MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus)

AU1+2 (inner and outer brow raiser)

FACS describes independent movements of the inner and outer portion of the brow; however, clear independent movements were not observed in either species of macaques. Thus, the action units AU1 and AU2 have been jointed into a single combined movement AU1+2 describing the raising and lifting of the browline. This movement reveals greater surface area in the underbrow region, so visibility of the underbrow is a particularly salient appearance change for identifying this movement in Barbary macaques (Video S1). Also, depending on the curvature of the brow in the monkey’s neutral state, AU1+2 can function to curve the brow into a smooth arc. A final appearance change of AU1+2 is that it can create a bulging of the hair superior to the brow region. This is achieved by the contraction of the frontalis muscle.

In the Barbary macaques, we observed the use of unilateral AU1+2 in three different individuals (Fig. 2) that has not been reported in rhesus macaques. The unilateral AU1+2 was observed in natural context with non-social behaviours when the individuals glanced to the left or right. This movement was not associated with a feeding context only, where a subordinate would have to pay attention to his/her surrounding and look for the presence of dominant individuals. The unilateral AU1+2 was also exhibited when an individual was sitting alone.

This facial movement of the brows was the most common expression observed through the 30 h of footage collected (AU1+2 = 20.30% of the AUs produced within the 190 scored video clips; see Table 3). The frequency of a given AU was calculated as the ratio between the number of times a specific AU was produced within the 190 video clips coded and the total number of AUs produced within the 190 clips. As the sample was ad libitum, we deemed this frequency measure more appropriate than signals per hour. Moreover, during direct observations at the Monkey Haven, the individuals presented this behaviour not only when presented with cognitive tasks but also as natural, spontaneously occurring expression.

AU41 (glabella lowerer)

One of the most conspicuous movements in the FACS is AU4, the brow lowerer (used primarily in human frowning/anger (Ekman & Friesen, 1978; Friesen & Ekman, 1983)). This is achieved by the contraction of three muscles, the corrugator supercilii, depressor supercilii and procerus, which results in both a lowering and medial contraction, e.g., knitting of the brow. FACS also reports individual AUs for the contraction of each muscle independently, AU41 (procerus), AU42 (depressor supercilii) and AU44 (corrugator), although it is very rare that these can be differentiated in humans. Although clear brow lowering movements were observed in rhesus macaques (Parr et al., 2010), the medial contraction, or knitting, characteristic of AU4 in humans was not observed. In MaqFACS, Parr et al. (2010) reported that the brow lowering movement appears to consist mostly of a medial bulging in the glabella region due to the action of the procerus. Because of this, brow lowering in MaqFACS is specifically identified as AU41 (glabella lowerer). This movement pulls the brow downward, reducing the visibility of the underbrow and changes the curvature of the brow such that it becomes lowered at the midpoint (Video S3).

In Barbary macaques, the medial bulging in the glabella region is less pronounced or less visible due to the fur of the individuals. However, the lowering of the brow line and the reduced visibility of the underbrow are present. The change in the curvature of the brow is not conspicuous but we do observe clearly the lowering of the central part of the browline.

AU9 (nose wrinkle), AU10 (upper lip raiser)

In FACS, the movements of AU9 and AU10 can be tightly coupled. Extreme nose wrinkling, for example, functions to raise the upper lip slightly, and many expressions in humans combine AU9+AU10, as in disgust (Friesen & Ekman, 1983). In the rhesus macaques, the AU9, by itself, can be difficult to detect. However, a combined AU9+AU10 has been observed, in addition to the independent action of AU10. Therefore, in describing these two movements, MaqFACS have attempted to describe the appearance changes of each, although in most cases AU9 would be reported in combination with an AU10. The AU9+10 is achieved by the contraction of two muscles, the levatorlabii superioris alaeque nasii and the levatorlabii superioris; the contraction of the latter result in AU10 alone.

In addition to the action of AU10, which pulls the upper lip upward in a smooth arc causing wrinkles and furrows in the infra-orbital triangle, AU9 in MaqFACS functions to pull the nose upward, causing oblique nose wrinkles to deepen. AU9 alone pulls the lateral aspect of the nostril wings upward and medially towards the root of the nose, which causes the nasal groove to deepen.

In Barbary macaques, the conjuncture of AU9 and AU10 is marked by the deepened wrinkles on the infra-orbital furrow and a shortened nasal groove (Video S4). Unique occurrence of AU9 was not observed, as in the rhesus macaques.

AU12 (lip corner puller)

The function of AU12 is to pull the lip corners back and slightly upward in a movement that produces the homologous expressions of human smiling and the rhesus macaque bared-teeth displays (Parr et al., 2010). This is achieved by contracting the zygomatic major. AU12 functions to retract the lips laterally and upwards towards the ears. It narrows and slightly bulges the upper lip, reducing the visibility of the vertical lip ridge and deepening the furrows at the mouth corners (Video S5). In both rhesus and Barbary macaques, AU12 also creates oblique wrinkles and deepens the furrows of the infraorbital triangle, one of its most prominent appearance changes.

