Early learning by predatory mites in foraging contexts

Learning, behavioral change by experience, is a ubiquitous phenomenon in animals. Learning may affect every major life activity such as foraging, reproduction or social interactions. Learning is generally considered a behavioral optimization process and assumed to help animals to adjust their behaviors to varying environments. The proposed project focuses on learning in the very early stages of life by plant-inhabiting predatory mites in foraging contexts. These predatory mites are important natural enemies of herbivorous mites and insects, used in biological control around the world. The principal project ideas are based on own recent findings that early in life, including in the prenatal phase, the mites are well able to learn the features of a given prey. Relatively brief experiences made soon after hatching in the larval stage persist through juvenile development, including three molting events, and lead to profound and consistent behavioral changes after reaching adulthood. The proposed project addresses three major intertwined issues. Issue (1) pursues the questions which learning mechanisms (associative and non-associative) the mites are able to use early in life, which cues they learn and how different learning mechanisms affect adult foraging behaviors. Issue (2) seeks to unravel the ultimate costs and benefits of early learning, i.e. how early learning affects fitness-related life-history traits and whether learning and improved foraging on a given prey comes at the expense of being less flexible in exploiting other prey and in processing novel information later in life. Issue (3) aims at determining the population level consequences of early learning. How can early learning by predatory mites be exploited in biological control, how do early experiences with a given prey affect the predators` impact on target and non-target herbivorous mites and insects. It should be possible to create phenotypic lines of the predators experienced with a given prey or its cues, which should then perform better with this prey than nave predators do. The experimental work of the proposed project consists primarily of manipulative experiments at the individual and population levels. The spatial scale of the experiments ranges from small scale cages and arenas to whole plants, and plant groups. The core research will be accomplished by two PhD students and a MSc student. In an ideal case, this trans-disciplinary project shows how the knowledge gained in fundamental research can be translated into applied aspects. It breaks new scientific ground by linking comprehensive research on learning mechanisms, sensitive periods, memory persistence and adaptive significance, the cascading effects of learning to the population level and biological control. The findings of this proposal should have relevance beyond the model animals used, i.e. predatory mites, and considerably improve our understanding of early learning by arthropods in general.

This project pursued three major objectives: (i) scrutinizing and characterizing the early learning ability of foraging plant-inhabiting predatory mites; (ii) revealing the adaptive benefits of early learning and possible trade-offs arising from physiological and cognitive constraints; (iii) elucidating organizational cascades of individual learning to the population and community levels, which is relevant for biological control of herbivorous mite and insect pests. The project successfully met all three objectives. Ad (i) Our experiments revealed that predatory mites with generalist feeding habits, such as Amyblyseius swirskii and Neoseiulus californicus, have a sensitive window early in life where experience with a given prey species results in profound and persistent effects in foraging behavior later in life. Predators experiencing one type/species of prey or their cues early in life retain memory of this experience over two to three molting events into adulthood, allowing adult predators to recognize and attack familiar prey more quickly, and feed more and more efficiently on this prey. Both non-associative and associative learning types are at work. The learning ability of offspring is greatly influenced by the maternal food; purely plant-based maternal diet leads to degraded offspring learning ability. Ad (ii) Early learning allows a higher net energy gain per prey item, i.e. enhances prey profitability, which commonly translates into higher egg production by the predators, an adaptive benefit of learning. In contrast, first prey experience by adult predators produces mainly physiological effects. Maintenance of the ability to learn and the processes of learning are energetic costly and bind resources that could be used for other tissues, physiological and cognitive processes and life activities; physiological trade-offs were observed in longer developmental times of thrips-experienced predators, relative to nave ones, obviously because of energy allocated to consolidation of memory. Cognitive trade-offs were observed when the predators were challenged to attend to multiple stimuli during their early learning phase. Ad (iii) Early learning effects cascade up to the population and community levels, apparently by providing a head- start in population establishment and growth on plants infested by familiar target prey. Populations founded by thrips-experienced predators were more efficacious in suppressing herbivorous thrips on whole plants than populations founded by thrips-nave predators, ultimately enhancing plant fitness (more and heavier seeds). Together, the results of this project provide for important gains and scientific advance in both fundamental and applied aspects of early learning. Favorable experimental accessibility and manipulability, and a broad behavioral repertoire, render plant-inhabiting predatory mites extremely well-suited model organisms for addressing behavioral and ecological research topics. Their well-developed learning abilities, allowing to improve foraging on a target herbivorous pest, may well translate into improved mass-rearing and release strategies in biological control. The results of this project lay the foundation for future research endeavors addressing the potential and relevance of early life experiences to establishing and shaping mite personalities.