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.     

Juvenile prey induce antipredator behaviour in adult predators

It is generally assumed that the choice of oviposition sites in arthropods is affected by the presence of food for the offspring on the one hand and by predation risk on the other hand. But where should females oviposit when the food itself poses a predation risk for their offspring? Here, we address this question by studying the oviposition behaviour of the predatory mite Amblyseius swirskii in reaction to the presence of its counterattacking prey, the western flower thrips Frankliniella occidentalis. We offered the mites a choice between two potential oviposition sites, one with and one without food. We used two types of food: thrips larvae, which are predators of eggs of predatory mite but are consumed by older predator stages, and pollen, a food source that poses no risk to the predators. With pollen as food, the predators preferred ovipositing on the site with food. This might facilitate the foraging for food by the immature offspring that will emerge from the eggs. With thrips as food, female predators preferred ovipositing on the site without thrips. Predators that oviposited more on the site with thrips larvae killed more thrips larvae than females that oviposited on the site without food, but this did not result in higher oviposition. This suggests that the females killed thrips to protect their offspring. Our results show that predators display complex anti-predator behaviour in response to the presence of counter-attacking prey.     

Survey of flowering plants in Hawaii as potential banker plants of anthocorid predators for thrips control

Flowering plants in gardens and along roadsides on the Big Island of Hawaii were sampled for thrips and anthocorid predators of thrips. A total of 171 plant samples, comprising 859 plant sample units (e.g. flowers or flower clusters) were collected from 56 species of plants in 25 families. Adult thrips were found on 43 plant species, and 32 of these also had larval thrips of the same species, indicating the plant species was a breeding host for thrips. Five different species of anthocorids – Orius persequens, Orius tristicolor, Paratriphleps laeviusculus, Montandoniola confusa, and Blaptostethus pallescens – were collected on 22 different plant species in 10 plant families. The plants with the highest numbers of anthocorid adults and nymphs present were Macaranga tanarius (Blush Macaraga), Verbesina encelioides (Golden Crownbeard), Tithonia diversifolia (Tree Marigold), Acalypha hispida (Chenille bush), and Coreopsis lanceolata (Lance-leaf Coreopsis). Macaranga tanarius was found to be the best host plant for anthocorids, with an average of 25.5 adult and 21.1 larval anthocorids per plant sample. Orius persequens was the most abundant anthocorid on M. tanarius with average adult and larval densities of 24.1 and 17.3 per plant sample, respectively. None of the insects found in association with M. tanarius are known pests. Macaranga tanarius has great potential as a banker plant to help suppress thrips populations in greenhouse crops with anthocorid predators.     

Comparison of the predation capacities of two soil-dwelling predatory mites,Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae), on three thrips species

Soil-dwelling predatory mites are natural enemies of various soil pest insects and mites. Both Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) are commercialized natural enemies of thrips, but there is little information on the predation rate of these predatory mites on different thrips species. We compared their predation capacities on three thrips species, Frankliniella occidentalis, F. intonsa, and Thrips palmi, which are major pests of various horticultural plants. The predatory rate of G. aculeifer was higher than that of S. scimitus. Both predator species fed on more T. palmi thrips than F. occidentalis or F. intonsa thrips, which may be attributable to the smaller body size of T. palmi than the other thrips. Predation rates of female adults were 2.6–2.8 times higher than those of deutonymphs in both species. Predation rates were not separated according to the various developmental stages (i.e., second instar larva, pupa, or adult) of thrips; however, deutonymphs fed on fewer adults than larvae or pupae of F. occidentalis. Our results suggest that both G. aculeifer and S. scimitus are active predators that can prey during any of their developmental stages and on any species of thrips tested.     

Biotic resistance limits the invasiveness of the western flower thrips,Frankliniella occidentalis (Thysanoptera: Thripidae), in Florida

The spread of the western flower thrips, Frankliniella occidentalis (Pergande), has resulted in the world‐wide destabilization of established integrated pest management programs for many crops. It is hypothesized that frequent exposure to insecticides in intensive agriculture selected for resistant populations, which allowed invasive populations in the eastern USA to overcome biotic resistance from the native community of species. Research conducted in Florida to understand the role of biotic factors in limiting the abundance of the western flower thrips is reviewed. Orius spp. (Hemiptera: Anthocoridae) are effective predators that suppress populations of thrips on crop and non‐crop hosts in southern and northern Florida. Orius are more effective predators of the western flower thrips than the native flower thrips, F. tritici (Fitch) and F. bispinosa (Morgan). The native species are competitors of the western flower thrips. Excessive fertilization and the use of broad‐spectrum insecticides in crop fields further enhances populations of the western flower thrips. Interactions with native species clearly limit the abundance of western flower thrips in Florida, but populations are abundant in fertilized crop fields where application of insecticides excludes predators and competitor species.     

