Sex pheromone titre in the glands of Spodoptera litura females: circadian rhythm and the effects of age and mating

The present study investigates the effects of age and mating status on the circadian variations of gland sex pheromone titre in female Spodoptera litura Fabricius. Similar to other nocturnal moths, S. litura females exhibit circadian variations of gland sex pheromone contents, with higher levels during scotophase and lower levels during photophase. The sex pheromone titre in the glands peaks during the first scotophase after eclosion and sharply declines afterwards. Higher pheromone contents during scotophase may facilitate female reproductive activities, and the negative relationship between pheromone titre and female calling is likely the result of pheromone release during female calling. Interestingly, the present study demonstrates that mated S. litura females have significantly higher sex pheromone titre in their pheromone glands (PGs) than virgin females. This finding contrasts with all previous studies of other insect species, in which mating generally reduces the sex pheromone titre in female PGs. In S. litura, mating and male accessory gland fluids can suppress female calling behaviours and re‐matings. These results suggest that the suppression of female calling behaviours by mating and male accessory gland fluids may significantly reduce the release of sex pheromones and thus result in higher sex pheromone titre in the PGs of mated females.     

Sex pheromone-releasing behaviour in females of the dermestid beetle,Trogoderma glabrum

Adult Trogoderma glabrum females assume stationary postures characterized by abdominal elevation and partial exposure of the ovipositor segments. The postural activity was studied in relation to sex pheromone production and was designated calling, or sex pheromone-releasing behaviour because it was accompanied by an increase in the rate of release of sex pheromone(s). Calling was largely restricted to an 8 hr interval centered toward the middle of a 16 hr photophase. Mating frequency and female pheromone content increased during the same interval. Because females extracted during the calling period yielded at least 10 times more pheromone than extracts prepared at other times, and because pheromone activity released during one calling period was estimated to be at least 10-fold higher than that which could be extracted from whole females several hours prior to the start of calling, heightened production of active pheromone(s) was postulated to occur during calling. Functional significance of the calling posture is discussed in relation to sex pheromone gland location.     

Modelling female mating success during mass trapping and natural competitive attraction of searching males or females

Simulation models of insects encountering sex pheromone with or without mass trapping in which the searching sex is either male (moths and many insect species) or female (some true bugs, beetles, and flies) were developed. The searching sex moved as a correlated random walk, while the opposite sex remained stationary (calling) and released an attractive sex pheromone. The searching sex was caught when encountering a pheromone‐baited trap, and females mated when encountering a male. An encounter with pheromone was defined by the searcher's interception of a circle termed the effective attraction radius (EAR_c). Parameters of movement (speed and duration), initial numbers of calling sex and searching sex, number of traps, area, and EAR_c of traps and calling sex were varied individually to evaluate effects on the percentage of females mating. In the natural condition without traps, female mating success in both models was identical. Increasing the EAR_c of the calling sex caused diminishing increases in female mating success, suggesting that evolution of larger pheromone release and EAR_c is limited by increasing costs (production/sensitivity) relative to diminishing increases and benefits of mating encounters. With mass trapping, increasing the EAR_c of traps or density of traps caused similar declines in female mating in both models, but the female‐searching model predicted slightly lower mating success than the male‐searching model. Increasing the EAR_c of calling insects or the initial density of insects caused similar increases in female mating in both models, but again the female‐searching model had slightly lower mating success than the male‐searching model. The models have implications for mating lek formation and for understanding the variables affecting the success of mass trapping programs for insect pests with either male or female sex pheromones.     

