The influence of facultative endosymbionts on honeydew carbohydrate and amino acid composition of the black bean aphid Aphis fabae

The facultative endosymbionts Hamiltonella defensa and Regiella insecticola are commonly found in aphids. They are linked with various ecological benefits but generally occur at low prevalence, which indicates a possible harbouring cost. Little is known about how the presence of facultative endosymbionts is reflected in honeydew composition. Honeydew is the key mediator of the mutualism between aphids and their tending ants. The present study examines whether endosymbionts have an influence on aphid honeydew quality by comparing the amino acid and carbohydrate concentrations between infected and uninfected aphids. To this end, two genetic lines of the aphid Aphis fabae Scopoli are experimentally infected with different strains of Hamiltonella and Regiella. Infected aphids are shown to have reduced concentrations of amino acids in the honeydew compared with uninfected aphids. However, the presence of endosymbionts has no effect on the absolute amount of carbohydrates produced. Nevertheless, interclonal variation in honeydew composition between aphid genotypes is observed for both carbohydrate and amino acid production. These results imply that the nutritional value of honeydew depends on aphid genotype, as well as on the presence of secondary bacterial endosymbionts, which suggests that there is a physiological cost of harbouring endosymbionts and which could also impact aphid attractiveness to tending ants.     

寄主龄期对可疑柄瘤蚜茧蜂寄生及其后代适合度的影响

采用单选试验,观察了可疑柄瘤蚜茧蜂（Tysiphlebus anbiguus）对不同发育时期黑豆蚜的寄生选择及其后代生长发育适合度相关特征,以检验寄主大小与其质量是否存在正相关关系。结果表明,黑豆蚜（Aphis fabae）1～4龄和成蚜均被寄生,但对2龄若蚜的寄生率最高（35．25％）,对成蚜寄生率最低（14．75％）;寄生低龄蚜虫的羽化率显著高于高龄若蚜和成蚜。寄生2龄若蚜的发育历期（8．4d）最短,而寄生1龄若蚜最长（9．3d）;寄生2～4龄蚜虫的后代蜂体型显著大于寄生1龄和成蚜;寄生4龄若蚜的后代中,雌蜂比例（75．74％）显著高于1龄若蚜（62．89％）和成蚜（65．19％）,但与寄生2～3龄若蚜无显著差异。寄主黑豆蚜的质量从高至低依次为2龄〉3龄=4龄〉成蚜〉1龄,因此,对可疑柄瘤蚜茧蜂而言。寄主大小与其质量并非存在正相关性。     

The influence of black bean aphid, Aphis fabae Scop., and its honeydew on the photosynthesis of sugar beet

The effect of black bean aphids on the photosynthesis of sugar beet plants was studied under glasshouse and field conditions. The presence of up to several hundred aphids per leaf had no significant effect on CO₂ exchange rates over a range of light intensities between complete darkness and light saturation. Artificially prepared honeydew, sprayed onto leaves in the same amounts and composition as was found on severely aphid-infested plants, covered 30% of the stomata on the upper epidermis but did not significantly alter the rate of photosynthesis of these leaves in the light or the rate of respiration in the dark. The stomata on the lower epidermis were uncovered and functional. High pressure liquid chromatography of aphid-produced honeydew detected 20 different amino-acids. Three amino-acids, aspartic acid, glutamic acid and gluta-mine, made up the bulk of the amino-acid weight in the honeydew produced on young plants, up till the 8 leaf-stage. In the 10 to 12 leaf-stage, several different amino-acids occurred in substantial amounts. The amino-acids to sugars ratio of the honeydew produced by the aphids decreased strongly as the sugar beet plants aged: from 1:6 in plants with 3 or 4 leaves to 1:25 in plants having 10 to 12 leaves.     

The consequences of clustering by Aphis fabae foundresses on spring migrant production

Aphis fabae (Homoptera: Aphididae) foundresses were shown to have a clustered distribution on leaves of their primary host, Euonymus europaeus. Two field experiments were carried out to determine the costs or benefits of this clustering behaviour to aphid clones. The first experiment, in spring 1996, excluded predators from colonies formed by single fundatrices or clusters of three. No density-dependent effects on colony growth were observed early in the season, but the total production of migrants per foundress was significantly lower for clustered foundresses. This demonstrated that there was no synergistic effect of group feeding on clonal performance. All colonies were initiated on randomly selected leaves and all grew successfully, therefore clustering was not due to a shortage of feeding sites. The second experiment, in spring 1997, tested whether natural enemies cause selection for selfish herding by the foundress generation. Colonies were initiated by one or three foundresses, but half were left unbagged. If natural enemy attack is a selective force inducing clustering behaviour in foundresses, the costs of clustering should have been reduced or negated in unbagged colonies. Colonies grown from clusters produced significantly fewer migrants per foundress, irrespective of bagging treatment. Other potential factors causing clustering behaviour are discussed. Received: 19 August 1998 / Accepted: 16 November 1998     

