The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression

Intraguild predation (IGP) occurs when consumers competing for a resource also engage in predatory interactions. A common type of IGP involves aphid predators and parasitoids: since parasitoid offspring develop within aphid hosts, they are particularly vulnerable to predation by aphid predators such as coccinellid beetles. Other intraguild interactions that include non-lethal behavioral effects, such as interference with foraging and avoidance of IGP, may also hamper parasitoid activity and reduce their effectiveness as biological control agents. In this study, we quantified mortality in and behavioral effects on Aphidius colemani Viereck (Hymenoptera: Aphidiidae) by its IG-predator Coccinella undecimpunctata L. (Coleoptera: Coccinellidae), and compared the impact of two release ratios of these natural enemies on aphid populations. Parasitoids did not leave the plant onto which they were first introduced, regardless of the presence of predators, even when alternative prey was offered on predator-free plants nearby. In 2-hour experiments, predator larvae interfered with wasp activity, and the level of aphid parasitism was lower in the presence of predators than in their absence. In these experiments, the parasitoids contributed more to aphid mortality than the predators and aphid suppression was higher when a parasitoid acted alone than in combination with a predator larva. These results were confirmed in a 5-day experiment, but only at one parasitoid:predator release ratio (4:3) not another (2:3). The over-all impact on aphid population growth was non-the-less stronger when both enemies acted together than when only one of them was present. Results indicate that for given release ratios and time scale, the negative lethal and non-lethal effects of the predator on parasitoid performance did not fully cancelled the direct impact of the predator on the aphid population.     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers

Interaction between a predator and a parasitoid attacking ant-attended aphids was examined in a system on photinia plants, consisting of the aphid Aphis spiraecola, the two ants Lasius japonicus and Pristomyrmex pungens, the predatory ladybird beetle Scymnus posticalis, and the parasitoid wasp Lysiphlebus japonicus. The ladybird larvae are densely covered with waxy secretion and are never attacked by attending ants. The parasitoid females are often attacked by ants, but successfully oviposit by avoiding ants. The two ants differ in aggressiveness towards aphid enemies. Impacts of the predator larvae and attending ant species on the number of parasitoid adults emerging from mummies per aphid colony were assessed by manipulating the presence of the predator in introduced aphid colonies attended by either ant. The experiment showed a significant negative impact of the predator on emerging parasitoid numbers. This is due to consumption of healthy aphids by the predator and its predation on parasitized aphids containing the parasitoid larvae (intraguild predation). Additionally, attending ant species significantly affected emerging parasitoid numbers, with more parasitoids in P. pungens-attended colonies. This results from the lower extent of interference with parasitoid oviposition by the less aggressive P. pungens. Furthermore, the predator reduced emerging parasitoid numbers more when P. pungens attended aphids. This may be ascribed to larger numbers of the predator and the resulting higher levels of predation on unparasitized and parasitized aphids in P. pungens-attended colonies. In conclusion, a negative effect of the predator on the parasitoid occurs in ant-attended aphid colonies, and the intensity of the interaction is affected by ant species.     

Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure

In this study we examined the influences that differing life history strategies and population structures at the time of pesticide exposure have on population susceptibility to pesticides. We used life table data and a matrix projection model to incorporate combinations of mortality (lethal effect) and reductions in fecundity (sublethal effect) into estimates of intrinsic population growth rates (r) for a predator, the seven-spot lady beetle, Coccinella septempunctata L., and its prey, the pea aphid, Acyrthosiphon pisum Harris, and an aphid parasitoid, Diaeretiella rapae (M’Intosh). All three species exhibited differences in key life history variables. The aphid had the highest r and shortest generation time, the ladybeetle had the lowest r and longest generation, while the parasitoid exhibited intermediate life history characteristics. When the model was run with populations started as neonates (aphids) or eggs (lady beetle, parasitoid) for each species, ladybeetle populations were much more susceptible than either aphid or parasitoid populations 30 days after simulated exposure to a pesticide. For example, 50% mortality and a 50% reduction in fecundity resulted in a population headed toward extinction (negative r) for the ladybeetle while the parasitoid population grew exponentially (positive r) even after sustaining 70% mortality and a 70% reduction in fecundity. The aphid species maintained exponential growth after sustaining 80% mortality and an 80% reduction in fecundity. Thus, differences in life history variables accounted for the greater susceptibility of the ladybeetle to a pesticide than its aphid prey or the parasitoid over a set time interval. These differences in susceptibility were greatly reduced when the model was run starting with a mixed age/stage population (the stable age distribution) for each species indicating that population structure at the time of pesticide exposure plays a critical role in population susceptibility. These results suggest that life history attributes as well as population structure at the time of pesticide exposure both play a major role in population susceptibility to pesticides, highlighting the need to explicitly consider differences in life history variables among species when calculating compatibility of pesticides and biological control agents as well as the population structure of beneficial species at the time of pesticide application.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.     

Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi （Hymenoptera： Aphidiinae）

Intraguild predation （IGP） can be an important factor influencing the effective- ness of aphid natural enemies in biological control. In particular, aphid parasitoid foraging could be influenced by the presence of predators. This study investigated the effect of larvae of the predatory hoverfly Episyrphus balteatus DeGeer （Diptera： Syrphidae） and the multicolored Asian ladybird Harmonia axyridis Pallas （Coleoptera： Coccinellidae） on the foraging behavior of the aphid parasitoid, Aphidius ervi Haliday （Hymenoptera： Aphidiidae） in choice experiments using a leaf disc bioassay. Wasp response to chemical tracks left by those predator larvae was also tested. Parasitoid behavior was recorded using the Observer （Noldus Information Technology, version 5.0, Wageningen, the Netherlands）. The experiments were conducted under controlled environmental conditions using leaves of the broad bean plant, Viciafaba L. （Fabaceae） with Myzus persicae Sulzer （Homoptera： Aphididae） as the host complex. A. ervi females avoided aphid patches when larvae of either predator were present. A similar avoidance response was shown by A. ervi to aphid patches with E. balteatus larval tracks, whereas no significant response was observed to tracks left by H. axyridis larvae. It was concluded that IG predator avoidance shown by the aphid parasitoid A. ervi may be a factor affecting their distribution among host patches.     

Effect of host plant,prey species and intergenerational changes on the prey preferences of the predatory mirid <Emphasis Type="Italic">Macrolophus caliginosus</Emphasis>

The outdoor establishment of non-native biocontrol agents released for inundative control of glasshouse pests is determined primarily by two factors: ecophysiological compatibility with local climate, particularly winter cold tolerance, and ability to locate and utilise wild prey. Observations on the number and diversity of acceptable wild prey as part of an assessment of establishment potential therefore overlap with more focused studies to determine host range. This study investigated two aspects of the interactions between biocontrol agents and non-target prey that are rarely considered in tests for establishment or host range: the role of different host plant–prey associations in modifying the development and reproduction of biocontrol agents, and the longer term sustainability of such relationships beyond the single generation observed in most laboratory studies. Using the glasshouse whitefly (Trialeurodes vaporariorum) predator Macrolophus caliginosus Wagner (Hemiptera: Miridae) as a case study, the mirid was able to sustain viable populations over three generations on the related cabbage whitefly Aleyrodes proletella (Linnaeus) (Hemiptera: Aleyrodidae) and the aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae), including when these prey were feeding on different host plants (Chinese cabbage, cabbage and Brussels sprout). However, the rate of development, fecundity and mortality of the predator varied between the different prey and host plant combinations, and in all cases differed than when feeding on its glasshouse prey T. vaporariorum reared on tobacco (Nicotiana tabacum). The results are discussed in the light of the current debate on methods for conducting host range testing as part of an environmental risk assessment. Handling Editor: Dirk Babendreier     

Effect of wheat resistance, the parasitoid Aphidius rhopalosiphi, and the entomopathogenic fungus Pandora neoaphidis, on population dynamics of the cereal aphid Sitobion avenae

The influence of wheat (Triticum aestivumL.) resistance, the parasitoid Aphidius rhopalosiphiDe Stephani-Perez (Hymenoptera: Braconidae) and the entomopathogenic fungus Pandora neoaphidis(Remaudière et Hennebert) Humber (Zygomycetes: Entomophthorales) on the density and population growth rate of the cereal aphid Sitobion avenae(F.) (Hemiptera: Aphididae) was studied under laboratory conditions. Partial wheat resistance was based on hydroxamic acids, a family of secondary metabolites characteristic of several cultivated cereals. The partial resistance of wheat cultivar Naofén, the action of the parasitoid and the joint action of the parasitoid and fungus, reduced aphid density. The lowest aphid densities were obtained with the combination of the parasitoid and the fungus, but wheat resistance under these circumstances did not improve aphid control. Significant reductions of population growth rate (PGR) of aphids were obtained with the joint action of wheat resistance and natural enemies. In particular, the combined effects of parasitoids and fungi showed significantly lower PGR than the control without natural enemies in both wheat cultivars. Our results support the hypothesis that wheat resistance and the utilization of biological control agents could be complementary strategies in an integrated pest management program against cereal aphids.     

Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii

Colonization of tomato greenhouses by native predatory mirid bugs at the end of the spring cycle is common in the western Mediterranean area when no broad-spectrum insecticides are applied. Due to their polyphagy, these predators interact with pest populations and also with other natural enemies present in the crop. In this work we evaluate the abundance and timing of greenhouse colonization by these predators and their interaction with the greenhouse whitefly Trialeurodes vaporariorum, a key crop pest, and its introduced parasitoid Encarsia formosa. Although quite unpredictable, natural colonization of greenhouses by Macrolophus caliginosus and Dicyphus tamaninii, the two predominant species in our location, usually leads to the establishment of predator populations in the crop that subsequently prey on greenhouse whitefly. No preference for parasitized pupae was observed in greenhouse samples, while laboratory experiments revealed a marked tendency to avoid parasitoid pupae. In our area, IPM programs for greenhouse tomatoes and other vegetables should take advantage of the presence of this predator complex by allowing the immigration and establishment of its populations without disturbing them with highly toxic and non-selective insecticides.     

Efficacy of multiple biocontrol agents against the sweet potato whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on tomato

Abstract: Biological control provides an environmentally harmonious and potentially stable management tactic to combat noxious pests such as Bemisia tabaci, notorious for its resistance to synthetic pesticides. Bioassays conducted under control chamber conditions integrating applications of the parasitoid Encarsia formosa, reared for 20 years on Trialeurodes vaporariorum, and the fungus Verticillium lecanii on the third‐fourth instar nymphs of B. tabaci on tomato, showed a comparable effect between the parasitoid‐fungus combined treatment and the fungus treatment alone (70.7% vs. 70.4%). Analysis of our results indicates antagonism between the two biocontrol agents related to the parasitoids’ ability to discriminate between infected and healthy B. tabaci nymphs. The parasitoid treatment alone produced 36.3% mortality, with no mortality in the distilled water controls. The behavioural performance of the parasitoid could have either genetic or environmental causes. Bioassays studying the feeding habit of the imported mirid predator Macrolophus caliginosus (adults) and the indigenous mirid Camptotylus reuteri (nymphs and adults) on eggs, or early second instar nymphs of B. tabaci, and choice preference tests indicated a significant difference in feeding between M. caliginosus and C. reuteri. There was no significant difference in percentage feeding of M. caliginosus on eggs (2.2%) or second instar nymphs (8.0%). There was a significant difference in feeding of M. caliginosus adults (18.6%) when offered eggs and second instars in the same arena compared with eggs or second instars offered separately. These results could be attributed to the biological behaviour of the predator having a type III functional response. Studies with the local C. reuteri species showed no significant difference in adult and nymphal consumption on second instars of B. tabaci compared with nymphs on eggs. However, C. reuteri adults fed less on eggs compared with nymphs. This local predatory species appears to be more efficient than M. caliginosus in feeding on particular stages of B. tabaci without depending on prey density. This is further supported by the low consumption of both adults and nymphs in the choice test (4% and 2.3%, respectively) compared with M. caliginosus adults (18.6%).     

The brine shrimp Artemia sp. as alternative prey for rearing the predatory bug Macrolophus caliginosus

The predatory bug Macrolophus caliginosus, which is widely used in greenhouse crops, is limited in its application by its high price. An important factor in the cost is the high price of Ephestia kuehniella eggs, the prey used in their mass rearing. In order to reduce their price, alternatives to moth eggs are currently being investigated. The brine shrimp Artemia sp. is produced in large quantities in saline lakes and is fed as live food source to the larvae of a variety of marine and freshwater organisms. In this study, we tested Artemia sp. as prey for rearing M. caliginosus from two strains. We evaluated developmental and reproduction parameters of the predator when fed nauplii, enriched nauplii with a fatty acid, dry cysts and hydrated cysts, and were compared with those obtained when the predator was fed with E. kuehniella eggs. Nauplii had a significant reduction in survivorship, a delay in development of nymphs and a low reproduction of adults. Nauplii enriched with docosahexaenoic acid (DHA, 22:6n − 3), a common practice for larviculture of some marine fish species, resulted toxic to M. caliginosus nymphs and survival was quite low. On the contrary, either dry or hydrated cysts from the two strains tested of the brine shrimp produced the same nymphal survivorship, nymphal development time and weight and fecundity of adults as those obtained with E. kuehniella eggs. Demographic parameters of the eighth generation of the predator reared with cysts of the two strains, either dry or hydrated, were as good as those of moth eggs. We concluded that Artemia sp. cysts were a good substitution prey for the mass rearing of M. caliginosus.     