Release mechanism of sex pheromone in the female gypsy moth <Emphasis Type="Italic">Lymantria dispar</Emphasis>: a morpho-functional approach

A morpho-functional investigation of the sex pheromone-producing area was correlated with the pheromone release mechanism in the female gypsy moth Lymantria dispar. As assessed by male electroantennograms (EAG) and morphological observations, the pheromone gland consists of a single-layered epithelium both in the dorsal and ventral halves of the intersegmental membrane between the 8th and 9th abdominal segments. By using the male EAG as a biosensor of real-time release of sex pheromone from whole calling females, we found this process time coupled with extension movements of the ovipositor. Nevertheless, in females in which normal calling behavior was prevented, pheromone release was detected neither in absence nor in presence of electrical stimulation of the ventral nerve cord/terminal abdominal ganglion (TAG) complex. Tetramethylrhodamine-conjugated dextran amine stainings also confirm the lack of any innervation of the gland from nerves IV to VI emerging from the TAG. These findings indicate that the release of sex pheromone from the glands in female gypsy moths is independent of any neural control exerted by the TAG on the glands, at least by way of its three most caudally located pairs of nerves, and appears as a consequence of a squeezing mechanism in the pheromone-producing area.     

Electrophysiological and Behavioral Responses of Female Beet Armyworm Spodoptera exigua (Hübner) to the Conspecific Female Sex Pheromone

Electroantennogram (EAG) recordings showed that female Spodoptera exigua can detect their own sex pheromones (two single components and their mixture), displaying a similar dose–response pattern to that of males, although intensities of female responses were much less at all doses compared with males. Furthermore, the female calling behavior was inhibited and late-shifted by the presence of the female sex pheromone. When the pheromone components were presented, the calling female proportion in the peak calling period was significantly reduced and the calling peak time and calling termination time postponed, compared with controls. Although the calling behavior was inhibited, the pheromone titer of treated females was not different to the control, implying a reduced pheromone biosynthesis in the pheromone glands of treated moths. However, observations during the olfactometer experiments revealed that there were no obvious behavioral responses of females exposed to sex pheromone stimuli including whole gland extracts, 0.1, 1 or 10 μg binary pheromone mixtures.     

Nocturnal Calling Behavior in Mantids

Females of Mantis religiosa and Empusa pennata were video taped for several 24 h periods to determine if they showed behaviors associated with pheromone release. In the photophase the abdomen of both species was motionless and rested in continuous contact with the wings. However, at the beginning of the scotophase the females bent the abdomen ventrally so that the space between the abdomen and the wings increased significantly with respect to the daytime posture. Calling behavior (abdominal bending) was maintained throughout the 8 h scotophase and ended abruptly at lights on. Females of M. religiosa did not start calling until they were 30 days of age. Calling disappeared in mated females, but it reappeared two weeks later. Males stayed motionless in response to the odors emitted by other males or by noncalling females, but walked when a calling female was placed in the air flow. These observations suggest that female mantids bend their abdomens at night to release a sex pheromone. The adaptive function of nocturnal sex pheromone release in sexually cannibalistic species that rely strongly on visual cues for mating is discussed.     

Conspecific females promote calling behavior in the noctuid moth,Pseudaletia adultera

Changes in female calling behavior in response to the presence of conspecific pheromones (pheromone autodetection) have been demonstrated in a number of moth species. However, the observed changes vary between species, and several ecological and adaptive explanations for autodetection have been proposed. We studied the effect of conspecific females on the calling behavior of the noctuid moth Pseudaletia adultera (Schaus) (Lepidoptera: Noctuidae, Hadenini), by comparing the age of first calling, as well as the onset and pattern of calling, when females were held individually or in the presence of conspecifics. Grouped females started calling at a lower age, a higher percentage of females called during the scotophase, and they called longer compared to females held in isolation. We also demonstrated that female antennae respond to each of the three main components of the sex pheromone – (Z)‐11‐hexadecen‐1‐ol, (Z)‐11‐hexadecen‐1‐yl acetate, and (Z)‐11‐hexadecenal – and that the response patterns differed from those of male antennae. By calling more and extending her calling window in presence of conspecific females, a female may increase her chances of accessing males. However, the potential benefits need to be considered within an ecological context, considering factors such as migration, oviposition, and foraging.     

Moths behaving like butterflies. Evolutionary loss of long range attractant pheromones in castniid moths: a Paysandisia archon model

Background

In the course of evolution butterflies and moths developed two different reproductive behaviors. Whereas butterflies rely on visual stimuli for mate location, moths use the ‘female calling plus male seduction’ system, in which females release long-range sex pheromones to attract conspecific males. There are few exceptions from this pattern but in all cases known female moths possess sex pheromone glands which apparently have been lost in female butterflies. In the day-flying moth family Castniidae (“butterfly-moths”), which includes some important crop pests, no pheromones have been found so far.

