Photoperiodic induction of winged females in the black bean aphid. Aphis fabae

Abstract. The Photoperiodic of winged females (alatae) in the black bean aphid, Aphis fabae Scop. (Homopetera: Aphididae), is investigated in detail with emphasis on the interaction of the maternal and embryonic/young larval photoperiodic clocks. Previous work had shown that in uncrowded conditions the induction of gynoparae (winged females that produce sexual females) requires both prenatal and postnatal exposure to long-night (12 h) Photoperidic cycles: present results show that sole postantal exposure to long nights of any lenght does not induce wing formation in early-born aphids.
When aphids were exposed to experimental light-dark cycles postanatally only, their daughters developed as alate in long nights and as apterae in short nights: the critical night lenght (CNL) was 11:1 h. Additional prenatal exposure to experimental regimes resulted in a significantly shorter CNL (10.6 h). This difference could be accounted for by the fact that more experimental light-dark cycles were experienced in the latter case.
Apterous aphids transferred from LD 16:8 h to LD 12:12 h as either third-or fourth-stadium larvae, or young adults, switched for aptera-production to alata-production. The transition form aptera- to alata-production was rather abrupt in third-stadium transfers but more gradual when transfers occurred as fourth-stadium larvae and adults. Moreover, s the number of days required for 50% of the aphids to become alata-producers increased from 7–8 in third-stadium transfers, to 9–10 and 11–12 in the later transfers.     

The effect of juvenile hormone on host-plant preference in the black bean aphid, Aphis fabae

ABSTRACT. When offered the choice between a germinating tick bean (summer host) and a detached spindle leaf (winter host) adult gynoparae of Aphis fabae Scop. showed a distinct preference for spindle, as judged by site of larviposition. However, when offered the same alternatives, all four larval instars showed a settling preference for bean. A switch in host preference therefore occurs at or shortly after final (fourth) moult. Fifth instar, supernumerary larvae induced by juvenile hormone (JH I) treatment also preferred bean, indicating that the host preference switch at the fourth moult had been inhibited. Larval/adult intermediate forms produced by JH I treatment, but which were capable of parturition, showed a significant increase in the acceptability of bean as a larviposition site. Acceptability was proportional to the degree of juvenilization. Thus, although larviposition is an adult prerogative, JH I can influence the preferred site. This may, however, be an indirect effect which reflects a juvenilized settling preference.     

Perception of volatiles associated with sex and food by different adult forms of the black bean aphid, Aphis fabae

Abstract. Electroantennograms (EAGs) were recorded from adult male and asexual forms (winged and wingless virginoparae and gynoparae) of the black bean aphid, Aphis fabae , during stimulation with two sex pheromone components, (+)-(4a S ,7 S ,7a R )-nepetalactone and (-)-(1 R ,4a S ,7 S ,7a R )-nepetalactol, as well as six plant volatiles, i.e. ( E )-2-hexenal, ( E )-2-hexenol-1, ( Z )-3-hexenol-1, ( Z )-3-hexenyl acetate, hexanal and allyl isothiocyanate. The male antennae are 1000-10,000 times more sensitive to nepetalactol and nepetalactone than to the plant compound ( E )-2-hexenal. Besides this marked difference of EAG peak responses in males, the EAG rise and decay are slower for the sex pheromone components. Males are also much more sensitive to the sex pheromone components than asexual females. This high sensitivity correlates with a predominance of antennal secondary rhinaria, the major sites of pheromone perception in the male. However, it is the primary rhinaria on the antennae of the wingless asexual females that are responsible for pheromone perception. Male antennae are as responsive as the asexual female antennae to the plant volatiles. The specialization of the male for mate location is discussed.     

