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).     

生物因子对寄生蜂滞育的影响

在影响寄生蜂滞育的生物因子中,寄主及亲代是主要影响因子。寄主可以从种类、类型、生理状态及丰富度等方面影响寄生蜂的滞育:寄生不同种类的寄主,寄生蜂的滞育反应、滞育进度、滞育比例以及光周期反应表现等均有不同;寄主类型的影响在蚜茧蜂类群中表现最为突出,不同寄主类型能对蚜茧蜂的滞育诱导产生不同影响;此外,寄主生理状态和寄主丰富度也是影响寄生蜂滞育的重要因子。亲代对寄生蜂滞育的影响则通过其所经历的环境条件以及自身因素等方面来表现:亲代经历的光周期和温度等能显著影响子代的滞育,甚至起完全决定作用;在亲代自身因素的影响中,亲代虫龄差异是主要因素。本文同时对寄生蜂滞育的研究及应用前景也一并作了展望。     

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.     

Indirect population interaction between two aphid species

We designed an experiment to test whether two species of aphid feeding on different species of host plant influence each others population dynamics via shared parasitoids (apparent competition) or other indirect processes. Pea aphid ( Acyrthosiphon pisum ) colonies declined faster towards mid-summer when there were nearby colonies of nettle aphid ( Microlophium carnosum ), though the significance of the difference ( P  = 0.06) was just short of the traditional 0.05 level. Observations suggested that parasitoids were not responsible for this difference, however, and that it was highly likely to be caused by aphid-specific predators.     

Diapause in the egg parasitoid Trichogramma cordubensis: role of temperature

The role of temperature in the induction of diapause in Trichogramma cordubensis (Hymenoptera: Trichogrammatidae), under controlled laboratory conditions, was investigated using Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as hosts. Results indicate that prestorage temperatures and the duration of exposure of the parasitoids to these temperatures affected the induction of diapause. It was possible to induce diapause in prepupae of T. cordubensis by exposing the preimaginal stages (prior to the prepupal stage) to 10°C for at least 30 days, but adults emerged without diapause when the duration of exposure was of only 10 or 20 days. Parasitoids failed to enter diapause when prestorage temperatures were 7 or 12°C, regardless of the duration of exposure. However, at these two temperatures, preimaginal development of T. cordubensis was delayed, allowing short-term storage (40 days at induction temperatures followed by 30 days at 3°C) by keeping parasitoids in quiescence without reducing the percentages of adult emergence. Good percentages of adult emergence after long-term low-temperature storage (30 or 40 days at 10°C followed by six months at 3°C) occurred only when T. cordubensis was in diapause. The long-term storage of parasitoids in diapause allows an enlargement in the mass rearing potentialities of this species for future biological control releases by allowing producers to stockpile the parasitoids for release in the field season.     

Variation in diapause and sex ratio in the parasitoidAsobara tabida

Asobara tabida Nees (Hymenoptera: Braconidae) is a widespread parasitoid, attacking larvae ofDrosophila (Diptera: Drosophilidae) species in fermenting substrates. In this species, geographic variation is found in the percentage of parasitoids entering diapause and in the sex ratio of emerging parasitoids. Percentage diapause appears to be influenced by host species (more parasitoids enter diapause inD. melanogaster Meigen than inD. subobscura Collin) and temperature. It is not correlated with any of the abiotic factors investigated, but is correlated with survival probability inD. melanogaster larvae and with the time of year in which the experiment was conducted (even though none of the parasitoids experienced natural day light). Sex ratio was only found to correlate with percentage diapause, suggesting that males enter diapause more frequently than females. It is concluded thatA. tabida uses diapause to survive both unfavourable abiotic and biotic circumstances.     

Are aphid parasitoids from mild winter climates losing their winter diapause?