Methodology/Principal Findings

Using a multidisciplinary approach we described the steps involved in the courtship of P. archon, showing that visual cues are the only ones used for mate location; showed that the morphology and fine structure of the antennae of this moth are strikingly similar to those of butterflies, with male sensilla apparently not suited to detect female-released long range pheromones; showed that its females lack pheromone-producing glands, and identified three compounds as putative male sex pheromone (MSP) components of P. archon, released from the proximal halves of male forewings and hindwings.

Conclusions/Significance

This study provides evidence for the first time in Lepidoptera that females of a moth do not produce any pheromone to attract males, and that mate location is achieved only visually by patrolling males, which may release a pheromone at short distance, putatively a mixture of Z,E-farnesal, E,E-farnesal, and (E,Z)-2,13-octadecadienol. The outlined behavior, long thought to be unique to butterflies, is likely to be widespread in Castniidae implying a novel, unparalleled butterfly-like reproductive behavior in moths. This will also have practical implications in applied entomology since it signifies that the monitoring/control of castniid pests should not be based on the use of female-produced pheromones, as it is usually done in many moths.     

Mating Effect on Sex Pheromone Production of the Oriental tobacco budworm,Helicoverpa assulta

This study was undertaken to clarify the suppression phenomenon of sex pheromone production after mating and its relationship to the physiological mechanism in adult females of Helicoverpa assulta, and determine the mating factor from males causing depletion of sex pheromonc production. Sex pheromone production of H. assulta females was mostly terminated in 3 hours after mating. Mated females maintained with a low titer of sex pheromone until 3 days when it started to increase again, which showed a characteristic of species mating more than once. The mated female again produced pheromone upon injection of pheromone biosynthesis activating neuropeptide (PBAN) or extracts of brain-suboesophageal ganglion complexes (Br-Sg) of mated female, which were shown similar pheromonotropic activities as compared with virgin females. These results indicated that the mating did not inhibit the receptivity of pheromone gland itself and PBAN biosynthesis in suboesophageal ganglion of the mated females. And it seems to support that the depletion of sex pheromone production is responsible for blocking of PBAN release from head. To investigate the mating factor from adult males, when extracts of reproductive organs of male were injected into hemocoel of virgin females evoking depletion of sex pheromone production as shown in mated female. The results suggest that a chemical substance(s) from the male reproductive organs could be responsible for the loss of sex pheromone biosynthesis in H. assulta.     

Male moth songs tempt females to accept mating: the role of acoustic and pheromonal communication in the reproductive behaviour of Aphomia sociella

Background

Members of the subfamily Galleriinae have adapted to different selective environmental pressures by devising a unique mating process. Galleriinae males initiate mating by attracting females with either chemical or acoustic signals (or a combination of both modalities). Six compounds considered candidates for the sex pheromone have recently been identified in the wing gland extracts of Aphomia sociella males. Prior to the present study, acoustic communication had not been investigated. Signals mediating female attraction were likewise unknown.

Methodology/Principal Findings

Observations of A. sociella mating behaviour and recordings of male acoustic signals confirmed that males initiate the mating process. During calling behaviour (stationary wing fanning and pheromone release), males disperse pheromone from their wing glands. When a female approaches, males cease calling and begin to produce ultrasonic songs as part of the courtship behaviour. Replaying of recorded courting songs to virgin females and a comparison of the mating efficiency of intact males with males lacking tegullae proved that male ultrasonic signals stimulate females to accept mating. Greenhouse experiments with isolated pheromone glands confirmed that the male sex pheromone mediates long-range female attraction.

Conclusion/Significance

Female attraction in A. sociella is chemically mediated, but ultrasonic communication is also employed during courtship. Male ultrasonic songs stimulate female sexual display and significantly affect mating efficiency. Considerable inter-individual differences in song structure exist. These could play a role in female mate selection provided that the female''s ear is able to discern them. The A. sociella mating strategy described above is unique within the subfamily Galleriinae.     

