Larval competition between Aphidius ervi and Praon volucre (Hymenoptera: Braconidae: Aphidiinae) in Macrosiphum euphorbiae (Hemiptera: Aphididae)

Interspecific competition between parasitoid larvae may influence the size, structure, and stability of the population, leading to a reduction in total parasitism and thus restricting the pest control. Aphidius ervi (Haliday) and Praon volucre (Haliday) are endoparasitoids that possess a wide host range and present considerable potential for the biological control of the aphid Macrosiphum euphorbiae (Thomas). The larval competition between A. ervi and P. volucre, and the possible intrinsic competitive superiority of one of the parasitoids in M. euphorbiae, have been studied. In single parasitism experiments, mated parasitoid females (n=10) were maintained individually in contact with M. euphorbiae hosts (n=30) inside petri dishes containing lettuce leaf discs and maintained in environmental chamber at 22 ± 1°C, 70 ± 10% RH, and 12-h photophase. The multiple parasitism experiments consisted of exposing single parasitized aphids (n=120) to the second parasitoid species. Two oviposition events were performed with a 4-h interval between them, namely the following: sequence A (oviposition by A. ervi, followed by P. volucre) and sequence B (oviposition by P. volucre, followed by A. ervi). Oviposition sequence A generated 24 A. ervi and 55 P. volucre adults, whereas oviposition sequence B generated 23 and 49 adults. P. volucre is an intrinsically superior competitor compared with A. ervi, and the use of the two species simultaneously may result in competitive exclusion and influence the stability of the parasitoid population.     

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.     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

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

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

A survey of aphids and aphid parasitoids in cereal fields in Denmark, and the parasitoids' role in biological control

In 1996 and 1997 a field survey of the abundance and species composition of cereal aphid primary and secondary parasitoids in spring barley, winter wheat and durum wheat was conducted in Zealand, Denmark. The purpose was to create a better understanding of the mechanisms underlying aphid–parasitoid dynamics in the field. Such an understanding can be used when developing biological control methods in cereals. In both years aphid attacks in cereals began in late June and never exceeded the economic threshold. In 1996 the first aphids were found in wheat on 26 June; in 1997 the first aphids were found on 24 June on both crops. The highest densities reached in 1996 were an average of six aphids per shoot in winter wheat and one aphid per shoot in spring barley. In 1997 the highest densities reached were 11 aphids per shoot in winter wheat and four aphids per shoot in spring barley. The aphid population collapsed by the end of July to early August in 1996, but it collapsed by mid-July in 1997. The onset and peak of parasitization were delayed in comparison to aphid infestation. Parasitism was 20–60% by the end of the cropping season in spring barley, and 30–80% in winter wheat and durum wheat in 1996. In 1997 parasitism did not exceed 3–11% in barley and was less than 2% in one winter wheat field but more than 40% in the other winter wheat field sampled. In both years most parasitism was due to Aphidiidae (Hymenoptera). The two dominant species were Aphidius ervi Haliday and Aphidius rhopalosiphi De Stefani-Perez. Hyperparasitism began after primary parasitism and increased progressively during the cropping season. The two years were similar in many respects, including for species composition of aphids and parasitoids. The late start of the aphid infestation may have contributed to the high level of parasitization found in 1996, but in 1997 the aphid infestation period was so short that a parasitoid population did not have time to build up.     

Semiochemicals associated to spacing behaviour of the bird cherry-oat aphid Rhopalosiphum padi L. (Hem., Aphididae) do not affect the olfactometric behaviour of the cereal aphid parasitoid Aphidius rhopalosiphi De Stephani-Pérez (Hym., Braconidae)

Volatiles produced by the interaction of Rhopalosiphum padi and wheat, and semiochemicals which elicit the spacing behaviour of R. padi on wheat and oat, were evaluated in an olfactometer against the cereal aphid parasitoid Aphidius rhopalosiphi . The parasitoid was attracted by volatiles produced by the R. padi -wheat interaction at high density of aphids, but not by the R. padi -wheat interaction at low density. Compounds produced by the interaction of wheat or oat that was infested with a high density of aphids (approximately 9 aphids/cm²), 6-methyl-5-hepten-2-one (MHO), 6-methyl-5-hepten-2-ol (MHOH), 2-tridecanone (2-T), and methyl salicylate (MS), neither attracted nor repelled A. rhopalosiphi as pure compounds or in the naturally occurring mixture. The results are discussed in terms of the use of semiochemicals and parasitoids in the integrated management of aphid pests.     

