Turbulence, trees and semiochemicals: wind-tunnel orientation of the predator, Rhizophagus grandis, to its barkbeetle prey, Dendroctonus micans

Abstract. Insects apparently responding to the visual stimulus offered by a tree or other object may also be responding to the variety of physical effects caused by the obstruction, including turbulence, a reduction in wind velocity and eddies. The relative importance of prey odour associated with the bark beetle Dendroctonus micans (Kugelann) (Scolytidae), prey-host-tree odour, silhouette, and physical barrier to the wind, in the orientation and landing behaviour of a predatory beetle, Rhizophagus grandis Gyllenhall (Rhizophagidae), were investigated. R. grandis responded very positively to the frass of its prey when presented on a 'tree' but not to the same quantity of frass presented alone. Frass on black plastic uPVC pipes was significantly more attractive than frass on real host tree logs, suggesting that host-tree volatiles do not enhance the attractiveness of prey frass.
The beetles responded to 'transparent' Mylar three-dimensional cylinders in the same way as they did to the black plastic pipes. Beetles were also tested with frass and two-dimensional stimuli offering a visual stimulus or physical barrier alone or in combination. Frass with a two-dimensional visual stimulus was no better than frass alone: few insects landed. Significantly more insects were attracted to the same two-dimensional visual stimulus with a hidden upwind barrier producing turbulence, but a similar number were attracted to the frass in front of a hidden barrier alone. As many plants are similar in size to the logs used in these experiments, comparable effects might influence the behaviour of other phytophagous insects, their predators and parasitoids.     

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.     

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.     

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.     

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.     

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.     

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.     

Odour-mediated upwind flight of Culex quinquefasciatus mosquitoes elicited by a synthetic attractant

Abstract A wind tunnel and video equipment are used to study the long-range and close-range responses of gravid females of Culex quinquefasciatus Say to a synthetic pheromone, eryrthro -6-acetoxy-5-hexadecanolide. In response to water and acetoxyhexadecanolide, together or independently, in the presence of wind, females follow meandering flight paths upwind. Females have a higher rate of turning and a lower flight-speed when landing at a site containing pheromone than at a comparable site without pheromone. Females stay longer at oviposition sites containing the attractant than at sites with no attractant.     

Attraction range of a sex pheromone trap for the damson‐hop aphid Phorodon humuli (Hemiptera: Aphididae)

The attraction range of olfactory response by winged female gynoparae (autumn migrants that give birth to oviparae, the sexual females) and male damson–hop aphids Phorodon humuli (Schrank) is investigated in field experiments over 2 years by analyzing the spatial patterns of catches in concentric circles of yellow‐painted traps (60 in total) around a central trap releasing the species' sex pheromone, (1RS,7S,7aS)‐nepetalactol. Males are more likely than females to be found in the central trap, with 65.6% of the 1824 males caught there compared with 11.2% of 1346 females. Both morphs are more numerous in traps axial with the mean wind direction and centred on the pheromone‐release trap than at other angles. Males are approximately five‐fold more numerous in traps downwind than at similar distances upwind of the pheromone, showing that its presence stimulates landing. For males, the estimated active space of the lure extends 6 m downwind. Catches of females are equally numerous up and downwind of the pheromone lure because females orienting on the axis of the pheromone source continue to respond to visual cues in their flight path if they overshoot the olfactory one. For females, the active space of a pheromone lure is less than 2 m downwind. It is unimportant for either morph whether the pheromone‐release trap is yellow or transparent. In these experiments, both morphs orient with, track and probably arrive in the pheromone source trap from at least 26 m, the distance to the nearest aphid‐infested hops.     

Behaviour of flying oriental fruit moth males during approach to sex pheromone sources

Abstract. The pheromone-modulated upwind flight tracks of Grapholita molesta (Busck) males were video recorded as they approached a point-source of pheromone in a wind tunnel. The field of view of the video recording was divided longitudinally into 33 cm sections and the flight behaviour of the males in these sections was measured and compared as they approached from 233 cm to 50 cm downwind of the pheromone source. As the males approached the source, their mean ground speeds decreased. The mean values of their track angles increased with respect to due upwind (0), indicating movement more across the wind. These changes resulted mainly from the males decreasing their air speeds as they progressed up the plume toward the source. They did not change the average direction of their steering (course angle). Thus, the increase in track angles resulted from the males allowing themselves to drift more in the wind as they approached the odour source. The males also increased their average rate of counterturning as they approached the source. The net result of all these behavioural changes was a track that slowed and grew narrower, giving the impression that the males were 'homing-in' on the pheromone source as they approached. Causes of these systematic changes in behaviour are considered with respect to the known systematic changes in pheromone plume structure as the distance to the source decreases.     

Close encounters: contributions of carbon dioxide and human skin odour to finding and landing on a host in Aedes aegypti

In a wind‐tunnel study, the upwind flight and source location of female Aedes aegypti to plumes of carbon dioxide (CO₂) gas and odour from human feet is tested. Both odour sources are presented singly and in combination. Flight upwind along the plumes is evident for both CO₂ and odour from human feet when the odours are presented alone. Similarly, both odour sources are located by more than 70% of mosquitoes in less than 3 min. When both CO₂ and odour from human feet are presented simultaneously in two different choice tests (with plumes superimposed or with plumes separated), there is no evidence that females orientate along the plume of CO₂ and only a few mosquitoes locate its source. Rather, the foot odour plume is navigated and the source of foot odour is located by over 80% of female Ae. aegypti. When a female is presented a plume of CO₂ within a broad plume of human foot odour of relatively low concentration, the source of CO₂ is not located; instead, flight is upwind in the diffuse plume of foot odour. Although upwind flight by Ae. aegypti at long range is presumably induced by CO₂ and the threshold of response to skin odours is lowered, our findings suggest that, once females have arrived near a prospective human host, upwind orientation and landing are largely governed by the suite of human odours, whereas orientation is no longer influenced by CO₂.     

