Primates

DOI 10.1007/s10329-016-0558-7

ORIGINAL ARTICLE

The first smile: spontaneous smiles in newborn Japanese

macaques (Macaca fuscata)
Fumito Kawakami1 • Masaki Tomonaga1 • Juri Suzuki1

Received: 6 January 2016 / Accepted: 19 July 2016

© Japan Monkey Centre and Springer Japan 2016

Abstract Spontaneous smiles are facial movements that are characterized by lip corner raises that occur during irregular
sleep or drowsiness without known external or internal causes. They are shown by human infants and infant chimpanzees.
These smiles are considered to be the developmental origin of smiling and laughter. There are some case studies showing
that spontaneous smiles occur in Japanese macaques. The goals of this study were to investigate whether newborn Japanese
macaques show a considerable number of spontaneous smiles thus to exam- ine the mechanism of them. Seven newborn
Japanese macaques were observed in a room for an average of 44 min, and incidental sleeping situations were
monitored twice. All seven participants showed spontaneous smiles at least once during the observation. They showed 8.29
spontaneous smiles in average (SD = 10.89; 58 smiles in total), all found in the state of REM sleep. Thirty-nine of the 58
smiles were produced on the left side of the mouth. These characteristics were similar to those of spontaneous smiles in
human infants. This is the first evidence that macaques as well as hominoids show a considerable number of spontaneous
smiles. These phenomena may facilitate the development of the zygomaticus major mus- cle, which is implicated in
smiling-like facial expressions.

Electronic supplementary material The online version of this article (doi:10.1007/s10329-016-0558-7) contains supplementary material,
which is available to authorized users.

& Fumito Kawakami fumito0118@gmail.com

1
Primate Research Institute, Kyoto University, Kanrin,Inuyama, Aichi 484-8506, Japan

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Keywords Smiles · Emotion · Neonates · Allometrictiming constancy

Introduction

Although smiles and laughs have been a topic of interest since the time of Aristotle, Darwin (1872) was the first researcher
who shed light on the phylogeny of smiles and other emotions. In developing his theory of evolution, he recognized and
demonstrated emotions in other species. Although many researchers have revealed that great apes and macaques show
smiling-like expressions (van Hooff 1972), it is not clear how the smiles in humans and other primates are the same or
different.

Humans begin to show smiling-like displays from the fetal period (Kawakami and Yanaihara 2012). Neonates also show
smiles during irregular sleep, drowsiness, and alert inactivity, with no known external or internal causes (Wolff 1959,
1963). These smiles are called spontaneous (neonatal) smiles. Wolff (1959) defined them as a ‘‘slow, gentle, sideward, and
upward pull of the mouth, without rhythmical mouthing movements or contraction of other facial muscles’’ (p. 115). It
should be noted that these researchers do not focus on the emotional aspects of these smiles, but rather on the smiling-like
facial configuration. Shimada (1969) observed that infants do not show spon- taneous smiles in unpleasant conditions, for
example, after crying, but in many circumstances, it is difficult to specify the emotional states during spontaneous smiles.
Never- theless, spontaneous smiles are the first topic in discussions of the development of smiling in many books on devel-
opmental psychology (e.g., Cole and Cole 1989; Messinger 2008, 2009). Preterm neonates tend to show more sponta-
neous smiles than full-term neonates (Emde et al. 1971). In

a series of longitudinal and cross-sectional observations, Spitz et al. (1970) found that spontaneous smiles decrease
gradually by the sixth week after birth, and social smiles increase during the same period of time. Social smiles are so-
called usual smiles, which express feelings of happiness to other people. Ambrose (1961) also showed that social smiles
increase from around 2 months. These observations led to the accepted developmental theory that spontaneous smiles, as
signs of immaturity, disappear at 2–3 months and are replaced by social smiles (e.g., Kagan and Fox 2006; Sroufe and
Waters 1976).