Electrophysiological characterisation of olfactory sensilla in the black bean aphid, Aphis fabae

Electrophysiological responses of three different olfactory sensilla (proximal primary rhinaria (PPR), distal primary rhinaria (DPR) and secondary rhinaria (SR)) to the sex pheromone components, nepetalactol, nepetalactone, and a plant volatile, (E)-2-hexenal, were investigated in four different morphs of the black bean aphid, Aphis fabae Scopoli. The DC responses recorded directly from the antennal sensilla and termed electrosensillograms (ESGs) were generally much larger (up to 14 mV) than electroantennogram (EAG) responses (up to 2.5 mV). Characteristic morph-specific response profiles to these compounds were observed in each type of rhinarium and response waveforms were different between (E)-2-hexenal and the sex pheromone components. (E)-2-Hexenal elicited the largest responses at PPR, while nepetalactol and nepetalactone elicited the largest responses at SR in gynoparae and males. Nepetalactol and nepetalactone also showed significant activities on DPR and PPR in all morphs. In contrast, (E)-2-hexenal had almost no activity on SR. However, almost all of the SR investigated in males and gynoparae were sensitive to both nepetalactol and nepetalactone. A small sub-set of male SR responded mainly to nepetalactol. SR of winged virginoparae did not respond to the sex pheromone compounds. Paraffin oil (the solvent control) also elicited significant responses at PPR in virginoparae but not in other morphs. In a further experiment, SR of winged virginoparae showed no response to 30 other plant volatile compounds or the alarm pheromone component, (E)-beta-farnesene. Nepetalactol and nepetalactone had similar dose-response profiles in the SR of gynoparae. The results indicate that SR in males and gynoparae are highly specialised to detect sex pheromone compounds, while the DPR and PPR are relatively broadly tuned to both plant volatiles and sex pheromone components. The presence of SR in winged virginoparae that are not responsive to sex pheromone components, alarm pheromone, or any of the plant volatile compounds tested may indicate a possible role of these sensilla to detect, as yet, unknown compound(s) with a high specificity. The present study also suggests that PPR may play a role in detecting paraffin-related compounds such as cuticular hydrocarbons of plants.     

The photoperiodic control of wing development in the black bean aphid,Aphis fabae

Newly born presumptive gynoparae of Aphis fabae were transferred from their prenatal short-day rearing conditions (light-dark 12:12, 15°C) to a variety of postnatal photoperiodic regimes. Long days prevented wing formation and the majority of aphids developed into apterous or alate-apterous intermediate adults. Continued short days resulted, almost exclusively, in winged adults. The photoperiodic-response curve (T = 24) revealed a critical photoperiod of light-dark 13.5:10.5 and further investigations showed that morphogenesis depended more upon night- than day-length. Maximal apterization occurred with 8 or 9 h dark regardless of the length of the photophase but at photophases of 12 h or less the critical night length was reduced to 8.5 h. Night-interruption experiments revealed two peaks of photosensitivity when the scotophase was 12–14 h long but only a single peak was seen with longer dark periods. A series of experiments using early night interruptions followed by extended dark revealed apparent critical night lengths which decreased as the interruption was placed later in the scotophase. Resonance experiments involving 12 or 16 h photophases and extended scotophases at 15°C revealed long-day effects with scotophases shorter than critical and short-day effects with longer dark periods. However, similar regimes at 20°C produced three peaks of apterization 24 and 20 h apart indicating the possibility of a circadian element involved in the photoperiodic response. The results are compared with the photoperiodic responses of other insects.     

Lipid composition in long-day and short-day forms of the black bean aphid,Aphis fabae

Long-day reared winged (alate) virginoparae from laboratory stock cultures which had been reared throughout larval development on bean stipules were significantly smaller (0.46+/-0.02 mg; mean+/-SEM) than short-day-reared gynoparae (0.69+/-0.04 mg; the winged autumn migrant) which completed development on intact beans. When winged virginoparae were raised from the third stadium on bean seedlings they grew larger (0.86+/-0.02 mg) but the gynoparae contained proportionally more total lipid (12.1+/-0.4%, gynoparae; 7.4+/-0.6%, stipule-reared virginoparae; 9.2+/-0.8%, seedling-reared virginoparae). Wingless aphids (apterae) were heavier, whether reared in short (0.99+/-0.03 mg) or long days (0.95+/-0.04 mg) but the lipid content was low (4.5+/-0.7% and 4.9+/-0.6%, respectively). The triacyl-, diacylglycerol and the phospholipid contents followed this trend but analysis of the fatty acid moieties of the triacylglycerides showed phenotypic differences. The ratios of myristic acid:palmitic acid were significantly higher in the winged forms than the wingless forms and were much higher in the gynoparae than the winged virginoparae. Short-day-reared wingless females also had a higher myristic acid:palmitic acid ratio than long-day-reared apterae, possibly reflecting the embryonic gynoparae maturing in their ovaries.     

