the hawkmoth, Manduca sexta, track wind-borne plumes of female sex pheromone by flying upwind, while continuously turning from side-to-side and changing altitude. Their characteristic “zigzagging” trajectory has long been thought to result from the interaction of two mechanisms, an odor-modulated orientation to wind and a built-in central nervous system turning program. An interesting and as of yet unanswered question about this tracking behavior is how the cross-section of an odor plume or its clean-air “edges” affects moths’ odor tracking behavior. This study attempts to address this question by video recording and analyzing the behavior of freely flying M. sexta males tracking plumes from pheromone sources of different lengths and orientations with equal odor concentration per unit area. Our results showed that moths generated significantly wider tracks in wide plumes from the longest horizontally-oriented sources as compared to narrower point-source plumes, but had relatively unaltered tracks when orienting to plumes from the same length sources oriented vertically. This suggests that in addition to wind and the presence of pheromones, the area of the plume’s cross section or its edges may also play an important role in the plume tracking mechanisms of M. sexta.     

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

1. 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.     

Field and laboratory electroantennographic measurements of pheromone plume structure correlated with oriental fruit moth behaviour

Abstract. Peak-to-trough electroantennogram amplitudes (bursts), caused by the individual filaments of a plume of female pheromone, diminish as high-emission-rate sources are approached by male Grapholita molesta , and this reduction is correlated with in-flight arrestment (ceasing to advance upwind). These findings are consistent with the hypothesis that one cause of in-flight arrestment in response to high-concentration point sources is the attenuation of the peak-to- trough amplitudes close to the source. High burst frequency, high pheromone flux, or low levels of continuous neuronal activity all are less well correlated with arrestment. Rather, arrestment appears due to a reduction of chemosensory input to the CNS during flight up the plume, even though the actual molecular concentration continues to increase. In a laboratory wind tunnel, upwind flight initiation by more than 20% of males was elicited only by pheromone source concentrations evoking significant fluctuations in EAG amplitudes at downwind release points. The burst frequencies that evoked high levels of upwind flight initiation ranged from a mean of 0.4-2.2 bursts/s. Because a previous study revealed that flying male G. molesta change their course angle within 0.15 s of losing or contacting pheromone, these EAG burst frequencies indicate that during flight in a pheromone plume, many manoeuvres are probably made in response to contact with individual plume filaments. Thus, upwind flight tracks may be shaped by hundreds of steering reactions in response to encounters with individual pheromone filaments and pockets of clean air. Field-recorded EAGs reveal that burst amplitudes diminish from 3 to 30 m downwind of the source, whereas burst frequencies do not, averaging c. 1/s at 3, 10 and 30 m downwind.     

Upwind anemotaxis in response to cue-lure by the Queensland fruit fly, Bactrocera tryoni

Movements of mature male Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) were observed individually in a wind tunnel under conditions of ‘cue-lure with wind’, ‘cue-lure with no wind’, ‘wind only’ and ‘no wind or cue-lure’. Further observations were made using a dense foliage array in the wind tunnel and a structured plume of cue-lure. Patterns of walking or flying were essentially the same in all of the first four treatments except that in the ‘cue-lure with wind’ treatment, over half of the flies moved in a consistent track upwind for at least 400 mm at some time during the first 5 min of observation. With clean wind, only 10% of the flies did this. The result was that mean net upwind displacement after 5 min in the ‘cue-lure with wind’ treatment significantly exceeded that in the other three treatments, the results of which did not differ significantly from each other. The upwind tracks were accomplished by either walking or flying (with or without stops) or by a combination of both. When the wind tunnel was filled with a dense foliage array, the results with cue-lure laden wind were similar to those obtained with the equivalent treatment without foliage, except that upwind tracks were predominantly in short stages. When flies were exposed to a structured plume of cue-lure odour (without foliage present), they did not apparently alter their behaviour on leaving or entering the plume, but some did make consistent upwind tracks while they were in the plume.     

Emergence, Mating, and Postmating Behaviors of the Oriental Beetle (Coleoptera: Scarabaeidae)

In a previous field-trapping study of the oriental beetle, Exomala orientalis (Waterhouse), by using synthetic sex pheromone on golf course fairways, numerous males were observed and trapped during the hours of peak mating activity. However, very few beetles were observed in the same areas when synthetic pheromone was absent. To investigate the hypothesis that mating in nature occurs cryptically within vegetation at the soil surface, laboratory studies on female emergence and pheromone release, male emergence and mate-locating, and female and male mating behaviors were conducted. Mate acquisition and copulation occurred on the soil surface near the female emergence site, with both sexes engaging in pheromone-mediated behaviors after having emerged from the soil. A highly stereotyped female pheromone release, or calling, behavior was observed, consisting of insertion of the female's head into the soil and elevation of the tip of her abdomen into the air. Bioassays conducted in a wind tunnel that simulated a turf fairway environment showed that walking and flying were both important in the upwind response of males to females. Mating and copulation occurred without an obvious complex courtship, but observations of postmating behaviors suggested that mate guarding occurs.     