This developmental pathway appears to be simple and reasonable. The actual course of development, however, is not so
straightforward. Kawakami et al. (2007) observed an infant for 6 months and found that spontaneous smiles can be seen in
6-month-olds. Kawakami et al. (2009) demon- strated that even 1-year-olds show spontaneous smiles. These data have
made it difficult to understand the early developmental stage of smiling. Dondi et al. (2010) con- cluded, ‘‘unlike ‘social
smiling’ that emerges later… and has been analyzed in several early and more recent empirical contributions, little is known
about the signifi- cance of neonatal smiles or their developmental relevance for later smiling’’ (p. 116).

Spontaneous smiles were once considered a species- specific phenomenon of humans, but Mizuno et al. (2006) observed
those smiles in chimpanzees. They observed three newborn chimpanzees longitudinally for 4 months and discovered that
two subjects showed 60 spontaneous smiles during irregular sleep. Mizuno et al. compared the fre- quency of spontaneous
smiles and social smiles and found that the former was frequent in infants less than 7-weeks- old and the latter was
frequent in infants older than 8 weeks. Spontaneous smiles disappeared during the sec- ond month in chimpanzees, and
social smiles took their place. There is no evidence that spontaneous smiles were ‘‘replaced’’ by social smiles.

Social smiles in primates are called play faces or relaxed open-mouth displays (ROM). ROM features ‘‘a rather widely
opened mouth, and lips that remain covering all or the greater part of the teeth’’ (van Hooff 1972, p. 217). In geladas, play
face features ‘‘mouth opened with only the lower teeth exposed’’ and full play face features ‘‘lower/ upper teeth and gums
exposed via the actively retraction of the upper lip’’ (Palagi and Mancini 2011). These displays are typically observed in
social play. The silent bared-teeth display (SBT or grimace) is another display which in configuration resembles human
smiles. SBT is character- ized by ‘‘fully retracted mouth-corners and lips, so that an appreciable part of the gums is bared;
closed or only slightly opened mouth; absence of vocalization’’ (van Hooff 1972, pp. 212–213). Although there are
similarities in the morphological configurations of SBT and smiles in humans, SBT expresses submission, not enjoyment.
In the phylogenetic model of smiling and laughter proposed by van Hooff, ROM is linked to more hedonic laughter, and
SBT is related to smiling, a display of non-hostility or friendliness.

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This widely accepted model assumes two pathways of evolution in smiling and laughter (but seeDavila-Ross et al. 2015 for
alternate thesis on the evolu- tionary origin of human laugh faces).

Chimpanzees use ROM and SBT in daily life, as described in numerous studies (e.g., Matsusaka 2004; Preuschoft
2000; Waller and Dunbar 2005). Such displays have also been found in other primates. Preuschoft and van Hooff (1995)
investigated ROM, SBT, and other facialexpressions in 16 species of macaques. Japanese macaques(Macaca fuscata) were
found to show both ROM and SBT. Masataka and Fujii (1980) reported that caged Japanese macaques showed SBT when
submissive males were threatened by dominant males. There is a general lack of data on ROM in Japanese macaques
[Shimada (2014), personal communication]. We observed that wild Japanese macaques and their subspecies, Yaku
macaques (Macaca fuscata yakui) frequently showed ROM and SBT (Kawa- kami, unpublished data). Infant and
adolescent Japanese macaques showed many examples of ROM when they were engaged in social play (Fig. 1a) and SBT
when they encountered conflicts (Fig. 1b).

Species in which the existence of spontaneous smileshas been confirmed also show laughter (ROM) and smiling (SBT).
We previously reported a few cases of spontaneous smiles in Japanese macaques (Kawakami 2009; Kawakamiet al. 2003).
In the present study, we report more intensive observations that have provided data for more detailed analysis. The
purpose of this report is to explore the properties of spontaneous smiles in Japanese macaques and to clarify the aspects of
spontaneous smiles that are the same and different among humans, chimpanzees, and Japanese macaques.

