The relationship between aphid infestations and oviposition by aphidophagous Syrphidae (Diptera)

Oviposition by aphidophagous Syrphidae varies with the size of aphid infestations and different syrphid species have different optimum aphid population sizes for oviposition. In one experiment using potted brussels sprout plants infested with Brevicoryne brassicae L., Platycheirus manicatus (Meig.) preferred about 100 aphids per plant, P. scutatus (Meig.) about 1000 aphids per plant and Syrphus ribesii (L.) about 2000 aphids per plant. These preferences were less clear in certain Platycheirus species (e.g. P. peltatus (Meig.)), than in Syrphus species (e.g. S. luniger Meig.). Once a plant has been selected for oviposition there may still be selection of suitable colonies on that plant. For a given aphid population, S. luniger preferred a small number of large aggregates to a larger number of smaller ones, whereas S. balteatus (Deg.) preferred the opposite. The tendency of the different species to select aphid populations of different sizes and distributions is likely to decrease interspecific competition.     

Some factors influencing the occurrence and site of oviposition by aphidophagous Syrphidae (Diptera)

Syrphids were not deterred from ovipositing on suitable plants by the presence of other syrphid eggs, larvae or larval gut contents. Heavy infestations of Aphis fabae Scop, on bean plants (Viciafaba L.) induced Platycheirus manicatus (Meig.) to lay preferentially on neighbouring uninfested plants. Such behaviour was not found for Syrphus species. Nor did flowers, a source of adult food, stimulate oviposition nearby. The site of oviposition in relation to Brevicoryne brassicae L. on brussels sprouts (Brassicae oleracea gemnifera L.) varied markedly according to species: in similar conditions Syrphus luniger Meig. laid over 50% of its eggs touching aphids and less than 1% on uninfested plants, whereas P. manicatus laid less than 5% touching aphids and over 50% on uninfested plants. Most eggs were laid close to the edge of the leaf, especially by Platycheirus species, e.g. P. scutatus Meig. which laid over 90% within 5 mm of the edge of the leaf.     

Divergent preferences of Rhagoletis pomonella host races for olfactory and visual fruit cues

The quality of different species of aphids as food for aphidiphagous ladybird beetles varies greatly. The optimal oviposition theory predicts that a female should lay eggs preferentially in patches of suitable prey and should be reluctant to oviposit in patches of less suitable prey. A no‐choice experiment was used to test whether aphids (Homoptera: Aphididae) of different suitability influence the oviposition behaviour of the two‐spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae). The results indicate that A. bipunctata females are not more reluctant to lay eggs in the presence of moderately suitable compared to highly suitable aphids. However, females laid fewer eggs in the presence of toxic aphids.     

Aphidophagous guilds on nettle （Urtica dioica） strips close to fields of green pea, rape and wheat

The common nettle （Urtica dioica L.） is a perennial and cosmopolitan plant species and is known to be the source of food for a great diversity of insects. To understand the importance of the nettle in agro-ecosystems, a field experiment was carried out in an experimental farm at Gembloux （Belgium） to study the effect of nettle margin strips on aphid and aphidophagous populations in close field crops, namely wheat （Triticum aestivum L.）, green pea （Pisum sativum L.） and rape （Brassicae napus L.）. The aphids and related beneficial populations were weekly assessed, from March to August 2005, by visual observations in two plots per field crop. A higher abundance of aphidophagous beneficials was collected in nettle strips when compared to the field crops. Particularly, the presence of predatory anthocorids, mirids and green lacewings was observed on nettle only. Nevertheless, the most abundant aphid predatory family, the Coccinellidae, was distributed in both environments, in nettle strips and in crop fields. The field margin supported a significantly higher density ofHarmonia axyridis than the field crops. In contrast, the field crops, green pea particularly, supported a higher density of Coccinella septempunctata. The distribution of the aphidophagous species, mainly the ladybirds, was discussed in relation to the host plant and related aphid species and their potential effect on integrated pest management.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.     