Biological control of aphids in the presence of thrips and their enemies

Generalist predators are often used in biological control programs, although they can be detrimental for pest control through interference with other natural enemies. Here, we assess the effects of generalist natural enemies on the control of two major pest species in sweet pepper: the green peach aphid Myzus persicae (Sulzer) and the western flower thrips Frankliniella occidentalis (Pergande). In greenhouses, two commonly used specialist natural enemies of aphids, the parasitoid Aphidius colemani Viereck and the predatory midge Aphidoletes aphidimyza (Rondani), were released together with either Neoseiulus cucumeris Oudemans, a predator of thrips and a hyperpredator of A. aphidimyza, or Orius majusculus (Reuter), a predator of thrips and aphids and intraguild predator of both specialist natural enemies. The combined use of O. majusculus, predatory midges and parasitoids clearly enhanced the suppression of aphids and consequently decreased the number of honeydew-contaminated fruits. Although intraguild predation by O. majusculus on predatory midges and parasitoids will have affected control of aphids negatively, this was apparently offset by the consumption of aphids by O. majusculus. In contrast, the hyperpredator N. cucumeris does not prey upon aphids, but seemed to release aphids from control by consuming eggs of the midge. Both N. cucumeris and O. majusculus did not affect rates of aphid parasitism by A. colemani. Thrips were also controlled effectively by O. majusculus. A laboratory experiment showed that adult predatory bugs feed on thrips as well as aphids and have no clear preference. Thus, the presence of thrips probably promoted the establishment of the predatory bugs and thereby the control of aphids. Our study shows that intraguild predation, which is potentially negative for biological control, may be more than compensated by positive effects of generalist predators, such as the control of multiple pests, and the establishment of natural enemies prior to pest invasions. Future work on biological control should focus on the impact of species interactions in communities of herbivorous arthropods and their enemies.     

Effects of Bt maize on Frankliniella tenuicornis and exposure of thrips predators to prey-mediated Bt toxin

As a part of a risk assessment procedure, the impact of Bt maize expressing Cry1Ab toxin on the thrips Frankliniella tenuicornis (Uzel) (Thysanoptera: Thripidae) was investigated, and the potential risks for predators feeding on thrips on Bt maize were evaluated. The effects of Bt maize on F. tenuicornis were assessed by measuring life‐table parameters when reared on Bt and non‐Bt maize. The content of Cry1Ab toxin in different stages of F. tenuicornis reared on Bt maize and the persistence of the toxin in adults where determined in order to evaluate the possible exposure of predators when feeding on thrips. In addition, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) was used as a model predator to assess how the behaviour of prey and predator may influence the exposure of a natural enemy to the Bt toxin. Life‐table parameter results showed that F. tenuicornis was not affected when it was reared on Bt maize. This indicates that the potential for prey quality‐mediated effects on predators is low. Bt content was highest in thrips larvae and adults, and negligible in the non‐feeding prepupal and pupal stages. The persistence of the Cry1Ab toxin in adult F. tenuicornis was short, resulting in a decrease of 97% within the first 24 h. Predation success by young C. carnea larvae varied among the thrips stages, indicating that exposure of predators to Bt toxin can additionally depend on the prey stage. When combining the current knowledge of the susceptibility of major thrips predators with our findings showing no potential for prey quality‐mediated effects, relatively low toxin content in thrips as well as short persistence, it can be concluded that the risks for predators when feeding on thrips in or next to Bt maize fields are negligible.     