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

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

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

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

Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi

Aphidius ervi and Aphidius eadyi, two parasitoids of the pea aphid Acyrthosiphon pisum, were attracted to components of the aphid sex pheromone in laboratory bioassays. Pre-test experience with host aphids in the presence of aphid sex pheromone did not affect the response of A. ervi to pheromone in a 4-way olfactometer, compared with that of naive parasitoids. Aphidius ervi females exposed only to the pheromone prior to testing did not respond in the olfactometer, suggesting habituation to the foraging cue by the parasitoid. In a wind tunnel, aphid sex pheromone increased the attraction of A. ervi to the plant-host complex (Vicia faba/A. pisum), suggesting an additive effect when two different foraging cues are present simultaneously.     

A physiologically based model of pest–natural enemy interactions

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

Evidence for the existence of a species closely related to the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez based on host ranges, morphological characters, isoelectric focusing banding patterns, cross-breeding experiments and sex pheromone specificities (Hymenoptera, Braconidae, Aphidiinae)

Abstract. Host transfer trials with six strains of the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez revealed the presence of two differing host ranges: three strains parasitized Sitobion uvenae (F.) and S.fragariae (Wlk.) exclusively, whereas the others successfully developed in both Sitobion species and also in Metopolophium dirhodum (Wlk.), M.festucue cerealiurn Stroyan, Rhopalosiphum padi (L.) and Diuraphis muehlei Börner. The two host range groups were poorly distinguishable by means of morphological characters. In con trast, isoelectric focusing proved to be a much better tool for discrimi nation. Reproductive isolation between the two host range groups was clear but not complete, as evidenced by crossing experiments with laboratory-bred and field-collected material. Under field conditions, males showed a specific response to virgin females of the two groups. Hence, the sex pheromones of the females were obviously different. Considering these results, a species ( Aphidius sp. A) closely related to A.rhopalosiphi seems to occur. As a detailed study of morphological characters is still lacking, Aphidius sp. A is not yet formally established here. Due to its dependence upon Sitobion spp., Aphidius sp. A may be an economically important parasitoid of the pest aphid S.avenae .     

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.     

Aphid clonal resistance to a parasitoid fails under heat stress

Parasitoid virulence and host resistance are complex interactions depending on metabolic rate and cellular activity, which in aphids additionally implicate heritable secondary symbionts among the Enterobacteriaceae. As performance of the parasitoid, the aphid host and its symbionts may differentially respond to temperature, the success or failure of aphid parasitism is difficult to predict when temperature varies. We tested the hypothesis that resistance of the pea aphid Acyrthosiphon pisum to the parasitoid Aphidius ervi, which is linked to aphid secondary symbionts, may depend on temperature in several resistant and non-resistant aphid clonal lineages of different geographic origin and of known bacterial symbiosis, using experiments in controlled environments. Complete immunity to A. ervi at 20 degrees C in three different aphid clones whose symbiosis is characterized by the possession of Hamiltonella defensa reversed to high susceptibility at 25 degrees C and especially 30 degrees C, suggesting that the aphid's immune responses to the establishment and early development of the parasitoid is strongly reduced at moderately high temperatures. There was no evidence that a pea aphid control genotype that was susceptible to A. ervi at 20 degrees C could become more resistant as temperature increases, as has been suggested for insect fungal pathogens. By contrast, our results suggest that aphid clonal resistance to A. ervi and related parasitoids is characteristic of cool temperature conditions, similar to various other fitness attributes of aphids. Based on evidence that H. defensa symbionts characterized all three A. ervi resistant pea aphid clones studied, but was absent in control aphids that remained susceptible at all temperatures, we suggest that secondary symbiosis plays a key role in the heat sensitivity of aphid clonal resistance. Our study may also indicate that aphid natural control of variably susceptible host populations by aphid parasitoids is more likely at moderate to high temperatures.     

