Foraging and mate-finding in the silver Y moth, Autographa gamma (Lepidoptera: Noctuidae) under the risk of predation

Animal foraging and reproductive behaviour is influenced by other simultaneous demands such as predator avoidance. The trade-offs between these demands may depend on sex or mating experience. This study demonstrates that the olfactory-mediated foraging and mate-seeking behaviours in the silver Y moths, Autographa gamma , are affected by auditory cues mimicking their bat predators. Both males and females changed their foraging behaviour under simulated predation risk. Fewer moths reached the odour source following sound stimulation and the time to find the odour source increased by up to 250%. However, there were no significant differences between male and female ability to reach the plant odour source or the duration of the flight towards the source when stimulated with ultrasound. Hence females are not more cautious than males when observed in the same behavioural context. Risk-taking in males was independent of whether they were flying toward a flower odour or sex pheromones having equal attractive value. This indicates that the trade-off between olfactory and acoustic cues is independent the type of odour. Mated females were not as strongly affected by sound as non-mated, indicating that flower odours have a higher adaptive value for mated females, suggesting that some processes following mating experience influence the trade-off between flower odours and simulated bat sounds.     

Habituation of sexual response in male Heliothis moths

It has been generally hypothesized that habituation mediates the effects of pheromone‐based disruption strategies used in the management of moth pests. The current study demonstrates that pheromone‐mediated sexual response in the tobacco budworm moth, Heliothis virescens (F.) (Lepidoptera: Noctuidae), can in fact be modulated by conditions consistent with the production of habituation. An ethogram was used to measure response strength in a wind tunnel experiment where male moths were allowed to respond freely to one of two different blends of female pheromone in 16 trials over 4 days. Post‐test measures were collected to investigate stimulus specificity and long‐term effects. In conditions appropriate to the formation of habituation, habituation will develop and disrupt male sexual response to female sex pheromone. Males repeatedly exposed to plumes of synthetic pheromone blends display a habituated response lasting up to 96 h. Habituation rate and spontaneous recovery of response strength are greater with less intense stimuli. Additionally, males habituated to one blend express no habituation of sexual response when exposed to a different blend. This indicates a high degree of stimulus specificity, which could facilitate outbreeding, and that moths attend to the configuration of the pheromone blend, not simply to its elements.     

Disruption of the odour-mediated mating behaviour of Plodia interpunctella using high-frequency sound

Abstract Indian meal moths, Plodia interpunctella Hübner (Lepidoptera: Pyralidae), have ears which are sensitive to high‐frequency calls produced by echolocating, insectivorous bats. The influence of artificially generated, high‐intensity, ultrasound signals (25 kHz, 106 dB SPL at 1 m distance) on different parameters involved in the odour‐mediated mating behaviour of this species and its potential use in population control was investigated. All moths flying towards olfactory cues in flight tunnel experiments reacted strongly to a 1 s ultrasound pulse by cessation of flight and falling out of the odour plume. The source contact proportion of both male moths orienting towards the female‐produced sex pheromone and of mated female moths orienting towards an oviposition cue was reduced by 40%, compared to unexposed moths. Calling females responded to the sound by retraction of the ovipositor or by falling to the ground. Long‐term exposure to repetitive pulses of ultrasound suppressed female calling by up to 27%. Furthermore, mating in plastic tents was disrupted by up to 58% in ultrasound‐treated tents using different sound regimens, compared to control tents. The results are discussed in relation to the potential use of ultrasound technology for the population control of pyralid stored product pests.     

