Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
http://www.baillement.com

mystery of yawning 

 

 

mise à jour du
25 avril 2002
Animal Behavior
12022;187:209e219
The causes and consequences
aof yawning in animal groups
Andrew C. Gallup
a Psychology and Evolutionary Behavioral Sciences Programs,
SUNY Polytechnic Institute, Utica, NY, U.S.A.
b Department of Biological Sciences, Nova Southeastern University
Ft Lauderdale, FL, U.S.A. 
 

Chat-logomini

 
Abstract
 
Yawning is a stereotyped action pattern that is prevalent across vertebrates. While there is growing consensus on the physiological functions of spontaneous yawning in neurovascular circulation and brain cooling, far less is known about how the act of yawning alters the cognition and behavior of observers. By bridging and synthesizing a wide range of literature, this review attempts to provide a unifying framework for understanding the evolution and elaboration of derived features of yawning in social vertebrates. Recent studies in animal behavior, psychology and neuroscience now provide evidence that yawns serve as a cue that improves the vigilance of observers, and that contagious yawning functions to synchronize and/or coordinate group activity patterns. These social responses to yawning align with research on the physiological significance of this behavior, as well as the ubiquitous temporal and contextual variation in yawn frequency across mammals and birds. In addition, these changes in mental processing and behavior resulting from the detection of yawning in others are consistent with variability in the expression of yawn contagion based on affinity and social status in primates. Topics for further research in these areas are discussed.
 
Résumé
 
Le bâillement est un comportement stéréotypé chez tous les vertébrés. Si l'on s'accorde de plus en plus sur les fonctions physiologiques du bâillement spontané dans la circulation neuro-vasculaire et le refroidissement du cerveau, on en sait beaucoup moins sur la façon dont l'acte de bâiller modifie la cognition et le comportement des observateurs. En reliant et en synthétisant un large éventail de littérature, cette revue tente de fournir un cadre unifié pour comprendre l'évolution et l'élaboration des caractéristiques dérivées du bâillement chez les vertébrés sociaux. Des études récentes sur le comportement animal, la psychologie et les neurosciences prouvent aujourd'hui que les bâillements servent d'indice pour améliorer la vigilance des observateurs, et que les bâillements contagieux ont pour fonction de synchroniser et/ou de coordonner les modèles d'activité de groupe. Ces réponses sociales au bâillement s'alignent sur les recherches concernant la signification physiologique de ce comportement, ainsi que sur la variation temporelle et contextuelle omniprésente de la fréquence des bâillements chez les mammifères et les oiseaux. En outre, ces changements dans le traitement mental et le comportement résultant de la détection du bâillement chez les autres sont cohérents avec la variabilité dans l'expression de la contagion du bâillement basée sur l'affinité et le statut social chez les primates. Des sujets pour des recherches ultérieures dans ces domaines sont discutés.
Tous les articles d'Andrew Gallup
Tous les articles sur la contagion du bâillement
All articles about contagious yawning

 
Yawning is considered a stereotyped or fixed action pattern and appears to have similar within-species duration, interval and variability (Provine, 1986). Characterized by a three-phase response, yawns are defined by an involuntary and powerful gaping of the jaw, a temporary period of peak muscular contraction with head titling and eye closure and a passive closure of the jaw (Barbizet, 1958). Among terrestrial vertebrates, the first two phases of this response often include a deep inhalation of air, while the third phase is accompanied by a shorter expiration. Yawning and similar yawn-like gaping behaviors are conspicuous in nature and have been documented within all classes of vertebrates (e.g. Baenninger, 1987; Craemer, 1924; Luttenberger, 1975; Rasa, 1971; Sauer & Sauer, 1967). The omnipresence of this behavior across diverse species and lineages suggests that it is phylogenetically old and likely evolved with the emergence of jawed fishes.
 
The widespread nature of spontaneous, or nonsocial, yawning suggests it is an adaptation that holds important functionality. In fact, Charles Darwin even contemplated the conserved nature of yawning among humans and nonhuman animals in formulating his theory of natural selection (Darwin, 1987). Yet, clearly the mere pervasiveness of a trait both within and across species does not imply functional significance, since it could represent a by-product or spandrel (Gould & Lewontin, 1979). For yawning, however, the case for adaptation becomes stronger when considering its hedonistic properties (Provine, 1986), the risks for subluxation of the jaw (Tesfaye & Lal, 1990) and associated costs of drawing unwanted attention, momentarily decreasing alertness and/or conflicting with immediate anti-predatory behaviors (Miller et al., 2010). Moreover, recent neurological studies provide further support for an adaptive significance to this behavior (Gallup, Church, & Pelegrino, 2016). In particular, recent phylogenetically controlled analyses from >100 species of birds and mammals revealed robust positive correlations between yawn duration and brain mass and overall and cortical/pallium neuron totals (Massen et al., 2021). These findings demonstrate a link between yawn duration and brain size and complexity that cannot be explained by allometry alone, indicating yawns likely serve an important neurophysiologic function that has been conserved across amniote evolution.
 
Studies examining the ultimate mechanisms of yawning typically focus on roles either in physiology or in social behavior (Guggisberg et al., 2010). Instead of one or the other, however, emerging research indicates that yawning holds both physiological and social functionality. That said, the ubiquity of yawning across lineages, within nonsocial animals and during periods of seclusion leads to the conclusion that the primitive feature of this behavior is physiologic. Accordingly, any social roles of yawning in gregarious species would represent a more recently derived feature of this trait, built upon the original neurophysiological function(s) shared across vertebrates (Gallup, 2011). This perspective can be further
illustrated when comparing spontaneous yawns, which are generated by internal changes in physiology, with contagious yawns, which are triggered socially by sensing the yawns of others. By definition, every contagious yawn can be traced back to an original spontaneous yawn, and thus contagious yawning must have evolved more recently in time. Further lines of evidence also lead to the same conclusion. Spontaneous yawning is ubiquitous among vertebrates (Baenninger, 1987; Massen et al., 2021), appears to be a universal act within a given species (Walusinski, 2018) and begins early on during embryological development (de Vries et al., 1982). These features all indicate that spontaneous yawning holds basic and important functionality that is not social. Conversely, contagious yawning has only been documented in social species (Massen & Gallup, 2017; Palagi et al., 2020), shows individual variability in expression (humans, Homo sapiens: Provine, 1986; chimpanzees, Pan troglodytes: Anderson et al., 2004) and does not develop until after infancy (humans: Cordoni et al., 2021; Millen & Anderson, 2011; chimpanzees: Madsen et al., 2013; domesticated dogs, Canis lupus familiaris: Madsen & Persson, 2013). Collectively, these lines of evidence suggest a more recent phylogenetic origin for yawn contagion.
 
This review will highlight the current scientific understanding of the ways in which yawns alter the cognition of observers and facilitate changes in group dynamics across diverse species, as well as offer suggestions for future investigation in these areas. In particular, various lines of research will be presented that reveal adaptive outcomes to (1) the mere detection of yawns as well as (2) subsequent yawn contagion. In both cases, it is essential to understand the underlying physiological causes and consequences of spontaneous yawning. First, when it comes to yawn detection, the internal changes that initiate this behavior in the actor are what determines the information that is transmitted to receivers. In other words, the way yawns change the behavior of observers hinges upon what they reveal about the internal state of the yawner. Second, when it comes to contagious yawns, an under- standing of the biological significance of this motor action pattern is essential to appreciate how its propagation via contagion may then go on to alter subsequent behavior of the collective. Not only do spontaneous and contagious yawns share a similar morphology (i.e. they appear indistinguishable from one another), but based on the cumulative properties of evolution, we should expect that they also share similar fundamental mechanistic and perhaps functional properties. Accordingly, the factors known to trigger spontaneous yawns should have a similar effect on yawn contagion. This view is supported by psychological research showing that the expression of contagious yawning can be effectively modulated by the same physiological variables known to modulate spontaneous yawning. These include circadian factors (Gallup et al., 2021; Giganti & Zilli, 2011), cooling and warming of the brain via temperature manipulations to the neck and skull (Gallup & Gallup, 2007; Ramirez et al., 2019), ambient temperature variation (e.g. Eldakar et al., 2015; Massen et al., 2014) and stressful situations (Eldakar et al., 2017). Therefore, prior to focusing on the social nature of yawning, I discuss the literature on the physiology, contexts and environ- mental triggers of spontaneous yawning.
 
FUNCTION(S) OF SPONTANEOUS YAWNING
Numerous hypotheses have been proposed to explain the physiological significance of yawning (e.g. Smith, 1999), but most lack empirical support or have been falsified. This includes the common, but incorrect, assertion that yawning functions to equilibrate blood oxygen levels. Through a series of elegant experiments on human subjects, Provine, Tate, et al. (1987) demonstrated that yawn frequency is not altered by breathing enhanced or decreased levels of O2 or CO2, and physical exercise sufficient to double breathing rates had no effect on yawning. It has therefore been concluded that yawning and breathing are controlled by different mechanisms, and it is now widely accepted in the scientific liter- ature that respiration is not a necessary component of yawning (Corey et al., 2012; Guggisberg et al., 2010). These conclusions also align with recent research showing that yawn-like behavior of common bottlenose dolphins, Tursiops truncatus, occurs in the absence of breathing (Enokizu et al., 2021).
 
