Comparative selectivity of pesticides used in greenhouses,on the aphid parasitoid Aphidius colemani (Hymenoptera: Braconidae)

A series of bioassays were conducted under laboratory conditions to determine the relative toxicities of various pesticides (acetamiprid, cypermethrin, chlorantraniliprole and emamectin benzoate, Bacillus thuringiensis var. kurstaki and Helicoverpa armigera nucleopolyhedrovirus, copper oxychloride, iprodione, mandipropamid, a mixture of propamocarb?+?fluopicolide and mixture of fludioxonil?+?cyprodinil) on Aphidius colemani adults and mummies, as well as sublethal effects on female fecundity. Cypermethrin was highly toxic to pupa of A. colemani within host mummies. Acetamiprid, cypermethrin, emamectin benzoate, a mixture of propamocarb?+?fluopicolide and mixture of fludioxonil?+?cyprodinil were also highly toxic to A. colemani adults (92–100% mortality at 48?h post treatment). Mandipropamid, iprodione and copper oxycloride treatments significantly reduced fecundity of the female parasitoids. In contrast B. thuringiensis var. kurstaki, H. armigera nucleopolyhedrovirus and chlorantraniliprole were harmless (<30% mortality) to the parasitoid species tested according to International Organisation for Biological Control toxicity classification and are likely to be compatible with integrated pest management programmes.     

Functional responses of aphid parasitoids,Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae)

We evaluated the functional responses of two aphid parasitoids: Aphidius colemani on the green peach aphid Myzus persicae (Hemiptera: Aphididae), and Aphelinus asychis on M. persicae and the potato aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Parasitoid oviposition occurred at host densities of 5, 10, 20, 30, 50, 80 or 100 aphids for A. colemani and 5, 10, 20, 30 or 50 aphids for A. asychis. More M. persicae were parasitized by A. colemani than by A. asychis at an aphid density of 50. Among the three types of functional response, type III best described the parasitoid response to the host densities both in A. colemani and A. asychis. The estimated handling time was shorter for A. colemani than for A. asychis (0.017 and 0.043 d, respectively). The proportion of aphids that were parasitized exhibited the same characteristic curve among the three host-parasitoid combinations: a wave form that appeared to be a composite of a decelerating (as in type II) response at low host density and an accelerating-and-decelerating (as in type III) response at medium to high host density. We hypothesize that the novel host species (and its host plant), density-dependent superparasitism, and/or density-dependent host-killing may have induced the modified type III response.     

Male wing fanning by the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) produces a courtship song

We, herein, report evidence that wing fanning by the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) constitutes a courtship song. Complete removal of the forewings or only the distal half of them reduced male copulation success in comparison to intact males. Males that achieved copulation within the observation period produced wing fanning at a higher rate than males that did not copulate. Playback of wing fanning sound altered the behaviour of virgin females, increasing the time they devoted to grooming, as compared with subjects that were exposed to silence or white noise. Our findings contribute to the understanding of the acoustic dimension of the sensory modalities employed by this aphid parasitoid in sexual signalling.     

Consequence of emergence pattern on inbreeding risk in the aphid parasitoid Aphidius matricariae (Hymenoptera: Braconidae)

In insect parasitoids, mating strategy depends on mate availability and is influenced by the spatial and temporal emergence patterns of adults. For quasi-gregarious species, simultaneous emergence favors local mating and reduces search costs for partners while increasing the risk of inbreeding, particularly when only one female parasitizes the initial host patch. Consequently, in inbreeding sensitive species, mating on the place of adult emergence (patch mating) between siblings should be counter selected. In practice, the timing of male and female emergence and of their dispersal influences mate availability and can limit on patch mating. To test the role of these two factors, we analyzed the daily distribution of emergence and patch residence time of a cohort in the aphid parasitoid Aphidius matricariae (Hymenoptera: Braconidae). We observed that adult emergence is concentrated on the morning with males emerging on average before females with some overlaps. A more precise evaluation of emergence pattern within a brood suggests that brothers and sisters rarely emerge at the same time and rapid dispersal of males and females favors off-patch mating. The relationships between timing of emergence including differences between sex and consequences on inbreeding probability in these species are thus discussed.     

