Biology of Aphidius rhopalosiphi, a parasitoid of cereal aphids

Summary Aphidius rhopalosiphi produced 212 offspring on average but in one case 509 deposited eggs were found. Superparasitization occurred but the frequency distribution of parasitoid larvae in aphids differed significantly from random, indicating a certain degree of host discrimination. Average life span of adults was 13.1 days and sex ratio was 1:1. It changed in time among successively produced offspring.Handling time was about 2 sec and was somewhat longer in the fourth instar than in the second. Second and third aphid instars were preferred for oviposition. Functional response was sigmoid and at an aphid density of 100 aphids per cage percentage parasitization decreased.

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Résumé Nous avons examiné quelques aspects des relations entre le parasitoïde Aphidius rhopalosiphi et son hôte Sitobion avenae. La fécondité potentielle à l'émergence (144 ufs) était inférieure à la fécondité réalisée: nombre de pucerons momifiés (212). La plupart des ufs étaient pondus dans la première semaine de la vie imaginale (fig. 1). Le super-parasi-tisme s'est produit dans les conditions expérimentales, mais la distribution des larves (fig. 2) s'écartait souvent de la distribution au hasard, ce qui indiquait une certaine discrimination parmi les hôtes.La longévité moyenne était de 13,1 jours et le maximum de 23 jours. Le taux sexuel (fig. 3) pour l'ensemble de la descendance était 1/1, mais changeait dans le temps. Après le premier jour de ponte, plus de femelles que de mâles étaient obtenues; mais après 6 jours, il n'y avait presque plus que des mâles.Le taux de rencontre des aphides et des parasitoïdes augmentait avec la taille (fig. 4a). Le temps de prospection de l'hôte était en moyenne de 2 secondes, mais dans certains cas il atteignait 10 secondes ou plus. La proportion de rencontres efficaces était plus faible au 4ème stade (fig. 4b). Il n'y avait pas de différence significative dans le nombre de larves de parasitoïdes obtenues par rencontre pendant les stades 1 à 3 des pucerons, mais elle était significativement inférieure au 4ème stade par rapport au second. Les taux globaux de succès (taux de rencontre et nombre de larves formées par rencontre) étaient plus élevés aux 2ème stades des pucerons. La réponse fonctionnelle était sigmoïde (fig. 5).

     

Development of selective aphicide treatments for integrated control of summer aphids in winter wheat

Field experiments on the use of recommended and reduced application rates of aphicides for control of summer aphid infestations on winter wheat have been done at five sites each year from 1990 to 1992. The experiment compared sprays of pirimicarb at recommended rate (140g a.i. ha^-1) and reduced rate (25 g a.i. ha^-1) and of alphacypermethrin at recommended rate (15 g a.i. ha^-1) and one third recommended rate (5 g a.i. ha^-1), each applied either at flag leaf emergence or at flowering. Aphid infestations were allowed to develop naturally and were measured at critical growth stages. In 1990, overwintered aphid infestations, together with established populations of parasitoids, were detected at four of the five sites when the first assessment was made in April. Parasitoids provided sufficient aphid control to prevent yield loss at two sites, without pesticide applications. At three sites both aphicides gave similar levels of control and yield response at both recommended and reduced application rates. In 1991 and 1992 no overwintered aphids were detected in the crops and aphid infestations developed much later. Aphicide applications gave significant yield responses at four sites in 1992. Recommended rates gave better control of aphids than reduced rates. There was no significant difference in the yield response obtained with different rates of aphicide.     

Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid

We examine the effects of fecundity‐limited attack rates and resistance of hosts to parasitism on the dynamics of two‐host–one‐parasitoid systems. We focus primarily on the situation where one parasitoid species attacks two host species that differ in their suitability for parasitism. While all eggs allocated to suitable hosts develop into adult parasitoids, some of the eggs allocated to marginal host do not develop. Marginal hosts can therefore act as a sink for parasitoid eggs. Three‐species coexistence is favoured by low levels of parasitoid fecundity and by low levels of suitability of the marginal host. Our model also produces an indirect (+, ?) interaction in which the suitable host can benefit from the presence of the marginal host, but the marginal host suffers from the presence of the suitable host. The mechanism driving the indirect (+, ?) interaction is egg limitation of parasitoids incurred by allocating eggs to marginal hosts.     

