The effect of egg load and host deprivation on oviposition behaviour in aphidophagous hoverflies

1. Two species of aphidophagous hoverfly, Episyrphus balteatus and Syrphus ribesii, were tested for the effects of egg load and host deprivation on oviposition choices. 2. Egg load affected the total number of eggs laid in E. balteatus but not in S. ribesii, however it did not affect the proportion laid on any one aphid in E. balteatus but did affect the proportion laid on any one aphid in S. ribesii. The rank order of preferences remained unchanged by age or host deprivation. 3. The dominant effects on host choices were aphid species (in both syrphids) and presentation order (in E. balteatus). 4. Being deprived of hosts increased egg load substantially in E. balteatus, and increasing time of deprivation also had an effect on discrimination; there was no effect of host deprivation in S. ribesii. 5. Reasons for these patterns are discussed.     

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     

Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus

Introductions of the harlequin ladybird Harmonia axyridis into Belgium for aphid biological control have been followed by declines in native aphid natural enemies. We first examined, in laboratory and field conditions, the impact of larval mobility of either H. axyridis or Episyrphus balteatus, the most abundant native hoverfly in central Europe, on aphid suppression. The hoverfly larvae consumed more aphids (Megoura viciae) in a short term, whereas the ladybird ones were more efficient in a long term. We second investigated the intraguild interactions between H. axyridis and E. balteatus larvae and adults. In larva pairings between the two species in laboratory microcosms containing aphid (M. viciae) infested broad bean (Vicia faba) plants, H. axyridis had an intraguild predation (IGP) advantage over the hoverfly. When conspecific larvae were paired together on aphid‐infested plants, no cannibalism between them was detected. The presence of either H. axyridis or E. balteatus larvae on aphid‐infested plants negatively influenced the ovipositional behaviour of H. axyridis and E. balteatus females; lower numbers of laid eggs were recorded compared to control treatment. Moreover, eggs laid by E. balteatus females were also dropped as victims of predation mainly by H. axyridis larvae. Our results suggest that while the exotic ladybird was more efficient in aphid biological control, larvae and eggs of the native hoverfly species face increased IGP by H. axyridis, which would contribute, as a consequence, to the decline in E. balteatus population following invasion.     

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.     

Predatory hoverflies select their oviposition site according to aphid host plant and aphid species

The hoverfly Episyrphus balteatus De Geer (Diptera: Syrphidae) is an abundant and efficient aphid‐specific predator. Several aphidophagous parasitoids and predators are known to respond positively to aphid‐infested plants. Semiochemicals from the latter association usually mediate predator/parasitoid foraging behavior toward sites appropriate for offspring fitness. In this study, we investigated the effect of aphid host plant and aphid species on foraging and oviposition behavior of E. balteatus. Behavioral observations were conducted using the Noldus Observer v. 5.0, which allows observed insect behavior to be subdivided into different stages. Additionally, the influence of aphid species and aphid host plant on offspring fitness was tested in a second set of experiments. Acyrthosiphon pisum Harris and Megoura viciae Buckton were equally attractive for E. balteatus whereas Aphis fabae Scopoli (all Homoptera: Aphididae) were less attractive. These results were correlated with (i) the number of eggs laid, which was significantly higher for the two first aphid species, and (ii) the fitness of hoverfly larvae, pupae, and adults. Two solanaceous plant species, Solanum nigrum L. and Solanum tuberosum L. (Solanaceae), which were infested with Myzus persicae Sulzer (Homoptera: Aphididae), were also compared using the same approach. Discrimination between these two M. persicae host plants was observed, with S. tuberosum being preferred as an oviposition site by the predatory hoverfly. Larval and adult fitness was correlated with the behavioral observations. Our results demonstrated the importance of the prey–host plant association on the choice of the oviposition site by an aphid predator, which is here shown to be related to offspring fitness.     

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.     

Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus

To cope with pathogen and insect attacks, plants develop different mechanisms of defence, in both direct （physical and chemical） and indirect ways （attractive volatiles to entomophagous beneficials）. Plants are then able to express traits that facilitate ＂top-down＂ control of pests by attracting herbivore predators. Here we investigate the indirect defence mechanism of potato plants by analyzing the volatile patterns of both healthy and aphid- infested plants. Important changes in the emitted terpene pattern by the Myzus persicae infested host plant were observed. Using Solid Phase MicroExtraction （SPME） and GC-MS, the （E）-fl-farnesene （EBF） appeared to be emitted by aphid-infested potato and not by healthy plants. To assess the infochemical role of these volatile releases after aphid damage on the aphidophagous predators Episyrphus balteams, the hoverfly foraging behavior was assessed using the Observer 5.0 software （Noldus, Wageningen, The Netherlands）. Aphidfree potato plants were also used as a control volatile source in the predator behavioral study. While aphid-infested plants induced efficient searching and acceptation behaviors leading to egg-laying, no kairomonal effect of healthy potato plants was observed, leading to longer immobility durations and shorter searching periods in the net cage. High oviposition rate of E. balteatus was observed when aphid-infested potato was used （mean of 48.9 eggs per laying and per female）. On the other hand, no egg was produced by the hoverfly on healthy aphid-free plants. The E. balteatus foraging and reproductive behaviors according to the volatile emission from aphid-infested plants are discussed in relation to the potential use of active infochemical molecules in integrated aphid pest management.     

Influence of intraguild predation between Episyrphus balteatus and Hippodamia variegata on their prey

Intraguild predation (IGP) is an interaction that frequently occurs in natural enemy communities, especially aphidophagous predators. This research investigated IGP intensity between Episyrphus balteatus De Geer (Diptera: Syrphidae), with Hippodamia variegata Goeze (Coleoptera: Coccinellidae). Five predator combinations including second and third larvae of H. variegata and third instar larvae of E. balteatus plus control treatment (totally six treatments) were tested. The effect of IGP on cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae) population density was investigated on sweet pepper seedlings under laboratory microcosms. In most combinations, the third instar larvae of E. balteatus alone reduced an A. gossypii population more efficiently than ladybird larvae and their combinations. Furthermore, IGP between third instar of E. balteatus and second larvae of H. variegata was asymmetrical; second instar H. variegata larvae were always the intraguild prey for third instar E. balteatus. The obtained result showed that outcome of IGP interaction on cotton aphid density was non-additive.     

Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi （Hymenoptera： Aphidiinae）

Intraguild predation （IGP） can be an important factor influencing the effective- ness of aphid natural enemies in biological control. In particular, aphid parasitoid foraging could be influenced by the presence of predators. This study investigated the effect of larvae of the predatory hoverfly Episyrphus balteatus DeGeer （Diptera： Syrphidae） and the multicolored Asian ladybird Harmonia axyridis Pallas （Coleoptera： Coccinellidae） on the foraging behavior of the aphid parasitoid, Aphidius ervi Haliday （Hymenoptera： Aphidiidae） in choice experiments using a leaf disc bioassay. Wasp response to chemical tracks left by those predator larvae was also tested. Parasitoid behavior was recorded using the Observer （Noldus Information Technology, version 5.0, Wageningen, the Netherlands）. The experiments were conducted under controlled environmental conditions using leaves of the broad bean plant, Viciafaba L. （Fabaceae） with Myzus persicae Sulzer （Homoptera： Aphididae） as the host complex. A. ervi females avoided aphid patches when larvae of either predator were present. A similar avoidance response was shown by A. ervi to aphid patches with E. balteatus larval tracks, whereas no significant response was observed to tracks left by H. axyridis larvae. It was concluded that IG predator avoidance shown by the aphid parasitoid A. ervi may be a factor affecting their distribution among host patches.     

Effect of hunger on the allocation of time among pea plants by the larvae of an aphidophagous hover fly,Eupeodes corollae [Dipt: Syrphidae]

We observed the movement of predatory larvae of the syrphid flyEupeodes corollae (F.) (formerlyMetasyrphus corollae) among small pea plants with and without aphids. Starved larvae spent longer time than well-fed larvae on similar plants and both groups of larvae stayed longer on plants with aphids than on plants without aphids. On plants with aphids, larvae which failed to capture prey left the plant sooner than those which captured aphids. The capture of at least one aphid on a plant increased the persistence of syrphid larvae. The average rate of energy gain was higher for well-fed larvae than for starved larvae because starved larvac stayed on plants even when their rate of return was lower. When larvae that had captured aphids left plants, their rate of energy gain, tended to be lower than at any time following capture of the 2^nd, aphid. The 1^st aphid was captured in less time than similar larvae spent on plants without aphids. Time between captures of aphids by well-fed larvae was less than the time such larvae spent on plants without aphids. Among starved larvae, the intercatch intervals were similar to the time on plants without aphids. We discuss the significance of these results relative to current predator foraging theory and the efficiency ofE. corollae as a biological control agent.      

