Population dynamics of the bird cherry‐oat aphid,Rhopalosiphum padi (L.), during the autumn and winter: a modelling approach

1 A simulation model was developed to investigate the inter‐relationship of factors influencing the population dynamics of the bird cherry‐oat aphid (Rhopalosiphum padi (L.)) in barley crops during the autumn and winter. 2 The model incorporated algorithms describing alate immigration, development and survival of adults and nymphs, fecundity and morph determination in newly born nymphs. 3 The model was validated against pest outbreaks in barley fields in south‐east England. 4 It simulated accurately the size of the outbreaks with predictions of peak aphid populations within 20% of the observed in all but one case. Similarly, all but one of the year‐sowing date combination predictions of timing of peak abundance fell within 14 days of the observed. 5 A sensitivity analysis of the model highlighted the relative importance of various population processes in determining simulated aphid population dynamics; decreasing mortality rates of apterous nymphs by as little as 5% over the autumn and winter increased peak densities by as much as 60‐fold, whereas increasing daily temperatures by only 1 °C more than doubled peak aphid abundance. 6 The model identified our understanding of the mechanisms of aphid mortality as a limiting factor in the accurate prediction of R. padi outbreaks in the field.     

Population growth rate and relative virulence of the two South African biotypes of Russian wheat aphid,Diuraphis noxia,and bird cherry‐oat aphid,Rhopalosiphum padi,on resistant and non‐resistant barley

In South Africa a new biotype of the Russian wheat aphid (RWA), Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae), RWASA2, has appeared which exhibits an improved performance compared to the original biotype (RWASA1) on wheat containing the Dn1 resistance gene. We examined population growth rates as well as damage caused by RWASA1 and RWASA2, in addition to a different aphid species, the bird cherry‐oat aphid (BCA), Rhopalosiphum padi L. (Hemiptera: Aphididae), on three RWA‐resistant barley [Hordeum vulgare L. (Poaceae)] lines (STARS‐9577B, STARS‐0502B, and STARS‐9301B) and one susceptible control (PUMA). RWASA2 had a higher reproductive rate than RWASA1 on all barley lines tested, which is consistent with previous results on wheat. Two of the RWA‐resistant lines (STARS‐0502B and STARS‐9301B) also exhibited a similar resistance phenotype against BCA. In our experiments, severe chlorosis and leaf roll appeared earlier on the control PUMA barley variety as a result of RWASA2 feeding than was the case with RWASA1, probably due to the differences in reproductive rate. Although chlorosis appeared earlier on resistant plants after RWASA2 feeding, this symptom developed much faster during RWASA1 feeding on all three resistant lines tested. As chlorosis did not correlate well with aphid population numbers, we surmise that the differential chlorosis effects may be related to differences in the amount of saliva introduced by the two aphid clones during feeding. Our results indicate that the difference between RWASA2 and RWASA1 are broader than a ‘gene for gene’ interaction with the Dn1 resistance (R) gene in wheat, and that these biotypes also differ in important aspects of their biology.     

Flight behaviour of the bird cherry aphid, Rhopalosiphum padi

Abstract Seasonal winged forms of the bird cherry aphid, Rhopalosiphum padi L., were flown in an automated flight chamber. During their maiden flights, autumn migrants (gynoparae) had a greater initial rate of climb than summer (exules) and spring migrants (emigrants). Autumn migrants, presented with a laterally-positioned green-illuminated target for 2.5 s during each minute of flight, flew for a longer period before responding to the target (110 min) than summer migrants (36 min), while spring migrants responded after an intermediate time (72 min). This period is equivalent to the migratory phase of flight. The summer migrants were maximally responsive to targets illuminated by green monochromatic light (X, 555 nm). Targets illuminated with ultraviolet (γλ 360 nm) were attractive during the migratory and green-responsive phases of flight, but infrared (γλ700 nm) wavelengths were not attractive. The results are discussed with respect to aphid behaviour in the field.     

Triticum monococcum lines with distinct metabolic phenotypes and phloem‐based partial resistance to the bird cherry–oat aphid Rhopalosiphum padi