Methods

Participants

Seven newborn Japanese macaques, born and bred in the Primate Research Institute (PRI) of Kyoto University were
observed twice. They were reared by their own mothers and lived together in individual stainless steel cages (0.87 m
W 9 0.8 m D 9 0.87 m H). Average age in days was 10.64 (SD = 5.40), and average weight at the time of observation was
531.71 g (SD = 94.98). Participants were assigned an ID letter by ascending order of their age at the first observation (A–
G), and the number of the observation (1 or 2) was added to the ID. For example, A2 represented
the second observation of the participant who was youngest in the first observation. Table 1 shows basic data for the
participants. There were only two male neonates, so sex differences were not examined. The data reported in this manuscript
were collected from April 2000 to March 2010.

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Fig. 1 Facial expressions in Japanese macaques: a relaxed open-mouth display; b silent bared-teeth display

Table 1 Participant data

ID Sex Age in days Weight (g) Arousal state (min) Frequency of smiles Duration of
smiles (s)
Waking REM Non-REM Left Right Bilateral

A1 F 4 373 35.68 9.95 0 11 3 6 0.97

A2 F 13 486 33.87 8.86 0 2 3 1 0.51
B1 F 5 470 41.65 1.72 0 2 0 0 665.60
B2 F 9 480 37.72 0 0 0 0 0 n/a
C1 F 7 590 58.50 6.03 0 1 0 1 2.17
C2 F 11 633 57.08 11.78 8.10 1 1 1 0.86
D1 M 8 620 40.05 3.63 0 1 0 0 0.88
D2 M 17 695 28.75 8.12 0 0 0 0 n/a
E1 F 9 418 26.47 10.70 0.40 1 0 0 0.86
E2 F 18 528 17.72 10.08 0 20 1 0 0.88
F1 M 3 560 27.94 0 0 0 0 0 n/a
F2 M 10 650 27.42 1.85 0 0 0 1 1.50
G1 F 14 461 45.46 8.70 0 0 1 0 0.50
G2 F 21 480 45.07 3.35 0 0 0 0 n/a
Average 10.64 531.71 37.38 6.06 0.61 2.79 0.64 0.71 23.84
SD 5.40 94.98 11.66 4.19 2.16 5.71 1.08 1.59 174.56

Procedure

The observations were made during sleeping time inci-dental to other research on the calming effect of stimuli presentation
on infant macaques (cf. Kawakami et al. 2002). Each participant was individually brought to a treatment room at PRI
after anesthetizing the mother to shut out the effect of other monkeys and to keep the same experimental conditions for
that research. There were two to four observers including a veterinarian in the room. Observations were conducted on a
table, and participants stayed on it supported by an observer. The observers were careful not to present visual, auditory, or
tactile stimuli that may have induced non-spontaneous smiling responses (Wolff 1963). One observer recorded the
neonate’s face by means of a digital camera recorder (SONY, DCR-PC110) and a tripod en face during sleep. This
procedure took 30–75 min in total. Participants were returned to their cages immediately as possible, and a veterinarian
con- firmed that their mothers hold them as usual.

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Definition of arousal states

The arousal states were divided into three categories: non- REM sleep, REM sleep, and waking (Wolff 1959; Mizuno et al.
2006). Sleeping was defined as the state in which eyes were more than half closed and gross body movements were absent.
During the sleeping period, eye movement and respiratory patterns were carefully checked. If irregular respiration and/or
eye movement was observed, that period was classified as REM sleep.

Definition of spontaneous smiles

The criteria for identifying spontaneous smiles in human infants (e.g., Kawakami et al. 2008, 2009) were adapted for
macaques: (1) involving the raising of lip corners (Ekman et al. 2002); (2) occurring during sleep; (3) occurring with no
known internal or external causes (Wolff 1963); (4) continuing for more than 0.25 s. Internal causes (urination and
evacuation) and external causes (visual, auditory, and tactile stimuli) can elicit smiling responses (Wolff 1963). The
criterion of the minimum duration of a spontaneous smile was modified from human studies (1 s), because many
spontaneous smiles in Japanese macaques are shorter than this, and the present study adopted Gunderson and Sackett’s
observation that maturation of infant macaques is four times faster than that of human infants (Gunderson and Sackett
1984). This criterion was established to exclude very subtle and unrelated movements of the lip corners.

