Effects of photoperiod and mating on sex pheromone production and release by oviparae of the aphid Schizaphis graminum

ABSTRACT. By extraction and bioassay procedures, it is shown that the sex pheromone released by oviparae of the greenbug, Schizaphis graminum (Rondani), during the daylight hours of a light: dark regime, is present in the tibia of the metathoracic legs only during daily photophases.
Shortly after mating, pheromone-emitting oviparae cease to produce as well as to release the pheromone. This mating-induced response requires that copulation be completed, and suggests the involvement of sperm or seminal substances transferred by the males to the oviparae during copulation.
Although multiple matings increase the number of eggs deposited by an ovipara, the mating-induced termination of pheromone production/ release would enhance the chances for mating of neighbouring oviparae. This would result in a further increase in egg production as well as in the number of genetically similar offspring, because neighbouring oviparae are most probably sisters. The phenomenon is discussed in terms of kin selection.     

Pheromone production and mating behaviour by allatectomized males of the cockroach, Nauphoeta cinerea

Males of Nauphoeta cinerea produce a volatile pheromone which attracts the female for mating. Allatectomy of males either 5 days prior to or within 12 hr following the imaginal ecdysis does not impair pheromone production, pheromone release, nor any observable aspect of mating behaviour. It is proposed that in N. cinerea, and in other cockroach species where the male releases a volatile pheromone to attract the female, pheromone production is not controlled by the corpora allata, and pheromone release is under direct motor control.     

Production of males and gynoparae by apterous viviparae of Myzus persicae continuously exposed to different scotoperiods

At 18–19°C, apterous viviparae of a holocyclic strain of Myzus persicae raised from birth under constant scotoperiods of 9 hr 26 min–15 hr darkness per diem deposited apterous viviparae, alate viviparae, and males, in that sequence. Under the shortest scotoperiod (9 hr 26 min) in which males were recorded, only a few were deposited at the end of reproduction. With increasing duration of the scotoperiods, the aphids switched to the exclusive deposition of males progressively earlier in their reproductive lives. Thus more males and fewer females were produced; however the proportion of wingless females increased. Similar trends were recorded when the number of prenatal exposures to each scotoperiod was increased from 0 to 7.Alatae developed into gynoparae at scotoperiods of 10 hr 29 min or longer, and into virginoparae at 9 hr 40 min or shorter scotoperiods. Gynoparae and alate virginoparae, as well as alates that produced both oviparae and viviparae were found at 10 hr and 10 hr 15 min.When apterous viviparae were transferred to scotoperiods of 10 hr 29 min or 15 hr only when they attained adulthood, they also deposited males but only toward the end of their reproductive lives.     

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.     

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.     

Cereal aphid responses to sex pheromones and host-plant odours in the laboratory

Abstract. The movement of Sitobion fragariae (Wlk.) (Homoptera: Aphididae) males towards odours from conspecific sexual females (oviparae) and the aphid sex pheromone component (4a S ,7 S ,7a R )-nepetalactone were demonstrated in a linear-track olfactometer. Males of the closely related Sitobion avenae (Fab.) were attracted to odours from conspecific oviparae and also oviparae of S. fragariae. These results were consistent with the recent identification of this nepetalactone isomer as the major component of the sex pheromone in these species. Males of S.fragariae were not significantly attracted to oviparae of S.avenae. indicating some qualitative or quantitative difference in the pheromones of the two species. Males did not respond to the related (1R,4aS,7S,7aR)-nepetalactol or to host-plant odours. Gynoparae of these species moved towards the nepetalactone and also to host-plant odours. A combination of both stimuli was more attractive than plant odour alone. Gynoparae of S.fragariae also responded significantly to the combined treatment when this was tested against the nepetalactone.     

