G.J. Messelink

Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber

Ten predatory mite species, all phytoseiids, were evaluated for control of western flower thrips (WFT), Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), on greenhouse cucumber. This study was done to further improve biological control of thrips on this crop. Neoseiulus cucumeris (Oudemans) is at present used for biological control of thrips in greenhouses. Compared to this species, Typhlodromalus limonicus (Garman & McGregor), Typhlodromips swirskii (Athias-Henriot) and Euseius ovalis (Evans) reached much higher population levels resulting in a significantly better control of thrips. T. limonicus was clearly the best predator of WFT. Also Euseius scutalis (Athias-Henriot) increased to higher populations levels than N. cucumeris, but without controlling the thrips, probably because of an unequal distribution of this predator on the plant. Iphiseius degenerans (Berlese), Neoseiulus barkeri (Hughes), Euseius finlandicus (Oudemans) and Typhlodromus pyri (Scheuten) did not establish better than N. cucumeris. A non-diapausing exotic strain of N. cucumeris did not differ from the North European strain. The best performers in this study were all of sub-tropical origin. T. limonicus, T. swirskii and E. ovalis have good potentials for controlling not only thrips but also whiteflies. Factors affecting the efficacy of phytoseiids on greenhouse cucumbers are discussed.

The Banker Plant Method in Biological Control

In the banker plant method, long-lasting rearing units for beneficials are created in the crop by distributing plants infested with herbivores or carrying other food items, such as pollen. The method has been widely investigated over many years and used to aid establishment, development and dispersal of beneficial organisms employed in biological control. In this review, we refine the definition of the banker plant method based on previous concepts and studies and offer the term “banker plant system” to describe the unit that is purposefully added to or established in a crop for control of pests in greenhouses or open field. The three basic elements of a banker plant system (banker plant, food source, beneficials) are discussed and illustrated with examples, and the diversity of banker plant systems (classified by target pest) used or investigated is documented. The benefits of using banker plant systems, such as low cost, increased freshness of beneficials, possibility for preventive control and for integration within IPM frameworks, make the method an interesting plant protection option with potential to enhance adoption of biological control in pest management programs.

Approaches to conserving natural enemy populations in greenhouse crops: current methods and future prospects

Biological pest control in greenhouse crops is usually based on periodical releases of mass-produced natural enemies, and this method has been successfully applied for decades. However, in some cases there are shortcomings in pest control efficacy, which often can be attributed to the poor establishment of natural enemies. Their establishment and population numbers can be enhanced by providing additional resources, such as alternative food, prey, hosts, oviposition sites or shelters. Furthermore, natural enemy efficacy can be enhanced by using volatiles, adapting the greenhouse climate, avoiding pesticide side-effects and minimizing disrupting food web complexities. The special case of high value crops in a protected greenhouse environment offers tremendous opportunities to design and manage the system in ways that increase crop resilience to pest infestations. While we have outlined opportunities and tools to develop such systems, this review also identifies knowledge gaps, where additional research is needed to optimize these tools.

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.

Natural enemy‐mediated indirect interactions among prey species: potential for enhancing biocontrol services in agroecosystems

Understanding how arthropod pests and their natural enemies interact in complex agroecosystems is essential for pest management programmes. Theory predicts that prey sharing a predator, such as a biological control agent, can indirectly reduce each others density at equilibrium (apparent competition). From this premise, we (i) discuss the complexity of indirect interactions among pests in agroecosystems and highlight the importance of natural enemy-mediated indirect interactions other than apparent competition, (ii) outline factors that affect the nature of enemy-mediated indirect interactions in the field and (iii) identify the way to manipulate enemy-mediated interactions for biological control. We argue that there is a need to increase the link between community ecology theory and biological control to develop better agroecological methods of crop protection via conservation biological control. In conclusion, we identify (i) interventions to be chosen depending on agroecosystem characteristics and (ii) several lines of research that will improve the potential for enemy-mediated indirect interactions to be applied to biological control.