Body size, reproductive allocation, and maximum reproductive rate of two species of aphidophagous Coccinellidae exploiting the same resource

To test the predictions of allometric analyses of laboratory data on aphidophagous ladybirds, a study was carried out on a small [Propylea quatuordecimpunctata (L.); dry female body mass 3.7 mg] and large species (Coccinella septempunctata L.; 15.4 mg) (both Coleoptera: Coccinellidae) of predatory ladybird, which regularly exploit cereal aphids. In 2003–2006, females of C. septempunctata and in 2006 P. quatuordecimpunctata were collected at 2‐ to 5‐day intervals during the 30‐day period around the peak in cereal aphid abundance, and the number of eggs they laid in the following 24 h in the laboratory was recorded. In addition to the number of eggs laid, clutch mass, live weight, and scutum width of ovipositing females and the sizes of the clutches laid in the field were recorded. As predicted, the reproductive allocation in both species was similar. The weight of the eggs of C. septempunctata (0.20 mg) and P. quatuordecimpunctata (0.18 mg) differed little, and the proportion of body mass allocated to daily reproduction (ca. 12%) was identical in both species. In addition, the maximum number of eggs laid per day in the field by the large species was, as predicted, greater than by the small species. Interestingly, the size of the egg clutches laid by C. septempunctata in the field was similar to the daily oviposition of field‐collected adults recorded in the laboratory, whereas for P. quatuordecimpunctata it was significantly smaller. The role of morphology and physiology of ladybirds in structuring aphidophagous ladybird guilds is discussed.     

Assessment of aphid colonies by hoverflies. II pea aphids and 3 syrphid species;Betasyrphus serarius (Wiedemann),Metasyrphus frequens Matsumura andSyrphus vitripennis (Meigen) (Diptera: Syrphidae)

In the aphidophagous syrphid species,Betasyrphus serarius (Wiedemann),Metasyrphus frequens Matsumura andSyrphus vitripennis (Meigen), females in search of oviposition sites assess the qualitative and quantitative value of pea aphid colonies for securing the successful development of their offspring. They select, as their oviposition sites, young and “promising” aphid colonies consisting of nymphs and/or adult aphids including few winged adults. They neglect large, older colonies of 4th-instar nymphs and/or winged adult aphids. The 3 syrphid species adopt “buy-futures” ovipositional tactic as doesEpisyrphus balteatus (de Geer), although some tinge of “spot-transaction” is noticed inM. frequens andS. vitripennis.     

The influence of intraguild competitors on reproductive decisions by two predatory Heteroptera,Orius insidiosus (Anthocoridae) and Nabis americoferus (Nabidae)

The relationship between the oviposition site preferences of predators in the face of intraguild competitors has received little attention, but it likely shapes the reproductive ecology of predatory species. In this study, oviposition intensity and the within-plant distribution of Orius insidiosus (Heteroptera: Anthocoridae) and Nabis americoferus (Heteroptera: Nabidae) eggs on Phaseolus vulgaris plants was studied when the two species were present independently or in combination. Both predators laid more eggs in the presence of the other species relative to when they were only exposed to conspecifics. When only exposed to conspecifics, O. insidiosus preferred to lay eggs on leaves and petioles on the upper half of the plant, whereas N. americoferus laid eggs mostly on the petioles and petiolules equally throughout the height of the plant. But when both species were present, O. insidiosus preferred to lay eggs on the leaf, whereas N. americoferus altered their behavior to lay an even greater proportion of their eggs on the petioles and petiolules. They altered their preferences for different plant strata too: N. americoferus laid more eggs on the upper quarter of the plant when O. insidiosus was present, and O. insidiosus was marginally more likely to lay eggs lower on the plant in the presence of N. americoferus. This study indicates that these two Cimicomorpha can detect the presence of one another, and that they adjust their reproductive decisions, presumably to avoid potential competitive interactions.     

Hoverfly oviposition response to aphids in broccoli fields

The oviposition response of predacious hoverflies (Diptera: Syrphidae) to Brevicoryne brassicae L. and Myzus persicae (Sulzer) (Homoptera: Aphididae) in commercial broccoli, Brassica oleracea var. italica L., Plenck (Brassicaceae), fields was investigated at two sites over the course of a growing season. The hoverfly oviposition responses to these aphid species on different parts of the broccoli plant canopy were also examined. There were no hoverfly eggs on broccoli plants without aphids, egg numbers were very low on plants with fewer than 50 aphids, and no peak in oviposition relative to aphid numbers was observed. Within individual plants that were colonized by aphids, there was some oviposition on individual leaves without aphids, and no hoverfly eggs were seen on leaves that had more than 400 aphids. Leaves in the broccoli plant canopy, and the datasets associated with them, were divided into three sections vertically, ‘upper’, ‘middle’, and ‘lower’. Brevicoryne brassicae was more abundant in the upper and middle canopy sections, while M. persicae was found mostly in the lower section. The rate of hoverfly oviposition per aphid was higher in the upper section than in the two other sections. Modeling of the oviposition response using logistic regression showed that the presence of hoverfly eggs was positively correlated with numbers of each aphid species and sampling date.     

