Humans are the only species that smiles.
Other apes do not smile, nor do dogs smile. Apes “fear grin” and dogs bare their teeth in “agonistic puckers” and “submissive grins.” Humans are entirely unique in all of the animal kingdom by expressing ease, pleasure and amusement by raising the corners of our mouth and exposing our teeth.
Even so, the human smile is believed to have evolved out of the grimace. The most that can be said towards the commonality of smile-like behavior among humans, apes, and dogs is that baring the teeth is sometimes used to influence the attitude of the viewer during an uneasy greeting. Whereas humans are often genuinely confident and cheerful in this display, ascribing a happy and sure attitude on to animals that are baring their teeth is an ignorant and deluded form of anthropomorphism.
The Grimace, Fear-Grin, or Smile
The silent bared-teeth grimace with corners of the lips drawn back, is general to monkeys and apes when expressing fear or intending to appease. Grimaces or grins are made routinely by lower-ranking adults or juveniles towards a dominant individual, male or female. When monkeys grimace at a dominant it resembles nothing so much as a human ingratiating smile.
It should be noted in relation to the smile or grin that the social contexts and purposes of seemingly familiar facial displays among monkeys and apes can be quite different from those in human societies (Preuschoft & van Hoff 1995). Functional adaptations during the course of evolution may have created different forms, uses, and contexts for any given display even if the displays in question may be homologous (ultimately deriving from shared ancestors).
In rhesus macaques, the bared-teeth display is almost always made only from subordinate to dominant individuals as a signal of submission (de Waal & Luttrell 1985). Emphasizing the proximate level of explanation, there are questions about the degrees of intentionality that the use of this signal could reflect. If it is first-order intentionality then the signaller wants to influence the actions of the other, to reduce the likelihood of aggression. If it is second-order intentionality these subordinate monkeys are sending a message to dominants that they accept their lower status (Maestripieri 1996); perhaps we could even say, with intention to modify their attitudes. From a functional point of view, the bared-teeth display is an expressive appeasement signal, it effectively reduces the risk of attack and there is little more to add.
–Developing a Social Psychology of Monkeys and Apes by John K. Chadwick-Jones 1998
Notice how the anthropologist is careful to dissuade the reader from attributing human motivations to ape behavior. We should follow this advice when examining canid behavior as well. In general, dog owners are horrible readers of canine body language and signaling; they all too often impute human motivations on to their dogs such as duplicity, contempt, or the desire to subjugate their humans by establishing a higher status in the “pack.” This nonsense only leads to trouble.
Thus we shall limit our discussions of canine behavior and emotion to commonalities that we can substantiate instead of assume so as to not inject false meaning. It is not anthropomorphism to discuss emotions and behaviors that are common to both dogs and humans, as we are not imparting human-only traits on to dogs, but we must be careful to not be overly generous in assuming that commonality.
Dog behaviors that can are colloquially referred to as smiles can be broadly grouped into three categories: the submissive grin, the greeting grin, and the agonistic pucker.
The Submissive Grin
The submissive grin is a behavior in which a canid retracts the lips horizontally revealing their teeth. It represents passive submission, is a distance reducing submissive signal, and is intended to pacify or appease the response of an approaching animal. The following several passages are from Canine Behavior: Insights and Answers by Dr. Bonnie V. Beaver, the Executive Director of the American College of Veterinary Behaviorists and President of the AVMA.
Distance-Reducing (Submissive) Signals
Body signs that tend to decrease a threat or encourage an approach are classified as distance-reducing, or submissive, signals. Showing submission helps stop or attenuate aggression or punishment by a more dominant dog, (Hart 1978) and puppies quickly learn the usefulness of these signals as appeasement gestures (Shepherd 2002). It represents an effort by a lower ranking animal to attain a harmonic social integration and assumes that the higher ranking individual will respond appropriately (Clutton-Brock 1981, Schnekel 1967). This type of communication can be broadly divided into three categories: passive submission, active submission, and play (Beaver 1981, Beaver 1994, Fox 1972).
These signals are highly analogous to the appeasement gestures in apes referenced above. The submissive grin falls in the category of passive submission.
The body signals of passive submission are derived from postures the young adopt when being cleaned by their mother (Schenkel 1967). These signals range from the very subtle to the very extreme (Fox 1972). At the subtle end of the scale is the simplest of responses–that of avoiding direct eye contact. Progressively more obvious signs may follow in any order. The dog will tend to lower the ears back against the neck, and the head will be lowered as the neck is lowered and extended forward or twisted sideways. The lowered years, head, and neck for submission must be carefully interpreted to be consistent with other body signs because of the similarity with signals used by aggressive dogs. The tongue can flick in and out, or the more dominant animal may be licked in greeting (Fox 1977, Simpson 1997). A submissive grin, with its horizontal retraction of the lips, may be observed (Fox 1977). If the submissive dog is touched, it will hold completely still.
The tail is held lower, often between the legs, as an indicator of fear or submission. It may be wagged there. Tail wagging has been equated with a human’s smile and can be used as an index of emotionality (Kiley-Worthington 1976). Motion in the tail should be viewed cautiously though. The flagging of dominance, while stiffer, more upright, and more rigid, is still easily confused with the wagging of submission.
So here we have a renowned canine behaviorists pointing out that the dog’s tail, not its lips, are a more appropriate signal of emotionality to compare with the complexity of the human smile and that the submissive grin is a signal of submission not of joy.
It is important to note that submissive postures are often associated with fear. In addition to the tendency to shrink in size, dogs may also tremble, freeze in place, or run away. There are physiologic changes of stress that can include increased salivary cortisol levels (Beerda 1998).
