Monika Hilker

Early Herbivore Alert: Insect Eggs Induce Plant Defense

Plants are able to “notice” insect egg deposition and to respond by activating direct and indirect defenses. An overview of these defenses and the underlying mechanisms is given from a tritrophic perspective. First, the interface between plant and eggs is addressed with respect to the mode of attachment of eggs on the plant surface. It is elucidated which plant cells might respond to components from insect eggs or the egg deposition. The scarce knowledge on the elicitors associated with the eggs or the egg-laying female is outlined. Since endosymbiotic microorganisms are often present on the eggs, and microorganisms are also abundant on the leaf surface, the role of these hidden players for eliciting oviposition-induced plant responses is considered. Furthermore, the question of which physiological and molecular processes are induced within the plant in response to egg deposition is addressed. Second, studies on the response of the herbivorous insect to oviposition-induced plant defenses are outlined. Third, the importance of oviposition-induced plant volatiles and contact cues for host and prey location of parasitoids and predators is discussed in the context of other informative chemicals used by carnivores when searching for food. Finally, physiological and ecological costs of oviposition-induced plant responses are addressed.

Chemoecology of Insect Eggs and Egg Deposition

The insects that cause or transmit human and animal disease constitute a wide range of taxa sharing a similar feeding habit, but differing in most other aspects of their life histories, including oviposition. This chapter mainly deals with oviposition or larviposition behaviour within the Diptera, since the major groups that exhibit such behaviour and that constitute pests of major medical or veterinary importance are true flies. Aggregation behaviour in bloodsucking Hemiptera is discussed briefly. Bloodfeeding groups generally oviposit at sites remote from their vertebrate hosts: mosquitoes (Culicidae) and blackflies (Simuliidae) oviposit in aquatic environments, and sandflies (Psychodidae), tsetse flies (Glossinidae), bedbugs (Cimicidae) and kissing bugs (Reduviidae) oviposit in terrestrial environments. Facultative or obligatory carnivorous Diptera, where the immature stages can be saprotrophic or parasitic on the same animals on which the adult flies feed, also locate and select oviposition or larviposition sites using chemical cues. These include warble flies, bot flies (Oestridae), blowflies, screwworms (Calliphoridae) and flesh flies (Sarcophagidae). Not surprisingly, given the range of life histories of these diverse groups, the interaction of pheromones with visual cues, odours of environmental origin and the physical properties of the oviposition site, is wide-ranging in nature. Knowledge of the chemoecology of oviposition in these insects lags behind that on herbivorous and parasitic insects and attractant compounds have been identified in only a few cases. A number of plant species have evolved to mimic animal odour cues to attract carnivorous fly species as pollinators. Because of the importance of these insects as vectors of human and animal disease, interest in this field has been driven primarily by a search for chemically baited traps for monitoring and control. Odour baited oviposition traps are currently used in the surveillance of a number of important pest species. Odour baited trapping for the control of pest populations may be feasible for certain species. 5.

Induction of Plant Synomones by Oviposition of a Phytophagous Insect

Earlier investigations of host habitat location in the egg parasitoid Oomyzus gallerucae have shown that oviposition of the elm leaf beetle (Xanthogaleruca luteola) induces the field elm (Ulmus minor) to emit volatiles that attract the egg parasitoid. In this study we investigated the mechanism of this induction by testing the effects of differently treated elm leaves on O. gallerucae in a four-arm olfactometer. First we investigated which sequence of the herbivore oviposition behavior is necessary for the synomone induction. The following major sequences were observed: (1) Prior oviposition, the gravid female gnawed shallow grooves into the leaf surface. (2) After gnawing upon the leaf surface, the female attached about 20–30 eggs with oviduct secretion in the grooves. We experimentally mimicked the shallow grooves on the leaf surface by scratching the leaf surface with a scalpel (= scratched leaves). Volatiles from such scratched leaves did not attract the egg parasitoid. However, as soon as eggs with oviduct secretion, or only oviduct secretion, was applied to these scratched leaves, they emitted attractive volatiles. Application of oviduct secretion and eggs on undamaged leaves did not elicit release of attractive synomones. Thus, an elicitor is located in the oviduct secretion, but becomes active only when the leaf surface is damaged. Jasmonic acid is known as a mediator of plant responses induced by feeding of herbivorous arthropods, and we demonstrate that it mediates production of elm synomones that attract O. gallerucae. The plants reaction to oviposition was systemic, and leaves without eggs near leaves with eggs emitted attractants.