Instead, studies suggest that yawning functions to facilitate state change (Provine, 1986, 2005) and increase arousal (Greco & Baenninger, 1991; Matikainen & Elo, 2008; Walusinski, 2006). The state change hypothesis has shown to be a powerful framework for understanding this behavior, as yawns are by far most frequent during changes in state associated with behavioral transitions, such as from sleeping to waking, from waking to sleeping and from fluctuations of attentiveness and boredom, and even sexual arousal (Provine, 2005). Related to the switching of activity patterns, yawns commonly occur in anticipation of important events and tend to be followed by an arousing effect both behaviorally and physiologically (reviewed by Baenninger, 1997). In addition, laboratory studies have shown that electrical and chemical stimulation of the paraventricular nucleus of the hypothalamus, the brain area that controls yawning (Argiolas & Melis, 1998; Melis et al., 1987), evokes both yawning and cortical arousal in Wistar rats (Sato-Suzuki et al., 1998; Seki et al., 2002). Mechanistically, state change and arousal could be achieved through the acceleration of heart rate, intracranial circulation and cerebrospinal fluid flow produced by the deep inhalation and powerful stretching of the jaw during yawning (Askenasy, 1989; Matikainen & Elo, 2008; Schroth & Klose, 1992; Walusinski, 2014).
 
Given the rise in yawn frequency prior to sleep onset (e.g. Provine, Hamernik, et al., 1987; Zilli et al., 2007), however, it be- comes clear that not all yawns result in increased arousal. Although yawning consistently precedes initial increases in motor activity (Baenninger et al., 1996) and skin conductance (Greco & Baenninger, 1991), subsequent changes in arousal and alertness from this behavior may be governed by circadian factors. This perspective can potentially explain differences in the neurological effects documented after yawns in humans as measured by elec- tro-encephalography. For example, during the intravenous induction of general anaesthesia, which produces a controlled loss of awareness during an otherwise active state, yawns are frequently observed and induce counteracting spikes in arousal (Kasuya et al., 2005). Among individuals experiencing excessive sleepiness, however, yawns occur during periods of progressive drowsiness and sleep pressure but fail to produce increases in arousal (Guggisberg et al., 2007). Therefore, while yawning is consistently triggered during low vigilance, it may be that increases in arousal from this action pattern occur primarily during waking and active states rather than during periods of sleepiness/fatigue prior to resting or sleep onset.
 
More recent research provides evidence for a thermoregulatory function to yawning in homeotherms (Gallup & Gallup, 2007, 2008). This hypothesis proposes that yawns function to cool the brain, which in turn could improve alertness and mental processing efficiency of the yawner. Accordingly, yawns should be triggered by initial rises in brain temperature and the action pattern of yawning should function as a compensatory brain cooling mechanism by promoting increased cerebral blood flow, ventilation of the sinus system and countercurrent heat exchange with the ambient air (reviewed by Gallup & Eldakar, 2013). Consistent with these pre- dictions, laboratory studies on humans, rodents and birds show that yawns are preceded by rises in brain/skull temperature and that, following the execution of this behavior, temperatures
decrease significantly (Eguibar et al., 2017; Gallup & Gallup, 2010; Gallup et al., 2017; Shoup-Knox et al., 2010). Moreover, the manipulation of brain temperature in humans has recently been shown to produce predicted changes in yawn frequency (Ramirez et al., 2019). In addition, consistent with the view that yawning evolved a brain cooling function, comparative studies on humans (Massen et al., 2014), nonhuman primates (Macaca fascicularis: Deputte, 1994; Cebus capucinus: Campos & Fedigan, 2009), rats (Rattus norvegicus: Gallup et al., 2011) and birds (Melopsittacus undulatus: Gallup et al., 2009, 2010) all show that yawn frequency can be reliably manipulated by changes in ambient temperature.
 
CONTEXTS OF SPONTANEOUS YAWNING
Consistent with the aforementioned physiological significance of yawning, a large number of comparative studies have revealed similar contexts and behavioral changes that accompany yawns across diverse species that relate to state change, arousal and thermoregulation. In particular, this includes the close temporal connection between sleeping and waking, activity patterns and stress.
 
Circadian Variation and Behavioral Transitions
The most well-documented feature of yawning across different species is its link to circadian changes in sleep and activity. Studies in humans consistently show a bimodal distribution in yawn fre- quency during the day, with an initial rise in the rate of yawning shortly after waking in the morning and a larger increase in yawn frequency in the evening prior to sleep onset (Baenninger et al., 1996; Giganti et al., 2010; Provine, Hamernik, et al., 1987; Giganti & Zilli, 2011; Zilli et al., 2007, 2008). Consistent with links to drowsiness, human yawns are also more common during periods of boredom and/or low levels of stimulation (Provine & Hamernik, 1986). In addition to showing clear connections to state change and modified arousal, changes in yawn frequency before and after sleeping correlate strongly with circadian fluctuations in brain/ body temperature (Landolt et al., 1995).
 
Similar temporal patterns of yawning are observed in wild nonhuman primates, including grey-cheeked mangabeys, Lophocebus albigena, and crab-eating macaques, M. fascicularis, where pre- and post-sleep yawning peaks occur throughout the day (Deputte, 1994). Analogous patterns are also observed in Sprague Dawley rats in the laboratory, whereby yawns occur with greatest frequency during transitional sleep/wake phases (Anias et al., 1984). In captive chimpanzees, one study found that nearly all in- stances of yawning (98.2%) occurred during periods of rest while sitting and lying down (Vick & Paukner, 2010). Yawning also commonly occurs under similar contexts in sea lions (Otaria flavescens) (Palagi, Guille_n-Salazar, et al., 2019) and has been linked with sleep or recumbency periods in African elephants, Loxodonta africana (Rossman et al., 2017).
 
Yawning appears to be driven by similar circadian factors in birds as well. In the South African ostrich, Struthio camelus australis, for example, it is noted that yawning occurs just prior to sleeping/ resting and again when a rest has been interrupted (Sauer & Sauer, 1967). In captive budgerigars, M. undulatus, the temporal variation in yawning also varies across the day and is frequent in the evening prior to sleep onset (Miller, Gallup, Vogel, Vicario, et al., 2012).
 
Based on the circadian factors that influence yawning and the purported arousing function of yawns (Baenninger, 1997), this behavior has also been noted to precede increases in activity levels across taxa. In preterm human infants, yawns appear to increase behavioral arousal and predict higher motoric activation (Giganti et al., 2002). Similarly, among young adults (e.g. college students), instances of yawning seem to be unvaryingly followed by an increase in activity (as measured by wrist movement) (Baenninger et al., 1996). Likewise, an increase in locomotion within the first few minutes after yawning has been documented in both captive chimpanzees (Vick & Paukner, 2010) and bottlenose dolphins (Enokizu et al., 2021). Yawning is also common during varied behavioral transitions in wild populations of ringtailed lemurs, Lemur catta, and white sifaka, Propithecus verreauxi (Zannella et al., 2015). Analogously, yawns occur primarily upon arousal from recumbency in African elephants (Rossman et al., 2017) and alongside new phases in activity among South African ostriches (Sauer & Sauer, 1967).
 
Stress and Anxiety
Yawning also tends to increase during and following periods of stress across diverse species. Stressful situations naturally elicit changes in mental state and arousal, and among varied physio- logical effects, stress produces rises in bodily temperature (i.e. stress-induced hyperthermia: Olivier et al., 2003; Zethof et al., 1994). In humans, increases in yawning have been observed lead- ing up to stressful and anxiety-provoking events, such as in para- troopers prior to their first free-fall, musicians waiting to perform and Olympic athletes prior to competition (Provine, 2005). Among nonhuman primates, yawning and other self-directed behaviors (e.g. scratching, self-grooming) are considered an indicator of psychosocial stress and anxiety (Maestripieri et al., 1992). In female olive baboons, Papio anubus, for example, self-directed behaviors like yawning increase substantially when the closest neighbour is dominant compared to subordinate (Castles et al., 1999). For wild chimpanzees, yawning has been noted to increase in the presence of humans (Goodall, 1968) as well as following vocalizations from neighbouring groups of conspecifics (Baker & Aureli, 1997). Simi- larly, a positive correlation has been observed between yawn frequency and aggressive behavior in Przewalski horses, Equus ferus przewalskii (Gorecka-Bruzda et al., 2016). Yawning also increases following nonsocial stressors. In strepsirrhine primates, yawns in- crease following alarm calls or after predator attacks (Zannella et al., 2015), and fear conditioning trials have been shown to induce yawning in Wistar rats (Kubota et al., 2014).
 
A combination of experimental and observational studies across a diverse array of mammals and birds have revealed a distinct temporal relationship between the onset of stress and the associ- ated yawning response (Demuru & Palagi, 2012; Eldakar et al., 2017; Fenner et al., 2016; Liang et al., 2015; Miller et al., 2010; Miller, Gallup, Vogel, & Clark, 2012; Moyaho & Valencia, 2002). For example, in a study of captive budgerigars, yawns were measured over a 1 h period following handling restraint (Miller et al., 2010). In the first 20 min following this encounter, yawning was relatively infrequent (~1.5 M yawns/h), but in the next 20 min, yawn frequency more than tripled (>5 yawns/h). Moreover, yawn latency was negatively correlated with body temperature increases due to handling, i.e. birds that were more hyperthermic yawned sooner. In a separate study on wild Nadza boobies, Sula granti, yawning was measured in adult birds during and after a comparable human capture-restraint stressor (Liang et al., 2015). Similar to budgerigars, booby yawns were absent during the stressor itself and remained at low frequency from 0 to 30 min following release (median 14 0) before increasing significantly 30e60 min thereafter (median 14 2). Lastly, in a study on humans, Eldakar et al. (2017) examined the impact of an acute physical stressor (cold pressor test) on contagiously triggered yawning. Analogous to the avian research, yawns were infrequent immediately following the stressor, but 20min thereafter both the overall frequency of yawning and the number of participants that yawned at least once during testing doubled. Taken together, these findings appear to reveal a homologous temporal effect regarding the relationship between yawning and acute physical stress in birds and mammals, whereby yawning is inhibited during stressors, but then becomes potentiated thereafter.
 
