The doctoral dissertation in the field of Environmental and Biological Science will be examined online at the Faculty of Science, Forestry and Technology, Kuopio campus.
What is the topic of your doctoral research? Why is it important to study the topic?
Plants use a wealth of chemical compounds to defend against herbivores but also to adapt to variable environmental conditions. Both natural and agroecosystems are filled with volatile organic chemical signal compounds and non-volatile direct feeding deterrents that affect plant-herbivore dynamics. Brassica crops are globally important for food production, but they also have a remarkably diverse specialist herbivore fauna, and many species can easily reach the status of pests.
This thesis assessed the direct and indirect defence of broccoli (Brassica oleracea var. italica) against herbivores and the potential role of companion plants (CPs) e.g., aromatic shrub Rhododendron tomentosum [RT] and nectar-providing flowering buckwheat (Fagopyrum esculentum [FE]) plants that produced herbivore-repellent and parasitoid-attractive volatile organic compounds (VOCs) to provide ecosystem services based on their chemical and morphological traits.
The thesis is based on laboratory experiments and fieldwork. In the laboratory, the herbivores (diamondback moth, Plutella xylostella [DBM] (Lepidoptera: Yponomeutidae) and the large cabbage white butterfly, Pieris brassicae Linn. (Lepidoptera: Pieridae)) and their parasitoids (Cotesia vestalis and C. glomerata, respectively) were studied. The behaviour of the parasitoid Cotesia spp. was assessed on the insect herbivores and their interactions between the broccoli and RT companion plants.
The laboratory experiments showed that the effects of RT VOCs depended on temperature. RTVOC exposed-broccoli plants were more resistant to oviposition and less preferred by larvae of both herbivorous moth species than controls. The thesis provided insight into early responses in parasitoid behaviour involved in the perception of RTVOCs. The damaged broccoli plants were more susceptible than intact plants to orientation by both Cotesia spp. parasitoids. The P. brassicae parasitoid preferred host-damaged plants over RT-exposed host-damaged plants, while preceding RT exposure did not disturb the orientation of the DBM parasitoid.
The field experiment was established to test the effect of repellent RT boundary plants and natural enemy-attracting buckwheat boundary plant effects on the density of major broccoli pests. In the field, DBM was the major outbreak pest (with an early migration to Finland), and as a result, the monitoring of this insect and its plant damage was the focus of this work. The control plants had higher larval densities and suffered more severe damage than plants in other treatments. In RT plant plots (boundary plantings RT around broccoli plots), DBM adult densities were reduced significantly as compared with both control and early-season mechanical control (MC) plots by using floating row covers in organic farming. Also, DBM larval densities and damage intensities were highest in the latter half of July, when the second generation larvae were feeding. The effects of buckwheat plants on broccoli were variable, but DBM larval densities were reduced when compared to the controls.
This thesis highlights the importance of plant-plant interactions mediated by RTVOCs. R. tomentosum is an excellent model companion plant because it releases RTVOCs in the air that may protect broccoli plants by disturbing DBM female oviposition inside and outside RT-plant plots. In the laboratory, RTVOC adsorption disturbed insect herbivores in both oviposition and feeding choices but did not disturb parasitoid orientation. There was the presence of RT-specific VOCs, e.g., palustrol and ledol, on RT-exposed broccoli in laboratory experiments. In the field, however, there was no evidence of adsorption and rerelease of RTVOCs from broccoli plants grown in RT plots with RT as boundary plants. The RTVOCs resulted in a decrease in the susceptibility of broccoli plants to DBM's oviposition, reducing both larval densities and damage intensities. The result of a direct repellent effect of the RT boundary plants on the arriving DBM adults if typical RTVOCs were not detected on broccoli plants. Thus, RTVOCs can be considered potential natural alternatives to chemical insecticides. This thesis provides evidence that RT plants are great potential VOC sources for use in integrated pest management (IPM) strategies to control DBM as a tool in Brassica crop protection.
What are the key findings or observations of your doctoral research?
The thesis represents a novel significant scholarly merit to the field of Applied Chemical Ecology. The research was aimed at investigating the potential for volatile organic compounds (VOCs) released by Rhododendron tomentosum to be incorporated into strategies for the biological control of Plutella xylostella, the diamondback moth, which is a major agricultural pest. Plant-plant interactions mediated by VOCs play important roles in ecology and have potential to be used as tools in integrated pest management. In the early season, row covers can assist in control of P. xylostella in organic farming.
