Environmental stressors during early life may have persistent consequences for phenotypic development and fitness. In group-living species, an important stressor during juvenile development is the presence and familiarity status of conspecific individuals. To alleviate intraspecific conflicts during juvenile development, many animals evolved the ability to discriminate familiar and unfamiliar individuals based on prior association and use this ability to preferentially associate with familiar individuals. Assuming that familiar neighbours require less attention than unfamiliar ones, as predicted by limited attention theory, assorting with familiar individuals should increase the efficiency in other tasks. We assessed the influence of social familiarity on within-group association behaviour, development and foraging of juvenile life stages of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. The observed groups consisted either of mixed-age familiar and unfamiliar juvenile mites or of age-synchronized familiar or unfamiliar juvenile mites or of pairs of familiar or unfamiliar larvae. Overall, familiar mites preferentially grouped together and foraged more efficiently, i.e. needed less prey at similar developmental speed and body size at maturity, than unfamiliar mites. Preferential association of familiar mites was also apparent in the inter-exuviae distances. Social familiarity was established by imprinting in the larval stage, was not cancelled or overridden by later conspecific contacts and persisted into adulthood. Life stage had an effect on grouping with larvae being closer together than nymphal stages. Ultimately, optimized foraging during the developmental phase may relax within-group competition, enhance current and future food supply needed for optimal development and optimize patch exploitation and leaving under limited food.
BackgroundSocial familiarity, which is based on the ability to recognise familiar conspecific individuals following prior association, may affect all major life activities of group-living animals such as foraging, reproduction and anti-predator behaviours. 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 unfamiliar group members, has cognitive and associated physiological and behavioural costs with respect to the attention paid to other tasks, such as anti-predator vigilance and response. Accordingly, we hypothesised that social familiarity enhances the anti-predator success of group-living predatory mites, Phytoseiulus persimilis, confronted with an intraguild predator, the predatory mite Amblyseius andersoni.Methodology/Principal FindingsWe videotaped and analysed the response of two P. persimilis larvae, held in familiar or unfamiliar pairs, to attacks by a gravid A. andersoni female, using the behavioural analyses software EthoVision Pro®. Familiar larvae were more frequently close together, reacted more quickly to predator attacks, survived more predator encounters and survived longer than unfamiliar larvae.SignificanceIn line with the predictions of limited attention theory, we suggest that social familiarity improves anti-predator behaviours because it allows prey to shift attention to other tasks rather than group member assessment.
In many group-living animals, within-group associations are determined by familiarity, i.e. familiar individuals, independent of genetic relatedness, preferentially associate with each other. The ultimate causes of this behaviour are poorly understood and rigorous documentation of its adaptive significance is scarce. Limited attention theory states that focusing on a given task has interrelated cognitive, behavioural and physiological costs with respect to the attention paid to other tasks. In multiple signal environments attention has thus to be shared among signals. Assuming that familiar neighbours require less attention than unfamiliar ones, associating with familiar individuals should increase the efficiency in other tasks and ultimately increase fitness. We tested this prediction in adult females of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. We evaluated the influence of social familiarity on within-group association behaviour, activity, predation and reproduction. In mixed groups (familiar and unfamiliar), familiar predator females preferentially associated with each other. In pure groups (either familiar or unfamiliar), familiar predator females produced more eggs than unfamiliar females at similar predation rates. Higher egg production was correlated with lower activity levels, indicating decreased restlessness. In light of limited attention theory, we argue that the ability to discriminate between familiar and unfamiliar individuals and preferential association with familiar individuals confers a selective advantage because familiar social environments are cognitively and physiologically less taxing than unfamiliar social environments.
The social environment early in life is a key determinant of developmental, physiological and behavioural trajectories across vertebrate and invertebrate animals. One crucial variable is the presence/absence of conspecifics. For animals usually reared in groups, social isolation after birth or hatching can be a highly stressful circumstance, with potentially long-lasting consequences. Here, we assessed the effects of social deprivation (isolation) early in life, that is, absence of conspecifics, versus social enrichment, that is, presence of conspecifics, on developmental time, body size at maturity, mating behaviour and group-living in the plant-inhabiting predatory mite Phytoseiulus persimilis. Socially deprived protonymphs developed more slowly and were less socially competent in grouping behaviour than socially enriched protonymphs. Compromised social competence in grouping behaviour was evident in decreased activity, fewer mutual encounters and larger interindividual distances, all of which may entail severe fitness costs. In female choice/male competition, socially deprived males mated earlier than socially enriched males; in male choice/female competition, socially deprived females were more likely to mate than socially enriched females. In neither mate choice situation did mating duration or body size at maturity differ between socially deprived and enriched mating opponents. Social isolation-induced shifts in mating behaviour may be interpreted as increased attractiveness or competitiveness or, more likely, as hastiness and reduced ability to assess mate quality. Overall, many of the social isolation-induced behavioural changes in P. persimilis are analogous to those observed in other animals such as cockroaches, fruit flies, fishes or rodents. We argue that, due to their profound and persistent effects, early social deprivation or enrichment may be important determinants in shaping animal personalities.
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