Intraguild Predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and Other Aphidophagous Predators

Aphidophagous predators compete for the same prey species. During their foraging activity they frequently encounter heterospecific aphid predators. These situations can lead to intraguild predation and may disrupt biological control efforts against aphids where more than one predator species is present. We investigated the behavior of larvae of the hoverfly Episyrphus balteatus de Geer and its interaction with three other aphid predators: the ladybird Coccinella septempunctata L., the lacewing Chrysoperla carnea Stephens, and the gall midge Aphidoletes aphidimyza (Rondani). Interspecific interactions between predators were examined in arenas of different sizes and in the presence of extraguild prey. The outcome of interactions between E. balteatus larvae and the other predators depended predominantly on the relative body size of the competitors. Relatively large individuals acted as intraguild predators, while relatively smaller individuals became intraguild prey. Eggs and first- as well as second-instar larvae of E. balteatus were highly susceptible to predation by all other predators, whereas pupae of E. balteatus were preyed upon only by the larvae of C. carnea. Interactions between A. aphidimyza and E. balteatus were asymmetric and always favored the latter. Eggs and first- as well as second-instar larvae of E. balteatus sustained intraguild predation irrespective of the size of the arena or the presence of extraguild prey. However, the frequency of predation on third-instar larvae of E. balteatus was significantly reduced. This study indicated that the same species can be both intraguild predator and intraguild prey. It is suggested that combinations of predators must be carefully chosen for success in biological control of aphids.     

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.     

Assessment of the maple aphid colony by the hover fly,Episyrphus balteatus (de Geer) (Diptera: Syrphidae) I

The aphidophagous syrphid fly,Episyrphus balteatus (de Geer), actively visits the Japanese maple,Acer palmatum Thunb., in early spring and oviposits adjacent to colonies of 2 maple aphids,Periphyllus californiensis (Shinji) andYamatocallis tokyoensis (Takahashi). Female flies, in the field, chose small, young colonies with nymphs and wingless adult aphids for their oviposition sites rather than older colonies including winged adults. Same tendency was clearly observed in the experiments with models. It was demonstrated experimentally that they can discriminate between the wingless and winged adult models. It is suggested that females of the hover fly assess the value of aphid colonies as the food resource of their offspring. Contribution No. 211 from Lab. Entomol., Kyoto Pref. Univ.     

The influence of some honeybee products as a diet substitute on the different stages of Coccinella undecimpunctata L. in Egypt

Several natural diets of honeybee products were tested for rearing Coccinella undecimpunctata L. under laboratory conditions. Two groups of tested adult and larval insect have been fed on the tested diets, the first group were fed on the tested honey bee products diets without adding aphids, while the second group fed on the same honeybee products with aphids added. The oviposition period in the first group was significantly shorter than control. The tested diets supplied with royal jelly + aphid and/or pollen grains + aphid caused the longest oviposition period. Diets of aphid alone and bee honey with aphid recorded the shortest oviposition period. Fecundity of ladybird was the highest in the tested diets with aphids than diets without aphid and/or aphid diet alone. The durations of larval and pupal stages were significantly different when compared with the diets with or without aphid and/or aphid diet alone. Further results indicated that the diets of royal jelly caused the shortest duration in larval and pupal stages.     

Oviposition site selection of Episyrphus balteatus

The oviposition behaviour of Episyrphus balteatus DeGeer (Diptera: Syrphidae) was investigated in four-choice experiments in screen cages and in experiments with direct behavioural observations. Females laid hardly any eggs in the absence of aphids and preferred larger aphid colonies to small ones. Honeydew attracted the females via olfaction and elicited oviposition. Females were able to perceive the presence of conspecific eggs and oviposited less often in aphid colonies in which eggs were present. The oviposition deterring stimulus was also active when the eggs were removed, hence, the deterrent did not act visually, but probably olfactorily.     