Predators marked with chemical cues from one prey have increased attack success on another prey species

1. To reduce the risk of being eaten by predators, prey alter their morphology or behaviour. This response can be tuned to the current danger if chemical or other cues associated with predators inform the prey about the risks involved. 2. It is well known that various prey species discriminate between chemical cues from predators that fed on conspecific prey and those that fed on heterospecific prey, and react stronger to the first. It is therefore expected that generalist predators are more successful in capturing a given prey species when they are contaminated with chemical cues from another prey species instead of cues from the same prey species. 3. Here, a generalist predatory mite was studied that feeds on thrips larvae as well as on whitefly eggs and crawlers. Mites were marked with cues (i.e. body fluids) of one of these two prey species and were subsequently offered thrips larva. 4. Predators marked with thrips cues killed significantly fewer thrips than predators marked with whitefly cues, even though the predator's tendency to attack was the same. In addition, more thrips larvae sought refuge in the presence of a predatory mite marked with thrips cues instead of whitefly cues. 5. This suggests that generalist predators may experience improved attack success when switching prey species.     

Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator

To test the hypothesis that pest species diversity enhances biological pest control with generalist predators, we studied the dynamics of three major pest species on greenhouse cucumber: Western flower thrips, Frankliniella occidentalis (Pergande), greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and two-spotted spider mites, Tetranychus urticae Koch in combination with the predator species Amblyseius swirskii Athias-Henriot. When spider mites infested plants prior to predator release, predatory mites were not capable of controlling spider mite populations in the absence of other pest species. A laboratory experiment showed that predators were hindered by the webbing of spider mites. In a greenhouse experiment, spider mite leaf damage was lower in the presence of thrips and predators than in the presence of whiteflies and predators, but damage was lowest in the presence of thrips, whiteflies and predators. Whitefly control was also improved in the presence of thrips. The lower levels of spider mite leaf damage probably resulted from (1) a strong numerical response of the predator (up to 50 times higher densities) when a second and third pest species were present in addition to spider mites, and (2) from A. swirskii attacking mobile spider mite stages outside or near the edges of the spider mite webbing. Interactions of spider mites with thrips and whiteflies might also result in suppression of spider mites. However, when predators were released prior to spider mite infestations in the absence of other pest species, but with pollen as food for the predators, we found increased suppression of spider mites with increased numbers of predators released, confirming the role of predators in spider mite control. Thus, our study provides evidence that diversity of pest species can enhance biological control through increased predator densities.     

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

Pollen increases fitness and abundance of Orius insidiosus Say (Heteroptera: Anthocoridae) on banker plants

Banker plants are intended to enhance biological control by sustaining populations of natural enemies. Banker plants do this by providing alternative sources of food for natural enemies, such as pollen for omnivorous predators, thus decreasing the likelihood of their starvation and emigration from a cropping system when pest populations are low or absent. A banker plant system consisting of the Black Pearl pepper, Capsicum annuum ‘Black Pearl’, and the omnivorous minute pirate bug, Orius insidiosus Say (Hemiptera: Anthocoridae) has recently been proposed to improve biological control of thrips. Therefore, we studied how pollen from the Black Pearl pepper plant affects O. insidiosus fitness and abundance through a series of laboratory and greenhouse experiments. We found that a mixed diet of pollen and thrips increased O. insidiosus female longevity, decreased nymphal development time, and yielded larger females compared to a diet of thrips alone. Furthermore, O. insidiosus abundance was greater on flowering pepper plants than non-flowering pepper plants. From these results, we suggest that pollen from Black Pearl pepper banker plants could increase adult O. insidiosus abundance for the purpose of biological control in two ways: (1) reduce starvation and increase longevity of O. insidiosus when prey is absent; (2) enhance O. insidiosus fitness and fecundity when prey is present by mixing plant and prey diets. These results encourage future studies with the Black Pearl pepper as a banker plant for improving biological control of thrips in commercial greenhouses.     

Relationships between insect predator populations and their prey,Thrips tabaci,in onion fields grown in large-scale and small-scale cropping systems

Onion thrips, Thrips tabaci Lindeman, is the primary pest of onion, which is grown in either large-scale, monoculture systems surrounded by other onion fields, or in small-scale systems surrounded by multiple vegetable crops. In 2011 and 2012, populations of insect predators and their prey, T. tabaci, were assessed weekly in onion fields in both cropping systems. Insect predator taxa (eight species representing five families) were similar in onions grown in both systems and the most commonly occurring predators were from the family Aeolothripidae. Seasonal population dynamics of predators and T. tabaci followed similar trends within both cropping systems and tended to peak in late July and early August. Predator abundance was low in both systems, but predator abundance was nearly 2.5 to 13 times greater in onion fields in the small-scale system. T. tabaci abundance often positively predicted predator abundance in both cropping systems.     

