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.     

Entomophthora species infecting pea aphis

• 1 Three species of Entomophthora infected the pea aphis, Acyrthosiphon pisum, on lucerne at Rothamsted Experimental Station, Harpenden, Hertfordshire, between 1967 and 1972 and caused a maximum mortality of 83% in July 1968.
• 2 E.thaxteriana, the commonest species, occurred each year and frequently infected aphids during cool weather in spring and autumn. E.aphidis and E.planchoniana were absent in some years and were most common during warm weather in midsummer.
• 3 The incidence of infection by the three species was correlated with the density of conidia in the air above the crop, host density and rainfall, but not with any other weather factor considered.
• 4 Infection at any time was much more closely related to environmental factors during the preceding 12 than 3 days. The regressions, however, were weak and the relative importance of different environmental factors for the spread of infection can probably only be determined under controlled conditions in the laboratory.

     

The survival of Entomophthora spp. in mummified aphids at different temperatures and humidities

Entomophthora aphidis survived for at least 32 weeks at 0°C and 20 or 50% RH and E. thaxteriana for at least 16 weeks at 10°C and 20 or 50% RH in mummified infected pea aphids, Acyrthosiphon pisum. The fungi produced infective conidia when the aphids were moistened. This probably explains the survival of Entomophthora species infecting aphids during short periods when the weather is unsuitable for conidial discharge and host infection.     

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.     

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.     

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.     

New records of aphid hosts of Entomophthora aphidis and E. planchoniana in New Zealand

Examination of diseased aphids from the Christchurch area of New Zealand during summer 1974 established new records of Entomophthora aphidis and E. planchoniana attacking Macrosiphum hellebori and E. planchoniana parasitising Aulacorthum solani, plus the first record for New Zealand of E. aphidis infecting Myzus persicae.     

The spatial distribution of canopy-resident and ground-resident cereal aphids (Sitobion avenae and Metopolophium dirhodum) in winter wheat

We investigated, within two cereal fields in Southern England, the within-canopy spatial distribution of the aphids Sitobion avenae and Metopolophium dirhodum in relation to crop yield and plant nitrogen. We extended the study to investigate the spatial distribution of aphids that fell to, or returned from, the ground in order to estimate availability of the within-canopy aphid population to ground-active predators. We revealed that crop canopy aphid spatial pattern was associated with nitrogen or yield. Differences were evident between species: S. avenae was generally negatively associated with yield or plant nitrogen, whilst M. dirhodum exhibited positive association. For both aphid species, we observed strong spatial pattern for aphids falling to the ground and conclude that this could, in part, mediate the effectiveness of ground-active predators as pest control agents.     

The effect of barley yellow dwarf virus on honeydew production by the cereal aphids, Sitobion avenae and Metopolophium dirhodum

Individual S. avenae and M. dirhodum excreted significantly fewer droplets of honeydew on plants infected with BYDV than on healthy plants. S. avenae excreted less honeydew on the ears than on the leaves of wheat. M. dirhodum excreted less than S. avenae on the leaves. The size of honeydew droplets increased with the age of aphids but was not affected by BYDV infection. Possible reasons for the observed effects of BYDV on honeydew excretion are discussed.     

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.     

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.     

Could Behaviour and Not Physiological Thermal Tolerance Determine Winter Survival of Aphids in Cereal Fields?

Traits of physiological thermotolerance are commonly measured in the laboratory as predictors of the field success of ectotherms at unfavourable temperatures (e.g. during harsh winters, heatwaves, or under conditions of predicted global warming). Due to being more complicated to measure, behavioural thermoregulation is less commonly studied, although both physiology and behaviour interact to explain the survival of ectotherms. The aphids Metopolophium dirhodum, Rhopalosiphum padi and Sitobion avenae are commercially important pests of temperate cereal crops. Although coexisting, these species markedly differ in winter success, with R. padi being the most abundant species during cold winters, followed by S. avenae and lastly M. dirhodum. To better understand the thermal physiology and behavioural factors contributing to differential winter success, the lethal temperature (physiological thermotolerance) and the behaviour of aphids in a declining temperature regime (behavioural thermotolerance) of these three species were investigated. Physiological thermotolerance significantly differed between the three species, with R. padi consistently the least cold tolerant and S. avenae the most cold tolerant. However, although the least cold tolerant of the study species, significantly more R. padi remained attached to the host plant at extreme sub-zero temperatures than S. avenae and M. dirhodum. Given the success of anholocyclic R. padi in harsh winters compared to its anholocyclic counterparts, this study illustrates that behavioural differences could be more important than physiological thermotolerance in explaining resistance to extreme temperatures. Furthermore it highlights that there is a danger to studying physiological thermotolerance in isolation when ascertaining risks of ectotherm invasions, the establishment potential of exotic species in glasshouses, or predicting species impacts under climate change scenarios.     