Juvenile hormones: Their role in the regulation of the pheromonal communication system of the armyworm moth,Pseudaletia unipuncta

Recently, much effort has been devoted to the elucidation of the neuro-endocrine mechanisms regulating the biosynthesis and emission of sex pheromones in the Lepidoptera. The available data indicate that the hormonal mechanisms involved vary considerably among species. For example, compelling evidence that juvenile hormones (JH) play a role in the control of sex pheromone production has been presented only for the armyworm moth, Pseudaletia unipuncta. In this species, females that are allatectomized at emergence neither produce nor release pheromone, but both activities are restored following replacement therapy with synthetic JH. However, injection of synthetic JH into neck-ligated females does not induce pheromone biosynthesis, whereas treatment with either a brain homogenate or synthetic PBAN results in a rise in the pheromone titer. These results indicate that the role played by JH is an indirect one and that the tropic factor is a PBAN-like substance. Studies on in vitro JH biosynthesis by isolated corpora allata of P. unipuncta have shown that the low JH output observed early in the life of adult females coincides with the absence of both calling behavior and pheromone production. The subsequent increase in the rates of JH biosynthesis correlates with the onset of pheromone production and release. We have therefore proposed that JH titers must pass a threshold level before the circadian release of PBAN and calling behavior can begin. Furthermore, recent experiments suggest that the continuous presence of JH is necessary for calling behavior to be maintained once initiated. Lastly, we present data suggesting a role for JH or JH acids in the receptivity of P. unipuncta males to the female sex pheromone. © 1994 Wiley-Liss, Inc.     

Sound production in Scolytidae: Female sonic stimulus of male pheromone release in two Dendroctonus beetles

The hypothesis that female sonic stimulus may evoke male pheromone release in a behavioural interaction analogous to the known male sonic stimulus of female pheromone release, was confirmed in Dendroctonus pseudotsugae, and also in D. brevicomis. In both species known male-produced substances collected from males stimulated by recorded female stridulation were identified by coupled gas chromatography/mass spectrometry. In a second test with D. pseudotsugae, male pheromone release during recorded female stridulation was evident in the change of male stridulation from the simple attractant chirp to the interrupted chirp, which is known to result from a medium concentration of 3,2-MCH. Also, the D. pseudotsugae male attractant chirp was synthesised with an electronic pulse generator and used to evoke pheromone release. It is concluded that the antiaggregative pheromone of this species is released by each sex at the sonic stimulus of the other sex.     

蜀柏毒蛾生殖行为及性信息素产生与释放节律

为了探索蜀柏毒蛾Parocneria orienta Chao性信息素产生和释放规律, 为利用性信息素监测和防治蜀柏毒蛾奠定基础, 本研究在野外及室内温度22±1℃、 相对湿度75%~80%、 光周期14L∶10D条件下观察研究了蜀柏毒蛾成虫的羽化、 求偶、 交尾、 产卵行为, 触角电位反应测定处女雌蛾性信息素产生与释放的时辰节律。结果表明： 蜀柏毒蛾羽化行为全天可见, 主要集中在1:00-5:00, 占总羽化量的44.94%, 7:30-11:00进行婚飞和交尾, 交尾高峰期出现在8:30左右, 交配时间少则2 h, 多则8 h, 求偶、 交配均发生在光期。随着日龄的增加, 召唤时间前移并且延长, 1日龄的处女雌蛾交尾时间较短; 雌蛾羽化当天就可交尾, 2日龄雌蛾交尾率最高, 达36.67%。雌蛾分多处产卵, 雌蛾一生最高产卵量达402粒, 最低产卵量为78粒。羽化当天的雌蛾体内性信息素含量较低, 第2天最高, 以后逐日下降; 2日龄蜀柏毒蛾处女雌蛾性信息素的产生量从7:00起逐渐增加, 8:30-9:30时最高, 9:30后逐渐减小。雄蛾对处女雌蛾腺体提取物的触角电位反应在8:30-9:00最强, 说明8:30-9:00是雌蛾产生和释放性信息素的高峰期。蜀柏毒蛾的羽化、 求偶、 交尾及性信息素的产生与释放存在一定的时辰节律, 野外处女雌蛾诱蛾试验证实了性信息素释放与交配行为在时辰节律上的一致性。     