Biological control of thrips and whiteflies by a shared predator: Two pests are better than one

We studied the capacity of one species of predator to control two major pests of greenhouse crops, Western flower thrips (Frankliniella occidentalis (Pergande)) and the greenhouse whitefly (Trialeurodes vaporariorum (Westwood)). In such a one-predator–two-prey system, indirect interactions can occur between the two pest species, such as apparent competition and apparent mutualism. Whereas apparent competition is desired because it brings pest levels down, apparent mutualism is not, because it does the opposite. Because apparent competition and apparent mutualism occurs at different time scales, it is important to investigate the effects of a shared natural enemy on biological control on a time scale relevant for crop growth. We evaluated the control efficacy of the predatory mites Amblyseius swirskii (Athias-Henriot) and Euseius ovalis (Evans) in cucumber crops in greenhouse compartments with only thrips, only whiteflies or both herbivorous insects together. Each of the two predators controlled thrips, but A. swirskii reduced thrips densities the most. There was no effect of the presence of whiteflies on thrips densities. Whitefly control by each of the two predators in absence of thrips was not sufficient, yet better with E. ovalis. However, whitefly densities in presence of thrips were reduced dramatically, especially by A. swirskii. The densities of predators were up to 15 times higher in presence of both pests than in the single-pest treatments. Laboratory experiments with A. swirskii suggest that this is due to a higher juvenile survival and developmental rate on a mixed diet. Hence, better control may be achieved not only because of apparent competition, but also through a positive effect of mixed diets on predator population growth. This latter phenomenon deserves more attention in experimental and theoretical work on biological control and apparent competition.     

Reducing the abundance of leafhoppers and thrips in a northern California organic vineyard through maintenance of full season floral diversity with summer cover crops

1 Maintenance of floral diversity throughout the growing season in vineyards in the form of summer cover crops of buckwheat (Fagopyrum esculentum Moench) and sunflower (Helianthus annus Linnaeus), had a substantial impact on the abundance of western grape leafhoppers, Erythroneura elegantula Osborn (Homoptera: Cicadellidae), and western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), and associated natural enemies. 2 During two consecutive years, vineyard systems with flowering cover crops were characterized by lower densities of leafhoppers and thrips, and larger populations and more species of general predators, including spiders. 3 Although Anagrus epos Girault (Hymenoptera: Mymaridae), the most important leafhopper parasitoid, achieved high numbers and inflicted noticeable mortality of grape leafhopper eggs, no differences in egg parasitism rates were observed between cover cropped and monoculture systems. 4 Mowing of cover crops forced movement of Anagrus and predators to adjacent vines resulting in the lowering of leafhopper densities in such vines. 5 Results indicate that habitat diversification using summer cover crops that bloom most of the growing season, supports large numbers of predators and parasitoids thereby favouring enhanced biological control of leafhoppers and thrips in vineyards.     

Performance of the predator Amblyseius swirskii (Acari: Phytoseiidae) on greenhouse eggplants in the absence and presence of pine Pinus brutia (Pinales:Pinaceae) pollen

In Turkey, the western thrips Frankliniella occidentalis (Pergande) is a key pest affecting eggplants grown in greenhouses for which an appropriate control strategy is under investigation. It was observed in a previous study that the release of the beneficial predatory mite Amblyseius swirskii (Athias‐Henriot) alone did not result in an effective control of thrips on eggplants. Since pollen is known to improve control efficiency of predators, this study was undertaken to investigate if provision of pollen to eggplants can greatly improve the efficiency of A. swirskii in controlling thrips. The experiments were carried out in both greenhouse and low tunnel. The provision of pollen led to a significant increase in the predator population density on the eggplants but did not result in an effective control of the thrips populations. In this paper, various factors are discussed that could have affected the efficiency of the predatory mite in controlling F. occidentalis on eggplants.     