How can the results of your doctoral research be utilised in practice?
This thesis provides evidence that RT plants are potential VOC sources for use in IPM strategies to control DBM and reduce plant damage in agriculture. In the laboratory, RT-exposed Brassicaceae plants added protection against specialist herbivores' attack on larval developmental and egg deposition stages and reduced herbivore pressure in different stages of attack by DBM and P. brassicae. RTVOCs are one of positive influencing factors for incorporating into biocontrol and push-pull strategies to repel DBM and P. brassicae, and RT-exposed plants did not disturb parasitoid C. vestalis or C. glomerata wasps’ orientation towards DBM- or P. brassicae-damaged plants.
In the field, there was the presence of semi-volatile palustrol and ledol in the emission of RT boundary plants, but no evidence of adsorption and rerelease of RT volatiles from Brassica plants grown in these plots was found. However, R. tomentosum as boundary plant directly repelled P. xylostella and reduced damage on Brassica. Plant-plant interactions mediated by VOCs play important roles in plant ecology, so they have great potential to be used as a tool for the protection of crops. The potential applications of the thesis could be the extraction of key RT SVOCs and the release of these compounds from a dispenser to control Brassica pests in the field. R. tomentosum was earlier discovered to render associational resistance in nature. The ability of this plant species to influence larval feeding and adult oviposition of Brassica herbivores can be encouraged by further field studies of its potential for biocontrol.
To better explain the herbivore repellence effects in RT plots, further VOC emission measurements from the atmosphere above the RT plants, particularly during summer nights, are needed. The specialisation level, the olfactory use, and the visual and chemoreceptor cues of targeted herbivores should be investigated to distinguish the important role of other neighbouring and VOC-based potentiated defences.
The regulatory role of temperature on VOC-related associational resistance should be studied more extensively in natural and agricultural plant systems with varying VOC compositions and on alternative IPM strategies for DBM pest control of Brassica crops. The protective effects of row cover against DBM damage suggest that crop covers will be a potential early-season DBM control method for organic farming.
What are the key research methods and materials used in your doctoral research?
Insects are one of the most important class to damage crops, with estimated annual global average yield losses of 23 to 40% of food production due to insect pests (Abhilash and Singh 2009, Savary et al. 2019). Many farmers have used excessive doses and banned CIs, affecting human health, environment, water resources, natural enemies, etc. Effective biocontrol methods can be used to simultaneously provide crop security and environmental sustainability in the future. These prospects and promises of biocontrol methods aim to reduce herbivores (Stenberg et al. 2021) and replace chemical pesticides via non-synthetic insecticide means, e.g., natural enemies, and companion plants using plant VOCs (Ninkovic et al. 2021) to manage insects.
Plant VOCs play key roles in herbivore’s orientation towards their host plants as well as in the prey’s location (Marques Arce et al. 2021) by natural enemies, so better knowledge of the VOCs function in defence is needed. Intercropping combined with non-host companion plants (CPs) (Ninkovic et al. 2021, Stenberg et al. 2015), which with efficient defence mechanisms or favouring natural enemies via increased diversity in agroecosystems might provide such solutions, can become one of the effective management methods that can overcome the defects of CIs (Kayukawa et al. 2020). On the field, a flowering CP buckwheat, F. esculentum Möench (Polygonales: Polygonaceae), would attract natural enemies (Sarkar et al. 2018), whereas some other CPs would repel insects. For examples, aromatic R. tomentosum Harmaja (syn. Ledum palustre L.), a perennial dwarf shrub known as wild rosemary or northern Labrador tea, is a plant species having repellent properties against various insect species (Jesionek et al. 2021).