Migratory and targeted flight in seasonal forms of the black bean aphid, Aphis fabae

ABSTRACT. Adult winged forms of Aphis fabae Scop., the spring migrants (fundatrigeniae; alate virginoparae), the summer migrants (alate virginoparae) and the autumn migrants (gynoparae), were flown in an automated vertical wind tunnel, with a small green target presented every 60 s. On average, targeted flight developed in the spring and summer migrants after 19 and 15 min, respectively. However, in autumn migrants targeted flight occurred after 184 min of flight. No evidence of target approach was found up to 30 min prior to this time, although some movement towards the target was observed in the 30 min before the first response of autumn migrants, suggesting that a gradual change from migratory to targeted flight occurred. No correlation was found between aphid weight and the time to first response for spring or summer migrants, but a positive correlation was found for autumn migrants. Flight patterns of autumn migrants, in the absence of a target, are described and compared with flight patterns previously reported for summer migrants.     

Maternal reproductive decisions are independent of feeding in the black bean aphid,Aphis fabae

Aphids are phloem feeders and an important assumption has been that reproduction is initiated only after phloem ingestion. Here we investigate the plant tissue location of parturition cues in winged and wingless, summer virginoparae and autumn migrants (gynoparae) of the black bean aphid, Aphis fabae. These seasonal forms have different host preferences. Using electrical penetration graph (EPG: to observe activity of the mouthparts) and video-monitoring procedures we demonstrate that the time to first parturition after host-plant contact is significantly shorter than the time to first registered phloem contact in the summer winged form. In gynoparae, the time to first parturition does not significantly differ from time to first phloem contact but is shorter than time to first phloem ingestion. Times to first parturition, first registered phloem contact and first phloem ingestion do not differ significantly in the summer wingless form. Simultaneous EPG and video recording procedures show that a high proportion of individuals of all morphs (45-70%) initiate reproduction before sustained phloem activities (salivation/ingestion). The only behaviours that all individuals demonstrate before first parturition are ‘non-penetration’ (aphid on plant surface with mouthparts outside plant) and stylet ‘pathway activity’, including secretion of gelling saliva and penetration of the non-vascular (epidermis and mesophyll) cells. A short period of penetration of the peripheral plant tissues (five cell punctures per individual) by aphids tethered and monitored by EPG decreases the time to first parturition of the winged summer form when subsequently placed on a Parafilm sachet containing 15% sucrose solution. This treatment also significantly increases the incidence of reproduction and individual reproductive output of gynoparae over a 24-h period. No detectable effects of tissue penetration on subsequent reproductive output are observed in the wingless summer form. Additionally, EPGs reveal that a number of aphids of all morphs display xylem ingestion, which occurs predominantly before initiation of phloem feeding but is not necessary to initiate parturition. It is concluded that aphids are likely to detect parturition cues during stylet punctures of cells within peripheral tissue layers, before reaching the phloem vessels.     

'Bistability' experiments and photoperiodic morph determination in the aphid Aphis fabae

Abstract. Newly born larvae (presumptive gynoparae) of the aphid Aphis fabae were exposed to 'symmetrical skeleton' photoperiods, consisting of two equal pulses of light per 24 h. The general form of the photoperiods tested was LDLD 1:10:1:12 h. This regime is open to two 'interpretations', LDLD 1:10:1:12 h (PP_s12) and LDLD 1:12:1:10 h (PP_s14). As both light pulses are close to 12 h apart, it is expected that the interpretations result in two distinct steady state phase relationships, i.e. this regime would show bistability. If this is true and both interpretations could be adopted, PP_s12 is expected to result in a low and PP_s14 in a high percentage of 'apterized' insects.
Experiments undertaken with the aphid showed that bistability did not occur either at 15C or 20C, and the results could be entirely explained on the basis of an 'instantly' damping circadian oscillator clock.     

