Biological control of arthropod pests using banker plant systems: Past progress and future directions

The goal of banker plant systems is to sustain a reproducing population of natural enemies within a crop that will provide long-term pest suppression. The most common banker plant system consists of cereal plants infested with Rhopalosiphum padi L. as a host for the parasitoid Aphidius colemani L. Aphidius colemani continually reproduce and emerge from the banker plants to suppress aphid pests such as Aphis gossypii Glover and Myzus persicae Sulzer. Banker plant systems have been investigated to support 19 natural enemy species targeting 11 pest species. Research has been conducted in the greenhouse and field on ornamental and food crops. Despite this there is little consensus of an optimal banker plant system for even the most frequently targeted pests. Optimizing banker plant systems requires future research on how banker plants, crop species, and alternative hosts interact to affect natural enemy preference, dispersal, and abundance. In addition, research on the logistics of creating, maintaining, and implementing banker plant systems is essential. An advantage of banker plant systems over augmentative biological control is preventative control without repeated, expensive releases of natural enemies. Further, banker plants conserve a particular natural enemy or potentially the ‘right diversity’ of natural enemies with specific alternative resources. This may be an advantage compared to conserving natural enemy diversity per se with other conservation biological control tactics. Demonstrated grower interest in banker plant systems provides an opportunity for researchers to improve biological control efficacy, economics, and implementation to reduce pesticide use and its associated risks.     

Evaluation of pest control efficiencies for different banker plant systems with a simple predator–prey model

The banker plant system has been introduced for the biological control of various pest species in Japanese greenhouses. With the banker plant system, non-crop plants infested with a host insect (a non-commercial crop pest) are placed in the greenhouse to provide alternative resources for the parasitoids or predators. We want to evaluate the effectiveness for controlling pests on the crop in a quantitative way by immigrating predators from the banker plant. Therefore, we developed a simple model for the interaction of the pest and predator in the crop and included the banker plant only as a source for predators. For three different pest-predator systems we parameterised the model and used these models to predict under what conditions biological control in a banker plant system is successful. We defined successful as keeping the pest below the economic injury level of the crop estimated from damage analysis. Because the crop is mostly grown during a period that lasts less than a year our analysis should not only focus on the equilibrium dynamics. In contrast, it should also focus on the transient dynamics. Our main analytical result, from the equilibrium analysis, is that for successful control the maximum lifetime consumption of immigrating predators should exceed the daily prey growth at half the value of the maximum consumption rate. For practical purpose this translates into the fact that the immigration of predators at a low initial pest density is crucial for successful control.     

Biological control of Myzus persicae (Hemiptera: Aphididae) through banker plant system in protected crops

Banker plants with Aphidius colemani were tested in greenhouse for control of Myzus persicae on arugula and sweet pepper crops and compared to inoculative releases of parasitoids. Banker plants system consisted of pots of oat (non-crop plant) infested with Rhopalosiphum padi (non-pest herbivore). The non-pest herbivore serves as an alternative host for A. colemani (parasitoid of the target crop pest). In the arugula crop significant differences in the pest population between the two strategies of biological control showed the lowest densities of the pest when introducing the banker plant system. In the sweet pepper crop, there was no difference in the pest population between the two strategies of biological control.     

Tracking the movement of Nesidiocoris tenuis among banker plants and crops in a tomato greenhouse by DNA markers of host plants

The zoophytophagous predator, Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae), is an important biological control agent. To maintain this insect, several non-crop host plants are used as banker plants in greenhouse crop systems. To optimize the efficiency of the predator-banker plant interaction, it is necessary to investigate how individual predators move between banker plants and crops. However, the movement is difficult to quantify under field conditions. Therefore, we investigated the movement of N. tenuis between tomato plants (Solanum lycopersicum L., Solanales: Solanaceae) and three banker plants (Cleome hassleriana Chod., Brassicales: Cleomaceae; Sesamum indicum L., Lamiales: Pedaliaceae; and Verbena × hybrida Voss, Lamiales: Verbenaceae) in a greenhouse by conducting PCR using plant-species-specific primers. Laboratory analysis results showed that our molecular method could detect N. tenuis activity within a relatively short time (≤ 24 h). In addition, N. tenuis predation on a pest species was unlikely to result in false detection of plant DNA in the pest (suggesting that N. tenuis had been on the plants). Multiple plant species were detected in adult insects collected from the greenhouse plants, indicating that N. tenuis frequently moved across the mentioned plant species. The movement patterns of N. tenuis between plant species varied substantially based on the plant species from which they were collected, which suggested each of the plant species had different functions for N. tenuis. Our findings revealed that planting multiple host plants would stabilize the N. tenuis population in biological control programs.