Crop protection is an integral part of establishing food security, by protecting the yield potential of crops. Cereal aphids cause yield losses by direct damage and transmission of viruses. Some wild relatives of wheat show resistance to aphids but the mechanisms remain unresolved. In order to elucidate the location of the partial resistance to the bird cherry–oat aphid, Rhopalosiphum padi, in diploid wheat lines of Triticum monococcum, we conducted aphid performance studies using developmental bioassays and electrical penetration graphs, as well as metabolic profiling of partially resistant and susceptible lines. This demonstrated that the partial resistance is related to a delayed effect on the reproduction and development of R. padi. The observed partial resistance is phloem based and is shown by an increase in number of probes before the first phloem ingestion, a higher number and duration of salivation events without subsequent phloem feeding and a shorter time spent phloem feeding on plants with reduced susceptibility. Clear metabolic phenotypes separate partially resistant and susceptible lines, with the former having lower levels of the majority of primary metabolites, including total carbohydrates. A number of compounds were identified as being at different levels in the susceptible and partially resistant lines, with asparagine, octopamine and glycine betaine elevated in less susceptible lines without aphid infestation. In addition, two of those, asparagine and octopamine, as well as threonine, glutamine, succinate, trehalose, glycerol, guanosine and choline increased in response to infestation, accumulating in plant tissue localised close to aphid feeding after 24 h. There was no clear evidence of systemic plant response to aphid infestation.     

Diapause termination and egg hatch in the bird cherry aphid, Rhopalosiphum padi

Conclusion TastePROBE is a convenient and flexible electronic circuit designed to record action potentials from taste sensilla of insects. It facilitates the recording of slow potentials arising in taste sensilla, improves the signal to noise ratio, and preserves spike shapes. This new amplifier design combines excellent signal to noise ratio with complete compatibility as regards existing electrophysiological equipment.DC recordings have higher information content than filtered recordings. With DC recordings, spike shapes are not modified and thus better sorting is possible. Moreover, slow variations in the transepithelial potential (i.e. less than 10 Hz) are preserved. Both aspects are of considerable importance when studying the physiology of taste receptors.     

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.     

Chemical aspects of host‐acceptance behaviour in the bird cherry‐oat aphid Rhopalosiphum padi: host‐acceptance signals used by different morphs with the same genotype

Host acceptance by gynoparae and winged virginoparae of the bird cherry‐oat aphid Rhopalosiphum padi (L.) is investigated utilizing leaves and aqueous extracts of the primary and secondary hosts, as well as nonhost plants. Gynoparae are specialized to reproduce on bird cherry Prunus padus L., whereas virginoparae reproduce and feed on various grasses. Host acceptance is assessed using levels of reproduction and survival for adults, as well as survival for nymphs. Little is known of host acceptance by nymphs. The data show that gynoparae and winged virginoparae produce nymphs almost exclusively on their host plants, bird cherry and barley leaves, respectively, over 72 h. When tested with aqueous plant extracts, however, gynoparae produce nymphs almost exclusively on bird cherry extract and progeny numbers are found to be similar to those on plant leaves. Few nymphs are produced on artificial diet. By contrast, winged virginoparae produce nymphs on aqueous extracts of barley, bird cherry and bean, as well as on artificial diet. The numbers of nymphs deposited by gynoparae are similar on aqueous extracts of bird cherry leaves collected at different times during the growing season. When extracts from leaves of various Prunus species are tested, only leaves of P. padus and Prunus virginiana stimulate parturition. Oviparae, the sexual female nymphs of gynoparae, survive well for 96 h on both bird cherry and barley leaves but not on bean seedlings, whereas nymphs of winged virginoparae survive well only on barley leaves. They do not survive for 96 h on any plant‐leaf extracts, although they do survive on artificial diet.     

Reproduction and probing behaviour of the bird cherry‐oat aphid Rhopalosiphum padi on detached leaves and leaves on intact seedlings of the winter host,bird cherry Prunus padus

Video recording and electrical penetration graph techniques are used simultaneously to investigate host acceptance (in terms of reproduction) and probing activities of autumn migrants (gynoparae) of the bird cherry‐oat aphid Rhopalosiphum padi (L.) on detached leaves and on leaves on intact plants of the winter host, bird cherry Prunus padus. There are no significant differences between the times taken to first parturition or the number of nymphs produced over a 6‐ or 18‐h period on intact plants or detached leaves. Stylet probing activities (i.e. total probe duration, xylem ingestion, the time to first phloem contact and phloem salivation) are also similar in the two situations.     