The cost of ant attendance and melezitose secretion in the black bean aphid Aphis fabae

1. The aphid Aphis fabae (Scopoli) is facultatively tended by Lasius niger (Linnaeus) ants. Previously, we found that A. fabae colonies can be made up of several clones, and that clones display significant differences in the composition of their honeydew sugars, especially in the amount of the ant attractant sugar melezitose that they produce. 2. These clonal differences could greatly impact the strength of the mutualistic interaction with ants as well as the aphids' fitness. 3. Hence, the aim of this study was to compare the fitness of different A. fabae clones that differed in their melezitose secretion, and whether or not they were tended by ants. 4. Individual fitness indices, colony growth, and alate production of single‐clone aphid colonies were analysed. 5. The results demonstrate that the fitness consequences of ant attendance critically depend on an interaction between levels of melezitose production. In particular, we show that high‐melezitose secreting clones produce fewer alates and hence might have a lower dispersal ability in the presence of ants. 6. Furthermore, these data confirm previous evidence that ant attendance is costly and results in the production of fewer apterae.     

Levels of clonal mixing in the black bean aphid Aphis fabae, a facultative ant mutualist

Aphids are a worldwide pest and an important model in ecology and evolution. Little is known, however, about the genetic structure of their colonies at a microgeographic level. For example, it remains largely unknown whether most species form monoclonal or polyclonal colonies. Here, we present the first detailed study on levels of clonal mixing in a nonsocial facultative ant mutualist, the black bean aphid Aphis fabae. In contrast to the earlier suggestion that colonies of this species are generally monoclonal, we found that across two subspecies of the black bean aphid, A. fabae cirsiiacanthoidis and A. fabae fabae, 32% and 67% of the aphid colonies were in fact polyclonal, consisting of a mix of up to four different clones, which resulted in an overall average relatedness within colonies of 0.90 and 0.79 in the two subspecies. Data further show that the average relatedness in A. f. cirsiiacanthoidis remained relatively constant throughout the season, which means that clonal erosion due to clonal selection more or less balanced with the influx of new clones from elsewhere. Nevertheless, relatedness tended to decrease over the lifetime of a given colony, implying that clonal mixing primarily resulted from the joining of pre‐existing colonies as opposed to via simultaneous host colonisation by several foundresses. Widespread clonal mixing is argued to affect the ecology and evolution of the aphids in various important ways, for example with respect to the costs and benefits of group living, the evolution of dispersal and the interaction with predators as well as with the ant mutualists.     

Flight behaviour of the black bean aphid, Aphis fabae, and the cabbage aphid, Brevicoryne brassicae, in host and non-host plant odour

Abstract. Walking alate virginoparae of Brevicoryne brassicae (L.) and Aphis fabae Scopoli were presented with odours of steam-distilled extracts of the non-host plants summer savoury ( Satureja hortensis L.) and tansy ( Tanacetum vulgare L.) in an olfactometer. No effects of the extracts were observed on B. brassicae. However, A.fabae were repelled by summer savoury and tansy odour; both extracts also masked an attractant response to bean (host plant) odour. In a flight chamber, air permeated with odour from host or non-host plants was blown over flying alates of both species, with a green, plant-mimicking target presented once a minute. The incidence of targeted (host-responsive) flight of B.brassicae was not affected by odour from a growing host plant ( Brassica oleoracea ) or a non-host plant tansy. Host plant ( Vicia faba ) odour did not affect the initial rate of climb or the incidence of targeted flight of A.fabae , but when the bean odour was alternated with odour from non-host tansy plants a greater number of targeted flights occurred in the host plant odour. The volatile extracts of tansy and summer savoury were also presented to flying A.fabae. Aphids flying in air permeated with tansy odour at 450g plant equivalents initiated fewer targeted flights than when flying in clean air. However, no differences in flight behaviour were observed with summer savoury extract. In a horizontal wind tunnel the tansy extract at 90 g plant equivalents blown across the surface of yellow targets reduced the numbers of alate A.fabae landing. The results indicate that plant odours can affect flight and landing of aphids.     

