Every plant is a member of a complex insect community that consists of tens to hundreds of species that belong to different trophic levels. The dynamics of this community are critically influenced by the plant, which mediates interactions between community members that can occur on the plant simultaneously or at different times. Herbivory results in changes in the plant's morphological or chemical phenotype that affect interactions with subsequently arriving herbivores. Changes in the plant's phenotype are mediated by molecular processes such as phytohormonal signaling networks and transcriptomic rearrangements that are initiated by oral secretions of the herbivore. Processes at different levels of biological complexity occur at timescales ranging from minutes to years. In this review, we address plant-mediated interactions with multiple species of the associated insect community and their effects on community dynamics, and link these to the mechanistic effects that multiple attacks have on plant phenotypes.
Crop domestication is the process of artificially selecting plants to increase their suitability to human requirements: taste, yield, storage, and cultivation practices. There is increasing evidence that crop domestication can profoundly alter interactions among plants, herbivores, and their natural enemies. Overall, little is known about how these interactions are affected by domestication in the geographical ranges where these crops originate, where they are sympatric with the ancestral plant and share the associated arthropod community. In general, domestication consistently has reduced chemical resistance against herbivorous insects, improving herbivore and natural enemy performance on crop plants. More studies are needed to understand how changes in morphology and resistance-related traits arising from domestication may interact with environmental variation to affect species interactions across multiple scales in agroecosystems and natural ecosystems.
Abstract. Populations of wild Brassica oleracea L. grow naturally along the Atlantic coastlines of the United Kingdom and France. Over a very small spatial scale (i.e., ,15 km) these populations differ in the expression of the defensive compounds, glucosinolates (GS). Thus far, very few studies have examined interactions between genetically distinct populations of a wild plant species and associated consumers in a multitrophic framework. Here, we compared the development of a specialist (Pieris rapae) and a generalist (Mamestra brassicae) insect herbivore and their endoparasitoids (Cotesia rubecula and Microplitis mediator, respectively) on three wild populations and one cultivar of B. oleracea under controlled greenhouse conditions. Herbivore performance was differentially affected by the plant population on which they were reared. Plant population influenced only development time and pupal mass in P. rapae, whereas plant population also had a dramatic effect on survival of M. brassicae. Prolonged development time in P. rapae corresponded with high levels of the indole GS, neoglucobrassicin, whereas reduced survival in M. brassicae coincided with high levels of the aliphatic GS, gluconapin and sinigrin. The difference between the two species can be explained by the fact that the specialist P. rapae is adapted to feed on plants containing GS and has evolved an effective detoxification system against aliphatic GS. The different B. oleracea populations also affected development of the endoparasitoids. Differences in foodplant quality for the hosts were reflected in adult size in C. rubecula and survival in M. mediator, and further showed that parasitoid performance is also affected by herbivore diet.
It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical-and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata , a parasitoid of the leaf herbivore Pieris brassicae , mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.
Summary Related plant species with different spatial and/or temporal life‐history characteristics often possess differences in secondary chemistry and thus direct defensive capability. These differences are often attributed to a range of divergent selection pressures from herbivores and pathogens. Most studies of insect–plant interactions have examined the effects of plant defence on herbivore performance, with less attention being paid to higher trophic levels, such as parasitoid wasps. Moreover, to date it is not known whether secondary plant compounds may affect organisms in the fourth trophic level. Here, we study interactions in a four‐trophic‐level system. The development of a solitary secondary hyperparasitoid, Lysibia nana, and its primary endoparasitoid host, Cotesia glomerata, are compared when reared from a primary herbivore host, Pieris brassicae, which was itself reared on two cruciferous plants with contrasting life histories. Whereas L. nana is known to attack the pupae of a number of primary parasitoids in the genus Cotesia, both C. glomerata and P. brassicae are intimately associated with plants in the family Brassicaceae. Insects were reared from a feral population of the spring perennial, Brassica oleracea, and a naturally occurring population of a summer annual, B. nigra. Like other cruciferous plants, both species are known to produce glycoside toxins (= glucosinolates) after they are attacked by foliar herbivores. However, concentrations of glucosinolates were more than 3·5 times higher in young shoots of B. nigra than in corresponding shoots of B. oleracea. Cocoon weight in C. glomerata was unaffected by the foodplant on which P. brassicae was reared, whereas in 24‐h‐old host cocoons emerging adult hyperparasitoid body mass increased significantly with cocoon size and wasps were significantly larger, and survived better on B. oleracea than on B. nigra. Moreover, body mass in L. nana was typically larger in young (c. 24 h), than in older (c. 72 h) cocoons of C. glomerata. Egg‐to‐adult development time in L. nana generally increased with host size and age, and wasps on younger hosts completed their development more rapidly on B. nigra. Our results clearly demonstrate that qualitative differences in herbivore diet can differently affect the performance of interacting organisms across several trophic levels, and suggest that bottom‐up forces may also play a role in mediating interactions involving plants–herbivores–parasitoids and hyperparasitoids.
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