Host age and fitness-related traits in a koinobiont aphid parasitoid

Abstract.  1. Trade-offs play a key role in species evolution and should be found in host–parasitoid interactions where the host quality may differ between host age categories.
2. The braconid wasp, Aphidius ervi , is a solitary endoparasitoid that allows its aphid hosts to continue to feed and grow after parasitisation. The hypotheses that host age influences their quality and that female parasitoids exploit their hosts based on that quality were tested under laboratory conditions using no-choice tests.
3.  Aphidius ervi females accepted the aphid Myzus persicae for oviposition and their progeny developed successfully in all host ages. The fitness-related traits of parasitoids did not increase linearly with the host age in which they developed. Host quality was found to be optimal at intermediate host ages and the females preferred to parasitise these hosts. The shortest progeny development time and a more female-biased sex ratio were observed in hosts of intermediate age.
4. This study suggests the existence of multiple interactive trade-offs occurring during host–parasitoid interactions according to host age related quality.     

Snowdrop lectin (Galanthus nivalis agglutinin) in aphid honeydew negatively affects survival of a honeydew- consuming parasitoid

1 Insecticidal proteins can be excreted in the honeydew when sap-sucking insects feed on insect-resistant transgenic plants. Honeydew can be an important source of carbohydrates, thus potentially exposing a broad range of honeydew-feeding insects to transgene products.
2 Snowdrop lectin ( Galanthus nivalis agglutinin; GNA) dissolved in a 2 m sucrose solution had no antifeedant effect on female aphid parasitoids ( Aphidius ervi ) but had a direct negative effect on their longevity.
3 When feeding on honeydew from Rhopalosiphum padi feeding on a GNA-containing artificial diet, Aphidius ervi suffered a longevity reduction that was more pronounced than was to be expected based on the detected GNA concentration in the honeydew.
4 Analysis of carbohydrate and amino acid composition revealed that a change in honeydew composition caused by a GNA-effect on the aphids could be a possible explanation for the additional reduction in parasitoid longevity.
5 When comparing the effect of honeydew from Sitobion avenae and R. padi feeding on GNA-expressing or nontransformed wheat plants on A. ervi longevity, aphid species was found to have a significant effect, whereas the wheat variety had no effect. The latter result was probably due to low GNA expression levels in the plants. Differences in nutritional suitability between honeydew from R. padi and S. avenae could be explained by differences in carbohydrate and amino acid composition.
6 This is the first study to demonstrate that GNA ingested by aphids and transported into the honeydew can negatively affect the parasitoids consuming this honeydew.
7 We recommend that honeydew should be considered as a route of exposure to transgene products in future risk assessment studies.     

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

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

Landscape structure and agricultural intensification are weak predictors of host range and parasitism rate of cereal aphids

Proportions of specialist and generalist primary parasitoids have been described by the resource breadth and the trade-off hypothesis. These alternative hypotheses predict either decreased or increased, respectively, parasitism rate of shared aphid species by specialist parasitoids. We tested both hypotheses and the confounding effects of landscape structure and agricultural intensification (AI) using extensive samplings of aphids and their parasitoids in Polish agricultural landscapes. Abundances, species composition of aphids, primary parasitoids, and parasitism rate of aphids by specialists and generalist parasitoids were analysed. Contrary to our expectations we found equally decreased parasitism rates by both types of primary parasitoids at higher aphid densities and thus proportion of specialists to generalists did not change with increasing host density. In line with the resource breadth hypothesis, specialist parasitoids had always lower abundances and parasitism rates than generalist parasitoids. Landscape diversity and agricultural intensification did not influence the host-parasitoid population dynamics. We speculate that these contrasting results could be caused by the additional density effects of secondary parasitoids. We conclude that simplistic two-trophic-level population models are not able to fully describe the complex dynamics of trophic networks. We also argue that agricultural intensification has lower effects on abundance and effectiveness of parasitoids than predicted by respective predator–prey models and empirical studies performed in controlled and artificial conditions.     