     

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.     

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.     

Mechanisms for flowering plants to benefit arthropod natural enemies of insect pests： Prospects for enhanced use in agriculture

Reduction of noncrop habitats, intensive use of pesticides and high levels of disturbance associated with intensive crop production simplify the farming landscape and bring about a sharp decline of biodiversity. This, in turn, weakens the biological control ecosystem service provided by arthropod natural enemies. Strategic use of flowering plants to enhance plant biodiversity in a well-targeted manner can provide natural enemies with food sources and shelter to improve biological control and reduce dependence on chemical pesticides. This article reviews the nutritional value of various types of plant-derived food for natural enemies, possible adverse effects on pest management, and the practical application of flowering plants in orchards, vegetables and field crops, agricultural systems where most research has taken place. Prospects for more effective use of flowering plants to maximize biological control of insect pests in agroecosystem are good but depend up on selection of optimal plant species based on information on the ecological mechanisms by which natural enemies are selectively favored over pest species.     

小麦－玉米蚜－龟纹瓢虫载体植物系统的构建初探

载体植物系统（Banker plant system, BPS）通过建立自然天敌的自我维持机制以持续控制田间及保护地害虫。本研究分别以玉米蚜Rhopalosiphum maidis (Fitch)和小麦Triticum aestivum L.作为替代猎物和载体植物,构建龟纹瓢虫Propylaea japonica (Thunberg)载体植物系统防控桃蚜Myzus persicae (Sulzer),通过正交试验设计优化该载体植物系统中各因子的组合,并对该系统繁殖的龟纹瓢虫对玉米蚜和目标害虫桃蚜的取食选择性进行研究。结果显示,龟纹瓢虫成虫获得量最大的组合是小麦播种后第四天接蚜720头,待蚜虫扩繁5天后,投入龟纹瓢虫初孵幼虫30头。取食选择性试验结果表明小麦载体植物扩繁的龟纹瓢虫对靶标害虫桃蚜具有良好的捕食作用。     

Improving containment strategies in biopharming

This review examines the challenges of segregating biopharmed crops expressing pharmaceutical or veterinary agents from mainstream crops, particularly those destined for food or feed use. The strategy of using major food crops as production vehicles for the expression of pharmaceutical or veterinary agents is critically analysed in the light of several recent episodes of contamination of the human food chain by non-approved crop varieties. Commercially viable strategies to limit or avoid biopharming intrusion into the human food chain require the more rigorous segregation of food and non-food varieties of the same crop species via a range of either physical or biological methods. Even more secure segregation is possible by the use of non-food crops, non-crop plants or in vitro plant cultures as production platforms for biopharming. Such platforms already under development range from outdoor-grown Nicotiana spp. to glasshouse-grown Arabidopsis , lotus and moss. Amongst the more effective methods for biocontainment are the plastid expression of transgenes, inducible and transient expression systems, and physical containment of plants or cell cultures. In the current atmosphere of heightened concerns over food safety and biosecurity, the future of biopharming may be largely determined by the extent to which the sector is able to maintain public confidence via a more considered approach to containment and security of its plant production systems.     

Development of a PCR‐based method to monitor arthropod dispersal in agroecosystems: Macrolophus pygmaeus (Hemiptera: Miridae) from banker plants to tomato crops

Development of conservation biological control programs requires the identification of sources that contribute to predator colonization of crops. Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae) is an efficient polyphagous predator used in biological control programs in vegetable crops in Europe. We have developed a marking method based on spraying with a solution of the brine shrimp Artemia spp. (Anostraca: Artemiidae) cysts, followed by a PCR detection of Artemia DNA to monitor M. pygmaeus dispersal from banker plants to tomato crops. Experiments conducted in climatic chambers show that the topical application of this marking solution on M. pygmaeus does not significantly reduce adult longevity and that it is detected up to 6 d after the application. When this Artemia solution was applied on Calendula officinalis L. banker plants harboring M. pygmaeus and maintained outdoors, Artemia DNA was still detected on 62% of the insects after 6 d. The conducted field applications in commercial greenhouses have confirmed the usefulness of this method to monitor M. pygmaeus dispersal from banker plants to a newly planted tomato crop. This method can be used to assess arthropod movement, being an interesting molecular approach for further improving future pest management strategies.     