THE DETECTION OF YAWNS IN OTHERS
Atop the physiological significance of yawning, researchers have long posited additional social functions to this behavior (Deputte, 1994; Leone et al., 2014; Moyaho et al., 2017; Sauer & Sauer, 1967). In particular, it was initially suggested that, among primates, yawns preceded by a social interaction could provide a communicative function to conspecifics (Bolwig, 1959). In order to function in this capacity, however, yawns must be detected and distinguished from background noise by receivers (Wiley, 2006). In support of this view, recent neurological research shows that human infants as young as 5 months old can discriminate yawning from other types of mouth movements (Tsurumi et al., 2019). Using functional near- infrared spectroscopy, the presentation of yawning stimuli produced a significantly increased haemodynamic response at the superior temporal sulcus, as measured by the concentration of oxyhaemoglobin. This work indicates that the neural mechanism underlying the processing of yawning movements develops very early on in humans e at about the same time infants begin to discriminate emotional facial expressions (Kotsoni et al., 2001; LaBarbera et al., 1976) e suggesting that the detection of yawns in conspecifics is biologically important.
 
Given the close relation to sleeping, it has been proposed that yawns serve as a paralingual signal for drowsiness in humans (Provine, Hamernik, et al., 1987). As yawns are also noted during states of hunger and psychological stress in nonhuman primates, Deputte (1994) suggested that yawning could be viewed as an indicator of 'uneasiness' similar to other self-directed behaviors. More recently, in an attempt to account for the varied contexts and situations in which yawning is elicited, Guggisberg et al. (2010) proposed that yawns function in communicating mild to moderately unpleasant, but not immediately threatening, states to other members of a group. However, this appears overly general and nonspecific. In order for traits to evolve a signalling function as stated, the information transmitted by the sender must be reliable and easily interpreted (Searcy & Nowicki, 2010).
 
One potentially unifying feature of spontaneous yawns is that they reflect a current state of low arousal and vigilance and rising brain temperature. Therefore, the act of yawning could provide meaningful information to conspecifics. Recently, following the observation that yawning is absent during physical stressors but then potentiated thereafter in Nazca boobies, Liang et al. (2015) introduced the arousal reduction hypothesis, which predicts that yawns signal to others that the individual is experiencing a down regulation of arousal and vigilance. This hypothesis is consistent with psychological studies showing yawns increase in frequency during sleepiness and fatigue (Giganti et al., 2010; Provine, Hamernik, et al., 1987; Zilli et al., 2008) and periods of boredom (Provine & Hamernik, 1986), as well as neurological studies demonstrating that brain markers of decreased vigilance precede the act of yawning (Guggisberg et al., 2007; Kasuya et al., 2005). However, this hypothesis falls short in a number of important areas. At its basis, signals are traits that evolved to alter the behavior of another organism (Maynard Smith & Harper, 2003), and the receiver must benefit from the information being transmitted (Searcy & Nowicki, 2010). As stated, the arousal reduction hypothesis is functionally unclear and fails to stipulate the benefits of yawning and who receives such benefits. In addition, this hypothesis is inconsistent with evidence for a clear arousing effect to some yawns (for a commentary, see Gallup & Clark, 2015).
 
To date, the view that yawning evolved as a signal has not been empirically supported. That is, there are no studies showing that spontaneous yawns are elicited in ways or contexts that serve to intentionally convey information and alter the behavior and/or mental processing of recipients. An exception to this would be a distinct pattern of yawn-like behaviors within sexually dimorphic nonhuman primates. In particular, modified mouth-gaping actions from males, which are referred to as tension or aggression yawns, are known to play a role in threat displays (Altmann, 1967; Bertrand, 1969). This was in fact first described by Charles Darwin in The Expression of the Emotions in Man and Animals (Darwin, 1872). In such cases, a dominant male will gape his mouth open while fixing his eyes on a target individual (a subordinate) and displaying his canines. These yawn-like displays have been documented dur- ing antagonist interactions and hostile social situations across different old world monkeys (Macaca nigra: Hadidian, 1980; M. fascicularis and Macaca fuscata: Troisi et al., 1990; Cercocebus albigena and M. fascicularis: Deputte, 1994; Theropithacus gelada: Leone et al., 2014). Unlike true yawns (see definition above), however, which typically include the tilting of the head and closure of the eyes (Deputte, 1994), the display yawner fixes their attention on the target during the episode to monitor the effect of the threat. These tension/aggression yawns also vary in other morphological characteristics, whereby the yawner uncovers their gums to more clearly expose their canines (Leone et al., 2014; Zannella et al., 2017), which is consistent with the view that these yawns are most common in species with sexual dimorphism in canine size. Therefore, while these threat displays indeed appear to hold a communicative function, they are distinct from the more ubiquitous forms of yawning related to sleeping, arousal and thermo- regulation in other animals.
 
Yawning as a Cue
Yawns could still alter the behavior of conspecifics without evolving a specific communicative function. Building from ideas presented in the arousal reduction hypothesis (Liang et al., 2015), and linking directly to known physiological function(s) and con- texts of spontaneous yawns, Gallup and Meyers (2021) recently proposed specific yawn-induced changes in mental processing that should follow the observation of yawns in others. In particular, it was predicted that seeing others perform this action pattern would enhance the vigilance of observers as a means of compensating for the diminished arousal and vigilance experienced by the yawner. Independent of the resultant changes to the mental state of the yawner, which are likely tied to circadian factors (as discussed above), yawns are consistently triggered during states of low arousal and vigilance (Guggisberg et al., 2007; Kasuya et al., 2005) and rising brain temperature (Shoup-Knox et al., 2010). Although initially described as a signal, in this case yawns likely serve as a cue whereby the detection of this behavior provides information about the current (reduced) alertness of the yawner, which in turn induces neurological changes to enhance the vigilance of observers. This was termed the group vigilance hypothesis.
 
In support of this hypothesis, neuroimaging studies on humans show distinct patterns of brain activation following exposure to yawning stimuli that are indicative of improved threat detection. For example, merely seeing and hearing other people yawn activates regions of the prefrontal cortex (Arnott et al., 2009; Nahab et al., 2009) and the superior temporal sulcus (Schürmann et al., 2005; Tsurumi et al., 2019). These brain regions are known to be involved in attentional allocation to visual search (Bichot et al., 2015; Ellison et al., 2004), the detection of biologically relevant and threatening stimuli (Dinh et al., 2018; Mobbs et al., 2007) and vigilance (Nelson et al., 2014; Parasuraman et al., 1998).
 
As a direct test of the group vigilance hypothesis, Gallup and Meyers (2021) had 38 human subjects complete a series of visual search tasks for detecting snakes and frogs (repeated measures design). Snakes represented a recurrent evolutionary threat to humans (Headland & Greene, 2011; Isbell, 2006; Kasturiratne et al., 2008), while frogs served as a control stimulus. Participants were displayed eight-image arrays, where a single snake or single frog was presented among seven distractor images. During each trial, participants were tasked with locating the single target image (a frog or snake) as quickly as possible. A series of snake-target and frog-target searches were performed both after viewing videos of people yawning and after viewing the same people display neutral behavior with non-yawning mouth movements. Eye tracking was used to measure the latency to fixate on target images across trials. As predicted by the group vigilance hypothesis, vigilance was selectively enhanced after viewing videos of other people yawning. That is, participants detected snakes more rapidly after seeing other people yawn, while this manipulation had no effect on the detection of frogs. The results from Gallup and Meyers (2021) are consistent with studies on the physiological significance and con- texts of spontaneous yawning and represent the first experimental evidence for changes in cognitive performance induced merely by the observation of yawns in others.
 
CONTAGIOUS YAWNING
The detection of yawns from conspecifics is also known to elicit more overt behavioral changes, such as yawn contagion, whereby the yawns of others can trigger the reflexive matching of this action pattern in observers. Studies show that contagious yawning can be triggered through visual and/or auditory cues (Massen et al., 2015; Norscia et al., 2020; Palagi et al., 2009; Silva et al., 2012), and in humans can even be induced in solitude by thinking or reading about the act of yawning (Greco & Baenninger, 1991; Provine, 1986, 2005). The neural mechanisms governing contagious yawning are not well known, but perhaps involve mirror neurons (Haker et al., 2013). Comparatively, there is a growing number of species with documented evidence for yawn contagion, with the phylogeny of this behavior possibly reflecting the conservation of a homologous trait in great apes and convergent evolution in other lineages.
 
Among the great apes, experimental evidence for contagious yawning is present in humans (Platek et al., 2003), chimpanzees (Anderson et al., 2004; Campbell et al., 2009), bonobos, Pan paniscus (Tan et al., 2017), and orang-utans, Pongo pygmaeus (van Berlo et al., 2020). Chimpanzees also yawn contagiously in response to human yawners (e.g. Campbell & de Waal, 2014). However, there is no evidence for yawn contagion among gorillas, Gorilla gorilla (Amici et al., 2014; Palagi, Norscia, et al., 2019). In other primates, the evidence for contagious yawning is limited. However, observations of gelada baboons indicate yawn contagion in both captive and wild populations (Gallo et al., 2021; Palagi et al., 2009). There is also a report of video-induced yawning in stump-tailed macaques, Macaca arctoides (Paukner & Anderson, 2006), but this response has been interpreted as a sign of stress and anxiety rather than contagion since the yawning stimuli also produced an increase in other self-directed behaviors (i.e. scratching). Other studies show no evidence for contagious yawning in crab-eating macaques and grey-cheeked mangabeys (Deputte, 1978), common marmosets, Callithrix jacchus (Massen et al., 2016), or in either ringtailed lemurs, L. catta, or red-ruffed lemurs, Varecia variegata rubra (Reddy et al., 2016).
 