Hopkins' 'host selection principle', another nail in its coffin

Abstract. Adult female parasitoids (Aphidius rhopalosiphi De Stef.) (Hymenoptera: Aphidiidae) reared on the aphid Metopolophium dirhodum (Walk.) (Homoptera: Aphididae) changed their responses to odours of two wheat cultivars ('Maris Huntsman' and 'Rapier') when the parasitized aphids had been moved from the former to the latter cultivar at various times after parasitization. If the aphids were moved after less than 6 days, the female parasitoids emerging from mummies by then formed on 'Rapier' responded positively to that cultivar, whereas parasitoids emerging from mummies transferred as still living aphids after 8 days on 'Maris Huntsman', responded positively to that cultivar rather than to 'Rapier' on which they had emerged. This appeared to be evidence for Hopkins' 'host selection principle', which states that chemical experience acquired by the larva of an endopterygote insect can be transferred through the pupal stage to the adult. However, discrimination in favour of either cultivar disappeared when the parasitoids were reared in aphids on both cultivars, and the emerging females were tested following excision of the pupae from the aphid mummies. The previous discrimination shown by adult parasitoids emerging from aphid mummies must therefore be determined by the chemicals contacted by a parasitoid on the skin of the mummy or while biting its way out of the dead aphid.     

Spatially aggregated parasitism on pea aphids, Acyrthosiphon pisum, caused by random foraging behavior of the parasitoid Aphidius ervi

We investigated the role of the foraging behavior of the parasitoid wasp Aphidius ervi in producing nonrandom spatial patterns of parasitism among pea aphids, Acyrthosiphon pisum . We measured spatial variability in percent parasitism by determining the number of aphids and percent parasitism in 40 sampling plots (0.65-m2 circles) located within a homogeneous alfalfa field. In one replicate of this experiment, mean parasitism of aphids was 18.7%, and percent parasitism showed density-independent aggregation (i.e., greater than random variability in percent parasitism among sampling plots). In the other replicate, mean parasitism was 56.3%, and percent parasitism was not aggregated among plots. We used a combination of field observations of parasitoid foraging and mathematical models to explore these results. In particular, we asked whether the presence or absence of density-independent aggregation at different mean percent parasitism can be explained even if parasitoids forage randomly, without changing their behavior in response to encounters with aphids. Observations show that parasitoids tend to move short distances between nearby alfalfa stems (mean=10.8 cm), and the turning angle between successively visited stems was uniformly distributed. We incorporated this behavior into both simulation and analytical models of parasitoid foraging. The models show the same pattern as that observed in the field: parasitism is aggregated in a density-independent fashion when mean percent parasitism is low but not when mean percent parasitism is high. Therefore, density-independent aggregation in percent parasitism does not necessarily imply behavioral responses of parasitoids to host encounters and previously parasitized hosts.     

The response of aphid secondary parasitoids to different patch densities of their host

Aphids are attacked by a large guild of natural enemies including many primary parasitoids which mummify their hosts. These mummies are themselves attacked by a guild of mummy parasitoids which are potentially important in regulating primary parasitoids at densities below which they can exert biological control. The response of mummy parasitoids to mummy densities was investigated in an experiment in which mummy densities of the pea aphid (Acyrthosiphon pisum) attacked by the parasitoid Aphidius ervi were manipulated across host plant patches. Overall, the risk of parasitism was density independent, though with very high inter-patch variability which may allow probabilistic refuges from secondary parasitism. Six species of four genera of mummy parasitoids were recorded. Of the responses of the individual genera, Coruna were reared most frequently from patches of high host density while amongst patches from which Syrphophagus was reared parasitism was inversely density dependent.