棉花型和黄瓜型棉蚜对寄主植物的适合度

采用寄主转换建立生命表及触角电位 (EAG)方法比较了棉蚜两寄主专化型 (棉花型和黄瓜型 )对不同夏季作物的适合度。结果表明 ,棉花型蚜转到黄瓜上及黄瓜型蚜转接到棉花上均不能正常产仔繁殖和建立种群。两种蚜型均不能在茄子和苋菜上建立种群。黄瓜型蚜能在豇豆上建立种群 ,但棉花型蚜不能 ,表现出两种寄主型棉蚜对夏寄主利用上存在显著差异。受棉蚜为害 12～ 36 h后的黄瓜或棉花植株仍不适合于棉花型或黄瓜型蚜 ,表现出黄瓜型蚜不能在被棉花型蚜为害过的棉株上正常存活和繁殖 ,棉花型蚜也不能在被黄瓜型蚜为害过的黄瓜苗上存活和繁殖。两种寄主型蚜对不同寄主叶片丙酮提取物的触角电位表明 ,黄瓜型蚜对棉花、哈密瓜和马铃薯叶片提取物的反应显著强于棉花型蚜 ,而对黄瓜和甜瓜叶片提取物的反应上两种蚜型差异不显著。文中同时对棉花型和黄瓜型棉蚜产生的生态机制进行了讨论。     

The influence of black bean aphid, Aphis fabae Scop., and its honeydew on leaf growth and dry matter production of sugar beet

A. fabae populations, started at the 3–4 leaf-stage of sugar beet in the glasshouse and peaking at 3000 individuals per plant, reduced leaf area by 64% at the 14 leaf-stage. The size of the heavily-infested leaves number 5 to 10 was reduced by 80% or more. The rate of leaf growth regained normal values after the aphid populations collapsed, but the infested plants did not make up for the decrease in leaf area production that had been incurred during the infestation. Total dry matter production over a period of 15 weeks was reduced by 47%. Honeydew had no effect on leaf size or dry matter production. Sugar beet plants in the field became infested with A. fabae at the 2–3, 4–5 and 6–8 leaf stages. Maximum populations of 800, 2100 and 2200 aphids per plant were recorded, respectively. The pertinent reductions in leaf area were 91%, 67% and 34% at the 10–12 leaf-stage and 79%, 65% and 14% at harvest while the total dry matter produced was reduced by 91%, 79% and 16%. Neighbouring plants of the early-infested sugar beet plants gained significantly higher weights than control plants. Honeydew had no effect on leaf area or dry matter production. The consequences of these results for our understanding of Aphis fabae injury in sugar beet and aphid control in the field are discussed.     

Phenotypic plasticity in host-plant specialisation in Aphis fabae

Abstract.  1. The study of phenotypic plasticity in host utilisation is crucial for predicting evolutionary patterns of insect – plant interactions. The presence of sufficient variation in plasticity may facilitate host race formation and sympatric speciation.
2.  Aphis fabae genotypes showed high levels of phenotypic plasticity in the intrinsic rate of natural increase ( r _m), relative growth rate (RGR), birth weight (BW), adult weight (AW), fecundity ( F ), and development time (1/ d ).
3. Thirteen A. fabae genotypes reared both on broad bean and nasturtium exhibited statistically significant genotypic variability in phenotypic plasticity.
4. Some genotypes displayed fitness improvement on novel host plants.
5. Differences in genotypic correlation among fitness components between the two hosts and increased variance on nasturtium indicated different genomic expression on nasturtium.
6. The results indicated that phenotypic plasticity in a novel environment may be a major determinant of the evolutionary trajectory of a parasitic species and might support the idea that speciation starts with phenotypic plasticity.     

New polymorphic microsatellite loci,cross‐species amplification and PCR multiplexing in the black aphid,Aphis fabae Scopoli

Aphis fabae includes four morphological cryptic subspecies, which are mostly identified by their partially distinct secondary host range. To determine the extent of gene flow and isolation between these four taxa, we isolated and characterized 12 microsatellite loci from Aphis fabae fabae and tested cross‐species amplification of eight loci from the closely related species Aphis gossypii. Using eight previously described microsatellite loci, we have developed the polymerase chain reaction (PCR) multiplexing of 24 loci, which were separated in tree sets and five PCRs. These sets of microsatellite loci provide high throughput capacity for large‐scale population genetic studies at a minimum cost.     