Across other mammals, experimental evidence for contagious yawning has been documented in domesticated dogs in response to human yawns (Joly-Mascheroni et al., 2008; Romero et al., 2013; Silva et al., 2012) but not in response to conspecifics (Harr et al., 2009), which could reflect selection on the emphasis of attending to human cues during domestication. There is also experimental evidence for contagious yawning in a subline of Spraguee Dawley rats (Moyaho et al., 2015). Observational evidence for contagious yawning is present in captive wolves (Canis lupus lupus) (Romero et al., 2014), and most recently, domesticated pigs, Sus scrofa (Norscia, Coco, et al., 2021), and African lions, Pantheo leo (Cassetta et al., 2021). Other mammalian species with limited evidence of yawn contagion, thus requiring further investigation, include sheep, Ovis aries (Yonezawa et al., 2017), African elephants (Rossman et al., 2020), and southern elephant seals, Mirounga leonine (Wojczulanis-Jakubas et al., 2019). One study on horses, Equus caballus, provided no evidence for yawn contagion (Malavasi, 2014).
 
Only a few studies have investigated contagious yawning among nonmammalian species. No formal investigations have been per- formed on amphibians or fish, although Baenninger (1987) assessed the temporal expression of yawn-like behaviors in Sia- mese fighting fish, Betta splendens, and found no evidence for contagion. In the only study on reptiles, the responses of red-footed tortoises, Geochelone carbonaria, were observed following the observation of conditioned yawn-like behavior in a conspecific (Wilkinson et al., 2011). No increase in tortoise yawning occurred when compared to control conditions. To date, the only evidence for yawn contagion in a nonmammalian species comes from studies on captive budgerigars, whereby yawns appear temporally clustered within flocks under seminatural conditions (Miller, Gallup, Vogel, Vicario, et al., 2012) and can be experimentally triggered following exposure to both live and videorecorded yawns from conspecifics (Gallup et al., 2015). In the only other study on yawn contagion among birds, observations of captive ravens, Corvus corax, found no evidence for this effect (Gallup et al., 2014).
 
Comparative studies of contagious yawning have thus far been relatively limited, so there are bound to be other species that show this behavior. However, it is worth noting that there are a number of methodological challenges to the study of yawn contagion (Campbell & Cox, 2019; Campbell & de Waal, 2010). Experimental studies offer the most robust test, whereby explicit yawn versus control comparisons can be made, but experiments are often limited to animals in captivity. In addition, many experiments designed to elicit yawn contagion use video stimuli with repeated clips of yawning, which could inadvertently produce a supernormal stimulus (Anderson, 2010). Moreover, video stimuli might not be optimal for all species (D'Eath, 1998). As an alternative experimental approach, live animals can be paired together both with and without visual and/or auditory access, and the temporal association of yawning between individuals can be assessed across conditions (e.g. Gallup et al., 2015).
 
Observational studies offer a more naturalistic depiction of yawn contagion, but these also present methodological challenges. Such studies often classify yawns as contagious when they occur within predetermined time periods (i.e. 3 min or 5 min) following the observation of a yawn from another individual (e.g. Demuru & Palagi, 2012; Palagi et al., 2009). However, the clustering of yawns within groups could also result from the individuals sharing com- mon circadian rhythms or activity patterns and have nothing to do with contagion. In addition, the time frames used are often arbitrary, and different species could have longer or shorter contagion latencies (Campbell & Cox, 2019). As a solution to these problems, observational studies can examine the temporal distribution of yawning across recording sessions to rule out circadian effects (Miller, Gallup, Vogel, Vicario, et al., 2012), as well as develop response curves, whereby the rate of yawning significantly above the baseline would be evidence of yawn contagion (Campbell & Cox, 2019).
 
Function(s) of Contagious Yawning
While numerous studies have examined individual differences and social-psychological correlates of yawn contagion in different species (reviewed by Massen & Gallup, 2017; Neilands et al., 2020; Palagi et al., 2020), only limited research has attempted to uncover its functional significance. That said, it has long been speculated that the spreading of yawns across groups may function to synchronize and/or coordinate group behavior (e.g. Baenninger et al., 1996; de Waal & Preston, 2017; Deputte, 1994; Guggisberg et al., 2010; Massen et al., 2012; Miller, Gallup, Vogel, & Clark, 2012; Prochazkova & Kret, 2017; Provine, Hamernik, et al., 1987; Sauer & Sauer, 1967; Vick & Paukner, 2010), which could provide survival benefits to group members (Duranton & Gaunet, 2016). This hy- pothesis is consistent with the large and aforementioned literature connecting yawns to circadian rhythms and behavioral transi- tions. For example, given that the neurovascular consequences of yawning produce changes in state (Provine, 1986) and initiate behavioral transitions and increased movement (Baenninger et al., 1996; Vick & Paukner, 2010), contagion could generate coordinated or synchronized group activity. In line with this view, ethological studies of wild animals show that yawns are naturally clustered within groups during collective transitions in behavior (Deputte, 1994; Sauer & Sauer, 1967). However, these studies fail to take into account that the individuals within these groups are under- going similar circadian and physiologic changes that may lead to a nonrandom distribution of yawns and a synchronization of activity that is independent of social influence or function (see Campbell & Cox, 2019; Miller, Gallup, Vogel, Vicario, et al., 2012).
 
To date, only one study has systematically examined the role of contagious yawning on behavioral synchronization. In an observational study of wild African lions, Casetta et al. (2021) marked the occurrence of all yawns from 19 individuals across two social groups in order to classify the connection between yawn contagion and motor synchrony. Yawn contagion was defined by a yawn that followed a yawn from another lion within a 3 min window when there were no visual obstructions between the individuals. Motor synchrony was defined by the collective switching of behavior status by either transitioning from moving to resting or resting to moving, also within a 3 min window. It was found that motor synchrony between lions increased by a factor of 11 when one yawned contagiously in response to the other, which was significantly higher than situations without contagion or when there were no yawns observed. In particular, the results showed that yawn contagion increased the likelihood that observers would replicate the motor patterns of actors. These findings from Casetta et al. (2021) are notable in providing the first direct evidence for a potential function to contagious yawning, which will most surely lead to follow-up research examining the role of yawn contagion in motor synchrony across different species.
 
A separate, but not mutually exclusive, adaptive hypothesis for yawn contagion stems from the purported brain cooling function of yawning. In particular, Gallup and Gallup (2007) proposed that contagious yawns may have evolved to promote overall group vigilance. Accordingly, if yawns serve to counteract rising brain temperature and reduced alertness and mental processing, the transfer of this behavior to nearby conspecifics could then in- crease their vigilance as well. This hypothesis is consistent with interdisciplinary lines of research suggesting that yawns are trig- gered to counteract decrements in alertness and arousal (Baenninger, 1997; Kasuya et al., 2005; Walusinski, 2006). Yet, to date, the vigilance hypothesis has not been directly tested. One study showed that auditory disturbances, which elicit startle responses and vigilance behavior, also enhance yawn contagion in budgerigars (Miller, Gallup, Vogel, & Clark, 2012). However, this work did not examine whether contagious yawning produced a change in vigilance thereafter. As previously discussed, recent research on humans has also shown that merely witnessing others yawn improves individual threat detection (Gallup & Meyers, 2021). The small number of participants that yawned contagiously (N 14 5) in this study did not permit statistical comparisons, but the results were highly similar for yawners and non-yawners. Even if vigilance is not improved further among contagious yawners e which remains an empirical question e the spreading of this cue across the group via contagion should enhance collective vigilance under natural conditions.
 
In addition to extending upon existing functional hypotheses of spontaneous yawning, and accounting for the contexts and behavioral activities in which nonsocial yawns are most common, the synchronization and vigilance hypotheses are consistent with studies documenting how various social factors modulate yawn contagion among primates: i.e. social status and affiliation. For example, within dominance hierarchies, patterns of vigilance contagion and synchronized movement are most often initiated by high-ranking individuals (Iki & Kutsukake, 2021), and research on chimpanzees and bonobos shows that yawn contagion most often stems from the yawns of dominant group members (male chimpanzees: Massen et al., 2012; female bonobos: Demuru & Palagi, 2012). Similarly, within freely moving groups, individuals with greater contact and affiliation are more likely to display coordinated movement (Farine et al., 2016), and a number of studies have reported biases in yawn contagion based on social closeness or affiliation. This includes naturalistic observations of humans, bonobos and gelada baboons (Demuru & Palagi, 2012; Gallo et al., 2021; Palagi et al., 2009, 2014; Norscia & Palagi, 2011; Norscia et al., 2020; but see Massen et al., 2015) as well as video-induced experiments on captive chimpanzees (Campbell & de Waal, 2011; Madsen et al., 2013). As a general rule, it seems that attention drives yawn contagion (Gallup, 2021; Massen & Gallup, 2017). Among chimpanzees and bonobos, attention is disproportionately directed towards individuals that are familiar and of the dominant sex (Lewis et al., 2021). Biased attention towards higher-ranking individuals is also present in other primates, such as Angolan talapoin monkeys, Miopithecus talapoin (Keverne et al., 1978), and rhesus macaques, Macaca mulatta (Shepherd et al., 2006). Similarly, primates tend to stay in close proximity to genetic relatives and socially bonded individuals (Macaca maurus: Matsumura & Okamoto, 1997; C. capucinus: Perry et al., 2008; chimpanzees: Langergraber et al., 2009), increasing the chances of detecting and responding to the yawns from these group members (Gallo et al., 2021). From an evolutionary perspective, biases in yawn contagion based on genetic relatedness (as has been shown in humans; Norscia & Palagi, 2011; Norscia et al., 2020) may hold fitness benefits by facilitating greater social cohesion and protection among kin. Moreover, these hypotheses offer further explanatory power for observed differences in yawn contagion based on reproductive status in humans. For example, during pregnancy, women appear more susceptible to contagious yawning (Norscia, Agostini, et al., 2021). Given that pregnant women also have increased reactions to threatening stimuli (Roos et al., 2012), heightened yawn contagion could improve vigilance and group synchronization during a period of increased danger sensitivity. Therefore, the synchronization and vigilance hypotheses offer fruitful avenues for further study.
 
