A transgenerational interval timer inhibits unseasonal sexual morph production in damson-hop aphid, Phorodon humuli

Abstract.  The induction of sexual and parthenogenetic morphs of the damson-hop aphid, Phorodon humuli , on hops is controlled by daylength. The ability of P. humuli , to produce winged pre-sexual females (gynoparae) in the short-day conditions of spring is inhibited by an interval timer present in generations immediately after hatching of the overwintering egg. The inhibition expires after three generations when nymphs are born and reared in short days (LD 12 : 12 h), irrespective of whether their parents are reared in short or long days (LD 18 : 6 h). No gynoparae are produced by aphids maintained for 13 generations in long days. Two wingless aphids from 35 survive transfer from Prunus spinosa to hops. No winged females are produced during nine generations among their progeny maintained in long days on hops, but gynoparae, followed by males, are produced one generation after these aphids are transferred to short days.     

Electroantennogram responses of the three migratory forms of the damson-hop aphid, Phorodon humuli, to aphid pheromones and plant volatiles

Electroantennogram (EAG) responses were recorded from alate fundatrigeniae (spring migrants), gynoparae (the winged female form that produces sexual females) and males, the three migratory forms of the damson-hop aphid, Phorodon humuli (Schrank). EAG responses of gynoparae and males showed typical dose response characteristics to (E)-2-hexenal, (-)-R-carvone, hexanenitrile and (1RS,4aR,7S,7aS)-nepetalactol, the sex pheromone of this species. The 34 plant volatiles elicited broadly similar EAG response profiles in the three migratory forms. Green leaf volatiles produced large responses in all forms; however, the relative order of responsiveness varied. EAG responses to isomers of the monoterpene carvone differed between forms, with males being most, and spring migrants least, responsive. The hop-plant volatile and aphid alarm pheromone, (E)-beta-farnesene, evoked similar EAG responses in all forms. By contrast, males were most responsive to the three sex pheromone components, (-)-(4aS,7S,7aR)-nepetalactol, (+)-(4aS,7S,7aR)-nepetalactone and (1RS,4aR,7S,7aS)-nepetalactol. Males were no more responsive to their own sex pheromone, (1RS,4aR,7S,7aS)-nepetalactol, than to the other aphid sex pheromone components tested. Spring migrants and gynoparae also responded to the three sex pheromone components. This study indicates that migratory forms of P. humuli detect a wide range of volatile compounds, and that they are equally well-adapted for the detection of volatiles associated with host and non-host plants and with other species of aphid.     

Effects of plant spacing and interplanting with oilseed rape on colonisation of dwarf hops by the damson-hop aphid, Phorodon humuli

The pattern of colonisation of dwarf hops (Humulus lupulus) by damson-hop aphid (Phorodon humuli (Schrank)) migrating from Prunus spp. was investigated at six plant spacings and where some of the hops were replaced by oilseed rape (Brassica napus L.), a non-host of the aphid. The number of migrant aphids that accumulated on hop stems (bines) increased with increasing bine size and density. The numbers of aphids that colonised hops interplanted with oilseed rape reflected the density of the hop plants only and not the overall plant density. As the physical size of the wind shadow within which flying aphids can manoeuvre and land was unimportant unless provided by a host plant, the finding supports the theory that flying aphids respond to olfactory stimuli associated with their hosts. Variation in bine height (as a measure of plant size) explained 29–93% of the variance in aphid counts during the 3 years' study and bine density 1–14%. Standardising the data as the numbers of aphids per metre of bine and taking a square-root transformation of these standardised counts improved the precision of the analyses and, by stabilising variances, facilitated comparisons between years as growth became more vigorous as the plants matured. Each year, the rate of increase in numbers of aphids settling on plots of hops declined curvilinearly with increasing bine density. Maximum colonisation by P. humuli occurred at a bine density of five per metre row, a density similar to that used commercially by growers of dwarf hops.     

Flight activity of the damson–hop aphid, Phorodon humuli.

