Effect of wheat resistance, the parasitoid Aphidius rhopalosiphi, and the entomopathogenic fungus Pandora neoaphidis, on population dynamics of the cereal aphid Sitobion avenae

The influence of wheat (Triticum aestivumL.) resistance, the parasitoid Aphidius rhopalosiphiDe Stephani-Perez (Hymenoptera: Braconidae) and the entomopathogenic fungus Pandora neoaphidis(Remaudière et Hennebert) Humber (Zygomycetes: Entomophthorales) on the density and population growth rate of the cereal aphid Sitobion avenae(F.) (Hemiptera: Aphididae) was studied under laboratory conditions. Partial wheat resistance was based on hydroxamic acids, a family of secondary metabolites characteristic of several cultivated cereals. The partial resistance of wheat cultivar Naofén, the action of the parasitoid and the joint action of the parasitoid and fungus, reduced aphid density. The lowest aphid densities were obtained with the combination of the parasitoid and the fungus, but wheat resistance under these circumstances did not improve aphid control. Significant reductions of population growth rate (PGR) of aphids were obtained with the joint action of wheat resistance and natural enemies. In particular, the combined effects of parasitoids and fungi showed significantly lower PGR than the control without natural enemies in both wheat cultivars. Our results support the hypothesis that wheat resistance and the utilization of biological control agents could be complementary strategies in an integrated pest management program against cereal aphids.     

Analysis of wheat resistance to the cereal aphidSitobion avenae using electrical penetration graphs and flow charts combined with correspondence analysis

The behaviour ofSitobion avenae (F.), was compared on resistant wheat lines ofTriticum monococcum (L.) and a susceptible variety ofTriticum aestivum (L.). Firstly, stylet penetration activities were monitored with the Electrical Penetration Graph (EPG) technique and subsequently analysed using flow charts combined with correspondence analysis. Plant resistance was shown to be associated with repeated penetrations without access to either the xylem or the phloem, and with numerous failures in starting a sustained sap ingestion (as represented by pattern E2). Access to sieve elements of the phloem did not seem to be much affected on resistant plants but it took the aphid three times as long to produce a sap ingestion pattern when maintained on the resistant lineT. monococcum n^o 44 (Tm44) as compared with aphids maintained on susceptible plants. As a result the total time spent in ingesting from sieve elements was reduced by 72% on Tm44. Secondly, direct observations of freely-moving apterous adults were performed. Aphids did not discriminate between resistant and susceptible wheat during the first 30 min of access to test leaves, but only 4 out of 25 aphids were still probing after eight hours on resistant Tm44. The relevance of these results to possible location of the resistance factor(s) are discussed. Although detection of plant resistance before sieve elements are reached can not be rigorously excluded, the factors involved inT. monococcum resistance toS. avenae undoubtedly occur within the phloem vessels.     

Aphelinus albipodus(Hymenoptera: Aphelinidae) andDiaeretiella rapae(Hymenoptera: Braconidae) Parasitism onDiuraphis noxia(Homoptera: Aphididae) Infesting Barley Plants Differing in Plant Resistance to Aphids

Russian wheat aphid,Diuraphis noxia(Mordvilko), as a pest of small grains, has prompted research into biological control and host plant resistance. In the presence of Russian wheat aphid, leaves of a susceptible barley (Morex) are curled and chlorotic and sustain large densities of this aphid, while leaves of a resistant barley (STARS-9301B) remain flat and green and sustain fewer aphids. Might parasitism of Russian wheat aphid byAphelinus albipodusHayat & Fatima andDiaeretiella rapaeMcIntosh be affected differently by these plant types? When presented the plants separately and based on parasitism rate relative to aphid density, the largerD. rapaewas more effective in parasitizing relatively high densities of aphids within curled leaves of Morex than relatively low densities of aphids on uncurled leaves of STARS-9301B. Parasitism byA. albipodusdid not significantly differ among the plants. When given a choice of plants, approximately equal rates of parasitism occurred on the two plant lines for both parasitoid species, and parasitism byD. rapaewas greater thanA. albipodus.These data indicate that using parasitoid size as an indicator of success in a physically restricted environment may be misleading, when considered in a plant environment responsive in several manners to aphids (chlorosis, curling, and ability to sustain Russian wheat aphid). We expect that use of resistant barley will result in decreased parasitoid abundance as aphid densities decrease. However, parasitism rates are expected to be approximately equal on resistant and susceptible barley. In this system, plant resistance and biocontrol are compatible management strategies.     