The effects of organic and conventional fertilizers on cereal aphids and their natural enemies

• 1 Aphids are important pests of spring cereals and their abundance and the impact of their natural enemies may be influenced by fertilizer regime.
• 2 We conducted a 2‐year field study investigating the effects of organic slow‐release and conventional fertilizers on cereal aphids, hymenopteran parasitoids and syrphid predators and considered how the effects of fertilizers on barley morphology and colour might influence these species.
• 3 Barley yield was greater in conventionally fertilized pots. Barley morphology was also affected by treatment: vegetative growth was greater under conventional treatments. Barley receiving organic fertilizers or no fertilizer was visually more attractive to aphids compared with plants receiving conventional fertilizers.
• 4 Aphids were more abundant in conventionally fertilized barley but the reason for this increased abundance was species specific. Metopolophium dirhodum was responding to fertilizer effects on plant morphology, whereas Rhopalosiphum padi was sensitive to the temporal availability of nutrients.
• 5 Syrphid eggs were more numerous in conventionally fertilized pots, whereas the response of parasitoids appeared to be dependent on the abundance of aphids, although the number of parasitoid mummies was low in both years.
• 6 This research shows that the fertilizer treatment used can affect numerous characteristics of plant growth and colour, which can then influence higher trophic levels. This knowledge might be used to make more informed fertilizer application choices.

     

Plant virus and parasitoid interactions in a shared insect vector/host

Interactions between barley yellow dwarf luteovirus (BYDV) and the aphid parasitoid, Aphidius ervi Haliday (Hymenoptera: Aphidiidae), were investigated while sharing the vector/host, Sitobion avenae (F.) (Homoptera: Aphididae). Aphids, which were parasitized during their second larval stadium, had access to virus-infected plants before, immediately after, or several days after parasitoid attack. The larval development of A. ervi in S. avenae was significantly delayed when virus acquisition took place before or shortly after the parasitoid had hatched, but not when the parasitoid was at the second larval stage during virus acquisition. Similarly, the presence of BYDV led to a significantly higher aphid mortality when they acquired virus up to and including the time that A. ervi was at the first larval stage. Adult female parasitoids deposited fewer eggs in viruliferous aphids. Virus transmission was not reduced by parasitization, and in some experiments aphids which were subjected to parasitoid attack transmitted BYDV more efficiently than unattacked insects.     

Quantifying the impact of polyphagous invertebrate predators in controlling cereal aphids and in preventing wheat yield and quality reductions

Exclusion barriers were used to manipulate numbers of polyphagous invertebrate predators so that their impact on cereal aphids and consequently wheat yield and quality could be examined. Experiments were conducted within the framework of the LINK Integrated Farming Systems Project which allowed comparisons to be made between the integrated and conventional farming systems under examination on a study farm in Hampshire, UK. Only in 1995 were the numbers of aphids per tiller, the aphid peak and rate of increase to the peak significantly greater in the exclusion areas where the density of polyphagous predators had been reduced. The maximum increase in aphids as a result of excluding polyphagous predators was 31%, which was equivalent to 130 aphid days. However, the polyphagous predators did not reduce the number of tillers infested. The relatively low impact of polyphagous predators was attributed to the aphid population phenology and greater effects may have been found had aphids infested the crops earlier in their development. Sowing date was shown to govern the time over which a crop may be susceptible to yield loss from aphids, with later-drilled crops being more susceptible to late-summer aphid infestations. Aphid numbers rarely affected grain yield but were found to be related to some grain quality parameters, but reducing polyphagous predators had no direct impact on grain yield or quality even where the aphid burden increased. The peak period of activity and density differed between the species of Carabidae, Staphylinidae and Araneae consequently influencing their relationship with the aphids. Some negative correlations were found between these groups of polyphagous predators and aphids. Species composition and abundance differed between fields thereby influencing the level of aphid predation. The exclusion barriers were most effective at reducing numbers of Carabidae although numbers of Staphylinidae and Araneae were also reduced. The consequences for Integrated Crop Management are discussed.     

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.     

Changes in activity of superoxide dismutase and catalase within cereal aphids in response to plant o-dihydroxyphenols

Abstract:  Superoxide dismutase and catalase activity was found in the bird cherry-oat aphid, Rhopalosiphum padi (L.) and the grain aphid, Sitobion avenae (F.). Among the aphid morphs studied, the highest activity of the antioxidant enzymes was noted for winged adults (alatae) and the lowest for wingless (apterae) ones. Higher activity of superoxide dismutase and catalase was observed in the polyphagous species R. padi that alternates between woody host plants and grasses. On some ocassions, activity of superoxide dismutase in cereal aphids was increased by twofold, when aphids were exposed to toxic plant o -dihydroxyphenols. An opposite tendency was observed in case of activity of the catalase that was strongly reduced within body of phenolics-treated insects. Among the plant allelochemicals studied, caffeic acid showed the strongest effect on the activity of the antioxidant enzymes of the cereal aphids. The experiments carried out indicate that antioxidant enzymes might play an important role in interactions between cereal aphids and their host plants.     

