Spontaneous yawning and scratching are common fixed action patterns that are relatively widespread among vertebrates1. First, yawning can have a strong physiological component2, and its occurrence can increase when individuals are aroused or need to facilitate thermoregulation and brain oxygenation3,4. However, according to the social-communicative hypothesis, yawning also conveys information about the internal or emotional state of the yawner, which can be used by other group members to adjust their behavioral response5,6. Second, spontaneous scratching is the mechanical result of the unpleasant itch sensation7, and can be influenced by both physical and psychological factors, including anxiety8. Through scratching, individuals can alleviate the sensation of itchiness9, and the enjoyable feeling produced by scratching can reinforce and encourage further scratching behavior9.
Intriguingly, both scratching and yawning can trigger behavioral contagion, which is the propensity to show a behavior after observing it displayed (i.e. trigger event) by another individual (i.e. model), so that the behavior can spread among individuals10–11. From a functional perspective, behavioral contagion might increase individual fitness by facilitating individuals’ synchronization, which can in turn foster group coordination and effective defense against predators12–13. While spontaneous yawning and scratching are common, contagious yawning and scratching seem to be present in only few species14.
Contagious yawning takes place when a model yawns, causing another group member to also yawn15. This phenomenon has been observed in several species16, mainly in the ones living in complex social groups (e.g. often engaging in cooperative interactions17, being highly prosocial18, showing high levels of fission-fusion dynamics19). Evidence of contagious yawning has been for instance found in budgerigars (Melopsittacus undulates)20, a social bird from Australia, and in mammals like sheep (Ovis aries)21, wolves (Canis lupus)22, domesticated dogs (Canis lupus familiaris)23, elephant seals (Mirouga leonina)24, domestic pigs (Sus scrofa)16, wild lions (Panther leo)1 and African elephants (Loxodonta africana)25. Among primates, studies have primarily focused on Catarrhines species. For instance, contagious yawning has been observed in orangutans (Pongo spp.)14, bonobos (Pan paniscus)18,26, chimpanzees (Pan troglodytes)27,28, stump-tailed macaques (Macaca arctoides)29, wild geladas (Theropithecus gelada)30 and humans (Homo sapiens)31, although there is yet no evidence of contagious yawning in lowland gorillas (Gorilla gorilla gorilla)32. More recently, contagious yawning has been shown also in primates other than Catarrhines, including Platyrrhines (i.e. spider monkeys, Ateles geoffroyi)33 and Strepsirrhines (i.e. indri lemurs, Indri indri)13. In Strepsirrhines, in particular, behavioral contagion has long been thought to be absent. In the first study on lemurs, Reddy and colleagues (2016)17 detected no contagious yawning in ring-tailed lemurs (Lemur catta) and red ruffed lemurs (Varecia rubra), when using video stimuli as trigger events, and suggested that contagious yawning might have evolved in the common ancestor of Catarrhines and Platyrrhines after the lineage split from Strepsirrhines. However, Valente and colleagues (2022)13 recently found evidence of contagious yawning in wild indri lemurs, with individuals being more likely to yawn after observing a trigger event.
As for yawning, scratching can also be contagious34. In humans, for instance, scratching can be triggered by hearing the word "itching" or the sound associated with itching, as well as by witnessing others scratching9,35,36. Previous studies have shown that videos or pictures of people scratching can induce scratching behavior in healthy individuals35. Besides humans, contagious scratching has been observed in few other species, including rhesus macaques (Macaca mulatta)37, Japanese monkeys (M. fuscata)38, Tibetan macaques (M. thibetana)39 and spider monkeys33. A study on mice, instead, failed to detect contagious scratching40.
Several studies have also identified factors that might modulate behavioral contagion. For some authors, behavioral contagion is linked to empathy and to the ability to align to others’ internal states, and it may thus be higher between kin or individuals that have close social bonds14,17,28,41,42. In line with this, humans are more likely to yawn after close friends or family members yawn43, and bonobos and geladas are more likely to yawn when triggers are kin or close social partners18,44. Similarly, in wild Indri indri, individuals that more often groom with each other are also more likely to show contagious yawning13, and chimpanzees are more likely to yawn after observing yawning by group members rather than outgroup members28. Other authors, however, contend that behavioral contagion is more frequent among close friends and family members because of higher selective visual attention paid to individuals that are more relevant to the observer (attentional bias hypothesis)41,42. If this is true, behavioral contagion should be more frequent not only when models are kin or close social partners, but also when they play a relevant social function in the group (i.e. highly ranking or socially integrated group members). In chimpanzees, for instance, there is evidence that male models are more likely to trigger contagious yawning than females, especially when they are dominant46.
Despite numerous studies on the mechanisms and the physiological and social effects of behavioral contagion, its evolutionary origins remain unclear. Although some studies suggest that behavioral contagion should be present only in highly social species and may have appeared only recently in vertebrate evolution17,42, recent evidence of behavioral contagion in other taxa challenges this hypothesis13,33. In this study, we aimed to investigate the presence of behavioral contagion in two captive groups of Strepsirrhines characterized by complex sociality (i.e. high levels of fission-fusion dynamics, alarm/call synchronization, cooperative nest-sharing, communally infant care)47–50: black-and-white ruffed lemur (Varecia variegata) and red ruffed lemurs (Varecia rubra). We predicted that individuals would be more likely to yawn or scratch after observing a conspecific yawning or scratching, rather than if they did not observe such trigger event (Prediction 1). Furthermore, according to the attentional bias hypothesis, more dominant and socially integrated individuals may be more relevant to the observers41 and thus more likely to trigger behavioral contagion. Therefore, we predicted that behavioral contagion would be more likely triggered by higher-ranking and more socially integrated models, than by lower-ranking and less socially integrated ones (Prediction 2).