Flight activity of Phorodon humuli was monitored using suction traps, laboratory studies and mark and recapture experiments. Emigrants were trapped as they flew from a Myrobalan (Prunus cerasifera) hedge and among dwarf hops (Humulus lupulus). Daily flight curves were bimodal with 69% and 38% of emigrants caught in the morning peak near Myrobalan and among hops, respectively. The median period of flight activity was from 2 h after sunrise until 30 min before sunset. The lower temperature for flight was 13.5°C in the field and 14.9°C for take off in the laboratory. Variations in wind speed had little effect on flight activity explaining <2.5% of the total variance among insect counts. The percentage of emigrants on hop declined exponentially with time. The relationship, y= 10.9(±2.0) + 64.3(±2.3) × 0.92(±0.01)^t where t = daylight hours (standard error in parentheses), explained 98.3% of the variance. Hence, 62% of new arrivals flew within 1 day of arrival and 79% within 2 days. Similar numbers arrived as departed at 08:30, 10:30 and 12:30 h, but at 14:30 h twice as many arrived than departed and at 16:30 h, the accumulation was threefold. Daily flight curves of return migrants and males leaving hop were bimodal with 70% and 80%, respectively, trapped in the earlier peak. In the field, the median lower temperature for flight was 13.2°C for return migrants and a nonsignificantly different 12.8°C for males. The mean temperature for take off by return migrants was 15.7°C in the laboratory.     

Cost-benefits of reduced aphicide usage on dwarf hops susceptible and partially resistant to damson-hop aphid

Soil‐applied imidacloprid at full (125 g a.i. ha^?1) and half approved doses gave levels of control of damson‐hop aphid, (Phorodon humuli), similar to that provided by foliar spray(s) of tebufenpyrad on the aphid‐susceptible dwarf hop cvs First Gold and Herald. On those cultivars, aphid control was unreliable on plots treated with quarter dose imidacloprid and was generally no better than on untreated plants. Aphids were virtually eliminated from the leaves by the end of July each year in all treatments consistent with the action of natural enemies. Aphid contamination of cones reflected the numbers on foliage at flowering time, but varied widely between years. Yields and percentage α‐acids content of dried hops were unaffected by the numbers of aphids on leaves early in the season and in cones at harvest, but aphid contamination reduced the economic values of crops by as much as 80%. Few P. humuli colonised the partially aphid‐resistant breeding line 23/90/08 before their numbers were regulated and consistent with natural enemy activity. Yields, percentage α‐acids content, and commercial value of harvested cones were similar in all treatments on 23/90/08 whether or not plants were treated with aphicides. The commercial risks posed by P. humuli preclude substantial reductions in aphicide usage on aphid‐susceptible dwarf hop cultivars, but future cultivars expressing a similar level of partial resistance to aphids as 23/90/08 should not need treatment with aphicides.     

Electrical penetration graphs of the damson-hop aphid, Phorodon humuli on resistant and susceptible hops (Humulus lupulus)

Electrical penetration graphs (EPG's) were used to locate resistance to Phorodon humuli (Schrank) (Homoptera, Aphididae) in hops (Humulus lupulus, Cannabinaceae). Aphids on those hops showing resistance had a much reduced E2 pattern (uptake of phloem). In addition, many aphids on the resistant plants spent time non-probing within two minutes of withdrawing from the phloem. This was not observed with aphids on susceptible hops. The results suggest that resistance is located in the phloem. The involvement of a mechanical factor such as the blocking of aphid stylets, the presence of antinutritional factors, or simply an inadequate supply of nutrients, are discussed as possible resistance mechanisms.     

Insecticide resistance in damson-hop aphid, Phorodon humuli in commercial hop gardens in Kent

From 1966 to 1976, samples of Phorodon humuli were collected annually from five commerical hop gardens in Kent and from other hop gardens where problems in control occurred. A susceptible stock was obtained from wild hop growing in northern England in 1969. The samples were cultured in isolation on potted hops and bioassayed against insecticides in common use. The level of resistance to demeton-S-methyl was c. 10X in 1966 after 10 yr use, and more than doubled from 1968–1974 apparently due to the spread of a more resistant type; there was a further increase to c. 50X in 1975–1976. There was also resistance of C. 20–30X to omethoate, 2–7X to methidathion and 4–8X to methomyl. Assays and field results show an increased resistance to methidathion and less certainly to methomyl after 5 yr use. There was no clear change in response to endosulfan. The LC₅₀'s estimated from a single dose and a mean probit slope were found to agree satisfactorily with the LC₅₀'s calculated from serial doses and so should be adequate for monitoring trends in resistance.     

Associations between weather factors and the spring migration of the damson-hop aphid, Phorodon humuli

The dates of the beginning and end of the spring migration of P. humuli, as monitored by the Rothamsted Insect Survey suction traps at Wye College and Rosemaund Experimental Husbandry Farm, were linearly regressed on temperature, rainfall and sunshine for varying periods. The beginning of migration at both sites was associated with temperature in late March and early April, and periods of rainfall in mid-January and mid-April, while the end of migration was associated with temperature and sunshine in mid- and late June, and with mid-January rainfall. These regression equations were used to predict the timing of the migration in 1980 and 1981, those for mean maximum temperature predicting most accurately both the beginning and end of migration. The use of multiple regression equations did not increase the accuracy of predictions. The critical periods of weather are discussed in the context of the life-cycle of the aphid.     

