Contagion

Behavioral contagion - the tendency to unconsciously imitate the attitude, manners, facial expressions and behaviour of others. An interesting aspect of human social life that has been widely described in the literature, also known as the chameleon effect.

One good introductory video serves better than a hundreds of words. Let’s then start this chapter with a little video on contagious yawning (the most frequently examined behaviour in respect to contagion).

As you could hear on the video, there are several hypotheses that could explain why the yawning is contagious. Three of those were presented: yawning is a reflex (fixed action pattern), yawning is related to mirror neurons activity, and yawning is socially contagious behaviour.

A fixed action pattern is an ethological term describing an instinctive behavioral sequence that is highly stereotyped and species-characteristic. Fixed action patterns are said to be produced by the innate releasing mechanism, a “hard-wired” neural network, in response to a sign/key stimulus or releaser. Once released, a fixed action pattern runs to completion. Six characteristics of fixed action patterns have been identified (Páez-Rondón et al. 2018):

• Stereotyped: Fixed action patterns occur in rigid, predictable, and highly-structured sequences.

• Complex: Fixed action patterns are not a simple reflex. They are a complex pattern of behavior.

• Species-characteristic: Fixed action patterns occur in all members of a species of a certain sex and/or a given age when they have attained a specific level of arousal.

• Released: Fixed action patterns occur in response to a certain sign stimulus or releaser.

• Triggered: Once released, a fixed action pattern continues to completion, even when there are changes in the surrounding environment.

• Independent of experience: A fixed action pattern is not learned. This is known as a fixed action pattern is complete upon the very first release.

Mirror neurons are a distinct class of neurons that transform specific sensory information into a motor format. In other words, they fire both when an animal acts and when the animal observes the same action performed by another. Thus, the neurons “mirrors” the behavior of the other, as though the observer were itself acting.

Mirror neurons have been originally discovered in the premotor and parietal cortex of the monkey. Subsequent neurophysiological and brain imaging studies have shown that a mirror mechanism is also present in humans, and very recently it turned out they are also in birds (Mukamel et al. 2010), (Fabbri-Destro and Rizzolatti 2008), (Prather et al. 2008).

According to its anatomical locations, mirror mechanism plays a role in action and intention understanding, imitation, speech, and emotion feeling (Fabbri-Destro and Rizzolatti 2008). Although recent meta-analysis question the crucial role of the frontal mirror neuron area during imitation and suggest that parietal and frontal regions which extend beyond the classical mirror neuron network are crucial for imitation (Molenberghs et al. 2009).

These three (and other) hypotheses are not mutually exclusive. Some part of the behavioural contagion indeed may be a reflex but there are evidence, at least in some species, on mirror neurons taking a great role here, even if not the entire mechanism could be explained with that hypothesis. Importantly, there are evidence that behavioural imitation may have a positive effect on later social life, enhancing relationships, liking others and smoothing social interactions. It may also increase the likelihood of displaying other prosocial behaviours, such as helping others. Contagious behaviours that facilitate group living are therefore likely to be evolutionarily adaptive. For sure, different mechanisms and functions may be related with behavioural contagion in various species, and they may exhibit similarities in contagious behaviours either because of a common ancestor or as a result of convergent evolution. We are still far from understanding how common the phenomena is and what exactly the contagion serves for but what we know so far is truly fascinating.

Examining behavioural contagion in animals is not an easy task (as it is often the case in studies on animal behaviour) but the number of studies and number of studied species are continuously growing. Various behaviours are considered but everything has started and still very much focus on yawning.

Contagious yawning has been demonstrated in social mammals such as primates (chimpanzees, bonobos, geladas; (Palagi et al. 2009), (Demuru and Palagi 2012), (Massen et al. 2012)), carnivores (wolves and domestic dogs) (Romero et al. 2014), and more recently also in social birds (budgerigers; Gallup et al. 2015).

Sometimes some sex-differences may be exhibited in responsiveness to contagious yawning. For example yawn contagion in the chimpanzee (Pan troglodytes) was significantly higher when the video model was a yawning male than when the video model was a yawning female, and that this effect was most apparent among males. As males are dominant in chimpanzee societies, male signals may be more relevant to the rest of the group than female signals. Moreover, since chimpanzees form male-bonded societies, male signals may be especially relevant for other males. Therefore, sex-differences of yawning contagion among chimpanzees may reflect the function of yawning in the synchronisation of behaviour (Massen et al. 2012).

Mean proportion of videos to which each individual responded with a yawn: males’ (n = 3) reaction to male yawn videos (MM), males’ reaction to female yawn videos (MF), females’ (n = 11) reaction to male videos (FM), and females’ reaction to female videos (FF). *p>0.05. From Massen et al. 2012.

Interestingly, and what has already been denoted in the introductory video, the contagion very much depends on the participants of the interactions. Apparently, the stronger the bond is between the “demonstrater’ and the “observer” the more likely the contagion is to happen and it strongly suggests the adaptive function of the contagious behaviour.