ELAN Linguistic Annotator Version 4.1.0 (Max Planck Institute of Psycholinguistics, Nijmegen, the Netherlands) was
used to play back the images. The onset and offset of smiles were determined as follows. When a smile was observed, the
video was rewound sequentially to the onset frame (immediately prior to which there were no facial movements). From the
onset, the video was forwarded sequentially to the offset (immediately following which there were no facial movements).
Smile peak refers to the moment at which the corner of the lip was maximallyraised.

Laterality of smiles was designated as left-sided (LS), right-sided (RS), or bilateral (BS). LS and RS were also combined
into unilateral smiles (US). During a smile, if the part of the lip that was raised shifted (e.g., from left to right), the final
form was recorded.

Coding

For each participant, the total amount of time in each arousal state was calculated. The measures for spontaneous smiling
included frequency, duration, interval between onset and peak, laterality, and arousal state.

One of two coders identified smiles from the video. Another coder independently judged 20 % of the smiles, which
were randomly selected from all the smiling scenes, with 100 % intercoder agreement. Additionally, two coders
independently identified onset timing in seconds from randomly selected un-edited videos from two observations (74.43
min; 12 % of total observation time). The inter- coder agreement from un-edited video was also sufficiently high (Cohen’s
j = 0.86). The event durations recorded by the two coders were strongly correlated, r = 0.99 (p \ 0.001). Both
coders had experience coding smiles of human infants in previous studies (e.g., Kawakami et al. 2008, 2009).

Data analysis

Correlations of smiling outcomes with age and with weight of participants were conducted. IBM SPSS Statistics Ver- sion
20 (IBM Corporation) was used for analyses of gen- eral linear mixed model and generalized linear mixed model.

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Results

Arousal states

The total observation time was 616.64 min, and the average was 44.05 min (SD = 13.88; Table 1) per participant.
Participants were awake for approximately 85 % of the observation time. Although the amount of sleeping time was limited
in comparison with waking, they slept for 93.27 min (REM sleep: 84.77 min; non-REM sleep: 8.50 min) in total,
almost 91 % of which was REM sleep. The percentage of REM sleep in this study was much higher than human neonates (50
% in de Weerd and van den Bossche 2003) and chimpanzee neonates (33 % in Mizuno et al. 2006). Those data were
obtained from naturalistic observations without any interventions, while in this study saliva sampling and blood sampling
were performed for theparallel research (Kawakami et al. 2002). Those interven- tions might affect the arousal states in this
study.

Spontaneous smiling

Participants showed 8.29 spontaneous smiles in average (SD = 10.89; 58 spontaneous smiles in total) during the observation
time (Table 1). Participants who did not show smiles (i.e., B2, D2, F1, and G2) were excluded from subsequent analyses,
except for the analyses of arousalstate.
Figure 2 shows examples of spontaneous smiles. (Sev- eral video images of smiles are provided as a supplementary
material.) All spontaneous smiles were found in the state of REM sleep. The youngest individual who showed the smile
was 4 days old and the oldest was 18 days old. These data do not mean that spontaneous smiles in Japanese macaques can
be observed in this period of their development specifically, because these were not exhaustive observations, but
incidental ones. There were no correlation between age/weight and frequency of smiles. The average duration of
spontaneous smiles in newborn Japanese macaques was 0.92 s (SD = 0.64). The longest

Fig. 2 Sample pictures of spontaneous smiles in Japanese macaques

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Fig. 3 Average intervals between

onset and peak ofsmiles. Error
bars indicatestandard errors

smile was 3.90 s, which was shown by a 7-day-old neonate (C1). The shortest smiles were 0.43 s, which were shown by 11-
day-old (C2) and 13-day-old (A2) neonates. Sixteen smiles lasted more than 1 s. The average duration of those 16 smiles
was 1.70 s (SD = 0.71). There were no corre- lations between age/weight and duration of smiles.