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.     

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.     

Optomotor anemotaxis polarizes self-steered zigzagging in flying moths

ABSTRACT. Experiments with oriental fruit moth males, Grapholita molesta (Buck), provide evidence that a pheromone plume in zero wind elicits an endogenous, self-steered programme of counterturning (zigzagging) flight, and that wind experienced in flight establishes the polarity of the counterturns; they become aligned so that displacement occurs toward the source, even after the wind is stopped. In zero wind, males located a pheromone source more frequently when they had experienced a wind after having already taken flight before the wind was stopped (46%) compared with those that took flight later and therefore only experienced wind while they were in contact with the ground (14%). Furthermore, males placed in a stationary pheromone plume in zero wind located the source, eventually, on 21% of occasions. The flight tracks of these males, as well as those having experienced a wind only while on the ground, often exhibited repetitive counterturns (zigzags) of c. 180–200. However, the counterturns meandered around the flight tunnel, the inter-reversal track angles having no consistent direction. Sometimes the males displaced down-tunnel in the stationary plume, sometimes up, eventually locating the source and performing a courtship display. The inter-reversal track angles of males counterturning in wind, on the other hand, displayed a consistent orientation of c. 60 to either side of the wind line, resulting in consistent upwind displacement toward the source. With no pheromone present, with or without wind, counterturns were not observed.     

Orientation of tsetse flies to wind, within and outside host odour plumes in the field

Abstract Free-flying wild tsetse flies ( Glossina pallidipes Aust. and G. m. morsitans Westw.) were video recorded in Zimbabwe as they flew within an artificial host odour plume at 3, 7 or 15 m from the source, or in no odour, with and without a 0.75 m² vertical, black visual target present aligned with the wind. With no visual target present, flights in odour were strongly biased upwind, and in the absence of odour strongly biased downwind. With the target present, between 16% and 40% of the upwind approaching flies responded visually as they passed the target, by circling it, in proportion to the proximity of the source (taken to be proportional to the mean odour concentration). Crosswind approaching flies (for whom the target will have been visible for some metres away) circled more frequently (34–56%), but without obvious correlation with the odour concentration. Circling flies also responded orthokinetically, by slowing down as they passed the target. The departure directions relative to the wind of flies leaving the target were significantly affected by the odour concentration. At 3 m they left the target in all directions, except possibly avoiding due upwind. At 7 m they left with an obliquely upwind bias, but at 15 m and also in no odour, they left with a strong crosswind bias.     

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.     

Male mate searching behavior in the black chafer Holotrichia loochooana loochooana (Sawada) (Coleoptera: Scarabaeidae): response to pheromone lures of various colors and intensities

In order to understand the visual orientation mechanisms of the male black chafer Holotrichia loochooana loochooana to females, we examined male behavioral response to colored objects (lures) when female sex pheromone was present. In the field, males landed more frequently on darker lures than on lighter ones of the same color. Among lures of different colors but with the same brightness, males preferred landing on black, blue, or red ones to green or grey ones. The reflectance intensities of preferred lures were weaker than those of green and grey in the range of 540–580 nm. This range is considered to affect choice by males. When females perch on the leaf edges of the food plant to adopt a calling posture, the dominant background color is that of the leaves (i.e., green). This means that the landing target forms a silhouette (dark spot) which is prominent against a background of green leaves, providing maximum visual acuity for mating.     

Elevation of pheromone response threshold in almond moth males pre-exposed to pheromone spray

Abstract. High percentages of naive Cadra cautella (Walker) (Lepidoptera: Pyralidae) males not pre-exposed to pheromone flew upwind to sources containing 50 ng (83%) and 500 ng (97%) of pheromone, but not to sources containing 5 μg (23%) and 50 μg (4%).Of the naive males that flew upwind in response to 50 ng sources, 67% located and landed on the source, whereas fewer than 19% of the naive males that flew upwind in response to higher doses located and landed on the sources.A 2-minute pre-exposure of C.cautella males to a spray cloud containing 50 ng, 500 ng, 5 μg or 50 μg of pheromone, induced shifts in response levels such that in wind-tunnel bioassays performed 1 h later, there was an increase in the doses that optimally elicited upwind flight and landing on the source that was proportional to the pre-exposure dose.Few of the pre-exposed males flew upwind to (10–43%) and landed on (0–33%) 50 ng sources, whereas they now perferentially flew upwind to(58–81% and 52–73%) and landed on (33–68% and 55–60%) pheromone sources of doses of 500 ng and 5 μg, respectively.Therefore pre-exposure to pheromone promoted a shift of threshold for response, and not an overall reduction in responsiveness to pheromone.     

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.     

The effect of host odour on the landing responses of tsetse flies (Glossina morsitans morsitans) in a wind tunnel with and without visual targets

Abstract The effect of artificial host odour on the landing responses of males of Glossina m.morsitans West, and on their reaction to visual targets has been investigated in a wind tunnel. Landing was induced in flies that traversed steep odour gradients as they flew upwind and downwind across the edge of an odour plume, irrespective of whether visual targets were present or not; the landing response could be elicited over a wide range of odourconcentrations. When targets were present such odour gradients also tended to increase the proportion of landing flies which alighted on or near the targets; and the bigger the target, or the hungrier the flies, the greater was the propensity for target landing. In air which was more uniformly permeated with odour, the propensity to land on targets was increased only at high odour concentration.