A good example is the study on dog puppies (Madsen and Perrson 2013). When experimenter was unfamiliar the puppy did not respond to the stimulus. In contrast, when puppy observed familiar individual yawning repeated the behaviour (video). Interesting, this propensity to behavioural contagion changes over the time. Very young puppies didn’t respond to the yawning of experimenter, does not matter they were familiar or not. This shows that contagious yawning in dogs can’t be a simple reflex (otherwise tested puppies would respond to the stimuli regardless of age).

From Madsen and Perrson 2013

Another behaviour relatively frequently considered in the context of contagion is stretching, that is thought to be an ‘accompanying response’ to yawning. It has been reported to be contagious in some species, such as budgerigers (Gallup et al 2017).

In one of the studies on budgerigers stretching was significantly more frequent when the birds could see each other, so we could say they inspired themselves to stretch. Contrary to the aforementioned study on puppies, however, there was no difference in the frequency of stretching when paired birds with well-known and unknown individuals were compared (Gallup et al 2017).

Stretching was significantly more common when birds could see one another, but there was no difference in stretching frequency when comparing birds paired with familiar and unfamiliar conspecifics. From Gallup et al 2017.

Other more species-specific contagious behaviours have also been reported: contagious jump-yip in prairie dogs (Hare et al 2014); contagious scent marking in marmosets (Massen et al 2016), and contagious play in ravens (Osvath and Sima 2014).

Results about contagious behaviour in animals may not consistent across species, although we need to be very careful here when drawing conclusions (see below). For example, two lemur species - ring-tailed lemurs (Lemur catta) and Verreaux’s sifaki (Propithecus verreauxi) - did not respond to yawning in an experimental study. Such a differences in response of closely related species (other primates) may very much important to understand the evolution of the behaviour and its functionality – the fact that contagion exists in some species but not the others (while they have so much in common due to genetic relatedness) indicates that contagion has an important function in given species, and the present pattern may be the result of the subsequent evolution of this behaviour, following the separation of the two main primate lineages (Reddy et al 2016).

Ring-tailed lemurs and ruffed lemurs were exposed to video projections of yawning conspecifics in the group and individual context. The figure presents the number of individuals who yawned in individual and group contexts in experiment. From Reddy et al 2016.

By the way, the presented figure is an example of a bad figure. If the situation is like that the figure is rather redundant, just saying that three of n individuals (n%) responded to the treatment would be enough.

It is also worth to highlight here the question of negative results. These are always tricky to interpret, as lack of individuals response could be the question of behaviour evolution (the assumption/interpretation of the study) but to conclude that one has to rule out the alternative explanations related to responsiveness of the individual to the experimental treatment. Here the experiment was carried out with presenting video footage to the individuals. What if lemmurs do not yawn being exposed to video footage with another yawning individual because of specifity of the treatment??

Let’s now consider another study of yawning contagion, this time with non-social species. Given one of the most commonly evoked hypothesis on the functionality of contagious behaviour (social life enhancing), we would not expect contagion here. As expected, the study performed by Wilkinson et al 2011 on red-footed tortoise showed no evidence of yawning contagion. Fortunately, here the experiment was quite well thought. To do it, researchers used a demonstrator tortoise that was conditioned to yawn when presented with a red square-shaped stimulus. Observer tortoises were exposed to three conditions: a yawning condition in which they observed a single conditioned yawn; a control condition in which a conspecific was present but did not yawn; and a second control condition in which the red square-shaped stimulus was presented without the presence of the demonstrator. Then the number of yawns for each observer animal in each condition was counted. The results showed that tortoises yawned indeed but regardless of the behaviour of the individuals they were watching.

The total percentage of yawns of all subjects in (bar a) the experimental condition in which the tortoises observed the demonstrator perform a single con- ditioned yawn (bar b) the no yawn control condition in which the demonstrator was present but did not perform the conditioned yawn and (bar c) the no demonstrator control condition in which the stimulus was presented but the demonstrator was not there. From Wilkinson et al 2011.

But interestingly, other tortoise are responsive to other behaviours such as following a gaze (Wilkinson et al. 2010). How would you interpret that??

The percentage of trials in which the tortoises responded by looking up. The whiskers represent the standard error. From Wilkinson et al. 2010.

Intepretation: Gaze following refers to the ability of an animal or human to orient its gaze direction to that of another organism. This is highly adaptive as it can alert the observer to important objects in the environment such as food or predators (it may have not much to do with social life). A precursor to gaze following is gaze sensitivity. The “evil-eye hypothesis” proposes that gaze sensitivity evolved as an anti-predator response Hampton 1994. A propensity to avoid the gaze of another (particularly a predator) allows an animal to judge when it is safe to move or come out of hiding Hampton 1994. Gaze sensitivity is a prerequisite for gaze following. In other words, gaze following is very much relevant/adaptive behaviour, so one can expect it to be exhibited even in non-social species; following someone else eye/head movement may lead to find a mate/partner/predator. The ability to follow a gaze may also result from a general ability to learn, here demonstrated in reptiles.