Photoperiodic regulation of the development of winged gynoparae in the aphid, Aphis fabae

ABSTRACT. In uncrowded rearing conditions, determination of the winged gynopara of the Aphis fabae Scopoli is dependent upon both pre- and postnatal short days (LD 12:12). Extension of the photophase to produce longday (LD 16:8) conditions localized on the head or abdominal region, showed that during the early larval instars of the parent generation (G1) there is a maternally-controlled induction of gynoparae. However, during later stages of embryonic development the presumptive gynoparae respond directly to photoperiod through the mother's abdominal wall. During early postnatal development, presumptive gynoparae (G2) remain sensitive to photoperiodic conditions; the photoperiodic receptors lie in the head. These results are discussed with respect to possible endocrine mediators of this photoperiodically controlled polymorphism.     

Distribution of damson-hop aphid (Phorodon humuli) migrants on hops in relation to hop variety and wind shelter

The distribution of migrant Phorodon humuli was studied in two hopgardens during June 1972. Migrants accumulating upon the young tissues near the bines' apices were counted. Plant size affected distribution, 100 % more migrants were found on 2-bine than on single bine strings and there was a positive linear relation between bine height and log₁₀ aphid numbers. Plants surrounding wire-trellis support poles were more heavily infested than plants not at poles, and migrants were more abundant on leeward orientated than windward strings. It is argued that the distribution of alatae reflected local patterns of wind shelter. Differences between plants declined in successive weeks. The influence of hop variety on migrant settling was studied in one of the hop-gardens. Fewer migrants settled on the variety Tolhurst than on Northern Brewer, and Fuggle was intermediate. Part, but not all, of the difference between varieties was explained by the larger average size of Northern Brewer plants. The observed aphid deposition rates in the two hop gardens were compared with hypothetical deposition rates calculated from numbers of P. humuli caught in a nearby 12-2 m Rothamsted Insect Survey suction-trap, and used to estimate flight durations. The estimates indicated that most infestation probably resulted from aphids within 1 h flying time of their primary host source.     

蚜虫雄蚜与雌性母对性信息素及植物挥发物的田间反应

田间观察了桃蚜Myzus persicae (Sulzer)、绣线菊蚜Aphis spiraecola Patch 、山楂圆疣蚜Ovatus crataegarius (Walker)等3种蚜虫对性信息素[(4aS,7S,7aR)-荆芥内酯和 (1R,4aS,7S,7aR)-荆芥醇]的反应,并且调查了性信息素与植物挥发物对桃蚜的田间引诱活性的相互作用.在有冬寄主或夏寄主植物的田中,性信息素诱捕器诱捕到桃蚜雄蚜与雌性母的数量显著多于对照诱捕器的诱捕数;但在非寄主植物的田中,却引诱不到桃蚜.苯甲醛(冬寄主植物桃树Prunus persica的主要挥发物组分之一)能够增强桃蚜雄蚜的引诱作用.绣线菊蚜雄蚜和雌性母对植物中提取的荆芥内酯有反应,而山楂圆疣蚜雄蚜和雌性母对植物中提取的和人工合成的荆芥内酯都没有反应,但对荆芥醇有反应.并且在荆芥醇中添加荆芥内酯之后对山楂圆疣蚜雄蚜引诱活性显著提高.还讨论了雌性蚜产生化合物被雄蚜作为性信息素、被雌性母作为聚集信息素以及性信息素与寄主植物挥发物的相互作用.     

Pheromone Traps for the Dissemination of an Entomopathogen by the Damson-hop Aphid Phorodon humuli

Two types of sex pheromone-emitting trap, a simple louvred trap and a commercially-produced wasp trap (Waspy®) designed or modified as delivery systems for entomopathogens, were tested using an isolate of the pathogen Verticillium lecanii . Their efficiencies for capturing winged autumn females (gynoparae) and males of Phorodon humuli in a hop garden and a plum orchard were compared with each other and with catches by yellow-painted water traps. Gynoparae rarely entered either type of pathogen dissemination trap. Males only entered traps that released (1 R , S ,4a R , 7 S , 7a S )-nepetalactol, the sex pheromone of P. humuli . In the hop garden, approximately five times as many males entered the modified Waspy® as entered the louvred traps, whereas in the plum orchard similar numbers of males were caught in both traps. On average, males visited the modified Waspy® trap for 34.1 ±7.9 (SE) min. Males spent about 50% of their time in the arena where the entomopathogen would normally be present and a further 20% of the time on the inside of the arena lid alongside the pheromone source. Out of a sample of 16 live aphids removed from a trap dispensing V. lecanii , 9 died from infection by the pathogen and 5 of the 16 initiated colonies of the fungus after they walked on a sterile agar plate for five minutes. None of the 15 aphids collected from traps without V. lecanii became infected or initiated colonies of the fungus on agar plates.     

