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.     

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.     

Flying Faster: Flight Height Affects Orthokinetic Responses During Moth Flight to Sex Pheromone

Male Oriental Fruit Moths (Grapholita molesta) flew faster toward a pheromone source as they flew higher above striped and dotted floor patterns. The moths significantly (P?<?0.05) increased their ground speed over floor patterns of transverse stripes or pseudo randomly placed dots. The moths’ track angles (flight path angle off the windline) decreased significantly (P?<?0.05) when they flew 40 cm above the floor patterns vs. flight at 10 cm up, and they tended to steer more upwind flight (smaller course angles) at the upper, 40 cm, height compared to 10 cm up. Turn frequencies and reversal distances across the wind line were also affected by dot density. However, the interaction of small changes in flight speed, course angle, turn widths and turn frequencies are difficult to assess; I have subsumed all their affects into a simple measure of “total distance” flown by the moths by summing the length of all flight vectors analyzed for the other metrics, but no differences were found. By far, the largest change in flight was the positive orthokinetic response to increased flight height above both striped and dotted floor patterns (Fig. 2; P?<?0.05), and nearly all other changes appear to be entirely due to faster moth flight with little or no changes in steering or turning patterns.     

Orientation of male gypsy moths,Lymantria Dispar (L.), to pheromone sources: The role of olfactory and visual cues

The role of olfaction and vision in the close-ranging flying and walking orientation of male gypsy moths, Lymantria dispar(L.), to females was studied in the forest and in the laboratory. In the forest, feral males found an isolated pheromone source as readily as one supplemented with female visual cues; dead, acetonerinsed females deployed without pheromone received virtually no visitations. In flight tunnel choice experiments using cylinders as surrogate trees and pheromone in different spatial configurations, visual attributes of the female did not influence either the males' choice of landing site or the efficiency with which they located the female. Rather, the presence of pheromone on the cylinder was necessary to elicit orientation as well as landing and walking on the cylinder. When a female visual model was placed in various positions around a pheromone source, walking males oriented primarily to the chemical stimulus. There were, however, indications that males would alter their walking paths in response to female visual cues over short distances (<5 cm), but only if they continued to receive pheromone stimulation. When visual and chemical cues were abruptly uncoupled by altering the trajectory of the pheromone plume, most males responded to the loss of the odor cue rather than to visual cues from the female. Temporal pheromone stimulation patterns affected male walking orientation. When stimulated by pheromone, males oriented toward the source; loss of the odor cue prompted an arearestricted local search characterized by primarily vertical and oblique movements with frequent reversals in direction. Presumably these maneuvers enhance the likelihood of recontacting the plume or serendipitously encountering the female. The apparent lack of visual response to the female is discussed in light of morphological and behavioral evidence suggesting that gypsy moths were formerly nocturnal.     

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     

Physiological age-grading and ovarian physiology of Prostephanus truncatus

Abstract. The reproductive tracts of male and female Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) were described for beetles between emergence and 30 days old in order to determine age-grading criteria. Seminal vesicles were bigger among non-mated males than among mated males due to accumulation of sperm; no age-specific differences were found for male P. truncatus. Ovaries (germarium size, number of follicles and follicle size) were similarly developed for females between 5 and 30 days old and did not differ between mated and non-mated females. Starved females were found to resorb follicles. Yellow body formation was strongly dependent on age, and was used as an age-grading criterion for female P. truncatus. Females flying off maize cobs and caught with pheromone traps were of varying physiological age and mated, and their ovarian development was suspended. All migrating females were mated, indicating that lone females may act as colonizers, independently of males. The applicability of migration theories to P. truncatus and adaptive inter-reproductive dispersal as part of its life history strategy are discussed.     

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.     

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.     