Effects of maternal diet on offspring fitness in the bird cherry‐oat aphid

1. Maternal and offspring diet effects on life‐history traits of the bird cherry‐oat aphid Rhopalosiphum padi were tested on three wheat varieties. Using nine reciprocal combinations of wheat varieties, the effects of previous experience (maternal diet effect) on the aphid's response to resistant and susceptible varieties (offspring diet effect) were tested. Batis was susceptible, and Xiaoyan22 and Ww2730 were both resistant, but with different mechanisms. 2. Aphids produced the most alatae in the treatments with the most resistant maternal diet variety Xiaoyan22. The fecundity (F) and intrinsic rate of increase (r_m) of these alatae were at their greatest in the most resistant offspring diet variety, but these traits were not influenced in the apterae. 3. There were significant interactions in the alatae production and apterae life‐history traits, such as r_m, development time, weight gain, and mean relative growth rate, between the maternal and offspring diet varieties. The interactions in apterae responses between varieties, some of which were reciprocal, indicated phenotypic plasticity in these parthenogenetic aphids. 4. Rhopalosiphum padi produced more alatae on the most resistant variety; the alatae would disperse and were more fecund. The growth responses of the apterae showed phenotypic plasticity to the different combinations of maternal and offspring diet varieties. The phenotypic plasticity would allow R. padi to better utilise the variable environments represented by the small wheat plots of different varieties in China.     

Inheritance of photoperiodic response in the bird cherry aphid, Rhopalosiphum padi

Abstract. The photoperiodic induction of presexual females (gynoparae) and males of the aphid Rhopalosiphum padi (L.) was examined in single clones collected from different latitudes (N clone from Blair Atholl, 56.5N 3.1W; C clone from Leeds, 53.5N 1.4W and S clone from Exeter, 50.4N 3.3W). Critical night lengths (CNLs) for gynopara and male production (CNLs: 50% of maximum production) and inter-clonal differences, defined by the different forms of progeny produced at a single discriminating night length (12 h 30 min), were measured at 16 ± 1C. The aphid clones differed in CNL and in the morphs produced at the discriminating night length. These differences were used to investigate the inheritance of the photoperiodic response. In crosses between clones the photoperiodic response showed considerable overall variation. The variation in CNLs indicated that the photoperiodic response was unlikely to affect the overwintering success after long-distance movement of clones from one latitude to another.     

Coinfection of the secondary symbionts,Hamiltonella defensa and Arsenophonus sp.contribute to the performance of the major aphid pest,Aphis gossypii(Hemiptera:Aphididae)

Bacterial endosymbionts play important roles in ecological traits of aphids.In this study,we characterize the bacterial endosymbionts of A.gossypii collected in Karaj,Iran and their role in the performance of the aphid.Our results indicated that beside Buchnera aphidicola,A.gossypii,also harbors both Hamiltonella defensa and Arsenophonus sp.Quantitative PCR(qPCR)results revealed that the populations of the endosymbionts increased throughout nymphal development up to adult emergence;thereafter,populations of Buchnera and Arsenophonus were diminished while the density of H.defensa constantly increased.Buchnera reduction caused prolonged development and no progeny production.Furthermore,secondary symbiont reduction led to reduction of the total life span and intrinsic rate of natural increase as well as appearance of the deformed dead offspring in comparison with the control insects.Reduction of the secondary symbionts did not affect parasitism rate of the aphid by the parasitic wasp Aphidius matricariae.Together these findings showed that H.defensa and Arsenophonus contributed to the fitness of A.gossypii by enhancing its performance,but not through parasitoid resistance.     

Ovariole number and fecundity for the two emigrating generations of the bird cherry-oat aphid (Rhopalosiphum padi) in Sweden

Abstract. 1. The number of ovarioles and the potential fecundity in first (fundatrigenia) and second generation emigrants of Rhopalosiphum padi (L.) was investigated.
2. The relationships between weight and host quality on ovariole number were investigated.
3. The first generation of emigrants had a greater number of ovarioles and a higher fecundity than the second.
4. There was a positive relationship between ovariole number and weight.
5. The number of ovarioles and weight decreased with decreasing host quality.
6. The results do not agree with a recently proposed reproductive strategy of aphids where the number of ovarioles are supposed to be independent of weight and host quality.
7. In years with a high initial population on bird cherry, the migration to grasses, e.g. cereals, will be earlier, probably larger and, to a greater extent, consists of aphids which have a higher reproductive rate than in years with a small initial number on bird cherry.     

Effects of two types of semiochemical on population development of the bird cherry oat aphid Rhopalosiphum padi in a barley crop

1 Field experiments were performed in barley using volatile semiochemicals affecting population density (density‐related substances – DRS) and spring migration (methyl salicylate) in bird cherry oat aphid Rhopalosiphum padi (L.). Natural infestations of aphids were used, and semiochemical dosages were chosen to be biologically relevant based on previous studies. A simple formulation method for active substances using wax pellets was developed. 2 The effect of treatments on aphid populations was analysed in terms of initial colonization of the crop, temporal dynamics of the population and maximum aphid incidence. 3 Treatments caused a significant delay in aphid establishment in the crop, and reduced the average infestation by 25–50% compared with the untreated control. At a moderate attack rate, the treatments with methyl salicylate and DRS gave a significant reduction in maximum aphid numbers. 4 The significant control effect of the treatment encourages further investigation both to increase understanding of the ecological role of the active substances, and to establish the limitations for their use in plant protection.     

Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi

We have identified and completely sequenced a novel plasmid isolated from the aphid Rhopalosiphum padi. Evidence which suggests that the plasmid occurs localized within the bacterial endosymbionts is presented. The plasmid contains the four genes that constitute the entire leucine operon. This fact makes it really unique since most plasmids are dispensable and lack genes that encode essential anabolic functions. Four more phloem-feeding aphid species also seem to contain homologous plasmids.Although further work is necessary, we hypothesize that this plasmid has appeared during the evolution of the symbiotic association between the aphid and the bacterial endosymbiont. The fact that this plasmid contains the entire leucine operon can be related to physiological evidence showing that the aphid host's diet of plant phloem is deficient in essential amino acids.     

The potential of hydroxamic acids in tetraploid and hexaploid wheat varieties as resistance factors against the bird‐cherry oat aphid,Rhopalosiphum padi

The potential for exploiting natural wheat resistance to control the cereal aphid Rhopalosiphum padi, the most important aphid pest of small grain cereals in the UK, was investigated as an alternative approach to the use of insecticides. The investigation focussed on a group of secondary metabolites, the hydroxamic acids or benzoxazinones, present naturally as glucosides, but which hydrolyse on tissue damage to give biologically active aglycones, e.g. 2,4‐dihydroxy‐7‐methoxy‐1,4‐benzoxazin‐3‐one (DIMBOA) which are associated with natural plant defence. These can be important for resistance against insects, fungi, bacteria and nematodes for a range of cultivated monocotyledonous plants and could ultimately be combined with other defence mechanisms to provide a general approach to cereal aphid control. Levels of hydroxamic acids, particularly DIMBOA‐glucoside, were determined in hexaploid (Triticum aestivum) and tetraploid (Triticum durum) wheat varieties and differences were found between species and varieties. The effect of feeding by R. padi on the level of hydroxamic acids in the leaf tissue was also investigated. Thus, after 24 h of aphid feeding, as an apparently localised hydrolytic defence reaction in the leaf, levels of DIMBOA‐glucoside decreased noticeably. When aphids were fed on sucrose solution containing low doses of DIMBOA there was a significant mortality compared to the sucrose control. However, the levels of and variation in hydroxamic acids in the wheat varieties investigated were insufficient for significant differences in aphid behaviour and development.     

Estimating costs of aphid resistance to parasitoids conferred by a protective strain of the bacterial endosymbiont Regiella insecticola

Heritable bacterial endosymbionts are common in aphids (Hemiptera: Aphididae), and they can influence ecologically important traits of their hosts. It is generally assumed that their persistence in a population is dependent on a balance between the costs and benefits they confer. A good example is Hamiltonella defensa Moran et al., a facultative symbiont that provides a benefit by strongly increasing aphid resistance to parasitoid wasps, but becomes costly to the host in the absence of parasitoids. Regiella insecticola Moran et al. is another common symbiont of aphids and generally does not influence resistance to parasitoids. In the green peach aphid, Myzus persicae (Sulzer), however, one strain (R5.15) was discovered that behaves like H. defensa in that it provides strong protection against parasitoid wasps. Here we compare R5.15‐infected and uninfected lines of three M. persicae clones to test whether this protective symbiont is costly as well, i.e., whether it has any negative effects on aphid life‐history traits. Furthermore, we transferred R5.15 to two other aphid species, the pea aphid, Acyrthosiphon pisum (Harris), and the black bean aphid, Aphis fabae Scopoli, where this strain is also protective against parasitoids and where we could compare its effects with those of additional, non‐protective strains of R. insecticola. Negative effects of R5.15 on host survival and lifetime reproduction were limited and frequently non‐significant, and these effects were comparable or in one case weaker than those of R. insecticola strains that are not protective against parasitoid wasps. Unless the benefit of protection is counteracted by detrimental effects on traits that were not considered in this study, R. insecticola strain R5.15 should have a high potential to spread in aphid populations.     

The evolutionary ecology of symbiont‐conferred resistance to parasitoids in aphids

Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal transmission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts have achieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont‐conferred resistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show that defensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of the host–parasitoid interaction, and by inducing environment‐dependent trade‐offs. These effects are conducive to very dynamic, symbiont‐mediated coevolution that is driven by frequency‐dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem by exploiting the parasitoids’ demonstrated ability to rapidly evolve counteradaptations to symbiont‐conferred resistance.