Transmission of barley yellow dwarf virus by field collected aphids (Homoptera: Aphididae) and their relative importance in barley yellow dwarf epidemiology in southwestern Idaho

Populations of cereal aphids were sampled from 1985–1988 and assayed for transmission of barley yellow dwarf virus (BYDV), Rhopalosiphum padi, Rho-palosiphum maidis, Sitobion avenae, Metopolophium dirhodum, Schizaphis graminum and Macrosiphum euphorbiae collected from host plants transmitted BYDV in bioassays. Of the 1028 Diuraphis noxia collected from plants, one may have transmitted BYDV. The isolate involved resembled SGV in serological and biological characteristics, but since it was not recoverable by any of more than 800 D. noxia subsequently tested, we suspect it may have been a contaminant. Among those aphids collected during the autumn from a suction trap adapted for live collection, R. padi transmitted BYDV most frequently. Other trapped species which transmitted BYDV included: R. maidis, Rhopalosiphum insertum, Macrosiphum euphorbiae, Metopolophium dirhodum and Ceruraphis eriophori. An adapted Infectivity Index indicated that R. padi is by far the most important vector of BYDV during the autumn sowing season in southwestern Idaho. Male R. padi consistently transmitted BYDV more frequently than did females collected during the same period.     

Barley yellow dwarf virus infectivity of alate aphid vectors in west Wales

Live trapping at 0.9 m of alate aphid vectors of barley yellow dwarf virus (BYDV) at Aberystwyth from 1970 to 1979 showed that ten species transmitted the virus to oat test plants. Conversion of percentage infective at 0.9 m to numbers infective based on continuous trapping at 1.2 m showed Rhopalosiphum padi and R. insertum to be the main vector species in most years, whilst Metopolophium dirhodum and Sitobion auenae were normally of minor importance. The data obtained suggest that epiphytotics of BYDV in autumn-sown cereals were caused by numerous infective vectors flying late in the year and transmitting severe strains of the virus. Evidence is presented that gynoparae and males of R. padi are involved in the autumn spread of BYDV and that three further aphid species, Anoecia corni, Metopolophium albidum and M. frisicum are BYDV vectors. The use of live and continuous trapping techniques in forecasting BYDV epiphytotics is discussed.     

Assessing the risk of primary infection of cereals by barley yellow dwarf virus in autumn in the Rennes basin of France

In the Rennes basin, Rhopalosiphum padi is anholocyclic and represents more than 90% of suction trap catches of potential vectors of barley yellow dwarf virus (BYDV) during autumn. From 1983 to 1987 the possibility of predicting the risk of BYDV infection of batches of barley test seedlings (sampling units) exposed each week from September to December near a 12.2 m high suction trap was investigated. Three kinds of variables were checked as possible predictors: weekly mean or maximum temperatures; weekly catches of R. padi (including or excluding males); and percentage of sampling units infested by aphids. Three contrasting examples were observed: during the first three years (1983–1985), infection was high and its change with time followed temperature, aphid catches and plant infestation changes; in 1986, high numbers of aphids caught and a high proportion of plants infested resulted in only low infection and in 1987, both infestation and infection were very low. Simple linear regression analysis showed that the more reliable predictors of infection were the proportion of infested plants and to a lesser extent the numbers of trapped aphids. Multiple linear regressions including either of the three groups of ‘predicting’ variables did not result in any improvement in the prediction. At a practical level, the use of counts of aphid catches would seem a better compromise between accuracy and consistency of prediction and ease of gathering data than that of plant infestation but any significant improvement of the prediction should be sought in an early estimate of the amount of virus available to aphids before they colonise the plants.     

Vector specificity of barley yellow dwarf virus serotypes and variants in southwestern Idaho

Plants with symptoms of barley yellow dwarf virus (BYDV) obtained in infection feeding assays of aphids collected in the field in Idaho between 1986 and 1988 were tested for virus transmissibility by possible aphid vectors. Isolates obtained during 1987–1988 were also tested with a range of polyclonal antisera which distinguished PAV, MAV, SGV, RPV and RMV serotypes. In 1989 some Idaho (ID) BYDV isolates, maintained as standards for comparison, were serotyped and tested for aphid transmissibility, using 11 species of aphids. There was not always the expected correspondence between serotype and vector specificity for ID isolates. For isolates obtained from field-collected Rhopalosiphum padi, vector transmissibility and serotype corresponded with previous reports; however, 44% of isolates which were serotyped as RMV were also transmissible by species other than Rhopalosiphum maidis. Similarly, the transmissibility of the ID laboratory standards did not always conform to the reported vector specificity of serotypes. The laboratory ID-MAV culture was transmitted by Metopolophium dirhodum and Myzus persicae as well as by Sitobion avenae. The laboratory ID-SGV culture was transmitted by R. padi and 5. avenae as well as by Schizaphis graminum. The ID-RPV culture was transmitted by S. graminum and Rhopalosiphum insertum as well as R. padi. Both of two laboratory ID-RMV cultures were transmissible by R. insertum and R. padi transmitted one of them. The results indicate that, for isolates collected in Idaho, vector specificity cannot be assumed from their serotypes.     