Ecological relationships between non-cultivated plants and insect predators in agroecosystems: the case of Dittrichia viscosa (Asteraceae) and Macrolophus melanotoma (Hemiptera: Miridae)

Species of the genus Macrolophus (Hemiptera: Miridae) are thought to be effective predators in reducing the numbers of several pests in vegetable crops. These predators are omnivorous as in addition to prey they also utilize plant sap for growth and development. Populations of these predators build in non-crop host plants and provide inoculum that augments natural control of insect pests in adjacent crops. However, to enhance their effectiveness in crops requires knowledge of their trophic relationships with host plants. In this study, the ecological relationships between the predator Macrolophus melanotoma (Costa) ( =  M. caliginosus Wagner) and its most important natural host plant Dittrichia viscosa L. (W. Greuter) (Asteraceae) were investigated in the laboratory and in field studies. A 2-year field study of M. melanotoma populations on D. viscosa was made using the percentage of plants infested by C. inulae as a measure of aphid prey abundance. The field studies revealed that M. melanotoma populations were present throughout the year on D. viscosa reaching highest numbers in June and July despite very low levels of aphid infested plants. Laboratory life table studies were used to compare the survival and reproduction of the predator on D. viscosa leaves alone and leaves plus aphid prey (Capitophorus inulae (Passerini)). Predators reared on D. viscosa leaves plus aphid prey had an average developmental time of 16.73 days, fecundity was 69.55 eggs/female and the intrinsic rate of population increase was 0.0614/day. When fed only leaves, the developmental time was 21.13 days, fecundity was 10.80 eggs/female and the intrinsic rate of population increase was 0.0229/day. The results of the two studies suggest an important role for D. viscosa in conserving and augmenting M. melanotoma in agro ecosystems, and in the development of natural control augmentation strategies in vegetable crops.     

Abundance of the rose-grain aphid,Metopolophium dirhodum,on barley in Canterbury,New Zealand, 1984–87

Abstract

Spring populations of Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) on barley, at Lincoln and elsewhere in Canterbury, New Zealand, declined markedly during 1984–87. Spring suction-trap catches of M. dirhodum also declined at the same time. Numbers of immigrant M. dirhodum on young barley, and maximum aphid population density on the crop, were positively correlated with suction-trap catches of M. dirhodum during the preceding week or month, respectively. Egg numbers of the most abundant predator, Micromus tasmaniae Walker (Neuroptera: Hemerobiidae), and mummy numbers of the parasitoid, Aphidius rhopalosiphi De Stefani-Perez (Hymenoptera: Aphidiidae), increased relative to aphid numbers during the study. Entomophagous fungus-disease incidence could not be related to monthly rainfall, and the decline in aphid numbers during the study period was apparently not related to disease incidence. It is suggested that aphid population regulation by predators and parasitoids in the wider habitat of M. dirhodum could reduce the rate of immigration, and hence aphid population growth, in a given crop.     

Two protagonists on aphidophagous patches: effects of learning and intraguild predation

In aphidophagous systems, trophic interactions between parasitoids and predators, termed intraguild predation, are frequently asymmetric. To mitigate predation risk for themselves and their offspring, intraguild prey may exploit associative learning to gain accurate information about patch quality. Therefore, costs of unnecessary escape behavior are avoided. We used sweet pepper patches (Capsicum annuum L., cv. ‘Mazurka’) (Solanaceae), sustaining Macrosiphum euphorbiae (Thomas) or Myzus persicae (Sulzer) (Homoptera: Aphididae) aphids, as a model system to quantify the foraging behaviors of the parasitoid Aphelinus abdominalis (Dalman) (Hymenoptera: Aphelinidae), when confronted with predatory second instar Chrysopa carnea (Stephens) (Neuroptera: Chrysopidae). The behavior of predator‐naive or predator‐experienced A. abdominalis foraging in a patch with or without C. carnea was recorded and analyzed using a multiple video observation system. We investigated (i) whether A. abdominalis could learn to detect the presence of a predator in a patch, (ii) the impact of the predator presence on the learning and motor learning of the parasitoid, and (iii) the effects of the aphid species on the guild interactions. Results showed that the presence of, or experience with the predator does not affect A. abdominalis learning or motor learning. We discuss the behavioral and ecological implications of our finding. Overall, predator‐induced aphid mobility increased the frequency and allocation time of Aphelinus oviposition activities, especially when Ma. euphorbiae was the host. The predator imposed indirect fitness costs on the parasitoid. Aphelinus abdominalis searched more often and longer, resulting in a tendency towards reduced Ma. euphorbiae parasitism rate in patches harboring C. carnea.     

