Hyperparasitoid aggregation in response to variation in Aphidius ervi host density at three spatial scales

1. This article investigates the pattern of hyperparasitism of the host Aphidius ervi Haliday (Hymenoptera, Aphidiidae), a primary parasitoid of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) at three spatial scales.
2. In the laboratory, the hyperparasitoid Asaphes lucens (Provancher) (Hymenoptera: Pteromalidae) was introduced into cages containing sixteen alfalfa plants with varying numbers of A. ervi mummies (the stage susceptible to hyperparasitism). The pattern of hyperparasitism at the end of the 48-h trials showed no density-dependent hyperparasitoid aggregation, although there was strong density-independent hyperparasitoid aggregation.
3. In the field, the density of A. ervi mummies was manipulated in twelve 2 × 2-m plots containing 1309–1654 alfalfa stems. Variation in hyperparasitism among plots showed no density-dependent aggregation, although there was strong density-independent aggregation.
4. Finally, at the largest scale of the study, the distribution of hyperparasitism was sampled among twelve alfalfa fields within a 5 × 3-km area. At this scale there was both density-dependent and density-independent hyperparasitoid aggregation.
5. The natural variation in A. ervi mummy density is greatest at the larger scales of study. Therefore, density-dependent hyperparasitism occurs only when there is high natural variation in mummy density.     

Parasitoids aid dispersal of a nonpersistently transmitted plant virus by disturbing the aphid vector

• 1 Aphids are the major group of insects that vector plant viruses, and they often display a preference for foliage showing disease symptoms. Although this behaviour will increase the numbers of vectors acquiring the pathogen, it will not in itself result in a greater spread of the disease.
• 2 The present study examined how infection of Vicia faba by the nonpersistently transmitted virus bean yellow mosaic virus (BYMV) affected colonization by pea aphids Acyrthosiphon pisum. We then examined how foraging by the hymenopterous parasitoid Aphidius ervi affected aphid settling/movement behaviour and the consequences for dissemination of the virus.
• 3 In Petri dish arenas, aphids colonized discs from BYMV‐infected leaves more rapidly than discs from uninfected plants. Reflectance from infected foliage was approximately 20% higher than from uninfected leaves in the green–yellow wavelengths, indicating that aphids might be responding to visual cues from the brighter foliage. Settling was reduced by A. ervi, with the foraging wasps preventing the aphids reaching and/or remaining on the leaf tissue.
• 4 In multiple plant arenas, A. ervi caused a reduction in aphid numbers but also a nine‐fold increase in BYMV infection. It is hypothesized that disturbance by the parasitoids resulted in more aphid movement as well as more cases of aphids probing on a BYMV‐infected plant and then a new host within the critical time period for successful inoculation to occur. This effect of parasitoids on virus dispersal should be considered in epidemiological models of insect‐vectored plant diseases, and also when evaluating the use of natural enemies in biocontrol strategies of insect herbivore/vector pests.

     

Host-range evolution in Aphidius parasitoids: fidelity, virulence and fitness trade-offs on an ancestral host

The diversity of parasitic insects remains one of the most conspicuous patterns on the planet. The principal factor thought to contribute to differentiation of populations and ultimately speciation is the intimate relationship parasites share with hosts and the potential for disruptive selection associated with using different host species. Traits that generate this diversity have been an intensely debated topic of central importance to the evolution of specialization and maintenance of ecological diversity. A fundamental hypothesis surrounding the evolution of specialization is that no single genotype is uniformly superior in all environments. This "trade-off" hypothesis suggests that negative fitness correlations can lead to specialization on different hosts as alternative stable strategies. In this study we demonstrate a trade-off in the ability of the parasitoid, Aphidius ervi, to maintain a high level of fitness on an ancestral and novel host, which suggests a genetic basis for host utilization that may limit host-range expansion in parasitoids. Furthermore, behavioral evidence suggests mechanisms that could promote specialization through induced host fidelity. Results are discussed in the context of host-affiliated ecological selection as a potential source driving diversification in parasitoid communities and the influence of host species heterogeneity on population differentiation and local adaptation.     

