Olfactory response towards its prey Frankliniella occidentalis of wild and laboratory‐reared Orius insidiosus and Orius laevigatus

Orius species are important biological control agents of thrips in protected crops. Rearing conditions in mass production facilities may affect their performance in the crop when searching for the target prey. The aim of this study was to evaluate and compare the search behaviour and orientation towards prey of two Orius species, O. laevigatus (Fieber) and O. insidiosus (Say) that have been reared in the laboratory under different conditions, with wild (field‐collected) individuals. Adult predator females were placed in a Y‐tube olfactometer and offered a choice between the odours released by plants of different species (cotton, common bean, sweet pepper and cucumber), which were either non‐infested or infested with Frankliniella occidentalis (Pergande) adults.O. laevigatus and O. insidiosus responded to odours from thrips‐infested plants and these responses were influenced by the origin of the colonies. A larger percentage of laboratory‐reared O. laevigatus females (42%) did not made a choice between thrips‐infested or clean plants, compared with wild individuals (17%). Of those females that did respond to plant odours, a smaller percentage of laboratory‐reared O. laevigatus females (34%) responded to the odours from thrips‐infested plants compared with wild insects (76%). No significant differences were found inO. insidiosus females that did not make a choice between thrips‐infested or clean plants (14% for wild vs. 17% for lab individuals). Also, no significant differences were found between O. insidiosus females that selected thrips‐infested plants at the corresponding proportion of wild (75%) and laboratory‐reared (70%) individuals. We propose that the olfactometer test could be a complementary evaluation aspect to the already developed quality criteria for performance of mass‐reared Orius predators.     

Attraction of a generalist predator towards herbivore-infested plants

The occurrence and strength of interactions among natural enemies and herbivores depend on their foraging decisions, and several of these decisions are based on odours. To investigate interactions among arthropods in a greenhouse cropping system, we studied the behavioural response of the predatory bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) towards cucumber plants infested either with thrips (Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)) or with spider mites (Tetranychus urticae Koch (Acari: Tetranychidae)). In greenhouse release-recapture experiments, the predatory bug showed a significant preference for both thrips-infested plants and spider mite-infested plants over clean plants. Predatory bugs preferred plants infested with spider mites to plants with thrips. Experience with spider mites on cucumber leaves prior to their release in the greenhouse had no effect on the preference of the predatory bugs. However, this experience did increase the percentage of predators recaptured. Y-tube olfactometer experiments showed that O. laevigatus was more attracted to odours from plants infested with spider mites than to odours from clean plants. Thus, O. laevigatus is able to perceive odours and may use them to find plants with prey in more natural conditions. The consequences of the searching behaviour for pest control are discussed.     

Continuous rearing of the predatory anthocorid Orius laevigatus without plant materials

The omnivorous anthocorid predator Orius laevigatus is an economically important biological control agent of several small arthropod pests including the western flower thrips Frankliniella occidentalis. Mass rearing systems for Orius bugs typically make use of plant materials such as bean pods as an oviposition substrate and moisture source. Omission of plant materials from the mass rearing system of these beneficial arthropods could drastically improve the cost‐effectiveness of their production and thus stimulate their use in augmentative biological control. This study investigated the effect of a plantless rearing system, using wax paper as a walking substrate, water encapsulated in Parafilm domes, and an artificial oviposition substrate made of Parafilm and moist cotton wool, on the developmental and reproductive fitness of O. laevigatus. Plantless rearing during four generations resulted in females with an 11% lower body weight and a pre‐oviposition period that was prolonged by 29%. However, other biological parameters were not negatively affected by the absence of plants. In addition, plantless‐reared females had similar predation rates on F. occidentalis larvae as their peers maintained on plants. Our study indicates that the omission of plant material from the production cycle of O. laevigatus is possible when Ephestia kuehniella eggs are provided as a nutritionally optimal food source.     

