Testing
Yawning Hypotheses in Wild Populations of Two
Strepsirrhine Species: Propithecus Verreauxi and
Lemur Catta
Alessandra Zannella, Ivan Norscia, Roscoe
Stanyon, Elisabetta Palagi
Anthropology Laboratories,
Department of Biology, University of Florence,
Italy
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Introoduction
Yawning has long been a subject of
evolutionary biology. Darwin (1872) described
yawning as an act of deep inspiration, followed
by a lengthy, forceful expiration with
simultaneous contraction of many skeletal muscle
groups. Yawning can be easily recognized in
mammals and even birds [Gallup et ah,
2009]. Many authors have offered
physiological hypotheses to explain yawning. It
has been hypothesized that yawning is modulated
by factors such as respiration, circulation,
brain oxygenation, thermo-regulation, arousal
and the sleep-wake cycle [Gallup, 2014;
Giganti & Zilli, 2011; Guggisberg et ah,
2010; Matikainen & Elo, 2008]. These
base-line physiological functions do not rule
out the possibility that yawning has social and
communicative roles in some taxa [Gallup,
2011]. In primates, Altmann [1967]
de-] defined three different types of yawns:
the "drowsiness yawn" (strongly dependent on the
sleep-wake cycle), the "tension yawn" related to
anxiety, and the "threat yawn" used to display
canines during aggressive encounters.
In many primate species characterized by
high sexual dimorphism, yawning is often used as
an aggressive, threat signal, emitted by
high-ranking males [Adams & Shoel,
1982]. This link between sexual dimorphism
and male threat yawning is probably related to
both intra-group rank competition and
inter-group territorial defense [Macaca
fascicularis, M. nigra, M. fuscata,
Theropi-thecus gelada; Deputte, 1994; Hadidian,
1980; Leone et ah, 2014; Troisi et ah,
1990]. Sex differences in yawning are less
evident in species characterized by low levels
of sexual dimorphism, especially in canine size
[Pan paniscus, Demuru & Palagi, 2012;
Homo sapiens, Schino & Aureli, 1989; Pan
troglodytes, Vick &Paukner, 2010].
Provine [1986, 2005] attempted to
combine multiple behavioral state changes
associated with yawning (wakefulness to sleep,
sleep to wakefulness, alertness to boredom,
etc.) within a single framework and stated,
"yawning is a vigorous, widespread act that may
stir up our physiology and facilitate these
transitions". Several reports indicated that
yawns serve to stimulate or facilitate arousal
during state changes [Baenninger, 1997;
Provine, 2005; Vick & Paukner, 2010;
Walusin-ski & Deputte, 2004]. These
reports led to the general consensus that
yawning, as well as scratching and other
self-directed behaviors [Buckley &
Semple, 2012; Tinbergen, 1952], anticipates
important events and behavioral transitions. In
humans [Giganti & Zilli, 2011] and
geladas [Leone et al., 2014] spontaneous
yawning shows daily fluctuations linked to the
sleep-wake cycle. Yawning is probably associated
with increasing activity levels even outside the
sleep/wake context [Baenninger et al.,
1996]. In chimpanzees yawning is related to
changes in the level of general activity with
increased locomotion during the one-minute
interval preceding and following a yawning
event. Thus yawning could be related to social
synchronization by punctuating changes in
behavioral activity [Vick & Paukner,
2010].
Propithecus verreauxi (Verreaux's
sifaka) à gauche, Lemur catta
(ring-tailed lemur) à
droite
photo Norscia and
Palagi
Yawning may also be affected by stressful
environmental and socially stressful stimuli
[Liang et al., 2015; Schino et al.,
1990]. Laboratory studies on birds and
mammals showed that yawning frequency initially
decreases or remains unchanged in the first
20-min following a stressful event. As the
effect of the anxiogenic events clears, yawning
generally increases in a 20-40 min time window
[Miller et al, 2010; Miller et al, 2012;
Moyaho & Valencia, 2002]. In primates
there are only anecdotal reports on the possible
linkage between stressors and "tension yawns."
In Macaca nigra, for example, low ranking adult
males yawned frequently after dominant males had
approached and sat nearby [Hadidian,
1980]. When two unfamiliar female macaques
were paired in a relatively small cage there was
an increase in the frequency of yawning in both
subjects perhaps due to stress between
individuals for whom there was not yet a
clear-cut dominance relationship [Schino et
al., 1990]. Wild chimpanzees yawn more
frequently in the presence of humans
[Goodall, 1968] and captive chimpanzees
yawn more in response to social tension
[Baker & Aureli, 1997]. Recent
studies on chimpanzees [Vick & Paukner,
2010] and geladas [Leone et al.,
2014] support the idea that different forms
of yawning can have different functions. In
particular, the "tension yawn" seems to be
linked to anxiety even though yawning has been
mostly studied in association with other
well-known displacement behaviors (like
scratching) and rarely analyzed independently
[Pomerantz & Terkel, 2009]. In L.
catta yawns were observed in contexts of unclear
dominance reversals and during intergroup
conflicts [Pereira & Kappeler 1997],
suggesting that there might be a link between
yawning and potentially stressful events.