Effect of cabbage cultivars with varying levels of resistance to aphids on the performance of the parasitoid,Aphidius colemani (Hymenoptera: Braconidae)

The effect of aphid resistance in plant cultivars on parasitism of Myzus persicae (Sulzer) and Brevicoryne brassicae (Linnaeus) by Aphidius colemani Viereck was investigated under laboratory conditions using three cultivars of common cabbage, Brassica oleracea var. capitata. Significantly greater aphid populations were found on cv. Derby Day (green-leaved, susceptible to both aphid species), regardless of the presence or absence of parasitoids, compared with cv. Minicole (green-leaved, partially resistant with antibiosis factors for B. brassicae) or cv. Ruby Ball (red-leaved, partially resistant with antixenosis factors for B. brassicae). Minicole had the greatest proportion of parasitized aphids and Derby Day the least. A significantly lower percentage of emerged parasitoids were recorded on Minicole for both aphid species compared with Derby Day and Ruby Ball. The implication of the results are discussed in relation to the integrated control of aphids.     

The effect of entomopathogenic Lecanicillium spp. (Hypocreales: Cordycipitaceae) on the aphid parasitoid Aphidius colemani (Hymenoptera: Aphidiinae)

The effects of entomopathogenic Lecanicillium spp. (Zare and Gams) on Aphidius colemani (Viereck) adult longevity and ovipositional behavior and on the emergence rate and longevity of the F₁ generation of this parasitoid insect were evaluated under laboratory conditions. Moreover, the ability of three strains of Lecanicillium spp. to penetrate the cuticle of aphids parasitized by A. colemani at different larval stages was investigated. Although fungal treatments at high concentrations (10⁷?conidia/ml) reduced adult longevity, no significant effects were observed at lower concentrations. The number of ovipositional probings, sting failure rate of the ovipositor, and time intervals between periods of ovipositional behavior were not significantly different between the experimental groups and controls at all concentrations for all fungal strains. Fungal inoculation showed no significant effects on the emergence rate and longevity of the adult A. colemani F₁ generation. Fungal penetration was detected in 60?% of aphids inoculated with fungi 7?days after parasitoid exposure. However, fungal detection was drastically reduced and undetectable when fungal inoculation occurred 8 and 9?days after parasitization, respectively. Our results suggest the coapplication of Lecanicillium spp. and A. colemani for aphid control is possible under certain conditions because of their high compatibility.     

Olfactory conditioning in mate searching by the parasitoid Aphidius ervi (Hymenoptera: Braconidae)

Despite the fact that insect learning capacity has been broadly demonstrated, the role that this process plays during mate searching has been scarcely explored. We studied whether the sexual behaviour of a male parasitic wasp can be conditioned to the odours from two alternative host plant complexes (HPCs) present during its first copulation. The experimental subjects were newly emerged males of the aphid parasitoid, Aphidius ervi, and two alternative HPCs (alfalfa or wheat). In the training protocol, copulation experience corresponded to an unconditioning stimulus and HPC odours to the conditioning stimuli. The initial (just after eclosion) and trained responses were assessed in a glass Y-olfactometer. The results showed that neither alfalfa HPC nor wheat HPC stimuli elicited sexual-related behaviours in initial male responses. Conversely, both HPCs triggered strong attraction and wing fanning courtship behaviour in trained responses when the male was exposed to a female plus HPC during training. In males trained with females plus a given HPC but tested with the alternative HPC in the olfactometer, trained response showed a similar trend to the non-associative treatments. Hence, through learning, the olfactory stimulus context present during copulation could become a predictive cue for further mate searching. These results are discussed in terms of parasitic wasp ecology and host fidelity.     

Larval anatomy and structure of absorbing epithelia in the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)

The present work describes Aphidius ervi Haliday (Hymenoptera, Braconidae) larval anatomy and development, focusing on time-related changes of body structure and cell ultrastructure, especially of the epithelial layers involved in nutrient absorption. Newly hatched 1st instar larvae of A. ervi are characterised by gut absence and a compact cluster of cells makes up their body. As the parasitoid larva develops, the central undifferentiated cell mass becomes hollowed out, leading to the formation of gut anlage. This suggests that absorption of nutrients at that stage may take place through the body surface, as more directly demonstrated by the occurrence on the epidermis of proteins associated with transepithelial transport, such as Na(+)/K(+)-ATPase and alkaline phosphatase (ALP). Second instar larvae show the presence of the gut with a well-differentiated brush border and a peritrophic membrane. Gut cells are filled by masses of glycogen granules and lipid droplets. The tracheal system starts to be visible. The haemocoel becomes evident in late 2nd instar, and contains large silk glands. Mature 3rd instar larvae are typically hymenopteriform. The midgut accounts for most of the body volume and is actively involved in nutrient absorption, as indicated by the well developed brush border and by the presence of Na(+)/K(+)-ATPase and ALP on the basolateral and luminal membrane respectively. At this stage, large lipid droplets have gradually replaced the cellular glycogen stores in the midgut cells. The tracheae are completely differentiated, but their internal lumen still contains fibrillar material, suggesting that they are not functional as long as host fluids bath the parasitoid larva. In late 3rd instar larvae, silk glands, structurally similar to Malpighian tubules, show a very intense vesicular traffic toward the internal lumen, which, eventually, results in being filled by secretion products, suggesting the possible recycling of metabolic waste products during mummy formation.     