Phenology of the black bean aphid,Aphis fabae,on organic crops and effect of parasitoid communities

1. Parasitoids represent the third trophic level in plant-insect food webs. They develop in or on herbivorous insects at the second trophic level, which in turn feed on plants that constitute the first trophic level. This food web system might be affected by agricultural landscape and practices.
2. We studied the phenology and population density of Aphis fabae (Hemiptera: Aphididae) and determined the impact of parasitoids in organic fields of beans and beet plants.
3. Twenty leaves per field were collected weekly. For each leaf, the total number of aphids, apterous and alate morphs, the number of mummies, and mortality of aphids were recorded.
4. Our results showed that the phenology of A. fabae varied throughout the season with maximal numbers observed at the beginning of summer. In addition, the production of alate morphs and the proportion of parasitism were positively correlated to an increase in aphid densities.
5. Six parasitoid species were recorded attacking A. fabae in the field, with Lysiphlebus fabarum and Binodoxys angelicae (Hymenoptera: Aphidiinae) being the most abundant parasitoids.
6. Field characteristics and availability of host plants in the surroundings affected A. fabae density. Lysiphlebus fabarum and B. angelicae appeared to be good biocontrol candidates against A. fabae.

     

Large interclone differences in melezitose secretion in the facultatively ant-tended black bean aphid Aphis fabae

Many aphids are known to engage in a trophic mutualism with ants, whereby the aphids secrete sugary-rich honeydew which is collected by the ants for food, and the ants, in exchange, protect the aphids against natural enemies. Previous results, however, suggest that the production of some of the honeydew sugars, such as the ant-attractant trisaccharide melezitose, may induce an indirect cost to the aphids. This led us to believe that large differences in the nature of the secreted honeydew might exist, due to some clones capitalizing more or less on their mutualistic interaction with ants, or due to some “cheater” clones foregoing the production of particular sugars, instead taking advantage of the ant-attracting effect of other non sugar-deficient clones, co-occurring on the same plant. Here we present data on clonal variation in the composition of honeydew of the black bean aphid Aphis fabae which confirm this prediction. In particular, our results show that there was large interclone variation in the amount of glucose, melezitose and total sugar produced. The variation in the production of melezitose, however, showed particularly large differences, with 54% (7 out of 13) of the clones screened being virtually deficient for the production of this sugar, irrespective of whether the aphid colonies were ant-tended or not. The consequences of this finding in the context of the evolution and maintenance of the ant–aphid mutualism, as well as the adaptive benefits of oligosaccharide synthesis in aphids and other insects are discussed.     

Juvenile Hormone Stimulation of Oocyte Development and Embryogenesis in the Parthenogenetic Ovaries of an Aphid,Aphis fabae

Summary

The parthenogenetic ovaries of the black bean aphid, Aphis fabae, contain developing embryos. When reared at 15°C in long days (LD 16:8) oocyte development begins within the ovaries of the largest embryos of a fourth instar mother 24–48 hr after her ecdysis from the third instar. Starvation, decapitation and precocene III treatment inhibit embryonic oocyte development; juvenile hormone treatment reverses this inhibition. A method for the in vitro culture of embryos is described and under these conditions juvenile hormone again stimulates oogenesis. Embryogénie growth in vivo, as measured by the increase in length of the oldest daughter embryos, is also stimulated by juvenile hormone treatment. The results are discussed in relation to other roles proposed for juvenile hormone in aphid development.     

The effect of certain antibiotics on reproduction of the black bean aphid, Aphis fabae Scop.

The antibiotic terramycin at 0.2% concentration was consistently effective in greatly reducing the populations of Aphis fabae on Vicia faba when sprayed on larvae on and off the plant. The insects were not killed, but their fertility was decreased by over 97% in the first generation, leading to total sterility in the second generation. At 0.01% concentration, terramycin was not effective and only moderately so at 0.1% Larval development was invariably delayed by 1 day and the weight and size of the resulting adults were significantly reduced. After the most effective treatments, the adults were very inactive in their feeding and excretion, and sometimes became completely sterile. Even when the aphids reproduced, they ceased to do so after 6–10 days in different terramycin treatments and frequently the larvae were born dead. The affected insects could not, apparently, regain their reproductive capacity even after their transfer to untreated plants. When the insects were sprayed on the plants, terramycin in water was as effective as with surfactants: but when the insects were sprayed off the plants an oxyethyl phenol derivative (NP 10) greatly increased the efficiency of terramycin: surfactants alone had no effect on the insects. The other four antibiotics, namely tetracycline, aureomycin, chloramphenicol and reverin were not effective at the 0.2% concentration when the plants alone were sprayed before introducing the apids. The addition of glycerin to the antibiotics and keeping plants in a high humidity for 24 hr. after the treatment also had no effect.     