The photoperiodic responses and phenology of an English strain of the pea aphid Acyrthosiphon pisum

Abstract. 1. The response curves for the photoperiodic induction of the sexual forms (oviparae and males) differ significantly in an English clone of the pea aphid Acyrthosiphon pisum Harris. Male production is sharply peaked. The late summer scotophases (dark periods) that initiate male production are 1.0–1.5 h shorter than those that initiate ovipara production; the induction of males, but not oviparae, virtually ceases at scotophases longer than 12 h. This disparity suggests that there are two photoperiodic clocks.
2. All ovipara-producing aphids switch spontaneously to virginopara production part-way through the progeny sequence, irrespective of photoperiod. This may confer the ability to overwinter partheno-genetically under favourable climatic conditions. Since males are always born last in the progeny sequence this possibility would be pre-empted unless the terminal male sequences were suppressed by long winter scotophases.
3. The role of the photoperiodic response in determining the seasonal phenology was tested in the field by exposing a succession of laboratory-reared aphids to natural photoperiods, in late summer and autumn. Adult males and oviparae developed synchronously in early October, the difference in critical scotophase compensating for the late appearance of males in the progeny sequence. A large part of the 'civil twilight' is photoperiodically active.
4. Clones propagated outdoors by isolating aphids in each generation from the terminal sequence of virginoparae did not survive the whole winter of 1985/86. The chances of survival were reduced by severe weather and by the inability of the photoperiodic system to 'turn off' the production of early born oviparae which are, therefore, 'wasted'.     

Sexual forms of the pea aphid, Acyrthosiphon pisum, produced on an artificial diet

In recent years a number of aphid species have been successfully reared on chemically defined diets (Dadd & Mittler, 1966; Auclair, 1965; Dadd & Krieger, 1967; Ehrhardt, 1968). The development of such diets has offered an opportunity to study in detail several aspects of the physiology of these insects. In particular, the composition of the artificial diet has been shown to influence the production of winged forms by Myzus persicae (Sulzer) (Mittler & Dadd, 1966; Dadd, 1968). In all studies thus far, the aphids have been maintained in the parthenogenetic condition in order to accumulate data concerning the growth and fecundity of females of successive generations. However, it was clearly of interest to determine whether sexual forms could be produced by diet-reared aphids. If so, further information regarding the sexual reproduction of these insects would be forthcoming. Attempts to achieve this using local strains of Myzus persicae, Aphis fabae Scopoli and Acyrthosiphon pisum (Harris) were unsuccessful, presumably because these strains were anholocyclie (Kunkel, unpubl.). A clone of a green strain of A. pisum, previously found to be holocyclic (Sutherland, unpubl.), was then obtained from England and was cultured at 20° C in a photoperiodic regime of 16 hr light: 8 hr dark per day on young bean plants (Vicia faba). The artificial diet on which the experimental aphids were maintained was formulated according to Dadd (1967) and enclosed in sachets of stretched parafilm (Dadd, Krieger & Mittler, 1967). The aphids were provided with fresh sachets every 3–4 days. Adult apterous females taken from the plant culture were caged in groups of five, and exposed to a photoperiodic regime of 10 hr light: 14 hr dark per day at 15°. Successive batches of larvae deposited by these aphids were maintained in this environment until they were adult and had produced offspring for several days. These developed into oviparae and males. Compared to the sexual forms produced on host plants, these diet-reared individuals grew relatively poorly and mortality was high. Nevertheless, the surviving oviparae deposited numerous eggs, but these remained pale green whereas viable, fertilized eggs deposited by plant-reared oviparae rapidly become black. In the case of aphids reared on host plants in a short-day environment the possibility exists that the photoperiod may act indirectly via the plants and not directly on the insects themselves — a doubt which has been raised concerning Megoura viciae Buckton (von Dehn, 1967). However, our results with A. pisum reared on artificial diet demonstrate, as Lees did for M. viciae (Lees, 1960, 1967), that it is unnecessary to implicate the host plant in the determination of males and oviparae. This does not, of course, exclude the possibility that photoperiod-induced changes in a host plant may play a role as well. Nor have we ruled out the possibility that dietary composition may influence the aphids directly or their response to other environmental stimuli leading to the production of sexual forms.     

Sex Pheromone in the Aphid <Emphasis Type="Italic">Megoura viciae</Emphasis>

THE adult egg-laying females (oviparae) of most holocyclic aphid species bear on their swollen hind tibiae circular plaques or tubercles which taxonomists variously refer to as sensoria, pseudosensoria, or pseudorhinaria. It has been suggested that they aid the ovipara in fixing her eggs to the host plant¹, that they are sensory receptors², or that they produce a sex pheromone which attracts the males^3–5. Pettersson⁶ has advanced preliminary evidence for the latter function in a species of Schizaphis. Recent studies have shown that these structures (Fig. 1) in Megoura viciae Buckton do indeed secrete a sex pheromone and, moreover, that striking changes in the daily pattern of pheromone release occur as the female ages. In this article these pseudosensoria will be referred to as “scent plaques”, an appropriate term first used by Stroyan⁷.     