Induced plant defences: from molecular biology to evolutionary ecology

Abstract Phenotypic plasticity enables invididuals to change their phenotype in response to their environment. These phenotypic changes can affect many interactions between the members of a community. Plants are able to respond towards herbivore attack by defensive mechanisms directly affecting the herbivore and by so-called indirect defences that negatively affect the herbivore by maintenance or attraction of carnivores. The phenotypic changes of plants caused by induced defences may vary with the type of attackers. Different attackers can evoke different plant responses due to specific elicitors or wounding. These different plant responses may be mediated by different choreographies of gene expression. Symbiotic and pathogenic microorganisms associated with the plant or the herbivore may play an important role in the induction process. Thus, a plethora of biotic factors affect the physiological, chemical, and molecular characteristics of plants in response to attack. The adaptiveness of phenotypic plasticity in terms of induced responses depends on the balance of their physiological and ecological costs and benefits. An integrated approach is necessary considering ecological, molecular and chemical aspects to gain deeper insight into induced defence and its application in environmentally benign crop protection. Phanotypische Plastizitat befahigt Individuen, ihren Phanotyp in Reaktion auf Umweltreize zu andern. Die phanotypischen Veranderungen konnen zahlreiche Interaktionen zwischen den Mitgliedern einer Biozonose beeinflussen. Angriffe von Herbivoren konnen in Pflanzen direkte und indirekte Verteidigungsmechanismen induzieren. Wahrend die direkte Verteidigung sich unmittelbar gegen die Herbivoren richtet, wirkt die indirekte Abwehr uber die Beherbergung oder Anlockung von Carnivoren auf die Herbivoren ein. Die induzierten phanotypischen Veranderungen der Pflanze sind je nach Typ des Angreifers sehr unterschiedlich. Unterschiedliche Herbivore konnen aufgrund verschiedener Frasverhalten und aufgrund spezifischer Elicitoren jeweils ganz unterschiedliche pflanzliche Reaktionen hervorrufen. Die Vielfalt der pflanzlichen Antworten auf Herbivorenfras wird bestimmt durch unterschiedliche Muster in der Expression der an der Abwehr beteiligten Gene. Symbiontische und pathogene Mikroorganismen, die mit der Pflanze oder den Herbivoren assoziiert sind, konnen eine wichtige Rolle im Induktionsprozess spielen. Demnach beeinflusst eine Fulle biotischer Faktoren die physiologischen, chemischen und molekularen Charakteristika der frasinduzierten pflanzlichen Verteidigung. Der adaptive Wert der phanotypischen Plastizitat, die sich in der Vielfalt der induzierten Verteidigungsmechanismen spiegelt, hangt vom Gleichgewicht der physiologischen und okologischen Kosten und Nutzen der Abwehrreaktionen ab. Zum tieferen Verstandnis der induzierten pflanzlichen Abwehr gegen Herbivore sowie zur Nutzung der induzierten Abwehrreaktion im umweltvertraglichen Pflanzenschutz ist eine integrierte Herangehensweise notwendig, die sowohl okologische wie auch molekulare und chemische Aspekte berucksichtigt.

The Relevance of Background Odor in Resource Location by Insects: A Behavioral Approach

ABSTRACT Insects live in a highly complex odorant world. Within a variety of odor blends, they need to locate potential food sources, mates, and oviposition sites to gain reproductive success. In nature, volatile cues leading to a resource are always present with numerous other volatiles—here referred to as background odor—which may affect the parasitoids response to resource-indicating cues. Three different types of background odor are discussed in this article: (a) irrelevant background odor, (b) background odor that may mask the resource-indicating signals, and (c) background odorants that may “sharpen the view” for resource-indicating odor and enhance the response to these. Odor orientation to resources especially in herbivorous and parasitic insects are addressed.

Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison

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 plants defensive responses. The reactions of herbivores to oviposition induced plant responses are compared with their reactions to feeding induced plant responses.

How do plants “notice” attack by herbivorous arthropods?