However, the relationship between yawns and
disturbing events was never demonstrated. As for
many behavioral topics, lemurs have been
neglected for the study of the mechanisms
underpinning yawning behavior. The lemurs, found
exclusively in Madagascar, represent an
independent radiation from continental primates
[Tattersall, 1982]. Comparing
strepsirrhines with the better-known
haplorrhines may be useful because these two
primate taxa, although distantly related, share
a long period of common ancestry in which common
foundations of yawning may have been forged.
Investigating yawning and testing some of its
possible functions in strepsirrhines can add
some pieces to the complex picture
characterizing the evolution of this puzzling
behavior in primates. To test various hypotheses
of yawning we studied two sympatric species of
strepsirrhines living in multimale-multifemale
groups characterized by linear hierarchy, female
dominance and male dispersal [Jolly, 1966;
Richard, 1974]: Propithecus verreauxi (Fig.
la) and Lemur catta (Fig. lb). We tested three
hypotheses, as follows:
1. The Dimorphism Hypothesis: Except for
some differences in the sexual distribution of
scent glands, L. catta and P. verreauxi show no
obvious sexual dimorphism. Males and females
have similar body size, coat color, and length
of canines [Lewis, 2002; Pereira &
Kappeler, 1997]. Because L. catta and P.
verreauxi lack sexual dimorphism, we expect no
difference in the frequency of yawns between
males and females in either species (Prediction
1).
2. The State Changing Hypothesis: If yawning
is involved in behavioral transitions, the
frequency of yawning should increase with such
transitions (from behavior A to behavior B) (YW
in between behaviors A and B > YW in between
behaviors A and A) (Prediction 2a). As yawning
is influenced by the sleep-wake cycle, we
predicted spontaneous yawning to peak during
transition to and from periods of rest
(Prediction 2b). L. catta is more active than P.
verreauxi, which spends a large part of the day
resting for fiber digestion due to its
folivorous diet [Jolly, 1966; Norscia et al,
2006]. Therefore, yawning should be more
frequent in L. catta than in P. verreauxi,
because L. catta has more frequent transitions
between one state and another (Prediction
2c).
3. The Anxiety Hypothesis: Yawning seems to
be associated to tense situations in primates
[Good et al, 1968; Hadidian, 1980; Schino et
al, 1990; Baker & Aureli, 1997; Pomerantz
& Terkel, 2009; Leone et al, 2014],
including lemurs [Pereira & Kappeler,
1997]. If yawning is indeed a behavioral
response to anxiety its frequency should
increase in both study species after exposure to
stressful stimuli (Prediction 3).
DISCUSSION
The aim of this study was to test various
hypotheses of yawning and examine how some
morphological, motivational and social factors
affect yawning frequencies in lemurs. We first
tested whether the lack of sexual dimorphism in
Lemur catta and Propithecus verreauxi, would
determine a lack of yawning differences between
males and females as predicted by the Dimorphism
Hypothesis. Indeed, we found no differences in
yawning frequency between males and females in
either of these strepshirrine species
[Prediction 1 supported].
In many highly sexually dimorphic primates
males have longer canines than females, are
often dominant and actively defend their groups
and territories (e.g., Macaca fascicularis, M.
nigra, M. fuscata, Theropithecus gelacla). In
these species, males yawn more frequently than
females since they display the so-called "threat
yawn" characteristic of aggressive, competitive
interactions [Hadidian, 1980; Leone et al,
2014; Troisi et al, 1990]. However, in both
P. verreauxi and L. catta females are dominant
[Jolly, 1966; Kappeler, 1997; Norscia &
Palagi, 2015]. The canines of the females
are used during attacks directed towards both
sexes and seasonal peaks of inter-sex aggression
have been widely recorded [Pereira &
Kappeler, 1997; Vick & Pereira, 1989].
In an evolutionary perspective, the high level
of both intra- and inter-sexual competition may
have resulted in reduced morphological
differences between sexes [Kappeler, 1997;
Plavcan & van Schaik, 1999]. As
expected, in Propithecus verreauxi and Lemur
catta the hourly frequency of yawns did not
differ between males and females. Our results
are in agreement with previous findings in
species with low sexual dimorphism, i.e. Homo
sapiens [Schino & Aureli, 1989], Pan
troglodytes [Vick & Paukner, 2010]
and Panpaniscus [Demuru & Palagi,
2012], in which no sex difference in yawning
frequency were reported.