Horizontal transfer of facultative endosymbionts is limited by host relatedness

Heritable microbial symbionts can have important effects on many aspects of their hosts’ biology. Acquisition of a novel symbiont strain can provide fitness benefits to the host, with significant ecological and evolutionary consequences. We measured barriers to horizontal transmission by artificially transferring facultative symbionts from the grain aphid, Sitobion avenae, and five other aphid species into two clonal genotypes of S. avenae. We found the symbiont Hamiltonella defensa establishes infections more easily following a transfer from the same host species and that such infections are more stable. Infection success was also higher when the introduced symbiont strain was more closely related to the strain that was originally present in the host (but which had previously been removed). There were no differences among successfully established symbiont strains in their effect on aphid fecundity. Hamiltonella defensa did not confer protection against parasitoids in our S. avenae clones, although it often does in other aphid hosts. However, strains of the symbiont Regiella insecticola originating from two host species protected grain aphids against the pathogenic fungus Pandora neoaphidis. This study helps describe the extent to which facultative symbionts can act as a pool of adaptations that can be sampled by their eukaryote hosts.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.     

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.     

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.     

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.     

Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack

The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid‐free plants but only when they are connected to aphid‐infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.     

The significance of a facultative bacterium to natural populations of the pea aphid Acyrthosiphon pisum

Abstract. 1.  Laboratory studies have implicated various accessory bacteria of aphids as important determinants of aphid performance, especially on certain plant species and under certain thermal regimes. One of these accessory bacteria is PABS (also known as T-type), which is distributed widely but is not universal in natural populations of the pea aphid Acyrthosiphon pisum in the U.K.
2.  To explore the impact of PABS on the performance of A. pisum , the nymphal development time and fecundity of aphids collected directly from natural populations and caged on the host plant Vicia faba in the field were quantified. Over 4 consecutive months June–September 1999, the performance of PABS-positive and PABS-negative aphids did not differ significantly.
3.  Deterministic modelling of the performance data showed that the variation in simulated population increase of PABS-positive and PABS-negative aphids would overlap substantially.
4.  Analysis of aphids colonising five host plants ( Lathyrus odoratus , Medicago sativa , Pisum sativum , Trifolium pratense , Vicia faba ) between April and September 2000 and 2001, identified no robust differences between the distribution of PABS-positive and PABS-negative aphids on different plants and with season or temperature.
5.  It is concluded that PABS is not an important factor shaping the performance or plant range of A. pisum under the field conditions tested. Reasons for the discrepancies between this study and laboratory-based studies are considered.     

豌豆蚜翅分化相关miRNA及其预测靶基因对蜕皮激素的应答及miR-92a-1-p5靶基因的验证

[目的]蜕皮激素对孤雌蚜翅两型性分化具有重要调控作用.在前期研究中我们发现5个微小RNA(microRNA,miRNA)在豌豆蚜Acyrthosiphon pisum翅两型性分化中也发挥关键作用,但蜕皮激素是否与miRNA互作参与蚜虫翅型分化未知.本研究旨在探索蜕皮激素对5个miRNA及其预测靶基因表达的影响,揭示蜕皮...     

The role of the plant in attracting parasitoids: response to progressive mechanical wounding

