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.     

Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis

Coincidental intraguild predation is expected to be less disruptive to biological control than omnivorous intraguild predation, and strong intraguild predation is not expected to occur in natural systems. Coincidental intraguild predation in a foodweb involving introduced pest and natural enemy species was examined to determine whether intraguild predation would be disruptive of biological control services in soybean agroecosystems. Introduced natural enemies are important regulators of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), populations in North America. Seven-spotted lady beetles, Coccinella septempunctata L., and multicolored Asian lady beetles, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), are key predators of soybean aphid in North America while the chalcidoid wasp, Aphelinus certus Yasnosh (Hymenoptera: Aphelinidae), is the most common parasitoid of soybean aphid in Ontario, Canada. Predation of parasitized soybean aphids at two stages (newly parasitized aphids and mummified aphids) by adults and third instar larvae of both C. septempunctata and H. axyridis was examined in laboratory experiments. In choice experiments, all stages of lady beetles preferred non-parasitized aphids over mummified aphids. In cage experiments, third instar larvae and male and female adults of both lady beetles did not discriminate between newly parasitized and non-parasitized aphids. The influence of coincidental intraguild predation on the efficacy of parasitoids as biological control agents, and implications for soybean aphid management decisions based on natural enemies, are discussed.     

Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras

A video technique that allows simultaneous behavioural observations of several experimental replicates under field and laboratory conditions is described. The technique was used to analyse predation risk of parasitised aphids in a sugar beet field. The images of 16 black and white video cameras were recorded by a video multiplexer in combination with a time-lapse video recorder. Each camera was weather protected and equipped with a single infrared diode to allow observations during night times. Single leaves carrying aphid mummies only or mummies and unparasitised aphids were monitored. All colonies were exposed to predation and parasitation by the community of natural enemies in the field. Colonies with mummies and unparasitised aphids were visited significantly more often by predators than those without additional aphids. Predators also stayed significantly longer in patches with unparasitised aphids. Although an equal proportion of aphid mummies were destroyed in both treatments, the video analysis showed differences in predator species spectrum between treatments. In patches with aphids, coccinellid and hemipteran predators preyed on mummies, while in patches with only mummies, chrysopids accounted for most of the damage. The decrease in parasitoid survival could be attributed to the increasing number of predator visits in aphid patches and to a lesser extent to the decreasing number of unparasitised aphids (alternative prey). Parasitoid survival in colonies without alternative prey was correlated with the number of predator visits and the time predators spent on a leaf.Continuous video observations gave additional behavioural information for the interpretation of field data. Other prospective research fields for the use of the multi video camera technique are outlined and general advantages and disadvantages are discussed.     

Feeding History Affects Intraguild Interactions between Harmonia axyridis (Coleoptera: Coccinellidae) and Episyrphus balteatus (Diptera: Syrphidae)

While the effect of several factors such as predator and prey size, morphology and developmental stage on intraguild predation (IGP) is widely investigated, little is known about the influence of diet on the occurrence and outcome of IGP. In the present study, the effect of the diet experienced during larval development on IGP between the ladybird Harmonia axyridis and the syrphid Episyrphus balteatus is investigated. Four diets were tested for H. axyridis: eggs of the Mediterranean flour moth Ephestia kuehniella, pea aphids, Acyrthosiphon pisum, in an ad libitum amount, pea aphids in a limited amount, and honey bee pollen. For E. balteatus only the two aphid diets were tested. First, experiments were performed to determine the quality of the various diets for development of both predators. Second, IGP experiments between H. axyridis and E. balteatus were performed both in Petri dishes and on potted pepper plants. The diet of both species influenced the incidence of IGP between H. axyridis and E. balteatus both in Petri dishes and on potted plants. In general, smaller larvae of H. axyridis (those fed on poor or restricted diet) fed more on hoverflies than large (well-nourished) ladybird larvae. Further, poorly nourished (smaller) larvae of E. balteatus were more susceptible to predation than well-fed (larger) hoverfly larvae. The observed effects were not only due to the lower fitness of larvae of both predators reared on an inferior quality diet but also to changes in predator behaviour. The results from this study show that IGP interactions are influenced by a multitude of factors, including feeding history of the organisms involved, and emphasize the importance of taking these factors into account in order to fully understand the ecological relevance of IGP.     