A few dogs that are passively submissive will show the “mimic grin” facial expression (left, Beaver 1981). The expression is easily confused with an aggressive one because of the bared teeth, but with the mimic grin, all other body signals indicate submission. Although some authors feel the mimic grin is a learned behavior (Fox 1972), it is most likely an inherited submissive behavior, as it is common in certain bloodlines in both purebred and mixed-ancestry dogs.
The “mimic grin” mentioned here is the very same submissive grin we’ve been discussing and given the behavioral context for its use it is highly correlated with the fear grin we see in apes. While this form of grinning is not overtly aggressive, we must remember that fear is a real component in canine submissive behaviors and that fear can lead to fear-biting. The failure of a human to read the increasing distress of a timid dog during an encounter can lead to a bite:
The person’s presence becomes more threatening instead of less so, and the dog increases its submissive response or avoidance to the maximum extent. Eventually, the perception of threat can become so great that a warning fear-bite may occur as an attempt to stop the progression of events.
This is why it is so critical that we do not confuse a signal of fear and anxiety with confidence and joy by calling it a “smile” the way we’d most often interpret that word in human encounters.
The Greeting Grin
A similar but distinct canid behavior is the Greeting Grin which is distinguished from the Mimic or Submissive Grin by lacking the display of teeth. Because of this, the Greeting Grin is rarely misinterpreted by laymen as a canine “smile.” The Greeting Grin is a form of active submission by the dog.
Individual dogs use active submission significantly more often than passive submission. This behavior pattern is derived from the puppy’s initial begging for milk and food, olfactory investigation, and receiving anogenital licking from the mother (Clutton-Brock 1981, Kiley-Worthington 1976, Schnekel 1967).
The most distinguishing characteristic of active submission is the approach of the dog to a person or other dog. The approach is usually accompanied initially by the head and tail held high as the dog bounds forward. Tail wagging is common when a dog greets a social peer or superior (Kiley-Worthington 1976).
Once the dog has reached its goal, it will show one or more signs of passive submission: diverted eyes, lowered head, immobile response to touch, submissive urination. Shortly after acknowledgment, the dog may bound around again.
The “greeting grin” is associated with active submission (left) (Beaver 1981, Fox 1972). This facial expression resembles a human smile, with the corners of the mouth pulled back (Fox 1972). It is seen only in human-dog interactions, not in dog-dog ones (Fox 1976).
Because this display represents more confidence in the dog–whereas the submissive grin suggests little–this behavior is known to progress in intensity and positivity into a more playful and happy countenance: the play face.
The “play face” expression is an intensification of the greeting grin (Fox 1972, Fox 1977). The ears are erect and forward, anatomy permitting, and panting may occur. At the same time, the tail is often high and wagging while the front is in the play bow (Fox 1972).
This is the most appropriate behavior that humans should associate with “smiling” in dogs. Note that the mouth is open but the lips are not retracted in a way to bare the front teeth, the whisker pad is relaxed, the brow is not furrowed, the ears are active and forward, and the tail is engaged. The dog is not sending mixed signals and is truly at ease and inviting positive interactions without fear. By its effect, the play face is a distance reducing behavior (come play with me!). This behavior is often coupled with the “play bow.”
The above “grins” belong to the distance-decreasing set of behaviors where the dog either actively or passively eases an approach by another dog or human that is the dominant actor. There is, however, another behavior that is related in expression which is used instead to increase the distance of the approaching or approached actor.
The Agonistic Pucker
This behavior falls in the dominant, aggressive, and agonistic type of signals.
In the case of canine interactions “agonistic” is most often used to refer to aggressive behavior but can also include behaviors related to dominance displays, submission, and defensiveness.
According to the University of Wisconsin, primate glossary, agonistic refers to:
A range of fighting or competitive behaviors between members of the same species, including attack, threat, appeasement/conciliation, or retreat/flight; regarding aggressive encounters including offensive attacks as well as defensive fighting. (Handleman 2008)
This display, although it can often be expressed in much the same way as a submissive grin is correctly called a “snarl” in lay-speak.
The technical term for an offensive warning snarl.
During an agonistic pucker, the canid’s lips are drawn away from the teeth exposing the incisors and canine teeth; the skin above and to the sides of the nasal plane (nose pad) wrinkles; the corners of the mouth are drawn forward shortening the commissures; the tongue may be drawn back in preparation for a bite, or it may protrude to create a combination of an agonistic pucker with a tongue flick/distancing signal. (Handleman 2008)
Direct eye contact, with eyelids wide open—the stare—is the most subtle of threats but one generally recognized among dogs. Its use effectively settles disputes between most dogs, minimizing the need for escalation of the confrontation and reducing the potential for life-threatening injuries.
The mouth shows the next signals when the lips are pulled back at the corners and eventually retracted vertically into a snarl (bared teeth) (Fox 1977). The aggressive gape also shows teeth, but adds a partially open mouth (Fox 1970). The head, neck, and ears are elevated during the initial phases of distance-increasing communication, but as the threat becomes more intense, they may be lowered.52 This is to protect the throat and ear pinnas during an actual attack. This lowered position can resemble the posture of passive submission, but each leads to a very different next step.
Behaviors and emotions are complex and stochastic, they are not always deterministic and unique and monotonic. What appears to be the same behavior can be sending different messages depending on the context and combination of other signals. Dogs can and do send mixed signals. The first lesson we need to learn, however is that we can and should not anthropomorphise our dog’s behaviors because we think they look like something we understand more clearly in human behavior.
In the next post I’ll examine why learning the root cause and motivation behind certain behaviors like the submissive smile are crucial to understanding the serious side of canine behavior; namely, when it goes wrong and they bite.
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