Host-plant-mediated competition via induced resistance: interactions between pest herbivores on potatoes

Abstract

Plant-mediated competition among insect herbivores occurs when one species induces changes in plant chemistry, nutrition, or morphology that render plants resistant to attack by others. We explored plant-mediated interspecific interactions between the potato leafhopper (Empoasca fabae) and the Colorado potato beetle (Leptinotarsa decemlineata), two important pests on potatoes. Leafhoppers colonize fields in advance of beetles, and thus the possibility exists that previous feeding by leafhoppers induces changes in potato plants that have adverse consequences for beetles. The consequences of leafhopper-induced resistance for beetle performance were studied in the greenhouse, field cages, and in large open-field plots. Potato plants were exposed to four densities of leafhoppers (none, low, moderate, and high), and visible feeding symptoms were measured as percentage leaf curling, chlorosis, and necrosis. The oviposition preference, performance, and survivorship of Colorado potato beetles were then measured on the four categories of induced plants in field-cage and greenhouse settings. In open field plots, survival on the four categories of induced plants was determined by placing cohorts of beetle adults onto plants and measuring the densities of resulting eggs, larvae, and emerging Fl adults. Leafhopper-induced symptoms on potato plants were density dependent, with the percentage of curled, chlorotic, and necrotic leaves increasing with leafhopper density. Previous feeding by leafhoppers adversely affected oviposition and larval performance of beetles. Fewer egg masses were deposited on plants that incurred high levels of leafhopper feeding. Similarly, larval development was delayed and emerging adult beetles weighed less when fed induced foliage from the high leafhopper-density treatment. Beetles survived less well in the field on plants experiencing moderate and high levels of leafhopper feeding as evidenced by lower densities of eggs, larvae, and emerging F1 adults. Overall, leafhoppers and beetles competed through feeding-induced changes in plant quality. Notably, the asymmetric interaction took place at a large spatial scale in open field plots and had negative consequences that persisted to the next beetle generation. Ultimately, to establish an effective management strategy for crop pests such as leafhoppers, it is essential to consider the positive indirect effects of induced resistance along with the negative direct effects on crop yield.