Crowding leads to higher incidence of brachypterous females in the tobacco thrips,Frankliniella fusca (Hinds) (Thysanoptera: Thripidae)

The effects of larval density on the wing form determination of female tobacco thrips, Frankliniella fusca, were investigated by rearing thrips on leaf disks at 27.5 °C. The developmental period, head width, body length, and forewing length of individuals in each wing morph were determined to assess the relationships among larval density, growth, and wing form. Data showed that higher rearing densities increased the production of female F. fusca brachypters. There was no consistent difference in the mean developmental periods between the two wing morphs or among all 5 density treatments. The body length of females tended to decrease with increasing rearing density, but there was no significant difference in body size between the two wing morphs when they were reared under the same density level.     

Influence of diet on the predation rate of <Emphasis Type="Italic">Orius laevigatus</Emphasis> on <Emphasis Type="Italic">Frankliniella occidentalis</Emphasis>

The predation rate of fifth instars and female adults of Orius laevigatus (Fieber) fed honeybee pollen, Ephestia kuehniella Zeller eggs or an egg yolk based artificial diet on second instars of the western flower thrips Frankliniella occidentalis (Pergande) was examined in the laboratory. Predation rate of both fifth instars and female adults was not influenced by their diet. Despite a lower body weight, O. laevigatus reared on artificial diet or pollen killed as many prey as their peers reared on E. kuehniella eggs, suggesting that body weight is not a reliable predictor of predation rate. The use of non-prey foods for O. laevigatus for mass production or as a supplementary food to sustain its populations in the field when prey are scarce is discussed.     

Effects of laboratory colonization on Bactrocera dorsalis (Diptera,Tephritidae) mating behaviour: ‘what a difference a year makes’

Laboratory-reared insects are widely known to have significantly reduced genetic diversity in comparison to wild populations; however, subtle behavioural changes between laboratory-adapted and wild or ‘wildish’ (i.e., within one or very few generations of field collected material) populations are less well understood. Quantifying alterations in behaviour, particularly sexual, in laboratory-adapted insects is important for mass-reared insects for use in pest management strategies, especially those that have a sterile insect technique component. We report subtle changes in sexual behaviour between ‘wildish’ Bactrocera dorsalis flies (F1 and F2) from central and southern Thailand and the same colonies 12 months later when at six generations from wild. Mating compatibility tests were undertaken under standardised semi-natural conditions, with number of homo/heterotypic couples and mating location in field cages analysed via compatibility indices. Central and southern populations of Bactrocera dorsalis displayed positive assortative mating in the 2010 trials but mated randomly in the 2011 trials. ‘Wildish’ southern Thailand males mated significantly earlier than central Thailand males in 2010; this difference was considerably reduced in 2011, yet homotypic couples from southern Thailand still formed significantly earlier than all other couple combinations. There was no significant difference in couple location in 2010; however, couple location significantly differed among pair types in 2011 with those involving southern Thailand females occurring significantly more often on the tree relative to those with central Thailand females. Relative participation also changed with time, with more southern Thailand females forming couples relative to central Thailand females in 2010; this difference was considerably decreased by 2011. These results reveal how subtle changes in sexual behaviour, as driven by laboratory rearing conditions, may significantly influence mating behaviour between laboratory-adapted and recently colonised tephritid fruit flies over a relatively short period of time.     

Loss of sex-allocation plasticity in the predatory mite Metaseiulus occidentalis and possible triggering cues

In two recent studies, we showed that females from a long-established Metaseiulus (Typhlodromus or Galendromus) occidentalis laboratory colony reared under crowded conditions for approximately 27 years produced equal numbers of male and female progeny. This contrasts with our previous results that showed the females from the same colony produced progeny with a female-biased sex ratio. These discrepant findings raised the possibility that dense rearing conditions can affect the sex-allocation plasticity in this important biological control agent. In the current study, we show that females from a newly collected M. occidentalis colony initially were capable of producing progeny with a female-biased sex ratio, but lost this ability over a 12-month period (43 generations) when reared under dense rearing conditions and provided with damaged prey. We demonstrate that females from this newly collected colony initially could adjust offspring sex ratio in response to both conspecific cues and cues produced by their damaged prey. The results suggest that dense rearing conditions, which are often used in commercial rearing facilities, may have detrimental effects on the reproductive fitness of M. occidentalis and, possibly, other predatory mites.     

