Water and salt stresses do not trigger bottom-up effects on plant-mediated indirect interactions between a leaf chewer and a sap-feeder

Abstract

Soil abiotic stresses can trigger bottom-up effects on insect pests. However, it remains unknown whether the bottom-up effects differentially affect leaf chewers and sap-feeders, and whether abiotic stresses alter the extent of indirect interactions between insect herbivores sharing a host plant. We carried out a set of manipulative experiments to investigate how abiotic and biotic stresses affected performance associated with insect herbivory (eating by leaf chewer or sap-feeder) and plant physiological conditions (manipulating water and/or salt inputs). We examined the performance of response species (sap-feeder Macrosiphum euphorbiae and leaf chewer Tuta absoluta) on tomato plants Solanum lycopersicum that were exposed to eight conditions in a full factorial design based on (1) optimal or limited water inputs, (2) with or without 100 mM NaCl, and (3) with or without pre-infestation by insect herbivors showing distinct feeding habit. Water and salt stresses slowed down plant growth in terms of plant height and node number, which subsequently negatively affected the herbivores via bottom-up effects. Tuta absoluta larval development was adversely affected by water limitation, while M. euphorhiae survival and fertility were adversely affected by salinity stress. After pre-infestation by the inducing species (i.e. feeding activity on the plant), the test species (either M. euphorbiae or T. absoluta) exhibited a lower performance, that is, lower M. euphorbiae survival and fewer offspring, and extended T. absoluta developmental duration and reduced pupal weight. These results suggested an apparent competition between the herbivores; however, neither water limitation nor salt stress affected the magnitude of the negative indirect interactions between the two insect species. Our findings shed light on how cascading force(s) and induced indirect resistance(s) could be used to improve integrated pest management programs.