Review: predatory soil mites as biocontrol agents of above- and below-ground plant pests

Biological pest control is becoming increasingly important for sustainable agriculture. Although many species of natural enemies are already being used commercially, efficient biological control of various pests is still lacking, and there is a need for more biocontrol agents. In this review, we focus on predatory soil mites, their role as natural enemies, and their biocontrol potential, mainly in vegetable and ornamental crops, with an emphasis on greenhouse systems. These predators are still underrepresented in biological control, but have several advantages compared to predators living on above-ground plant parts. For example, predatory soil mites are often easy and affordable to mass rear, as most of them are generalist predators, which also means that they may be used against various pests and can survive periods of pest scarcity by feeding on alternative prey or food. Many of them can also endure unfavourable conditions, making it easier for them to establish in various crops. Based on the current literature, we show that they have potential to control a variety of pests, both in greenhouses and in the field. However, more research is needed to fully understand and appreciate their potential as biocontrol agents. We review and discuss several methods to increase their efficiency, such as supplying them with alternative food and changing soil/litter structure to enable persistence of their populations. We conclude that predatory soil mites deserve more attention in future studies to increase their application in agricultural crops.

     

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.     

Constraints to the implementation of biological control in Sri Lanka

Sri Lanka is a tropical island with a rich diversity of arthropods, with many species of indigenous natural enemies of economic pests. However, no extensive island wide surveys have been carried out for natural enemies of major crop ecosystems and only a few of the indigenous natural enemies are reported useful for augmentation biological pest control by massive field releases of laboratory-produced insects. Most successful biological control programs on the island are importation (i.e. classical) biological control programs, where established exotic natural enemies control certain pest populations in valuable crops. There is growing interest in the use of native natural enemies in pest management, thus creating a need for intensive research on the ecology of indigenous natural enemies and development of infrastructure and technology to produce natural enemies for augmentation. This paper examines constraints and opportunities for implementation of biological control in Sri Lanka.     

Behavioral studies,molecular approaches,and modeling: Methodological contributions to biological control success

Modern biological control practitioners must increasingly demonstrate a level of rigor that can only be achieved through use of effective methodological tools such as modeling, behavioral studies and molecular approaches. The use of these technologies is maturing rapidly in biological control and makes tangible contributions to its success. Behavioral studies often uncover important aspects of biology that would otherwise be overlooked, such as the influence of pre-release handling on establishment success and the response of natural enemies to host-induced plant volatiles. Molecular approaches allow the identification and detection of genetically distinct populations of invasive pest species and their natural enemies, tracing the origin of invasive pest populations and compatible natural enemies, and development of improved recombinant natural enemies. Modeling enables theory and empirical observation to optimize agent selection and release, and to predict quantitative impacts on target and non-target populations. All three methodologies, particularly in combination, contribute to our understanding of the reasons for success and failure in biological control, and together with post-release validation studies build the foundations to improve the success of future biological control releases.     

A simple criterion for successful biological control on annual crops

Population dynamics of pest insect-natural enemy systems on annual crops is quite different from those seen in classic biological control programes. On an annual crop, for example, the persistence of populations of pest insects is forced to terminate when crops are harvested. Pest control on annual crops aims to suppress the maximum density of the pest below a certain level, and a low level equilibrium is not always the aim. It is important to determine the initial impact just after release of a natural enemy in order to determine the success of a biological control program. Therefore, effectiveness of natural enemies should be evaluated by prediction of such short-term population dynamics. This paper presents a new and simple analytical model for successful biological control on annual crops. A criterion of successful biological control is given as the ratio of the pest and natural enemy populations just when the pest begins to decrease. This ratio is derived from the intrinsic rates of natural increase of both populations and the daily total predation by natural enemies. Using this model, criteria on appropriate number and time of release of natural enemies are obtained. The practical applications of this model are discussed with respect to evaluating the success or failure of natural enemy releases in future biological control programs.     

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.     

