4.14 Allelochemicals in Plant–Insect Interactions
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4.14 Allelochemicals in Plant–Insect Interactions Keiichi Honda and Hisashi Oˆ mura, Hiroshima University, Higashihiroshima, Japan Masatoshi Hori, Tohoku University, Sendai, Japan Yooichi Kainoh, University of Tsukuba, Tsukuba, Japan ª 2010 Elsevier Ltd. All rights reserved. 4.14.1 Introduction 563 4.14.2 Host Selection 563 4.14.2.1 Phytochemicals Involved in Oviposition 563 4.14.2.2 Feeding Attractants and Stimulants 570 4.14.3 Flower-Visiting and Foraging 580 4.14.3.1 Floral Volatiles 580 4.14.3.1.1 Attractants in nursery pollination 580 4.14.3.1.2 Attractants in sexual mimicry 581 4.14.3.1.3 Attractants in abiotic mimicry 582 4.14.3.1.4 Repellent volatiles in floral scents 583 4.14.3.1.5 Transfer of volatiles from flowers to insects 583 4.14.3.2 Food Constituents Affecting Foraging 584 4.14.3.2.1 Sugars 584 4.14.3.2.2 Amino acids 584 4.14.3.2.3 Toxic components 584 4.14.4 Insect–Plant Interface in Multitrophic Interactions 585 4.14.4.1 Parasitic Wasps 585 4.14.4.2 Parasitic Flies 588 4.14.4.3 Predators 588 4.14.4.4 Elicitors 589 References 590 4.14.1 Introduction The majority of insects are herbivores that depend on plants for their nutrients. The chemicals produced by plants and insects can have significant effects on their lives, and insect–plant interactions have therefore been of long- standing interest in chemical ecology. Biological and chemical analyses of the interplay between insect pests and crops are of great importance from the perspective of future agriculture as the need to develop environmentally benign pest control agents for practical use continues to grow.1 Phytochemicals, particularly secondary metabolites, play important and often crucial roles in many types of insect behaviors, and can even regulate their growth and reproduction in various ways, thus ultimately exerting considerable influence on their fitness. The abilities of insects to counteract the plants’ chemical barriers, which might have developed through coevolutionary interactions between insects and plants, allow them to make use of certain phytochemicals as cues to locate and recognize suitable food or host plants. Various attractants, stimulants, repellents, and deterrents are usually involved in this process. Some insects even sequester and store noxious phytochemicals to use for their own chemical defenses. Owing to the complexity of insect–plant relationships, the allelochemicals mediating these interactions include a wide array of chemical compounds with a variety of ecological functions. In this chapter, we have focused our attention on selected topics in which significant progress has been made during the last decade, and have not discussed those chemicals of little or no ecological relevance. Since antifeedants are covered in another chapter, plant chemicals that deter food ingestion have also been omitted. This chapter initially deals with plant constituents involved in host selection: those affecting oviposition by females and those stimulating feeding by both larvae and adults. Later, pollination strategies of plants involving 563 564 Allelochemicals in Plant–Insect Interactions manipulation of their floral scents to lure or repel insects are reviewed, along with the gustatory responses of foragers to a few groups of nutrients and other chemicals in the nectar. Finally, we have addressed the multitrophic interactions among plants, insects, and their parasitoids, which have aroused increasing interest in recent years, and further commented on induced plant volatiles that mediate the attraction of predators to prey-infested plants. 4.14.2 Host Selection Host selection by phytophagous insects usually consists of two phases: food choice through preimaginal feeding (also feeding by adults in certain insect taxa) and host-plant seeking and assessment by ovipositing females. Among the most important factors influencing host selection by insects are the chemical constituents present in the plants, although other factors such as visual and/or mechanical stimuli also act concurrently on deciding whether to accept potential host plants or not. 4.14.2.1 Phytochemicals Involved in Oviposition Behavioral, sensory, and phytochemical bases for egg-laying by moths and butterflies have previously been fully reviewed.2,3 Subsequently a number of newly identified plant chemicals serving as oviposition stimulants or deterrents have been reported for many lepidopterans and other insects. The majority of swallowtail butterflies of the genus Papilio (family Papilionidae) exclusively utilize plants of the family Rutaceae as hosts, with a few species exploiting limited plant species of the families Apiaceae or Lauraceae. The North American black swallowtail butterfly, Papilio polyxenes, a