Attractiveness of year-old polyethylene Isonet sex pheromone dispensers for Lobesia botrana

In this study, we have compared the release of sex pheromone from mating disruption dispensers exposed in the field for 12 months and from calling females. The main pheromone component of the grapevine moth, Lobesia botrana (D. and S.) (Lepidoptera: Tortricidae), is (E)‐7,(Z)‐9‐dodecadienyl acetate, and a minor component is (Z)‐9‐dodecenyl acetate. Aged dispensers from two different years emitted a much higher amount of both pheromone components than calling females. However, the summer temperature during field exposure influenced the release from mating disruption dispensers the following year. In the wind tunnel, male L. botrana were equally attracted to 12‐month, field‐exposed dispensers, a standard monitoring pheromone lure, and to synthetic (E)‐7,(Z)‐9‐dodecadienyl acetate sprayed at the rate of 0.6–60 ng h^?1. Field trapping tests confirmed that aged dispensers from both years were at least as attractive to L. botrana males as a standard monitoring pheromone lure. The possible contribution of previously applied dispensers to the mating disruption efficacy during following applications is discussed.     

Mating systems in primitive Lepidoptera, with emphasis on the reproductive behaviour of Korscheltellus gracilis (Hepialidae)

Adults of Korscheltellus gracilis (Grote) are crepuscular. Flight is restricted to two 20–40 minute periods each day: the first flight follows sunset during evening twilight, the other precedes dawn. Four to five times as many adults are active during the evening when courtship, mating and oviposition occur. Of these behaviours, only oviposition occurs during the pre-dawn period of activity. Field observations indicate that females release a sex pheromone while fanning their wings. Females usually fly before pairing. There is no obvious female choice or stereotyped courtship behaviour prior to pairing.
In some hepialid genera females attract males, while in others ( Hepialus Fabricius, Phymatopus Wallengren, Sthenopis Packard and Zenophassus Tindale) the calling system is reversed, with males attracting females. Cladistic analysis of the Hepialidae suggests that the plesiomorphic condition for the family is for females to release the long-distance attractant, and that the reversed calling system represents a derived condition restricted to lineages within a single clade.
Available information on the mating systems of other basal lepidopteran lineages and Trichoptera support the hypothesis that ancestral Lepidoptera possessed a female-released, long-range attractant. Support for this position comes from (1) published literature; (2) field observations made by DLW; (3) the apparent absence of male scent structures and recognizable male calling behaviour among the pre-Neolepidoptera; and (4) cases of male antennal elaboration in several basal lepidopteran lineages.     

Disruption of pheromone communication in Tecia solanivora (Lepidoptera: Gelechiidae): flight tunnel and field studies

The moth Tecia (Scrobipalpopsis) solanivora Povolny (Lepidoptera: Gelechiidae) is the most important pest of potato, Solanum spp., in Central America and adjacent South American countries. Insecticide treatments are not sufficiently effective; therefore, we investigated the feasibility of pheromone-mediated mating disruption for control of T. solanivora. Pheromone dispensers were formulated with 70 mg of the three sex pheromone compounds (E)-3-dodecenyl acetate, (Z)-3-dodecenyl acetate, and dodecyl acetate, in a ratio of 100:56:100, respectively. Male attraction to these compounds is optimal at a ratio of 100:1:20, thus the mating disruption dispensers contained an off-blend, which attracted only a few males. Nonetheless, one mating disruption dispenser suppressed male attraction to calling females in a flight tunnel and reduced male activation in response to female pheromone. Communication disruption is accordingly due to camouflage of the female signal and possibly due to a reduction of male responsiveness by sensory imbalance. Only a few males were observed in a 3-ha potato field treated with 84 g pheromone/ha, compared with an untreated control field. During 2 mo, male attraction to traps baited with calling females or synthetic pheromone was strongly reduced. This reduction confirms the potential of mating disruption for management of T. solanivora. The efficacy of the pheromone treatment can be further improved by earlier dispenser application, by increased dispenser load, and by treatment of larger fields to reduce immigration of mated females.     