Climate effects on life cycle variation and population genetic architecture of the black bean aphid, Aphis fabae

Aphid species may exhibit different reproductive modes ranging from cyclical to obligate parthenogenesis. The distribution of life cycle variation in aphids is generally determined by ecological forces, mainly climate, because only sexually produced diapausing eggs can survive harsh winters or periods of absence of suitable host plants. Aphids are thus interesting models to investigate intrinsic and environmental factors shaping the competition among sexual and asexual lineages. We conducted a Europe-wide sampling of black bean aphids, Aphis fabae, and combined population genetic analyses based on microsatellite data with an experimental determination of life cycle strategies. Aphids were collected from broad beans (Vicia faba) as well as some Chenopodiaceae, but we detected no genetic differentiation between aphids from different host plants. Consistent with model predictions, life cycle variation was related to climate, with aphids from areas with cold winters investing more in sexual reproduction than aphids from areas with mild winters. Accordingly, only populations from mild areas exhibited a clear genetic signature of clonal reproduction. These differences arise despite substantial gene flow over large distances, which was evident from a very low geographic population structure and a lack of isolation-by-distance among 18 sites across distances of more than 1000 km. There was virtually no genetic differentiation between aphids with different reproductive modes, suggesting that new asexual lineages are formed continuously. Indeed, a surprising number of A. fabae genotypes even from colder climates produced some parthenogenetic offspring under simulated winter conditions. From this we predict that a shift to predominantly asexual reproduction could take place rapidly under climate warming.     

Effect of black bean aphid, Aphis fabae, on transpiration, stomatal conductance and crude protein content of faba bean

This study was initiated to investigate effects of damage by 0, 5 and 10 aphids/plant on the physiology of faba bean plants throughout different feeding periods and at two plant development stages. Immediately following removal of Aphis fabae, measurements showed 84–229% increase in transpiration rate. These changes were proportional to the number of aphids and infestation duration. Injury by A. fabae caused the stomatal conductance to be much higher in the leaves of infested plants. Leaf stomatal conductance of the infested plants increased significantly by 51–224% depending on initial aphid densities and feeding intervals. This increase was proportional to the infestation level for each date. Length of infestation period and plant growth stage seemed to have no clear effect on stomatal apertures. Aphid feeding caused a damage of about 7–33% of crude protein levels in the leaf tissue. This reduction increased with increasing infestation levels and time, except for 28‐day‐old plants on 28 days. The physiological effects of aphid feeding on water vapour and chemical composition of damaged leaves are particularly serious when the population is high.     

Economics of forecasting for chemical control of the black bean aphid, Aphis fabae, on the field bean, Vicia faba

The economics of a forecasting scheme for predicting the need for chemical control of the black bean aphid, Aphis fabae, on spring-sown field beans, Vicia faba, are compared with alternative control strategies, namely no treatment, eradicant treatment and routine preventive treatment. Two criteria are assessed. First, the ‘risk’ of lost revenue from wrong control decisions and, secondly, the overall profitability of the strategy. A wrong decision is made when a profitable treatment is not applied or when an unprofitable one is applied. These constitute ‘risk’ for the grower. The forecasting scheme involves least risk of monetary loss and the most acceptable alternative strategy is the routine preventive treatment. Relative to the routine treatment, a gain averaging £3.78/ha of bean crop would have been made between the years 1970-5 by adopting control based on the forecasting scheme. There was considerable year-by-year and area-to-area variation in monetary benefits, with the largest gains in areas where economic damage occurred least frequently and where relatively large areas of beans are grown, as in East Anglia. Other benefits of using the forecasting scheme, e.g. correct timing of chemical application, are discussed but not evaluated.