It was found that for few decades, plant diversity and CPs in intercropping played important roles and could favour predators and parasitoids against pest insects (Han et al. 2022). Additional CP VOCs, when sprayed as extracts on herbivore host plants, e.g., on vegetable crops, may repel herbivore insects (Ibrahim et al. 2005) and attract their natural enemies (Egigu et al. 2011). Some plant species could hide from their herbivores by olfactory camouflage when they accumulate herbivore-repellent semivolatile organic compounds (SVOCs) on their surfaces (Mofikoya et al. 2019. Himanen et al. (2010) showed that SVOCs emitted by R. tomentosum plants may condense on CPs in an experimental field and a peatland site in temperature-dependent manners. They also noted that high emission rates of specific RTVOC from companion plant surfaces could be seen in the morning after a colder night, but they disappeared in the afternoon with warming temperatures. In a forest site, an accumulation of volatiles released by understory RT vegetation was found on mountain birch foliage (Mofikoya et al. 2018a). In this thesis, the adherence of RTVOCs to a crop plant was selected as the main defence mechanism to be studied. Another potential application of CP plants is flowering plants that attract natural enemies during their flowering season (Fountain 2022, Kati et al. 2021). Buckwheat is a valuable pollen and nectar source to increase natural enemies (Fountain 2022) and reduce crop pests on broccoli (Berndt et al. 2002). The combination of buckwheat as a rewarding plant and methyl salicylate (MeSA-C8H8O3) as an attractant boosted Scelonidae egg-parasitoid wasp abundance on broccoli plants (Ayelo et al. 2021). In previous studies with grape vines (Scarratt et al. 2008) and on apples, Stephens et al. (1998) recorded that using buckwheat as a companion plant resulted in higher parasitism percentages of leaf rolling tortricids (34% compared with 20% in unsown plots).
Global warming supports the dispersion of invasive pest insects and increases their outbreaks at higher latitudes and in mountainous areas (Skendžić et al. 2021, Pureswaran et al. 2018). In air-polluted environments, ozone-mediated degradation of many herbivore-induced plant volatiles (HIPVs) (Pinto et al. 2007) may weaken the parasitoid response to the emission of herbivore-damaged plants (Himanen et al. 2009). Insects often respond rapidly to environmental changes. A typical example of such a herbivorous species is the northward-migrating DBM, which has had more frequent outbreaks in recent years in a boreal climatic zone (Dancau et al. 2018). Temperature can directly affect the behaviour and performance of insect pests and indirectly impact the performance of natural enemies if the emissions of important signalling compounds released by the damaged host plant of herbivores are disturbed (Himanen et al. 2009, Holopainen and Gershenzon 2010). For example, sesquiterpenes (C15-terpenoids built from three isoprene units) and methyl salicylate are among the important induced VOCs that are emitted by a plant damaged by herbivores (Tamiru et al. 2017, Holopainen 2011). HIPVs can either repel or attract insects (Gebreziher 2020, Turlings and Erb 2018) and play a role in communication among plants by alerting neighbouring plants about herbivory (Gebreziher 2020). Brassica ssp. plants are globally important crop species that provide oil and food for humans and animals (Kumar 2017). Those plants are attacked by a wealth of Brassica specialist herbivores (Mertens et al. 2021). Agricultural insect-control method improvements are key to more sustainable Brassica vegetable production globally. The need for more efficient food production is increasing because of fast-growing populations and frequently emerging or re-emerging pests in the developing world (Fróna et al. 2019).
This thesis investigated the direct and indirect defence of broccoli plants against herbivores, the role of plant-plant interactions mediated by VOCs, and particularly RTVOCs emitted by a companion plant and adsorbed on the surface of a crop plant as applied to the biocontrol of DBM and P. brassicae, which are economically important global insect pests. Studies of the herbivore repelling capacity of RTVOCs as one main defence mechanism were carried out in two laboratory studies and one field study. However, more research efforts regarding the field experiments focused on the development of push-pull strategies were conducted to translate the promising VOC results from the laboratory to real field conditions to deal with economic insect herbivores. In the field experiment of this thesis (Study II), the volatiles of CPs, e.g., aromatic R. tomentosum as the study model could be repellent to herbivores, whereas pollen and nectar providing flowering, buckwheat could attract natural enemies of the specialist herbivores of crop plants, e.g., DBM and P. brassicae.
The doctoral dissertation of Thuy Nga Bui Thi, MSc, entitled Potential to use sticky semivolatiles emitted by companion plants in biocontrol of Brassica insect pests be examined at the Faculty of Science, Forestry and Technology, Kuopio Campus. The opponent will be Associate Professor Velemir Ninkovic, Swedish University of Agricultural Sciences, Sweden, and the custos will be Professor James D. Blande, University of Eastern Finland. Language of the public defence is English.
For more information, please contact:
MSc, Thuy Nga Bui Thi, ngabui@uef.fi, p. +358 449 866 777