AU16 (lower lip depressor)

The appearance changes associated with AU16 are common to humans and rhesus macaques, despite considerable differences in the morphology of the lips, e.g., thick red reverted lips in humans, and thin lips (appearing to invert) in rhesus and Barbary macaques. Appearance changes associated with AU16 (contraction of the depressor labii inferioris) include lowering the bottom lip to expose the teeth and lower gum. In both rhesus macaques and Barbary macaques, AU16 also causes a slight eversion of the lower lip, which may cause the inner portion of the lip to appear to thicken slightly. AU16 can also increase the curvature of the lower lip by pulling the medial aspect downwards towards the chin, in contrast to the resting shape of the mouth, in which the medial portion of the lower lip can appear to turn upward.

AU18i/AU18ii (true pucker and outer pucker)

In FACS, there are two main movements responsible for protruding the lips: AU18—the lip pucker, e.g., when kissing, and AU22—the lip funneler, which pushes the lips outward as if saying the word “flew.” In the rhesus macaque, however, lip puckering was attributed to two movements.

The first is a pucker similar to AU18 in humans and referred as AU18i, the true pucker, in MaqFACS. To achieve this movement, three muscles appear to be needed: the orbicularis oris, the incisivii labii superioris, and the incisivii labii inferioris. The AU18i purses the lips medially forward towards each other, narrowing the mouth corners medially, protruding the lips and reducing the mouth aperture in both the horizontal and vertical directions. This movement causes distinct oblique wrinkles to appear extending from the cheek along the length of the upper lip. Because rhesus and Barbary macaques do not have reverted lips, this movement causes the medial portion of the lip to take a scalloped appearance on either side of the midline as the lips are pursed forward. AU18i causes the philtral region to deepen and produces a depression in the medial portion of the lower lip causing it to appear slightly curved (Video S6).

The second lip protrusion movement observed in macaque species contained distinct appearance changes from AU18i, but was also insufficient to be labelled AU22. This movement is instead described as AU18ii, the outer pucker, in which the lips and the lower jaw are pushed forward so as to protrude slightly, causing oblique wrinkles to extend from the cheek along the upper lip. What distinguishes this movement from AU18i is that the furrow between the nose and upper lip (philtral region) is reduced and the lips cinch together at a point distal to the midline causing them to part and appear inflated. Also the movement of the lower jaw helps coding AU18ii. We speculate that the AU18i is produced by the joint action of orbicularis oris, incisivii labii superioris, and incisivii labii inferioris while the movement of AU18ii is produced by contraction of the incisivii portions specifically (incisivii labii superioris and inferioris). This variant was observed as it is described in the MaqFACS in Barbary macaques but was really rare: only two individuals, one in each group, were observed doing an AU18ii (Video S7).

In addition to these, MaqFACS includes an action descriptor, AD181 (lip smacking, contraction of the orbicularis oris), to denote tightening of the lips together followed by a rapid opening and parting motion, which is a common facial movement associated with AU18i and the lip-smacking expression of the rhesus macaque. In Barbary macaques, the ‘lip smacking’ is present also associated with a bared-teeth display. Hence, the Barbary macaques present both a lip-smacking and a teeth chattering (Wiper & Semple, 2007), that was not reported in rhesus macaques.

EAU1 (ears forward), EAU2 (ears elevator), EAU3 (ears flattener)

Unlike many mammals, humans lost the ability to move their ears independently. Therefore, FACS does not contain descriptions of ear movements. Among rhesus and Barbary macaques, three prominent and independent ear movements are described. EAU1 (ears forward) functions to push the ears forward towards the face via the contraction of the anterior auricularis, increasing the visibility of the ear if viewed from a frontal orientation, but reducing the visibility of the ear if viewed in profile (Video S8). EAU2 (ear elevator) pulls the ears superiorly towards the top of the head; this movement if still present in the Barbary macaques appeared less common than in the rhesus macaques or less easy to observe due to the facial fur of the Barbary macaques (Video S2). This results from the contraction of the superior auricularis. Finally, EAU3 (ear flattener) pulls the ears towards the back of the head, flattening them against the skull, by contracting the posterior auricularis. This may reduce the visibility of the ears if viewed from a frontal orientation, but increase the visibility of the ears if viewed in profile (Video S3).

It should be noted that coding specific EAUs can be very difficult if the neutral position of the ears is unknown, e.g., an EAU1 may actually be the release of an EAU3. Moreover, fighting among macaques often injures the ears, and these injuries can reduce the visibility of the pinnae that are required to denote the appearance changes described above. Also, the Barbary macaques present an abundant facial fur, which makes it even more difficult to code subtle ear movements (Fig. 1). Thus, in the MaqFACS, it is recommended that users code an EAD, Ear Action Descriptor, to denote movement of the ears without specifying its muscular basis unless there is clear sufficient evidence about the neutral position of the ears to justify a specific EAU code.