SUMMARY AND FUTURE DIRECTIONS
Yawning is a neurophysiological adaptation that is omnipresent across vertebrates (Massen et al., 2021), and the detection of this action pattern in others appears to be biologically important among social species (Tsurumi et al., 2019). Moreover, recent studies indicate that yawning serves as a cue that enhances individual vigilance and promotes motor synchrony through contagion (see Fig. 1 for a graphic illustration of these processes). However, additional research is needed to replicate and further examine the nature of these effects, as well as investigate potential comparative differences in these responses based by on ecological factors and evolutionary history. In particular, future studies could examine how exposure to yawns alters the detection of threatening stimuli across different species, as well as how experimentally induced yawn contagion influences different patterns of motor synchrony and group coordination among human and nonhuman animals in the laboratory. In addition, naturalistic studies could investigate how the detection of yawning alters scanning rates and vigilance monitoring in free-moving groups, as well as how yawning and other patterns of behavioral contagion influence collective movement across different species. For example, among many species, yawning and stretching tend to co-occur, and both behaviors have been found to be contagious in budgerigars (Gallup et al., 2017; Miller, Gallup, Vogel, Vicario, et al., 2012). Since yawn and stretch contagion could have similar functions among animal groups in initiating collective action, future research could assess whether behavioral contagion in general is a key feature in initiating synchrony.
 
The current evidence suggests that yawning serves as a cue rather than as a signal, but future studies could further examine whether spontaneous yawns evolved specifically to communicate internal states and/or alter the behavior of observers in some species. For example, studies could investigate whether yawning occurs more readily in the presence of others and in contexts in which synchrony and/or vigilance would be most advantageous to the group. In addition, researchers could examine patterns in the variability of yawn expression. A recent study on macaques (Macaca tonkeana and M. fuscata) suggests differences in the morphology and duration of yawning are predictive of the contexts in which this behavior arises (Zannella et al., 2021), so follow-up studies could also assess how different types of yawns differentially impact the subsequent vigilance behavior and synchronization of observers. Similarly, researchers could assess differences in yawn-induced changes in behavior based on the presence or absence of auditory cues. Vocal components to yawning appear to be common among humans and non-primates (e.g. Massen et al., 2015; Palagi et al., 2009), yet seem unnecessary for the physiological function(s) of this action pattern. Thus, studies could investigate the factors that contribute to variation in vocal yawning and how the social outcomes of yawning vary based on visual and/or auditory detection.
Further examination of yawning in animals could provide important insights into the social role of this behavior and its function in altering group dynamics, which could in turn offer applications for improving performance in surveillance settings and organized group activities in our own species. Based on what is already known about the social nature of yawning, it appears time to systemically examine some of the more overt social features of this behavior in humans. This includes the stigmatization of yawning in some cultures (Schiller, 2002), which leads to the active concealment (Schino & Aureli, 1989) and/or inhibition of yawning when in the presence of others (Gallup, Church, Miller, et al., 2016; Gallup et al., 2019). For example, further research is needed to fully understand and disentangle the potential physiologic and social causes and consequences of inhibiting spontaneous and contagious yawning in groups. In line with the comparative perspective highlighted throughout this review, the bridging of both human and nonhuman animal research will provide the most comprehensive understanding of this evolutionarily conserved behavior.
 
 
References
Altmann, J. (1967). The structure of primate social organization. In S. A. Altamann (Ed.), Social communication among primates (pp. 325e362). The University of Chicago Press.
 
Amici, F., Aureli, F., & Call, J. (2014). Response facilitation in the four great apes: Is there a role for empathy? Primates, 55(1), 113e118.
 
Anderson, J. R. (2010). Non-human primates: A comparative developmental perspective on yawning. In O. Walusinski (Ed.), Mystery of yawning in physiology and disease (Vol. 28, pp. 63e76). Basel: Karger.
 
Anderson, J. R., Myowa-Yamakoshi, M., & Matsuzawa, T. (2004). Contagious yawning in chimpanzees. Proceedings of the Royal Society B: Biological Sciences, 271(Suppl. 6), S468eS470.
 
Anias, J., Holmgren, B., Holmgren, R. U., & Eguibar, J. R. (1984). Circadian variation of yawning behavior. Acta Neurobiologiae Experimentalis, 44, 179e186.
 
Argiolas, A., & Melis, M. R. (1998). The neuropharmacology of yawning. European Journal of Pharmacology, 343(1), 1e16.
 
Arnott, S. R., Singhal, A., & Goodale, M. A. (2009). An investigation of auditory contagious yawning. Cognitive, Affective, & Behavioral Neuroscience, 9(3), 335e342.
 
Askenasy, J. J. M. (1989). Is yawning an arousal defense reflex? Journal of Psychology, 123(6), 609e621.
 
Baenninger, R. (1987). Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. Journal of Comparative Psychology, 101(4), 349e354.
 
Baenninger, R. (1997). On yawning and its functions. Psychonomic Bulletin & Review, 4(2), 198e207.
 
Baenninger, R., Binkley, S., & Baenninger, M. (1996). Field observations of yawning and activity in humans. Physiology & Behavior, 59(3), 421e425.
 
Baker, K. C., & Aureli, F. (1997). Behavioral indicators of anxiety: An empirical test in chimpanzees. Behavior, 134(13), 1031e1050.
 
Barbizet, J. (1958). Yawning. Journal of Neurology, Neurosurgery, and Psychiatry, 21(3), 203.
 
van Berlo, E., Díaz-Loyo, A. P., Juarez-Mora, O. E., Kret, M. E., & Massen, J. J. (2020). Experimental evidence for yawn contagion in orangutans (Pongo pygmaeus). Scientific Reports, 10(1), 1e11.
 
Bertrand, M. (1969). The behavioral repertoire of the stumptail macaque. Basel: Karger.
 
Bichot, N. P., Heard, M. T., DeGennaro, E. M., & Desimone, R. (2015). A source for feature-based attention in the prefrontal cortex. Neuron, 88(4), 832e844.
 
Bolwig, N. (1959). A study of the behavior of the chacma baboon, Papio ursinus. Behavior, 14, 136e163.
 
Campbell, M. W., Carter, J. D., Proctor, D., Eisenberg, M. L., & de Waal, F. B. (2009). Computer animations stimulate contagious yawning in chimpanzees. Pro- ceedings of the Royal Society B: Biological Sciences, 276(1676), 4255e4259.
 
Campbell, M. W., & Cox, C. R. (2019). Observational data reveal evidence and parameters of contagious yawning in the behavioral repertoire of captive-reared chimpanzees (Pan troglodytes). Scientific Reports, 9(1), 1e13.
 
Campbell, M. W., & de Waal, F. B. (2010). Methodological problems in the study of contagious yawning. In O. Walusinski (Ed.), The mystery of yawning in physiology and disease (Vol. 28, pp. 120e127). Basel: Karger.
 
Campbell, M. W., & de Waal, F. B. (2011). Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy. PLoS One, 6(4), Article e18283.
 
Campbell, M. W., & de Waal, F. B. (2014). Chimpanzees empathize with group mates and humans, but not with baboons or unfamiliar chimpanzees. Proceedings of the Royal Society B: Biological Sciences, 281(1782), 20140013.
 
Campos, F. A., & Fedigan, L. M. (2009). Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa Na- tional Park, Costa Rica. American Journal of Physical Anthropology, 138(1), 101e111.
 
Casetta, G., Nolfo, A. P., & Palagi, E. (2021). Yawn contagion promotes motor synchrony in wild lions, Panthera leo. Animal Behavior, 174, 149e159.
 
Castles, D. L., Whiten, A., & Aureli, F. (1999). Social anxiety, relationships and self- directed behavior among wild female olive baboons. Animal Behavior, 58(6), 1207e1215.
 
Cordoni, G., Favilli, E., & Palagi, E. (2021). Earlier than previously thought: Yawn contagion in preschool children. Developmental Psychobiology, 63(5), 931e944.
 
Corey, T. P., Shoup-Knox, M. L., Gordis, E. B., & Gallup, G. G., Jr. (2012). Changes in physiology before, during, and after yawning. Frontiers in Evolutionary Neuroscience, 3, 7.
 
Craemer, E. (1924). Uber Sodbrennen und Gahnen. Gastroenterologia Archiv fiir Verdauungskrankheiten, 33, 149e162.
 
D'Eath, R. B. (1998). Can video images imitate real stimuli in animal behavior experiments? Biological Reviews, 73(3), 267e292.
 
Darwin, C. R. (1872). The expression of the emotions in man and animals. London: John Murray.
 
Darwin, C. R. (1987). Notebook M (1838). In P. H. Barrett, P. J. Gantrey, S. Herbert, D. Kohn, & S. Smith (Eds.), Charles Darwin's notebooks, 1836e1844 (pp.
517e562). Ithaca, NY: Cornell University Press.
 
Demuru, E., & Palagi, E. (2012). In bonobos yawn contagion is higher among kin and friends. PLoS One, 7(11), Article e49613.
 
Deputte, B. L. (1978). Study of yawning in two species of Cercopithecidae; Cercocebus albigena Gray and Macaca fascicularis Raffles: Research on causal and functional factors; a consideration of socio-bioenergetic factors (Master's dissertation). Rennes, France: University of Rennes 1.
 
Deputte, B. L. (1994). Ethological study of yawning in primates. I. Quantitative analysis and study of causation in two species of Old World monkeys (Cerco- cebus albigena and Macaca fascicularis). Ethology, 98(3-4), 221e245.
 
Dinh, H. T., Nishimaru, H., Matsumoto, J., Takamura, Y., Le, Q. V., Hori, E., Maior, R. S., Tomaz, C., Tran, A. H., Ono, T., & Nishijo, H. (2018). Superior neuronal detection of snakes and conspecific faces in the macaque medial prefrontal cortex. Ce- rebral Cortex, 28(6), 2131e2145.
 