Reduced antennal sensitivity, behavioural response, and attraction of male codling moths, Cydia pomonella, to their pheromone (E,E)-8,10-dodecadien-1-ol following various pre-exposure regimes

The effects of pre‐exposing male codling moths, Cydia pomonella (L.) (Lepidoptera: Tortricidae), to their pheromone (E,E)‐8,10‐dodecadien‐1‐ol (codlemone), in static and moving air, under laboratory and field conditions, on subsequent antennal sensitivity, behavioural responsiveness, and attraction to codlemone were investigated. In flight tunnel experiments, the percentage of moths wing fanning and taking flight were mostly unaffected, but upwind flight to, and contact with, pheromone sources known to elicit responses of both were shown to depend on the intensity and duration of previous exposure to codlemone and recovery time between exposure and assessment. Ten to 30‐min pre‐exposures to codlemone in static air (≈ 35 µg l^?1) not only caused a 99% reduction in attraction, but also significantly reduced electroantennogram response to codlemone. Recovery of full antennal sensitivity to codlemone took more than 1 h, but recovery of attraction took over 4 h, suggesting that habituation is also partially involved in reduced behavioural responsiveness following pre‐exposure. Seventy‐five min exposures to codlemone in moving air (5–10 cm s^?1) at rates of 0.9, 4.5, and 18 µg h^?1 from Celcon fibres caused 75, 86, and 99% disruption, respectively. However, 30–34‐h exposure of caged moths to air moving through an orchard treated with 1000 Isomate‐C® dispensers ha^?1 releasing approximately 20 µg h^?1 per dispenser during tests, had no impact on moth response in flight‐tunnel assays 30 min after removal from the orchard. In this treated orchard, catches of free‐flying moths in pheromone‐baited traps were completely inhibited. If observed mechanisms such as long‐lasting antennal adaptation or habituation of the central nervous system contribute to the disruption of pheromone communication among codling moths under field conditions, it seems unlikely that they occur following exposure to the average atmospheric concentrations of codlemone. For these effects to be important, codling moths may require close contact with pheromone sources for extended periods, or repeated close encounters.     

Spring dispersal ofSitona lineatus: The use of aggregation pheromone traps for monitoring

The spring dispersal ofSitona lineatus L. (Coleoptera; Curculionidae) was investigated on a Danish farm.S. lineatus dispersed by flight in the early spring on sunny, calm days with temperatures above ca. 15°C. Two thirds of the population ofS. lineatus dispersed from perennial leguminous crops (clover and lucerne) in the first period of flight activity. The next dispersal did not occur until one month later despite several intermediate flight activity periods. The first period of dispersal occurred before the germination of the spring sown summer host crop,Vicia faba L. The field bean crop was infested in three later invasions during a period of more than three weeks. The aggregation pheromone, 4-methyl-3,5-heptanedione, had a significant effect on captures of both males and females in cone traps placed on the ground. There was no effect of the pheromone on captures in yellow sticky traps placed 1.5 m above ground. The pheromone effect is discussed in relation to behavioural observations. Both types of traps may be used in a survey system for monitoring spring dispersal ofS. lineatus and optimal timing of insecticide spraying. However, the pheromone cone traps were highly specific whereas all kinds of flying insects were caught in the yellow sticky traps, thus making the latter traps less suitable for monitoring.     

Close-range behaviour of male pea moths, Cydia nigricana, responding to sex pheromone re-released via the substrate

The close-range orientation behaviour of male pea moths, Cydia nigricana (F.) (Lepidoptera: Tortricidae), to a substrate contaminated with synthetic sex pheromone was studied in the field. The substrate was a sheet of polypropylene grass on a 1 m diam arena, on the upwind edge of which a pheromone trap had been placed previously for 1 h. After removal of the trap, moths continued to be attracted to the arena and to the vacated trap position. Video-recorded tracks showed that the moths behaved anemotactically whilst on the arena. When the arena was revolved so that the vacated trap position was on the downwind edge, moths continued to fly upwind on the arena, even though they were flying away from the original trap position and down a concentration gradient.     

