Barley yellow dwarf virus, wheat, and Sitobion avenae: a case of trilateral interactions

We analysed interactions in the system of two Barley Yellow Dwarf Virus (BYDV) strains (MAV and PAV), and wheat (cv. Tinos) as host plant for the virus, and the cereal aphid Sitobion avenae (F.) as vector, in particular whether or not infection by the virus might alter host plant suitability in favour of vector development. By measuring the amino acid and sugar content in the phloem sap of infected and non‐infected wheat plants we found a significant reduction in the concentration of the total amount of amino acids on BYDV‐infected plants. Qualitative and quantitative analysis of honeydew and honeydew excretion indicated a lower efficiency of phloem sap utilisation by S. avenae on infected plants. In addition, S. avenae excreted less honeydew on infected plants. Both BYDV strains significantly affected aphid development by a reduction in the intrinsic rate of natural increase. Hence, infection by the virus reduced the host suitability in terms of aphid population growth potential on BYDV‐infected plants. However, more alate morphs developed on virus‐infected plants. These findings are discussed in relation to the population dynamics of S. avenae, and, as a consequence, the spread of BYDV.     

The effect of barley yellow dwarf virus on field populations of the cereal aphids, Sitobion avenae and Metopolophium dirhodum

The numbers of cereal aphids, especially Metopolophium dirhodum in 1979, and Sitobion avenae in 1980, were significantly increased on BYDV infected wheat and oats in 1979, and wheat, barley and oats in 1980. The differences were probably caused by attraction of alates of each species to virus infected plants which had changed colour as a result of their infection. Significantly more alates of M. dirhodum were found on virus infected oats in 1979, and of S. avenae on oats and barley in 1980, although not on wheat in either year. probably because the colour contrast in wheat was less intense than in the other crops. Flight chamber experiments with alates of both species confirmed their visual attraction to virus-infected leaves. The interaction between virus, vector and host plants is discussed with reference to the ecology of virus spread.     

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.     

Bionomics of aphids reared on cereals and some Gramineae

In controlled temperature, light and relative humidity, Metopolophium dirhodum and Sitobion avenae multiplied more on young Proctor barley than on Blenda oats, and less on Cappelle wheat. Rhopalosiphum padi increased in number fastest on barley and slowest on oats. More survived, and generation lengths seemed shorter, on barley for M. dirhodum and S. avenae and on wheat for R. padi. Tests with young cereals outdoors generally agreed with those in controlled conditions. On mature plants, there were more M. dirhodum on barley, more R. padi on wheat and more S. avenae on oats than on the other cereals. Given a free choice in large cages outdoors, most aphids were found on barley. When allowed to choose between grasses, more M. dirhodum were on Dactylis glomerata, Poa pratensis and Festuca pratensis, more R. padi on Lolium perenne and F. pratensis, and more S. avenae on D. glomerata and L. perenne. Most aphids of all species combined were on F. pratensis, Lolium and Phleum, and fewest on Festuca rubra and Holcus mollis.     

Comparison of the potential rate of population increase of brown and green color morphs of Sitobion avenae (Homoptera: Aphididae) on barley infected and uninfected with Barley yellow dwarf virus

Life tables of brown and green color morphs of the English grain aphid, Sitobion avenae (Fabricius) reared on barley under laboratory conditions at 20 ± 1°C, 65% ± 5% relative humidity and a photoperiod of 16 : 8 h (L : D) were compared. The plants were either: (i) infected with the Barley yellow dwarf virus (BYDV); (ii) not infected with virus but previously infested with aphids; or (iii) healthy barley plants, which were not previously infested with aphids. Generally, both color morphs of S. avenae performed significantly better when fed on BYDV‐infected plants than on plants that were virus free but had either not been or had been previously infested with aphids. Furthermore, when fed on BYDV‐infected plants, green S. avenae developed significantly faster and had a significantly shorter reproductive period than the brown color morph. There were no significant differences in this respect between the two color morphs of S. avenae when they were reared on virus‐free plants that either had been or not been previously infested with aphids. These results indicate that barley infected with BYDV is a more favorable host plant than uninfected barley for both the color morphs of S. avenae tested, particularly the green color morph.     

