Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae)

Abstract. 1. A study of searching behaviour on wheat and host preference of Aphidius rhopalosiphi (DeStefani-Perez) is described.
2. Parasitoids divided their time equally between the leaves but spent very little time on the ear.
3. After contact with honeydew or an aphid host, parasitoids were arrested in a particular area and increased the time spent searching.
4. Aphids feeding on the ear were parasitized less successfully, since their position between the grains protected them from parasitoid attacks.
5. A.rhopalosiphi exhibited no preference for Metopolophium dirhodum (Walker) or Sitobion avenae (Fabricius), although the handling time for the latter was significantly longer; this resulted in fewer S.avenae being parasitized when it was abundant. Parasitoids did not switch between hosts in these experiments.
6. As a result of its searching behaviour, A.rhopalosiphi will encounter and parasitize M.dirhodum feeding on the leaves more frequently than S.avenae, which feeds on the ear. This will limit the parasitoid's ability to regulate populations of the cereal aphid S. avenae.     

Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability

Superparasitism avoidance by the endoparasitoid Aphidius rhopalosiphi De Stefani Perez on the grain aphid, Sitobion avenae was studied. Experiments were carried out in which aphids were exposed to two consecutive attacks by parasitoids. Results showed that superparasitism avoidance in A. rhopalosiphi was mediated by two successive stimuli whose effectiveness depended on the time interval between attacks. For short time intervals (<16 h), host rejections were mainly associated with the presence of dried cornicle secretion on the host's body which was exuded during the first attack. The repellency of this secretion declined with the time interval between attacks, becoming ineffective 2 days after the first parasitization, and allowed females to reject up to 30% of parasitized hosts. For longer time intervals (>/=16 h), host rejection behavior was a response of parasitoid females to internal changes in host quality associated with parasite development. This response gradually increased with an increase in time interval, reaching no more than 60%, 96 h after initial parasitization. This host discrimination ability did not allow females to distinguish between hosts parasitized by themselves or by conspecifics. Consequently, these findings suggest that superparasitism is a common event in A. rhopalosiphi and especially on recently parasitized hosts.     

Host specialization in habitat specialists and generalists

Generalists and specialists use different cues to find their habitat and essential resources. While generalists have the advantage of exploiting a wider range of resources, they are predicted to be less efficient in using one particular resource compared to specialists. The level of specialization of parasitoids can be either at the habitat or at the host level; strategies used by either type are expected to differ. We examined interactions between three aphid parasitoid species that are a habitat specialist Aphidius rhopalosiphi, a habitat generalist Aphidius ervi, and a host generalist Praon volucre on three cereal aphids, Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi. We compared total parasitism rate across behavioral and physiological variation in a non-choice test. Next, we addressed total parasitism in two phases to examine: (1) the response of parasitoids to different hosts through the behavioral sequence from antennation through oviposition, and (2) the physiological suitability of different hosts for oviposition and larval development. Parasitization typically involved the following behavioral steps: (1) antennal contact, (2) abdominal bending, and (3) ovipositor insertion (acceptance). A. rhopalosiphi had the same number of antennal contacts with the three aphids but showed fewer instances of abdominal bending towards R. padi. Pre-contact host preference was found for A. ervi but it did not correspond to the level of acceptance. The number of antennal contacts by P. volucre corresponded to the parasitization level of the aphid species but more mummies were produced on M. dirhodum than on R. padi. These results suggest that parasitoid species that are habitat specialists react similarly to the different host species present in the same habitat, whereas generalist species exhibit clear preferences during host selection. Preferences were, however, not always related to host suitability.     

Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey

Abstract. In Y-tube olfactometer tests, Aphidius ervi Hal., Trioxys sp., Praon sp., Aphelinus flavus (Nees), Lysiphlebus fabarum (Marsh.) and Aphidius rophalosiphi De Stef. responded positively to the odour of the plant on which aphid mummies containing them had been collected. The response to host plant odour was greater than the response to the odour of host aphids, their honeydew or a combination of the two. The strongest response was to a combination of plant and host aphids. A. rhopalosiphi showed a strong positive response to three wheat volatiles (cis-3-hexenyl acetate, cis-3-hexen-1-ol and trans-2-hexenal) as well as to indole-3-acetaldehyde (a breakdown product of tryptophan in aphid honeydew). In both olfactometer tests with odours and choice trials with whole plants, newly emerged A. rhopalosiphi distinguished and preferred the variety of wheat on which their development had occurred to other wheat varieties.     

Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae)

The role of winter diapause in two aphid parasitoid species, Aphidius ervi Haliday and Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae: Aphidiinae), in host synchronization and the induction of cold hardiness was investigated. Parasitoids were reared during three successive generations on Sitobion avenae Fabricius, at 15 degrees C under a photoperiod of 9 h light 15 h dark. Although these conditions are known to be strongly diapause inducing, neither parasitoids showed an incidence of diapause above 65% over the three generations; the rest of the population underwent quiescence. In both parasitoid species, diapausing mummies exhibited greater cold hardiness than non-diapausing mummies, resulting in significantly lower supercooling points (SCP) and in a higher survival rate during long-term exposures at 0 and -10 degrees C. The induction of increased cold hardiness in parasitoids was thus associated with the diapause state. SCPs of third instar larvae of S. avenae were similar to those of non-diapausing mummies of both parasitoid species, but significantly higher than those of diapausing mummies. The effect of winter climate on the stability of the host-parasitoid interaction is discussed.     

The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants

ABSTRACT. A Y-tube olfactometer was used to test the reactions of the hymenopteran cereal aphid parasitoids Aphidius uzbekistanicus Luzhetski and A. ervi Haliday to odours from aphids and their host plants. Only females responded to aphids but both sexes responded to plant odours. A. uzbekistanicus responded to the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Walker) whilst A. ervi , which has a broad host range, responded to M. dirhodum and the pea aphid, Acyrthosiphon pisum. Female A. uzbekistanicus responded to wheat leaves only but males responded to a range of plant material. Both male and female A. ervi responded to wheat and bean leaves. The failure of A. ervi to respond to either nettle aphids, Microlophium carnosum (Bukt.), or nettle leaves, despite its frequent parasitization of this aphid in the field, suggests the existence of more than one race of the parasitoid and casts doubts on the usefulness of alternative hosts as reservoirs for A. ervi in integrated control programmes. Males of both species responded to their respective females suggesting the presence of a sex specific attractant.     

Development of the aphid parasitoid,Aphidius ervi, in asexual and sexual females of the pea aphid,Acyrthosiphon pisum, and the blackberry-cereal aphid,Sitobion fragariae

The aphid parasitoid,Aphidius ervi Haliday, overwinters in larval diapause. The possibility that the parasitoid might prefer sexual (oviparae) rather than asexual females (virginoparae) as overwintering hosts (oviparae predominate in autumn when host numbers are generally declining) was tested by comparing these aphid morphs as potential hosts. Two host species were also examined, the pea aphid,Acyrthosiphon pisum (Harris), and the blackberry aphid,Sitobion fragariae (Walker). The parasitoids took longer to develop inS. fragariae than inA. pisum but the development of non-diapausingA. ervi was similar in sexual and asexual females. This observation, together with the greater variation in the duration of the different parasitoid stadia inS. fragariae, indicated that the parasitoid is specialized on the pea aphid. In photophases of 12 h and longer, the proportion ofA. ervi entering diapause inA. pisum oviparae was higher than in virginoparae. The critical daylength (where 50% of parasitoids entered diapause) was therefore longer in oviparae (12.6 h) than in virginoparae (11.7 h) with the inference that parasitoids developing in the oviparae would enter diapause earlier in the field. InS. fragariae, critical day-lengths were similar in both aphid morphs. The duration of diapause was unaffected by host morph and emergence in short days (10:14 L:D) occurred over a long period (c. 60 days).     