Cereal aphids and the infectivity index for barley yellow dwarf virus (BYDV) in northern England

Suction traps at Leeds University Farm, N. Yorkshire, monitored aerial populations of cereal aphids over three autumns. Different migration patterns were observed between the four main species, Sitobion avenae, Metopolophium dirhodum, Rhopalosiphum padi and R. insertum. The relevance of these patterns to the epidemiology of barley yellow dwarf virus (BYDV) is discussed. Transmission tests revealed S. avenae to be the major vector of BYDV, rather than R. padi, which is responsible for disease outbreaks in the south and west of Britain. An Infectivity Index (II) of 50 has been advocated for R. padi-transmitted BYDV, above which economic damage is likely to occur. This value is shown not to be applicable to the Vale of York, and methods of adapting the data are proposed. Such adjusted II values depend on the behaviour and reproduction of the aphids during the transmission tests, and produce II values that correlate well with levels of field infection in the area.     

Suitability of the biomass crop Miscanthus sinensis as a host for the aphids Rhopalosiphum padi (L.) and Rhopalosiphum maidis (F.), and its susceptibility to the plant luteovirus Barley Yellow Dwarf Virus

1 The reproductive performance of two aphid pest species, Rhopalosiphum padi and Rhopalosiphum maidis, was investigated on two seedling growth stages of Miscanthus sinensis, rhizomatous M. sinensis‘Giganteus’ and barley. Rhopalosiphum padi was unable to complete its development on Miscanthus. Rhopalosiphum maidis was most fecund on rhizomatous plants compared with seedling stages. 2 The ability of R. maidis to transmit the RPV isolate of Barley Yellow Dwarf Virus (BYDV) to M. sinensis seedlings was further investigated. Following successful transmission, host plant symptomology and the effect of infection on the yield of Miscanthus were investigated. Total above soil biomass was reduced by around 23% following infection. 3 The inability of R. padi to utilize Miscanthus is reviewed in light of this species’ origin and inability to utilize C₄ host plants. 4 The potential pest status of R. maidis on Miscanthus is discussed together with the impact that Miscanthus cultivation could have on the ecology of this aphid species and BYDV in the U.K.     

The effect of increasing dosage of barley yellow dwarf virus on some resistant and susceptible barleys

Five spring barleys, grown either in pots out of doors or in the field, were inoculated with barley yellow dwarf virus (BYDV) using 5, 10, 20 or 50 infective aphids (Rhopalosiphum padi) per plant. Control plants of each variety received no aphids. Infection with all aphid numbers had highly significant adverse effects on all varieties except Cb 1029, an early maturing BYDV-resistant barley of Ethiopian origin. 12583 Co, a locally bred, late maturing barley possessing the same resistance gene as Cb 1029 suffered more in a pot experiment, but less than three susceptible varieties all of which were severely damaged even when few infective aphids were used. Progressive effects with increasing aphid numbers, indicative of dosage response, occurred in some varieties. These effects included delay in heading and increased stunting, but not less yield. In Cb 1029, BYDV infection caused a reduction in the number of heads per plant, but this was partly compensated for by an increase in the number of grains per head. Conversely, BYDV infection in 12583 Co caused an increase in the number of heads, partly offset by a decrease in the number of Brains tier head.     

Winter wheat (Triticum aestivum) response to Barley yellow dwarf virus at various nitrogen application rates in the presence and absence of its aphid vector,Rhopalosiphum padi