According to the State Changing Hypothesis
[Provine, 2005] yawning, like other
self-directed behaviors such as scratching and
body shaking, is associated with neural
mechanisms related to arousal. Yawns may stir up
an individual's physiology thus being associated
to the transition from one behavior to another.
From this perspective, yawning can be considered
as a displacement behavior [Tinbergen,
1952]. The association between yawning and
behavioral transitions, including sleep/wake
cycle, has been demonstrated in several primate
species including humans, macaques, hamadryads
[Hadidian, 1980; Kummer, 1968; Maestipieri
et ah, 1992; Troisi et ah, 1990] and,
recently, in geladas [Leone et ah,
2014]. In Lemur catta and Propithecus
verreauxi the frequency of yawns around
behavioral transitions was significantly higher
than when there was no transition, independent
of any audience effect (defined as the presence
of another subject within two meters from the
yawner) (Prediction 2a supported). In humans,
yawning is associated with increased activity
levels even outside the context of
waking/sleeping [Beanninger et ah,
1996]. In chimpanzees yawning is related to
a change in general activity levels [Vick
& Paukner, 2010]. Displacement
behaviors, and specifically self-scratching,
were shown to increase sharply around behavioral
state changes in Lemur catta [Buckley &
Semple, 2012]. Our data on yawning show the
same trend: yawning punctuates changes in
general activity levels of individuals.
The frequency of yawns in the two lemur
species differed strongly and was strictly
related to their activity level. Lemur catta,
characterized by higher levels of basal activity
(defined as behavioral transitions per unit of
time) also yawned significantly more frequently
than Propithecus verreauxi (Prediction 2b
supported). Even though the two study species
show some similarities&emdash;i.e., phylogenetic
closeness, sharing of the same environment (to
the extent that animals living in the same
habitat in the Berenty Reserve often feed on the
same tree)&emdash;their ecology differs. The
frugivorous omnivorous L. catta (in Berenty, the
individuals of these species can hunt
grasshoppers, spiders and cicadas) have a more
dynamic life-style characterized by an active
search and competition for food [Jolly,
1966] whereas the folivorous P. verreauxi
spend more time feeding and a large part of the
day resting for digestion [Jolly, 1966;
Norscia et al., 2006]. Our analysis on the
behavioral transitions per unit of time clearly
demonstrates more frequent behavioral shifts and
more frequent yawns in L. catta than P.
verreauxi as predicted by the State Change
Hypothesis [Baenninger, 1997]
(Prediction 2c supported). The Anxiety
Hypothesis predicts that environmental and
social stressors can induce yawning.
Chimpanzees and gorillas were reported to
yawn in the proximity of human observers
[van Lawick-Goodall, 1968; Nishida, 1970;
Schaller, 1963]. In Macaca nigra, yawns were
reported to occur in contexts that elicited
anxiety [Hadidian, 1980], and in captive
Macaca silenus yawning increased in the presence
of visitors [Mallapur et al., 2005].
Lemur catta was observed yawning during
agonistic scent-marking displays [Jolly,
1966] even though the author was not able to
clearly associate yawning with a specific
context. Roeder et al. [1994] described
yawning in L. catta as temporally associated
with stressful encounters. However, these
reports are mostly anecdotal. Indeed, our
findings provide the first empirical evidence of
a direct connection between potential stressors
and the yawning response in lemurs.
Both Lemur catta and Propithecus verreauxi
yawned within 10 minutes of exposure to a
disturbing event (Prediction 3 supported). This
finding contrasts with literature on
non-primates showing a 20-40 min delayed yawning
response to stressful stimuli, such as isolation
[Sula grand, Liang et al., 2015],
confinement and handling [Melopsittacus
undulatus; Miller et al., 2010] and electric
shocks [Rattus norvegicus; Moyaho &
Valencia, 2002]. In these studies, the
delayed response is explained through the
Arousal Reduction Hypothesis, predicting that
yawning is elicited by arousal reduction, when
the animal starts relaxing. Our results do not
challenge the Arousal Reduction Hypothesis
because the study setting and the nature of
stressing stimuli were different from those of
previous studies. Lemurs were observed in their
natural environment and everyday social
stimuli.
Therefore, we hypothesize that the arousal
provoked by natural, familiar stimuli is usually
milder than that caused by extraneous,
infrequently encountered stimuli. Additionally,
in the wild, animals can minimize their exposure
to stressors by escaping. This can lower the
arousal response, meaning that animals in their
natural habitat can recover from some arousal
increases (stress) faster than their laboratory
counterparts.