Seuils et risques de pertes en cultures de maïs et de blé. Protection rationnelle,importance des auxiliaires,travaux actuels en France

It is difficult to establish economic thresholds since they vary with current commercial practices. «Indicative intervention thresholds» are used in maize and wheat; these are non-acceptable risk levels. The decision to treat or otherwise may be taken either at a high level (potential risk of high infestation) or for each field (after assessing the pest(s) present). Systematic chemical control appears to be one of the causes of the recent pest population explosions in these two crop plants. There is insufficient knowledge of sampling methods, dangerous pest levels and the role of beneficials —naturally-occurring parasites and predators. Studies must be directed towards the establishment of forecast intervention thresholds and indirect means for evaluating the risk of losses.     

A prospective research on the hedgerow's 'source' function

In pear tree, Forficula auricularia and Forficula pubescens are considered as active predators of the pest Cacopsylla pyri, since that their dispersal characteristics are of crucial importance for biological control. We studied their movement using capture-mark-release-recapture techniques. The aim of this study was to underline a hedge effect as source of beneficials spreading through the orchard. Our results show that movements are mainly linked to the C. pyri fluctuations with a food specialisation for the two species when co-occurring.     

Flowering banker plants for the delivery of multiple agroecosystem services

Ecosystem services provided by agricultural ecosystems include natural pest control and pollination, and these are important to ensure crop productivity. This study investigates the use of the banker plant Calendula officinalis L. to provide multiple ecosystem services by increasing the abundance of natural enemies for biological control of tomato pests, providing forage resources to wild bees, and improving crop yield. C. officinalis was selected for this experiment as it is used as a banker plant for Dicyphini (Hemiptera: Miridae) predators. Strips of flowering C. officinalis were established in the field edges of tomato fields and arthropod visitation to C. officinalis strips and tomato was measured. Crop damage from multiple pests of tomato was assessed in fields with C. officinalis strips and control sites. The contribution of pollination to crop yield was assessed through a pollinator exclusion experiment. The inclusion of C. officinalis in tomato fields was associated with increased abundance of Dicyphini, parasitoids, bees and other arthropod groups within these strips. A reduction in the total leaf crop damage from Lepidoptera pests was recorded in fields with C. officinalis strips. Increased fruit set and biomass were recorded in open-pollinated tomato but this was not significantly different between control and C. officinalis fields. Results presented here demonstrate that the inclusion of a companion plant can improve the conservation of beneficial arthropods and the delivery of agroecosystem services but efficacy is likely to be improved with the addition of plants, with different functional traits, and with improved attractiveness to crop pollinators.     

Establishment of papaya banker plant system for parasitoid, Encarsia sophia (Hymenoptera: Aphilidae) against Bemisia tabaci (Hemiptera: Aleyrodidae) in greenhouse tomato production

The silverleaf whitefly, Bemisia tabaci biotype B (Gennadius) (Hemiptera: Aleyrodidae), is a key pest of tomato (Solanum lycopersicum L.) and other vegetable crops worldwide. To combat this pest, a non-crop banker plant system was evaluated that employs a parasitoid, Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae) with whitefly, Trialeurodes variabilis (Quaintance) (Hemiptera: Aleyrodidae), as an alternative host for rearing and dispersal of the parasitoid to the target pest. (a) Multi-choice and no-choice greenhouse experiments were conducted to determine host specificity of T. variabilis to papaya (Carica papaya L.) and three vegetable crops including tomato, green bean (Phaseolus vulgaris L.), and cabbage (Brassica oleracea L.). The result showed that papaya was an excellent non-crop banker plant for supporting the non-pest alternative host, T. variabilis, whose adults had a strong specificity to papaya plants for feeding and oviposition in both multi-choice and no-choice tests. (b) The dispersal ability of E. sophia was investigated from papaya banker plants to tomato and green bean plants infested with B. tabaci, as well as to papaya control plants infested with T. variabilis; and (c) the percent parasitism by E. sophia on T. variabilis reared on papaya plants and on B. tabaci infested on tomato plants was also evaluated. These data proved that E. sophia was able to disperse at least 14.5 m away from papaya plants to target tomato, bean or papaya control plants within 48–96 h. Furthermore, E. sophia was a strong parasitoid of both T. variabilis and B. tabaci. There was no significant difference in percent parasitism by E. sophia on T. variabilis (36.2–47.4%) infested on papaya plants or B. tabaci (29–45.9%) on tomato plants. Thus, a novel banker plant system for the potential management of B. tabaci was established using papaya as a non-crop banker plant to support a non-pest alternative host, T. variabilis for maintaining the parasitoid to control B. tabaci. The established banker plant system should provide growers with a new option for long-term control of B. tabaci in greenhouse vegetable production. Ongoing studies on the papaya banker plant system are being performed in commercial greenhouses.     