Barley yellow dwarf (BYD) is one of the most common diseases of cereal crops, caused by the phloem‐limited, cereal aphid‐borne Barley yellow dwarf virus (BYDV) (Luteoviridae). Delayed planting and controlling aphid vector numbers with insecticides have been the primary approaches to manage BYD. There is limited research on nitrogen (N) application effects on plant growth, N status, and water use in the BYDV pathosystem in the absence of aphid control. Such information will be essential in developing a post‐infection management plan for BYDV‐infected cereals. Through a greenhouse study, we assessed whether manipulation of N supply to BYDV‐infected winter wheat, Triticum aestivum L. (Poaceae), in the presence or absence of the aphid vector Rhopalosiphum padi L. (Hemiptera: Aphididae), could improve N and/or water uptake, and subsequently promote plant growth. Similar responses of shoot biomass and of water and N use efficiencies to various N application rates were observed in both BYDV‐infected and non‐infected plants, suggesting that winter wheat plants with only BYDV infection may be capable of outgrowing infection by the virus. Plants, which simultaneously hosted aphids and BYDV, suffered more severe symptoms and possessed higher virus loads than those infected with BYDV only. Moreover, in plants hosting both BYDV and aphids, aphid pressure was positively associated with N concentration within plant tissue, suggesting that N application and N concentration within foliar tissue may alter BYDV replication indirectly through their influence on aphid reproduction. Even though shoot biomass, tissue N concentration, and water use efficiency increased in response to increased N application, decision‐making on N fertilization to plants hosting both BYDV and aphids should take into consideration the potential of aphid outbreak and/or the possibility of reduced plant resilience to environmental stresses due to decreased root growth.     

Barley yellow dwarf virus in aphids caught in suction traps, 1969-73

Suction traps operating at low level (1 5 m) were used to catch live alate Rhopalosiphum padi, Macrosiphum (Sitobion) avenae and Metopolophium dirhodum which were tested for transmission of barley yellow dwarf virus (BYDV). The first species caught and infective was R. padi, followed by M. (S.) avenae infective some 2–3 wk later and M. dirhodum 3–4 wk later still. Never more than 11-5% of the annual catch of any species transmitted BYDV and the proportion fluctuated from week to week and between seasons in different years. The relative abundance of infective vectors of ths three species varied; annual numbers of infective M. (S.) avenae and M. dirhodum varied inversely with infective R. padi, the latter also usually transmitted severer virus. The results of the infectivity tests have been compared with the catches of these aphids by the Rothamsted Insect Survey and show that numbers of alate aphids do not necessarily indicate the likely incidence of BYDV.     

Serological and biological characterisation of isolates of barley yellow dwarf virus in Sweden in 1983

In 1983, cereal plants showing symptoms of barley yellow dwarf virus (BYDV), collected from 15 localities in Sweden, were tested for BYDV using enzyme-linked immunosorbent assay (ELISA). Antisera against two Swedish isolates of BYDV were used, a mild isolate (27/77) transmitted specifically by Sitobion avenae and a severe one (39/78) transmitted mainly by Rhopalosiphum padi. No virus was detected in 57 of 607 plants of oats and barley tested. Of the 550 plants in which virus was detected, 366 were infected with viruses similar to isolate 27/77, 116 with viruses similar to 39/78 and the remaining 68 reacted strongly with both antisera. When tested, the latter isolates were shown to be mixtures. Thirty-nine selected samples were also tested with antisera against the USA isolates RPV, RMV, MAV and PAV, and for transmission by S. avenae and R. padi. Twenty-six of these samples were transmitted specifically by S. avenae, one was transmitted only by R. padi and the remaining 12 samples were shown to be infected with a mixture of an S. avenae-specific isolate and one transmitted mainly by R. padi. Antisera against PAV and MAV each detected all isolates tested and the results were very similar to those with the antisera to the 39/78 and 27/77 isolates, respectively. None of the field isolates reacted with antisera against RMV or RPV. It was concluded that 1983 was an epidemic year for BYDV in Sweden and that isolates specifically transmitted by S. avenae predominated. Symptoms of infection by these isolates on oat plants ranged from mild to severe.     

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.     

Vector activity of three aphid species (Hemiptera: Aphididae) modulated by host plant selection behaviour on potato (Solanales: Solanaceae)

Viral diseases non-persistently transmitted by aphids are of great economic importance in several annual crops. Transmission efficiency of these non-persistent phytoviruses is dependant on vector efficiency (i.e. vector intrinsic ability to transmit the virus) but also on the vector activity that implies the early steps of aphid host plant selection process (i.e. brief intracellular stylet punctures after landing) and to their interplant movement ability. In Europe, Macrosiphum euphorbiae (Thomas 1878) is considered as one of the most serious virus vectors on potato (Solanum tuberosum L. 1753). Nevertheless, several alate aphid species that do not colonise potato plants are trapped in potato crops. Therefore, we investigated, through laboratory experiments, vector activity of one potato colonising aphid, M. euphorbiae, and two non-colonising potato aphids, the bird cherry-oat aphid Rhopalosiphum padi (L. 1758) and the pea aphid Acyrthosiphon pisum (Harris 1776). A settling experiment was used to evaluate dispersal activity, and the electrical penetration graph (EPG) technique was used to investigate probing activity on potato plants. Results showed that M. euphorbiae exhibited a better vector activity than other two aphid species in terms of landing and probing. By contrast, interplant movements were only recorded on non-colonising aphids, suggesting a better vector activity than M. euphorbiae in terms of locomotive behaviour. These data confirm the involvement of A. pisum and R. padi in the spread of non-persistent viruses.     