Developmental threshold, day-degree requirements and voltinism of the aphid predator Episyrphus balteatus (Diptera: Syrphidae)

Episyrphus balteatus is the dominant syrphid predator of aphids in the UK, reestablishment of populations each season is mainly by migration from warmer climes, as overwintering in this country is minimal with an uncertain level of success. The effects of temperature on the developmental rate of E. balteatus were investigated to determine the potential voltinism of this species in the UK. Estimates of the developmental threshold temperature from oviposition to adult emergence varied between 6.0d?C and 7.1d?C with a day-degree (DD) requirement of between 256 and 280 depending on the method of analysis used. Using the DD requirement derived from a weighted linear regression (261 DD above a threshold of 6.8d?C) in combination with the required value from adult emergence to first oviposition, suggests a total requirement of approximately 374 DD above 6.8d?C per generation. These data, together with climate records, indicate that one to three generations are possible each year, depending on the available DD and origin of the population. The advantages and limitations of different approaches and models used to estimate developmental thresholds and DD requirements are discussed.     

七星瓢虫对不同初始密度棉蚜种群的调控作用

为明确七星瓢虫成虫对棉蚜的自然控制能力,本文通过密度-天敌双因素控制试验分析了不同棉蚜初始密度(200头/株、400头/株、800头/株)和不同七星瓢虫数量(0头、1头、2头、4头)组合处理下棉蚜的种群动态;使用棉蚜种群增长率、益害比、控制效果等指标评估了天敌的控制能力,并建立简单的模型来明确天敌有效控制棉蚜的益害比....     

Predatory effect of Coccinella septempunctata on Thrips tabaci and Trialeurodes vaporariorum

Abstract:  The predatory effect of adult ladybird Coccinella septempunctata L. on adults of thrips, Thrips tabaci Lindeman, and whiteflies, Trialeurodes vaporariorum (Westwood), was examined in controlled environment chambers, on tomato leaves, in transparent small plastic cages at proportions of 1/(10 + 10), 1/(20 + 20), 1/(30 + 30) and 1/(40 + 40) predator/number of thrips and whiteflies. We conclude that C. septempunctata could be used with success for the biological control of thrips and whiteflies in greenhouse crops, with almost the same effectiveness as for aphids, at predator/prey proportions near 1 : 30. Additionally, it was found a prey preference for T. tabaci in comparison with T. vaporariorum . According to the model used, effective predation is correlated with predator/prey ratio rather than to prey preference.     

Influence of six aphid prey species on development and reproduction of a ladybird beetle, Coccinella septempunctata

Pre-imaginal development, immaturesurvival, and reproduction of a ladybird, Coccinella septempunctata Linnaeus, werestudied in response to six aphid species, Aphiscraccivora Koch, Aphis gossypii Glover,Aphis nerii Boyer de Fonscolombe,Lipaphis erysimi (Kaltenbach), Myzuspersicae (Sulzer) and Uroleuconcompositae (Theobald) to quantify theirrelative suitability as prey. Pre-adultdevelopment was shortest (13.93 ± 0.12 days)when fed on L. erysimi and longest(22.85 ± 0.10 days) on A. nerii. Immaturesurvival, adult emergence, growth index,relative growth rate, development rate, maleand female longevity, oviposition period,fecundity and hatching percent were maximal, i.e. 73.47 ± 0.89%, 90.07 ± 1.43%,8.62 ± 0.23, 1.52 ± 0.02, 0.07,81.10 ± 1.26 days, 85.70 ± 1.45 days,69.80 ± 1.32 days, 1764.10 ± 8.46,and 87.88 ± 1.05, respectively when C.septempunctata were fed on L. erysimi.The same parameters were minimal, i.e.43.86 ± 1.33%, 71.65 ± 2.75%,2.02 ± 0.08, 0.49 ± 0.02, 0.04,44.40 ± 1.39 days, 53.50 ± 1.00 days,16.40 ± 0.60 days, 203.20 ± 11.83, and48.68 ± 2.06, respectively on A. nerii. Theweights of different ladybird life stages weremaximal after feeding on L. erysimi and minimalon A. nerii. Regression analyses of thedata revealed linear relationships betweendevelopment rate and weight of adult; dailyprey consumption and relative growth rate; logweight of adult male and female; and longevityand fecundity of female. On the basis of thesefindings, the order of suitability of aphidspecies for C. septempunctata is L. erysimi >M. persicae > A. craccivora > A. gossypii >U. compositae > A. nerii. Thus, the presentinformation can be utilized for the massrearing of C. septempunctata by supplyingthe best food and can also help in theprediction of the relative abundance of theladybird on different aphid infestations in thefields.     