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.     

Prevalences of fungal pathogens and othernatural enemies of cereal aphids (Homoptera:Aphididae) in wheat under dryland and irrigatedconditions in South Africa

Surveys were conducted in the summer andwinter rainfall wheat producing regions of SouthAfrica in a first attempt to investigate theidentity and impact of entomopathogenic fungi withinthe cereal aphid complex. Wheat produced underdryland and irrigated conditions was surveyed duringthe 1996 and 1997 seasons. Six cereal aphid specieswere recorded of which the Russian wheat aphid, Diuraphis noxia, was the most abundantunder dryland conditions in the summer rainfallregion as opposed to the oat aphid, Rhopalosiphum padi, in the winter rainfallregion. Rose grain aphid, Metopolophiumdirhodum, was most prevalent underirrigated conditions in the summer rainfall region.Five species of entomopathogenic fungi were recordedincluding four entomophthorales and the hyphomycete,Beauveria bassiana. TheEntomophthorales included Pandora neoaphidis, Conidiobolus obscurus, C.thromboides, and Entomophthoraplanchoniana. Pandora neoaphidis wasthe most important etiological agent recorded fromD. noxia, with up to 50% mycosis recordedunder dryland conditions in the Bethlehem summerrainfall region. Similarly, P. neoaphidis wasthe most prevalent species within populations ofM. dirhodum. under irrigated conditions in theBergville/Winterton summer rainfall region (up to77% mycosis). However, mycoses of R. padi didnot exceed 1.7% in samples from these areas,suggesting that R. padi may be lesssusceptible to P. neoaphidis than M.dirhodum. Epizootics in populations of D.noxia under dryland conditions in both the winterand summer rainfall regions indicated a high levelof susceptibility to P. neoaphidis.Occurrences of hymenopterous parasitoids andpredators in populations of D. noxia were low,although a parasitism level of 25% was recorded inone small sample of R. padi collected from anirrigated field in the summer rainfall region.     

Population dynamics of cereal aphids: influence of a shared predator and weather

1 Aphid populations may show strong year-to-year fluctuations, but questions remain regarding the dominance of factors that cause this variation, especially the role of natural enemies. To better understand the dynamics of aphid species that occur as pests in cereals, we investigated the relative influence of top-down control by a predator and weather (temperature and precipitation) on population fluctuations of three cereal aphid species.
2 From 1987 to 2005, populations of Metopolophium dirhodum , Sitobion avenae and Rhopalosiphum padi in insecticide-free stands of winter wheat were monitored in the Praha-Ruzyné region of the Czech Republic. Densities of an aphidophagous predator, the ladybeetle Coccinella septempunctata , were recorded from an overwintering site in the landscape. Weather was quantified using historical records.
3 A significant bottom-up effect of densities of aphids on those of C.   septempunctata was found, but evidence of direct top-down regulation of aphids by C.   septempunctata was only significant in the case of R.   padi . There was no significant periodicity in the dynamics of the aphid or C.   septempunctata , suggesting that there was no clear predator-prey cycle. Combinations of C.   septempunctata and weather variables could be used to explain M.   dirhodum and R.   padi per capita rate of change. There were also indications that weather directly affected peak density of M.   dirhodum .
4 We conclude that regional estimates of C.   septempunctata densities are not sufficient to determine whether aphid population dynamics are driven by predator–prey interactions. Feasibility of time series analysis as an investigative tool in aphid population dynamics studies is discussed.     

A defensive endosymbiont fails to protect aphids against the parasitoid community present in the field

1. The value of protective mutualisms provided by some facultative endosymbionts has been well demonstrated in the laboratory, yet only recently has their effectiveness in the field been studied. ‘Candidatus Hamiltonella defensa’ is known to defend aphids from parasitoid wasps in laboratory trials. However, the efficacy of this defence varies among parasitoids, suggesting that protection will vary spatially and temporally depending on parasitoid community composition. 2. This demonstrated specificity and a dearth of studies on Hamiltonella in the field prompted the authors to quantify parasitism rates of Hamiltonella‐infected and ‐uninfected Aphis craccivora Koch aphid colonies in a manipulative field study. 3. It was found that A. craccivora in central Kentucky alfalfa were parasitised by Lysiphlebus testaceipes (Cresson) and Aphelinus sp. Surprisingly, Hamiltonella infection did not lower successful parasitism by the naturally occurring parasitoid wasps. Whether Hamiltonella was effective against L. testaceipes was subsequently tested in a controlled laboratory assay, and no effect on parasitism rate was found. 4. This study emphasises the fact that defensive symbionts sometimes provide no tangible defensive benefits under field conditions, depending on parasitoid community composition. It is hypothesised that the protective mutualism may be beneficial in geographically localised areas. When the symbiosis is effective against a local parasitoid community, aphid clones may experience eruptive population growth and rapidly disperse across a large area, allowing spread to habitats with different parasitoid communities where the mutualism is an ineffective defence.     

