Host specialization in habitat specialists and generalists

Generalists and specialists use different cues to find their habitat and essential resources. While generalists have the advantage of exploiting a wider range of resources, they are predicted to be less efficient in using one particular resource compared to specialists. The level of specialization of parasitoids can be either at the habitat or at the host level; strategies used by either type are expected to differ. We examined interactions between three aphid parasitoid species that are a habitat specialist Aphidius rhopalosiphi, a habitat generalist Aphidius ervi, and a host generalist Praon volucre on three cereal aphids, Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi. We compared total parasitism rate across behavioral and physiological variation in a non-choice test. Next, we addressed total parasitism in two phases to examine: (1) the response of parasitoids to different hosts through the behavioral sequence from antennation through oviposition, and (2) the physiological suitability of different hosts for oviposition and larval development. Parasitization typically involved the following behavioral steps: (1) antennal contact, (2) abdominal bending, and (3) ovipositor insertion (acceptance). A. rhopalosiphi had the same number of antennal contacts with the three aphids but showed fewer instances of abdominal bending towards R. padi. Pre-contact host preference was found for A. ervi but it did not correspond to the level of acceptance. The number of antennal contacts by P. volucre corresponded to the parasitization level of the aphid species but more mummies were produced on M. dirhodum than on R. padi. These results suggest that parasitoid species that are habitat specialists react similarly to the different host species present in the same habitat, whereas generalist species exhibit clear preferences during host selection. Preferences were, however, not always related to host suitability.     

Aphid parasitoid complex in potato in the context of IPM in Belgium

Parasitic hymenoptera of potato aphids were collected and identified in 2000 and 2001 in 11 potato fields in Belgium. Nine Aphidiidae species, parasiting seven aphid species, were found: Aphidius ervi, Aphidius matricariae, Aphidius picipes, Binodoxys angelicae, Diaeretiella rapae, Praon abjectum, Praon gallicium, Praon volucre and Toxares deltiger. A. ervi and A. picipes were the dominant and sub-dominant species, with 54% and 28% of the primary parasite collected, respectively. Both species and T. deltiger were found on Aphis nasturti, Aulacorthum solani, Macrosiphum euphorbiae and Myzus persicae, the four most important aphid potato in Belgium. Parasitism rate of A. nasturtii and, to a lesser extent, M. euphorbiae was low compared to A. solani and M. persicae. Parasitism of A. solani was particularly high, with 63.5% in 2000 and 89.2% in 2001, and this species was the preferred host of several Aphidiid species. The abundance of alternative hosts as other crops pest aphids or non-pest aphids on wild plants in agroecosystems could explains the efficacy of these species. The biological control of A. nasturtii and M. euphorbiae by parasitic hymenoptera was poorer, and several studies need to be undertaken to find suitable parasitic hymenoptera species effective on these aphids and agro-environmental measures able to promote them.     

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.     

Electrophoretic 'keys' for the identification of parasitoids (Hymenoptera: Braconidae: Aphelinidae) attacking Sitobion avenae (F.) (Hemiptera: Aphididae)

Polyacrylamide gel electrophoresis was used to construct electrophoretic 'keys' for identifying larval, pupal and adult hymenopterous parasitoids of Sitobion avenae (F.). In general, for each parasitoid and enzyme system tested, all life stages gave similar banding patterns. Although five enzyme systems were tested, esterase was found to be the most useful single system. Using laboratory-reared parasitoids and staining for esterase activity, all species examined, except Aphidius rhopalosiphi and A. ervi could be readily distinguished with the aid of the appropriate key.     

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.     

Interspecific variation in the response to low temperature storage in different aphid parasitoids

Cold storage of natural enemies usually involves placing insects under constant subambient temperatures. Even at non-freezing temperatures, a reduction in survival is the norm. Using fluctuating thermal regimes (FTR) instead of constant low temperature (CLT) has shown that mortality due to accumulation of chilling injuries was significantly reduced in Aphidius colemani . Whether this phenomenon can be generalised to other parasitoid species is not known. The aim of this study was to analyse interspecific variation in the ability to tolerate cold storage under CLT (continuous 2°C) versus FTR (daily cycle: 2°C for 22 h and 20°C for 2 h) for various durations (0–20 days). Survival, sex ratio and development of five different Aphidiine parasitoids were analysed: A. colemani , Aphidius ervi , Aphidius matricariae , Ephedrus cerasicola and Praon volucre. A marked interspecific variation in the ability to tolerate cold storage was observed: A. matricariae and A. ervi were most chill tolerant, P. volucre and E. cerasicola had an intermediate chill sensitivity and A. colemani was most chill sensitive. In all species tested, FTR significantly reduced cold-induced mortality. This phenomenon was manifested more in chill-sensitive species as they probably accumulate chilling injuries more rapidly. The sex ratio remained unaffected in all the species. Interspecific variation was also observed in developmental responses to cold storage. Under CLT, time to adult emergence of A. matricariae, A. colemani, A. ervi and P. volucre was temporarily stopped and in E. cerasicola it increased. Under FTR, the short daily intervals at 20°C for 2 h allowed parasitoids to continue development in all the species. Interspecific differences are discussed. This study suggests that positive impact of FTR may apply to a wide range of species.     

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.     

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.     

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.     

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.     

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 .     

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.     

