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Sub-Section (Under Human Uses Section): Biological control

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Morphological Plant Characteristics and Natural Enemy Success

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Beyond domatia and nutritional rewards there are numerous other plant characteristics that are involved in the successful colonization of natural enemies on plants. These can include the physical size, shape, density, maturity, colour, and texture of a given plant species. Specific plant features such as the hairiness or glossiness of vegetation can have mixed effects on different natural enemies. For example, trichomes decrease hunting efficiency in many natural enemies, as trichomes tend to slow or prevent movement due to the physical obstacles they present or due to the adhesive secretions they produce. However, this is not the case for all natural enemies. For example, E. formosa, a whitefly parasitiod is slowed by plant hairs, which allows the parsitoid to detect and parasitize a higher number of juvenile whiteflies. (Article reference #4)

Trials involving Coccinelids have illustrated that many of these beetles have a distinct preference on the type of leaf surface they frequent. Presented with the opportunity to land on glossy or normal Brassica oleracea foliage, the beetles preferred inhabiting the glossy foliage as they were better able to grasp to these leaves. With this knowledge, many studies have been and are being conducted which evaluate the variation in effect on natural enemies when different plant genotypes are introduced. (Article reference 4)

Volatile Organic Compounds and Biological Control

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Two potential aspects that benefit plants when they release volatile organic compounds (VOCs) are the deterring of herbivores and the attraction of natural enemies; the latter has been a source of much research, investigating the relationship between natural enemies and VOCs resulting in the biological control of pests.[1] There is the potential for synthesizing products which replicate the unique VOC composition released by different plants; these products could be applied on plants suffering from pests that are targeted by the attracted natural enemy.[1] This could cause natural enemies to enter crops that are occupied by pest populations that would otherwise likely remain undetected by the natural enemies.[2] The four elements that must be considered before manipulating VOCs are as follows. The VOCs must effectively aid the natural enemy in finding the prey; the pest must have natural enemies present; the fitness cost of potentially attracting additional herbivores must be exceeded by attracting enough natural enemies, and the natural enemies must not be negatively effected by direct plant defenses that may be present.[3]

Extrafloral Nectaries and Biological Control

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In a recent study comparing wild, cultivated and nectarless cotton varieties in both the field and greenhouse. The findings demonstrated that the level of domestication of cotton plants correlates to the level of indirect defense investment, observed in the form of EFNs. It showed that wild varieties produced higher volumes of nectar and attracted a wider variety of natural enemies. This research points towards the idea that the process of breeding new cotton varieties, has overlooked natural resistance traits in the pursuit of high yielding varieties that can be protected by pesticides. While this study did not find clear relationships between pest suppression and level of cotton domestication, it did highlight several studies which have shown this relationship. The studies illustrated a significant correlation between plants bearing EFNs and lower pest levels along with greater levels of natural enemies; one study also showed that the feeding of herbivores can directly induce nectar production.These collective findings illustrate the potential benefits that could be gained through incorporating the desirable genetics of wild varieties into cultivated varieties.[4]

Domatia and Biological Control

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Certain tropical plants have been observed hosting colonies of ants in their hollow domatia and providing the ants with nutrition delivered from nectaries or food bodies. These ant colonies have become dependent on the host plants for their survival and therefore, actively protect the plant; this protection can take the form of killing or warding off pests, weeds, and certain fungal pathogens. Knowledge of this mutualistic relationship has been held for many years by Chinese citrus farmers who have been known to incorporate artificial ant nests into their crop to provide suppression of pests.[5]

Tritrophic Interactions Involving Parasitoids

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A Brazilian parasitoid wasp raising it's ovipositor.

Parasitoids have been incorporated into biological pest control programs for many years successfully. It has been demonstrated that plants can directly influence the effect of parasitoids on herbivores by releasing chemical cues which alter host-seeking behavior and by providing food sources or domatia( Article reference #1). Certain parasitoids may be dependent on this plant relationship. Therefore, in production areas where parasitoid presence is desired, ensuring the crops being grown meet all of these requirements will likely correlate to higher parasitoid populations and potentially increased pest control.[2]

Parasitized aphids with visible parasitoid wasp exit holes.