Insect-resistant transgenic plants in a multi-trophic context

So far, genetic engineering of plants in the context of insect pest control has involved insertion of genes that code for toxins, and may be characterized as the incorporation of biopesticides into classical plant breeding. In the context of pesticide usage in pest control, natural enemies of herbivores have received increasing attention, because carnivorous arthropods are an important component of insect pest control. However, in plant breeding programmes, natural enemies of herbivores have largely been ignored, although there are many examples that show that plant breeding affects the effectiveness of biological control. Negative influences of modified plant characteristics on carnivorous arthropods may induce population growth of new, even more harmful pest species that had no pest status prior to the pesticide treatment. Sustainable pest management will only be possible when negative effects on non-target, beneficial arthropods are minimized. In this review, we summarize the effects of insect-resistant crops and insect-resistant transgenic crops, especially Bt crops, from a food web perspective. As food web components, we distinguish target herbivores, non-target herbivores, pollinators, parasitoids and predators. Below-ground organisms such as Collembola, nematodes and earthworms should also be included in risk assessment studies, but have received little attention. The toxins produced in Bt plants retain their toxicity when bound to the soil, so accumulation of these toxins is likely to occur. Earthworms ingest the bound toxins but are not affected by them. However, earthworms may function as intermediaries through which the toxins are passed on to other trophic levels. In studies where effects of insect-resistant (Bt) plants on natural enemies were considered, positive, negative and no effects have been found. So far, most studies have concentrated on natural enemies of target herbivores. However, Bt toxins are structurally rearranged when they bind to midgut receptors, so that they are likely to lose their toxicity inside target herbivores. What happens to the toxins in non-target herbivores, and whether these herbivores may act as intermediaries through which the toxins may be passed on to the natural enemies, remains to be studied.     

Biological pest control using cannibalistic predators and with provision of additional food: a theoretical study

Cannibalism is a conspecific lethal interaction, a typical phenomenon in many natural populations, which is used as a “life-boat strategy” to avoid circumstances leading to extinction. It is observed in many experimental studies that the cannibalistic nature of natural enemies deters the outcome of biological pest control programmes. One of the ways to deviate natural enemies from conspecific lethal interactions is to provide them with additional food. In this paper, using the theory of dynamical systems, we analyse the dynamics of a cannibalistic predator-prey system when predators are provided with additional food. A detailed mathematical analysis is carried out to study the permanence, stability and various bifurcations occurring in the system. The system analysis reveals several interesting phenomena. Depending on the choice of quality (characterised by the predator’s handling time towards additional food, and prey) and quantity of additional food, the system can exhibit multiple coexisting equilibria, leading to the emergence of a homoclinic loop. Further, it is observed that by varying the quality and quantity of additional food, one can not only limit and control the pest but also eradicate the predators. In the context of biological control programmes, the current theoretical study aids eco-managers in choosing the appropriate additional food that is to be supplied for enhancing the biocontrol efficiency of cannibalistic predators.     

Integrating biological and chemical controls in decision making: European corn borer (Lepidoptera: Crambidae) control in sweet corn as an example

As growers switch to transgenic crops and selective insecticides that are less toxic to natural enemies, natural enemies can become more important in agricultural pest management. Current decision-making guides are generally based on pest abundance and do not address pest and natural enemy toxicity differences among insecticides or the impact of natural enemies on pest survival. A refined approach to making pest management decisions is to include the impact of natural enemies and insecticides, thereby better integrating biological and chemical control. The result of this integration is a dynamic threshold that varies for each product and the level of biological control expected. To demonstrate the significance of conserved biological control in commercial production, a decision-making guide was developed that evaluates control options for European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), in sweet corn, Zea mays L., where the primary natural enemies are generalist predators. Management options are lambda-cyhalothrin (broad-spectrum insecticide), spinosad (selective insecticide), Trichogramma ostriniae (Peng and Chen) (Hymenoptera: Trichogrammatidae) (parasitoid), and Bacillus thuringiensis (Bt) sweet corn (transgenic variety). The key factors influencing thresholds for all treatments are the intended market, predator populations, and the presence of alternative foods for the predators. Treatment cost is the primary factor separating the threshold for each treatment within a common scenario, with the lowest cost treatment having the lowest pest threshold. However, when the impact of a treatment on natural enemies is projected over the 3-wk control period, the impact of the treatment on predators becomes the key factor in determining the threshold, so the lowest thresholds are for broad-spectrum treatments, whereas selective products can have thresholds > 6 times higher by the third week. This decision guide can serve as a framework to help focus future integrated pest management research and to aid in the selection of pest management tools.     