The role of sinigrin in host plant recognition by aphids during initial plant penetration

Plant penetration behaviour (probing) of the cabbage aphid, Brevicoryne brassicae, and the pea aphid, Acyrthosiphon pisum, was studied on excised leaves of broad beans, Vicia faba, kept in water or in a 1% aqueous solution of sinigrin. Using the DC EPG (Electrical Penetration Graph) technique it was shown that the cabbage aphid on sinigrin-untreated bean leaves showed numerous short probes into epidermis and mesophyll. None of these aphids showed either phloem salivation or ingestion waveforms on untreated leaves. In contrast, on sinigrin-treated bean leaves, 35% of the probing time was spent on phloem sap ingestion (E2) and almost all aphids reached phloem vessels and started feeding. The duration of phloem salivation before phloem ingestion and the mean duration of phloem ingestion periods were similar on a host and a sinigrin-treated non-host plant. However, the total probing time by B. brassicae was 10% longer, the total phloem sap ingestion time was twice as long, and the time to the first phloem phase within a probe was three times shorter on the host plant compared to sinigrin-treated broad beans. Acyrthosiphon pisum also responded to the addition of sinigrin to broad beans, but in this case sinigrin acted as a deterrent. On sinigrin-treated leaves, A. pisum terminated probes before ingestion from phloem vessels, and none of these aphids showed phloem salivation and ingestion on treated leaves. Glucosinolates were detected in the mesophyll cells of the brassicaceous plant, Sinapis alba. Based on this finding and in addition to the foregoing EPG analysis of aphid probing on these plants and broad beans, our hypothesis is that aphids may recognise their host plants as soon as they probe the mesophyll tissue and before they start ingestion from phloem vessels.     

Tolerance of antibiotic and susceptible cereal seedlings to the aphids Metopolophium dirhodum and Rhopalosiphum padi

Some cereal seedlings exhibit antibiotic and antixenotic resistance to the aphids Metopolophium dirhodum (Walker) and Rhopalosiphum padi (L.), because the seedlings contain hydroxamic acids or gramine. The association between tolerance to aphids and aphid antibiosis was investigated for three cereals, Dollarbird wheat Vulcan wheat and Yagan barley. The dry biomass gained by the aphids and the simultaneous reduction in the biomass of the plants (biomass conversion ratio) quantified tolerance. Biomass production and the density dependence of biomass production by the aphids quantified antibiosis more effectively than fecundity. Vulcan wheat, which has more hydroxamic acid than Dollarbird wheat showed the highest level of antibiosis, and the barley was not antibiotic for either aphid. The biomass conversion ratio was a constant; the biomass of an infested plant was reduced by 3 mg for each mg of aphid biomass gained, regardless of aphid species, plant cultivar, or aphid density. The three plants showed no differential tolerance to the aphids, and therefore tolerance is not associated with antibiosis in this case.     

小麦体内生化物质在抗蚜中的作用

综述了小麦体内生化物质的抗蚜作用 ,主要包括不同抗性品种对麦蚜的影响、小麦体内氨基酸、糖类、酚类物质、生物碱和非蛋白氨基酸等与抗蚜性的关系 ,以及蚜虫对小麦体内抗虫生化物质的诱导作用 ,并提出了深入研究小麦生化物质与抗蚜性关系的前景和意义。     

Interactions of Russian wheat aphid, a hymenopterous parasitoid and resistant and susceptible slender wheatgrasses

Interactions among three trophic levels of resistant and susceptible slenderwheat grasses, Elymus trachycaulum (Link) Goule ex Shinners ex. H.F. Lewis, Russian wheat aphid, Diuraphis noxia (Mordvilko), and a hymenopterous parasitoid were studied in the laboratory and greenhouse. These relationships were compared with a commercial susceptible wheat Triticum aestivum L. variety. Aphids reared on the resistant entries showed significantly lower weights and numbers. Significant reduction of parasitoid mummy weight and adult size was positively correlated with the effects on the aphids. Resistant entries also induced a longer prereproductive period for both the aphids and parasitoids. Numbers of aphids and aphid damage were significantly modified by the addition of parasitoids. Parasitism was higher on plants that did not have leaf rolling. These findings may indicate that antibiosis resistance studied here is not the most desirable because it decreases natural enemy vitality.     

The efficiency of a new lightweight suction sampler for sampling aphids and their predators in arable land

A petrol driven machine, normally used to collect leaf litter, was modified to be used as a suction sampler for polyphagous predators in cereals and grassy habitats and aphids in cereals. Recovery efficiency of Araneae, Carabidae and Staphylinidae did not differ significantly between winter sampling from Agrostis stolonifera, Dactylis glomerata, Festuca rubra, Holcus lanatus or Lolium perenne although the structure of these grasses was very different. Summer sampling of aphids and their predators in winter wheat showed that the new sampler captured significantly more target organisms per unit area than did a traditional suction sampler. The machine was also lighter, cheaper and much easier to use than a traditional machine.     

