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.

Phytophagy of omnivorous predator Macrolophus pygmaeus affects performance of herbivores through induced plant defences.

Plants possess various inducible defences that result in synthesis of specialized metabolites in response to herbivory, which can interfere with the performance of herbivores of the same and other species. Much less is known of the effects of plant feeding by omnivores. We found that previous feeding of the omnivorous predator Macrolophus pygmaeus on sweet pepper plants significantly reduced reproduction of the two-spotted spider mite Tetranychus urticae and western flower thrips Frankliniella occidentalis on the same plants, also on leaves that had not been exposed to the omnivore. In contrast, no effect was found on the reproduction of the green peach aphid Myzus persicae. Juvenile survival and developmental time of T. urticae and M. persicae, and larval survival of F. occidentalis were not affected by plant feeding by M. pygmaeus. Larvae of F. occidentalis feeding on leaves previously exposed to M. pygmaeus required longer to develop into adults. Defence-related plant hormones were produced locally and systemically after exposure to M. pygmaeus. The concentrations of 12-oxo-phytodienoic acid and jasmonic acid-isoleucine in the attacked leaves were significantly higher than in the corresponding leaves on the uninfested plants, and jasmonic acid concentrations showed the same trend, suggesting that jasmonic-acid-related defence pathways were activated. In contrast, similar concentrations of salicylic acid were found in the attacked leaves of M. pygmaeus-infested plants and uninfested plants. Our results show that plant feeding by omnivorous predators decreases the performance of herbivores, suggesting that it induces plant defences.

Correction to: Phytophagy of omnivorous predator Macrolophus pygmaeus affects performance of herbivores through induced plant defences.

Unfortunately, the citation of one of the papers was published erroneously in the original version and corrected here by this Erratum. The original article was corrected.

Biological control of Echinothrips americanus by phytoseiid predatory mites and the effect of pollen as supplemental food.

The poinsettia thrips, Echinothrips americanus Morgan, is an upcoming pest in greenhouse crops, causing serious damage in various vegetable and ornamental crops through extensive foliage feeding. We assessed which stages of E. americanus are attacked and killed by the phytoseiid predatory mites Amblyseius swirskii (Athias-Henriot), Amblydromalus limonicus (Garman and McGregor), Euseius gallicus Kreiter and Tixier and Euseius ovalis (Evans). Both the predation and oviposition rates were assessed in the laboratory to evaluate which mite species is potentially the most effective predator of E. americanus. In two greenhouse trials with non-flowering sweet pepper plants, we compared the efficacy of the predators E. gallicus and E. ovalis with A. swirskii and we assessed how this was affected by the application of cattail pollen. All stages of E. americanus, except adults, were consumed by all species of predatory mites. The highest predation and oviposition rates were recorded for A. limonicus followed by A. swirskii and E. ovalis when first and second larval stages were provided as prey, but E. ovalis appeared to be the best predator of thrips pupae. Euseius gallicus displayed very low predation and oviposition rates compared to the other species of predatory mites. Cattail pollen did not support the population growth of poinsettia thrips, but it strongly increased the predatory mite population densities, particularly those of E. ovalis. Both A. swirskii and E. ovalis significantly reduced thrips densities on plants. The application of pollen significantly enhanced the control of E. americanus by A. swirskii; this was not the case for E. ovalis. Euseius gallicus did not reduce densities of E. americanus on sweet pepper plants, not even at high densities in the presence of pollen.

Supplemental food that supports both predator and pest: a risk for biological control?

Supplemental food sources to support natural enemies in crops are increasingly being tested and used. This is particularly interesting for generalist predators that can reproduce on these food sources. However, a potential risk for pest control could occur when herbivores also benefit from supplemental food sources. In order to optimize biological control, it may be important to select food sources that support predator populations more than herbivore populations. In this study we evaluated the nutritional quality of four types of supplemental food for the generalist predatory mites Amblyseius swirskii Athias-Henriot and Amblydromalus (Typhlodromalus) limonicus (Garman and McGregor), both important thrips predators, and for the herbivore western flower thrips Frankliniella occidentalis Pergande, by assessing oviposition rates. These tests showed that application of corn pollen, cattail pollen or sterilized eggs of Ephestia kuehniella Zeller to chrysanthemum leaves resulted in three times higher oviposition rates of thrips compared to leaves without additional food. None of the tested food sources promoted predatory mites or western flower thrips exclusively. Decapsulated cysts of Artemia franciscana Kellogg were not suitable, whereas cattail pollen was very suitable for both predatory mites and western flower thrips. In addition, we found that the rate of thrips predation by A. swirskii can be reduced by 50 %, when pollen is present. Nevertheless, application of pollen or Ephestia eggs to a chrysanthemum crop still strongly enhanced the biological control of thrips with A. swirskii, both at low and high release densities of predatory mites through the strong numerical response of the predators. Despite these positive results, application in a crop should be approached with caution, as the results may strongly depend on the initial predator-prey ratio, the nutritional quality of the supplemental food source, the species of predatory mites, the distribution of the food in the crop and the type of crop.