Precise and deep comprehension of plant responses to herbivorous arthropods requires detailed knowledge of how a plant “notices” the attack. Herbivore attack is not restricted to plant wounding by feeding, but instead different phases of attack that elicit a plant response need to be distinguished: touch, oviposition and feeding. Touch, secretions released with eggs and regurgitate delivered during feeding may act in concert as elicitors of plant defence. Here, we discuss the current knowledge of what a plant “notices” during the different phases of herbivore attack and how it responds at the molecular, physiological and ecological level. Understanding the mechanisms of plant responses to the different phases of herbivore attack will be a key challenge in unravelling the complex communication pathways between plants and herbivores.

Chemical Analysis of Volatiles Emitted by Pinus sylvestris After Induction by Insect Oviposition

Gas chromatography – mass spectrometry analyses of the headspace volatiles of Scots pine (Pinus sylvestris) induced by egg deposition of the sawfly Diprion pini were conducted. The odor blend of systemically oviposition-induced pine twigs, attractive for the eulophid egg parasitoid Chrysonotomyia ruforum, was compared to volatiles released by damaged pine twigs (control) that are not attractive for the parasitoid. The mechanical damage inflicted to the control twigs mimicked the damage by a sawfly female prior to egg deposition. The odor blend released by oviposition-induced pine twigs consisted of numerous mono- and sesquiterpenes, which all were also present in the headspace of the artificially damaged control twigs. A quantitative comparison of the volatiles from oviposition-induced twigs and controls revealed that only the amounts of (E)-β-farnesene were significantly higher in the volatile blend of the oviposition-induced twigs. Volatiles from pine twigs treated with jasmonic acid (JA) also attract the egg parasitoid. No qualitative differences were detected when comparing the composition of the headspace of JA-treated pine twigs with the volatile blend of untreated control twigs. JA-treated pine twigs released significantly higher amounts of (E)-β-farnesene. However, the JA treatment induced a significant increase of the amount of further terpenoid components. The release of terpenoids by pine after wounding, egg deposition, and JA treatment is discussed with special respect to (E)-β-farnesene.

Plants and insect eggs: how do they affect each other?

Plant-insect interactions are not just influenced by interactions between plants and the actively feeding stages, but also by the close relationships between plants and insect eggs. Here, we review both effects of plants on insect eggs and, vice versa, effects of eggs on plants. We consider the influence of plants on the production of insect eggs and address the role of phytochemicals for the biosynthesis and release of insect sex pheromones, as well as for insect fecundity. Effects of plants on insect oviposition by contact and olfactory plant cues are summarised. In addition, we consider how the leaf boundary layer influences both insect egg deposition behaviour and development of the embryo inside the egg. The effects of eggs on plants involve egg-induced changes of photosynthetic activity and of the plants secondary metabolism. Except for gall-inducing insects, egg-induced changes of phytochemistry were so far found to be detrimental to the eggs. Egg deposition can induce hypersensitive-like plant response, formation of neoplasms or production of ovicidal plant substances; these plant responses directly harm the eggs. In addition, egg deposition can induce a change of the plants odour and leaf surface chemistry which serve indirect plant defence with the help of antagonists of the insect eggs. These egg-induced changes lead to attraction of egg parasitoids and their arrestance on a leaf, respectively. Finally, we summarise knowledge of the elicitors of egg-induced plant changes and address egg-induced effects on the plants transcriptional pattern.

Plant Responses to Insect Egg Deposition

Plants can respond to insect egg deposition and thus resist attack by herbivorous insects from the beginning of the attack, egg deposition. We review ecological effects of plant responses to insect eggs and differentiate between egg-induced plant defenses that directly harm the eggs and indirect defenses that involve egg parasitoids. Furthermore, we discuss the ability of plants to take insect eggs as warning signals; the eggs indicate future larval feeding damage and trigger plant changes that either directly impair larval performance or attract enemies of the larvae. We address the questions of how egg-associated cues elicit plant defenses, how the information that eggs have been laid is transmitted within a plant, and which molecular and chemical plant responses are induced by egg deposition. Finally, we highlight evolutionary aspects of the interactions between plants and insect eggs and ask how the herbivorous insect copes with egg-induced plant defenses and may avoid them by counteradaptations.