Aerial flow of barley yellow dwarf viruses and of their vectors in western France

During the years 1989–1992 cereal aphids were caught alive in a low level (1.5 m high) suction trap operated in Le Rheu (Brittany, France) and tested for BYDV transmission. In most cases comparisons with data collected simultaneously by a 12.2 m suction trap operating in the same site resulted in good relationships between weekly catches at both heights. Results from transmission tests showed that: (i) the two main BYDV vectors were Rhopalosiphum padi and Metopolophium dirhodum during the years of experiment; (ii) PAV and MAV were the commonest viruses and RPV was relatively scarce; (iii) during spring M. dirhodum appeared to be the most important MAV vector and nearly as good a PAV vector as R. padi; (iv) during autumn R. padi was the only vector of the three viruses with mixed transmission allowing it to transmit also MAV probably by heteroencapsidation. To give an indication of the risk of infection, infectivity indices were calculated by multiplying the numbers of aphids caught by the 12.2 m suction trap by the proportion that were infective. These infectivity indices agreed with field records of primary infections.     

Influence of drought on interactions between Rhopalosiphum padi and ground dwelling predators – A mesocosm study

Climate change will lead to extreme droughts, but it is difficult to predict how this will affect crop pests. In particular, it is unclear how interactions between natural enemies and pests will be influenced. In the field, bird cherry-oat aphids (Rhopalosiphum padi (L.)) have been observed to reside close to, or below the ground surface during dry conditions. We hypothesized that this will increase the niche overlap between R. padi and ground-dwelling predators such as carabid beetles and wolf spiders and that aphid numbers will therefore decline during dry conditions. A fully factorial mesocosm experiment was conducted testing the combined effects of drought and predator presence on aphid position and abundance on barley (Hordeum vulgare) plants. In support of our hypothesis, we found that (a) aphids moved below ground during dry conditions, (b) predators reduced aphid numbers, but only during dry conditions, and (c) predators reduced the proportion of aphids below ground in dry conditions. This increased predation effect during dry conditions was, however, compensated for by a corresponding increase in aphid performance on the plants and so the net effect of drought on aphid numbers ended up being neutral. Thus, pests can be affected by drought in complex ways via a combination top-down and bottom-up mechanisms. Predicting how pest populations will be affected by droughts in the future is thus a formidable research challenge.     

Predator density manipulation and its effects on populations of Rhopalosiphumpadi (Horn.: Aphididae) in spring barley

Experiments were carried out in 1981-83 to assess the impact of polyphagous predators (e.g. Carabidae, Staphylinidae and Araneae) on populations of cereal aphids in spring barley in Sweden. Barriers were erected around mid-field and field-edge plots at different times during the aphids' establishment phase in order to manipulate the predation pressure during the aphid pre-peak period; predators were emigrating from field boundaries. Rhopalosiphum padi was the dominant species of cereal aphid in 1981 and 1982, and was abundant in both years. Reduction of the predation pressure resulted in R. padi populations that were two to six times larger compared with those in unenclosed control plots. Aphid populations were much larger when the predation pressure was reduced earlier in June than when this was done later, in both years, since late erection of barriers excludes fewer predators because most had already entered the enclosed areas. In 1983, R. padi and Sitobion avenae were equally common but occurred in low numbers, and the effects of reducing the predation pressure were less obvious. Bembidion spp. (B. lampros and B. quadrimaculatum) and linyphiid spiders were the most abundant predators during the early establishment phase of aphid populations in each year, and significant inverse correlations were found between peak numbers of R. padi per shoot and numbers of predators from these taxa in 1981 and 1982. Similar relationships were found between total aphids and numbers of Staphylinidae, B. quadrimaculatum and Coccinella septempunctata in 1983. It was concluded that differences between the manipulated numbers of polyphagous predators caused the observed differences in peak population levels of R.padiin 1981,1982 and to a lesser extent, 1983. Apparent levels of parasitism and fungal disease were low during the pre-peak period. Aphid specific predators, abundant after the peak, were considered partly responsible for the decline of aphid populations each year. The results are compared with those from similar experiments elsewhere with S. avenae and Metopolophium dirhodum in winter wheat. Reasons why the effects of polyphagous predators are greater, and occur over a much shorter period of time in Sweden are discussed.     