A physiologically based model of pest–natural enemy interactions

The population dynamic processes in aphids and mites are very similar, because the two groups show strong similarities in their biology. Resource limitation, density-dependent emigration and natural enemies are major factors controlling aphid and mite populations, but an assessment of their relative importance has proven difficult. We used a physiologically based simulation model to investigate the relative impact of the three factors on aphid pest populations. The present simulation model includes winter wheat, three aphid species, Metopolophium dirhodum (Wlk.), Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hom.: Aphididae) and three parasitoids, Aphelinus abdominalis Dalman (Hym.: Apheliniidae), Aphidius rhopalosiphi De Stefani-Perez and Praon volucre (Hal.) (Hym.: Aphidiidae). We derived and parameterized the model from literature data and validated it against independent field data. The study showed that resource limitation and density-dependent alate production restricts aphid numbers in the field. The mortality due to parasitoids increased late in the season and reduced the peak aphid numbers only moderately. The modelling approach we used is appropriate for simulating other pest–natural enemy systems, such as the spider mite–predatory mite system. Using an object-oriented modelling framework as a template, acarologists can now efficiently develop the simulation model of their choice. This revised version was published online in November 2006 with corrections to the Cover Date.     

Do past experience and competitive ability influence foraging strategies of parasitoids under interspecific competition?

Abstract 1. In solitary parasitoids, several species can exploit the same host patch and competition could potentially be a strong selective agent as only one individual can emerge from a host. In cereal crops, Aphidius rhopalosiphi and A. ervi share the grain aphid Sitobion avenae as host. 2. The present work studied foraging strategies of both species on patches already exploited by the other species. The study analysed larval competition in multi‐parasitised hosts and compared the foraging behaviour of females with and without previous experience. 3. It was found that A. ervi wins larval competition three times more often than A. rhopalosiphi. Both species spent less time on patches exploited by a heterospecific than on unexploited ones. When they foraged on heterospecifically exploited patches, experienced females induced less mortality in aphids than inexperienced ones. 4. Although A. rhopalosiphi is a specialist on cereal aphids and is the most abundant species due to its early appearance in the season, S. avenae is still a profitable host for A. ervi, because: (i) A. rhopalosiphi leaves patches partially exploited, (ii) A. ervi wins larval competition in three out of four multi‐parasitised hosts, and (iii) A. ervi is only slightly deterred by the cornicular secretions of the host and can thus easily parasitise hosts.     

Flying with a 'death sentence' on board: electrophoretic detection of braconid parasitoid larvae in migrating winged grain aphids, Sitobion avenae (F.)

Polyacrylamide gel electrophoresis of enzymes (carboxylesterases) was used for the first time to monitor rates of parasitism in airborne alate (winged) grain aphid, Sitobion avenae (F.) population samples collected by suction trapping in Hertfordshire, UK. Using previously described electrophoretic 'keys', the species of hymenopterous parasitoids present in individual aphids were identified and found to be Aphidius ervi (Haliday) and/or Aphidius rhopalosiphi (De Stephani Perez) (Braconidae). Entomophthoralean fungal infection was also detected using this approach. Aphidiid wasp parasitism was detected from early June to mid-August and fungal infection from late June to late July. The results are discussed in relation to parasitoid population structure and dynamics, especially (i) the fact that winged aphids passively transport the early stages of their braconid parasitoids and fungal pathogens, potentially to newly-founded colonies, which may directly impact on the dual aphid-parasitoid populations genetics; and (ii) the approach used to collect and assay parasitised and fungal infected aphids involving both suction trapping and electrophoretic testing may have potential in assessing the level and efficacy of these biological control agents in integrated pest management (IPM) schemes to combat cereal aphid outbreaks.     

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.     

Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies

Abstract.  1. Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Most parasitoid species have evolved specific adaptations to exploit a single host stage. However, females of the aphid hyperparasitoid Syrphophagous aphidivorus (Mayr) (Hymenoptera: Encyrtidae) display a unique and atypical oviposition behaviour by attacking either primary parasitoid larvae in live aphids, or parasitoid pupae in dead, mummified aphids.
2. In the laboratory, the correlation between host suitability and host preference of S. aphidivorus on the host Aphidius nigripes Ashmead parasitising the aphid Macrosiphum euphorbiae (Thomas) was investigated.
3. The relative suitability of the two host stages was determined by measuring hyperparasitoid fitness parameters (survival, development time, fecundity, sex ratio, and adult size of progeny), and calculating the intrinsic rate of population increase ( r _m). Host preference by S. aphidivorus females and the influence of aphid defence behaviour on host selection was also examined.
4. Hyperparasitoid offspring performance was highest when developing from hosts in aphid mummies and females consistently preferred this host to hosts in parasitised aphids. Although aphid defensive behaviour may influence host selection, it was not a determining factor. Ecological and evolutionary processes that might have led to dual oviposition behaviour in S. aphidivorus are discussed.     