The oviposition behavior ofAphidius ervi andMonoctonus paulensis (Hymenoptera: Aphididae) encountering different host species (Homoptera: Aphididae) in sequential patches

Two-day-old mated females ofAphidius ervi Haliday andMonoctonus paulensis (Ashmead) were each provided with two sequential host patches. Patches were comprised of plastic petri dishes containing either 15 pea aphids,Acyrthosiphum pisum (Harris), or 15 alfalfa aphids,Macrosiphum creelii Davis. Both wasp species parasitized more hosts in patches containing pea aphids than in those containing alfalfa aphids, regardless of sequence. Females ofA. ervi also laid more eggs per aphid in patches containing pea aphids than in patches containing alfalfa aphids. When both patches contained alfalfa aphids,M. paulensis females parsitized more aphids in the second patch than in the first. Fewer alfalfa aphids were parasitized in the second patch when the first patch contained pea aphids, and fewer eggs were laid per alfalfa aphid. Parasitoid females of both species exhibited consistently higher rates of oviposition into their preferred host species and adjusted their reproductive allocation to hosts and host patches as a function of their experience in previous patches.     

Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management

Trichome-based tomato resistance offers the potential to reduce pesticide use, but its compatibility with biological control remains poorly understood. We evaluated Episyrphus balteatus De Geer (Diptera, Syrphidae), an efficient aphidophagous predator, as a potential biological control agent of Myzus persicae Sulzer (Hemiptera, Aphididae) on trichome-bearing tomato cultivars. Episyrphus balteatus’ foraging and oviposition behavior, as well as larval mobility and aphid accessibility, were compared between two tomato cultivars (Lycopersicon esculentum Mill. ‘Moneymaker’ and ‘Roma’) and two other crop plants; broad bean (Vicia faba L.) and potato (Solanum tuberosum L.). Hoverfly adults landed and laid more eggs on broad beans than on three species of Solanaceae. Hoverfly larval movement was drastically reduced on tomato, and a high proportion of hoverfly larvae fell from the plant before reaching aphid prey. After quantifying trichome abundance on each of these four plants, we suggest that proprieties of the plant surface, specifically trichomes, are a key factor contributing to reduced efficacy of E. balteatus as a biological agent for aphid control on tomatoes. Handling editor: Stanislaw Gorb     

Greater impact of host plant species on oviposition of a willow leaf beetle <Emphasis Type="Italic">Plagiodera versicolora</Emphasis> Laicharting (Coleoptera: Chrysomelidae) during the adult stage than in developing larval stage

In some herbivorous insects, such as Coleoptera and aphids, not only the host species of larvae, but also those of adults should be considered as key determinants of potential fecundity because oviposition is affected by the quality of host species during both larval and adult stages. This study examined the relatively greater impact on host species of the larval or adult stage on oviposition of the willow leaf beetle Plagiodera versicolora Laicharting (Coleoptera: Chrysomelidae). We conducted an experiment using a 2 × 2 experimental design, in which either of two different host plant species was fed in larval and adult stages. Females fed on a locally unavailable host Salix eriocarpa in the adult stage did not lay any eggs, but those fed on the locally available host S. babylonica laid 67–75 eggs on average, irrespective of larval host species. Such reproductively inactive females fed S. eriocarpa as an adult host recovered reproductive activity within 3 weeks after changing the host species to S. babylonica. This result indicated that the host species fed in the adult stage had a greater impact on oviposition than in the larval stage.     

Effects of conspecific and heterospecific competitors on feeding and oviposition of a predatory ladybird: a laboratory study

Abstract There are several examples of intraguild interactions among insect predators of aphids, but little is known regarding the effects of interactions on feeding and oviposition of individual competitors in a guild. In the laboratory, we determined the feeding and oviposition responses of a ladybird predator to its conspecific and heterospecific competitors in an aphidophagous guild. Gravid females of Menochilus sexmaculatus (Fabricius) (Coleoptera, Coccinellidae) reduced oviposition, but not feeding, when exposed to immobilised conspecific or Coccinella transversalis (Fabricius) (Coleoptera, Coccinellidae) individuals in the short‐term (3 h) and long‐term (24 h). Feeding and oviposition responses were not affected when M. sexmaculatus females were exposed to larvae or adults of Scymnus pyrocheilus Mulsant (Coleoptera, Coccinellidae) beetles or larvae of the syrphid fly Ischiodon scutellaris (Fabricius) (Diptera: Syrphidae). The ratio of eggs laid to numbers of aphids consumed by M. sexmaculatus females was also affected by the presence of conspecific or C. transversalis larvae. The results suggest that fecundity of this predator may be affected by both conspecific and heterospecific competitors in a patchy resource.     