This has been illustrated through monitoring aphid populations in an experimental sugar beet crop. When only beets were grown, the parasitism level of the aphid population was insignificant. However, when collard crops were grown simultaneously and adjacent to the sugar beets, aphid parasitism levels increased. Collard crops released much higher concentrations of VOC’s compared to the sugar beets. As a result, it was found that the companion collard plants provided stronger chemical cues than the sugar beets, attracting more aphid parasitoids which killed aphids in the collard plants and migrated to the sugar beets that were then in close proximity.[6]

Rice plants have been observed to release ethylene and other compounds in response to brown plant hopper feeding and it has been observed that this can attract a facultative parasitoid that parasitizes brown plant hopper eggs.[1]

In one study it was shown that the presence of plant extraforal nectaries in cotton, caused parasitoids to spend more time in the crop and caused the parasitization of more moth larva compared to a cotton crop with no nectaries. With the publishing of this discovery, farmers have transitioned to no longer growing cotton varieties that are without nectaries.[7] In a separate trial involving cotton, it was revealed that naturalized cotton emitted seven times the VOC’s compared to cultivated cotton varieties when experiencing feeding damage.[8] This could be the case for other highly cultivated crops plants but must be measured as there are cases of other crops that do not show the same trend.[2]

These findings reveal the specific aspects a farmer can manipulate to influence parasitoid populations and illustrate the potential impact parasitoid habitat management can have on pest control.[2] In the case of cotton and other similar high VOC crop scenarios, there is interest in genetically engineering the chemical pathways of cultivated varieties to selectively produce high VOC’s as observed in the naturalized varieties, in order to attract greater natural enemy populations. This presents numerous challenges but could produce promising pest control opportunities. [9]

Tritrophic Interactions Involving Insect Pathogens and Plant Defense

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Insect pathogens, also called entomopathogens, are another group of organisms that are influenced by plants. The extent of the influence largely depends on the evolutionary history shared between the two, as well as the pathogen's method of infection and survival duration outside of a host. There have been several studies published which have shown that different insect host plants, with various entomopathogens present, cause different levels of insect mortality (when the entomopathogens are injested in combination with the differing leaf material). In some cases significant increases in mortality are recorded, up to 50-fold in some studies. However, there is also research which reveals that certain plants influence entomopathogens in negative ways, reducing their efficacy.[10]

The leaf surface of a plant is the main platform for which these influences occur directly; plants can release various exudates, phytochemicals, and alleolochemicals through their leaves, some of which have the ability to inactivate certain entomopathogens.[10] Whereas, in other plant species, leaf characteristics can increase the efficacy of entomopathogens. For example, the mortality of pea aphids was higher in the group of aphids that were found on plants with less wax exudates, compared to plants with more wax exudates. It was explained that reduced waxiness increased the transmission of Pandora neoaphidus conidia from the plant to the aphids.[11]

Feeding-induced volatiles that are emitted by different plants, have been shown to increase the amount of spores released by certain entomopathogenic fungi, increasing the likelihood of infection of some herbivores but not others. Plants can also influence pathogen efficacy indirectly and this typically occurs either by increasing the susceptibility of the herbivore hosts or by changing their behavior. This influence can often take the form of altered growth rates, herbivore physiology or feeding habits. This research illustrates the differential impact that various host plant species can have on entomopathogenic interactions.[10]

In one study it was proved that Brassicas can defend themselves by acting as a vector for entomopathogens. It was shown that virus infected aphids feeding on the plants, introduced a virus into the phloem. The virus was passively transported in the phloem, throughout the plant. This caused aphids, feeding in separate locations from the infected aphids, to become infected as well. This finding presents the possibility of injecting crops with compatible entomopathogenic viruses to defend against susceptible insect pests.[12]