Effects of varying sex pheromone component ratios on the zigzagging flight movements of the oriental fruit moth,Grapholita molesta

As the ratio of (E)-8-dodecenyl acetate (E8–12Ac) to (Z)-8-dodecenyl acetate (Z8–12Ac) increased past optimal low levels in the pheromone blend, fewer males were able to fly 2.5 m upwind to the source. The tracks of males that flew in plumes of such high-(E)off-blends were slower and narrower than those of males flying to lower-(E)blends. The tracks were narrower, first of all, because as the proportion of E8–12Ac increased, the males steered more into the wind. More of their thrust was directed upwind and therefore their groundspeed to either side of the windline was reduced. In addition, males also reduced their airspeeds to high-(E)blends, which contributed to the decreased groundspeeds and narrower tracks. No significant changes in the frequency of counterturning were found in response to increasing proportions of E8–12Ac. The inability to continue upwind flight in a plume of an off ratio was indicated by in-flight arrestment in the plume. Arrestment resulted from changes in the course angles steered by the males and the airspeeds flown.     

Flight of Heliothis virescens males in the field in response to sex pheromone

Abstract. The behaviour of Heliothis virescens males flying upwind in the field in a sex pheromone plume was videorecorded and analysed. Males flew faster and straighter, with less counterturning, and heading more directly into the wind when they were 9-11m away from the odour source than when they were 1–3 m away. Regardless of their distance from the source or the windspeed, they maintained an average groundspeed of c. 200 cm s^_1, except when they arrived within 1 m of the source, when their groundspeed slowed significantly. Two or more males flying in the plume at the same instant often exhibited either extremely straight and directly upwind tracks or else zigzagging tracks with significant counterturning (as did males flying through the field of view of the cameras at slighdy different times). The males' position, either in the centre of the plume's axis or along one side, might explain these differences in track straightness, which previous studies with H.virescens have shown to be caused by higher frequencies of contact with plume filaments. When a significant shift in wind direction occurred, males tended to make an initial movement in the direction of the shift, perhaps due to latencies of response in both the olfactory and visual systems associated with flying into clean air. The males' behaviour in the field overall was similar to that observed in the wind tunnel, except that their airspeeds and groundspeeds were significantly higher than those observed in the laboratory. The fact that they flew faster in the field can be explained both by the significandy higher windspeeds that males need to compensate for in the field to attain a preferred velocity of image motion, as well as by a higher height of flight over the ground in die field causing a slower apparent motion of images at a given groundspeed compared with the laboratory.     

Manoeuvres of female Brachymeria intermedia flying towards host-related odours in a wind tunnel

Abstract. Mature female Brachymeria intermedia (Hymenoptera: Chalcididae) were conditioned to fly towards vanilla odour in a wind tunnel. We analysed the tracks of wasps flying along turbulent plumes of either host odour (pupae of the gypsy moth, Lymantria dispar) or vanilla odour, along either a ribbon plume or a turbulent plume of vanilla odour, and before and after plume removal. Wasps flew in similar shallow zigzagging tracks along the turbulent plume of host and vanilla odours. When the plume was removed while wasps were flying upwind along a turbulent plume of vanilla odour, wasps either maintained an upwind course or drifted sideways, alternating upwind and downwind courses before turning around and flying downwind. No wasp casted upon loss of the plume.     

Flying Slower: Floor Pattern Object Size Affects Orthokinetic Responses During Moth Flight to Sex Pheromone

Previous studies with Oriental Fruit Moth (OFM, Grapholita molesta) and Heliothis virescens males flying upwind along a pheromone plume showed that they increased their upwind flight speed as they flew higher above striped floor patterns and, for OFM, to a similar degree over dotted floor patterns. This response pattern has been demonstrated in another moth species, Epiphyas postvittana and in a beetle, Prostephanus truncatus. In all cases the role played by the change in angular size of the wind tunnel’s ventral floor pattern was not assessed. In the present study we specifically addressed this question with a systematic examination of moths’ flight control over different sizes of transverse stripes and dot patterns ranging down by halves from 5 to 0.625 cm and a blank white floor as a control, and showed that OFM males fly faster upwind and along their flight paths over floor patterns of decreasing size. Increased speeds over striped patterns were evident as stripe width decreased below 2.5 cm, whereas moths did not increase their flight speed over dot patterns until dot size had decreased to less than 1.25 cm. Another flight component that the moths can actively control, their course angles, was unchanged above both patterns, except for moths flying over 5 cm stripes. Turning frequency and interturn distances were mostly unchanged or offset each other, negating any effects on upwind progress. As in an earlier study examining flight speeds at three heights above floor patterns of three densities, the moths’ changes in speed appear to be exclusively affected by changes in their orthokinetic response to the size of the floor pattern objects.     

Impact of (Z)-7-dodecenol and turbulence on pheromone-mediated flight manoeuvres of male Trichoplusia ni

Abstract. Turbulence and chemical noise are two factors which may influence pheromone-mediated flight manoeuvres of a moth in natural habitats. In this study, the effects of turbulence and the behavioural antagonist (Z)-7-dodecenol on flight manoeuvres of male Trichoplusia ni (Hübner) were evaluated in a wind tunnel. Male moths increase airspeed and course angles when turbulence is increased. This leads to significant increases in the length of flight tracks, but significant reductions in the time taken to reach a pheromone source. In less disturbed pheromone plumes, distributions of course angles and track angles of male T.ni show a prominent peak centred about 0° relative to the upwind direction, indicating that moths can temporarily steer directly upwind toward a pheromone source.
When (Z)-7-dodecenol is released 10 cm upwind of a pheromone source to form an overlapping plume downwind, course angles, airspeeds and ground-speeds of male T.ni are reduced significantly compared with those in uncon-taminated pheromone plumes. This results in a longer flight time to reach a pheromone source. The decrease in flight speed would decrease the rate of contact with filaments, and thereby perhaps allow the moth to detect uncon-taminated pheromone filaments independently from filaments containing the behavioural antagonist.