Outbreaks of Trialeurodes vaporariorum (West.) (Hemiptera: Aleyrodidae) under field conditions in the State of São Paulo, Brazil

Trialeurodes vaporariorum (West.) is a pest of greenhouse vegetables and ornamentals and infests crops in Europe and in the American continent. In Brazil, just a few cases are known on economic crops, being all restricted to greenhouse crops. In 2003, in Itatiba and neighboring localities of State of S?o Paulo, Brazil, field infestations of T. vaporariorum were observed, mainly on tomato and green bean. So far, whitefly infestation in this area expanded to squash and kale also. Field studies are needed for determining interactions of T. vaporariorum with plants and natural enemies, injury levels, and methods of control.     

Landscape-scale forest cover increases the abundance of Drosophila suzukii and parasitoid wasps

Agricultural landscapes rich in natural and semi-natural habitats promote biodiversity and important ecosystem services for crops such as pest control. However, semi-natural habitats may fail to deliver these services if agricultural pests are disconnected from the available pool of natural enemies, as may be the case with invasive species. This study aimed to provide insights into the relationship between landscape complexity and the abundance of the recently established invasive pest species Drosophila suzukii and a group of natural enemies (parasitoid wasps), which contain species that parasitize D. suzukii in native and invaded ecosystems. The importance of landscape complexity was examined at two spatial scales. At the field scale, the response to introduction of wildflower strips was analysed, while the relationship with forest cover was assessed at the landscape scale. Half of the surveys were done next to blueberry crops (Vaccinium corymbosum), the other half was done in landscapes without fruit crops to examine effects of D. suzukii host presence. As expected, the number of observed parasitoid wasps increased with amount of forest surrounding the blueberry fields, but the number of D. suzukii individuals likewise increased with forest cover. Establishment of wildflower strips did not significantly affect the abundance of D. suzukii or parasitoid wasps and insect phenology was similar in landscapes with and without blueberry crops. This suggests that D. suzukii is enhanced by landscape complexity and is largely unlinked from the species group that, in its native range, hosts key natural enemies. Although management practices that rely on enhancing natural enemies through habitat manipulations can contribute to the long-term stability of agroecosystems and to control agricultural pests, other control measures may still be necessary in the short term to counteract the benefits obtained by D. suzukii from natural habitats.     

农业景观生物多样性与害虫生态控制

现代农业的一个重要特征就是人类对农田生态系统的干扰强度及频率不断增加,严重影响农业景观的结构及其生物多样性.农业景观结构的变化及其生物多样性的丧失,必然引起生态系统服务功能的弱化,不利于实施以保护自然天敌为主的害虫生态控制.农业的集约化经营导致自然生境破碎化,减少了农业景观的复杂性,使得作物和非作物变成一种相对离散化的生境类型和镶嵌的景观格局;破碎化的生境不仅会减少某些物种的丰度,还会影响物种之间的相互关系及生物群落的多样性和稳定性.非作物生境类型如林地、灌木篱墙、田块边缘区、休耕地和草地等,是一种比较稳定的异质化环境.非作物生境较少受到干扰,可以为寄生性和捕食性节肢动物提供适宜的越冬或避难场所以及替代猎物、花粉和花蜜等资源,因此,非作物生境有利于自然天敌的栖息和繁衍,也有利于它们迁入邻近的作物生境中对害虫起到调节和控制作用.景观的格局-过程-尺度影响农田生物群落物种丰富度、多度、多样性以及害虫与天敌之间的相互作用.从区域农业景观系统的角度出发,运用景观生态学的理论和方法来研究作物、害虫、天敌等组分在不同斑块之间的转移过程和变化规律,揭示害虫在较大尺度和具有异质性的空间范围内的灾变机理,可为利用农业景观生物多样性来保护农田自然天敌,实施害虫的区域性生态控制提供新的研究思路和手段.     