Effect of size,extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis> and the hoverfly <Emphasis Type="Italic">Episyrphus balteatus</Emphasis>

Intraguild predation (IGP) is a widespread interaction between predatory arthropods, and is influenced by several factors. The harlequin ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), has frequently been reported as an intraguild predator of other Coccinellidae, but little is known about its interactions with other aphidophagous predators, including syrphids. This study investigated the incidence of IGP between H. axyridis and Episyrphus balteatus (Diptera: Syrphidae), the most abundant hoverfly species in Europe and a commercially available aphid biocontrol agent. The influence of size, presence of extraguild prey and habitat complexity were investigated through laboratory experiments in Petri dishes and on potted broad bean plants. In both types of arenas, IGP between H. axyridis and E. balteatus was found to be asymmetric, with the coccinellid in the majority of cases being the intraguild predator. There was a significant effect of size on the frequency of IGP. The efficiency of H. axyridis as an intraguild predator increased with the developmental stage. Early instars of E. balteatus were the most vulnerable to IGP. Pupae of either species were not attacked. In the presence of extraguild prey, the frequency of IGP was substantially reduced. However, IGP still occurred, mainly in combinations of older larvae of H. axyridis with first or second instars of E. balteatus. The size of the arena affected the incidence of IGP in combinations with second instars of E. balteatus, but not in combinations with third instars. Field research is needed to elucidate the ecological relevance of IGP among these predators.     

Responses of Episyrphus balteatus DeGeer (Diptera: Syrphidae) in relation to prey density and predator size

Laboratory experiments were conducted to determine the functional and numerical responses of the aphidophagous hover fly Episyrphus balteatus DeGeer (Diptera: Syrphidae) to different densities of 4th instar black bean aphids, Aphis fabae Scopoli (Homoptera: Aphididae), on broad bean, Vicia faba L. (Fabaceae). Two different-sized larvae of predators were tested in different densities of similar-sized prey to determine whether functional response parameters depended on the body sizes of predator and prey. In numerical response experiments, gravid E. balteatus females were exposed individually to different densities of 4th instars of A. fabae on cut sections of the broad bean plant, V. faba L. Logistic regression suggested a type II functional response for both larval sizes of E. balteatus. The searching efficiency (a) of the larger larvae was higher than that of the smaller ones. Prey consumption was higher, and handling time (T_h) was lower for larger larvae than smaller ones. The theoretical maximum number of A. fabae nymphs eaten by the different-sized larvae was 125 and 269 nymphs per day. Larger E. balteatus larvae are more efficient predators for aphid management strategies. The reproductive numerical response, in terms of the number of eggs laid, increased curvilinearly with increasing prey density, but the proportion of eggs laid (egg number/prey density) decreased as the initial density of prey increased.     

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.     

Assessment of aphid colonies by hoverflies. I maple aphids andEpisyrphus balteatus (de Geer) (Diptera: Syrphidae)

In the syrphid hoverflyEpisyrphus balteatus (de Geer), females in search of oviposition sites are assessing the qualitative and quantitative value of aphid colonies for securing the successful development of their offspring. They select small, young and “promising” aphid colonies consisting of nymphs and/or fundatrices as their oviposition sites, and neglect large, older ones including winged adults. Such “buy-futures” tactics will benefit the offspring in finding suitable and sufficient food.     

Influence of sulphur plant nutrition on oviposition and larval performance of the cabbage root fly

1 Oilseed rape plants (Brassica napus) (L.) (Brassicaceae) were grown under different levels of sulphur supply and tested for the oviposition preference and larval performance of cabbage root flies Delia radicum (L.) (Diptera: Anthomyiidae). 2 Adult females laid more than three‐fold as many eggs on control S_n (normal field concentration) than on sulphur‐free S₀ plants. By contrast, no significant difference was observed between control and double normal concentration (S₊) plants. 3 The larval performance was evaluated using three additional, intermediate sulphur levels between S₀ and S_n, and the plants were infected with equal numbers of eggs. The percentage pupation at the end of larval feeding ranged from 6% (S₀) to 32% (S_n or S₊) and the average number of pupae, or of emerging flies, was significantly correlated with sulphur application. 4 The weight of emerging males and females was correlated with plant sulphur supply. 5 The duration of development from eggs to adult emergence was approximately 2 days longer in females than in males. Females originating from plants with a normal or higher sulphur supply tended to emerge 1–2 days earlier.