Intercropping impacts the host location behaviour and population growth of aphids

Increasing intrafield plant diversity has been shown to regulate pest populations in various agroecosystems. Among the suggested mechanisms for this bottom-up pest control, the disruptive crop hypothesis states that herbivores' abilities to locate and colonize their host plants are reduced by the presence of non-host plants. Under laboratory conditions, we evaluated how intercropping wheat and legumes modifies the behaviour of apterous cereal aphids, Sitobion avenae (Fabricius) (Hemiptera: Aphididae), in terms of host plant location and population growth. We compared two intercropping systems – soft winter wheat, Triticum aestivum L. (Poaceae), associated with winter pea, Pisum sativum L., or with white clover, Trifolium repens L. (both Fabaceae) – and sole stands of soft winter wheat. Aphids needed more time to locate their wheat host plant and then spent less time on wheat when it was intercropped with clover. At the population level, and accounting for host plant biomass, only intercropping wheat with clover significantly reduced aphid densities on wheat, as this was particularly disruptive to S. avenae behaviour and population growth. Our laboratory study points out that the species used as non-host plants and their density are important parameters that should be taken into account in field studies on intercropping systems.     

Spatial patterns and sampling plans for cereal aphids [Hom.: Aphididae] killed by entomophthoralean fungi and hymenopterous parasitoids in spring wheat

Cereal aphids infesting spring wheat in southwestern Idaho were surveyed during 1988 and 1989 for the presence of entomophthoralean fungi and hymenopterous parasitoids. Cereal aphids killed by the fungi (cadavers) and parasitoids (mummies) includedDiuraphis noxia (Mordvilko),Metopolophium dirhodum (Walker),Sitobion avenae (F.), andSchizaphis graminum (Rondani). Taylor's power law was used to describe the relationships between mean densities of cadavers or mummies (number per tiller) and associated variances. Except forS. graminum mummies, which were at low levels throughout the growing seasons and tended to be randomly distributed, Taylor's slopes exceeded 1.0 for all the aphid cadavers and mummies, indicating varying degrees of clumping in spatial pattern. The spatial patterns ofD. noxia andM. dirhodum cadavers were similar, simply reflecting those of their own populations, but more aggregated than were their respective mummies resulting from parasitoid attack. The intercepts and slopes from the power law analysis were used to generate functional relationships between the proportion of wheat tillers bearing cadavers or mummies of each aphid species and the mean density, and develop optimal numerical (direct counting) and binomial (presence or absence) sample size curves for both cadavers and mummies of each aphid species.      

Forecasting migration of cereal aphids (Hemiptera: Aphididae) in autumn and spring

The migration of cereal aphids and the time of their arrival on winter cereal crops in autumn and spring are of particular importance for plant disease (e.g. barley yellow dwarf virus infection) and related yield losses. In order to identify days with migration potentials in autumn and spring, suction trap data from 29 and 45 case studies (locations and years), respectively, were set‐off against meteorological parameters, focusing on the early immigration periods in autumn (22 September to 1 November) and spring (1 May to 9 June). The number of cereal aphids caught in a suction trap increased with increasing temperature, global radiation and duration of sunshine and decreased with increasing precipitation, relative humidity and wind speed. According to linear regression analyses, the temperature, global radiation and wind speed were most frequently and significantly associated with migration, suggesting that they have a major impact on flight activity. For subsequent model development, suction trap catches from different case studies were pooled and binarily classified as days with or without migration as defined by a certain number of migrating cereal aphids. Linear discriminant analyses of several predictor variables (assessed during light hours of a given day) were then performed based on the binary response variables. Three models were used to predict days with suction trap catches ≥1, ≥4 or ≥10 migrating cereal aphids in autumn. Due to the predominance of Rhopalosiphum padi individuals (99.3% of total cereal aphid catch), no distinction between species (R. padi and Sitobion avenae) was made in autumn. As the suction trap catches were lower and species dominance changed in spring, three further models were developed for analysis of all cereal aphid species, R. padi only, and Metopolophium dirhodum and S. avenae combined in spring. The empirical, cross‐classification and receiver operating characteristic analyses performed for model validation showed different levels of prediction accuracy. Additional datasets selected at random before model construction and parameterization showed that predictions by the six migration models were 33–81% correct. The models are useful for determining when to start field evaluations. Furthermore, they provide information on the size of the migrating aphid population and, thus, on the importance of immigration for early aphid population development in cereal crops in a given season.     

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.