Tritrophic Interactions Below-Ground and Plant Defense

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Less studied than above ground interactions, but proving to be increasingly important, are the below ground interactions that influence plant defense.[13] There is a complex network of signal-transduction pathways involved in plant responses when receiving various stimuli and it has been shown that soil microbes have a significant influence on a number of these responses. Certain soil microbes can aid plant growth, producing increased tolerance to various environmental stressors and can protect their host plants from many different pathogens, by inducing systemic resistance.[14] It is understood that organisms in above and below ground environments can interact indirectly through plants. There have been many studies that show both the positive and negative effects that one organism in one environment can have on other organisms in the same or opposite environment, with the plant acting as the intermediary between the two.[13]

Mycorhizal association with a plant root

A meta analysis documenting the effect of mycorhizae demonstrated this. The colonization of plant roots with mycorhizae typically results in a mutualistic relationship between the plant and the fungus, inducing a number of changes in the plant. The analysis reviewed the mixed impact that colonization can have on herbivores; it highlighted that insects with different feeding methods were affected very differently, some positively and others negatively. The type of mycorhizae species involved also had a notable impact on the performance of the insects. One common species, Glomus intradices had a negative effect on the feeding success of chewing herbivores, whereas other species studied had positive effects.[15]

One study showed that the roots of some maize plants produce a defense chemical when roots are damaged by leaf beetle larvae; this chemical was very attractive to the entomopathogenic nematode species Heterorhabditis megidis. It was found that only certain maize varieties produce this chemical; in the field, plants which released the chemical caused up to a five fold increase in leaf beetle larvae parasitization over those that didn't produce the chemical. Incorporating these varieties or their genes into commercial maize production could significantly increase the efficacy of nematode treatments.[16]

In a further study, expanding on this experiment, additional nematodes, herbivores and plant species were compared to record resulting interactions. The underlying findings suggested that the plant emitted chemicals acted as the primary source of attractant to the nematodes. It was suggested that the herbivores have evolved to be relatively undetectable to the nematodes, whereas the plants have evolved to release highly attractive chemical signals. It is clear that a high degree of specificity is involved; species that make up these tritrophic interactions have evolved closely with one another over a long period of time and as a result have very unique relationships.[17]

Considerations in Utilizing Tritrophic Interactions in Biological Control

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Sustainable crop production is becoming increasingly important, especially if humans hope to continue to support a growing population and avoid a collapse of the production system.[18] While the understanding and incorporation of tritrophic interactions in pest control offers a promising control option, it is important to note that the sustainable biological control of pests requires a dynamic approach that involves diversity in all of the species present, richness in natural enemies and limited adverse activity (ie. minimal pesticide use). This approach is especially important in conservation biological control efforts.[19] It is also important to note that there are typically more than three trophic levels at play in a given production setting, so it has been suggested that the tritrophic interaction research model is somewhat simplistic and should in some cases, incorporate the influence that higher trophic levels can have on biological control.[2] Furthermore, ecological complexity and interactions between species of the same trophic level are aspects that still require much research. Up to this point, the research has had a relatively narrow focus, which may be suitable for controlled environments such as greenhouses, but is lacking in it's documentation of multi-generational plant interactions with dynamic communities of organisms.[20]