Embryogenesis and oögenesis in alate virginoparae,gynoparae, and oviparae of the aphid Myzus persicae, in relation to photoperiod

The study reports on the effects of prenatal and/or postnatal exposures to short-night or long-night conditions, and of crowding, on embryogenesis and oögenesis in alate virginoparae, gynoparae, and oviparae of a holocyclic strain of the green peach aphid, Myzus persicae, from Yakima, Washington State.In alate virginoparae raised at a density of 10–20 per radish seedling in a short-night regime (8 hr darkness per diem), 3–4 embryos occurred in each of their 10 ovarioles, when the aphids attained adulthood. More than 30 larvae were deposited by most of these alatae. However, in young adult gynoparae, raised at these densities in a long-night regime (15 hr darkness per diem), only one viable embryo (a presumptive ovipara) occurred per ovariole. The follicle containing this embryo was followed by 1–2 abnormal follicles in each ovariole, and the number of larvae deposited by a gynopara was generally less than 10. In young adult oviparae similarly raised under a long-night regime, only one egg typically occurred in each of their 10 ovarioles, and the eggs deposited by an ovipara (only after it had mated) generally numbered less than 10. Alate virginoparae and gynoparae contained an additional embryo in some of their ovarioles when these morphs were raised at a lower density (1–5 per plant).Presumptive gynoparae partially developed the reproductive features of alate virginoparae when transferred to a short-night regime at birth; the converse was true when presumptive alate virginoparae were transferred to a long-night regime early in larval life. Oviparae maintained in short nights from before birth developed the appearance of apterous virginoparae but still produced eggs rather than embryos. However, their oögenesis was enhanced and eggs (10–20) were deposited by them without prior mating. Under all regimes tested, oviparae were always deposited early in the larviposition sequence of their alate mothers, and the number of oviparae deposited never exceeded 15.The possible involvement of juvenile hormone in the regulation of these events and the ecological significance of the results are discussed.     

Photoperiodic determination of the male and female sexual morphs of Myzus persicae

The chronology of the photoperiodic determination of sexual morphs in holocyclic Myzus persicae was studied in the laboratory by transfer of synchronized batches of aphids between long-day (16 hr) and short-day (10 hr) régimes at a constant temperature of 20°C. The length of exposure to the short-day régime was measured in terms of the number of long dark-periods received by the aphids. The photoperiodic response extended over four generations (P, G₁, G₂, and G₃ respectively). When P generation aphids were given short days from the fourth instar, alate viviparae and males appeared successively in generation G₂, oviparae in G₃. Increasing the number of long dark-periods received during the development of G₂ embryos had a cumulative effect on the number which developed into alate viviparae. Determination of all the first-born G₂ aphids as alatae occurred only if their mothers had been exposed to the short-day régime throughout larval development. Alate viviparae gave birth to oviparae if they received a minimum of 4 long dark-periods, starting from a late stage in their embryonic development. The critical stage for ovipara determination in the G₃ embryo was on the sixth or seventh day after ovulation, more than half-way through embryonic development. G₂ aphids were determined as males before ovulation if their parents received 4 (in some circumstances only 3) long dark-periods. In the clones studied, male determination, once initiated in the G₁ parent, could not be reversed by later back-transfer to the long-day régime.     

Esterase 6 of Drosophila melanogaster: Kinetics of transfer to females,decay in females and male recovery

Esterase 6 (E.C. 3.1.1.1) is an enzyme in the reproductive system of Drosophila melanogaster and is transferred from males to females at mating. This enzyme is conveyed during the first 3 min of a copulation lasting approximately 20 min and remains active in the female reproductive tract for 1–2 hr after mating. Males require 24–48 hr to recover premating levels of esterase 6 activity. These results suggest that the effect of esterase 6 on the rate of sperm loss in females, which extends to 4 days after mating, is indirect since activity in the female falls rapidly after insemination. It is suggested that esterase 6 may also be a part of a pheromone system which influences female reproductive behaviour.     