Based on the model system of Brussels sprouts [Brassica oleracea var. gemmifera (Brassicaceae)], the herbivore cabbage white caterpillar, Pieris brassicae (L.) (Lepidoptera: Pieridae), and the parasitoid wasp, Cotesia glomerata (L.) (Hymenoptera: Braconidae), the influence of plant damage type, and damage duration were assessed on plant volatile emission and subsequent recruitment of natural antagonists of the herbivore. Plants were damaged by three methods for a period of either 3 or 8 h: herbivore damage (HD), progressive mechanical damage, and final mechanical damage inflicted in a single event. Wind‐tunnel bioassays evaluated whether the mode of damage affected female parasitoid oriented flight. After both periods of damage, all treatments were highly significantly preferred by naïve C. glomerata to undamaged control plants. After 3 h, herbivore‐damaged plants were significantly preferred to plants with final damage (FD). Most remarkably, following 8‐h damage, the parasitoid preferred both herbivore‐damaged and progressively damaged plants to plants with FD and did not significantly discriminate between herbivore and progressively damaged plants, thus indicating a similarity in plant response to herbivore and progressive mechanical damage. In addition to wind‐tunnel bioassays, emitted plant volatiles were collected and analysed by thermal desorption gas chromatography/mass spectrometry, following 3 and 8 h of damage in order to correlate volatiles released from different damage types with the attraction of the parasitoid. Differences in volatile profiles from all damage types were similar following both 3 and 8 h of damage, with only (Z)‐3‐hexenyl acetate found to be emitted in significantly higher quantities by final mechanical damage compared with HD after 3 h. In conclusion, the plant's response to progressive mechanical damage was more similar to HD than final mechanical damage deployed at a single point in time, irrespective of damage duration, and C. glomerata did not significantly discriminate between progressive damage and HD.     

The response of an aphid tending ant to artificial extra-floral nectaries on different host plants

Sap-feeding homopterans, which reduce the fitness of their host plants, are often tended by ants that feed on their honeydew. The composition of the honeydew varies with both the aphid and the host plant. Extra-floral nectaries (EFNs) are believed to have evolved to attract attending ants, protecting the hosts, but it is unknown if EFNs on different plants have the same impact on the relations between an aphid species feeding on those plants and its tending ant. Experimental research was conducted to examine the attraction of Tapinoma erraticum scout ants to honeydew from the aphid Aphis gossypii feeding on two different plants, Prunus amygdalus and Mentha piperita, negligence of tending the aphids, and survival of the aphids in the presence of artificial EFNs. The scout ants were significantly more attracted to artificial nectar dispensed on P. amygdalus leaves than on M. piperita, or aphids on both plants and water. They neglected aphids in the presence of artificial EFNs on M. piperita but not on P. amygdalus. The aphid population on M. piperita did not statistically change in the presence of artificial EFNs during the 8 days of the third experiment. On P. amygdalus, the aphids succeeded in developing fully to winged form. In conclusion, the responses of the ants tending aphids to the presence of artificial EFNs were influenced by the host plant.     

Population level effects of cadmium and the insecticide imidacloprid to the parasitoid, Aphidius ervi after exposure through its host, the pea aphid, Acyrthosiphon pisum (Harris)

The objective of this study was to assess the influence of toxic substances with different modes of action on a two-species system: an aphid-specific parasitoid, Aphidius ervi Haliday, feeding on the pea aphid, Acyrthosiphon pisum (Harris). The instantaneous rate of population increase (r_i) was used as a measure of population level toxic effect in this study. The toxicants evaluated were imidacloprid, a nonpersistent neurotoxic insecticide, and cadmium, a chronic pollutant with a tendency to accumulate. We evaluated the effects of cadmium and imidacloprid on A. pisum and A. ervi because both toxicants can occur together in polluted areas where crops are grown. Cadmium (200 or 400 mg kg⁻¹ dry weight soil) and imidacloprid (4 or 40 g a.i. ha⁻¹) were applied to soil contained in plastic pots in which broad bean plants, Vicia faba L., were grown. Results of this study indicated that cadmium at the concentrations tested, reduced population growth rate of the pea aphid. Imidacloprid also reduced aphid growth rate, but only at the highest concentration tested (40 g a.i. ha⁻¹). Combinations of cadmium and imidacloprid had the greatest impact on aphid growth rate. Imidacloprid alone had no effect on population growth rate of the parasitoid. However, cadmium alone or in combination with imidacloprid had a negative impact on A. ervi by reducing population growth rate 77%. These results indicate that negative impacts on parasitoids may occur in areas where cadmium contamination is present and imidacloprid is used to control aphids.     