The intervals between the onset and the peak of the smiles were measured to compare humans and Japanese macaques.
The data of group A in Kawakami et al. (2006) was used for the analysis of human neonates (n = 10, age: M = 4.80, SD =
1.69; birth weight: M = 2914.80 g, SD = 424.70). Human neonates showed 24 spontaneous smiles in the observation.
The average intervals between onset and peak were 0.66 s (SD = 0.25) for each human neonate and 0.20 s (SD = 0.37) for
each newborn Japa- nese macaque (see Fig. 3). A general linear mixed model demonstrated that spontaneous smiles of
newborn Japanese macaques reached their maximum appearance significantly more quickly than those of human
neonates [F (1, 9) = 19.56, p = 0.002, humans: estimated marginal mean = 0.66, 95 % CI (0.51 0.81);
macaques: estimated marginal mean = 0.23, 95 % CI (0.04 0.42)].

Mizuno et al. (2006) observed three infant chimpanzees for 4 months (921 h in total). The infants spent 33 % of this
time in REM sleep, or approximately 304 h (18,236 min). Mizuno et al. observed 60 spontaneous smiles. Japanese
macaques showed 41.05 smiles/h in REM sleep, while chimpanzees showed 0.20 smiles/h in REM sleep. A t test revealed
that Japanese macaques showed more spontaneous smiles than chimpanzees in the respec- tive observation periods [t (6) =
3.195, p = 0.019].

Asymmetry in smile expression

Figure 4 displays the average frequency of smiles for each laterality (LS, RS, and BS). A generalized linear mixed model
demonstrated that unilateral smiles (US) were sig- nificantly frequent than BS (z = 2.84, p = 0.004).

Fig. 4 Average frequency of smiles for each laterality. Error bars indicate standard errors

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Discussion

Spontaneous smiles are facial movements, which are characterized by lip corner raises that occur during irreg- ular sleep
or drowsiness without known external or internal causes. This study revealed that all seven newborn Japa- nese macaques
showed spontaneous smiles at least once during the observation period (58 spontaneous smiles in total). This indicates that
spontaneous smiles in Japanese macaques are not rare cases. Japanese macaques are therefore the third species in which
the existence of spontaneous smiles has been confirmed. All of these spe- cies—humans, chimpanzees, and Japanese
macaques— exhibit social smiles (SBT) and social laughs (ROM). It should be noted that these ‘‘social smiles’’ and
‘‘social laughs’’ are based on morphology, not necessarily emotion. Spontaneous smiles involve the movement of the lip
corner puller (i.e., zygomaticus major). Movement of the same muscle produces smiles in humans and ROM and SBT in
chimpanzees and macaques (Parr et al. 2010), though the lip corner puller is included 19 % of ROM in adult chim- panzees
(Davila-Ross et al. 2015). The function of spon- taneous smiles is still not clear, but it can be speculated that spontaneous
smiles facilitate the development of the zygomaticus major muscle, enabling these species to pro- duce smiles, laughs,
ROM, and SBT. Spontaneous smiles may, therefore, play an important role in emotional development as the origin of
positive facial expressions. To examine the validity of this presumption, it is necessary to observe whether other species
that do not show SBT and/or ROM produce spontaneous smiles and examine the corre- lation between the frequency of
spontaneous smiles and that of SBT and/or ROM. The important result of the present study is that not only hominoids, but
also maca- ques, show spontaneous smiles.

Some researchers have argued that infants’ spontaneous smiles exist to make parents feel that their children are
adorable and to enhance parent–child communication (Takayanagi 2008). Povinelli et al. (2005) assume that
social smiles have the same function. Spontaneous smiles may facilitate caregiving behavior of parents, but this
could not be the principal reason for the existence of these smiles. The occurrence of spontaneous smiles in
chimpanzees, Japanese macaques, and human fetuses supports the view that spontaneous smiles occur for the
benefit of the fetuses, neonates, and infants themselves, and not for other people who happen to see the smiles.
First, the configuration of spontaneous smiles does not express hedonic feelings in chimpanzees and Japanese
macaques.

