Plant water stress and its consequences for herbivorous insects: a new synthesis

Traditionally, herbivorous insects are thought to exhibit enhanced performance and outbreak dynamics on water-stressed host plants due to induced changes in plant physiology. Recent experimental studies, however, provide mixed support for this historical view. To test the plant-stress hypothesis (PSH), we employed two methods (the traditional vote-counting approach and meta-analysis) to assess published studies that investigated insect responses to experimentally induced water-deficit in plants. For insects, we examined how water deficit affects survivorship, fecundity, density, relative growth rate, and oviposition preference. Responses were analyzed by major feeding guild (sap-feeding insects and chewing insects) and for the subguilds of sap-feeders (phloem, mesophyll, and xylem feeders) and chewing insects (free-living chewers, borers, leaf miners, and gall-formers). Both vote counting and meta-analysis found strong negative effects of water stress on the performance of sap-feeding insects at large and on members of the phloem- and mesophyll-feeding subguilds in particular. Both analytical techniques demonstrated a nonsignificant response for chewing insects at large due to the offsetting effects of water stress on the different subguilds. For example, our analyses found consistent positive responses for borers, negative responses for gall-formers, and inconsistent responses for free-living species and leaf miners. Overall, our analyses strongly challenge the historical view that herbivorous insects exhibit elevated performance and outbreak dynamics on water-stressed plants. Rather, there is widespread evidence that many phytophagous insects, especially sap-feeders, are adversely affected by continuous water stress. Despite enhanced foliar nitrogen during times of plant stress, concurrent reductions in turgor and water content interfere with an herbivore's ability to access or utilize nitrogen. To explain the discrepancy between the observed outbreaks of phytophagous insects on water-stressed plants in nature and the negative effects detected in many experimental studies where plants are continuously stressed, we propose a "pulsed stress hypothesis" whereby bouts of stress and the recovery of turgor allow sap-feeders to benefit from stress-induced increases in plant nitrogen. Our finding that phloemfeeding insects respond positively on intermittently stressed plants but exhibit poor performance on continuously stressed ones is consistent with this hypot