Duranton, C., & Gaunet, F. (2016). Behavioral synchronization from an ethological perspective: Overview of its adaptive value. Adaptive Behavior, 24(3), 181e191.
 
Eguibar, J. R., Uribe, C. A., Cortes, C., Bautista, A., & Gallup, A. C. (2017). Yawning reduces facial temperature in the high-yawning subline of SpragueeDawley
rats. BMC Neuroscience, 18(1), 1e8.
 
Eldakar, O. T., Dauzonne, M., Prilutzkaya, Y., Garcia, D., Thadal, C., & Gallup, A. C. (2015). Temperature-dependent variation in self-reported contagious yawning.
Adaptive Human Behavior and Physiology, 1(4), 460e466.
 
Eldakar, O. T., Tartar, J. L., Garcia, D., Ramirez, V., Dauzonne, M., Armani, Y., & Gallup, A. C. (2017). Acute physical stress modulates the temporal expression of self-reported contagious yawning in humans. Adaptive Human Behavior and Physiology, 3(2), 156e170.
 
Ellison, A., Schindler, I., Pattison, L. L., & Milner, A. D. (2004). An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS. Brain, 127(10), 2307e2315.
 
Enokizu, A., Morisaka, T., Murakami, K., Sakurai, N., Ueda, N., & Yoshioka, M. (2021). Yawn-like behavior in captive common bottlenose dolphins (Tursiops truncatus). Behavioral Processes, 189, 104444.
 
Farine, D. R., Strandburg-Peshkin, A., Berger-Wolf, T., Ziebart, B., Brugere, I., Li, J., & Crofoot, M. C. (2016). Both nearest neighbours and long-term affiliates predict individual locations during collective movement in wild baboons. Scientific Reports, 6(1), 1e10.
 
Fenner, K., Yoon, S., White, P., Starling, M., & McGreevy, P. (2016). The effect of noseband tightening on horses' behavior, eye temperature, and cardiac re- sponses. PLoS One, 11(5), Article e0154179.
 
Gallo, A., Zanoli, A., Caselli, M., Palagi, E., & Norscia, I. (2021). First evidence of yawn contagion in a wild monkey species. Scientific Reports, 11, 17957.
 
Gallup, A. C. (2011). Why do we yawn? Primitive versus derived features. Neuro- science & Biobehavioral Reviews, 35(3), 765e769.
 
Gallup, A. C. (2021). On the link between emotional contagion and contagious yawning. Neuroscience & Biobehavioral Reviews, 121, 18e19.
 
Gallup, A. C., Church, A. M., Miller, H., Risko, E. F., & Kingstone, A. (2016). Social presence diminishes contagious yawning in the laboratory. Scientific Reports, 6(1), 1e5.
 
Gallup, A. C., Church, A. M., & Pelegrino, A. J. (2016). Yawn duration predicts brain weight and cortical neuron number in mammals. Biology Letters, 12(10), 20160545.
 
Gallup, A. C., & Clark, A. B. (2015). Commentary: Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings. Frontiers in Psychology, 6, 1654.
 
Gallup, A. C., & Eldakar, O. T. (2013). The thermoregulatory theory of yawning: What we know from over 5 years of research. Frontiers in Neuroscience, 6, 188.
 
Gallup, A. C., & Gallup, G. G. (2008). Yawning and thermoregulation. Physiology & Behavior, 95(1e2), 10e16.
 
Gallup, G. G., & Gallup, A. C. (2010). Excessive yawning and thermoregulation: Two case histories of chronic, debilitating bouts of yawning. Sleep and Breathing, 14(2), 157e159.
 
Gallup, A. C., & Gallup, G. G., Jr. (2007). Yawning as a brain cooling mechanism: Nasal breathing and forehead cooling diminish the incidence of contagious yawning. Evolutionary Psychology, 5(1), 92e101.
 
Gallup, A. C., Kret, M., Eldakar, O. T., Folz, J., & Massen, J. J. M. (2021). People that score high on psychopathic traits are less likely to yawn contagiously. Scientific Reports, 11(1), 1e11.
 
Gallup, A. C., & Meyers, K. (2021). Seeing others yawn selectively enhances vigi- lance: An eye-tracking study of snake detection. Animal Cognition, 24(3), 583e592.
 
Gallup, A. C., Militello, J., Swartwood, L., & Sackett, S. (2017). Experimental evidence of contagious stretching and ingroup bias in budgerigars (Melopsittacus undu- latus). Journal of Comparative Psychology, 131(1), 69e72.
 
Gallup, A. C., Miller, M. L., & Clark, A. B. (2009). Yawning and thermoregulation in budgerigars, Melopsittacus undulatus. Animal Behavior, 77(1), 109e113.
 
Gallup, A. C., Miller, M. L., & Clark, A. B. (2010). The direction and range of ambient temperature change influences yawning in budgerigars (Melopsittacus undu- latus). Journal of Comparative Psychology, 124(2), 133e138.
 
Gallup, A. C., Miller, R. R., & Clark, A. B. (2011). Changes in ambient temperature trigger yawning but not stretching in rats. Ethology, 117(2), 145e153.
 
Gallup, A. C., Schild, A. B., Ühlein, M. A., & Massen, J. J. M. (2014). An observational study of behavioral contagion in ravens (Corvus corax). In Paper presented at the 51st Annual Meeting of the Animal Behavior Society Conference, Princeton Uni- versity, Princeton, NJ.
 
Gallup, A. C., Swartwood, L., Militello, J., & Sackett, S. (2015). Experimental evidence of contagious yawning in budgerigars (Melopsittacus undulatus). Animal Cognition, 18(5), 1051e1058.
 
Gallup, A. C., Vasilyev, D., Anderson, N., & Kingstone, A. (2019). Contagious yawning in virtual reality is affected by actual, but not simulated, social presence. Sci- entific Reports, 9(1), 1e10.
 
Giganti, F., Hayes, M. J., Akilesh, M. R., & Salzarulo, P. (2002). Yawning and behavioral states in premature infants. Developmental Psychobiology, 41(3), 289e296.
 
Giganti, F., & Zilli, I. (2011). The daily time course of contagious and spontaneous yawning among humans. Journal of Ethology, 29(2), 215e219.
 
Giganti, F., Zilli, I., Aboudan, S., & Salzarulo, P. (2010). Sleep, sleepiness and yawning. In O. Walusinski (Ed.), The mystery of yawning in physiology and disease (Vol. 28, pp. 42e46). Basel: Karger.
 
Goodall, J. (1968). A preliminary report on expressive movements and communication in the Gombe stream chimpanzees. In P. C. Jay (Ed.), Primates: Studies in adaptation and variability (pp. 313e374). New York: Holt Rinehart & Winston.
 
Gorecka-Bruzda, A., Fureix, C., Ouvrard, A., Bourjade, M., & Hausberger, M. (2016). Investigating determinants of yawning in the domestic (Equus caballus) and Przewalski (Equus ferus przewalskii) horses. Science of Nature, 103(9), 1e10.
 
Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society B: Biological Sciences, 205(1161), 581e598.
 
Greco, M., & Baenninger, R. (1991). Effects of yawning and related activities on skin conductance and heart rate. Physiology & Behavior, 50(5), 1067e1069.
 
Guggisberg, A. G., Mathis, J., Herrmann, U. S., & Hess, C. W. (2007). The functional relationship between yawning and vigilance. Behavioral Brain Research, 179(1), 159e166.
 
Guggisberg, A. G., Mathis, J., Schnider, A., & Hess, C. W. (2010). Why do we yawn? Neuroscience & Biobehavioral Reviews, 34(8), 1267e1276.
 
Hadidian, J. (1980). Yawning in an old world monkey, Macaca nigra (Primates: Cercopithecidae). Behavior, 133e147.
 
Haker, H., Kawohl, W., Herwig, U., & Ro¤ssler, W. (2013). Mirror neuron activity during contagious yawning e An fMRI study. Brain Imaging and Behavior, 7(1), 28e34.
 
Harr, A. L., Gilbert, V. R., & Phillips, K. A. (2009). Do dogs (Canis familiaris) show contagious yawning? Animal Cognition, 12, 833e837.
 
Headland, T. N., & Greene, H. W. (2011). Hunteregatherers and other primates as prey, predators, and competitors of snakes. Proceedings of the National Academy of Sciences of the United States of America, 108(52), E1470eE1474.
 
Helt, M. S., Sorensen, T. M., Scheub, R. J., Nakhle, M. B., & Luddy, A. C. (2021). Patterns of contagious yawning and itching differ amongst adults with autistic traits vs. psychopathic traits. Frontiers in Psychology, 12, 645310.
 
Iki, S., & Kutsukake, N. (2021). Social bias affects vigilance contagion in Japanese macaques. Animal Behavior, 178, 67e76.
 
Isbell, L. A. (2006). Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution, 51(1), 1e35.
 
Joly-Mascheroni, R. M., Senju, A., & Shepherd, A. J. (2008). Dogs catch human yawns. Biology Letters, 4(5), 446e448.
 
Kasturiratne, A., Wickremasinghe, A. R., de Silva, N., Gunawardena, N. K., Pathmeswaran, A., Premaratna, R., Savioli, L., Lalloo, D. G., & de Silva, H. J. (2008). The global burden of snakebite: A literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Medicine, 5(11), e218.
 
Kasuya, Y., Murakami, T., Oshima, T., & Dohi, S. (2005). Does yawning represent a transient arousal-shift during intravenous induction of general anesthesia? Anesthesia & Analgesia, 101(2), 382e384.
 
Keverne, E. B., Leonard, R. A., Scruton, D. M., & Young, S. K. (1978). Visual monitoring in social groups of talapoin monkeys (Miopithecus talapoin). Animal Behavior, 26, 933e944.
 
