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Citations Publications citing this paper. References Publications referenced by this paper. Spiroplasmas: evolutionary relationships and biodiversity. Laura B.

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Regassa , Gail E. Localization and morphological variation of three bacteriome-inhabiting symbionts within a planthopper of the genus Oliarus Hemiptera: Cixiidae. Alberto Bressan , Kathryn L Mulligan. Interestingly, these new techniques also offer new opportunities to temporarily adapt the greenhouse climate for other purposes, such as optimizing pest control with microbials. For example, increasing greenhouse humidity levels significantly increased pest control with B.

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Such decisions obviously need to be considered carefully, as some climatic benefits for microbials may have detrimental effects on crop growth, arthropod natural enemies or may favour some plant diseases. Also, it needs to be mentioned that the relative humidity in the microclimate can be significantly different to the ambient conditions. For example, high humidity levels at the leaf surface may be sufficient for infection by entomopathogenic fungi, even when the ambient relative humidity levels are lower.

Experiments showed that an extra benefit of this regime could be a reduced influx of thrips from outside into the greenhouse, because vents are opened less frequently than when traditional climate management is used Jakobsen et al.

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The lower temperatures at night and in the early hours of the morning may also increase efficacy of Entomophthorales Milner et al. Potential negative effects on arthropod natural enemies also require further evaluation. For example, lower night temperatures might be detrimental for arthropod natural enemies that are night active, such as the aphid predatory midge Aphidoletes aphidimyza Rondani, which requires a minimum temperature to be flight-active Markkula et al.

Overall it is a huge advantage to have the opportunity to adapt the greenhouse climate in order to optimize microbial efficacy, particularly when the potential damage by the target pest is larger than the potential crop losses that may occur due to less favourable climatic conditions, plant diseases or reduced efficacy of some arthropod natural enemies. Not only temperature and humidity, but also artificial light in greenhouses might influence pest control Johansen et al.

Hence, there are several methods now available to adapt the greenhouse environment and these warrant further study. For example, which combinations of artificial light and greenhouse climatic conditions are optimal for pest control with microbials and arthropod natural enemies? It is not only the direct environmental effects on microbials, but also the indirect effects through changes in pest behaviour that could affect these results Johansen et al.

A relatively new field of research in pest control with microorganisms aims to make use of fungal species that act as endophytes. The term endophyte refers to fungi and bacteria that develop within plant tissues without causing any conspicuous symptoms of disease in the plant Wilson Besides the class II fungal endophytes sensu Rodriguez et al. So far several studies provided evidence that entomopathogenic fungi are able to confer at least partial resistance to their host plants when colonizing plant tissues. Other examples include control of the diamondback moth, Plutella xylostella Linnaeus , on cabbage inoculated with an endophytic strain of A.

The underlying mechanisms mediating the effects on herbivorous insects remain, however, to be investigated in detail. The effects were hypothesized to be due to metabolic products produced by the endophytic fungi or by plant metabolites induced by their presence. Compounds produced by Class II fungal endophytes are mainly extracellular enzymes like proteases, lipases and cellulases, and metabolites like beauvericin, oosporein, fumonisin, harzianolide, butenolide and fusaric acid Gurulingappa et al.

However, some natural enemies also feed on the plants harbouring endophytic fungi and could attack herbivorous insects that may be experiencing negative effects due to fungal endophytes. This appeared to be the case for the omnivorous predatory bug M. Surprisingly, this endophyte still enhanced pest control by deterring the predator from feeding on the plant, thereby increasing its feeding activity on the prey. The parasitoid Bracon hebetor Say, when parasitizing larvae of Spodoptera litura Fabricius feeding on cauliflower inoculated by Aspergillus spp.

Thus, the use of Class II endophytic fungi for control of herbivorous pests in greenhouses needs to be tested on a case by case basis for each plant-herbivore-natural enemy-interaction. One of the most striking recent discoveries with regard to endophytic fungi is that several, if not all, isolates of entomopathogenic fungi can also act as endophytes. Most research on entomopathogenic fungi has focused on their virulence and the mechanisms they use to infect the host directly through the cuticle Vega et al. However, endophytic isolates of B. Bacterial endophytes have been studied mainly for their potential as plant growth promoters and for their ability to induce systemic resistance to plant pathogens Kavino et al.

Direct control of pests has not been reported for bacterial endophytes. Indirect effects caused by the induction of systemic resistance and by changes to the chemical profile of plants have been suggested as having the potential to influence the performance of some pests Kloepper and Ryu ; Valenzuela-Soto et al. The fact that bacterial and fungal endophytes might prime plants for resistance to both pests and diseases makes them formidable as biological control agents.

For example, endophytic isolates of F. The use of endophytes that decrease performance by extending pest developmental time might also provide an opportunity to increase the impact of arthropod natural enemies in greenhouses. Irrespective of the mechanism, the longer it takes the pest to develop and complete its life cycles, the more exposed it is to parasitoids and predators.

Finally, the use of endophytes introduced at an early stage of plant development such as seeds coated with endophytes circumvents the intrinsic problems of microbial use such as exposure to detrimental environmental factors, competition with other microorganisms and the challenge of synchronizing microbials with herbivore presence.