Why are males more attractive after brood care? Proximate causes of enhanced sex pheromone emission in a burying beetle

Recent studies demonstrate that pheromones can be costly to produce and emit and, therefore, the types and quantities that they express are likely to covary with individual condition. Previous experiments reveal that, when given the opportunity to breed and care for young, male burying beetles Nicrophorus vespilloides go on to produce a higher amount of their sex pheromone and attract more females than control males that do not exhibit parental care. This finding is surprising because parental care is usually assumed to be energetically costly, reducing the future capacity to invest in sexual signalling. However, burying beetles reproduce on dead vertebrates and the carrion meal might enable males to acquire resources that can subsequently be allocated to pheromone signalling. Alternatively, males might accumulate pheromone precursors because they do not emit their sex pheromone during brood care. To shed light on the mechanisms of enhanced pheromone emission after brood care, in the present study, we test the effect of diet quality, social condition during care (biparental versus uniparental care) and an experimentally enforced calling pause on subsequent male pheromone emission, body weight and energy storage components. The experimentally enforced calling pause and social condition during brood care demonstrate no impact on pheromone quantity. However, the results of the present study suggest that the vertebrate carrion meal during brood care partly explains enhanced pheromone release after care. Unravelling the biosynthetic pathways of the pheromone components and analyzing the impact of potential microbial symbionts on pheromone production represents a fruitful avenue for future research.     

棉铃虫成虫对高浓度性信息素的行为反应

室内行为实验表明,在高浓度性信息素环境中棉铃虫Helicoverpa armigera (Hübner) 雌蛾更加活跃、觅偶行为更加积极主动、求偶时间显著延长,而雄蛾主动求偶时间显著缩短、静止时间显著延长。高浓度性信息素并未引起成虫在取食活动和产卵行为的明显改变,也未能有效阻断其交配行为,而是推迟了它们的交配日期、夜间初始交配时间,缩短了交配蛾的交配持续时间。因此,高浓度性信息素主要影响其交配质量,而不是交配率。     

Masculinization mechanism of hybrids in bitterlings (Teleostei: Cyprinidae)

The sex ratio of bitterling hybrids (subfamily: Acheilognathinae) is often likely to be biased toward males. Artificial hybridization was carried out in 10 species of bitterlings (three genera) in order to elucidate the masculinization mechanism of hybrids. Tanakia himantegus never produced viable F1 hybrids with other species, while hybrids of most other species were viable. In terms of sex ratio and fertility, hybrids were clearly divided into two groups: congeneric Tanakia hybrids and others. Both male and female congeneric Tanakia hybrids were fertile. The sex ratio was nearly 1:1 in all groups of Tanakia hybrids. Except for the congeneric Tanakia hybrids, sterile males appeared predominantly in groups of hybrids in which females were very rare but remained fertile. Sterile intersexes were also observed in five hybrid groups: T. lanceolata (female) x Acheilognathus cyanostigma (male), Rhodeus uyekii (female) x T. lanceolata (male), A. rhombeus (female) x T. lanceolata (male), A. rhombeus (female) x T. limbata (male), and A. tabira tabira (female) x A. cyanostigma (male). In the development of male-predominant hybrids, although hybrid and control (parental species) hatching and survival rates do not differ, no females appeared in hybrids, contrary to the controls. Taking the female heterogametic sex-determining system (ZW) and the phylogenetic relationship of bitterlings into consideration, the masculinization mechanism of hybrids in bitterlings can be explained by the interaction of two sex chromosomes, derived from each parental species. The basic genetic sex in bitterlings is male (ZZ) and the derivative is female (ZW). When parental species are related, the sex phenotype of hybrids coincides with the genetic sex. However, when the parental species differ, the sex phenotype of the ZW genotype is reversed to become male by an abnormal interaction between the Z and W chromosomes. The rare appearance of females and intersexes in male-predominant hybrids might be due to complete or partial functional expression of the W chromosome.     

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.