Sex pheromone production and perception in the mating disruption-resistant strain of the smaller tea leafroller moth, Adoxophyes honmai

Mating disruption is an environmentally safe plant protection strategy that uses a synthetic copy of an insect pheromone to interfere with sexual communication and hence reproduction. To date, a number of pest moths have been controlled with applications of formulated pheromones as mating disruptants. Recently, however, the first example of resistance to mating disruption was documented in one of the major tea pests in Japan, the smaller tea leafroller moth, Adoxophyes honmai Yasuda (Lepidoptera: Tortricidae). To avoid other such cases, it is important to elucidate the mechanism(s) by which the disruptant lost its effectiveness. To this end, we imposed further selection by rearing field‐collected resistant insects with a synthetic pheromone in the laboratory. After more than 70 generations of selection, a strain with quite strong resistance was established, males of which could find and copulate with their mates even in the presence of 1 mg l^?1 of disruptant. Although the mating ability of this strain was greatly increased, the composition and blend ratio of the sex pheromone produced and emitted by females were not obviously changed in comparison with those of females sensitive to mating disruption. However, male response to the pheromone blend was markedly broadened after selection so that resistant males could locate a synthetic pheromone source even when it lacked a pheromone component that is normally necessary for attraction. Males capable of locking onto off‐ratio pheromone blends may be better able to find calling females in pheromone‐treated environments than narrowly tuned males because of greater capability of overcoming sensory imbalance.     

Pre-exposure modulates attraction to sex pheromone in a moth

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

Pheromone-triggered orientation flight of male moths can be disrupted by trifluoromethyl ketones

In a wind tunnel trifluoromethyl ketones (TFMKs) have been found to disrupt the orientation flight of male moths to pheromone sources (virgin females or synthetic pheromone). This is demonstrated by comparison of the flight parameters of the Egyptian armyworm Spodoptera littoralis and the Mediterranean corn borer Sesamia nonagrioides, which had been topically treated with TFMKs, with those calculated for untreated insects. Inhibition occurred in all types of behavior and that of the source contact has been quantified and found to be dose-dependent. The same effect has also been noticed in Mediterranean corn borer males flying to an attraction source consisting of mixtures of (Z)-11-hexadecenyl trifluoromethyl ketone (8), a closely related analogue of the major component of the pheromone, and the natural pheromone blend. The most active TFMKs are those closest in structure to the natural pheromone, along with those chemicals which easily hydrate in solution, such as the beta-thiosubstituted derivatives. Along with the previously reported reduction of catches in the field, our results suggest the possible application of these chemicals in future new pest control strategies.     

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.     

Relative attractiveness of incomplete and complete blends of synthetic pheromone to male obliquebanded leafroller (Lepidoptera: Tortricidae) moths in a flight tunnel and in apple orchards: implications for sex pheromone-mediated mating disruption of this species

The relative attractiveness of synthetic Choristoneura rosaceana (Harris) pheromone consisting of the major compound Z-11-tetradecenyl acetate (Z11-14:OAc), or the major compound plus one, two, or all three of the minor compounds E-11-tetradecenyl acetate (E11-14:OAc), Z-11-tetradecenol (Z11-14:OH), and Z-11-tetradecenal (Z11-14:Ald), in amounts similar to those in the natural pheromone, was compared in a flight tunnel and in apple orchards. In the flight tunnel, there was an increase in the proportion of moths that were activated when E11-14:OAc was combined with the main compound, but no detectible additional increases in response with the addition of Z11-14:OH and Z11-14:Ald. The time required for activation was twice as long when using the major compound than when using the major compound and one or more of the minor compounds. There was a trend of increase in the proportion of males initiating the take-off, lock-on, close-in, and touchdown phases of upwind flight when progressively more complete blends were used. The time required for the initiation of these behavioral phases was statistically similar for each treatment. The proportion of moths landing at the pheromone source was 10 times greater when using the complete blend than when using the main compound alone. Similar results were obtained in apple orchards, where the four-compound blend was 17-55 times more attractive than the main compound. The superior attractiveness of the four-compound pheromone compared with the major compound, or to the major compound plus the minor compound E11-14:OAc, suggests that it would be the most effective synthetic pheromone if competitive attraction were an important mechanism of disruption in this species.     