Their configuration differs from that of ROM in two points: (1) ROM almost always emerges on both sides of the
hemiface, but there are more unilateral spontaneous smiles; (2) typical ROM includes ‘‘lips part’’ (AU25 in
Ekman et al. 2002; Parr et al. 2007), but some spontaneous smiles do not. If chimpanzees and Japanese macaques
see their infants’ spontaneous smiles, they may not recognize them as smiles. Second, as Kawakami and
Yanaihara (2012) pointed out, a special apparatus (i.e., four-dimensional ultrasonography), which has only been
recently invented, is required to see fetal smiles.

The present observations revealed some similarities and differences in the spontaneous smiles of humans, chim- panzees, and
Japanese macaques. Similar characteristics included laterality and the arousal state and age at which they showed the smiles.
The difference was the interval between the onset and the peak of the smiles.

The arousal states in which humans, chimpanzees, and Japanese macaques showed spontaneous smiles were exactly the
same: All showed spontaneous smiles only in the state of REM sleep (humans: Wolff 1959; chim- panzees: Mizuno et al.
2006). In this state, brain activity still occurs, so humans have dreams. It is possible that dreams affect the occurrence of
these smiles, especially for 1-year-old human infants. It is, however, difficult for us to determine whether or not chimpanzees
and Japanese macaques have dreams, much less the content of their dreams. Nevertheless, some mechanisms of REM sleep
must relate to the occurrence of spontaneous smiles, although they remain unclear.

Japanese macaques showed spontaneous smiles from the age of 4 days. Humans show them from the fetal period (Kawakami

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and Yanaihara 2012) and from 1 to 7 days after birth (Wolff 1959; Kawakami et al. 2006), and chimpanzees also from 1 to
7 days of age (Mizuno et al. 2006). There is no data on the fetal period of chimpanzees and Japanese macaques, but all three
species show spon- taneous smiles immediately after birth. All of the partici- pants showed spontaneous smiles at least once
during observation. These indicate that spontaneous smiles areinnately programmed behavior.

The laterality of spontaneous smiles in newborn Japa- nese macaques was similar to that of human neonates; although there
is an asymmetrical tendency that the left side of the face is involved in the production of emotional responses in
chimpanzees (Fernández-Carriba et al. 2002), there are no data on the laterality of spontaneous smiles in them. Participants
in this study showed more unilateral spontaneous smiles than bilateral ones, as do human neo- nates (Kawakami et al. 2006).
In humans, 80 % of spon- taneous smiles are bilateral at 2 months of age, thus there is a developmental change in laterality
of spontaneous smiles (Kawakami et al. 2007). Further investigation is necessary to examine this in Japanese macaques.

The most obvious difference between spontaneous smiles in humans and Japanese macaques was the interval between the
onset and the peak of the smiles. Spontaneous smiles in Japanese macaques reached the peak quicker than humans. This can
be explained in two ways: allometric timing constancy and anatomical differences. Allometric timing constancy is a lawful
timing relation between movement patterns and body mass. Actions performed by species smaller in body mass are much
faster than the same actions performed by larger species (Schmidt-Nielsen 1984; Steiner et al. 2001). Newborn Japanese
macaques are much smaller than human neonates; therefore, the timing difference is reasonable. A difference between
Japanese macaques and humans in the anatomy of the zygomaticus major muscle, which is associated with smiles, may also
contribute to the more rapid peaking of spontaneous smiles in macaques. In Rhesus macaques (Macaca mulatta), the
zygomaticus major muscle is interrupted by the depressor anguli oris muscle unlike humans, which is related to the opposite
facial movement (i.e., lip corner depressor; Bur- rows et al. 2009; Parr et al. 2010). This anatomical feature of Rhesus
macaques would be shared by Japanese maca- ques. Julle-Danière et al. (2015) reported that an anatom- ically based facial
action coding system used with rhesus macaques (Parr et al. 2010) could be used with Barbary macaques (Macaca
sylvanus), which are phylogenetically farther from Rhesus macaques than Japanese macaques (Hayasaka et al. 1996; Li
et al. 2009). A shorter zygo-maticus major would make the size of smiling actionssmaller. If allometric timing constancy
and anatomical difference are indeed related to the duration of spontaneous smiles, this should be reflected in other facial
expressions.Japanese macaques showed 58 spontaneous smiles in 1.41 h of REM sleep (n = 7).