害虫天敌的植物支持系统

保护天敌,使天敌长期有效地控制害虫是保护性生物防治的核心内容。其中,植物在维持和促进天敌控制害虫中的重要性和作用越来越受到关注。本文概述了各种支持天敌发挥效能的植物类群,论述了蜜源植物、储蓄植物、栖境植物、诱集植物、指示植物、护卫植物等在支持天敌生存和繁殖方面的生物功能,评述了研究和应用这些植物时需注意的问题,提出了科学利用这些植物以维持和增强农业生态系统中天敌发挥控害作用的植物支持系统,并指出了由于对这些植物类别的界定和定义模糊所带来的不便,给出了相应的建议。     

Does the cutting of lucerne (Medicago sativa) encourage the movement of arthropod pests and predators into the adjacent crop?

Abstract  Lucerne ( Medicago sativa ) has been suggested as an ideal refuge habitat as part of an integrated pest management (IPM) program because it harbours high numbers of beneficial arthropods. Whether or not cutting of lucerne encourages the movement of these beneficials into adjacent target crops is unknown. Vacuum samples were used to determine the effects of cutting lucerne on arthropod abundance (pests and predators) within lucerne and adjacent soybean ( Glycine max ) crops. Vacuum-sample collections of arthropods were conducted before and after lucerne cutting on seven occasions in four fields over two seasons. In the lucerne, 10 m by 1 m strips parallel to the crop interface were sampled at 5, 10, 15, 20 and 30 m from the interface. In the soybean, 10 m of row were sampled at the same distances from the crop interface. The abundance of predators in lucerne was reduced immediately after cutting at all distances from the interface. Predator abundance in soybean did not show any change. The cutting of lucerne significantly reduced pest numbers within the lucerne but had little effect on pest abundance in the adjacent soybean. The temporal pattern in pest and predator abundance was very different for each field sampled. Generally, arthropods decreased in abundance after cutting and gradually increased as the lucerne grew back. In soybeans, arthropod numbers fluctuated regardless of the cutting of the lucerne. Cutting of lucerne alone does not guarantee movement of predators into the adjacent target crop. The presence of lucerne fields within a cropping area may have some impact on regional predator populations, and so still be useful for IPM programs, but this has yet to be tested critically.     

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.     

Synergizing biological control: Scope for sterile insect technique,induced plant defences and cultural techniques to enhance natural enemy impact

When used alone, only a minority of biological control programs succeed in bringing the target pest population under sufficient control. Biological control is, therefore, usually employed with chemical, cultural, genetic or other methods in an integrated pest management (IPM) strategy. The interactions between different pest management methods, especially conventional pesticides and host plant resistance, is an area of growing research interest but relatively little consideration is given to novel combinations. This paper reviews the interactions between biological control and other forms of pest management, especially induced plant defences and the novel, non-toxic plant protection compounds that may boost these defences; and sterile insect technique. We also cover the cultural methods that offer scope to support synergies between the aforementioned methodological combinations. We conclude that despite the sometimes negative consequences of other pest management techniques for biological control efficacy, there is great scope for new strategies to be developed that exploit synergies between biological control and various other techniques. Ultimately, however, we propose that future use of biological control will involve integration at a greater conceptual scale such that this important form of pest management is promoted as one of a suite of ecosystem services that can be engineered into farming systems and wider landscapes.     

Grape powdery mildew as a food source for generalist predatory mites occurring in vineyards: effects on life-history traits

In several perennial cropping systems, generalist or omnivorous species represent important biocontrol agents. They can persist on plants by feeding on alternative foods when prey is scarce and potentially limit pest outbreaks. Among beneficials characterised by a wide food range, those belonging to the acarine family Phytoseiidae represent important biocontrol agents. Generalist predatory mites can develop and reproduce using various food sources as alternatives to their tetranychid prey. The presence of alternative food sources can also induce switching feeding behaviour of generalist predators from prey to alternative foods. We evaluated in the laboratory the role of the grape powdery mildew (GPM) for the survival, development and reproduction of Amblyseius andersoni and Typhlodromus pyri , two important beneficial phytoseiid mites, in European and North-American vineyards. We also compared life-history parameters obtained when feeding on GPM with those obtained feeding on tetranychids mite prey or cattail pollen. Results indicated that GPM is an adequate food source for generalist mite survival and development. Results suggest that GPM can sustain mite populations in the absence of higher quality food sources. Based on optimal foraging theory, comparison of life-history parameters on GPM and mite prey suggests that the disruption of phytophagous mite control by these predatory mites in the presence of GPM appears unlikely. Implications for biological control in vineyards are discussed.