Modification of sex pheromone blend discrimination in male Oriental fruit moths by pre-exposure to (E)-8-dodecenyl acetate

ABSTRACT. A pre-exposure regime was developed to test the hypothesis that arrestment of in-flight behaviour in Oriental fruit moths, Grapholitha molesta (Busck), to high dosage and/or high %( E )-8-dodecenyl acetate blends was due to a high proportion of E8-12: Ac in the pheromone blend. When tested in a sustained-flight tunnel to various ratios of ( Z )- and ( E )-8-dodecenyl acetate plus a constant % of Z8-12: OH at two dosages (3 and 100μg), males displayed an optimum number of completed flights to the source to the natural 6% E blend at 3 μg, with significant decreases in response levels occurring to high % E blends at both dosages. Pre-exposure of males to E8-12: Ac alone enhanced their response at each dosage to selected higher % E blends that normally elicited low numbers of completed flights. Pre-exposure enhanced all aspects of the flight response, but this was dependent on both dosage and duration of pre-exposure, with later behaviours in the sequence (landing and hairpencil display) requiring greater amounts of pre-exposure than early behaviour (taking flight). Pre-exposure did not affect high response levels to optimal blends or low response levels to the highest or lowest blends tested at each dosage. The selective nature of the pre-exposure effect implied alteration of central processes in discrimination of blend rather than disturbance of olfactory receptor function.     

Effects of exposure to predatory cues on territorial behaviour of male fathead minnows

We conducted a laboratory study to determine if male fathead minnows, Pimephales promelas, altered their territorial behaviour associated with reproduction in response to combinations of visual and chemical cues from northern pike, Esox lucius. We introduced the following stimuli to a territorial male: a brick (control), fathead minnow alarm pheromone, a pike fed brook stickleback, Culea inconstans, or a pike fed fathead minnow. The territorial behaviour of males did not change when the control was added. Male minnows experiencing threat from pike fed stickleback significantly reduced the frequency at which they performed three territorial behaviours, but, within 12 h, had returned to pre-exposure activity levels. Male minnows subjected to alarm pheromone alone and to pike fed fathead minnow significantly reduced their territorial behaviour, abandoned their nests, and did not return to pre-exposure levels of activity after 24 h. We suggest that because risk of predation triggers prolonged decreases in territorial defense, it may affect competition between nesting males and female mate choice. We conclude that fathead minnows can assess the severity of predatory threat and adjust their reproductive behaviour accordingly.     

Host odours enhance the responses of adult Rhyzopertha dominica to male-produced aggregation pheromone

The behavioural responses of adult male and female Rhyzopertha dominica (Coleoptera, Bostrichidae) to blends of host volatiles and male-produced aggregation pheromone were observed in a four-arm airflow olfactometer. The odour sources used were five pheromone-releasing males each on a single maize grain (lower maize-volatiles blend), five pheromone-releasing males on 500 g of maize (higher maize-volatiles blend) or the host volatiles emanating from 500g of maize (maize volatiles alone). Multiple-choice tests, in which volatiles from all three odour sources were presented in the exposure chamber at the same time, were used to study odour preferences of the males and females. Both sexes showed strongest attraction to the higher maize volatile blend but there were significant sex differences in response to the odour sources. Males spent significantly more time than females in the zone with only maize volatiles, and females spent significantly more time in the higher maize-volatiles zone. However, when odour sources were offered singly, females gave numerically greater responses than males to all sources although this difference was statistically significant for only the lower maize-volatiles blend. As males are more attracted than females to host odours alone it is suggested that they may be more highly adapted to seek out new hosts while females are more inclined to locate a food source by following the pheromone signals produced by males. However, both sexes responded most strongly to the odour source comprising aggregation pheromone with the higher proportion of maize volatiles.     

Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata

Abstract. 1. Adult males of the two-spot ladybird beetle, Adalia bipunctata , did not show a functional response to increase in aphid abundance and consumed markedly fewer aphids than do the females.
2. At high densities of prey, females spent more time in area-restricted search than when prey was scarce. Males were always less active than females and they did not respond to an increase in prey abundance by a change in searching behaviour.
3. After a brief encounter with a female, a male showed area-restricted searching behaviour. This behaviour occurred in response to encountering a female's elytra and in particular to a chloroform-soluble component (sex pheromone) present on or in the elytra.
4. Males needed to encounter a female in order to respond to her presence, which indicated the pheromone is a contact pheromone.
5. The searching behaviour of males appeared to be mainly directed towards locating females; that of females towards locating aphids. This difference between the sexes should be taken into account when quantifying the predatory response of ladybirds to aphid abundance in the field.     

Experimental evolution reveals that population density does not affect moth signalling behaviour and antennal morphology

Population density can play a vital role in determining investment in reproductive behaviours and morphologies of invertebrates. Males reared in high-density environments, where competition is high but difficulties in locating mates are low, may invest more in reproductive structures associated with sperm competition such as testes, at the expense of those traits associated with mate location, such as antennae. In species where females advertise for mates, such as most moths, a high-density environment may also lead to a reduction in pheromonal signalling (calling) length and frequency as a result of high mate abundance. While such responses have been shown at the phenotypically plastic level in moths, heritable evolutionary adaptations have seldom been tested, and studies of how population density influences pheromone signalling strategies are scarce. Here we use behavioural assays and scanning electron microscopic measurements to test whether larval population density influences, at the genetic level, the ability of males to locate females and male investment into antennal morphology, in addition to its effect on the frequency and duration of female calling. We used two replicated populations of the Indian meal moth Plodia interpunctella that had experimentally evolved under high or low population densities for 35 generations. We found no significant divergence in antennal morphology or mate acquisition behaviours between the two density populations. These findings suggest that although population density has the ability to create plastic changes in both morphological and behavioural traits, this factor alone is unlikely to be causing evolutionary change in male and female signalling in this species.     

A pulsed cloud of sex pheromone elicits upwind flight in male moths

ABSTRACT. Male oriental fruit moths do not fly upwind in a continuous uniform cloud of pheromone, but readily do so when the cloud is pulsed at 1 or 0.5/s or when a plume from a point source of pheromone is placed within the continuous cloud. It is suggested that males of moth species that require such fluctuating pheromone stimulation for upwind flight will normally receive it from a filamentous, point-source-produced plume. However, we hypothesize that upwind progress may cease close to the source due to excessively high emission rates or inappropriate blend ratios, when fluctuating sensory output becomes attenuated, despite higher actual molecular concentration fluctuations.     

The effects of pheromone concentration on the flight behaviour of the oriental fruit moth, Grapholitha molesta

ABSTRACT. Male oriental fruit moths, Grapholitha molesta (Busck) (Tortricidae), flew at lower overall and net ground velocities when they flew toward higher concentration pheromone sources. Turning frequency was greater with increased pheromone concentration, while the distance of turns from the plume axis back towards the axis decreased. Turning magnitude and inter-reversal track angles remained constant at all concentrations tested. Concomitant with the changes in ground velocity but constant inter-reversal angles, were decreases in airspeed, decreases in the moths' course angles and increases in their drift angles. The significance of these changes is discussed in relation to their possible role in a longitudinal chemoklinotactic programme of turning operating in conjunction with anemotaxis to allow location of a pheromone source in wind.     

Disruption of pheromone communication in moths: is the natural blend really most efficacious?

It is widely assumed that a blend of pheromone components, that is qualitatively and quantitatively similar to the natural sex attractant, is the most effective mating disruptant for moths. However, the literature contains only limited evidence supporting this assumption. The authors discuss the importance of comparing the relative effectiveness of complete and incomplete pheromone blends when evaluating the potential of mating disruption for controlling pest moths.     