Aphid colonization of spring cereals

In 1970-1, Metopolophium dirhodum, Rhopalosiphum padi and Sitobion avenae were the commonest alatae trapped from April/May to August, with most in July and early August. The first alatae appeared in the Rothamsted survey suction trap 0–34 days before aphids were found on the cereals, but during May and June no relationship was found between the numbers trapped and the number on the crop. Most species occurred first near the sheltered edge of the crop, but M. dirhodum was widespread over the field. Most infestations were quickly dispersed by the movements of older morphs; adults only stayed in one place for about 2 days. Alate M. dirhodum moved more often than apterae, but both morphs of S. avenae moved equally often and more frequently between larvipositions than did those of M. dirhodum. Apterae deposited more nymphs in a ‘group’ than alatae, and M. dirhodum deposited more than S. avenae. Few ‘groups’ persisted for more than a week. Although M. dirhodum occupied the crop area faster than S. avenae, all 0–3 m lengths of row sampled being infested within 2–5 wk of their first appearance, most or all of the tillers were colonized only in late July 1970.     

Identification, Distribution and Vector Population Dynamics of Barley Yellow Dwarf Virus in Three Cereal-Producing Areas of Spain

ELISA-based surveys during 1985–87 in three major cereal-growing areas of Spain confirmed the presence of barley yellow dwarf virus (BYDV). Samples of small grain cereals and grasses with and without BYDV-like symptoms were collected in the central, southwestern, and northeastern Spain. Infections were found in all cereal species sampled and in some grasses. About 37 % of the samples collected in 1985 were infacted with isolates of the PAV serotype. Isolates of the RPV serotype were less common, and were detected only in samples from the central region at El Encin, Madrid. Only a single sample, collected from El Encin in 1987, was unequivocally diagnosed as containing an isolate of the MAV serotype. Aphid vector population dynamics was monitored during fall and winter of 1984–87 in the central region. Rhopalosiphum padi L. appeared to be the most abundant species during fall and winter months, infesting grasses and volunteer wheat. Other species present were Sitobion avenae (F.), Metopolophium dirhodum (Walker) and Rhopalosiphum maidis (Fitch). Both R. padi and S. avenae seem to be anholocyclic in the central region of Spain, and are able to remain and reproduce on wheat volunteers and grasses until the beginning of spring. S, avenae populations increase quickly on wheat volunteers in April, while populations of R. padi remain low. Therefore, spread of S. avenae-transmitted BYDV types to neighbouring cereal fields seem more likely to occur than spread of other types. Other possible virus reservoirs, such as maize, also need investigation for a better understanding of BYDV epidemiology in the central and other cercal-growing areas of Spain.     

Distribution of aphids in cereal crops

Cereal crops were examined weekly for aphids during 1969. Plants in twenty samples of row 0.3 m long were examined in a sheltered perimeter of a crop and along a transect 36.6 m into the crop. Aphids were usually first found within 1–4 weeks of the first alatae caught in a suction trap operating 12.2 m above ground. When first alatae caught in a suction trap operating 12.2 m above ground. When the first found from 10 to 27% of the 0.3 m lengths sampled contained aphids. Rhopalosiphum padi, first found late in May, were scarce (< 0.53/0.3 m) throughout June and July. Sitobium spp. and Metapolophium dirhodum, which appeared in mid-June, were more numerous than R. padi; most occurred during the second half of July, and populations decreased just before harvest in early August. Sitobium avenae was more abundant (max. 19.3/sample) than either S. fragariae (0.91) or M. dirhodum (2.51). More aphids occurred in oats (max. 52/0.3 m) during July than in wheat (45), and barley had fewer (6.8). S. avanae was more abundant than M. dirhodum in sheltered areas of barley and wheat, and in exposed areas of the same crop M. dirhodum was commonest. Along sheltered perimeters, the ratio of S. avenae to M. dirhodum was largest in barley (11:1), intermediate in oats (6:1) and smallest in wheat (3.7:1). Sitobium spp. were most numerous on the ears, when most M. dirhodum were on the leaves. Regression analyses of log. S² on log. m suggested that S. avenae was more evenly distributed within (36.6 m) the field (b = 1.056 + 0.109) than along the sheltered perimeter (b = 1.432 + 0.132), though it seemed similarly distributed along perimeters of barley, oats and wheat. The distributions of M. dirhodum and Sitobium spp. along sheltered perimeters of all crops were apparently similar.     