可疑柄瘤蚜茧蜂对高温下不同龄期黑豆蚜的寄生及其适合度表现

研究寄生蜂对寄主不同龄期的寄生策略通常采用适温下（≈25℃）培养的寄主进行试验。 为探究蚜茧蜂对高温下生长的寄主蚜虫的寄生反应及其适合度表现,在30℃条件下饲养寄主孤雌胎生无翅黑豆蚜Aphis fabae Scopli,获得不同龄期若蚜和刚羽化的成蚜,分别提供给可疑柄瘤蚜茧蜂Lysiphlebus ambiguous Haliday寄生,观察蚜茧蜂的寄生率以及后代性比、体型大小和发育时间等适合度相关特性。结果表明： 可疑柄瘤蚜茧蜂对1至4龄若蚜及成蚜均寄生,但偏向寄生较早龄期的若蚜,对成蚜的寄生率为28.0％,显著低于对1龄（400％）和2龄（42.8%）寄主若蚜的寄生率。后代雌蜂比例和体型随寄主龄期（体型）增大而减小,而发育历期则呈现“中间低,两头高”的格局。后代性比、体型大小及发育历期等适合度表现与此前适温（≈25℃）下得到的结果截然相反。因此推测,寄主黑豆蚜体型或龄期可能不是或不全部是可疑柄瘤蚜茧蜂评价寄主质量的依据,其他与寄主蚜虫内共生菌动态相关的线索（如行为的,化学的等）可能才是其评价寄主质量的依据。     

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.     

棉花型和黄瓜型棉蚜(Aphis gossypii Glover)的寄主适应性及转移通道

采用寄主转接建立生命表的方法研究了棉花型和黄瓜型棉蚜对不同寄主植物的适应性,以及两寄主型棉蚜是否可通过中间桥梁寄主实现寄主互换的问题。结果表明,两寄主型棉蚜直接互换寄主后,其存活和繁殖力显著下降,表现为棉花型和黄瓜型棉蚜的净增殖率比在原寄主上分别下降980倍和12倍,平均世代寿命缩短5～12d。两寄主型棉蚜均能利用木槿植物,并且适应性没有显著差异。但是两寄主型棉蚜均不能在车前草和大叶黄杨上存活和繁殖后代。西葫芦作物对棉蚜在木槿、棉花和黄瓜寄主上的相互转移起到了重要的桥梁寄主作用。冬寄主木槿上棉蚜可通过甜瓜或西葫芦转移到黄瓜寄主上,棉花和黄瓜上棉蚜也可通西葫芦作物分别转移到黄瓜和棉花作物上,从而形成棉蚜在不同寄主植物间的相互转移通道,造成为害和病毒病的扩张。     

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.     

温度对黑豆蚜体内共生菌胞数量及宿主体型大小的影响

为了明确饲养温度对黑豆蚜Aphis fabae 内共生菌和宿主蚜虫体型大小的影响,对在室内不同温度下饲养的黑豆蚜内共生菌胞数量和宿主蚜虫体型大小进行了观察和统计分析。结果表明,温度对同一发育时期蚜虫内共生菌胞数量的影响在不同温度范围内有所不同,1龄若蚜体内的菌胞数量除在25℃与35℃间有显著差异外,在其余各温度间没有显著差异; 其余时期的蚜虫内共生菌胞数量在高温（> 30℃）下显著低于较低温度下的菌胞数量,存在负直线相关性。温度对菌胞数量随宿主发育到产仔前的变化趋势有不同程度的影响,在较低温度（15℃、20℃和25℃）下,菌胞数量随虫体发育显著增加; 但在高温（30℃和35℃）下,蚜虫体内菌胞数逐渐增加直到3龄达到最高,然后略有下降（30℃）或显著下降（35℃）。除1龄若蚜外,蚜虫体型大小总体呈现随温度升高而降低的格局,但随其内共生菌数量增多而增大（35℃下除外）。据此认为,温度可能通过作用于蚜虫内共生菌胞数量而影响蚜虫体型的大小。     

Amino acids as respiratory substrates in aphids: an analysis of Aphis fabae reared on plants and diets

Abstract. The fate of radioactively labelled amino acids injected into the haemolymph of the aphid Aphis fabae was investigated. Radioactivity from each of L-[U-¹⁴C]-glutamic acid, L-[U-¹⁴C]-serine and L-[U-¹⁴C]-threonine in the aphid tissues declined exponentially, at rates of 32, 9.3 and 1.0 pmol/aphid/min, respectively. For ¹⁴C-glutamic acid, radioactivity lost from the aphids was recovered quantitatively as carbon dioxide, and radioactivity in aphid saliva and honeydew was undetectable. When expressed on a per unit aphid biomass basis, the rate of respiratory loss of glutamic acid from aphids reared on chemically-defined diets was more than double that of aphids reared on the host plant, Vicia faba . It is concluded that respiration is a quantitatively important component to the aphid metabolism of glutamic acid and other amino acids.     