A study case - the elephant seal

The the elephant seals (Mirounga leonida) is one of the most polygynous mammalian species, in which a fierce inter-male competition is a core component of social life. During the breeding period, a single male usually holds sway over a group of up to 100 females. During the moulting (study period in the present study) that follows breeding, individual animals do not have stable bonds or relationships, but they remain gregarious, even though the groups are fluid in space and time .Since contagious behaviours are believed to facilitate group living in general one may expect such a behavioural system in this gregarious species.

There behaviours were considered here:

“sneezing”, yawning, scratching – two of those very much specific for the species/period and the other the most studied, and also exhibited by the seals during the study period. When you look at the group of the elephant seals, and consider these behaviour, you may have an impression they are performed in a time-clustered manner. So the question is whether it is just a coincidence or indeed we have a pattern, and if there is a pattern perhaps there is a contagion involved (pattern -> rule, see the chapter #3).

To test this spontaneous behaviour of individuals in a group was video-recorded, and then manually processed to annotated timestamps for all the occurrence of the considered behaviour. Then time intervals between the consecutive events of all three behaviours were calculated, and based on that the frequency of very short time intervals (<5 sec). To test how this frequency was different from that what could happened by chance a randomization procedure was applied (see details in Wojczulanis-Jakubas et al. 2019).

Results showed that indeed the behaviours exhibited by elephant seals are clustered in time, and so that could be a result of contagion.

Literature cited

Demuru E, Palagi E (2012) In Bonobos yawn contagion is higher among kin and friends. PLoS One 7:e49613. doi: 10.1371/journal.pone.0049613

Fabbri-Destro M, Rizzolatti G (2008) Mirror neurons and mirror systems in monkeys and humans. Physiology 23:171–179. doi: 10.1152/physiol.00004.2008

Gallup AC, Militello J, Swartwood L, Sackett S (2017) Experimental evidence of contagious stretching and ingroup bias in budgerigars (Melopsittacus undulatus). J Comp Psychol 131:69–72

Gallup AC, Swartwood L, Militello J, Sackett S (2015) Experimental evidence of contagious yawning in budgerigars (Melopsittacus undulatus). Anim Cogn 18:1051–1058. doi: 10.1007/s10071-015-0873-1

Hampton RR (1994) Sensitivity to information specifying the line of gaze of humans in sparrows (Passer domesticus). Behaviour 130:41–51

Hare JF, Campbell KL, Senkiw RW (2014) Catch the wave: prairie dogs assess neighbours ’ awareness using contagious displays. Proc R Soc B-Biological Sci 281:20132153. doi: 10.1098/rspb.2013.2153

Madsen AE, 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. Anim Cogn 16:233–240. doi: 10.1007/s10071-012-0568-9

Massen JJM, Šlipogor V, Gallup AC (2016) An observational investigation of behavioral contagion in common marmosets (Callithrix jacchus): Indications for contagious. Front Psychol 7:1–11. doi: 10.3389/fpsyg.2016.01190

Massen JJM, Vermunt DA, Sterck EHM (2012) Male yawning is more contagious than female yawning among chimpanzees (Pan troglodytes). PLoS One 7:1–5. doi: 10.1371/journal.pone.0040697

Molenberghs P, Cunnington R, Mattingley JB (2009) Is the mirror neuron system involved in imitation? A short review and meta-analysis. Neurosci Biobehav Rev 33:975–980. doi: 10.1016/j.neubiorev.2009.03.010

Mukamel R, Ekstrom AD, Kaplan J, et al (2010) Single-Neuron Responses in Humans during Execution and Observation of Actions. Curr Biol 20:750–756. doi: 10.1016/j.cub.2010.02.045

Osvath M, Sima M (2014) Sub-adult ravens synchronize their play: a case of emotional contagion ? Anim Behav Cogn 1:197–205. doi: 10.12966/abc.05.09.2014

Páez-Rondón O, Aldana E, Dickens J, Otálora-Luna F (2018) Ethological description of a fixed action pattern in a kissing bug (Triatominae): vision, gustation, proboscis extension and drinking of water and guava. J Ethol 36:107–116. doi: 10.1007/s10164-018-0547-y

Palagi E, Leone A, Mancini G, Ferrari PF (2009) Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci 106:19262–19267

Prather JF, Peters S, Nowicki S, Mooney R (2008) Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451:305–310. doi: 10.1038/nature06492

Reddy RB, Krupenye C, MacLean EL, Hare B (2016) No evidence for contagious yawning in lemurs. Anim Cogn 19:889–898. doi: 10.1007/s10071-016-0986-1

Romero T, Ito M, Saito A, Hasegawa T (2014) Social modulation of contagious yawning in wolves. PLoS One 9:. doi: 10.1371/journal.pone.0105963

Wilkinson A, Mandl I, Bugnyar T, Huber L (2010) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769. doi: 10.1007/s10071-010-0320-2

Wilkinson A, Sebanz N, Mandl I, Huber L (2011) No evidence of contagious yawning in the red-footed tortoise Geochelone carbonaria. Curr Zool 57:477–484

Wojczulanis-Jakubas K, Plenzler J, Jakubas D (2019) Indications of contagious behaviours in the southern elephant seal : an observational study. Behaviour 156:59–77. doi: 10.1163/1568539X-00003530