Female moths of cotton bollworm (Lepidoptera: Noctuidae) captured by waterbasin traps baited with synthetic female sex pheromone

Cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), is one of the most important pest insects in cotton fields in China. Female moths were captured by waterbasin traps with a synthetic female sex pheromone blend in cotton fields over three years. The blend contained (Z)‐11‐hexadecenal and (Z)‐9‐hexadecenal with a ratio of 97:3. Each pheromone dispenser was impregnated with 2.0 mg of pheromone blend and 0.2 mg of antioxidant dissolved with 0.1 mL of hexane, and there was a control dispenser with a similar amount of antioxidant and solvent only. Waterbasin traps were deployed in three configurations in the fields. ‘A’ was pheromone traps only, ‘B’ was both pheromone and control traps, ‘C’ was control traps only. (i) In four plots of ‘A’, the average weekly female catch was 1.5, and more females were captured by centrally located pheromone traps, (ii) In three plots of ‘Brsquo;, control traps also captured female as well as male moths, but average weekly female catches of control traps was significantly lower than that in pheromone‐baited traps. (iii) There were significant linear relationships between the average weekly female catch and the corresponding layer in pheromone‐baited traps in both ‘A’ and ‘B’ plots, and in quadratic equations in control in ‘B’ plots. (iv) With the increase of the interval of traps, average weekly female catches per trap increased but average weekly female catches per hectare decreased. (v) Among the female moths captured by pheromone traps, 88.3% were mated female moths which each containing 1.46 spermatophores, while in control traps 86.9% of the mated female moths had 0.90 spermatophores. There was a significant difference between the average numbers of spermatophores of mated females in pheromone traps and in controls.     

Correlation between male size and territory quality: consequence of male competition or predation susceptibility?

Territory characteristics correlate with male characteristics in several species. This can result from male competition for the best territories, or from males varying in their ability to pay other costs of territoriality, such as predation risk costs. In a population of threespine sticklebacks, Gasterosteus aculeatus , we found the biggest males to defend the biggest territories with a low structural complexity and a high female encounter rate. By experimentally manipulating competition intensity and habitat structure, we show that both male competition and predation exposure influenced the distribution of territories among males. Males increased the size of their territory when a neighbouring male was removed, whereas they reduced their territory when habitat complexity and cover from predators were reduced, with large males reducing their territory size less than smaller males. This suggests that large males occupy large, open territories both because of their superior competitive ability and because of their either lower predation susceptibility or higher risk-taking. Large, open territories were beneficial in mate attraction and male competition and predation exposure therefore biased mating opportunities towards large males. This suggests that cost of territoriality to males may reduce mate choice costs to females by securing that large males are encountered more often than small males, and by providing an additional cue, territory quality, which indicates which males are worth inspecting.     

The mate pursuit-predation avoidance tradeoff in the virile crayfish,Orconectes virilis

To better understand the tradeoff between mate pursuit and predation risk avoidance, the responses of male virile crayfish (Orconectes virilis) to female sex pheromone and conspecific alarm cue, alone and in combination were tested. Male crayfish were more active and exhibited less antipredator behavior in the pheromone treatment than in either the pheromone?+?alarm or alarm treatment. The results suggest a tradeoff in favor of risk avoidance when pheromone and risk stimuli are encountered together.     

Downwind migration of the African army worm moth, Spodoptera exempta, studied by mark-and-capture and by radar

Abstract. 1. About 166,000 African armyworm moths, Spodoptera exempta (Walk.), were marked at an emergence site near Nairobi when they fed at night on trees baited with dyed molasses.
2. Six marked moths were captured in pheromone traps, including one at 90 km after flying for only one night, and another at 147 km.
3. Moth flight trajectories deduced from radar and from marking showed that migration was downwind.
4. During migration, moths become dispersed; hence the high densities that lead to outbreaks must be produced by concentration.
5. Some moths were ready to mate on the same night they completed their long-distance flight.