The role of Anthocoris species (Hemiptera: Anthocoridae) in the integrated control of the damson-hop aphid (Phorodon humuli)

Field studies in 1974, 1975 and 1976 investigated integrated control of the damson-hop aphid Phorodon humuli on hops. After the aphicidal effects of an early-season soil drench of mephosfolan had declined, natural enemies controlled the aphids for the remainder of the season. Anthocorid bugs, particularly Anthocoris nemoralis, were the most abundant predators. In each year a rapid decline in aphid numbers occurred in mid- to late-July, coinciding with the peak numbers of fourth and fifth instar larvae and adults, the most voracious anthocorid stages. Aphids in the cones remained under control for the rest of the season in 1974 and 1975, and increased in 1976 but damaging numbers did not develop. When predators were excluded by caging mephosfolan-treated bines, high aphid densities developed on the leaves, and the cones were heavily infested. Plants not treated with an insecticide were almost completely defoliated by late-July. Heavily infested ‘missed bines’, due to uneven uptake of mephosfolan, attracted large numbers of anthocorids, which later dispersed into the surrounding plants.     

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.     

Consumption of Damson-hop Aphids (Phorodon humuli) by Larvae of Coccinella transversoguttata and Hippodamia convergens (Coleoptera: Coccinellidae)

Based on biomass, larvae of Hippodamia convergens Guerin consumed an average of 318 adult damson-hop aphids (Phorodon humuli (Schrank)), during their development at 20 C. Female larvae of Coccinella transversoguttata Falderman ate 413 adult P. humuli and males ate 357. This difference in the consumption of prey occurred only in the fourth stadium and was reflected in a corresponding size dimorphism between female and male larvae at pupation.     

Biological control of the damson-hop aphid,Phorodon humuli (Hom.: Aphididae), using the ladybeetleHarmonia axyridis (Col.: Coccinellidae)

The possibility of usingHarmonia axyridis (Pallas) to control the damson-hop aphidPhorodon humuli (Schrank) in a dwarf-hop garden was studied in northern France in 1994 and 1995. Second and third instar larvae ofH. axyridis were released at different stages of the aphid population increase (early, at the time of insecticide treatment threshold was exceeded and late). In the control, the number of aphids reached 191.3±30.8 per leaf at the end of June. In the plots where 50 larvae per plant were released, the best control was obtained when larvae were released early and the aphid population was approximately 20 per leaf. In this case, the average number of aphid per leaf did not exceed 54.5±10.3 aphids at the end of June, which is lower than the insecticide treatment threshold of 80 aphids per leaf. Indigenous predators, especiallyAdalia bipunctata L., complemented the effect ofH. axyridis.     

The time of determination of gynoparae and males in the bird cherry–oat aphid, Rhopalosiphum padi

Apterous exules of Rhopalosiphum padi which experienced short photoperiods only during the first half of their nymphal life all produced gynoparae which made up 57% of the offspring produced in the first 7 days of the mother's reproductive life. Short photoperiods during the second half of a mother's nymphal life did not induce the production of gynoparae. However, when short photoperiods were experienced throughout a mother's nymphal life significantly more gynoparae (82%) were produced. Ten per cent of the offspring of mothers that experienced short photoperiods only during their adult life developed into gynoparae. Of the offspring reared in short photoperiods, but born to mothers reared and kept in long photoperiods, 30% developed into gynoparae. When mothers were exposed to short photoperiods in their adult life and their offspring so treated, then 90% of the offspring developed into gynoparae. Males only occurred amongst the last offspring of mothers that experienced short photoperiods in either the first or the second half of their nymphal life.     

Spatial distribution of the green peach aphid used in estimating the populations of gynoparae

Summary In 2 years, during the initial invasion of peach leaves by the green peach aphid,Myzus persicae (Sulzer), the number of gynoparae was low, and the distribution on leaves was random. Then as the mean number increased, the distribution became intermediate and could not be distinguished from either a Poisson or a negative binomial. Finally, as the mean continued to increase, the variance increased rapidly, and the population was found to fit a negative binomial distribution. Thus the aggregation response was verified because the dispersion pattern fitted a contagious distribution. A sampling plan was devised by which the dispersion parameterk was used to estimate the density of aphids per leaf based on the percentage of leaves infested. Sampling the third year of the study confirmed the validity of the sampling parameter that had been calculated from data for the 2 previous years.