Cuelure but not zingerone make the sex pheromone of male Bactrocera tryoni (Tephritidae: Diptera) more attractive to females

In tephritid fruit flies of the genus Bactrocera Macquart, a group of plant derived compounds (sensu amplo ‘male lures’) enhance the mating success of males that have consumed them. For flies responding to the male lure methyl eugenol, this is due to the accumulation of chemicals derived from the male lure in the male rectal gland (site of pheromone synthesis) and the subsequent release of an attractive pheromone. Cuelure, raspberry ketone and zingerone are a second, related group of male lures to which many Bactrocera species respond. Raspberry ketone and cuelure are both known to accumulate in the rectal gland of males as raspberry ketone, but it is not known if the emitted male pheromone is subsequently altered in complexity or is more attractive to females. Using Bactrocera tryoni as our test insect, and cuelure and zingerone as our test chemicals, we assess: (i) lure accumulation in the rectal gland; (ii) if the lures are released exclusively in association with the male pheromone; and (iii) if the pheromone of lure-fed males is more attractive to females than the pheromone of lure-unfed males. As previously documented, we found cuelure was stored in its hydroxyl form of raspberry ketone, while zingerone was stored largely in an unaltered state. Small but consistent amounts of raspberry ketone and β-(4-hydroxy-3-methoxyphenyl)-propionic acid were also detected in zingerone-fed flies. Males released the ingested lures or their analogues, along with endogenous pheromone chemicals, only during the dusk courtship period. More females responded to squashed rectal glands extracted from flies fed on cuelure than to glands from control flies, while more females responded to the pheromone of calling cuelure-fed males than to control males. The response to zingerone treatments in both cases was not different from the control. The results show that male B. tryoni release ingested lures as part of their pheromone blend and, at least for cuelure, this attracts more females.     

Hormone-pheromone relationships of male Tenebrio molitor

Males of the beetle Tenebrio molitor produce a volatile sex pheromone which attracts females of the same species. The pheromone level peaks 8 days after emergence and then reaches a plateau. Elimination of endocrine centers by decapitating male adults 24 hr following adult ecdysis did not impair pheromone production. Treatment of decapitated males with juvenile hormone analogues did not make any detectable difference in the levels of pheromone activity. However, undecapitated males treated with juvenile hormone analogue showed a significant increase in pheromone activity when compared with those that had been decapitated and subsequently treated with juvenile hormone analogue. This observation is discussed in the light of published research on the effect of juvenile hormone on pheromone activity of females of T. molitor.     

A morphological study on autumnal morphs of Aphis glycines (Hemiptera: Aphididae)

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most important pests of soybean. The complex life cycle of A. glycines is characterized as heteroecious and holocyclic, and has seasonal polymorphisms occurring during its life cycle. In the autumn, A. glycines occur as winged and wingless virginoparae in soybeans, as gynoparae and males that migrate from soybeans to Rhamnus spp. and as gynoparae, males and oviparae on Rhamnus spp. In this study, wingless virginoparae, gynoparae, males and oviparae of A. glycines were successfully induced in the laboratory and morphological parameters of these morphs were selected for quantitation. To aid in identification of these A. glycines autumnal morphs, these aphids were imaged by microscope and significant differences in morphological characteristics were found: distal parts of hind leg femurs of gynoparae were grayish black, which were darker than those of winged virginoparae; the 4th instars of gynoparae, males and winged virginoparae differ greatly in dorsal abdomen coloration and covering. Our results provide an important guide for distinguishing adults of gynoparae and winged virginoparae, and for identifying nymphs of gynoparae, males and winged virginoparae.     

Sex Pheromone Composition and Male Trapping of the Peach Fruit Moth,Carposina sasakii (Matsumura) (Lepidoptera: Carposinidae) in Korea

Sex pheromone composition, mating behavior, and field trapping were analyzed for the peach fruit moth, Carposina sasakii(Matsumura) to develop a monitoring system with its sex pheromone. The upwind flying response of males to female was the most frequent at 4th to 5th hr after lights-off. The highest mating rate was seen at 5th hr after lights-off. The extract of female abdominal tip was analyzed with gas chromatography and proved to have two compounds, (Z)-7-eicosen-11-one and (Z)-7-nonadecen-11-one. In field-trapping, however, a lure containing (Z)-7-eicosen-11-one only showed the highest attractivity.     