Infection of cereal aphids by the fungus Entomophthora

Three species of Entomophthora killed many Metopolophium dirhodum, M. festucae and Sitobion avenae on wheat at Harpenden, Hertfordshire, in 1971. Rainfall was low and aphid numbers were small in May and there was no Entomophthora infection. E. planchoniana first infected M. dirhodum early in June and the percentage of each aphid species infected increased during and after heavier rain in the first 2 weeks of June. M. dirhodum and S. avenae were most often infected by E. planchoniana, and the less common M. festucae mostly by E. aphidis and E. thaxteriana. Relative frequencies of E. aphidis and E. thaxteriana were largest before, and of E. planchoniana after, mid-July. The largest percentages infected were 53% of M. dirhodum and 30% of S. avenae during the second half of July and 60% of M. festucae in late June. The percentages of old nymphs and apterous adults that were infected were similar and only about half those of infected alatae.     

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.     

Geographic and microgeographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe

Samples of the grain aphid Sitobion avenue (F.) and the rose-grain aphid Metopolophium dirhodum (Walker) were collected in late March from wheat fields and adjacent road-side grasses at a number of locations in southern England. Unparasitized aphids were DNA fingerprinted using the multilocus (GATA)₄ probe. Over all locations, the fingerprints of individual S. avenue caught in wheat had lower overall average distances of band migration (ADBM) and shared a higher proportion of bands, than fingerprints of individuals caught in adjacent road-side grasses. The ADBM of fingerprints of S. avenue collected on road-side grasses altered significantly with geographical location, while the ADBM of fingerprints of S. avenue caught on wheat did not. A comparison of the fingerprints of individual M. dirhodum caught in wheat and neighbouring road-side grasses did not reveal any genetic differentiation. Fingerprints of M. dirhodum that were caught in the same host type did however, show significant variation in ADBM between different locations. With both S. avenue and M. dirhodum, spatial autocorrelation revealed that locations that were close together were no more likely to have individuals with similar ADBM than locations mat were far apart Our results suggest that (i) particular clones of S. avenue prefer to colonize wheat; and/or that (ii) particular clones of S. avenae perform better on wheat man other clones. It is unclear why M. dirhodum did not show any genetic structuring according to host type, but this species appears to engage in sexual reproduction much more frequently than S. avenae in southern England. M. dirhodum is likely to have displayed genetic heterogeneity between locations either because of founder effects, or because of genetic drift.     

The effects of sowing date and choice of insecticide on cereal aphids and barley yellow dwarf virus epidemiology in northern England

During the mid-1980s, Sitobion avenae became recognised as an important vector of barley yellow dwarf virus (BYDV) in the Vale of York. A field trial at the University of Leeds Farm, North Yorkshire, was carried out during the autumn/winter of 1984-85 to evaluate different control procedures against S. avenae-transmitted BYDV and to investigate its epidemiology. Winter barley was sown on three dates in September, and plots were sprayed with either deltamethrin, demeton-S-methyl or pirimicarb on one of three dates between mid-October and mid-November, making a factorial design. Rhopalosiphum padi, the main vector of BYDV in southern England, were rarely found during the experiment, but the numbers of S. avenae were much higher, reaching a peak of 21% of plants infested in the unsprayed plots of the first sowing date. Single applications of each insecticide reduced populations of S. avenae to zero. Some treatments, particularly in the early sown plots and those treated with pirimicarb, however, did allow some recolonisation, and thus led to increased virus incidence and decreased yields. Sprays applied before the end of the migration of S. avenae were more efficient at controlling BYDV if the insecticide was persistent, otherwise a spray after this period, in November, was more effective. Virus incidence, although reduced by sprays, was generally low in plots sown on 18 and 27 September. In contrast, about 11% of plants were infected in unsprayed plots sown on 6 September and a small yield benefit was obtained with insecticidal treatments. Enzyme-linked immunosorbent assay (ELISA) of plants taken from the plots indicated that MAV- and PAV-like strains were present, and were most likely to have been transmitted by S. avenae.     

Olfactory response by the aphidophagous gall midge, Aphidoletes aphidimyza to honeydew from green peach aphid, Myzus persicae

Female adults of the aphidopagous gall midge, Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), showed an olfactory response to honeydew excreted by the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) under laboratory conditions. The response was only elicited by treatments with honeydew, whereas aphids, aphids with pepper plants or leaves, and pepper plants or leaves were not attractive to the midges. Dose‐dependent responses were observed from whole honeydew, honeydew volatiles extracted in pentane, and honeydew volatiles captured on Porapak Q®. When honeydew was eluted with three sequential pentane washes, a positive response was only observed from the midges for the first wash. Female midges laid more eggs on pepper plants infested with higher densities of M. persicae. The olfactory response of midges to honeydew is discussed with respect to prey location.     