Human full-term neonates showed 24 smiles in 10 h of observation (n = 10) (Kawakami et al. 2006), and infant
chimpanzees showed 60 smiles in 304 h of REM sleep (n = 3; Mizuno et al. 2006). The definitions of spontaneous smiles in
these studies are not completely identical. Japanese macaques and human neonates were removed from their mothers or
caregivers temporarily, whereas chimpanzees were observed via nighttime video cameras from a distance.Although there are
some differences in observational pro- cedures, the frequency/time ratio of Japanese macaques is obviously larger than that
of the other two species. Emde et al. (1971) indicated that preterm neonates showed more spontaneous smiles than full-
terms, so some researchers believe that these smiles are a sign of immaturity. Is it possible that the data of the present study
demonstrate the relative immaturity of newborn Japanese macaques? This inference is contradicted in two ways. As
mentioned above, 1-year-old human infants show spontaneous smiles. Thus, spontaneous smiles alone cannot be evidence of
immatu- rity. In addition, newborn Japanese macaques are consid- erably more precocious than human neonates in some
respects (immune system: Holsapple et al. 2003; foveal development: Hendrickson 1992; postural and locomotor behaviors:
Takeshita et al. 2009).

The duration of spontaneous smiles in Japanese maca- ques cannot be directly compared with data from human studies,
because the criteria of the minimum duration for spontaneous smiles are different. There is no data on the duration of
spontaneous smiles in chimpanzees. In human studies, some smiles exceeded 10 s. The maximum dura- tion of smiles in this
study was 3.90 s. Thus the duration of spontaneous smiles in Japanese macaques may indeed be shorter than that of humans.
As mentioned above, this could be accounted for by the allometric timing rule. In addition, the zygomaticus major muscle in
macaques is split by the muscle associated with the opposite facial action, lip corner depressor. This may make it difficult for
macaques to maintain the facial action of the lip corner puller.

In the chimpanzee, spontaneous smiles could not be observed after 2 months of age (Mizuno et al. 2006). By contrast,
human infants continue to show them at 15 months (Kawakami et al. 2009). The oldest participant who showed
spontaneous smiles in this study was aged 0.5 month. This age will doubtless be exceeded if infant Japanese
macaques are observed exhaustively. It is still unclear when spontaneous smiles in Japanese macaques disappear. In
addition, humans, chimpanzees, and maca- ques have different life history and velocity of growth (Blurton Jones et al.
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1999; Lee et al. 1991). The chrono- logical age of humans, chimpanzees, and macaques can not be compared directly.

In summary, this study has provided evidence that Japanese macaques display spontaneous smiles, which have been
previously been confirmed in hominoids. Because Japanese macaques are somewhat distant from hominoids in the
phylogenetic tree, it may be possible that many other primates also show spontaneous smiles. Further observations are
necessary to make clear which speciesshow spontaneous smiles and what function these smiles serve

Acknowledgments Financial support for this research was provided by JSPS KAKENHI Grant No. 11J07455, 13J00208, 16K21128, 11710035,
13610086, 19300091, 20002001, 23220006, 24000001,
and 15H05709. This study was supported by the Cooperative Research Program of the Primate Research Institute, Kyoto Univer- sity (2000-A-9-
1, 2003-B-1, 2007-B-1, 2008-B-15, 2009-B-15, and 2010-B-4). We would like to thank Drs. Tetsuro Matsuzawa, Kiy- obumi Kawakami,
Kiyoko Takai-Kawakami, and Akifumi Tokosumi for their kind support and suggestions. The experimental procedures used in this study were
approved by the Animal Welfare and Animal Care Committee of the Primate Research Institute, Kyoto University, and by the Animal Research
Committee of Kyoto University. All procedures adhered to the Japanese Act on the Welfare and Man- agement of Animals.

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