Floral resources to enhance the potential of the parasitoid Aphidius colemani for biological control of the aphid Myzus persicae

Flowering plants have been widely used to enhance biological control. However, this approach has been limited to some extent by the lack of suitable flowering plant species of wide applicability, particularly for global pests. A key example is the green peach aphid, Myzus persicae (GPA). It is commonly attacked by the polyphagous koinobiont aphidiidae, Aphidius colemani, which is also of global occurrence. Here, eight flowering plants were evaluated for the potential enhancement of GPA biological control using A. colemani under laboratory conditions. These included buckwheat (Fagopyrum esculentum), alyssum (Lobularia maritima), white rocket (Diplotaxis erucoides.), wild mustard (Sinapis arvensis), lavender (Lavandula angustifolia), wild marjoram (Origanum vulgare), thyme (Origanum marjorana) and pepper mint (Mentha piperita). The effects of access to these flowers on the longevity (days), potential fecundity (number of dissected eggs) and parasitism rate for A. colemani compared with the control treatment (water) were studied. Longevity of A. colemani which had access to buckwheat was 4–5 times longer than the control and 2–3 times longer than it was in the other plant treatments; the latter did not differ significantly between each other. Potential fecundity of A. colemani was the highest when it had been provided with buckwheat flowers. Exposing A. colemani to flowering plants for longer time intervals (12 hr and 24 hr) increased the number of eggs produced compared with 6 hr. The number of parasitized aphids/female A. colemani with buckwheat flowers was the highest of all treatments; it ranged from 14 in the control to 219 with buckwheat. Further studies should be carried out under field conditions to determine the effect of a range of flowering plants on A. colemani. For example, although buckwheat was highly effective, in many climates it may be a useful component in mixtures comprising other, more robust species.     

Intraguild Predation by Anthocoris nemorum (Heteroptera: Anthocoridae) on the Aphid Parasitoid Aphidius colemani (Hymenoptera: Braconidae)

The magnitude of intraguild predation by adult females of the predator Anthocoris nemorum on immature larvae of the aphid parasitoid Aphidius colemani inside mummies of peach-potato aphids Myzus persicae was investigated under laboratory conditions in a preference experiment. Each predator consumed a mean (95% confidence limits) of 2.8 (2.1; 3.8) immature parasitoids within mummies and 3.6 (2.7; 4.6) unparasitised aphid nymphs. Thereby A. nemorum engaged in intraguild predation with A. colemani and did not exhibit prey preference between mummies and unparasitised aphids.     

Potential effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)

Protease inhibitors (PIs) have been shown to cause lethal and sublethal effects on aphids depending on the kind of PI and aphid species. Therefore, these proteins might affect aphid parasitoids directly by inhibiting their digestive proteolysis or indirectly via their development in a less suitable host. In our study, the risk of exposure and the potential effects of soybean Bowman-Birk inhibitor (SbBBI) and oryzacystatin I (OCI) on the aphid endoparasitoid Aphidius ervi were investigated using artificial diet to deliver PIs. Immunoassays showed that both SbBBI and OCI were detected in the honeydew of aphids reared on artificial diet containing these recombinant proteins at 100 microg/mL. However, only SbBBI was detected in parasitoid larvae, while this PI could not be detected in adult parasitoids emerged from PI-intoxicated aphids. Enzymatic inhibition assays showed that digestive proteolytic activity of larvae and adults of A. ervi predominantly relies on serine proteases and especially on chymotrypsin-like activity. Bioassays using SbBBI and OCI on artificial diet were performed. A. ervi that developed on intoxicated aphids had impaired fitness. Thus development and parasitism success of parasitoids exposed to OCI were severely affected. On the contrary, SbBBI only altered significantly female size and sex ratio. Direct exposure to PIs through adult food intake did not affect female's longevity, while SbBBI and OCI (100 microg/mL) induced 69% and 30% inhibition of digestive protease activity, respectively. These studies made it possible to estimate the risk of exposure to plant PIs and the sensitivity of the aphid parasitoid A. ervi to these entomotoxins, by combining immunological, biochemical and biological approaches. First it pointed out that only immature stages are affected by PIs. Secondly, it documented two different modes of effect, according to the nature of the PIs and both host and parasitoid susceptibility. OCI prevented the development of A. ervi mainly due to the host susceptibility, whereas SbBBI only induced sublethal effects on the parasitoid, possibly due to both direct action on the parasitoid susceptible proteases, and host-mediated action through size reduction.     

Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae), alters individual fixed preferences for pea aphid color morphs

Learning, defined as changes in behavior that occur due to past experience, has been well documented for nearly 20 species of hymenopterous parasitoids. Few studies, however, have explored the influence of learning on population-level patterns of host use by parasitoids in field populations. Our study explores learning in the parasitoid Aphidius ervi Haliday that attacks pea aphids, Acyrthosiphon pisum (Harris). We used a sequence of laboratory experiments to investigate whether there is a learned component in the selection of red or green aphid color morphs. We then used the results of these experiments to parameterize a model that examines whether learned behaviors can explain the changes in the rates of parasitism observed in field populations in South-central Wisconsin, USA. In the first of two experiments, we measured the sequence of host choice by A. ervi on pea aphid color morphs and analyzed this sequence for patterns in biased host selection. Parasitoids exhibited an inherent preference for green aphid morphs, but this preference was malleable; initial encounters with red aphids led to a greater chance of subsequent orientation towards red aphids than predicted by chance. In a second experiment, we found no evidence that parasitoids specialize on red or green morphs; for the same parasitoids tested in trials separated by 2 h, color preference in the first trial did not predict color preference in the second, as would be expected if they differed in fixed preferences or exhibited long-term (> 2 h) learning. Using data from the two experiments, we parameterized a population dynamics model and found that learning of the magnitude observed in our experiments leads to biased parasitism towards the most common color morph. This bias is sufficient to explain changes in the ratio of aphid color morphs observed in field sites over multiple years. Our study suggests that for even relatively simple organisms, learned behaviors may be important for explaining the population dynamics of their hosts.     

Visual and Olfactory Female-Borne Cues Evoke Male Courtship in the Aphid Parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae)

We investigated the courtship and mating behavior of the pan-tropical polyphagous endoparasitoid Aphidius colemani Viereck. The courtship and mating displays, the magnitude of male-male sexual approaches and the role of female-borne cues evoking male courtship behavior were quantified. The sequence of events leading to copulation in this parasitoid did not differ from that found for other braconids. Females refused to copulate more than once. Same-sex courtships were observed among males and their possible role in an adaptive context is discussed. Olfactory female-borne cues played a key role in eliciting the courtship responses of males. Males were attracted by freshly dead females, but not by dead females soaked in hexane, nor by visual cues from females alone. Intense male wing fanning behavior was elicited by crushed abdomens of virgin females, suggesting that the female abdomen is the source of a short-distance pheromone crucial in evoking male courtship. Further studies are required to clarify the exact nature of the chemicals involved.     

Molecular identification of Aphidius transcaspicus (Hymenoptera: Braconidae: Aphidiinae), a closely associated species of Aphidius colemani,in Korea

Aphidius colemani (Braconidae: Aphidiinae) is an endoparasitoid and one of the most commercially used parasitoids for the control of various pest aphids. However, species identification of A. colemani is difficult because of the high degree of morphological similarity with closely associated species, such as A. transcaspicus and A. platensis. Recently, we identified a large-scale emergence of parasitoids from mummies of Rhopalosiphum maidis on barley banker plants in Yecheon County, Korea. The morphological characteristics of the forewing, petiole, and antenna indicated that our specimen is A. transcaspicus. The partial nucleotide sequence analysis of the mitochondrial cytochrome oxidase subunit I (COI) gene showed that it is 100% identical to Japanese specimens and 1.69% variable to Greek specimens. Analysis of the phylogenetic tree, haplotypes, and amino acid sequence of the COI gene, as well as the internal transcribed spacer 2 (ITS2) of the nuclear ribosomal DNA region, indicated that A. transcaspicus is closer to A. platensis than A. colemani, and Korean and Japanese populations were mostly diversified groups at the intraspecific level. This study provides important information to elucidate the genetic variation in A. transcaspicus and the relationships between closely related species within the A. colemani group.     