Cereal aphid responses to sex pheromones and host-plant odours in the laboratory

Abstract. The movement of Sitobion fragariae (Wlk.) (Homoptera: Aphididae) males towards odours from conspecific sexual females (oviparae) and the aphid sex pheromone component (4a S ,7 S ,7a R )-nepetalactone were demonstrated in a linear-track olfactometer. Males of the closely related Sitobion avenae (Fab.) were attracted to odours from conspecific oviparae and also oviparae of S. fragariae. These results were consistent with the recent identification of this nepetalactone isomer as the major component of the sex pheromone in these species. Males of S.fragariae were not significantly attracted to oviparae of S.avenae. indicating some qualitative or quantitative difference in the pheromones of the two species. Males did not respond to the related (1R,4aS,7S,7aR)-nepetalactol or to host-plant odours. Gynoparae of these species moved towards the nepetalactone and also to host-plant odours. A combination of both stimuli was more attractive than plant odour alone. Gynoparae of S.fragariae also responded significantly to the combined treatment when this was tested against the nepetalactone.     

Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer

Host plant nutritional quality can directly and indirectly affect the third trophic levels. The aphid–parasitoid relationship provides an ideal system to investigate tritrophic interactions (as the parasitoids are completely dependent for their development upon their hosts) and assess the bottom up forces operating at different concentrations of nitrogen applications. The effects of varying nitrogen fertilizer on the performance of Aphidius colemani (V.) reared on Sitobion avenae (F.) and Aphidius rhopalosiphi (D.) reared on Rhopalosiphum padi (L.) were measured. Parasitism and percent emergence of parasitoids were positively affected by nitrogen fertilizer treatments while developmental duration (egg, larval, and pupal stages) was not affected by increasing nitrogen inputs. In males and females of both parasitoid species, adult longevity increased with the increasing nitrogen fertilizer. Hind tibia length and mummy weight of both parasitoid species increased with nitrogen fertilizer concentrations, as a result of larger aphids. This study showed that nitrogen application to the soil can have important consequences for aboveground multitrophic interactions.     

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.     

The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae

Mutualisms with facultative, non-essential heritable microorganisms influence the biology of many insects, and they can have major effects on insect host fitness in certain situations. One of the best-known examples is found in aphids where the facultative endosymbiotic bacterium Hamiltonella defensa confers protection against hymenopterous parasitoids. This symbiont is widely distributed in aphids and related insects, yet its defensive properties have only been tested in two aphid species. In a wild population of the grain aphid, Sitobion avenae, we identified several distinct strains of endosymbiotic bacteria, including Hamiltonella. The symbiont had no consistent effect on grain aphid fecundity, though we did find a significant interaction between aphid genotype by symbiont status. In contrast to findings in other aphid species, Hamiltonella did not reduce aphid susceptibility to two species of parasitoids (Aphidius ervi and Ephedrus plagiator), nor did it affect the fitness of wasps that successfully completed development. Despite this, experienced females of both parasitoid species preferentially oviposited into uninfected hosts when given a choice between genetically identical individuals with or without Hamiltonella. Thus, although Hamiltonella does not always increase resistance to parasitism, it may reduce the risk of parasitism in its aphid hosts by making them less attractive to searching parasitoids.     

Electrophoretic 'keys' for the identification of parasitoids (Hymenoptera: Braconidae: Aphelinidae) attacking Sitobion avenae (F.) (Hemiptera: Aphididae)

Polyacrylamide gel electrophoresis was used to construct electrophoretic 'keys' for identifying larval, pupal and adult hymenopterous parasitoids of Sitobion avenae (F.). In general, for each parasitoid and enzyme system tested, all life stages gave similar banding patterns. Although five enzyme systems were tested, esterase was found to be the most useful single system. Using laboratory-reared parasitoids and staining for esterase activity, all species examined, except Aphidius rhopalosiphi and A. ervi could be readily distinguished with the aid of the appropriate key.     