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.     

Biologie des pucerons des céréales dans l'ouest de la France II. Répartition spatio-temporelle et action limitative de trois espèces d'Entomophthoraceae

Résumé L'étude comparée de l'action limitative de 3 espèces d'Entomophthoraceae sur les pucerons des céréales a été effectuée dans l'Ouest de la France (Bassin de Rennes essentiellement) de 1975 à 1978. La quasi-totalité des cas de mycose sont dus àErynia neoaphidis Remaud. & Henn.,Conidiobolus obscurus (Hall & Dunn) Remaud. & Keller etEntomophthora planchoniana Cornu. L'analyse de la répartition des différentesEntomophthoraceae au cours de l'année montre queE. neoaphidis est l'espèce qui a la plus grande période d'activité (elle se manifeste pendant pratiquement toute l'année sur les populations anholocycliques) et qui infecte, à un moment donné, le plus de pucerons.C. obscurus dispara?t en général en hiver après la formation abondante de spores durables et ne réappara?t qu'au cours du printemps. D'une année sur l'autre, à un instant donné,C. obscurus est rarement déterminé sur plus de 25% du total des pucerons mycosés récoltés. Enfin,E. planchoniana a une période d'activité essentiellement estivale qui peut se prolonger en automne sur les pucerons pullulant sur ma?s. C'est sur ces derniers qu'elle semble la plus efficace. Sur blé d'hiver, l'action apparente deE. neoaphidis et deC. obscurus n'est pas la même selon l'espèce de pucerons et la position de ceux-ci sur la plante:E. neoaphidis est encore plus pathogène pourM. dirhodum que pourS. avenae etC. obscurus semble davantage parasiter les pucerons situés sur le feuillage que ceux situés sur les épis. Enfin, l'étude de l'action deE. neoaphidis, C. obscurus etE. planchoniana en fonction de la taille de la colonie (ou du ?groupe? de pucerons) montre que l'action deE. neoaphidis semble indépendante de la densité de pucerons alors que le développement deC. obscurus dans les colonies est moins rapide que l'augmentation de taille de celles-ci. D'une manière générale, l'action deE. planchoniana est moins bien connue du fait du manque de matériel. La prédominance deE. neoaphidis s'explique par l'excellente adaptation de cette espèce à l'anholocyclie des pucerons, par sa faible spécificité à l'intérieur du groupe des aphides et par le nombre important de conidies qu'elle projette en atmosphère saturante. Cette espèce semble avoir les meilleures potentialités entomopathogènes en tant qu'agent de lutte biologique en cultures céréalières, mais son emploi futur sera subordonné à sa production de masse sous forme stable et pathogène.

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Summary The role of 3 species ofEntomophthoraceae on cereal aphids in the West of France from 1975 to 1978 was compared. Almost all the infected aphids were killed byErynia neoaphidis Remaud. & Henn.,Conidiobolus obscurus (Hall & Dunn), Remaud. & Keller andEntomophthora planchoniana Cornu. A study of the distribution of the different species ofEntomophthoraceae during the year shows thatE. neoaphidis has the longest period of activity and infects most aphids. C. obscurus generally disappears in winter after an abundant formation of resting spores and reappears during the spring. On each sampling date,C. obscurus infects generally no more than 25% of the diseased aphids.E planchoniana occurs essentially during the summer and autumn on aphids living on ma?ze on which it seems to spread efficiently. On winter wheat the action ofE. neoaphidis andC. obscurus is different, depending on the species of aphid and on the position occupied by the aphids on the plant:E. neoaphidis is more pathogenic forM. dirhodum than forS. avenae andC. obscurus seems more pathogenic for the aphids (whatever the species) on leaves than for the aphids on ears. Finally the efficiency ofE. neoaphidis, C. obscurus andE. planchoniana relative to the size of the populations of the different samples was studied: the pathogenicity ofE. neoaphidis seems to be density independant, whereas the development ofC. obscurus in the colonies is slower than the rate at which they increase in size. Little is known about the pathogenicity ofE. planchoniana because of the lack of material. The prevalence ofE. neoaphidis is explained by its adaptation to the anholocycly of the aphids, by the broad spectrum of species it infects and by the numerous conidia it produces in a moist atmosphere. This species seems to have the best potential as an agent of biological control in cereal but currently its mass production poses problems.