The influence of mixed aphid diets on larval performance of Coccinella septempunctata (Col., Coccinellidae)

Abstract: Three questions regarding possible benefits of mixed diets for the specialist aphid predator, Coccinella septempunctata larvae were investigated. (1) Do aphids species from different host plants complement each other nutritionally? (2) Is a mixed diet of high‐quality aphids beneficial? (3) How does the quality of mixed diets depend on the quality of constituent species? All mix‐combinations of aphid species of high (Metopolophium dirhodum), intermediate (Myzus persicae), and poor food quality (Aphis sambuci), and the three single‐species diets were compared. A mixed diet of two high‐quality species (Sitobion avenae and M. dirhodum) was also compared with single‐species diets. Larvae that were given pure A. sambuci and a mixed diet of A. sambuci + M. persicae died within 18 days and none of the larvae developed to fourth instar. Metopolophium dirhodum was generally of higher quality as food than M. persicae, whereas the mixed diet of M. dirhodum + M. persicae was intermediate. Sitobion avenae and M. dirhodum were found to have approximately the same food value. Coccinella septempunctatam larvae that were offered a mixed diet of these two high‐quality aphids gained no extra advantage. Overall, no benefit from mixing of aphid species was found. The quality of mixed diets depended on the quality of the constituent species.     

Field assessments of resistance to the aphids Sitobion avenae and Metopolophium dirhodum in old and modern spring-sown wheats

Three ancient varieties of wheat and two modern spring-sown cultivars were investigated in the field to assess their resistance to the cereal aphids Sitobion avenae and Metopolophium dirhodum; the monitoring of natural populations and detailed observations using clip-cages were both undertaken. The ancient variety Einkorn showed both antixenotic and antibiotic resistance to S. avenae, and antibiotic resistance to M. dirhodum. The resistance to S. avenae was greater than that to M. dirhodum. The value of Einkorn as a component of a resistance-breeding programme is discussed with reference to its agronomic and genetic characteristics and with reference to the pest status of cereal aphids.     

Preference of cereal aphids for different varieties of winter wheat

This paper reports on the development of a simple and robust preference meter (developed in-house) to score the host choice behavior of apterous aphids. With this tool, the preferences of two important cereal aphids Sitobion avenae (Fab.) and Metopolophium dirhodum (Walker) were investigated against four different varieties of winter wheat (Triticum aestivum L.) with a different susceptibility for Fusarium head blight (FHB). Differences in the choice behavior of both aphid species were observed for different wheat varieties. The preferred wheat variety of S. avenae and M. dirhodum was not the same. Also, both aphid species clearly had a differential preference for seedlings and ears. Using seedlings, M. dirhodum was about 1.8 times more rapid in making its choice than S. avenae. In separate experiments with ears, S. avenae was 4.5 times faster than in the experiments with seedlings. In the present study, we aim to highlight differences in preference behavior in relation to potential mechanisms for host selection.     

The value of three cereal aphid species as food for a generalist predator

The value of the cereal aphid species Metopolophium dirhodum (Wlk.), Sitobion avenae (F.) and Rhopalosiphum padi (L.) as prey for the linyphiid spider Erigone atra (Bl.) was assessed. Fecundity of females was determined for spiders fed on eight experimental diets: three single‐species aphid diets, a mixed diet of all three aphid species, three mixed diets with each aphid species in combination with fruit flies Drosophila melanogaster (Meig.), and pure D. melanogaster as a high quality comparison diet. The development and survival of first‐instar juveniles fed on three diets of single aphid species, and on a diet of Collembola were compared with those subjected to starvation. Prey value for adult females was assessed by egg production, hatching success and offspring size. In pure diets all three aphid species were of low value to the spiders, causing a rapid decline in egg production and supporting no growth of significance of first‐instar juveniles. No difference in value of aphid species of single‐species aphid diets was found in the fecundity experiment, while a ranking of aphid species of M. dirhodum > R. padi > S. avenae was revealed in the survivorship experiment. A mixed‐aphid diet was not found to be advantageous compared with single‐species aphid diets, and no advantage of including aphids in mixed diets with fruit flies was found. Metopolophium dirhodum and R. padi were neutral in mixed diets, while a diet of S. avenae and fruit flies caused reduced egg production compared with the pure diet of fruit flies, revealing a toxic effect of S. avenae on the spider. The value‐ranking of aphid species in mixed diets was similar to that of single‐species diets. A similar ranking of aphid species was found for different fitness parameters (fecundity of adult females and development of juveniles). A ranking of aphids by offspring size of mothers on aphid‐only diets was S. avenae > M. dirhodum > R. padi. All aphid‐fruit fly diets resulted in larger offspring than a diet of only D. melanogaster, with the overall largest offspring being produced on the diet of M. dirhodum and fruit flies.     