The role of honeydew as an ovipositional stimulant for two species of syrphids

The influence of honeydew contamination on egg laying by the syrphidsEpisyrphus balteatus (Deg.) andPlatycheirus albimanus (F.) on ears of wheat was investigated in a large laboratory flight cage. Artificially-applied honeydew elicited oviposition byE. balteatus but not byPlatycheirus albimanus.Episyrphus balteatus females landed more frequently on ears contaminated with honeydew than on clean ears, suggesting a response to honeydew volatiles. Honeydew from the rose-grain aphidMetopolophium dirhodum and from the pea aphidAcyrthosiphon pisum stimulatedE. balteatus to lay eggs, whereas honeydew from the nettle aphidMicrolophium carnosum did not. The number of eggs laid byE. balteatus increased with increasing honeydew concentration. At low honeydew concentrations the presence of aphids increased oviposition byE. balteatus, but aphid presence had little effect on the number of eggs laid at high honeydew concentrations.     

Oviposition preferences of Maculinea alcon as influenced by aphid (Aphis gentianae) and fungal (Puccinia gentianae) infestation of larval host plants

Abstract 1. The influence of infestation of the larval host plant Gentiana cruciata on the egg‐laying preferences of the xerophilous ecotype of Alcon Blue butterfly (Maculinea alcon) was studied in a semi‐dry grassland area (Aggtelek Karst Region, Northern Hungary). 2. We examined whether oviposition patterns of females differed when G. cruciata stems were uninfested compared with when they were infested by an aphid (Aphis gentianae) or a rust (Puccinia gentianae) species. 3. Females laid more than 90% of their eggs on fertile, uninfested G. cruciata stems, although these stems comprised only ～ 50% of the total stems available. Stems infested by aphids were similar to uninfested ones in properties that had a strong correlation with egg numbers, and yet there were significantly fewer eggs on infested stems than on intact ones. 4. Females never laid eggs on parts of Gentiana stems infested by aphids, and the presence of Lasius paralienus ants, which have a mutualistic interaction with Aphis gentianae, did not increase the repulsive effect of aphids. Infection of Gentiana by Puccinia did not influence the egg‐laying behaviour of females, even though the flowers and buds of infested stems exhibited a delayed development. 5. Aphid infestation can influence butterfly oviposition patterns through both direct and indirect effects. The presence of aphids directly excluded oviposition, but our data also indicated the possibility of an indirect effect of aphid infestation. Stems that had no aphids at the last egg counting, but were infested prior to it, had significantly fewer eggs than those that were never infested.     

Discrimination of parasitized aphids by a hoverfly predator: effects on larval performance, foraging, and oviposition behavior

The choice of oviposition site by female aphidophagous predators is crucial for offspring performance, especially in hoverflies whose newly hatched larvae are unable to move over large distance. Predator and parasitoid interactions within the aphidophagous guild are likely to be very important in influencing the choices made by predatory hoverfly females. In the present study, the foraging and oviposition behavior of the aphidophagous hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae) was investigated with respect to the parasitized state of its aphid prey, Acyrthosiphon pisum Harris (Homoptera: Aphididae), that were parasitized by Aphidius ervi Haliday (Hymenoptera: Aphidiidae). We also recorded the number of eggs laid by hoverfly females when subjected to parasitized aphids. Furthermore, we studied the influence of being fed with parasitized aphids on hoverfly larval performance. Hoverfly females did not exhibit any preference for plants infested with unparasitized or aphids parasitized for 7 days. On the other hand, plants infested with mummies or exuvia were less attractive for E. balteatus . These results were correlated with (i) the number of eggs laid by E. balteatus females and (ii) larval performance. Thus, our results demonstrate that E. balteatus behavior is affected by parasitoid presence through their exploitation of aphid colonies. Indeed, hoverfly predators select their prey according to the developmental state of the parasitoid larvae.     