Free flight capacity determination in a sustained flight tunnel: effects of age and sexual state on the flight duration of Prostephanus truncatus

Abstract. . Adult Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) steering anemotactically upwind to a pheromone source in a wind tunnel, respond normally to, and alter their ground speed according to the direction and speed of, the movement of ground patterns beneath them. By manipulating this optomotor reaction component of their behaviour, studies were conducted on their flight duration. The results show a great deal of individual variation in flight duration, and the general data on single flights were skewed towards short flights. Pre-reproductive and inter-reproductive male and female beetles flew significantly longer than older beetles that had passed their peak of reproduction. There was no significant difference in the flight duration of male and female beetles at any age. The overall results suggest mat younger P. truncatus are capable of long-distance flights, and support the proposition that flight could be important in the spread of the beetle.     

Sexual differences in the flight performance of the oriental fruit moth, Cydia molesta

Cydia molesta Busck (Lepidoptera: Tortricidae), a major pest of stone fruits and an increasingly important late season pest of apple, is predominately monitored by pheromone trapping of male moths. We investigated flight performance in relation to sex, age, and mating status using computer-linked flight mills, and also examined the relationship between female flight and reproduction. The crepuscular flight pattern of the experimental moths in relation to photointensity was very similar to that reported from field studies. Female moths significantly outperformed males in all measured flight parameters including total distance flown, distance of longest single flight, and velocity. The proportion of long-flying females (categorised as those completing an unbroken flight of greater than 1 km) was three to six times greater than that of males. Female flight performance was not related to mating status, but mated males displayed significantly greater flight than unmated males. The maximal flight period of mated females commenced on the third day after eclosion, following 30% egg deposition. Male flight was not significantly related to age. The data suggest that a limited proportion of the population, in particular females, may have the capacity to make inter-orchard flights. The limitations of monitoring C. molesta populations in apple orchards solely by pheromone trapping of males are discussed.     

Oriented flight responses of female Mediterranean fruit flies to calling males, odor of calling males, and a synthetic pheromone blend

Male Mediterranean fruit flies,Ceratitis capitata (Wiedemann), produce volatile chemicals thought to be attractive sex pheromones. We demonstrated for the first time that male odor elicits upwind flight and zigzagging upwind flight patterns in mature unmated females. Such flight patterns indicate the mechanisms involved in female location of the pheromone source and arrival at that source. Similar female oriented upwind flight responses occurred with a three component blend comprised of ethyl-(E)-octenoate, geranyl acetate, andE,E-alpha farnesene. These findings clarify the role of male sex pheromone in mate-location strategies in this species and provide new bioassay criteria for evaluating attraction responses to male pheromone and synthetic blends.     

Trapping and sex pheromone-mediated flight and landing behaviour of maleCtenopseustis obliquana

A sex pheromone-baited delta trap was found to be inefficient at eliciting landing and entering of the trap by maleCtenopseustis obliquana. The inefficiency of the delta trap related to turbulence altering the pheromone plume and the concomitant effect on the flight manoeuvres of male moths. In the wind tunnel, high proportions of males flew upwind and landed on the sides, outside, of the trap, but only a relatively small proportion of these males entered the trap and contacted the sticky surface. When males approached the delta trap, they tended to fly in wide zigzags (i.e., large inter-track reversal distances) and at an altitude near the top of the trap, where the trap was relatively narrow in width (compared to the bottom). Thus, these flight manoeuvres largely precluded males from entering the trap. Greater numbers of male moths entered the trap when: (i) the front barriers of the delta trap were removed, (ii) pheromone dosage was increased to 300 μg, and (iii) the trap design was changed to a rectangular one. The first two changes appeared to influence the flight manoeuvres of males (who appeared to fly with narrower inter-track reversal distances), while the third change apparently did not affect the glight manoeuvres of males, but rather allowed more males to enter the trap because of the greater area of the entrance. The low trap catches of maleC. obliquana in the field are also a consequence of the glue which is currently used. After contact with this glue most males are able to escape, flying off the sticky surface and losing contact with the pheromone. A field trial found that delta traps with another glue caught more than three times the number of males of the related tortricid moth,Epiphyas postvittana, than delta traps with the currently used glue.     