The response of Hyssopus pallidus to hosts previously parasitised by Ascogaster quadridentata: heterospecific discrimination and host quality

1. Two basic tenets of competition among parasitoids, that taxonomically distinct parasitoids are unable to discriminate against hosts that have previously been attacked by a competitor and that previous parasitism reduces the quality of a host, were tested by monitoring the oviposition response of Hyssopus pallidus, a gregarious ectoparasitoid, to healthy codling moth larvae and codling moth larvae that had previously been parasitised by a solitary endoparasitoid, Ascogaster quadridentata. 2. Hyssopus pallidus accepted both categories of host larva for oviposition when its competitor was constrained as a first‐instar larva by the diapause development of its host, but discriminated against previously parasitised host larvae when its competitor was present as a larger larva in a non‐diapausing host. 3. Hyssopus pallidus distinguished between the two categories of host larva by allocating twice as many eggs to host larvae previously parasitised by A. quadridentata, a response that was not influenced by previous oviposition experience. 4. The larger clutch sizes allocated to previously parasitised host larvae produced twice as many female progeny, each of a typical size, such that the total biomass was twice that produced from the smaller clutches laid on healthy host larvae. Possible confounding influences of host age and diapause are discounted. 5. These results demonstrate that interspecific discrimination does occur in H. pallidus and that host quality can be improved through previous parasitism by an endoparasitoid. Although interspecific discrimination appears rare among insect parasitoids, it may have been overlooked among ectoparasitoids and requires examination of the fitness consequences of interspecific interactions to clarify its adaptive significance.     

The influence of a parasitoid's response to temperature on the performance of a tri‐trophic food web

1. Food web interactions are complex and can respond to environmental changes in unpredictable ways that do not necessarily equate to the individual responses of each of the components of the food web. 2. Biomass can be used to evaluate the productivity of the three individual trophic levels, in the form of the Net Generational Productivity (NGP) and the performance of the entire food web with the newly developed tri‐trophic food web performance ratio (?_3t). 3. These parameters were used to evaluate the performance of nine plant‐based tri‐trophic food webs composed of: potato, Solanum tuberosum L. and two cultivars of bell pepper Capsicum annuum L; three biotypes of the aphid Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) and the parasitoid wasp Aphidius ervi (Haliday) (Hymenoptera: Braconidae). 4. The NGP showed that the thermal window for biomass productivity for each trophic level is different and is reduced by approximately 4 °C with respect to the inferior level. Aphidius ervi had the smallest thermal window for biomass productivity and development. 5. The present results showed that the performance (?_3t) of the tested food webs is influenced in a top‐down fashion, where the intra‐specific variation of the food web, namely the host plant, played a major role in the productivity of each of the subsequent trophic levels. 6. The ?_3t suggested that exposure to high and low temperatures might severely affect the effectiveness of A. ervi as a biocontrol agent of the aphid M. euphorbiae in bell pepper and potato crops.     

Plasticity in biochemical characteristics of cotton aphid,Aphis gossypii Glover in response to different host plants and neonicotinoid pesticides

In the present investigation an effort was made to realise the role of feeding host plants on some enzymes’ activities. The results showed that the enzymes’ activities were changed in the aphids feeding on different host plants which assist in detoxification of their host metabolites. It is important when the aphids are exposed to insecticides. The results indicated that the measured enzyme activity has significant changes depending on the host plant. It is shown in this study that there are no significant differences between different host plants on esterase activity (p = 0.446); however, there is a significant difference between GSH activity (p = 0.047) but this relationship is not significant on MFO activity (p = 0.417). Among three strains of Ag-PP, Ag-MO and Ag-FA, strain Ag-PP was the most resistant strain against neonicotinoids, and the resistance mechanism was related to metabolic increase in carboxyl esterase activity. The results showed that strain of Ag-MO was the most susceptible strain against neonicotinoids. The result of this investigation also showed that the general esterases might play an important role in conferring or contributing to neonicotinoid resistance in the cotton aphids.