However, entomopathogenic fungi are obviously not able to fully colonize all tissues of fast growing plants Behie et al.

Climate regimes in greenhouses may be beneficial for most fungi because they provide specific environmental conditions constant higher temperatures and humidity , and most probably are also favourable for endophytic establishment in plants. However, isolates specifically adapted to these conditions also need to be selected to increase colonization rates of plant tissues. Thus, a screening process to find the optimal combination of the different agents is mandatory for the implementation of this strategy.

The use of endophytic organisms as biological control agents might become even more complicated as a result of the findings of Yan et al. Endophytes are known for their complex metabolic capabilities Gutierrez et al.

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Thus, the method and timing of the inoculation of the crop plant, and the previous history of microbial colonization events, plays an important role in the potential for success with this strategy. Some of these problems may be addressed by the development of specific formulations for endophytes that enhance colonization rates and provide a headstart for these organisms within seedlings. However, these aspects need to be rigorously tested to gain a better understanding of the potential of microorganisms as biological control agents. In recent years, it has been increasingly recognized that microbial symbionts affect the ecology, life history and evolution of their arthropod hosts in many different ways Zchori-Fein and Bourtzis A lot of the key greenhouse pests are exclusively sap feeders, and like other insects with limited diets, harbour a wide range of microbial associates Zchori-Fein and Bourtzis Werren et al.

Furthermore, sap-feeders are usually associated with extracellular gut microbes, which may have nutritional or metabolic functions Kikuchi et al. Although studies on host-microbial symbionts in insects have focused on bacteria, archaeal and fungal symbioses have also been reported Gibson and Hunter Zindel et al. For example, symbiotic bacteria may induce cytoplasmic incompatibility, resulting in sterile eggs when a symbiont-infected female mates with an uninfected male.

A mixed population of symbiont-infected and noninfected individuals would thus reproduce more slowly than one in which all members carried the symbiont or where all members were symbiont-free. In addition, symbiotic microorganisms can increase or decrease the survivorship of an insect host under extreme environmental conditions or influence the transmission capacity of disease-vectoring arthropods Zindel et al.

The pea aphid, Acyrthosiphon pisum , has four different symbionts belonging to the bacterial genera Regiella, Rickettsia, Rickettsiella and Spiroplasma , which induce defences against the entomopathogenic fungus P. The presence of these distantly related symbionts in aphids reduces both their susceptibility to P. Although information on the symbionts of aphid species that are greenhouse pests is rather scarce, bacteria such as Rickettsia have been reported from the cotton aphid, A. Recently Hendry et al. There is every reason to assume that similar symbiotic interactions may occur in other insects colonizing greenhouse crops, and this needs to be taken into account when microbials are produced and applied for pest control in greenhouses and other crop systems.

Symbionts are, so far, not deliberately added to biological control systems, but this might be a field for future research. For example, aphid biotypes that contain particular symbionts might be used to select for parasitoids that are adapted to these symbionts, in order to enhance their performance in the field. Although greenhouse crop production seems ideal for the use of biological control agents, experience has taught us that there are a range of interactions that must be considered when incorporating organisms into a closed system.

For decades, research focussed on understanding the tritrophic interactions between plants, herbivores and their arthropod natural enemies Kennedy ; Price et al. However, it is now clear that tritrophic interactions are influenced by all the other components of the ecosystem, and as a result, research has shifted into understanding crop-pest management from the perspective of multitrophic interactions Van der Putten et al. As we have shown here, the combined use of microbial biological control with the use of arthropod natural enemies must take into account direct and indirect effects on each side.

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Understanding the complexity of ecological interactions between different types of biological control agents is itself a subject that requires further research. In terms of biological control, studies need to focus on unveiling direct and indirect effects of the application of microbial biological control agents and microbial communities within insects symbionts and plants endophytes on arthropod natural enemies. Although most cases show evidence of compatibility between different types of agents, it is necessary to pinpoint the essential conditions that ensure the success of their combination.

We consider that the following research areas should be prioritized: 1 optimizing the efficacy of the existing and new microbial products and 2 determining how to combine both microbial and arthropod natural enemies with available technologies. Optimization of microbial efficacy is an ongoing goal achieved by new formulation and conservation techniques and by selection of specific and virulent isolates with the most desirable characteristics to be effective and persist under greenhouse conditions.

Combining microbials with the existing and new technologies is already promising since greenhouse climate control and new delivery methods are already available. The use of endophytes and manipulation of symbionts to improve control of pests could also represent elegant solutions to many of the current problems with microbials, but further research is required. Understanding of the ecological consequences of using microbials in combination with other biological control agents needs closer examination, especially for organic greenhouse cropping systems that have evolved into complex ecosystems with persistent populations of multiple arthropod natural enemy species.

To our surprise, there are only a limited number of studies involving microbials and arthropod natural enemies under greenhouse conditions, confirming that this area is fertile ground for research. In our opinion, such studies deserve more attention as they may help to identify complementary and synergistic interactions between microbials and arthropod natural that increase the opportunities to enhance and further develop biological pest control. All authors contributed to the writing of this review. FG and GM edited and finalized the manuscript.

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