Partial application of insecticide to broad bean (Vicia fabae) as a means of controlling bean aphid (Aphis fabae) and bean weevil (Sitona lineatus)

The effects upon the nature of insect pest attack of treating only a certain proportion (0%, 25%, 50%, 75% and 100%) of the plants in a field bean (Vicia fabae) stand, with a systemic insecticide (aldicarb as Temik 10G, Rhone Poulenc Drugs Ltd; 10% a.i.) were assessed. Numbers of both the black bean aphid (Aphis fabae) and the bean weevil (Sitona lineatus) were proportionally reduced on untreated plants in plots with an increasing proportion of insecticide treated plants. A similar response was also observed with bean weevil leaf damage scores.
It is postulated that the observed effects are due to a reduction in insect numbers per plot brought about by redistribution of insects after initial invasion. Insects initially alighting on untreated plants later migrate to treated plants and either die or leave the plot altogether. This resulted in proportionally fewer insects on the untreated plants than would be expected.     

Probing behaviour of Aphis craccivora Koch on host plants of different nutritional quality

Abstract 1. Reciprocal transfer experiments were undertaken using four different hosts to examine the effects of a change in host at adult moult on the probing behaviour of the cowpea aphid Aphis craccivora Koch.
2. The highest intrinsic rate of increase r _m was achieved by aphids born and reared on cowpea, followed by those born and reared on broad bean, then Larissa, and finally Huia.
3. Mean probing time, time to first probe, number of probes per time allocation, and non-probing time were all examined. Host quality r _m did not affect the instantaneous probability of probing, and aphids that did not find a probing site within 200 s did not settle and did not probe further on that leaf/stem.     

Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae

This study investigated the relationship between the essential amino acid requirement of the aphid Aphis fabae Scop. and the phloem sap amino acid composition of its host plants. The dietary amino acid requirement of A. fabae varied between clones. One or more of the eight clones of A. fabae tested displayed depressed larval survival, larval growth rate, or r_m on diets lacking histidine, methionine, threonine, and valine, but none of the other five essential amino acids. The required amino acids corresponded closely to the essential amino acids that varied in relative concentrations among 16 plant species tested: histidine, threonine, tryptophan, and valine. It is suggested that the interclonal variation in the dietary requirements of an aphid species may contribute to the intraspecific variation in plant utilisation patterns. The phloem sap amino acid composition and sucrose : amino acid ratio did not differ consistently between host plant species of A. fabae and non‐host species, indicating that phloem amino acid composition is not an important factor in determining the host plant range of this aphid species.     

Aphid–ant mutualism: how honeydew sugars influence the behaviour of ant scouts

Honeydew is the keystone on which ant–aphid mutualism is built. The present study investigates how each sugar identified in Aphis fabae Scopoli honeydew acts upon the feeding and the laying of a recruitment trail by scouts of the aphid‐tending ant Lasius niger Linnaeus, and thus may enhance collective exploitation by the ant mutualists. The feeding preferences shown by L. niger for honeydew sugars are: melezitose = sucrose = raffinose > glucose = fructose > maltose = trehalose = melibiose = xylose. Although feeding is a prerequisite to the launching of trail recruitment, the reverse is not necessarily true: not all ingested sugar solutions elicit a trail‐laying behaviour among fed scouts. Trail mark laying is only triggered by raffinose, sucrose or melezitose, with the latter sugar being specific to honeydew. By comparing gustatory and recruitment responses of ant foragers to sugar food sources, the present study clarifies the role of honeydew composition both as a source of energy and as a mediator in ant–aphid interactions. Lasius niger feeding preferences can be related to the physiological suitability of each sugar (i.e. their detection by gustatory receptors as well as their ability to be digested and converted into energy). Regarding recruitment, the aphid‐synthesized oligosaccharide (melezitose) could be used by ant scouts as a cue indicative of a long‐lasting productive resource that is worthy of collective exploitation and defence against competitors or aphid predators.     

寄主植物对瓜蚜酯酶活性及其耐药性的影响

寄主植物对瓜蚜无翅胎生雌蚜体重、体色、体内酯酶活性均有明显影响。取食笋瓜、南瓜、瓠子、黄瓜和冬瓜的瓜蚜,体重依次增加,体色渐深,而体内羧酸酯酶活性依次渐低。取食不同奇主植物的瓜蚜对杀虫剂的耐药性与其体内酯酶活性呈正相关。瓜蚜体内羧酸酯酶活性（X）与乐果对瓜蚜的LC50（Y）附会Y=8．3827X－67．8530（r=0．952）,与功夫菊酯对瓜蚜的LC50（Y）附合Y=1．040X－28．89（r=0．985）的线性关系。     

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.