Evaluation of the establishment of Aphidius ervi Haliday (Hymenoptera: Braconidae) in lucerne aphid populations in New South Wales

The aphid parasitoid Aphidius ervi was released in the major lucerne-growing areas of New South Wales (NSW), Australia, between 1978 and 1981. With the collaboration of district agronomists of the New South Wales Department of Agriculture, five State-wide surveys were conducted in 1982–1983 to determine the success of the release program. In each survey, the distribution of the parasitoid was checked in relation to populations of the aphids Acyrthosiphon kondoi Shinji and Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae). The surveys confirmed the successful dispersal and establishment of A. ervi in the major lucerne-growing areas of NSW. They demonstrated its ability to survive and recover rapidly after a severe and widespread drought.     

Influence of the aphid pathogen Pandora neoaphidis on the foraging behaviour of the aphid parasitoid Aphidius ervi

Abstract.  1. The parasitoid Aphidius ervi and the entomopathogenic fungus Pandora neoaphidis both require successful invasion of an aphid host to complete their life cycle. A shorter developmental period allows P. neoaphidis to out-compete A. ervi. Aphidius ervi may reduce this fitness cost by avoiding aphid colonies containing P. neoaphidis . Here the response of A. ervi towards P. neoaphidis was assessed using sequential experiments designed to replicate different stages of parasitoid foraging behaviour.
2. Entry rate experiments showed that A. ervi entered aphid colonies containing P. neoaphidis -sporulating cadavers and that there was no significant difference in the attraction of A. ervi to aphid-damaged Vicia faba plants containing either healthy Acyrthosiphon pisum or P. neoaphidis -sporulating cadavers.
3. Observational behavioural experiments indicated that the presence of P. neoaphidis did not affect the search time or total foraging time of A. ervi on V. faba plants infested with either healthy A. pisum or P. neoaphidis -sporulating cadavers.
4. In Petri dish bioassays using aphids infected with P. neoaphidis over a period of 120 h, A. ervi showed no difference in attack rate against uninfected aphids or living aphids infected with P. neoaphidis for 1, 24, 48, 72, or 96 h. However, sporulating cadavers (120 h infection) were not attacked.
5.  Aphidius ervi appears only able to detect the presence of P. neoaphidis once the host is dead and sporulation has started. The fitness of A. ervi may therefore be severely reduced when foraging in P. neoaphidis -infected aphid colonies.     

Limitation of superparasitism by Aphidius rhopalosiphi: a consequence of aphid defensive behaviour

Abstract. 1. The behavioural mechanisms limiting superparasitism by Aphidius rhopalosiphi (DeStefani-Perez) are described.
2. A.rhopalosiphi did not discriminate between parasitized and unparasitized aphids, or avoid attacking and ovipositing in previously parasitized aphids.
3. Aphid defensive behaviour was increased for a short period after a parasite stabbing attack. In response to this behaviour the number of parasite stabbing attacks subsequently undertaken declined.
4. Once a stabbing attack had been initiated, parasite oviposition success was unaffected by aphid defensive behaviour.
5. It is concluded that applied defensive behaviour, by limiting the number of stabbing attacks undertaken by A.rhopalusiphi , effectively limits the number of parasite eggs laid and the extent to which super parasitism occurs.     

Primary and secondary parasitoids (Hymenoptera) of aphids (Hemiptera: Aphididae) on blueberry and other Vaccinium in the Pacific Northwest

Blueberry scorch virus, a commercially important Carlavirus in highbush blueberry, Vaccinium corymbosum L., is vectored by aphids (Hemiptera: Aphididae). We surveyed the aphids, primary parasitoids (Hymenoptera: Aphelinidae, Braconidae), and associated secondary parasitoids (Hymenoptera: Charipidae, Megaspilidae, Pteromalidae) on highbush blueberry and other Vaccinium in the Pacific Northwest from 1995 to 2006, with samples concentrated in 2005 and 2006, to lay the groundwork for augmentative biological control. Ericaphis fimbriata (Richards) was the principal aphid. The dominant parasitoid species were Praon unicum Smith, Aphidius n. sp., A. sp., and Aphidius ervi Haliday. Their frequency in relation to the other primary parasitoids varied significantly with geographical area; P. unicum dominated the frequency distribution in southwestern British Columbia, A. n. sp., west of the Cascades, and A. sp. and A. ervi east of the Cascades. Among the secondary parasitoids, pteromalids dominated, and their frequency in relation to the other secondary parasitoids was lowest in southwestern British Columbia. The parasitization rate for P. unicum and A. n. sp. in southwestern British Columbia increased from May or June to a maximum of 0.080 +/- 0.024 and 0.090 +/- 0.084 (SD), respectively, in late July or early August. P. unicum emerged in the spring 4 wk before A. n. sp. The parasitization rate for P. unicum was lower in conventional than organic fields. Whereas aphid density increased monotonically, P. unicum had two spring peaks. A simulation model showed that these peaks could reflect discrete generations. Releases of insectary-reared P. unicum at 150 or 450 DD above 5.6 degrees C, summing from 1 January, may effectively augment the natural spring populations by creating overlapping generations.     

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.     

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.     

An 'artificial aphid' for Aphidius ervi (Hym., Braconidae)

Abstract:  An artificial aphid was developed by making parafilm^® bubbles filled with aphid haemolymph and its suitability for parasitoid oviposition was tested. Aphidius ervi accepted the parafilm^® aphid and laid eggs on it. By stretching, the thickness of the parafilm could be changed. The thicker the parafilm, the higher was the mean number of ovipositional stings and the lower the mean number of eggs released by A. ervi .