Entomophthora infecting the cereal aphids Metapolophium dirhodum and Sitobion avenae

Entomophthora aphidis, E. planchoniana, and E. thaxteriana killed many Metapalophium dirhodum and Sitobion avenae in barley during 1970. E. planchoniana first infected M. dirhodum late in June, after rain ended a long dry period, but few aphids were infected until after July 7, when heavy rain killed 65–80% of aphids. E. planchoniana was the most frequent of the 3 species until July 27, when E. aphidis and E. thaxteriana each became more abundant. S. avenae was more often infected by E. thaxteriana than the other species of Entomophthora. During the second half of July, 40–76% of adult M. dirhodum and 34–80% of S. avenae were infected. The 3 fungus species were equally common in M. dirhodum in sheltered fields, but E. thaxteriana was less common in an exposed field. In a sheltered field, E. thaxteriana was less frequent than the other species along the perimeter, and E. planchoniana was most common and E. aphidis the least common about 37 m into the crop.     

The influence of nitrogen fertiliser on the population development of the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Wlk.) on field grown winter wheat

The effect of nitrogen fertiliser on populations of the cereal aphids Sitobion avenae and Metopolophium dirhodum on winter wheat was investigated in a three year field experiment. Naturally occurring aphid populations were monitored on three nitrogen treatments; none, nitrogen application using Canopy Management guidelines (130–210 kg ha^-1) and conventional practice (190 kg ha^-1). Inoculations of laboratory reared S. avenae were used to enhance field populations on half the plots. Natural populations of M. dirhodum remained below the current UK spray threshold level of two-thirds of shoots infested at the start of flowering, or five aphids per shoot in all years, whilst populations of S. avenae exceeded the threshold in all years. The response of the two species to nitrogen differed. Significantly higher populations of M. dirhodum were recorded in both treatments which received nitrogen in all years, whilst the response of S. avenae varied between years. In 1994 and 1995 when environmental conditions favoured aphid development, higher populations were recorded in the two treatments which received nitrogen. In 1993 when high rainfall created unfavourable conditions, higher populations were recorded in the plots receiving no nitrogen. Differences in peak density and cumulative aphid index of S. avenae resulted from differences in the rate of population increase between ear emergence and peak density on the different treatments. Populations prior to ear emergence were higher in the plots which received nitrogen but the differences were not statistically significant. There was no evidence of a difference in the timing of population decline in the different treatments. In 1993 higher levels of infection by entomopathogenic fungi were observed in all treatments. Significantly higher levels of infection were recorded in the treatments receiving nitrogen, which may have accounted for the lower S. avenae populations recorded. It is possible that the larger canopies recorded in these treatments produced conditions which favoured infection by fungi, thereby limiting aphid population growth. The results indicate that application of nitrogen increases natural populations of M. dirhodum, and under favourable conditions, populations of S. avenae. However, in suboptimal climatic conditions, the application of nitrogen fertiliser can lead to lower populations of 5. avenae. The data also suggest that there is no consistent difference between a conventional and Canopy Managed approach to nitrogen fertiliser use in terms of the risk of infestation by cereal aphids.     

The overwintering and abundance of cereal aphids

The longevity of Sitobion avenae varied inversely with temperature from 25 to over 100 days when reared outdoors on barley under lantern jars, being longest between December and April–May. This was due mainly to changes in the length of the pre- and post-reproductive periods rather than the length of the period of reproduction. Fecundity varied directly with temperature, from eight to sixty-seven nymphs per female. When reared on winter wheat and sheltered from wind, rain and snow, S. avenae survived best, Metopolophium dirhodum survived less well and Rhopalosiphum padi worst; when exposed in the open none of the three species survived. Close relationships were not demonstrable between the numbers of alate M. dirhodum, S. avenae and Rhopalosiphum spp. trapped in any year, between the abundance of these aphids and weather conditions between January and April, or between the numbers of these alatae and the size of crop infestations. This was probably because insufficient information was available about their biology, both inside and outside the crop.