Temperature is both a selective pressure and a modulator of the diapause expression in insects from temperate regions. Thus, with climate warming, an alteration of the response to seasonal changes is expected, either through genetic adaptations to novel climatic conditions or phenotypic plasticity. Since the 1980s in western France, the winter guild of aphid parasitoids (Hymenoptera: Braconidae) in cereal fields has been made up of two species: Aphidius rhopalosiphi and Aphidius matricariae. The recent activity of two other species, Aphidius avenae and Aphidius ervi, during the winter months suggests that a modification of aphid parasitoid overwintering strategies has taken place within the guild. In this study, we first performed a field survey in the winter of 2014/15 to assess levels of parasitoid diapause incidence in agrosystems. Then, we compared the capacity of the four parasitoid species to enter winter diapause under nine different photoperiods and temperature conditions in the laboratory. As predicted, historically winter-active species (A. rhopalosiphi and A. matricariae) never entered diapause, whereas the species more recently active during winter (A. avenae and A. ervi) did enter diapause but at a low proportion (maximum of 13.4 and 11.2%, respectively). These results suggest rapid shifts over the last three decades in the overwintering strategies of aphid parasitoids in Western France, probably due to climate warming. This implies that diapause can be replaced by active adult overwintering, with potential consequences for species interactions, insect community composition, ecosystem functioning, and natural pest control.     

The effect of rearing history and aphid density on volatile‐mediated foraging behaviour of Diaeretiella rapae

1. Parasitoid females foraging for hosts rely on cues derived from the insect host, the host plant and/or their interaction, and all of these can be learned during the immature and adult stages. 2. The present study investigated the importance of rearing history on foraging behaviour of Diaeretiella rapae, an endoparasitoid often associated with aphids feeding on brassicaceous plant species. 3. Parasitoids were reared on one of the four possible combinations, comprising two brassicaceous host plant species, Brassica nigra or Raphanus sativus, and two aphid species Brevicoryne brassicae or Myzus persicae. These parasitoids were tested in a Y‐tube olfactometer and given the choice between volatiles emitted by an aphid‐infested plant (25 or 100 aphids per plant) and an uninfested control plant. The parasitoid's responses were compared when offered: (i) the same plant–aphid combination as the one on which it had been reared; (ii) the same host plant infested with the alternative aphid species; or (iii) an alternative plant with the alternative aphid species. 4. Aphid density did affect the behavioural responses to the various odour sources, but rearing history did not. Diaeretiella rapae only preferred aphid‐induced to non‐induced plant volatiles at low aphid infestation level, whereas they did not discriminate between volatiles at high aphid infestation level. 5. It is concluded that aphid‐induced volatiles of brassicaceous plants play an important role during host habitat location, but seem less important for parasitoids to locate the aphid host itself. The data are discussed in the light of manipulation of host plant defences by aphids.     

Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.     

A universal method for the detection and identification of Aphidiinae parasitoids within their aphid hosts

Molecular methods are increasingly used to detect and identify parasites in their hosts. However, existing methods are generally not appropriate for studying complex host-parasite interactions because they require prior knowledge of species composition. DNA barcoding is a molecular method that allows identifying species using DNA sequences as an identification key. We used DNA amplification with primers common to aphid parasitoids and sequencing of the amplified fragment to detect and identify parasitoids in their hosts, without prior knowledge on the species potentially present. To implement this approach, we developed a method based on 16S rRNA mitochondrial gene and LWRh nuclear gene. First, we designed two primer pairs specific to Aphidiinae (Hymenoptera), the main group of aphid parasitoids. Second, we tested whether the amplified regions could correctly identify Aphidiinae species and found that 61 species were accurately identified of 75 tested. We then determined the ability of each primer pair to detect immature parasitoids inside their aphid host. Detection was earlier for 16S than for LWRh, with parasitoids detected, respectively, 24 and 48 h after egg injection. Finally, we applied this method to assess parasitism rate in field populations of several aphid species. The interest of this tool for analysing aphid-parasitoid food webs is discussed.     