Responses of male aphids to the female sex pheromone in Megoura viciae Buckton

Oviparae of Megoura viciae Buckton release a sex pheromone from numerous plaques on their hind tibiae. Adult males react to this scent in a variety of ways: inactive males are aroused; males already walking orient to the odour source; and copulatory activity is increased. These responses are only evoked within a few centimetres of the stimulus source and decline rapidly as the stimulus is diluted. Male responsiveness to the pheromone is unchanging throughout the light phase (of LD 12 : 12), although they show a marked circadian locomotor rhythm. Their sensitivity develops early in adult life and thereafter remains high, decreasing only slightly before death. However, although very young adults will orient to a pheromone source, they do not show copulatory responses until they are sexually mature. Larval males neither respond to the pheromone nor possess the antennal receptors (secondary rhinaria) which are essential for the adult reaction. Mating, and attempted copulation with suitable objects (e.g. coloured beads), is dependent upon appropriate visual and tactile stimuli; it can occur in the absence of the pheromone but is enhanced by its presence. Habituation to the scent does not prevent copulation, and conversely, copulation does not affect subsequent responsiveness to the pheromone. Once copulation has begun the pheromone has no effect on the efficiency of insemination. Vigorous intergeneric responses to the pheromones of female M.viciae and Acyrthosiphon pisum Harris were observed.     

Plant quality, progeny sequence, and the sex ratio of the sycamore aphid, Drepanosiphum platanoidis

The reproductive sequence of sexuparae of the sycamore aphid, Drepanosiphum platanoidis (Schrank) (Homoptera: Callaphididae), observed in the field and glasshouse was examined to elucidate the relationship between host nutrition and sex ratio. The observations were made in autumn when the transition from parthenogenetic to sexual reproduction occurred. A switch occurred in the reproductive sequence of the sexuparae. The production of apterous sexual females (oviparae) was followed by alate males, after a brief reproductive pause lasting 2.5–4.0 days. The switchover period was relatively constant across treatments and years. On poor hosts, the first appearance of the oviparae was a day later, whereas the first appearance of males was a day earlier than those on good nutrition. The primary sex ratio (i.e., proportion of males) was numerically female biased. Under semi‐natural field conditions it was 0.22, but altered to 0.18 and 0.29, respectively, under poor and good host nutrition in the glasshouse. In both the field and glasshouse, nymphal development time was significantly longer in oviparae (ca. 22 days) than in males (ca. 18 days). The time from birth to adult was significantly shorter on good hosts (oviparae: 20 days; males: 17 days) than on poor hosts (oviparae: 23 days; males: 19 days). The proportion of nymphs surviving to the adult moult was not dependent on sex in both the field and glasshouse, but the chances of survival were slightly enhanced under good (88%) compared with poor (82%) host nutritive status. In conclusion, the order of morph production and differences in maturation times ensured the synchronisation of the sexes so that mating and oviposition opportunities were optimised before the onset of winter. The female‐bias in the sex ratio maximised the fitness of sexuparae, and reduced the chances of local mate competition by economising in members of the competing sex.     

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.     

Nippostrongylus brasiliensis: Female incubation,release of pheromone,fractionation of incubates

The release of pheromone by female Nippostrongylus brasiliensis as a crude incubate was linear for the first 2 hr, but declined after this period. Pheromone release in solution increased with temperature elevations until a 37 C incubation temperature was reached. Higher temperatures of incubation apparently caused diminished pheromone release. Gel filtration of female pheromone that was prepared as a crude incubate revealed biologically active elutions at K_av, 0.64 and 1.0. The timed release of female pheromone activity at these two elution regions coincided additively with the production of activity as a crude incubate. Each individual Chromatographic fraction from females accounted for about 50% of the pheromone activity of the crude, nonfractionated incubate, based on the male's bioassay response. Recombination of the K_av 0.64 and 1.0 elutions enabled recovery of pheromone activity that was similar to crude incubate. The gel filtration elution of 260-nm absorbance from male- or female-produced incubate was qualitatively similar, but a range of quantitative differences were evident. The fractionation of incubate from several female densities revealed only quantitative differences.