主要抗蚜小麦品种(系)的抗性类型及其生化抗性机制

通过对10个抗麦蚜品种(系)室内苗期生命参数、抗性类型和抗蚜次生物质的研究,明确了不同抗性级别的品种对麦蚜种群控制力及部分生化抗蚜机制。实验结果表明,参试的抗蚜品种(系)中30%左右为不选择性：表现为爬行频繁,定殖率低,但是定殖个体生长发育良好;70%为抗生性;表现为使麦长管蚜Sitobion avenae(F.)和禾谷缢管蚜只Rhopalosiphum padi(L.)的发育历期分别延长2.1%～28.2%和3.7%～13.9%,若蚜死亡率增加1.0～3.6倍和1.0～2.25倍,平均寿命缩短10.2%～96.5%和37.5～97,1%,繁殖力下降3.4%～72.8%和25%～97.2%。苗期生化测定结果表明：不同抗源的单宁和总酚含量明显高于感蚜品种,其总酚含量与抗麦长管蚜级别呈显著负相关,以抗生性为主的品种其总酚含量亦与麦长管蚜的内禀增长力(r_m)呈显著负相关(P<0.05),表明总酚是小麦抗长管蚜的关键因子之一,而与禾谷缢管蚜抗性水平无关;单宁含量与麦蚜抗性关系不密切。     

The Influence of Previous Experience and Starvation on Aphid Feeding Behavior

It was hypothesized that (1) previous experience of aphids on a host plant leads to differences in their feeding behavior relative to aphids without previous experience on it and that (2) a change in the physiological state of the aphid modifies their experience-induced behavior. Using electronic recording, the feeding behavior of the aphid Sitobion fragariae (Walker) on wheat Triticum aestivum L. and oat Avena sativa L. was examined, comparing aphids with or without previous experience on a given host and with or without a period of starvation before assessing probing behavior. All comparisons were performed within a single aphid clone to minimize the effect of genetic variation. Feeding behavior on wheat was significantly affected by previous experience and starvation. The effect of previous experience interacted with the host plant where feeding behavior was tested. Aphids feeding on wheat following previous experience on wheat showed a longer time and a higher number of pathway activities and less time in waveform F (i.e., mechanical stylet work and penetration difficulties) than did aphids feeding on wheat after a previous experience on oat. No differences in the time from the beginning of the recording until the first salivation into the sieve elements were found. When aphids were subjected to a period of starvation, the time devoted to xylem ingestion increased compared with that of nonconstrained aphids. These results are discussed in terms of factors affecting foraging decisions.     

Jasmonate- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid,Sitobion avenae

Jasmonate and salicylatemediated signaling pathways play significant roles in induced plant defenses, but there is no sufficient evidence for their roles in monocots against aphids. We exogenously applied methyl jasmonate （MeJA） and salicylic acid （SA） on wheat seedlings and examined biochemical responses in wheat and effects on the grain aphid, Sitobion avenae （Fab.）. Application of MeJA significantly increased levels of wheat＇s polyphenol oxidase, peroxidase and proteinase inhibitor 1, 2 and 6 days after treatment. In twochoice tests, adult aphids preferred control wheat leaves to MeJA or SA treated leaves. Electrical penetration graph （EPG） recordings of aphid probing behavior revealed that on MeJAtreated plants, the duration of aphid＇s first probe was significantly shorter and number of probes was significantly higher than those on control plants. Also total duration of probing on MeJAtreated plants was significantly shorter than on control plants. Total duration of salivation period on SAtreated plants was significantly longer, while mean phloem ingestion period was significantly shorter than on control plants. However, no significant difference in total duration of phloem sap ingestion period was observed among treatments. The EPG data suggest that MeJAdependent resistance factors might be due to feeding deterrents in mesophyll, whereas the SAmediated resistance may be phloembased. We did not observe any significant difference of MeJA and SA application on aphid development, daily fecundity, intrinsic growth rate and population growth. The results indicate that both MeJA and SAinduced defenses in wheat deterred S. avenae colonization processes and feeding behavior, but had no significant effects on its performance.     

