Adaptive significance of social familiarity in mites

Information about the social environment is essential when individuals frequently interact with each other such as in group-living animals. Consequently, the ability to recognize familiar individuals is widespread in the animal kingdom but the adaptive value accruing from familiarity is only poorly documented. A possible explanation for the importance of familiarity in group-living animals is provided by limited attention theory. Limited attention theory predicts that the efficiency in a single task is reduced if animals have to simultaneously process information from several tasks. Therefore, in group-living animals assorting with familiar individuals may be adaptive if it allows to focus attention to other behaviorsasks enhancing survival and reproduction. I here propose to investigate the adaptive significance of familiarity in the plant-inhabiting predatory mite Phytoseiulus persimilis in light of limited attention theory. Phytoseiulus persimilis is an ideal species for these investigations because it lives in groups and has recently been shown to discriminate familiar and unfamiliar conspecific individuals. I hypothesize that having familiar neighbors is adaptively advantageous for P. persimilis because familiar individuals require less attention, for example because of being less agonistic, than unfamiliar ones. Assorting with familiar individuals allows P. persimilis to target more attention to other behaviorsasks and increases their efficiency in foraging and anti-predation behavior. Optimized foraging and anti-predation behaviors are reflected in enhanced life history components such as growth, developmental speed and reproductive output. In consequence, familiarity should lead to better coordinated patch exploitation, an optimized interplay between patch residence and patch-leaving tendencies, and finally enhanced local population growth. To the best of my knowledge, such a wide array of major behavioral activities and life history components of a terrestrial animal has never been looked at from the perspective of familiarity and limited attention theory.

Group-living is a common phenomenon in the animal kingdom. In many group-living animals, within-group associations are determined by social familiarity, i.e. familiar individuals, independent of genetic relatedness, preferentially associate with each other. As a consequence, social familiarity may affect other major life activities of group-living animals such as foraging, reproduction and anti-predator behaviors. A scarcely experimentally tested explanation why social familiarity is beneficial for group-living animals is provided by limited attention theory. Limited attention theory postulates that focusing on a given task, such as inspection and assessment of group members, has cognitive and associated physiological and behavioral costs with respect to the attention paid to other tasks, such as predator vigilance or foraging. The interrelations between social familiarity and limited attention and their effects on major behavioral, life history and fitness traits have never been addressed in a group-living terrestrial invertebrate species. In our project, we assessed the influence of social familiarity on within-group association behavior, reproduction and development, foraging, dispersal and anti-predator behavior of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. Our experiments revealed that social familiarity is an important modulator of numerous behavioral and life history traits and influences every life stage looked at (larvae, nymphs, adult females). Both juvenile and adult familiar mites preferentially grouped together and preferentially joined groups of familiar individuals in choice situations. Familiar juveniles foraged more efficiently, i.e. needed less prey at similar developmental speed and body size at maturity than unfamiliar mites. Moreover, familiar females produced more eggs than unfamiliar females at similar predation rates. Familiar mites were also more exploratory and dispersed earlier from a given prey patch, occupied more prey patches, depleted prey more quickly and had higher survival chances than unfamiliar mites. Under predation risk, familiar larvae reacted more quickly to attacks by an intraguild predator, survived more predator encounters and survived longer than unfamiliar larvae. A common observation in almost every experiment was the significantly lower general activity of familiar mites. We argue, that lower general activity is an indicator of decreased restlessness, which, at the physiological level, reflects less stress, and, at the cognitive level, a reduced need to explore the immediate social surrounding, leading to lower energy expenditure for neighbor inspection and assessment and leaving more energy for other processes such as development and egg production. Furthermore, reduced stress makes it possible to shift attention from neighbor inspection to predator vigilance enhancing the survival of familiar mites in dangerous environments. Altogether, our comprehensive study is the first to experimentally document the linkage between the adaptive significance of social familiarity and the underlying cognitive processes of shared attention.