  1. ^ a b c Nurindah, N., Wonorahardjo, S., Sunarto, D. A., Sujak, S. (2017). "Chemical Cues In Tritrophic Interactions On Biocontrol Of Insect Pest". The Journal of Pure and Applied Chemistry Research. 6(1): 49–56.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  2. ^ a b c d e Poppy, G. M. (1997). "Tritrophic interactions: Improving ecological understanding and biological control?". Endeavour. 21(2): 61–65 – via Elsevier Science Direct.
  3. ^ Kessler, A., Baldwin, I. T. (2002). "Plant-Mediated Tritrophic Interactions and Biological Pest Control" (PDF). AgBioTechNet. 4 – via Research Gate.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  4. ^ Llandres, A. L., Verdeny-Vilalta, O., Jean, J., Goebel, F., Seydi, O., Brevault, T. (2019). "Cotton Extrafloral Nectaries as Indirect Defence Against Insect Pests". Basic and Applied Ecology. 37: 24–34 – via Elsevier Science Direct.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  5. ^ Heil, M. (2008). "Indirect Defence via Tritrophic Interactions". The New Phytologist. 178(1): 41–61 – via JSTOR.
  6. ^ Read, D. P., Feeny, P. P., Root, R. B. (1970). "Habitat Selection By The Aphid Parasite Diaeretiella Rapae (Hymenoptera: Braconidae) And Hyperparasite Charips Brassicae (Hymenoptera: Cynipidae)". The Canadian Entomologist. 102: 1567–1578 – via Cambridge Core.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  7. ^ Stapel, J. O., Cortesero, A. M., DeMoraes, C. R., Tumlinson, J. H. and Lewis, W. J. (1996). "Extrafloral Nectar, Honeydew, and Sucrose Effects on Searching Behavior and Efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in Cotton". Environmental Entomology. 26(3): 617–623 – via Oxford Academic.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  8. ^ Loughrin, J. H., Manukian, A., Heath, R. R., Tumlinson, J. H. (1995). "Volatiles Emitted by Different Cotton Varieties Damaged by Feeding Beet Armyworm Larvae". Chemical Ecology. 21: 1217–1227 – via Springer Link.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  9. ^ Poppy, Guy M.; Sutherland, Jamie P. "Can biological control benefit from genetically‐modified crops? Tritrophic interactions on insect‐resistant transgenic plants". Physiological Entomology. 29(3): 257–268 – via Wiley Online Library.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  10. ^ a b c Cory, J. S., Hoover, K. (2006). "Plant-Mediated Effects in Insect-Pathogen Interactions". Trends in Ecology & Evolution. 21: 278–286 – via Elsevier Science Direct.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  11. ^ Duetting, P. S., Eigenbrode, S. D. (2003). "Plant Waxy Bloom on Peas Affects Infection of Pea Aphids by Pandora neoaphidus". Invertebrate Pathology. 84: 149–158 – via Elsevier Science Direct.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  12. ^ Van Munster, M., Janssen, A., Clerivet, A., Van Den Heuvel, J. (2005). "Can Plants Use an Entomopathogenic Virus as a Defense Against Herbivores?". Plant Animal Interactions. 143: 396–401 – via Springer Link.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  13. ^ a b Van Geem, M., Gols, R., Van Dam, N. M., Van Der Putten, W. H., Fortuna, T., Harvey, J. A. (2013). "The Importance of Aboveground–Belowground Interactions on the Evolution and Maintenance of Variation in Plant Defense Traits". Plant Microbe Interactions. 28 – via Frontiers in Plant Science.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  14. ^ Pineda, A., Dicke, M., Pieterse, C. M. J., Pozo, M. J. (2013). "Beneficial microbes in a changing environment: are they always helping plants to deal with insects?". Functional Ecology. 27(3): 574–586 – via British Ecological Society.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  15. ^ Koricheva, J., Gange, A. C., Jones, T. (2009). "Effects of Mycorrhizal Fungi on Insect Herbivores: A Meta-Analysis". Ecology. 90(8): 2088–2097 – via NCBI PubMed.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  16. ^ Rasmann, S., Kollner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., Turlings, T. C. J. (2005). "Recruitment of Entomopathogenic Nematodes by Insect-Damaged Maize Roots". Nature. 434: 732–737.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  17. ^ Rasmann, S., Turlings, T. C. J. (2008). "First Insights Into Specificity of Belowground Tritrophic Interactions". OIKOS. 117(3): 362–369 – via Wiley Online Library.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  18. ^ Berg, G. (2009). "Plant–Microbe Interactions Promoting Plant Growth and Health: Perspectives for Controlled Use of Microorganisms in Agriculture". Applied Microbiology and Biotechnology. 84: 11–18 – via Springer Link.
  19. ^ Gardarin, A., Plantegenest, M., Bischoff. A., Valantin-Morison, M. (2018). "Understanding plant–arthropod interactions in multitrophic communities to improve conservation biological control: useful traits and metrics". Journal of Pest Science. 91: 943–955 – via Springer Link.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  20. ^ Van Veen, F. (2015). "Plant-modified Trophic Interactions". Current Opinion in Insect Science. 8: 29–33 – via Elsevier Science Direct.