Allele-specific amplification of polymorphic sites for the detection of powdery mildew resistance loci in cereals

Primers for the polymerase chain reaction (PCR) were tailored to selectively amplify RFLP marker alleles associated with resistance and susceptibility for powdery mildew in cereals. The differentiation between marker alleles for susceptible and resistant genotypes is based on the discrimination of a single nucleotide by using allele-specific oligonucleotides as PCR primers. The PCR assays developed are diagnostic for RFLP alleles at the loci MWG097 in the barley genome and Whs350 in the wheat genome. The first marker locus is closely linked to MlLa resistance in barley, while the latter is linked to Pm2 resistance locus in wheat. PCR analysis of 31 barley and 30 wheat cultivars, with some exceptions, verified the presence or absence of the resistance loci investigated. These rapid PCR-based approaches are proposed as an efficient alternative to conventional procedures for selecting powdery mildew-resistant genotypes in breeding programs.     

Possible roles of esterase, glutathione S-transferase, and superoxide dismutase activities in understanding aphid–cereal interactions

Activities of the detoxification enzymes esterase, glutathione S‐transferase, and of superoxide dismutase in aphids and aphid‐infested cereal leaves were assayed using polyacrylamide gel electrophoresis and a spectrophotometer to elucidate the enzymatic mechanisms of aphid resistance in cereal plants. A chlorosis‐eliciting Russian wheat aphid, Diuraphis noxia (Mordvilko), and non‐chlorosis‐eliciting bird cherry‐oat aphid, Rhopalosiphum padi (L.), and four cereals were used in this study. The four cereal genotypes were ‘Arapahoe’ (susceptible) and ‘Halt’ (resistant) wheat (Triticum aestivum L.), ‘Morex’ (susceptible) barley (Hordeum vulgare L.), and ‘Border’ (resistant) oat (Avena sativa L.). Esterase isozymes differed between the two aphid species, although glutathione S‐transferase and superoxide dismutase did not. Esterase, glutathione S‐transferase, and superoxide dismutase activities in either aphid species were not affected by the level of resistance of a cereal to D. noxia. The assays of cereal leaf samples showed that D. noxia feeding elicited an increase in esterase activity in all four cereal genotypes, although R. padi feeding did not. The increase of esterase activity in cereals, however, was not correlated to aphid resistance in the cereals. The time‐series assays of aphid‐infested cereal leaves showed that D. noxia‐infested Morex barley had a significant increase in esterase activity on all sampling dates (3, 6, and 9 days) in comparison with either uninfested or R. padi‐infested barley. No difference in glutathione S‐transferase activity was detected among either aphid infestations or sampling dates. The electrophoretic assays, however, revealed that aphid feeding elicited a significant increase in superoxide dismutase activity, which served as the control of glutathione S‐transferase activity assays. The increase in esterase and superoxide dismutase activities suggested that D. noxia feeding imposes not only toxic, but also oxidative stresses on the cereals. The ramification of using these enzyme activity data to understand the etiology of D. noxia‐elicited chlorosis is discussed.     

Influence of wheat and oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi and the generalist aphid parasitoid Ephedrus plagiator

The effects of three wheat cultivars and two oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi De Steph. and the generalist aphid parasitoid Ephedrus plagiator (Nees) (Hymenoptera: Braconidae) were evaluated in the laboratory. The level of hydroxamic acids, a family of secondary metabolites that can affect the mean relative growth rate of cereal aphids in cereals, were measured in the different cultivars. The parasitoids were reared in Sitobion avenae (F.) (Homoptera: Aphididae), using plants grown under greenhouse conditions. A. rhopalosiphi showed a longer developmental time on wheat relative to oat cultivars. This effect was accounted for by a significant increase in the time from oviposition to pupation (mummy formation), while the duration of the pupal stage remained constant between treatments. No further effects were observed in other variables evaluating A. rhopalosiphi performance, such as adult longevity, adult body weight and secondary sex ratio. The generalist E. plagiator did not show significant differences in any of the variables analysed, both between cultivars and cereal species. Hydroxamic acids levels correlated negatively with mean relative growth rates of S. avenae, but positively with the observed developmental time of A. rhopalosiphi. The results are discussed in terms of tritrophic effects and the development of breeding programmes trying to improve plant resistance to aphids.     

Variation in the primary structure ofwaxy proteins (granule-bound starch synthase) in diploid cereals

The molecular weights ofwaxy proteins, by SDS-PAGE, and the N-terminal amino acid sequences of mature protein and of V8 protease-induced fragments were determined in diploid cereals. The homology of the primary structure was relatively high among cereals examined here, and there appeared to be a common sequence, V-F-V-G-A-E-M-A, in the vicinity of the N terminus. Based on the amino acid sequences, these cereals could be divided into two groups, including corn and rice in one and diploid wheat, fourAegilops species, rye, and barley in the other. In diploid wheat andAegilops species there were substitutions of amino acids in the primary structure. Variations of this sort suggest that the primary structure ofwaxy proteins would provide clues to the phylogenetic relations in the wheat group.     

