When is a herbivore not a herbivore?
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Plants are preyed upon by a diverse group of insect herbivores above- and belowground. Over the course of millions of years, plants have evolved an intricate immune system. When a plant perceives an attacker, responses are rapidly triggered, leading to the activation of defence mechanisms aimed at deterring or resisting the attacker. Activation of plant defence does not only occur locally but throughout the plant; this is in part to prepare for attack in systemic tissues, and in part because plant secondary metabolites may be produced in systemic tissues and transported to the site where they are needed. As such, defence responses triggered by one insect herbivore can affect another insect herbivore feeding on the same plant, even if they are separated in space and time. Such plant-mediated interactions between insects are common in natural settings, as plants are rarely visited by only a single herbivore. The outcome of these interactions between insect herbivores can range from facilitation to antagonism, depending on many factors such as the identity and feeding site of the herbivores involved. Most studies on plant defence and plant-mediated species interactions have focussed on aboveground tissues. As a result, there is a gap in our understanding of regulation of plant defence in the roots, and how these defence responses may be modulated in plant-mediated interactions. The aim of this thesis was to identify and understand the effects of aboveground herbivory, via plant-mediated interactions, on belowground herbivory. My study system consisted of cabbage plants and three of the most important pest species in the field; foliar feeding Brevicoryne brassicae aphids and Plutella xylostella caterpillars, and root feeding Delia radicum maggots. I focussed on the effects induction by the aboveground feeders on defence in the roots and consequences for D. radicum. To understand how plant-mediated interactions may occur, I extensively studied plant defence in the primary roots of cabbage plants against D. radicum alone or in combination with the leaf herbivores. Chapter 2 addresses the plant-mediated effects of P. xylostella and B. brassicae on the performance of D. radicum. To unravel the molecular mechanisms underlying these interactions, I included measurements of phytohormones and gene expression within these phytohormonal pathways. I discuss the plant responses to D. radicum in roots, and how aboveground herbivores may modulate them. This work was a stepping stone for chapter 3, in which I used RNA-sequencing to investigate how the plant root transcriptome changes in response to herbivory above- and/or belowground. The transcriptomic analysis led to novel hypotheses on plant responses to root herbivory and plant-mediated effects. I tested two of these hypotheses in follow-up experiments. First, I used mutant B. oleracea plants to study whether aliphatic glucosinolates confer resistance to D. radicum, and second, I studied whether P. xylostella primes plant roots to respond faster to D. radicum. Female D. radicum flies integrate cues from leaves in their oviposition choice behaviour as described above. As such, plant-mediated effects of aboveground herbivores may have additional effects on D. radicum through their host-searching behavior. Furthermore, while plant-mediated effects of aboveground chewers on root chewers have been targeted in many studies, they usually include only a single species combination. In chapter 4, I studied the plant-mediated effects of six different foliage-chewing herbivores on D. radicum preference and performance and induction of plant defence. The species of foliar herbivores spanned three insect orders and included both specialist and generalist herbivores. The combination of measurements and inclusion of multiple inducing herbivores allowed me to address two hypotheses in the field of insect-plant interactions: that “mother knows best”, i.e. that oviposition preference is linked to higher larval performance, and that generalist and specialist herbivores induce distinct plant responses. Plants influence the rhizosphere microbiome through root exudation, and this is altered upon herbivory. This way, plant-mediated species interactions may be mediated by changes in the soil microbiome. In chapter 5, I performed a plant-soil feedback experiment. In this experiment, I analysed the rhizosphere microbiome after treating plants with above- and belowground herbivores or beneficial microbes. Furthermore, the soil conditioned by these treated plants was used to grow a new set of plants on which plant defence against D. radicum was tested. Plant-mediated effects found in greenhouse studies are not necessarily translatable to a field setting. Therefore, in chapter 6, I studied D. radicum oviposition and abundance in the field. To connect the field data to results from the previous greenhouse experiments, I assessed the aboveground herbivore community prior to measurements of D. radicum oviposition and abundance. Moreover, when searching the roots and surrounding soil for D. radicum larvae and pupae, other belowground macrofauna was also recorded. Plants assessed for these experiments were part of a large intercropping trial, where different cropping systems were compared. In this chapter, I discuss how different cropping systems affect D. radicum oviposition and abundance, and how these measurements were connected to the abundance of above- and belowground macrofauna. Finally, in chapter 7, I discuss my findings and place them in the framework of plant defence in roots and plant-mediated interactions. This general discussion provides an extensive outline of plant defence against D. radicum, and the potential mechanisms that can cause plant-mediated species interactions. The results of this thesis advance the knowledge on plant defence against root feeding insects and provide new insights on how plants interact with their complex environment.