The price of protection:a defensive endosymbiont impairs nymph growth in the bird cherry-oat aphid,Rhopalosiphum padi

Bacterial endosymbionts have enabled aphids to adapt to a range of stressors,but their effects in many aphid species remain to be established.The bird cherry-oat aphid,Rhopalosiphum padi(Linnaeus),is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L-type symbiont endobacteria,although the resulting aphid phenotype has not been described.This study presents the first report of R.padi infection with the facultative bacterial endosymbiont Hamiltonella defensa.Individuals of R.padi were sampled from populations in Eastern Scotland,UK,and shown to represent seven R.padi genotypes based on the size of polymorphic microsatellite markers;two of these genotypes harbored H.defensa.In parasitism assays,survival of H.defensa-infected nymphs following attack by the parasitoid wasp Aphidius colemani(Viereck)was 5 fold higher than for uninfected nymphs.Aphid genotype was a major determinant of aphid performance on two Hordeum species,a modern cultivar of barley H.vulgare and a wild relative H.spontaneum,although aphids infected with H.defensa showed 16%lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals.These findings suggest that deploying resistance traits in barley will favor the fittest R.padi genotypes,but symbiontinfected individuals will be favored when parasitoids are abundant,although these aphids will not achieve optimal performance on a poor quality host plant.     

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.     

The effect of drought stress and temperature on spread of barley yellow dwarf virus (BYDV)

1 The effect of drought stress and temperature on the dispersal of wingless aphids Rhopalosiphum padi (L.) and the pattern of spread of BYDV (barley yellow dwarf virus) within wheat plants in controlled environment chambers was quantified. Combinations of three different drought stress levels, unstressed, moderate and high stress level, and three different temperatures, 5 ± 1 °C, 10 ± 1 °C, and 15 ± 1 °C, were investigated. 2 With increased temperature there was an increase in the mean distance of visited plants from the point of release and in the number of plants visited and infected with BYDV. Drought stress had no effect on mean distance moved by aphids at any temperature or on plants infected with virus at 10 °C and 5 °C. When plants were drought stressed, the numbers of plants visited and infected were greater at 15 °C than at 10 °C and 5 °C. 3 A greater proportion of plants visited by aphids was infected with BYDV when plants were stressed than when not stressed. At 15 °C a greater proportion of these plants was infected than at lower temperatures. There was no difference between treatments in the numbers of aphids present at the end of the experiment. 4 It is concluded that drought stress and temperature are of considerable importance in virus spread.     

Effect of mineral oils on host plant selection and probing behavior of Rhopalosiphum padi

Aphids that colonize and reproduce on potato are some of the most efficient vectors of Potato virus Y (PVY) (Potyviridae: Potyvirus), and hence these aphids have been the focus of the majority of studies to date. However, other non‐colonizing aphids can also function as vectors. Mineral oil is the only product available to growers that effectively prevents the spread of PVY in potato seed production. Most previous studies focused on the effect of mineral oil on the behavior of aphids on their preferential host plant, and consequently there is a lack of information for non‐colonizing aphids on potato plants. The objective of this study was to determine the effect of spraying potatoes with one of two mineral oils, Superior 70 or Vazyl‐Y, on host selection and probing behavior of the non‐colonizing aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae). The electrical penetration graph (EPG) technique, combined with ethological observations, determined that there was no difference in R. padi behavior on potato plants treated with Superior 70. However, there were few significant changes in R. padi behavior on plants sprayed with Vazyl‐Y, including a delay in the initiation of stylet penetration and an increase in the duration of xylem sap ingestion. These new data support previous results and confirm that the mode of action of mineral oil in the reduction of the spread of PVY is not solely due to the modification of the behavior of aphids.     

Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies

This study investigated the effects of airborne interaction between different barley cultivars on the behaviour of bird cherry-oat aphid Rhopalosiphum padi, the ladybird Coccinella septempunctata and the parasitoid Aphidius colemani. In certain cultivar combinations, exposure of one cultivar to air passed over a different cultivar caused barley to have reduced aphid acceptance and increased attraction of ladybirds and parasitoids. Parasitoids attacked aphids that had developed on plants under exposure more often than those from unexposed plants, leading to a higher parasitisation rate. Ladybirds, but not parasitoids, were more attracted to combined odours from certain barley cultivars than either cultivar alone. The results show that airborne interactions between undamaged plants can affect higher trophic levels, and that odour differences between different genotypes of the same plant species may be sufficient to affect natural enemy behaviour.