Global land-use change and the importance of zoophytophagous bugs in biological control: Coppicing willows as a timely example

Perennial plants, such as willows, miscanthus, and hybrid poplars, are promising bioenergy crops while lowering atmospheric CO₂. Increases in the acreage of perennial bioenergy crops will pose new challenges and opportunities for biological control. In this review, we suggest that zoophytophagous bugs could be expected to become increasingly important in biological control of arthropod pests in perennial bioenergy crops. The main reasons are: (1) perennial bioenergy crops provide suitable habitats for arboreal natural enemies like zoophytophagous bugs; (2) zoophytophagous bugs often increase in response to low disturbance frequencies; and (3) plant-feeding by zoophytophagous bugs will not likely affect plant biomass production in perennial crops. We review aspects of the biology of zoophytophagous bugs expected to be important in biological control of pests in perennial systems. We also present a predator–prey model investigating how alternative harvest methods affect biological control of herbivorous pests by zoophytophagous bugs in willow biomass plantations. Although there is good evidence that zoophytophagous bugs can provide pest control, more research is needed about factors affecting the dispersal and population dynamics of zoophytophagous bugs in agricultural landscapes.     

Plant volatiles: new perspectives for research in Brazil

Agroecosystems consist on complex trophic relationships among host plants, herbivores and their natural enemies. This article reviews the research of plant volatiles in Brazil, in order to determine multiple resistance mechanisms of economically important crops and to contribute to the understanding of insect-plant interactions. Most pest management programs, including chemical and biological control, do not consider the impact of these chemicals on herbivores and their natural enemies. Alternative control methods are being developed in order to improve our understanding on the endogenous mechanisms of plant induced defenses against phytophagous arthropods. The use of plant volatiles technology as an additional tool in integrated pest management programs would offer a new and environmentally sound approach to crop protection. This technique involves the development of baits that attract beneficial organisms and the manipulation of biochemical processes that induce and regulate plant defenses, key factors in the improvement of control programs against economically important pests. The elucidation of the mechanisms involved in the indirect defenses of plants will result in useful tools for biological control of crop pests.     

Review Behaviour and indirect interactions in food webs of plant-inhabiting arthropods

With the increased use of biological control agents, artificial food webs are created in agricultural crops and the interactions between plants, herbivores and natural enemies change from simple tritrophic interactions to more complex food web interactions. Therefore, herbivore densities will not only be determined by direct predator–prey interactions and direct and indirect defence of plants against herbivores, but also by other direct and indirect interactions such as apparent competition, intraguild predation, resource competition, etc. Although these interactions have received considerable attention in theory and experiments, little is known about their impact on biological control. In this paper, we first present a review of indirect food web interactions in biological control systems. We propose to distinguish between numerical indirect interactions, which are interactions where one species affects densities of another species through an effect on the numbers of an intermediate species and functional indirect interactions, defined as changes in the way that two species interact through the presence of a third species. It is argued that functional indirect interactions are important in food webs and deserve more attention. Subsequently, we discuss experimental results on interactions in an artificial food web consisting of pests and natural enemies on greenhouse cucumber. The two pest species are the two-spotted spider mite Tetranychus urticae and the western flower thrips, Frankliniella occidentalis. Their natural enemies are the predatory mite Phytoseiulus persimilis, which is commonly used for spider mite control and the predatory mites Neoseiulus cucumeris and Iphiseius degenerans and the predatory bug Orius laevigatus, all natural enemies of thrips. First, we analyse the possible interactions between these seven species and we continue by discussing how functional indirect interactions, particularly the behaviour of arthropods, may change the significance and impact of direct interactions and numerical indirect interactions. It was found that a simple food web of only four species already gives rise to some quite complicated combinations of interactions. Spider mites and thrips interact indirectly through resource competition, but thrips larvae are intraguild predators of spider mites. Some of the natural enemies used for control of the two herbivore species are also intraguild predators. Moreover, spider mites produce a web that is subsequently used by thrips to hide from their predators. We discuss these and other results obtained so far and we conclude with a discussion of the potential impact of functional indirect and direct interactions on food webs and their significance for biological control.     