Sublethal impacts of essential plant oils on biochemical and ecological parameters of the predatory mite Amblyseius swirskii.

The generalist predatory mite Amblyseius swirskii is a widely used natural enemy of phytophagous pests. Due to the negative effects of conventional pesticides on non-target organisms, the development of selective natural and eco-friendly pesticides, such as essential plant oils, are useful pest control tools to use in synergy with biological control agents. Essential oils of Nepeta crispa, Satureja hortensis, and Anethum graveolens showed promising results to control Tetranychus urticae. Hence an experiment was carried out to evaluate the effects of these essential oils on the biochemical and demographic parameters of A. swirskii. A significant reduction of carbohydrate, lipid, and protein contents of oil-treated predatory mites was observed. However, essential oils of S. hortensis and A. graveolens had no effect on lipid reserves. The glutathione S-transferase activity of A. swirskii was influenced by A. graveolens oil treatment. In addition, the enzyme activity of the α-esterases was elevated by all treatments. The essential oils showed no effect on ß-esterases activity compared to the control treatment. None of the concentrations of the different tested oils affected the population growth parameters of A. swirskii. However, a significant reduction was observed in oviposition time and total fecundity of predatory mites. A population projection predicted the efficacy of predatory mites will likely be decreased when expose to the essential oils; however, population growth in the S. hortensis treatment was faster than in the other two treatments not including the control. The results presented in this study may have critical implications for integrated pest management (IPM) programs. However, our observations show that using the tested essential plant oils requires some caution when considered as alternatives to synthetic pesticides, and in combination with A. swirskii. Semi-field and field studies are still required to evaluate the effects on T. urticae and A. swirskii of the essential oils tested in this study, before incorporating them into IPM strategies.

Biodiversity in and around Greenhouses: Benefits and Potential Risks for Pest Management.

One of the ecosystem services of biodiversity is the contribution to pest control through conservation and stimulation of natural enemies. However, whether plant diversity around greenhouses is beneficial or a potential risk is heavily debated. In this review, we argue that most greenhouse pests in temperate climates are of exotic origin and infest greenhouses mainly through transportation of plant material. For indigenous pests, we discuss the potential ways in which plant diversity around greenhouses can facilitate or prevent pest migrations into greenhouses. As shown in several studies, an important benefit of increased plant diversity around greenhouses is the stimulation of indigenous natural enemies that migrate to greenhouses, where they suppress both indigenous and exotic pests. How this influx can be supported by specific plant communities, plant characteristics, and habitats while minimising risks of increasing greenhouse pest densities, virus transmission, or hyperparasitism needs further studies. It also requires a better understanding of the underlying processes that link biodiversity with pest management. Inside greenhouses, plant biodiversity can also support biological control. We summarise general methods that growers can use to enhance pest control with functional biodiversity and suggest that it is particularly important to study how biodiversity inside and outside greenhouses can be linked to enhancement of biological pest control with both released and naturally occurring species of natural enemies.

The omnivorous predator Macrolophus pygmaeus, a good candidate for the control of both greenhouse whitefly and poinsettia thrips on gerbera plants.

