Learning is changed behavior following experience, and ubiquitous in animals including plant-inhabiting predatory mites (Phytoseiidae). Learning has many benefits but also incurs costs, which are only poorly understood. Here, we addressed learning, especially its costs, in the generalist predatory mite Amblyseius swirskii, a biocontrol agent of several herbivores, which can also survive on pollen. The goals of our research were (1) to scrutinize if A. swirskii is able to learn during early life in foraging contexts and, if so, (2) to determine the costs of early learning. In the experiments, we used one difficult-to-grasp prey, i.e., thrips, and one easy-to-grasp prey, i.e., spider mites. Our experiments show that A. swirskii is able to learn during early life. Adult predators attacked prey experienced early in life (i.e., matching prey) more quickly than they attacked unknown (i.e., non-matching) prey. Furthermore, we observed both fitness benefits and operating (physiological) costs of early learning. Predators receiving the matching prey produced the most eggs, whereas predators receiving the non-matching prey produced the least. Thrips-experienced predators needed the longest for juvenile development. Our findings may be used to enhance A. swirskii’s efficacy in biological control, by priming young predators on a specific prey early in life.

Animals are commonly exposed to multiple environmental stimuli, but whether, and under which circumstances, they can attend to multiple stimuli in multitask learning challenges is elusive. Here, we assessed whether simultaneously occurring chemosensory stimuli interfere with each other in a dual-task learning challenge. We exposed predatory mites Neoseiulus californicus early in life to either only conspecifics (kin) or simultaneously conspecifics (kin) and food (thrips or pollen), to determine whether presence of food interferes with social familiarization and, vice versa, whether presence of conspecifics interferes with learning the cues of thrips. We found that N. californicus can become familiar with kin early in life and use kin recognition later in life to avoid kin cannibalism. However, when the juvenile predators were challenged by multiple stimuli associated with two different learning tasks, that is, when they grew up with conspecifics in the presence of food, they were no longer capable of social familiarization. In contrast, the presence of conspecifics did not compromise the predators' ability to learn the cues of thrips. Memory of experience with thrips allowed shorter attack latencies on thrips and increased oviposition by adult N. californicus. Proximately, the stimuli for learning the features of thrips were apparently more salient than those for learning to recognize kin. We argue that, ultimately, learning the cues of thrips at the expense of impeded social familiarization pays off because of negligible cannibalism risk in the presence of abundant food. Our study suggests that stimulus-driven prioritization of learning tasks is in line with the predictions of selective and limited attention theories, and provides a key example of interference in dual-task learning by an arthropod.

The ability to learn is ubiquitous in animals but highly variable within and between species, populations and individuals. Diet-related circumstances, such as diet quantity and quality can influence both long-term constitutive (genetic; by selection) and short-term operational (non-genetic; by the immediate circumstances) learning performance. Here, we scrutinized the causes of loss of learning ability, following multi-generational feeding on pollen, in a line of the predatory mite Amblyseius swirskii, which was previously well able to learn prey during early life, enhancing foraging later in life. We investigated whether, and, if so, how quickly, a transgenerational diet switch to live prey restores the early learning ability of foraging predatory mites. The first experiment shows that the early learning ability was restored after switching the diet of the pollen-fed predator line to live spider mites for two generations before conducting the behavioral assay. The second experiment reveals that offspring regained their learning ability if the diet of their mothers was switched from pollen to spider mites for 3 or 10 days before offspring production. Both experiments in concert suggest transgenerational, pollen-induced operational loss of learning ability in the predatory mite A. swirskii. Maternally-transmitted nutrient deficiency and/or maternally-induced epigenetic changes are the most plausible explanations for the pollen diet-induced loss of learning ability. Our study represents a key example for maternal diet-induced variation in learning ability.

Behavioural plasticity can be categorized into activational (also termed contextual) and developmental plasticity. Activational plasticity allows immediate contextual behavioural changes, whereas developmental plasticity is characterized by time-lagged changes based on memory of previous experiences (learning). Behavioural plasticity tends to decline with age but whether this holds true for both plasticity categories and the effects of first-in-life experiences is poorly understood. We tackled this issue by assessing the foraging plasticity of plant-inhabiting predatory mites, Amblyseius swirskii, on thrips and spider mites following age-dependent prey experience, i.e. after hatching or after reaching maturity. Juvenile and young adult predator females were alternately presented thrips and spider mites, for establishing 1st and 2nd prey-in-life experiences, and tested, as gravid females, for their foraging plasticity when offered both prey species. Prey experience by juvenile predators resulted in clear learning effects, which were evident in likelier and earlier attacks on familiar prey, and higher proportional inclusion of familiar prey in total diet. First prey-in-life experience by juvenile but not adult predators resulted in primacy effects regarding attack latency. Prey experience by adult predators resulted mainly in prey-unspecific physiological changes, with easy-to-grasp spider mites providing higher net energy gains than difficult-to-grasp thrips. Prey experience by juvenile, but not adult, predators was adaptive, which was evident in a negative correlation between attack latencies and egg production. Overall, our study provides key evidence that similar experiences by juvenile and adult predators, including first-in-life experiences, may be associated with different types of behavioural plasticity, i.e. developmental and activational plasticity.

Scientific Reports 6: Article number: 23571; published online: 23 March 2016; updated: 01 March 2018 This Article contains an error in Figure 1 where the labelling within the ‘matching prey’ bars were inverted. The correct Figure 1 appears below.