Investigations of Mechanisms of Pheromone Communication Disruption of Choristoneura rosaceana (Harris) in a Wind Tunnel

Although atmospheric treatment with synthetic pheromone is used commercially to control several lepidopteran pests, little is known about how mate-finding behavior is altered by this procedure. Mechanisms of disruption of the mate-finding behavior of Choristoneura rosaceana (Lepidoptera: Tortricidae) were examined in wind tunnel bioassays. Male moths were exposed to synthetic sex pheromone or pheromone components prior to or during upwind flight to a calling virgin female. The proportion of males successfully contacting a calling female was reduced only when the synthetic pheromone treatment was presented simultaneously. A synthetic source of the attractive four-component pheromone placed upwind of a calling female was more effective than a less attractive two-component blend in achieving disorientation. Habituation of the central nervous system does not appear to be a significant factor in disruption of mate-finding behavior of male C. rosaceana, as exposure to pheromone prior to the bioassay did not alter the proportion of males that achieved subsequent upwind flight. Disruption of mate-finding behavior of C. rosaceana in a wind tunnel is probably the result of a combination of mechanisms including adaptation of antennal receptors, camouflage of the female-produced plume, and false-trail following which contributed to the additive disruption effect observed with the most attractive four-component pheromone.     

Mating disruption in Agrotis segetum monitored by harmonic radar

The long-range, pheromone-mediated, flight behaviour of male moths under natural and mating disruption conditions was monitored by means of harmonic radar. Individual male turnip moths, Agrotis segetum (Denis & Schiffermüller) (Lepidoptera: Noctuidae), tagged with radar transponders, were released and tracked in plots with or without disruptive doses of sex pheromone. In addition, male attraction to pheromone-baited traps and mating of calling females in treated and untreated plots was investigated. High doses of a four-component pheromone blend reduced trap catch by 79% and mating of females by 62% when compared with control plots in pre-radar experiments. Surprisingly, this effect was not associated with any pronounced differences in flight behaviour of males between a treatment and a control plot as revealed by harmonic radar recordings. In total, 20 flight tracks from a control plot and 22 flight tracks from a treatment plot were analysed. Moths could be followed for up to 77 min, corresponding to a track length of 7350 m. Mean ground speed ranged from 0.7 m s^–1 to 5.4 m s^–1. There was a strong trend (P = 0.06) for a greater number of male orientations to traps from downwind in the control field compared to the treatment field. Many flight tracks were fragmented due to radar shadow. Advantages and constraints using harmonic radar to study the pheromone-mediated flight behaviour of nocturnal moths are discussed.     

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.     

Modeling flight activity and population dynamics of the pine engraver, Ips pini, in the Great Lakes region: effects of weather and predators over short time scales

Ascertaining the relative effects of factors such as weather and predation on population dynamics, and determining the time scales on which they operate, is important to our understanding of basic ecology and pest management. In this study, we sampled the pine engraver Ips pini (Say) (Coleoptera: Scolytidae) and its predominant predators Thanasimus dubius (F.) (Coleoptera: Cleridae) and Platysoma cylindrica (Paykull) (Coleoptera: Histeridae) in red pine plantations in Wisconsin, USA, over 2 years. We sampled both the prey and predators using flight traps baited with the synthetic aggregation pheromone of I. pini. Flight models were constructed using weather variables (temperature and precipitation), counts of bark beetles and their predators, and temporal variables to incorporate possible effects of seasonality. The number of I. pini per weekly collection period was temperature dependent and decreased with the number of predators, specifically T. dubius in 2001 and P. cylindrica in 2002. The number of predators captured each week was also weather dependent. The predators had similar seasonal phenologies, and the number of each predator species was positively correlated with the other. Including a term for the number of prey did not improve the model fits for either predator for either year. Our results suggest that exogenous weather factors strongly affect the flight activity of I. pini, but that its abundance is also affected by direct density-dependent processes acting over weekly time scales. Adult predation during both colonization and dispersal are likely processes yielding these dynamics.     

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.