Simple SummaryThe mealybugs are a large family of sap-sucking herbivore insects comprising more than 2000 species. They feed on many economically important agricultural and ornamental plants. During the cold periods of the winter, insects overwintering without migrating often require special habitats to survive unfavorable environmental conditions. In the case of mealybugs inhabiting fruit orchards, it was believed that the trunk and the branches were the main overwintering sites where individuals diapause. Here it is shown for the first time that, in temperate climates, mealybugs spend half of the year on the tree canopy and the large majority move to the rhizosphere of the fruit tree during the winter to feed on the roots and reproduce (complete at least one generation) under the new “belowground habitat.” This unique adaptive strategy allows an aboveground herbivore to turn into a belowground root-feeding insect for part of the year. The preferred area to overwinter for the main female mealybug species is within 1 m in diameter around the fruit tree trunk, where more than 12,000 mealybug males per square meter can emerge every spring. These findings have implications at the ecological and agronomical levels since current treatments to control mealybug pests are based on the fruit trees’ canopy.AbstractInsects have limited ability to regulate their body temperature and have thus required a range of strategies to withstand thermally stressful environments. Under unfavorable winter conditions, insects often take refuge under the soil surface to survive. Here, the mealybug insect family was selected for the study. Field experiments were performed in fruit orchards in eastern Spain. We used specifically designed floor sampling methods combined with fruit tree canopy pheromone traps. We found that in temperate climates, the large majority of the mealybugs move from the tree canopy to the roots during the winter, where they turn into belowground root-feeding herbivores to survive and continue underground the reproductive process. Within the rhizosphere, mealybugs complete at least one generation before emerging on the soil surface. The preferred area to overwinter is within 1 m in diameter around the fruit tree trunk, where more than 12,000 mealybug flying males per square meter can emerge every spring. This overwintering pattern has not previously been reported for any other group of insects showing cold avoidance behavior. These findings have implications at the winter ecology level but also at the agronomical level since treatments to control mealybug pests are, until now, only based on the fruit trees’ canopy.