Does mass rearing of field collected Trichogramma brassicae wasps influence acceptance of European corn borer eggs?

The purpose of our study was to identify a trait that changes quickly during Trichogramma mass rearing, and that could therefore be used to monitor stock deterioration. Quality deterioration in mass reared Trichogramma wasps was evaluated by examining host acceptance behaviour of Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) on the target host Ostrinia nubilalis Hübner (Lepidoptera: Crambidae). We compared three replicate lines (designated ‘E’) reared in the laboratory on the factitious host Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) for 27 generations, a line ‘O’ reared in the laboratory on O. nubilalis for 24 generations, and a line ‘F’ reared in the laboratory on O. nubilalis for only two generations. All lines were initiated from field collections of O. nubilalis egg masses. We also evaluated natal host effects by rearing each line on E. kuehniella as well as on O. nubilalis for the last generation prior to testing. The percentage of wasps accepting the O. nubilalis egg mass was significantly higher for the E lines (69.6%) than for the F line (46.5%), while wasps of the O line showed intermediate (57.4%) acceptance. Thus, wasps laboratory reared on E. kuehniella performed better than wasps which had recently been collected in the field. Wasps of the O line showed extended probing behaviour compared to the other lines. Lines did not differ in the duration from the first host contact to the beginning of the drilling, probing or trembling behaviour. Natal host (E. kuehniella or O. nubilalis) did not affect acceptance of the target host O. nubilalis. Even though there is some evidence of adaptation to laboratory rearing conditions, we found no indication for quality deterioration in terms of acceptance behaviour of the target host O. nubilalis when T. brassicae was mass reared on the factitious host E. kuehniella.     

Two Meridic Diets for Perillus bioculatus (Heteroptera: Pentatomidae), a Predator of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Two artificial diets, devoid of insect components, were developed for the predator Perillus bioculatus (Fabricius). The diets based on chicken liver and tuna fish were designed to approach the nutritional characteristics of the primary insect prey, Leptinotarsa decemlineata (Say) eggs. P. bioculatus was reared on diet 2 for 11 consecutive generations without cumulative detrimental effects on its biology. Developmental time and preovipositional period were significantly longer, and egg viability, survival from egg to adult, and fecundity were significantly lower in P. bioculatus individuals reared on artificial diets than in those reared on L. decemlineata eggs. A significant reduction in developmental time, increase in survival from egg to adult, and reduction in length of the preovipositional period were observed after 11 generations of in vitro reared P. bioculatus on diet 2. These changes may indicate that the predators experience some degree of adaptation to the diet after several consecutive generations of in vitro rearing. No changes in egg viability were observed after 11 generations of in vitro rearing. Adult female weight was unaffected when reared on artificial diet, but a significant increase was observed after 11 generations of in vitro rearing. Females under all treatments weighed an average of 11.6 mg more than the males.     

Olfactometric evidence for aggregation pheromone production by females of the four-eyed fir bark beetle <Emphasis Type="Italic">Polygraphus proximus</Emphasis> Blandf. (Coleoptera,Curculionidae: Scolytinae)

Chemical communication of the four-eyed fir bark beetle Polygraphus proximus Blandf., an aggressive invasive pest of the Siberian fir Abies sibirica Ledeb., was experimentally studied using a four-way olfactometer of a modified design, in which the tested insects were allowed to move on their own from a lightproof plastic container onto the lighted arena. Young hibernated adults of P. proximus were offered four variants of odor: fir log segments infested with (1) 10 males, (2) 10 females, (3) 10 couples of P. proximus, and (4) clean air as the control. The pheromone of P. proximus was shown to be produced by females; a similar response of both sexes characterized it as an aggregation pheromone. All the three variants with infested fir logs were much more attractive than the control variant with clean air. Volatiles from fir tissues not only seem to serve as markers facilitating host selection by the first-to-arrive beetles before direct contact with the tree bark, but also to be used as pheromone precursors or synergists. The absence of difference in response to the logs infested with males and couples of the bark beetle indicated that pheromone synthesis was inhibited after couple formation.     

Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors

Plants under herbivore attack produce volatiles, thus attracting natural enemies of the herbivores. However, in doing so, the plant becomes more conspicuous to other herbivores. Herbivores may use the odours as a cue to refrain from visiting plants that are already infested, thereby avoiding competition for food, or, alternatively, to visit plants with defences weakened by earlier attacks. We investigated the response of one species of herbivore (the spider mite Tetranychus urticae) to odours emanating from cucumber plants infested by conspecific or heterospecific (the western flower thrips, Frankliniella occidentalis) herbivores. Olfactometer experiments in the laboratory showed that spider mites have a slight, but significant, preference for plants infested with conspecifics, but strongly avoid plants with thrips. These results were substantiated with greenhouse experiments. We released spider mites on the soil in the centre of a circle of six plants, half of which were infested with either conspecifics or heterospecifics (thrips), whereas the other half were uninfested. It was found that 60–70% of the mites were recaptured on the plants within 5 h after release. Results of these experiments were in agreement with results of the olfactometer experiments: (1) significantly fewer spider mites were found on plants infested with thrips than on uninfested plants and (2) more mites were found on plants with conspecifics than on clean plants (although this difference was not significant). From a functional point of view it makes sense that spider mites prefer clean plants over thrips-infested plants, since thrips are not only competitors, but are also known as intraguild predators of spider mites. Possible reasons for the slight attraction of spider mites to plants infested with conspecifics are discussed. Received: 22 June 1996 / Accepted: 29 September 1996     

The effect of two prey species, Chrysomphalusaonidum and Corcyra cephalonica, on the qualityof the predatory thrips, Aleurodothripsfasciapennis, reared in the laboratory

Periodic and augmentative releases of natural enemies are often required to enhance biological control and integrated pest management programs. One requirement for these programs to be practical is that natural enemies can be easily and economically mass-reared. This study assessed the effects of dieton the quality of the F₃ and F₄laboratory-reared generations of the predatory thrips,Aleurodothrips fasciapennis. Diets were eggs and crawlers of the diaspidid scale Chrysomphalusaonidum and eggs of the pyralid moth Corcyracephalonica. It was found that both the F₃ and F₄ generations were not viable when reared on the eggs and crawlers of C. aonidum due to very low fecundity and, in the F₄ generation, increased larval mortality. In contrast, thrips reared on the eggs of C. cephalonica were viable in both generations but an increase in larval mortality from the F₃ to the F₄ generation did result in are duction in viability. These results are discussed in terms of genetic, environmental and behavioural factors that may have influenced the quality of the thrips. It is concluded that genetic factors(inbreeding suppression, genetic drift or selection),the behaviour of scale crawlers and the predatory behaviour of thrips were probably of little value in explaining the results. The most likely explanation was that the diet supplied to thrips was of in adequatenutritional quality. It was not possible to distinguish whether this was due to low intrinsic quality of the prey or an indirect effect of experimental conditions on prey quality. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genetic variation and the performance of a mass‐reared parasitoid,Trichogramma pretiosum (Hymenoptera: Trichogrammatidae), in laboratory trials

During mass rearing, adaptation of biological control agents to the rearing environment is a potential problem. Using the parasitoid wasp Trichogramma pretiosum, the performance of 26 highly inbred lines, five composite ‘populations’ (created from the inbred lines) and one insectary‐reared population was compared using fertility life tables. Of the composite populations, three were created with maximal and identical genetic variation as a mixture of all 26 inbred lines, but these were then reared for a different number of generations (2, 6 or 17) before their performance was measured. The remaining two composite populations were created based on the performance of the individual inbred lines: one was a combination of two inbred lines with a high intrinsic rate of natural increase (rm), ‘high rm’; and the other was a combination of two lines with a ‘low rm’. High and low rm populations were reared for two generations prior to testing. Parameters measured were fertility, longevity and sex ratio. We found no difference between the maximally variable population reared for two generations and the ‘high rm’ population (rm = 0.285 and 0.282, respectively). ‘Low rm’ was the population with the lower performance (rm = 0.255). Genetically variable population reared for two generations for 48 h produced significantly more offspring than the populations reared for 6 and 17 generations. Hybrid population derived from the high‐rm lines did significantly better than that derived from the low‐rm lines. Low‐performance populations become more male based than high performance at 48 h. The potential benefits to improve population's performance using inbred lines for mass rearing are discussed.     

Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation

The combined release of species of generalist predators can enhance multiple pest control when the predators feed on different prey, but, in theory, predators may be excluded through predation on each other. This study evaluated the co-occurrence of the generalist predators Macrolophus pygmaeus Rambur and Orius laevigatus (Fieber) and their control of two pests in a sweet pepper crop. Both predators consume pollen and nectar in sweet pepper flowers, prey on thrips and aphids, and O. laevigatus is an intraguild predator of M. pygmaeus. Observations in a commercial sweet pepper crop in a greenhouse with low densities of pests showed that the two predator species coexisted for 8 months. Moreover, their distributions in flowers suggested that they were neither attracted to each other, nor avoided or excluded each other. A greenhouse experiment showed that the predators together clearly controlled thrips and aphids better than each of them separately. Thrips control was significantly better in the presence of O. laevigatus and aphid control was significantly better in the presence of M. pygmaeus. Hence, combined inoculative releases of M. pygmaeus and O. laevigatus seem to be a good solution for controlling both thrips and aphids in greenhouse-grown sweet pepper. The predators are able to persist in one crop for a sufficiently long period and they complement each other in the control of both pests. This study also provides further evidence that intraguild predation does not necessarily have negative effects on biological control.     

The influence of the rearing host on the response of the parasitoid Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) to odours from Ephestia kuehniella and Plodia interpunctella in a Y-tube olfactometer

Venturia canescens (Gravenhorst) is an ichneumonid generalist parasitoid that successfully attacks the larvae of different lepidopteran pests that infest stored products. These pest species include Plodia interpunctella and Ephestia kuehniella. In this study, we aimed to evaluate the influence of the rearing host on the parasitoid’s ability to detect and respond to a new host different from the rearing species. For this reason, the trials tested the preference of parasitoids reared on P. interpunctella or E. kuehniella for products that were or were not infested with larvae of these hosts. The trials were conducted in a Y-tube olfactometer. Regardless of the rearing host species, the parasitoids showed no preference for uninfested products. The parasitoids were attracted to products infested with larvae of their rearing host in preference to uninfested products. They also showed preferential attraction to products infested with the new host over uninfested products. E. kuehniella was the preferred host, irrespectively of the parasitoid host rearing species. The results are discussed to develop a better understanding of the ecology of V. canescens for its application in biological control.     

Ovipositing Orius laevigatus increase tomato resistance against Frankliniella occidentalis feeding by inducing the wound response

The anthocorid predator Orius laevigatus is widely used as biological control agent of thrips pests, including the western flower thrips Frankliniella occidentalis. In the current study, it was shown that O. laevigatus adults can increase plant resistance to feeding damage of F. occidentalis on tomato plants. The predator elicits a jasmonic acid (JA) mediated wound response during endophytic oviposition, resulting in reduced thrips feeding. A strong accumulation of H₂O₂, a molecule involved in different parts of the wound response, in leaf tissue surrounding the predator eggs or oviposition puncture sites was observed. Infestation of tomato plants with adult predators led to the upregulation of three JA regulated wound responsive genes: the precursor prosystemin, the jasmonic acid biosynthesis enzyme allene oxide synthase and the defence protein proteinase inhibitor I. Likewise, the presence of adults caused accumulation of proteinase inhibitor II, a principal marker for the wound response.     