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.     

Electrical Penetration Graph analysis reveals population differentiation of host-plant probing behaviors within the aphid species Uroleucon ambrosiae

Uroleucon ambrosiae collected from the eastern and the southwestern United States were studied in relation to host-plant probing. In the field, eastern aphids are highly specific on Ambrosia trifida, while southwestern aphids feed on Ambrosia trifida plus many other species in the family Asteraceae. Electrical penetration graphs of insects on the principal host, A. trifida, and an additional host of southwestern populations, Heterotheca subaxillaris, revealed regional differentiation in host-associated aphid behaviors, specifically in the first phase of subcuticular probing, and in phloem finding activities. Eastern aphids used A. trifidamore efficiently than southwestern aphids, but were demonstrably less vigorous in their probing activities on H. subaxillaris.     

Hydroxamic acids affecting barley yellow dwarf virus transmission by the aphid Rhopalosiphum padi

2,4-Dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), a hydroxamic acid (Hx) occurring in wheat, was shown to deter feeding by the aphid Rhopalosiphum padi (L.), and to reduce BYDV transmission to the plant. Dual choice tests with wheat leaves showed the preferential settlement of aphids on leaves with lower levels of DIMBOA. Electric monitoring of aphid feeding behaviour showed that in seedlings with higher DIMBOA levels fewer aphids reached the phloem and they needed longer times to contact a phloem vessel than in those with lower levels. When aphids carrying BYDV were allowed to feed on wheat cultivars with different DIMBOA levels, fewer plants were infected with BYDV in the higher DIMBOA cultivars than in the lower ones. Preliminary field experiments showed a tendency for wheat cultivars with higher Hx levels to be more tolerant to infection by BYDV than lower Hx level ones.     

Farm‐scale assessment of movement patterns and colonization dynamics of the grain aphid in arable crops and hedgerows

1 Integrated management of crop pests requires the identification of the appropriate spatial scale at which colonization processes occurs. We assessed, by coupling demographic and genetic methods, the relative contribution of local and transient migrants of the grain aphid Sitobion avenae to wheat field colonization in spring. 2 We examined, during two consecutive years, the daily colonization of wheat by aphid migrants and compared this with daily aphid flight monitored by a local 12.2‐m suction trap. The genetic profiles of aphids landing on crops were compared with those of both flying aphids caught by the suction trap and local populations from arable crops and hedgerows. 3 In the first year, we observed: (i) a strong correlation between aphids colonizing the crop and those moving within the crop and a close genetic similarity between aphids from these samples and (ii) a high level of genetic differentiation between these aphids and populations from local cereals and field margins. In the second year, the number of migrants recorded on the wheat was three‐fold higher than in the previous year, and less correlated with that recorded by the suction trap. This was associated with a lack of genetic differentiation between all samples. 4 This variation in the colonization processes resulted mainly in an abrupt increase in abundance of genotypes from local over‐wintering sites in 2004. This suggests that, despite the long range dispersal potential of the grain aphid, outbreak risks could be mainly determined at a local scale, encouraging the design of relatively small management units.     

An investigation of the differential performance of clones of the aphid Sitobion avenae on two host species

Individuals of the grain aphid Sitobion avenae were collected from wheat and cocksfoot stands around Hampshire, UK, during March and April 1994. Eight wheat and eight cocksfoot aphid clones were chosen on the basis of readily distinguishable RAPD-PCR fingerprint profiles. The performances (weight, fecundity and survival) of successive generations of each of these clones were then carefully monitored in the laboratory as new generations of aphids were transferred either to winter wheat or to cocksfoot in planned sequences. Even those clones that were originally caught on the same host showed significant variability in performance. Clones generally performed better on their host of origin than they did on the alternate host, and they performed less well on the alternate host compared to the clones that had originated there. A comparison of the performance of third generation aphids with first generation aphids showed that the experience of the mother in the second generation often influences the subsequent performance of their offspring. As the sequence of host transfers had more effect on the performance of wheat clones than cocksfoot clones, it is likely that wheat clones are more specialised, such that wheat is a satisfactory host for cocksfoot clones but not vice versa. The study provides evidence of genetic variation in performance on host and evidence for clonal adaptation to particular host species. This adaptation may well be a major cause of the observed consistent genetic differentiability of populations of S. avenae found on wheat and roadside grasses in early spring in southern England.