Host phylogeny and specialisation in parasitoids

The host range of insect parasitoids and herbivores is influenced by both preference-related traits which mediate host choice behaviour, and performance-related traits which mediate the physiological suitability of the consumer-resource interaction. In a previous study, we characterised the influence of preference- and performance-related traits on the host range of the aphid parasitoid Binodoxys communis (Hymenoptera: Braconidae) and herein we build upon those data sets by mapping a series of these traits onto the phylogeny of the (aphid) host species. We found a strong effect of host phylogeny on overall parasitoid reproduction on the 20 host species tested, but no effect of the phylogeny of host plants of the aphids. We found an effect of aphid phylogeny on host acceptance and sting rates (related to preference) from behavioural observations and for pupal survivorship (related to performance), showing that both classes of traits show phylogenetic conservatism with respect to host species.     

Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids

In studies of foraging behaviour in a multitrophic context, the fourth trophic level has generally been ignored. We used four aphid hyperparasitoid species: Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), Asaphes suspensus Walker (Hymenoptera: Pteromalidae), Alloxysta victrix (Westwood) (Hymenoptera: Alloxystidae) and Syrphophagus aphidivorus (Mayr) (Hymenoptera: Encyrtidae), to correlate their response to different cues with their ecological attributes such as host range and host stage. In addition, we compared our results with studies of primary parasitoids on the same plant–herbivore system. First, the olfactory response of females was tested in a Y‐tube olfactometer (single choice: plant, aphid, honeydew, parasitised aphid, aphid mummy, or virgin female parasitoid; dual choice: clean plant, plant with aphids, or plant–host complex). Second, their foraging behaviour was described on plants with different stimuli (honeydew, aphids, parasitised aphids, and aphid mummies). The results indicated that olfactory cues are probably not essential cues for hyperparasitoid females. In foraging behaviour on the plant, all species prolonged their total visit time and search time as compared to the control treatment (clean plant). Only A. victrix did not react to the honeydew. Oviposition in mummies prolonged the total visit time because of the long handling time, but the effect of this behaviour on search time could not be determined. No clear correlation between foraging behaviour and host stage or host range was found. In contrast to specialised primary aphid parasitoids that have strong fixed responses to specific kairomones and herbivore‐induced synomones, more generalist aphid hyperparasitoids seem to depend less on volatile olfactory stimuli, but show similarities with primary parasitoids in their use of contact cues while searching on a plant.     

Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae)

Transgenic plants expressing protease inhibitors (PIs) have emerged in recent years as an alternative strategy for pest control. Beneficial insects such as parasitoids may therefore be exposed to these entomotoxins either via the host or by direct exposure to the plant itself. With the objective of assessing the effects of PIs towards aphid parasitoids, bioassays using soybean Bowman-Birk inhibitor (SbBBI) or oryzacystatin I (OCI) on artificial diet were performed on Macrosiphum euphorbiae-Aphelinus abdominalis system. OCI significantly reduced nymphal survival of the potato aphid M. euphorbiae and prevented aphids from reproducing. This negative effect was much more pronounced than with other aphid species. On the contrary, SbBBI did not affect nymphal viability but significantly altered adult demographic parameters. Enzymatic inhibition assays showed that digestive proteolytic activity of larvae and adults of Aphelinus abdominalis predominantly relies on serine proteases and especially on chymotrypsin-like activity. Immunoassays suggested that OCI bound to aphid proteins and accumulated in aphid tissues, whereas SbBBI remained unbound in the gut. Bioassays using M. euphorbiae reared on artificial diets supplemented with both OCI and SbBBI showed a fitness impairment of Aphelinus abdominalis that developed on intoxicated aphids. However, only SbBBI was detected in parasitoid larvae, while no PI could be detected in adult parasitoids that emerged from PI-intoxicated aphids. The potential impact of PI-expressing plants on aphid parasitoids and their combined efficiency for aphid control are discussed.     