Kotsoni, E., De Haan, M., & Johnson, M. H. (2001). Categorical perception of facial expressions by 7-month-old infants. Perception, 30(9), 1115e1125.
 
Kubota, N., Amemiya, S., Yanagita, S., Nishijima, T., & Kita, I. (2014). Emotional stress evoked by classical fear conditioning induces yawning behavior in rats. Neuroscience Letters, 566, 182e187.
 
LaBarbera, J., Izard, C., Vietze, P., & Parisi, S. (1976). Four- and six-month-old infants' visual responses to joy, anger, and neutral expressions. Child Development, 47, 535e538.
 
Landolt, H. P., Moser, S., Wiesen, H. G., Borbeley, A. A., & Dijk, D. J. (1995). Intra- cranial temperature across 24 hour sleep wake cycles in humans. NeuroReport, 6, 913e917.
 
Langergraber, K., Mitani, J., & Vigilant, L. (2009). Kinship and social bonds in female chimpanzees (Pan troglodytes). American Journal of Primatology, 71(10), 840e851.
 
Leone, A., Ferrari, P. F., & Palagi, E. (2014). Different yawns, different functions? Testing social hypotheses on spontaneous yawning in Theropithecus gelada. Scientific Reports, 4(1), 1e9.
 
Lewis, L. S., Kano, F., Stevens, J. M., DuBois, J. G., Call, J., & Krupenye, C. (2021). Bonobos and chimpanzees preferentially attend to familiar members of the dominant sex. Animal Behavior, 177, 193e206.
 
Liang, A. C., Grace, J. K., Tompkins, E. M., & Anderson, D. J. (2015). Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings. Physiology & Behavior, 140, 38e43.
 
Luttenberger, E. (1975). On yawning in reptiles. Zeitschrift für Tierpsychologie, 37, 113e137.
 
Madsen, E. A., & Persson, T. (2013). Contagious yawning in domestic dog puppies (Canis lupus familiaris): The effect of ontogeny and emotional closeness on low- level imitation in dogs. Animal Cognition, 16(2), 233e240.
 
Madsen, E. A., Persson, T., Sayehli, S., Lenninger, S., & Sonesson, G. (2013). Chimpanzees show a developmental increase in susceptibility to contagious yawning: A test of the effect of ontogeny and emotional closeness on yawn contagion. PLoS One, 8(10), Article e76266.
 
Maestripieri, D., Schino, G., Aureli, F., & Troisi, A. (1992). A modest proposal: Displacement activities as an indicator of emotions in primates. Animal Behavior, 44(5), 967e979.
 
Malavasi, R. (2014). Social modulation of yawning behavior in the domestic horse e an exploratory analysis. In I. Estevez, X. Manteca, R. H. Marin, & X. Avero_s (Eds.), Proceedings of the 48th International Conference of the International Society for Applied Ethology, 29 July e 2 August 2014, Vitoria-Gasteiz, Spain: Moving on (p. 240). Wageningen Academic.
 
Massen, J. J. M., Church, A. M., & Gallup, A. C. (2015). Auditory contagious yawning in humans: An investigation into affiliation and status effects. Frontiers in Psy- chology, 6, 1735.
 
Massen, J. J. M., Dusch, K., Eldakar, O. T., & Gallup, A. C. (2014). A thermal window for yawning in humans: Yawning as a brain cooling mechanism. Physiology & Behavior, 130, 145e148.
 
Massen, J. J. M., & Gallup, A. C. (2017). Why contagious yawning does not (yet) equate to empathy. Neuroscience & Biobehavioral Reviews, 80, 573e585.
 
Massen, J. J. M., Hartlieb, M., Martin, J. S., Leitgeb, E., Bugnyar, T., Hockl, J., Kocourek, M., Olkowicz, S., Osadnik, C., Verkleij, J. W., Zhang, Y., Nemec, P., &
Gallup, A. C. (2021). Brain size and neuron numbers drive differences in yawn duration across mammals and birds. Communications Biology, 4(1), 1e10.
 
Massen, J. J. M., Maylor, E., Moulson, J. M., Muncer, A.-M., Taylor, L. A., Massen, J. J., Vermunt, D. A., & Sterck, E. H. (2012). Male yawning is more contagious than female yawning among chimpanzees (Pan troglodytes). PLoS One, 7(7), Article e40697.
 
Massen, J. J. M., Slipogor, V., & Gallup, A. C. (2016). An observational investigation of behavioral contagion in common marmosets (Callithrix jacchus): Indications for contagious scent-marking. Frontiers in Psychology, 7, 1190.
 
Matikainen, J., & Elo, H. (2008). Does yawning increase arousal through mechanical stimulation of the carotid body? Medical Hypotheses, 70(3), 488e492.
Matsumura, S., & Okamoto, K. (1997). Factors affecting proximity among members of a wild group of moor macaques during feeding, moving, and resting. Inter- national Journal of Primatology, 18(6), 929e940.
 
Maynard Smith, J., & Harper, D. (2003). Animal signals. Oxford University Press.
 
Melis, M. R., Argiolas, A., & Gessa, G. L. (1987). Apomorphine-induced penile erec- tion and yawning: Site of action in brain. Brain Research, 415(1), 98e104.
 
Millen, A., & Anderson, J. R. (2011). Neither infants nor toddlers catch yawns from their mothers. Biology Letters, 7(3), 440e442.
 
Miller, M. L., Gallup, A. C., Vogel, A. R., & Clark, A. B. (2010). Handling stress initially inhibits, but then potentiates yawning in budgerigars (Melopsittacus undulatus). Animal Behavior, 80(4), 615e619.
 
Miller, M. L., Gallup, A. C., Vogel, A. R., & Clark, A. B. (2012). Auditory disturbances promote temporal clustering of yawning and stretching in small groups of budgerigars (Melopsittacus undulatus). Journal of Comparative Psychology, 126(3), 324.
 
Miller, M. L., Gallup, A. C., Vogel, A. R., Vicario, S. M., & Clark, A. B. (2012). Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): An observational study of yawning and stretching. Behavioral Processes, 89(3), 264e270.
 
Mobbs, D., Petrovic, P., Marchant, J. L., Hassabis, D., Weiskopf, N., Seymour, B., Dolan, R. J., & Frith, C. D. (2007). When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science, 317(5841), 1079e1083.
 
Moyaho, A., Rivas-Zamudio, X., Ugarte, A., Eguibar, J. R., & Valencia, J. (2015). Smell facilitates auditory contagious yawning in stranger rats. Animal Cognition, 18(1), 279e290.
 
Moyaho, A., Urbina, A. F., Guzm_an, E. M., & Walusinski, O. (2017). Yawning: A cue and a signal. Heliyon, 3(11), Article e00437.
 
Moyaho, A., & Valencia, J. (2002). Grooming and yawning trace adjustment to un- familiar environments in laboratory SpragueeDawley rats (Rattus norvegicus). Journal of Comparative Psychology, 116(3), 263e269.
 
Nahab, F. B., Hattori, N., Saad, Z. S., & Hallett, M. (2009). Contagious yawning and the frontal lobe: An fMRI study. Human Brain Mapping, 30(5), 1744e1751.
 
Neilands, P., Claessens, S., Ren, I., Hassall, R., Bastos, A. P., & Taylor, A. H. (2020). Contagious yawning is not a signal of empathy: No evidence of familiarity, gender or prosociality biases in dogs. Proceedings of the Royal Society B: Bio- logical Sciences, 287(1920), 20192236.
 
Nelson, J. T., McKinley, R. A., Golob, E. J., Warm, J. S., & Parasuraman, R. (2014). Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation (tDCS). NeuroImage, 85, 909e917.
 
Norscia, I., Agostini, L., Moroni, A., Caselli, M., Micheletti-Cremasco, M., Varde_, C., & Palagi, E. (2021). Yawning is more contagious in pregnant than nulliparous women. Human Nature, 32, 301e325.
 
Norscia, I., Coco, E., Robino, C., Chierto, E., & Cordoni, G. (2021). Yawn contagion in domestic pigs (Sus scrofa). Scientific Reports, 11(1), 1e12.
 
Norscia, I., & Palagi, E. (2011). Yawn contagion and empathy in Homo sapiens. PLoS One, 6(12), Article e28472.
 
Norscia, I., Zanoli, A., Gamba, M., & Palagi, E. (2020). Auditory contagious yawning is highest between friends and family members: Support to the emotional bias hypothesis. Frontiers in Psychology, 11, 442.
 
Olivier, B., Zethof, T., Pattij, T., van Boogaert, M., van Oorschot, R., Leahy, C., Oosting, R., Bouwknecht, A., Veening, J., van der Gugten, J., & Groenink, L. (2003). Stress-induced hyperthermia and anxiety: Pharmacological validation. European Journal of Pharmacology, 463(1), 117e132.
 
Palagi, E., Celeghin, A., Tamietto, M., Winkielman, P., & Norscia, I. (2020). The neuroethology of spontaneous mimicry and emotional contagion in human and non-human animals. Neuroscience & Biobehavioral Reviews, 111, 149e165.
 
Palagi, E., Guille_n-Salazar, F., & Llamazares-Martín, C. (2019). Spontaneous yawning and its potential functions in South American sea lions (Otaria flavescens). Scientific Reports, 9(1), 1e8.
 
Palagi, E., Leone, A., Mancini, G., & Ferrari, P. F. (2009). Contagious yawning in gelada baboons as a possible expression of empathy. Proceedings of the National Academy of Sciences of the United States of America, 106(46), 19262e19267.
 
Palagi, E., Norscia, I., & Cordoni, G. (2019). Lowland gorillas (Gorilla gorilla gorilla) failed to respond to others' yawn: Experimental and naturalistic evidence. Journal of Comparative Psychology, 133(3), 406.
 
