Marmosets mutually compensate for differences in rhythms when coordinating vigilance

Synchronization is widespread in animals, and studies have often emphasized how this seemingly complex phenomenon can emerge from very simple rules. However, the amount of flexibility and control that animals might have over synchronization properties, such as the strength of coupling, remains underexplored. Here, we studied how pairs of marmoset monkeys coordinated vigilance while feeding. By modeling them as coupled oscillators, we noted that (1) individual marmosets do not show perfect periodicity in vigilance behaviors, (2) nevertheless, marmoset pairs started to take turns being vigilant over time, a case of anti-phase synchrony, (3) marmosets could couple flexibly; the coupling strength varied with every new joint feeding bout, and (4) marmosets could control the coupling strength; dyads showed increased coupling if they began in a more desynchronized state. Such flexibility and control over synchronization require more than simple interaction rules. Minimally, animals must estimate the current degree of asynchrony and adjust their behavior accordingly. Moreover, the fact that each marmoset is inherently non-periodic adds to the cognitive demand. Overall, our study provides a mathematical framework to investigate the cognitive demands involved in coordinating behaviors in animals, regardless of whether individual behaviors are rhythmic or not.Author summary: Research suggests that synchronized animal behaviors often emerge from simple interaction rules. Mathematical models have been instrumental in revealing these underlying rules. Here, we employed mathematical modeling to study how marmoset monkeys coordinate vigilance and feeding behaviors in a situation where doing both actions simultaneously is not possible. We found that pairs of marmosets progress to a state where they show opposite behaviors, i.e., when one individual is feeding, the other is vigilant, and vice-versa. In order to achieve such coordinated state, the individuals must influence each other’s behaviors, i.e., couple. We found that marmosets can couple flexibly and that they couple more strongly if they are initially out-of-sync with their partner. Such ability to detect the current state of synchrony and adapt behavior accordingly is cognitively demanding. Our research thus demostrates that animals with more complex cognitive abilities can do much more than following simple interaction rules to synchronize with other individuals. Overall, our research (1) establishes marmosets as a strong candidate species for studying the cognitive aspects of social timing, (2) provides a novel mathematical framework that is tailored for studying synchronization in biological systems, and (3) underlines the implications of synchrony for marmosets and other animals.