Impact of Rag1 aphid resistant soybeans on Binodoxys communis (Hymenoptera: Braconidae), a parasitoid of soybean aphid (Hemiptera: Aphididae)

Multiple strategies are being developed for pest management of the soybean aphid, Aphis glycines Matsumura; however, there has been little published research thus far to determine how such strategies may influence each other, thereby complicating their potential effectiveness. A susceptible soybean (Glycine max L.) variety without the Rag1 gene and a near isogenic resistant soybean variety with the Rag1 gene were evaluated in the laboratory for their effects on the fitness of the soybean aphid parasitoid, Binodoxys communis (Gahan). The presence or absence of the Rag1 gene was verified by quantifying soybean aphid growth. To test for fitness effects, parasitoids were allowed to attack soybean aphids on either a susceptible or resistant plant for 24 h and then aphids were kept on the same plant throughout parasitoid development. Parasitoid fitness was measured by mummy and adult parasitoid production, adult parasitoid emergence, development time, and adult size. Parasitoids that attacked soybean aphids on susceptible plants produced more mummies, more adult parasitoids, and had a higher emergence rate compared with those on resistant plants. Adult parasitoids that emerged from resistant plants took 1 d longer and were smaller compared with those from susceptible plants. This study suggests that biological control by B. communis may be compromised when host plant resistance is widely used for pest management of soybean aphids.     

Efficacy assessment of Aphidius colemani (Hymenoptera: Braconidae) for suppression of Aphis gossypii (Homoptera: Aphididae) in greenhouse-grown chrysanthemum

To assess biological control as a management tool for the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae), the efficacy of Aphidius colemani Viereck (Hymenoptera: Braconidae) for suppression of A. gossypii in greenhouse-grown chrysanthemums, Dendranthema grandiflora (Tzvelev), was compared with a pesticide standard, imidacloprid (Marathon 1% G) and an untreated check. No significant differences were found between aphid populations in the two treatments. A. colemani and imidacloprid kept aphid numbers very low, with the correspondent aphid populations exhibiting very low intrinsic rates of increase (r(m) = -0.0369 and r(m) = 0.0151, respectively), in contrast to the exponential growth of aphid populations (r(m) = 0.1085) observed on the untreated plants. Parasitism levels in A. colemani plots ranged from 48.93 to 83.38%. Esthetic damage parameters, including exuviae, honeydew, and sooty mold on leaves, were significantly different between treatments and untreated control, and damage levels were minimal with the insecticide treatment and natural enemy releases. The cost of A. colemani releases was 4.7 times greater than the cost of the imidacloprid treatment.     

Phototactic behaviour in Aphidius gifuensis (Hymenoptera:Braconidae)

We investigated the spectral sensitivity and response to light intensity of Aphidius gifuensis (Hymenoptera: Braconidae), a key natural enemy of the green peach aphid, Myzus persicae (Hemiptera: Aphididae). We used 15 monochromatic lights (emitting various specific wavelengths from 340 to 689 nm) and white light. Monochromatic light of different wavelengths and white light elicited photopositive behaviour from A. gifuensis. The strongest response was stimulated by blue light (492 nm), which induced a movement of 43.5 cm, a response that differed from all other groups. This was followed by green light (568 nm) and UV-light (380 nm). There was no significant response to orange light (601 nm) or red light (649, 668 and 689 nm) from A. gifuensis. The response intensity curve for A. gifuensis to monochromatic light (492 nm) decreased as light intensity increased. At 568 nm, the phototactic response showed an ‘S’ shaped curve. But at 628 nm, the phototactic response rose continuously with increasing intensity. We report here that the visual system of A. gifuensis is composed of three spectrum receptors, attuned to UV, blue and green light. While light intensity is a key factor in determining the photopositive response of A. gifuensis, the effect of intensity varies by wavelength.     

Fertility life table of Aphidius colemani Viereck (Hymenoptera: Braconidae, Aphidiinae) on Aphis gossypii Glover (Hemiptera: Aphididae)

The intrinsic rate of increase of a parasitoid related to its hosts play an important role in biological control programs. In this work, fertility of the parasitoid Aphidius colemani Viereck was evaluated on Aphis gossypii Glover by means of a fertility life table. To determine the immature mortality, the development time and the sex ratio, 12 mated females of A. colemani (24h old), and 240 nymphs of A. gossypii (3 days old) were used. To evaluate fertility 15 mated females (24h old) were used. For each parasitoid female, 300 nymphs were offered in the 1st day, 250 nymphs in the 2nd day, 200 nymphs in the 3rd day, 150 nymphs in the 4th day, 100 nymphs in the 5th day and 50 nymphs in the other days. Immature mortality of A. colemani was 22.1%, development time of males and females were 12.0 and 11.8 days, respectively, and sex ratio was 0.6. The females of A. colemani laid 420 eggs and had longevity of 5.9 days. The net reproduction rate (R(o)) was 194.81 females and the intrinsic rate of increase (r(m)) was 0.384 females/females/day. The finite rate of increase (lambda) was 1.48 females/day, the mean length of a generation (T) was 13.74 days and the time to duplication the population (TD) was 12.60 days. The parasitoid A. colemani had a great potential of population growth on A. gossypii as a host and could be an effective biological control agent of this aphid.