Plant Species Loss Affects Life-History Traits of Aphids and Their Parasitoids

The consequences of plant species loss are rarely assessed in a multi-trophic context and especially effects on life-history traits of organisms at higher trophic levels have remained largely unstudied. We used a grassland biodiversity experiment and measured the effects of two components of plant diversity, plant species richness and the presence of nitrogen-fixing legumes, on several life-history traits of naturally colonizing aphids and their primary and secondary parasitoids in the field. We found that, irrespective of aphid species identity, the proportion of winged aphid morphs decreased with increasing plant species richness, which was correlated with decreasing host plant biomass. Similarly, emergence proportions of parasitoids decreased with increasing plant species richness. Both, emergence proportions and proportions of female parasitoids were lower in plots with legumes, where host plants had increased nitrogen concentrations. This effect of legume presence could indicate that aphids were better defended against parasitoids in high-nitrogen environments. Body mass of emerged individuals of the two most abundant primary parasitoid species was, however, higher in plots with legumes, suggesting that once parasitoids could overcome aphid defenses, they could profit from larger or more nutritious hosts. Our study demonstrates that cascading effects of plant species loss on higher trophic levels such as aphids, parasitoids and secondary parasitoids begin with changed life-history traits of these insects. Thus, life-history traits of organisms at higher trophic levels may be useful indicators of bottom-up effects of plant diversity on the biodiversity of consumers.     

Strong parasitoid-mediated selection in experimental populations of aphids

Clonal diversity in asexual populations may be maintained if different clones are favoured under different environmental conditions. For aphids, parasitoids are an important variable of the biotic environment. To test whether parasitoids can mediate selection among host clones, we used experimental populations consisting of 10 clones of the peach-potato aphid, Myzus persicae, and allowed them to evolve for several generations either without parasitoids or in the presence of two species of parasitoid wasps. In the absence of parasitoids, strong shifts in clonal frequencies occurred, mostly in favour of clones with high rates of increase. The parasitoid Diaeretiella rapae hardly affected aphid densities but changed the outcome of competition by favouring one entirely resistant clone and disfavouring a highly susceptible clone. Aphidius colemani, the more infective parasitoid, strongly reduced aphid densities and dramatically changed host clonal frequencies. The most resistant clone, not a successful clone without parasitoids, became totally dominant. These results highlight the potential of temporal or spatial variation in parasitoid densities to maintain clonal diversity in their aphid hosts.     

Some dynamical consequences of parasitoid diapause

Parasitoid diapause usually serves to synchronize parasitoids with host populations that are undergoing diapause, to avoid some period of unsuitable conditions. Non-synchronizing diapause can occur, however, in a number of situations. For example, a fraction of the diapausing parasitoids may stay dormant for a number of seasons. Parasitoids attacking each generation of a multivoltine host may enter a "bank" of diapausing individuals that will emerge at the beginning of the next season. Finally, parasitoid diapause initiation may be driven by density-dependent processes. I examine the effect of these three scenarios on the stability of Nicholson – Bailey type models. I show that in general, non-synchronizing parasitoids can potentially have a strong de-stabilizing influence on parasitoid-host dynamics.     

The use of visual cues in host evaluation by aphidiid wasps I. Comparison between threeAphidius parasitoids of the pea aphid

Host evaluation behaviour was examined in three species of aphid parasitoids,Aphidius ervi haliday,A. pisivorus Smith, andA. smithi Sharma & Subba Rao (Hymenoptera: Aphidiidae). Parasitoids were provided under laboratory conditions with three kinds of hosts representing two aphid species: (green) pea aphid,Acyrthosiphon pisum (Harris), and green and pink colour morphs of the alfalfa aphid,Macrosiphum creelii Davis. Females of all threeAphidius species distinguished between aphids on the basis of colour, movement, and host species. Patterns of host acceptance by parasitoids were species-specific. InA. ervi, host preference was the same in light and dark conditions: pea aphid>green alfalfa aphid≫pink alfalfa aphid. In contrast,A. pisivorus attacked and accepted pea aphid and green alfalfa aphid equally in the light and preferred both of these over pink alfalfa aphid; however, it made no distinction between pea aphid and pink alfalfa aphid in the dark. Females ofA. smithi attacked all three kinds of hosts (pea aphid>green alfalfa aphid≫pink alfalfa aphid) but apparently laid eggs only in pea aphid. The frequencies of attack and oviposition by all wasps were higher on ‘normal’ pea aphids than on those anaesthetized with CO₂. Host recognition is confirmed by chemical cues in the aphid cuticle that are detected during antennation, and host acceptance is dependent on an assessment of host quality during ovipositor probing.     