Internal labelling of the eggs of the aphidophagous hoverfly Episyrphus balteatus (De Geer) (Diptera: Syrphidae) with a fluorescent dye

A method was developed to label the egg load of Episyrphus balteatus (De Geer) (Diptera: Syrphidae) by feeding adult females with the fluorescent dye Rhodamine B. In a preliminary experiment aimed at selecting an appropriate dye concentration, gravid females reared in insectary conditions were provided for two successive days with a 50% honey-water solution enriched with Rhodamine B at concentrations of 0.1%, 0.01% and 0.001%. Eggs deposited on aphid-infested broad bean plants by syrphid females fed with Rhodamine B 0.01% showed the most intense marking. The higher dye concentration induced irregular marking among the eggs, presumably due to its repellent taste and consequently lower intake by the flies. A second series of trials focused on the persistence of the marker, prior and after oviposition, at the selected (optimal) dilution. A reduction in the marking degree of eggs was observed when the first egg deposition was delayed for one day after removing the dye from the cage. When marked females were allowed to deposit further batches of eggs the subsequent days, fewer eggs were laid and their fluorescence properties was reduced. Exposure to direct sunlight during 10 hours had no detectable effect on the fluorescence level of marked eggs deposited on a bean plant. The egg-marking technique examined in this study could be useful to determine the crop area accommodating eggs deposited by marked syrphid females migrating from a release point into cultivated fields.     

The influence of mixed aphid diets on larval performance of Coccinella septempunctata (Col., Coccinellidae)

Abstract: Three questions regarding possible benefits of mixed diets for the specialist aphid predator, Coccinella septempunctata larvae were investigated. (1) Do aphids species from different host plants complement each other nutritionally? (2) Is a mixed diet of high‐quality aphids beneficial? (3) How does the quality of mixed diets depend on the quality of constituent species? All mix‐combinations of aphid species of high (Metopolophium dirhodum), intermediate (Myzus persicae), and poor food quality (Aphis sambuci), and the three single‐species diets were compared. A mixed diet of two high‐quality species (Sitobion avenae and M. dirhodum) was also compared with single‐species diets. Larvae that were given pure A. sambuci and a mixed diet of A. sambuci + M. persicae died within 18 days and none of the larvae developed to fourth instar. Metopolophium dirhodum was generally of higher quality as food than M. persicae, whereas the mixed diet of M. dirhodum + M. persicae was intermediate. Sitobion avenae and M. dirhodum were found to have approximately the same food value. Coccinella septempunctatam larvae that were offered a mixed diet of these two high‐quality aphids gained no extra advantage. Overall, no benefit from mixing of aphid species was found. The quality of mixed diets depended on the quality of the constituent species.     

Interference and competitive behaviour of the aphid predators,Chrysoperla carnea andCoccinella septempunctata in the laboratory

Interference and competition betweenChrysoperla carnea (Stephens) andCoccinella septempunctata L. was investigated in the absence and presence of aphid prey. When larvae of similar vigour encountered each other,C. carnea larvae were superior toC. septempunctata. Otherwise the larger of 2 individuals always killed the smaller. In the absence of preyC. carnea adults were attacked by their own 2nd and 3rd instar larvae as well as by 3rd instar larvae ofC. septempunctata. In all encounters the adults ofC. septempunctata were superior. Since the eggs ofC. carnea are protected to some extent by being on egg stalks, they were less susceptible to cannibalism and predation thanC. septempunctata eggs which are deposited in batches directly on plant leaves. In the presence of prey cannibalism and predation were reduced, especially between larvae. Only eggs and 1st instar larvae were endangered. In the present experimentsC. carnea showed a slight superiority overc. septempunctata. Paper presented at the 17th International Congress of Entomology held in August 20–26 1984 in Hamburg, F.R. Germany.     

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.     

Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis

The effects of the invasion ofan exotic predator, Harmonia axyridis(Pallas) (Coleoptera: Coccinellidae), wereinvestigated using three experiments on theecology of aphid predators on apple. Oneexperiment, 1992, was collected prior to theH. axyridis invasion, and two others,1996 to 1997 and 1999 to 2000, were collectedafter the invasion. Except for one year, 1999,H. axyridis was the dominant coccinellid,replacing the formerly dominant Coccinellaseptempunctata L. (Coleoptera: Coccinellidae),another exotic species. The dominance of H. axyridis was greater among larvae thanamong adults. There was no apparent effect ofthe H. axyridis invasion on abundance ofthe predator, Aphidoletes aphidimyza(Rondani) (Diptera: Cecidomyiidae) and apossible positive effect on the abundance ofchrysopids (Neuroptera: Chrysopidae). Principal component analysis indicated thatalthough individual species were affected, theoverall effect of H. axyridis invasion onthe predator guild as a whole was negligible. The data indicate that the interaction betweenthe two exotic species, H. axyridis andC. septempunctata, may be allowing nativecoccinellids to become more abundant on applethan when C. septempunctata was thedominant coccinellid.     

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.     

Foraging responses of Coccinella septempunctata,Hippodamia variegata and Chrysoperla carnea to changing in density of two aphid species

The successful use of predators in classical biocontrol programmes needs several background laboratory investigations, one of which is the evaluation of predator behavioural responses to changes in the density of their prey. The impact effect of the density of two prey species [Myzus persicae Sulzer and Aphis craccivora Koch (Hemiptera: Aphididae)] on the predation rates of third-instar Chrysoperla carnea Stephens (Chrysopidae: Neuroptera) and fourth-instar Coccinella septempunctata L. and Hippodamia variegata Goeze (Coccinellidae: Coleoptera) larvae was studied. Although prey species, predator species, prey density, and their interactions all had significant effects on the numbers of aphids consumed, the type of functional response did not vary, remaining a type II response in all treatments. However, the type II parameters differed among predator species on the same prey species, and for each predator species on the two prey species. Chrysoperla. carnea on M. persicae and H. variegata on A. craccivora were more voracious than other predators. In the context of functional response and biological control, the release of these predators, that show inverse density-dependent mortality, has to be started in early season to build up their population on low aphid densities and attack later high aphid populations.     

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.     

Oviposition behaviour and host colony size discrimination in Episyrphus balteatus (Diptera: Syrphidae)

Three bioassays were used to examine the oviposition behaviour of the hoverfly, Episyrphus balteatus (Degeer) in which various stimuli purported to influence host assessment and choice were tested. Episyrphus balteatus failed to exhibit enhanced behavioural responses, in terms of approaches and landings, to artificial leaves with the highest numbers of aphids, suggesting that females are merely responding to the colour of the artificial leaves. A density-dependent oviposition response was reported in a second bioassay using whole bean plants, although there was an asymptotic relationship. Syrphid responses, which were measured by oviposition over a five-day period, were greatest towards those plants with the highest number of aphids. In a final series of trials, gravid female E. balteatus showed a behavioural preference for filter papers treated with the greatest honeydew concentrations (0.26 mg microl(-1) honeydew). More time was spent in the treated areas and syrphids demonstrated more proboscis and ovipositor extensions in these treatments. These bioassays provided an opportunity to isolate some of the individual components of decision-making by female E. balteatus during egg-laying behaviour. A greater understanding of natural enemy behaviour is essential before enhanced control of pest populations in the field can be established.     

七星瓢虫和异色瓢虫四变种成虫对茶蚜蜜露的搜索行为和蜜露的组分分析

采用培养皿 ,1承接茶蚜自然分泌蜜露 ;2收集蜜露浓缩后点于培养皿中心。逐头释放瓢虫于分别盛有这 2类蜜露的培养皿中心进行生物测定 ,两个试验均证明 :1蜜露强烈地吸引七星瓢虫和异色瓢虫 ,随着蜜露浓度呈梯度地增大 ,搜寻时间极显著地延长 ( P<0 .0 1 ) ;2蜜露可激发瓢虫的搜索行为由广域搜索型转换为地域集中搜索型。前 0～ 5s局限在较小范围内不断地转向 ,即搜索速度小 ,转动角度大。七星瓢虫和异色瓢虫显明变种最敏感 ,搜索和滞留时间也最长。用高效液相色谱定性定量地分析出蜜露中有茶氨酸等 1 3种氨基酸和蔗糖等 7种糖分。