Life tables for the guava psyllid Triozoida limbata in southeastern Brazil

The aim of this study was to identify, quantify, and determine the importance of biological control agents of the psyllid Triozoida limbata (Enderlein) (Hemiptera: Sternorrhyncha: Triozidae). Ecological life tables were developed during four periods to determine the critical stage and key mortality factors of this pest. Predation and parasitism were found to be the two major factors driving the population dynamics of this pest. The major predators of eggs and nymphs of first and second instars were coccinellids, predatory thrips, lacewings, ants, and spiders, while the major predators of third, fourth, and fifth instars were several species of predatory wasps and syrphids. The endoparasitoid Psyllaephagus sp. (Hymenoptera: Encyrtidae) parasitized fifth instar psyllids. The fifth instar was found to be the critical mortality stage of T. limbata, and key mortality factors include the parasitoid Psyllaephagus sp. and predatory wasps.     

Amount and time course of ingestion of plant subcellular fractions by two thrips and one reference mite species

Thrips are known as cell-feeding sucking pests, but little information is available on which and how much of each subcellular fraction they ingest. In this study, the ingested amounts of nuclei and plastids in two representative thrips species (the western flower thrips, Frankliniella occidentalis, and the garden thrips, Frankliniella intonsa) along with two reference sucking pests (the two-spotted spider mite, Tetranychus urticae, a cell feeder, and the brown planthopper, Nilaparvata lugens, a sap feeder) were quantified by quantitative PCR using phytoene desaturase and rubisco as respective marker genes following feeding. The ingested amounts of plastids were significantly greater than those of nuclei in the thrips and mite species. In the thrips species, however, the fold differences in ingested amount between the two fractions were substantially lower than their original ratio in intact plant cells, suggesting that thrips ingest nuclei more selectively than plastids. Unlike the thrips species, the ratio between nuclei and plastids increased in T. urticae. In contrast to these cell-feeding insects, no subcellular fraction was detected in N. lugens. These findings suggest that transgenic expression of foreign hairpin RNA in the nucleus would deliver a substantial amount of target molecules to cell-feeding sucking pests, but not sap-feeding pests, when employing ingestion RNA interference-based control strategies.     

Thysanoptera of Bulgaria

The present checklist includes data on the species composition, geographic distribution and feeding preferences of thrips species in Bulgaria. In total, 155 species in 48 genera are listed. Of these, 125 species belong to suborder Terebrantia and include 103 species of 33 genera in family Thripidae, 14 species of two genera in Aeolothripidae, seven species of two genera in Melanthripidae and one species in Fauriellidae. In suborder Tubulifera, 30 species of 10 genera in the single family Phlaeothripidae are listed. Of the 155 Bulgarian thrips species, 87.7% are phytophagous, 4.5% are obligate predators, 5.8% are mycophagous and 1.9% are with unknown feeding preferences. Fourteen pest species are listed for Bulgaria, of which Frankliniella occidentalis, Thrips tabaci and Haplothrips tritici are of economic importance. The list provides detailed information on the horizontal and vertical distribution of Thysanoptera in 5 regions and 45 subregions of Bulgaria. The present paper also includes an evaluation of the biodiversity of Thysanoptera and the extent to which each region of the country has been studied.     

Positive association between thrips and spider mites in seedling cotton

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Oviposition patterns in a predatory mite reduce the risk of egg predation caused by prey

Abstract 1. Predatory arthropods lay their eggs such that their offspring have sufficient prey at their disposal and run a low risk of being eaten by conspecific and heterospecific predators, but what happens if the prey attacks eggs of the predator? 2. The egg distribution and time allocation of adult female predatory mites Iphiseius degenerans as affected by predation of their eggs by prey, the western flower thrips Frankliniella occidentalis, were studied on sweet pepper plants. The predatory mites attack the first instar of thrips but all active stages of thrips are capable of killing the eggs of the predator; however the predatory mite is used for biological control of thrips. 3. The majority of predatory mite eggs was laid on the underside of leaves in hair tufts (domatia). During the experiment, females spent increasing amounts of time in flowers where they fed on pollen and thrips larvae. The risk of predation on predator eggs by thrips was lower on leaves than in flowers where the majority of thrips resides. Moreover, predation risk was higher outside leaf domatia than inside. 4. This suggests that predators avoid ovipositing in places with abundant prey to prevent their eggs from being eaten by thrips.