Seasonal coincidence between rosy apple aphid fundatrices and their parasitoids: implications for an early biological control of Dysaphis plantaginea

The potential contribution of the aphid parasitoid Ephedrus persicae Froggatt (Hymenoptera: Braconidae, Aphidiinae) in regulating stem mothers of the rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae) was investigated in culture conditions using both species' phenological emergence data in spring and host stage suitability trials. In 2003, emergence of E. persicae started on April 1st, i.e., 108.2 degree-days (base: 4.5 degrees C; start date: January 1st) later than its host on March 10th. When less than 3% of parasitoids had emerged on April 12th, more than 97% of D. plantaginea stem mothers had moulted beyond their 1st instar. The latest parasitoids left their diapause mummies in late April as the majority of fundatrices had reached the adult stage. Parasitisation trials demonstrated the suitability for E. persicae of all developmental stages of rosy apple aphid fundatrices, including mature individuals. No offspring were deposited by fundatrices parasitised as Ist-instar nymphs but later instars did produce a progeny whose size was substantially reduced compared with unparasitised individuals, and scaled against their age at the time of parasitisation. Although the temperature accumulation required for emergence in spring is reached later for E. persicae than for its host aphids, thus allowing part of the stem mother population to temporarily escape parasitisation and reach maturity, the marked reduction in fecundity of individuals parasitised even as late-instar nymphs does confer to E. persicae a non-negligible role in potentially regulating D. plantaginea.     

Aestivation in Pieris brassicae (L.) affects the parasitoid load caused by Cotesia glomerata (L.)

The large white butterfly Pieris brassicae (L.) (Lepidoptera: Pieridae) undergoes a unique aestivation in southern Spain. Its pupae remain dormant for three months in summer, emerging in early September. Its main parasitoid, Cotesia glomerata (L.) (Hymenoptera: Braconidae), shows no such diapause behavior and is thus deprived of its main host for this period and has to switch to less suitable host species. To study the effect the aestivation has on the parasitoids, caterpillars were collected from the region in May and September and levels of parasitization were determined. Results show that parasitoid attacks decrease clearly after the summer diapause. The number of parasitized butterfly clutches in September was only one third as the number in May and the infestation rate of an attacked clutch decreased by 55% after aestivation. The distribution of brood sizes of C. glomerata showed clear signs of superparasitism before but not after the diapause. Therefore, the butterfly generation after summer diapause has to deal with distinctly diminished numbers of parasitoids. This increases the survival rate of the caterpillar and thus improves the fitness of the butterfly.     

Can aphid-induced plant signals be transmitted aerially and through the rhizosphere?

Aphids, through their close association with plants, cause systemic release of semiochemicals. These may have negative effects on subsequent aphid colonisation and can also have positive roles with insects that are antagonistic to aphid development, for example parasitoids. One of the semiochemicals involved in host selection by aphids is methyl salicylate, and since this compound was shown to have a role as a plant stress signal, the hypothesis that aphids might facilitate identification of new plant signals was examined. Confirmation was obtained during an investigation of avoidance of unsuitable hosts by the lettuce aphid, Nasonovia ribis-nigri. (Z)-Jasmone was identified as a plant-derived semiochemical acting negatively for a number of aphid species, and positively for insect antagonists such as parasitoids and predators. However, when the compound was employed at 0.1 ppm in air above intact plants, these plants then attracted aphid parasitoids long after the (Z)-jasmone itself was no longer detectable. A specific interaction was proposed, since the (Z)-jasmone appeared to be selectively taken up by the plants. Aerial interactions between intact barley plants from different cultivars, which may be differentially releasing stress associated signals, can also influence acceptability to aphids. Furthermore, it has been shown that exudates from the roots of aphid-infested plants, grown hydroponically or in soil, cause intact plants to become more attractive to parasitoids.