VARIATION IN PREFERENCE AND SPECIFICITY IN MONOPHAGOUS AND OLIGOPHAGOUS SWALLOWTAIL BUTTERFLIES

Although variation in oviposition preference and specificity for host plants has been demonstrated within populations of a variety of oligophagous insect species, it is unknown whether genetic variation in host choice is lost within populations of monophagous species. Analysis of a locally monophagous butterfly species, Papilio oregonius, and a locally oligophagous species, P. zelicaon, showed significant variation in oviposition preference within populations of both species. Females of both species chose primarily their native hosts. Nonetheless, the percentages of eggs laid by individual females among the plant species and the number of plant species on which individual females laid eggs differed significantly among isofemale strains within populations. Moreover, some females within all isofemale strains of both species laid a few eggs on Foeniculum vulgare, an umbelliferous species that does not occur in the native habitats of these populations but is a host for Papilio species in other geographic areas. The results suggest that local monophagy and oligophagy in these species reflect the relative ranking among potential plant species. Both populations harbor variation in oviposition choice that could allow for host shifts if these populations invaded new habitats.     

The effects of weed strips on aphids and aphidophagous predators in an apple orchard

Selected weeds were used to attract antagonists of apple aphids in an apple orchard near Berne, Switzerland. In the year before the experiment, in 1991, the apple aphidsDysaphis plantaginea (Pass.) andAphis pomi (DeGeer) and aphidophagous predators were homogenously distributed in the orchard. In April 1992, weed strips were sown between tree rows and along the border parallel to the first and the last row of trees in one part (the other part served as control). In both parts of the orchard, randomly chosen tress were controlled visually in weekly intervals in 1992 and 1993. During flowering of weeds more aphidophagous predators were observed on the apple trees within the strip-sown area than in the control area. The most abundant and permanent aphidophagous predators were spiders, predaceous Heteroptera, Coccinellidae, and Chrysopidae. Both species of aphids were significantly less abundant in the area with weed strips than in the control area during the vegetation period. The effects of the weed strips on aphidophagous predators, and those of predators on aphids, are discussed.     

Is assessment of oviposition sites using conspecific larval cues a general mechanism in aphidophagous ladybirds (Coccinellidae)?

Aphidophagous ladybirds of the Coccinellinae subfamily are deterred from oviposition in the presence of chemical cues deposited by conspecific larvae, therefore avoiding the detrimental effects of competition and cannibalism to their offspring. However, it is still unknown whether aphidophagous species from other Coccinellidae subfamilies similarly behave. Here, we investigate this question for species of the Scymninae subfamily. A GC‐MS analysis of Scymnus interruptus (Goeze) larval tracks shows that larvae deposit a cocktail of hydrocarbons containing at least five branched‐chain alkanes. Furthermore, our experiments on the oviposition behaviour of S. interruptus and S. nubilus (Mulsant) in the presence of conspecific larval tracks and of conspecific larval wax covering Scymninae larvae show that females do not refrain from ovipositing in the presence of these larval cues. We recommend that more attention is paid to the role of Scymnus spp. in the regulation of aphids because their oviposition strategy might strengthen aphid suppression in agrosystems.     

Aphid–hoverfly interactions under elevated CO2 concentrations: oviposition and larval development

The performance of predators of plant pests is mainly driven by their ability to find prey. Recent studies suggest that rising atmospheric carbon dioxide (CO₂) concentrations will affect the semiochemistry of plant–insect relationships, possibly altering prey‐finding behaviour. In the present study, we test the hypothesis that higher atmospheric CO₂ concentrations affect the oviposition behaviour of an aphidophagous hoverfly and alter the development of its larvae. We also test the hypothesis that volatile compounds released by the plant–aphid association are modified under elevated CO_2. Broad bean plants infested with pea aphids are grown under ambient (450 ppm) or elevated CO₂ (800 ppm) concentrations. Plants raised under each treatment are then presented to gravid hoverfly females in a dual‐choice bioassay. In addition, emerging Episyrphus balteatus larvae are directly fed with aphids reared under ambient or elevated CO₂ conditions and then measured and weighed daily until pupation. Odours emitted by the plant–aphid association are sampled. A larger number of eggs is laid on plants grown under ambient CO₂ conditions. However, no significant difference is observed between the two groups of predatory larvae grown under different CO₂ concentrations, indicating that the CO₂ concentration does not affect the quality of their aphid diet. Although plant volatiles do not differ between the ambient and elevated CO₂‐treated plants, we find that the quantity of aphid alarm pheromone is lower on the plant–aphid association raised under the elevated CO₂ condition. This suggests that an alteration of semiochemical emissions by elevated CO₂ concentrations impacts the oviposition behaviour of aphid predators.