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Wild radish is an annual plant that exhibits broad spectrum induced resistance to herbivores. In two experiments, we placed potted plants [control, manually clipped, and damaged byPieris rapae(L.) larvae] in the field and assayed for oviposition byP. rapae(a specialist herbivore), damage by flea beetles (a specialist herbivore), and damage by rabbits (a generalist herbivore). Induced responses attracted oviposition byP. rapaeand increased damage by flea beetles, while having a minimal effect on rabbit herbivory. Plant families had different levels of resistance to herbivory by rabbits and to oviposition byP. rapae,but not to herbivory by flea beetles. Manual clipping was a poor inducer of plant responses. Induced responses in wild radish can be a double-edged sword, increasing herbivory by some herbivores under certain conditions, while reducing herbivory by other herbivores.
Flea beetle
Pieris rapae
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Abstract Insect and gastropod herbivores are major plant consumers and their importance in the evolution of plant defensive traits is broadly recognized. However, their respective effects on plant responses have rarely been compared. Here we focused on plant volatile emissions (VOCs) following herbivory and compared the effects of herbivory by caterpillars of the generalist insect Spodoptera littoralis and by generalist slugs of the genus Arion on the VOCs emissions of 14 cultivated plant species. Results revealed that plants consistently produced higher amounts of volatiles and responded more specifically to caterpillar than to slug herbivory. Specifically, plants released on average 6.0 times more VOCs (total), 8.9 times more green leaf volatiles, 4.2 times more terpenoids, 6.0 times more aromatic hydrocarbons, and 5.7 times more other VOCs in response to 1 cm 2 of insect damage than to 1 cm 2 of slug damage. Interestingly, four of the plant species tested produced a distinct blend of volatiles following insect damage but not slug damage. These findings may result from different chemical elicitors or from physical differences in herbivory by the two herbivores. This study is an important step toward a more inclusive view of plant responses to different types of herbivores.
Spodoptera littoralis
Slug
Green leaf volatiles
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Plants and herbivores have been engaged in a co-evolutionary arms race for millions of years, during which plants evolved various defenses and other traits to cope with herbivores, whereas herbivores evolved traits to overcome the plants' resistance strategies. Herbivores may also avoid certain plants merely because these lack suitable nutrients for their development. Interestingly, the number of herbivores that attack individual early land plants like mosses and ferns is quite low. Among others, poor nutrient quality has been hypothesized to explain the apparent low herbivory pressure on such plants but still waits for scientific evidences. Here, the nutritive suitability of representative mosses and liverworts (bryophytes) and ferns (pteridophytes) for herbivores was investigated using feeding assays combined with quantifications of nutrients (proteins, amino acids, and sugars). Growth and survival of two polyphagous herbivores, a caterpillar and a snail, were monitored when fed on 15 species of bryophytes and pteridophytes, as well as on maize (Zea mays, angiosperm) used as an external indicative nutritional resource. Overall, our results show that the poor performance of the herbivores on the studied early land plants is not correlated with nutritional quality. The growth and performance of snails and caterpillars fed with these plants were highly variable and independent of nutrient content. These findings arguably dismiss the poor nutrient quality hypothesis as the cause of herbivory deficit in bryophytes and pteridophytes. They suggest the possible presence of early resistance traits that have persisted all through the long evolutionary history of plant-herbivore interactions.