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Avec la collaboration technique d'Augustine Gellé etSylvie Tanguy     

Studies on Entomophthora in populations of Aphis fabae on field beans

The population of Aphis fabae on field beans at a site in Highfield, Rothamsted in 1973 reached its peak 1 wk earlier than that at an equivalent site in Mill Dam Close, Woburn, 29 km NW of Rothamsted. Epizootics of Entomophthora caused weekly maximum mortalities of adult apterae of 71% at Highfield and 67% at Mill Dam Close. These epizootics and the periodicity of Entomophthora conidia in the air closely paralleled the development of the aphid population. There was little evidence of a consistent relationship between Entomophthora infection and any of the weather factors considered. At both sites most mortality was caused by E. planchoniana though many aphids were killed by E. aphidis and E. obscura. E. fresenii and E. virulenta killed very few aphids. Most conidia in the air were of the E. aphidis-type. Up to 44% of alatae emigrating from bean crops were infected with Entomophthora, confirming that aphid migration is an important means of distributing the fungi. Aphid numbers rose to more than 1600/plant at both sites, in spite of the action of Entomophthora, and would probably have been less had the fungi been more abundant earlier in the season.     

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.     

Facteurs de limitation des populations d'Aphis fabae dans l'ouest de la France III. Répartition et incidence des différentes espèces d'Entomophthora dans les populations

Résumé Plusieurs espèces d'Entomophthora participent à la régulation des populations d'Aphis fabae Scop. sur féverole dans l'Ouest de la France. Les r?les respectifs de chaque espèce ont été évalués en 1971 et de 1973 à 1975. Entomophthora fresenii Nowak. est l'espèce qui se dissémine le plus rapidement et le plus complètement dans les parcelles, et qui est la plus agressive au niveau des colonies. Ces deux caractères en font l'agent pathogène dominant d'A. fabae dans l'Ouest, 3 années d'observations sur 4.Entomophthora aphidis Hoffman, bien que présent tous les ans n'est le pathogène le plus efficace qu'en 1973.Entomophthora thaxteriana Petch etEntomophthora planchoniana Cornu n'apparaissent pas chaque année et, lorsqu'ils sont présents, n'interviennent que pour une faible part dans le développement des mycoses. Des facteurs inhérents à l'agent pathogène (spécificité, caractères du cycle) ainsi que des facteurs écologiques (climatiques) sont évoqués pour expliquer la prédominance d'E. fresenii.

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Summary Several species ofEntomophthora take part in the natural control ofAphis fabae Scop. on field beans (Vicia faba) in the West of France. The respective importance of each species was assessed in 1971 and from 1973 to 1975. Entomophthora fresenii Nowak. is the species that most completely and quickly spreads in the fields, and the most efficient in the colonies. For both reasonsE. fresenii is the main pathogen ofA. fabae in the West of France 3 years over 4. AlthoughEntomophthora aphidis Hoffman occurs every year, this species was the most efficient pathogen in 1973 only.Entomophthora thaxteriana Petch just occurred in 1974 and 1975 and, these years, its contribution in the total sum of infected aphids was low.Entomophthora planchoniana Cornu appeared in 1975 only, very late in the season, which makes its pathogenicity difficult to assess. Factors inherent to the pathogen (specificity ofE. fresenii, nature of its cycle, dependence of the aggregation of aphids) and ecological factors such as response to climate variations, may at least to a great extent explain the predominance ofE. fresenii. All these factors must be studied for a good understanding of this species.

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Les 2 premiers mémoires de cette étude ont été publiés dans Entomophaga respectivement parRobert et al. (18, 1973, 61–75) etRabasse & Robert (20, 1975, 49–63)     

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.     

Fungi attacking the blue-green lucerne aphid in New Zealand

Abstract

The blue-green lucerne aphid, Acyrthosiphon kondoi, is attacked on lucerne in New Zealand by the entomophthoraceous fungi Entomophthora aphidis and E. ignobilis (= E. thaxteriana). E. aphidis appeared to be the most pathogenic of the two species, causing an epizootic in one of the sampled fields which was severely infested by the aphid.