Palagi, E., Norscia, I., & Demuru, E. (2014). Yawn contagion in humans and bonobos: Emotional affinity matters more than species. PeerJ, 2, e519.
Parasuraman, R., Warm, J. S., & See, J. E. (1998). Brain systems of vigilance. In R. Parasuraman (Ed.), The attentive brain (pp. 221e256). Cambridge, MA: MIT Press.
 
Paukner, A., & Anderson, J. R. (2006). Video-induced yawning in stumptail ma- caques (Macaca arctoides). Biology Letters, 2(1), 36e38.
 
Perry, S., Manson, J. H., Muniz, L., Gros-Louis, J., & Vigilant, L. (2008). Kin-biased social behavior in wild adult female white-faced capuchins, Cebus capucinus. Animal Behavior, 76(1), 187e199.
 
Platek, S. M., Critton, S. R., Myers, T. E., & Gallup, G. G., Jr. (2003). Contagious yawning: The role of self-awareness and mental state attribution. Cognitive Brain Research, 17(2), 223e227.
 
Prochazkova, E., & Kret, M. E. (2017). Connecting minds and sharing emotions through mimicry: A neurocognitive model of emotional contagion. Neurosci- ence & Biobehavioral Reviews, 80, 99e114.
 
Provine, R. R. (1986). Yawning as a stereotyped action pattern and releasing stim- ulus. Ethology, 72(2), 109e122.
 
Provine, R. R. (2005). Yawning: The yawn is primal, unstoppable and contagious, revealing the evolutionary and neural basis of empathy and unconscious behavior. American Scientist, 93(6), 532e539.
 
Provine, R. R., & Hamernik, H. B. (1986). Yawning: Effects of stimulus interest. Bulletin of the Psychonomic Society, 24(6), 437e438.
 
Provine, R. R., Hamernik, H. B., & Curchack, B. C. (1987). Yawning: Relation to sleeping and stretching in humans. Ethology, 76(2), 152e160.
 
Provine, R. R., Tate, B. C., & Geldmacher, L. L. (1987). Yawning: No effect of 3e5% CO2, 100% O2, and exercise. Behavioral and Neural Biology, 48(3), 382e393.
 
Ramirez, V., Ryan, C. P., Eldakar, O. T., & Gallup, A. C. (2019). Manipulating neck temperature alters contagious yawning in humans. Physiology & Behavior, 207, 86e89.
 
Rasa, O. A. (1971). The causal factors and functions of yawning in M. chrysurus (Pisces: Pomacentridae). Behavior, 39, 39e57.
 
Reddy, R. B., Krupenye, C., MacLean, E. L., & Hare, B. (2016). No evidence for contagious yawning in lemurs. Animal Cognition, 19(5), 889e898.
 
Romero, T., Ito, M., Saito, A., & Hasegawa, T. (2014). Social modulation of contagious yawning in wolves. PLoS One, 9(8), Article e105963.
 
Romero, T., Konno, A., & Hasegawa, T. (2013). Familiarity bias and physiological responses in contagious yawning by dogs support link to empathy. PLoS One, 8,
Article e71365.
 
Roos, A., Lochner, C., Kidd, M., van Honk, J., Vythilingum, B., & Stein, D. J. (2012). Selective attention to fearful faces during pregnancy. Progress in Neuro-
Psychopharmacology and Biological Psychiatry, 37(1), 76e80.
 
Rossman, Z. T., Hart, B. L., Greco, B. J., Young, D., Padfield, C., Weidner, L., Gates, J., & Hart, L. A. (2017). When yawning occurs in elephants. Frontiers in Veterinary Science, 4, 22.
 
Rossman, Z. T., Padfield, C., Young, D., Hart, B. L., & Hart, L. A. (2020). Contagious yawning in African elephants (Loxodonta africana): Responses to other elephants and familiar humans. Frontiers in Veterinary Science, 7, 252.
 
Sato-Suzuki, I., Kita, I., Oguri, M., & Arita, H. (1998). Stereotyped yawning responses induced by electrical and chemical stimulation of paraventricular nucleus of the
rat. Journal of Neurophysiology, 80(5), 2765e2775.
 
Sauer, E. F., & Sauer, E. M. (1967). Yawning and other maintenance activities in the South African ostrich. Auk, 84(4), 571e587.
 
Schiller, F. (2002). Yawning? Journal of the History of the Neurosciences, 11(4), 392e401. Schino, G., & Aureli, F. (1989). Do men yawn more than women? Ethology and Sociobiology, 10(5), 375e378.
 
Schroth, G., & Klose, U. (1992). Cerebrospinal fluid flow. II. Physiology of respiration related pulsations. Neuroradiology, 35, 10e15.
 
Schürmann, M., Hesse, M. D., Stephan, K. E., Saarela, M., Zilles, K., Hari, R., & Fink, G. R. (2005). Yearning to yawn: The neural basis of contagious yawning.
NeuroImage, 24(4), 1260e1264.
 
Searcy, W. A., & Nowicki, S. (2010). The evolution of animal communication. Princeton University Press.
 
Seki, Y., Sato-Suzuki, I., Kita, I., Oguri, M., & Arita, H. (2002). Yawning/cortical activation induced by microinjection of histamine into the paraventricular nucleus
of the rat. Behavioral Brain Research, 134(1e2), 75e82.
 
Shepherd, S. V., Deaner, R. O., & Platt, M. L. (2006). Social status gates social attention in monkeys. Trends in Cognitive Sciences, 4, 138e147.
 
Shoup-Knox, M. L., Gallup, A. C., Gallup, G., & McNay, E. C. (2010). Yawning and stretching predict brain temperature changes in rats: Support for the thermo-
regulatory hypothesis. Frontiers in Evolutionary Neuroscience, 2, 108.
 
Silva, K., Bessa, J., & de Sousa, L. (2012). Auditory contagious yawning in domestic dogs (Canis familiaris): First evidence for social modulation. Animal Cognition,
15, 721e724.
 
Smith, E. O. (1999). Yawning: An evolutionary perspective. Human Evolution, 14(3),
191e198.
 
Tan, J., Ariely, D., & Hare, B. (2017). Bonobos respond prosocially toward members of other groups. Scientific Reports, 7(1), 1e11.
 
Tesfaye, Y., & Lal, S. (1990). Hazard of yawning. Canadian Medical Association Journal, 142(6), 533be533.
 
Troisi, A., Aureli, F., Schino, G., Rinaldi, F., & de Angelis, N. (1990). The influence of age, sex, and rank on yawning behavior in two species of macaques (Macaca fascicularis and M. fuscata). Ethology, 86(4), 303e310.
 
Tsurumi, S., Kanazawa, S., & Yamaguchi, M. K. (2019). Infant brain activity in response to yawning using functional near-infrared spectroscopy. Scientific
Reports, 9(1), 1e9.
 
Vick, S. J., & Paukner, A. (2010). Variation and context of yawns in captive chimpanzees (Pan troglodytes). American Journal of Primatology, 72(3), 262e269.
 
de Vries, J. I., Visser, G. H., & Prechtl, H. F. (1982). The emergence of fetal behavior. I. Qualitative aspects. Early Human Development, 7(4), 301e322.
de Waal, F. B., & Preston, S. D. (2017). Mammalian empathy: Behavioral manifestations and neural basis. Nature Reviews Neuroscience, 18(8), 498e509.
 
Walusinski, O. (2006). Yawning: Unsuspected avenue for a better understanding of
arousal and interoception. Medical Hypotheses, 67(1), 6e14.
 
Walusinski, O. (2014). How yawning switches the default-mode network to the attentional network by activating the cerebrospinal fluid flow. Clinical Anatomy,
27(2), 201e209.
 
Walusinski, O. (2018). Pathological yawning, laughing and crying. In J. Bogousslavsky (Ed.), Neurologic-psychiatric syndromes in focus - Part I (Vol. 41,
pp. 40e49). Basel: Karger.
 
Wiley, R. H. (2006). Signal detection and animal communication. Advances in the Study of Behavior, 36, 217e247.
 
Wilkinson, A., Sebanz, N., Mandl, I., & Huber, L. (2011). No evidence of contagious yawning in the red-footed tortoise Geochelone carbonaria. Current Zoology,
57(4), 477e484.
 
Wojczulanis-Jakubas, K., Plenzler, J., & Jakubas, D. (2019). Indications of contagious behaviors in the southern elephant seal: An observational study. Behavior,
156(1), 59e77.
 
Yonezawa, T., Sato, K., Uchida, M., Matsuki, N., & Yamazaki, A. (2017). Presence of contagious yawning in sheep. Animal Science Journal, 88(1), 195e200.
 
Zannella, A., Norscia, I., Stanyon, R., & Palagi, E. (2015). Testing yawning hypotheses in wild populations of two strepsirrhine species: Propithecus verreauxi and Lemur catta. American Journal of Primatology, 77(11), 1207e1215.
 
Zannella, A., Stanyon, R., Maglieri, V., & Palagi, E. (2021). Not all yawns tell the same story: The case of Tonkean macaques. American Journal of Primatology, 83(7), Article e23263.
 
Zannella, A., Stanyon, R., & Palagi, E. (2017). Yawning and social styles: Different functions in tolerant and despotic macaques (Macaca tonkeana and Macaca fuscata). Journal of Comparative Psychology, 131(3), 179e188.
 
Zethof, T. J., Van Der Heyden, J. A., Tolboom, J. T., & Olivier, B. (1994). Stress-induced hyperthermia in mice: A methodological study. Physiology & Behavior, 55(1), 109e115.
 
Zilli, I., Giganti, F., & Salzarulo, P. (2007). Yawning in morning and evening types. Physiology & Behavior, 91(2e3), 218e222.
 
Zilli, I., Giganti, F., & Uga, V. (2008). Yawning and subjective sleepiness in the elderly. Journal of Sleep Research, 17(3), 303e308.
A. C. Gallup / Animal Behavior 187 (2022) 209e219 219