Prospects for improved off-crop habitat management for pollen beetle control in oilseed rape

There is an urgent need to develop sustainable and environmentally benign integrated pest management (IPM) strategies for arable crops. The enhancement and manipulation of naturally occurring populations of the natural enemies of crop pests through habitat management for ‘conservation biological control’, as well as habitat management to manipulate populations of the pests themselves, have the potential to become major components of successful IPM strategies. We review the studies that have contributed to our current understanding of how the crop margin, local landscape, and regional landscape can influence pollen beetle Brassicogethes aeneus (syn. Meligethes aeneus) (Coleoptera: Nitidulidae) abundance and damage to oilseed rape crops (Brassica napus), and the efficacy of their natural enemies. We also discuss how habitat management across these multiple scales may improve pollen beetle control, reducing the need for insecticide use and contributing towards sustainable production of this important crop which is grown on increasing areas for both food and fuel.     

Connecting scales: Achieving in‐field pest control from areawide and landscape ecology studies

Areawide management has a long history of achieving solutions that target pests, however, there has been little focus on the areawide management of arthropod natural enemies. Landscape ecology studies that show a positive relationship between natural enemy abundance and habitat diversity demonstrate landscape‐dependent pest suppression, but have not yet clearly linked their findings to pest management or to the suite of pests associated with crops that require control. Instead the focus has often been on model systems of single pest species and their natural enemies. We suggest that management actions to capture pest control from natural enemies may be forth coming if: (i) the suite of response and predictor variables focus on pest complexes and specific management actions; (ii) the contribution of “the landscape” is identified by assessing the timing and numbers of natural enemies immigrating and emigrating to and from the target crop, as well as pests; and (iii) pest control thresholds aligned with crop development stages are the benchmark to measure impact of natural enemies on pests, in turn allowing for comparison between study regions, and generalizations. To achieve pest control we will need to incorporate what has been learned from an ecological understanding of model pest and natural enemy systems and integrate areawide landscape management with in‐field pest management.     

More intraguild prey than pest species in arachnid diets may compromise biological control in apple orchards

Understanding the full diet of natural enemies is necessary for evaluating their role as biocontrol agents, because many enemy species do not only feed on pests but also on other natural enemies. Such intraguild predation can compromise pest control if the consumed enemies are actually better for pest control than their predators. In this study, we used gut metabarcoding to quantify diets of all common arachnid species in Swedish and Spanish apple orchards. For this purpose, we designed new primers that reduce amplification of arachnid predators while retaining high amplification of all prey groups. Results suggest that most arachnids consume a large range of putative pest species on apple but also a high proportion of other natural enemies, where the latter constitute almost a third of all prey sequences. Intraguild predation also varied between regions, with a larger content of heteropteran bugs in arachnid guts from Spanish orchards, but not between orchard types. There was also a tendency for cursorial spiders to have more intraguild prey in the gut than web spiders. Two groups that may be overlooked as important biocontrol agents in apple orchards seem to be theridiid web spiders and opilionids, where the latter had several small-bodied pest species in the gut. These results thus provide important guidance for what arachnid groups should be targets of management actions, even though additional information is needed to quantify all direct and indirect interactions occurring in the complex arthropod food webs in fruit orchards.     

Predicting the effects of climate change on natural enemies of agricultural pests

Climate change can have diverse effects on natural enemies of pest species. Here we review these effects and their likely impacts on pest control. The fitness of natural enemies can be altered in response to changes in herbivore quality and size induced by temperature and CO₂ effects on plants. The susceptibility of herbivores to predation and parasitism could be decreased through the production of additional plant foliage or altered timing of herbivore life cycles in response to plant phenological changes. The effectiveness of natural enemies in controlling pests will decrease if pest distributions shift into regions outside the distribution of their natural enemies, although a new community of enemies might then provide some level of control. As well as being affected by climate through host plants and associated herbivores, the abundance and activity of natural enemies will be altered through adaptive management strategies adopted by farmers to cope with climate change. These strategies may lead to a mismatch between pests and enemies in space and time, decreasing their effectiveness for biocontrol. Because of the diverse and often indirect effects of climate change on natural enemies, predictions will be difficult unless there is a good understanding of the way environmental effects impact on tritrophic interactions. In addition, evolutionary changes in both hosts and natural enemies might have unexpected consequences on levels of biocontrol exerted by enemies. We consider interactions between the pest light brown apple moth and its natural enemies to illustrate the type of data that needs to be collected to make useful predictions.     

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.