Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints

Nitrogen (N) and water are crucial in crop production but increasingly scarce environmental resources. Reducing their inputs can affect the whole plant-arthropod community including biocontrol agents. In a multitrophic system, we studied the interaction of the bottom-up effects of moderately reduced N concentration and/or water supply as well as the top-down effects of pests of different feeding guilds on plant nutritional quality (N and carbon concentration), direct defense (alkaloids and phenolics), and indirect defense (plant volatile organic compounds); on herbivore performance and host quality (N and carbon) to parasitoids and the latter's performance. Studied organisms were tomato plants, the sap feeders Macrosiphum euphorbiae and Bemisia tabaci, the leaf chewers Tuta absoluta and Spodoptera littoralis, and the parasitic wasps Aphelinus abdominalis and Necremnus tutae. Resource limitation affected plant quality, triggering bottom-up effects on herbivore and parasitoid performance, except for T. absoluta and N. tutae. Feeding guild had a major influence: bottom-up effects were stronger on sap feeders; N effects were stronger on sap feeders while water effects were stronger with leaf chewers (S. littoralis). Top-down effects of leaf chewer herbivory partly attenuated bottom-up effects and partly suppressed plant defenses. Bottom-up effects weakened when cascading up trophic levels. In summary, the interaction between plants, pests, and beneficial insects was modulated by abiotic factors, affecting insect performance. Simultaneous abiotic and biotic impact shaped plant biochemistry depending on the feeding guild: the biotic top-down effect of leaf chewer herbivory attenuated the bottom-up effects of plant nutrition and hence dominated the plant biochemical profile whereas in sap feeder infested leaves, it corresponded to the abiotic impact. This study highlights the plant's finely tuned regulatory system facilitating response prioritization. It offers perspectives on how smart manipulation of plant nutrient solutions might save resources while maintaining efficient biocontrol in crop production.