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.

Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper

Zoophytophagous predators of the family Miridae (Heteroptera), which feed both on plant and prey, often maintain a close relationship with certain host plants. In this study, we aimed to select a suitable mirid predatory bug for aphid control in sweet pepper. Four species were compared: Macrolophus pygmaeus (Rambur), Dicyphus errans (Wolff), Dicyphus tamaninii Wagner and Deraeocoris pallens (Reuter). They were assessed on their establishment on sweet pepper plants with and without supplemental food (eggs of the flour moth Ephestia kuehniella Zeller and decapsulated cysts of the brine shrimp Artemia franciscana Kellogg) and on their effects on aphids with releases before and after aphid infestations. None of the predator species was able to control an established population of aphids on sweet pepper plants; however, the predators M. pygmaeus and D. tamaninii could successfully reduce aphid populations when released prior to an artificially introduced aphid infestation. The best results were achieved with M. pygmaeus in combination with a weekly application of supplemental food. Hence, our results demonstrate that the order and level of plant colonization by mirid predators and aphids determines how successful biological control is. Further studies are needed to evaluate the performance of mirid predatory bugs in sweet pepper crops in commercial greenhouses with multiple pests and natural enemies, in particular to understand how increased variation in food sources affects their feeding behaviour and preferences.

New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops

Biological pest control with mass-produced arthropod natural enemies is well developed in greenhouse crops and has often resulted in the evolution of complex ecosystems with persistent populations of multiple arthropod natural enemy species. However, there are cases where arthropod natural enemies are either not effective enough, not available, or their use is rather costly. For these reasons, biological control based on microorganisms, also referred to as ‘microbials’, represents a complementary strategy for further development. Although commercially available microbials have been around for quite some time, research on and the applied use of combinations of arthropod natural enemies and microbials have remained relatively under explored. Here, we review current uses of entomopathogenic fungi, bacteria and viruses, and their possible direct and indirect effects on arthropod natural enemies in European greenhouses. We discuss how microbials might be combined with arthropod natural enemies in the light of new methodologies and technologies such as conservation biological control, greenhouse climate management, and formulation and delivery. Furthermore, we explore the possibilities of using other microorganisms for biological control, such as endophytes, and the need to understand the effect of insect-associated microorganisms, or symbionts, on the success of biological control. Finally, we suggest future research directions to optimize the combined use of microbials and arthropod natural enemies in greenhouse production.

Generalist Predators, Food Web Complexities and Biological Pest Control in Greenhouse Crops

Biologische bestrijding van plagen in kassen was lange tijd voornamelijk gericht op specialistische natuurlijke vijanden die sterk zijn aangepast aan hun prooi. Gerben Messelink onderzocht de rol van generalistische predatoren bij de bestrijding van meerdere plagen in de teelt van vruchtgroenten in kassen. Uit zijn resultaten blijkt dat spintmijten en witte vliegen - twee wereldwijde plagen - op een komkommergewas veel beter worden bestreden met generalistische roofmijten wanneer er ook tripsen (een ander belangrijk plaaginsect) aanwezig waren. Dit komt vooral doordat de roofmijten zich op een dieet van verschillende prooien sneller ontwikkelen. Hierdoor worden er snel hoge predatordichtheden bereikt. Messelink vond een vergelijkbaar mechanisme bij de bestrijding van plagen in paprika: roofwantsen gaven een zeer goede bestrijding van bladluis in de aanwezigheid van tripsen. Messelink verwacht dat generalistische predatoren in toenemende mate gebruikt zullen worden voor biologische plaagbestrijding in kassen, omdat de predatoren profiteren van een gemengd dieet van verschillende plagen en de plaagbestrijding op die manier makkelijker maakt.

Prey temporarily escape from predation in the presence of a second prey species

1. Indirect interactions between populations of different prey species mediated by a shared predator population are known to affect prey dynamics.