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Parasitic and predatory arthropods often prevent plants from being severely damaged by killing herbivores as they feed on the plants. Recent studies show that a variety of plants, when injured by herbivores, emit chemical signals that guide natural enemies to the herbivores. It is unlikely that herbivore-damaged plants initiate the production of chemicals solely to attract parasitoids and predators. The signaling role probably evolved secondarily from plant responses that produce toxins and deterrents against herbivores and antibiotics against pathogens. To effectively function as signals for natural enemies, the emitted volatiles should be clearly distinguishable from background odors, specific for prey or host species that feed on the plant, and emitted at times when the natural enemies forage. Our studies on the phenomena of herbivore-induced emissions of volatiles in corn and cotton plants and studies conducted by others indicate that (i) the clarity of the volatile signals is high, as they are unique for herbivore damage, produced in relatively large amounts, and easily distinguishable from background odors; (ii) specificity is limited when different herbivores feed on the same plant species but high as far as odors emitted by different plant species and genotypes are concerned; (iii) the signals are timed so that they are mainly released during the daytime, when natural enemies tend to forage, and they wane slowly after herbivory stops.
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Overgrazing
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Abstract Plants may respond both to feeding and oviposition by herbivorous insects. While responses of plants to feeding damage by herbivores have been studied intensively during the past decades, only a few, but growing number of studies consider the reactions of plants towards egg deposition by herbivorous insects. Plants showing defensive response to oviposition by herbivores do not ‘wait’ until being damaged by feeding, but may instead react towards one of the initial steps of herbivore attack, the egg deposition. Direct plant defensive responses to feeding act directly against the feeding stages of the herbivores. However, a plant may also show direct defensive responses to egg deposition by (a) formation of neoplasms, (b) formation of necrotic tissue (= hypersensitive response), and (c) production of oviposition deterrents. All these plant reactions have directly negative effects on the eggs, hatching larvae, or on the ovipositing females. Indirect plant defensive responses to feeding result in the emission of volatiles (= synomones) that attract predators or parasitoids of the feeding stages. A few recent studies have shown that plants are able to emit volatiles also in response to egg deposition and that these volatiles attract egg parasitoids. Studies on the mechanisms of induction of synomones by egg deposition show several parallels to the mechanisms of induction of plant responses by feeding damage. When considering induced plant defence against herbivores from an evolutionary point of view, the question arises whether herbivores evolved the ability to circumvent or even to exploit the plant's defensive responses. The reactions of herbivores to oviposition induced plant responses are compared with their reactions to feeding induced plant responses.
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Data on plant herbivore damage as well as on herbivore performance have been previously used to identify key plant traits driving plant–herbivore interactions. The extent to which the two approaches lead to similar conclusions remains to be explored. We determined the effect of a free-living leaf-chewing generalist caterpillar, Spodoptera littoralis (Lepidoptera: Noctuidae), on leaf damage of 24 closely related plant species from the Carduoideae subfamily and the effect of these plant species on caterpillar growth. We used a wide range of physical defense leaf traits and leaf nutrient contents as the plant traits. Herbivore performance and leaf damage were affected by similar plant traits. Traits related to higher caterpillar mortality (higher leaf dissection, number, length and toughness of spines and lower trichome density) also led to higher leaf damage. This fits with the fact that each caterpillar was feeding on a single plant and, thus, had to consume more biomass of the less suitable plants to obtain the same amount of nutrients. The key plant traits driving plant–herbivore interactions identified based on data on herbivore performance largely corresponded to the traits identified as important based on data on leaf damage. This suggests that both types of data may be used to identify the key plant traits determining plant–herbivore interactions. It is, however, important to carefully distinguish whether the data on leaf damage were obtained in the field or in a controlled feeding experiment, as the patterns expected in the two environments may go in opposite directions.
Trichome
Spodoptera littoralis
Specific leaf area
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1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.
Pieris rapae
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