specialist on members of carrot family (Apiaceae), has already been shown to lay eggs in response to a mixture of two chemotactile stimulants, luteolin 7-O-(699 -O-malonyl)- -D-glucoside and trans-chlorogenic acid, identified from one of its major host plants, Daucus carota (wild carrot). Further study revealed that the oviposition response by the butterfly to another host plant, Pastinaca sativa (wild parsnip), was evoked by a combination of tyramine (1), trans- chlorogenic acid, and a neutral fraction from the plant.4 The zebra swallowtail butterfly, Eurytides marcellus, is an Annonaceae-feeding specialist. One of three hydroxycinnamoyl derivatives of 1,3,4,5-tetrahydroxycyclohexane-1-carboxylic acid, that is, 3-caffeoyl-muco- quinic acid (2), isolated from the foliage of its primary host plant, Asimina triloba, was active alone in stimulating oviposition.5 The action of compound 2 is unique because other papilionid butterflies for which oviposition stimulants have been reported are induced to oviposit by the synergistic action of multiple components.3 However, E. marcellus females were deterred from egg-laying by flavonoids (rutin and nicotiflorine) co-occurring in the host plant, thus using both qualitative and quantitative information about these compounds to assess host quality.6 Interestingly, the same compound (2), also identified from Sassafras albidum (Lauraceae), was found to act as an oviposition stimulant for the spicebush swallowtail, Papilio troilus, which feeds exclusively on plants of the family Lauraceae. This compound was inactive alone, but increased the oviposition activity of the females when combined with other as yet uncharacterized stimulant(s).7 Two oviposition stimulants, (À)-4-(E)-caffeoyl-L-threonic acid (3) and (À)-2-C-methyl-D-erythrono-1,4- lactone (4), have been reported8,9 for a Rutaceae-feeding swallowtail butterfly, Papilio bianor, which preferen- tially utilizes Orixa japonica as its principal host in the western districts of Japan. The former compound singly stimulated egg-laying by the females to a certain extent, while the latter on its own evoked no oviposition response, but turned out to be active when assayed in combination with other fractions derived from a methanolic extract of the plant. However, no synergistic action of the two compounds in stimulation of oviposition was shown. Papilio macilentus also feeds specifically on O. japonica, which ovipositing females chemically recognize as a host, partly by foretarsal detection of a benzofuran derivative, cnidioside A (5). Although a few species of Japanese swallowtail butterflies exploit O. japonica as larval food, the plant is rejected by many other swallowtails. Papilio xuthus, a typical Citrus feeder, never accepts O. japonica. The inhibition of colonization of this plant by the butterfly has been attributed to the presence of at least two compounds, 3,4-O-disyringoylaldaric acid (6) and 5-{[2-O-( -D-apiofuranosyl)- -D-glucopyranosyl]oxy}-2- hydroxybenzoic acid (7), which potently deter both larval feeding and female oviposition.10 Allelochemicals in Plant–Insect Interactions 565 Papilio polytes is a tropical swallowtail butterfly specializing on only a few rutaceous plants in Japan, such as Toddalia asiatica and Citrus depressa, while another sympatric potential host, Murraya paniculata (Rutaceae), remains entirely unexploited by the butterfly in its natural habitat. Strong oviposition responses to T. asiatica were found to be elicited by synergism between trans-4-hydroxy-N-methyl-L-proline (weakly active alone) (8) 11 and 2-C-methyl-D-erythronic acid (9). On the contrary, trigonelline (10) present in M. paniculata was partly responsible for the avoidance of the plant by ovipositing females.12 Glycosmis citrifolia, a relatively rare rutaceous plant occurring in sympatry with the above plants, is occasionally infested by P. polytes in nature. Oviposition on this plant also proved to be due to the presence of compounds 8 and 9.12 Pyrrolizidine alkaloids (PAs) are a typical class of plant secondary metabolites, which certain butterflies and moths in particular groups, that is, Danainae, Ithomiinae (Nymphalidae), and Arctiidae, sequester as larvae or adults and utilize as chemical defensive substances against predatory enemies, probably due to their bitter taste and hepatotoxicity.13 PAs also serve as precursors of male pheromones of PA-storing lepidopterans. The primitive danaine butterfly, Idea leuconoe (occurring in the Old World tropics), is a specialist on plants of the genus Parsonsia (Apocynaceae), which contain PAs, and uses the alkaloids as crucial cues in host recognition. The females were induced to oviposit by host-plant-specific macrocyclic PAs, including parsonsianine, parsonsianidine, and 17-methylparsonsianidine (Figure 1), each of which individually showed