Evaluation of an improved method for mass-rearing of thrips and a thrips parasitoid

Improved laboratory methods are described in detail for mass rearing of various thrips species, such as Frankliniella occidentalis, Frankliniella intonsa, Thrips palmi, Thrips tabaci (Thysanoptera: Thripidae) and a thrips parasitoid, Ceranisus menes (Hymenoptera: Eulophidae), using various foods. In one method, plant pollen and honey solution are used as food sources. In a second method, germinated broad bean seeds are used. Eggs, produced in large numbers in water, are collected by a suction funnel onto a filter paper and incubated in a Petri dish. Large numbers of larvae that hatch are collected by using food traps (plant pollen). Larvae can be reared on pollen or on germinated broad bean seeds until adult emergence without additional water and food. This method has been found useful for producing even-aged thrips at different densities (up to 500 larvae in a cage of 80 mm diameter) with relatively low mortality rates. Evaluation of this rearing method for F. intonsa, shows that during 2 weeks at 20 °C per 100 females more than 4000 females could be produced in the next generation. About 5 min per day is required to achieve this productivity of mass production. The method is also suitable for producing large numbers of the solitary endoparasitoid of thrips larvae, C. menes.     

The presence of inhibitors of the reproduction of Varroa jacobsoni Oud. (Gamasida: Varroidae) in infested cells

The mite Varroa jacobsoni was reared in artificial gelatin cells under laboratory conditions and the possible presence of factors inhibiting Varroa reproduction was studied. In cells infested with three mites, the mean offspring per female was reduced to 75% of that in singly infested cells. When gelatin cells were used for two successive rearing cycles, both the proportion of reproducing females and the offspring per reproducing female were significantly lower in cells that had contained an infested larva during the first rearing cycle than in those with an uninfested larva. The mean reduction of the offspring per female was 48%; this suggests that inhibitors of the reproduction are released into infested cells. Treatment of gelatin cells with the hexane extract of cells in which an infested bee pupa had developed caused a 21% reduction in the mean offspring per female, with a difference close to the significance level (p=0.07).     

Hyperthermic aphids: Insights into behaviour and mortality

Although the impact of warming on winter limitation of aphid populations is reasonably well understood, the impacts of hot summers and heat wave events are less clear. In this study, we address this question through a detailed analysis of the thermal ecology of three closely related aphid species: Myzus persicae, a widespread, polyphagous temperate zone pest, Myzus polaris, an arctic aphid potentially threatened by climate warming, and, Myzus ornatus, a glasshouse pest that may benefit from warming. The upper lethal limits (ULT₅₀) and heat coma temperatures of the aphid species reared at both 15 and 20 °C did not differ significantly, suggesting that heat coma is a reliable indicator of fatal heat stress. Heat coma and CT_max were also measured after aphids were reared at 10 and 25 °C for one and three generations. The extent of the acclimation response was not influenced by the number of generations. Acclimation increased CT_max with rearing temperature for all species. The acclimation temperature also influenced heat coma; this relationship was linear for M. ornatus and M. polaris but non-linear for M. persicae (increased tolerance at 10 and 25 °C). Bacteria known generically as secondary symbionts can promote thermal tolerance of aphids, but they were not detected in the aphids studied here. Assays of optimum development temperature were also performed for each species. All data indicate that M. persicae has the greatest tolerance of high temperatures.     

The influence of cultivar and cultivar-aphid odours on the olfactory response of the parasitoid Aphidius colemani

The olfactory response of the parasitoid Aphidius colemani (Viereck) (Hymenoptera: Braconidae) to odours in a tritrophic system involving three cultivars of common cabbage, Brassica oleracea var capitata, characterized by different levels of susceptibility to Myzus persicae (Sulzer) (Hemiptera: Aphididae) was studied in a four‐way olfactometer. Odours influenced A. colemani response in the olfactometer to varying degrees. The magnitude of parasitoid response to odours of uninfested cabbage depended on cultivar, with Derby Day [green‐leaved, susceptible to M. persicae and the crucifer specialist, Brevicoryne brassicae (Linnaeus) (Hemiptera: Aphididae)] and Minicole (green‐leaved, partially resistant with known antibiosis factors for B. brassicae) preferred over Ruby Ball (red‐leaved with antixenosis factors for M. persicae and B. brassicae). The odour of the cabbage cultivar on which the parasitoid had been reared was preferred over the other cultivars. However, when provided with a choice between odours of infested plants, parasitoids did not show a significant preference for the cultivar on which they were reared. Results from the study show that parasitioids differentiated between odour of the three cultivars in dependence of their rearing history when the plant is uninfested.