Density-dependent intraguild predation of an aphid parasitoid

A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (‘mummies’) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.     

Inundative field releases and evaluation of three predators for Bemisia tabaci (Hemiptera: Aleyrodidae) management in three vegetable crops

Abstract The sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is a global pest on numerous crops, including vegetables. Weekly inundative releases of a coccinellid predator (Coccinella undecimpunctata L. [Coleoptera: Coccinellidae]), a common green lacewing predator (Chrysoperla carnea Stephen [Neuroptera: Chrysopidae]), and a mirid predator (Macrolophus caliginosus[Wagner][Hemiptera: Miridae]) were independently made in three vegetable crops (cabbage [Brassica oleracea var. capitata L.], cucumber [Cucumis sativus L.], and squash [Cucurbita pepo L.]) for the management of the sweetpotato whitefly. Approximately 1 million to 2.5 million larvae or nymphs of each predator were released in the vegetable crops during 20 weeks. Whitefly populations were reduced by ≈ 25%–45% during most of the season in each crop where each predator was released. The effect of each predator was similar on whitefly population reduction. Late in the season (October) when whitefly populations were low, generally no benefit was obtained from releasing the predators. Numbers of predators recovered during sampling in all crops were greatest for C. carnea, but this corresponded with the fact that more individuals of this predator were released than any other predator in the experiment. These results help define the utility of these natural enemies for managing B. tabaci in vegetable crops.     

Predator Presence Moves <Emphasis Type="Italic">Helicoverpa armigera</Emphasis> Larvae to Distraction

Displacement of herbivorous insects by the presence of predators on whole plants has rarely been studied. By semi-continuous observations of an externally feeding insect herbivore and a predator, we show how the mere presence of the predator, Geocoris lubra Kirkaldy (Hemiptera: Geocoridae), on a plant can have a strong influence on the movement and behaviors of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) larvae. The presence of predators, as opposed to mortality by predators, influenced the proportion of larvae feeding, resting and implementing avoidance activities. In addition, the proportion of time individual larvae allocated to feeding, resting and dropping off plants was affected when predators were present with and without contact between the two. Predators do more than just reduce numbers of herbivores; they influence feeding, displacement and subsequently the distribution of plant damage.     

Impact of a parasitoid on the bacterial symbiosis of its aphid host

Embryo production in aphids is absolutely dependent on the function of symbiotic bacteria, mainly Buchnera, and the growth and development of koinobiont parasitoids in aphids requires the diversion of nutrients from aphid embryo production to the parasitoid. The implication that the bacterial symbiosis may be promoted in parasitized aphids to support the growing parasitoid was explored by analysis of the number and biomass of mycetocytes, and the aphid cells bearing Buchnera, in the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) parasitized by the wasp Aphidius ervi Haliday (Hymenoptera: Braconidae). Aphids hosting a young larval parasitoid bore more mycetocytes of greater total biomass, and embryos of lower biomass than unparasitized aphids. Furthermore, one of the three aphid clones tested, which limited teratocyte growth (giant cells of parasitoid origin having a trophic role), bore smaller mycetocytes and larger embryos, than one or both of the two aphid clones with greater susceptibility to the parasitoid. These data suggest that susceptibility of the aphid‐Buchnera symbiosis to parasitoid‐mediated manipulation may, directly or indirectly, contribute to aphid susceptibility to parasitoid exploitation.     

Tritrophic effects of organic and conventional fertilisers on a cereal‐aphid‐parasitoid system

The impact of parasitoids on pests varies between conventional and low‐intensity agricultural systems. Although the impacts on parasitoid natural enemies of many practices within these agricultural systems are well understood, the role of fertilisers has been less well studied. The effects of organic‐based and conventional fertilisers on Hordeum vulgare L. (Poaceae), the aphid Metopolophium dirhodum Walker (Hemiptera: Aphididae), and its parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) was investigated using cage release experiments and measures of aphid and parasitoid fitness were taken. Barley tiller number and aphid weight were increased by fertilisers, particularly under conventional treatments. Adult parasitoid size correlated positively with that of the host, M. dirhodum, whereas percentage parasitism was not affected by fertiliser treatment or host size. The results suggest that the increased parasitoid impact observed in some low‐intensity or organic systems is not a direct result of fertiliser treatment. Our results indicate that fertiliser treatments that improve cereal‐aphid fitness will improve parasitoid fitness as measured by parasitoid size but may not influence percentage parasitism.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.