Parasitoids and biocontrol of Russian wheat aphid, Diuraphis noxia (Kurdj.) expanding in central Europe

Hymenopterous parasitoids found on the Russian wheat aphid (RWA), Diuraphis noxia (Kurdj.) since the aphid was detected in the Czech Republic in 1995 have been studied. Parasitoids were obtained from aphid samples taken in small grains and from field exposures of banker-units containing laboratory mass-reared RWA. The parasitoid species are listed. Their presence on RWA was verified and their host species alternation was also tested in the laboratory. Evidence on some species was obtained only through unnatural host propagation. Aphidius colemani Vier. (a Chilean strain) was purposely introduced, released and became established; its host range, which included both target and non-target species, is listed. Prediction versus determination of RWA parasitoid complex in central Europe are discussed and the field samples and the exposure trials are compared. The RWA presence in relation to biodiversity in the small-grains agroecosystem is analysed. An overall parasitoid spectrum of RWA in the Old World (and the world background) is reviewed in relation to the RWA native range and the distribution (expansion) range, respectively. A corresponding analysis of the central European situation, derived from the expansion route of RWA to the Mediterranean, is presented.     

Winter host exploitation influences fitness traits in a parasitoid

Organisms can either evade winter's unfavourable conditions by migrating or diapausing, or endure them and maintain their activities. When it comes to foraging during winter, a period of scarce resources, there is strong selective pressure on resource exploitation strategy. Generalist parasitoids are particularly affected by this environmental constraint, as their fitness is deeply linked to the profitability of the available hosts. In this study, we considered a cereal aphid–parasitoid system and investigated (1) the host–parasitoid community structure, host availability, and parasitism rate in winter, (2) the influence of host quality in terms of species and instars on the fitness of the aphid parasitoid Aphidius rhopalosiphi De Stefani‐Perez (Hymenoptera: Braconidae: Aphidiinae), and (3) whether there is a detectable impact of host fidelity on parasitism success of this parasitoid species. Host density was low during winter and the aphid community consisted of the species Rhopalosiphum padi L. and Sitobion avenae Fabricius (both Hemiptera: Aphididae), both parasitized by A. rhopalosiphi at non‐negligible rates. Aphidius rhopalosiphi produced more offspring when parasitizing R. padi compared with S. avenae, whereas bigger offspring were produced when parasitizing S. avenae. Although aphid adults and old larvae were significantly larger hosts than young larvae, the latter resulted in higher emergence rates and larger parasitoids. No impact of host fidelity on emergence rates or offspring size was detected. This study provides some evidence that winter A. rhopalosiphi populations are able to take advantage of an array of host types that vary in profitability, indicating that host selectivity may drop under winter's unfavourable conditions.     

Increased Parasitization of Aphids on Trap Plants Alongside Vials Releasing Synthetic Aphid Sex Pheromone and Effective Range of the Pheromone

Aphid-infested cereal trap plants were used to detect the effects of aphid sex pheromone components on aphid parasitoid activity in arable field margins. The presence of aphid sex pheromones significantly increased parasitization levels by aphid parasitoids on the plants. By placing plants alongside and at varying distances away from a pheromone-releasing vial, the technique was used to measure the distance over which a point source of aphid sex pheromone could increase parasitization levels. Pheromone-releasing vials significantly increased parasitization by the generalist parasitoid Praon volucre on plants adjacent to vials and on plants placed 20 cm away. When the distance between pheromone-releasing vials and aphid-infested plants was increased to 1 m, parasitization by P. volucre was increased only on the plant adjacent to the vial, whereas parasitization by the specialist parasitoid Aphidius rhopalosiphi was also increased on plants placed 1 m away. This indicates a possible difference between the parasitoids in their foraging behaviour in response to semiochemical cues during host selection. When the experiment was repeated with some trap plants placed 3 m away from the pheromone-releasing vial, parasitization was again concentrated on plants directly alongside the vial, but only P. volucre appeared to be active in the field at the time of this experiment, so the effect on A. rhopalosiphi could not be assessed. The results are encouraging for the prospects of using aphid sex pheromones to manipulate parasitoids in order to improve aphid population control.