The poinsettia thrips Echinothrips americanus Morgan is a relatively new pest that has spread rapidly worldwide and causes serious damage in both vegetable and ornamental plants. In this study, we investigated if and how effective this pest can be controlled in gerbera by the omnivorous predator Macrolophus pygmaeus (Rambur). Because herbivores on plants can interact through a shared predator, we also investigated how poinsettia thrips control is affected by the presence of the greenhouse whitefly Trialeurodes vaporariorum (Westwood), a pest that commonly coexists with E. americanus in gerbera. In laboratory studies, we found that the predator M. pygmaeus fed on both pests when offered together. Olfactometer tests showed a clear preference of the predators for plants infested by whiteflies but not by thrips. In a greenhouse experiment, densities of both pests on single gerbera plants were reduced to very low levels by the predator, either with both pests present together or alone. Hence, predator-mediated effects between whiteflies and thrips played only a minor role. The plant feeding of the shared predator probably reduced the dependence of predator survival and reproduction on the densities of the two pests, thereby weakening potential predator-mediated effects. Thus, M. pygmaeus is a good candidate for biological control of both pests in gerbera. However, further research is needed to investigate pest control at larger scales, when the pests can occur on different plants.

Induced plant defences in biological control of arthropod pests: a double-edged sword.

Biological control is an important ecosystem service delivered by natural enemies. Together with breeding for plant defence, it constitutes one of the most promising alternatives to pesticides for controlling herbivores in sustainable crop production. Especially induced plant defences may be promising targets in plant breeding for resistance against arthropod pests. Because they are activated upon herbivore damage, costs are only incurred when defence is needed. Moreover, they can be more specific than constitutive defences. Nevertheless, inducible defence traits that are harming plant pest organisms may interfere with biological control agents, such as predators and parasitoids. Despite the vast fundamental knowledge on plant defence mechanisms and their effects on natural enemies, our understanding of the feasibility of combining biological control with induced plant defence in practice is relatively poor. In this review, we focus on arthropod pest control and present the most important features of biological control with natural enemies and of induced plant defence. Furthermore, we show potential synergies and conflicts among them and, finally, identify gaps and list opportunities for their combined use in crop protection. We suggest that breeders should focus on inducible resistance traits that are compatible with the natural enemies of arthropod pests, specifically traits that help communities of natural enemies to build up. © 2017 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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.

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 other's 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.

Nonlinearities lead to qualitative differences in population dynamics of predator-prey systems.

Since typically there are many predators feeding on most herbivores in natural communities, understanding multiple predator effects is critical for both community and applied ecology. Experiments of multiple predator effects on prey populations are extremely demanding, as the number of treatments and the amount of labour associated with these experiments increases exponentially with the number of species in question. Therefore, researchers tend to vary only presence/absence of the species and use only one (supposedly realistic) combination of their numbers in experiments. However, nonlinearities in density dependence, functional responses, interactions between natural enemies etc. are typical for such systems, and nonlinear models of population dynamics generally predict qualitatively different results, if initial absolute densities of the species studied differ, even if their relative densities are maintained. Therefore, testing combinations of natural enemies without varying their densities may not be sufficient. Here we test this prediction experimentally. We show that the population dynamics of a system consisting of 2 natural enemies (aphid predator Adalia bipunctata (L.), and aphid parasitoid, Aphidius colemani Viereck) and their shared prey (peach aphid, Myzus persicae Sulzer) are strongly affected by the absolute initial densities of the species in question. Even if their relative densities are kept constant, the natural enemy species or combination thereof that most effectively suppresses the prey may depend on the absolute initial densities used in the experiment. Future empirical studies of multiple predator - one prey interactions should therefore use a two-dimensional array of initial densities of the studied species. Varying only combinations of natural enemies without varying their densities is not sufficient and can lead to misleading results.

Identification and characterization of a DNA photolyase-containing baculovirus from Chrysodeixis chalcites.

A hitherto unknown single nucleocapsid nucleopolyhedrovirus (SNPV) with a unique property was isolated from larvae of the looper Chrysodeixis chalcites (Lepidoptera, Noctuidae, Plusiinae). Polyhedrin, lef-8, and pif-2 gene sequences were obtained by PCR with degenerate primers and used for phylogenetic analysis. ChchNPV belonged to class II NPVs and its polyhedrin sequence was most similar to that of class II NPVs of other members of the subfamily Plusiinae. Further genetic characterization involved the random cloning of HindIII fragments into a plasmid vector and analysis by end-in sequencing. A gene so far unique to baculoviruses was identified, which encodes a putative DNA repair enzyme: cyclobutane pyrimidine dimer (CPD) DNA photolyase (dpl). The transcriptional activity of this gene was demonstrated in both ChchNPV-infected C. chalcites larvae and infected Trichoplusia ni High Five cells by RT-PCR and 5' and 3' RACE analysis. The possible role of this gene in the biology of the virus is discussed.