Behavior functions according to the
principles of homeostasis and may therefore be
called regulatory. The term "maintenance
behavior" used here to describe activities that
help regulate the physiological state of the
organism. When given in the presence of another
organism certain maintenance activities may have
secondary, communicative effects through
"sympathetic induction" causing social
facilitation; for example, some complex and
derived maintenance activities, such as the
collecting of food by individuals and groups for
the benefit of all participants or their
dependents, have become social events in both
primary and ritualized contexts.
Yawning and stretching are examples of
basic regulatory behavior for the purpose of
maintenance of bodily functions. These
activities are stimulated by endogenous
metabolic events and serve to regulate
physiological processes of respiration and blood
circulation. Several endogenous factors can
stimulate and trigger yawning and stretching
behavior. Insufficient blood circulation in the
brain leading to oxygen deficiencies is said to
elicit yawning and the accompanying acts of
stretching; in turn, this behavior improves
circulation as it is associated with deep
inhaling and exhaling (Dumpert, 1929). Further,
a homeostatic relationship is thought to exist
between the neural center for breathing and the
extrapyramidal motor system (Selbach and
Selbach, 1953 ). When the stimulation of the
breathing center becomes insufficient, an
increased amont of carbon dioxide is required to
reactivate it. This is accomplislied the act of
stretching by muscle contraction that delivers
the neccesary carbon dioxide (Peiper, 1956). It
is also possible to trigger and stretching in
cats through electrical stimulation of the brain
stem in the region of the diencephalon between
the anterior commisure and the infundibulum
(Waldvogel, 1945; Hess, 1954).
While the relevant internal events do both
stimulate and elicit yawning and stretching,
this behavior can be released also by
environmental stimulation when the organism is
sufficiently and specifically motivated. In man
and other mammals, and equally among birds, one
can observe a strong social induction of this
behavior when it it is exhibited within a social
group. Therefore, one should ignore neither the
existence and releasing values of specific,
environmentally controlled releasing mechanisms
nor the social implications of yawning and
stretching in species. Tembrock (1964) while
noting certain environmental effects, overlooked
these behaviorally, and particularly socially,
important exogenous components in his treatment
of this behavior complex. In calling this the
Räkelsyndrom, Tembrock followed an earlier
usage of this term by Selbach and Selbach
(1953).
Yawning and stretching frequently follow each
other, or they appear together in various
combinations. They consist largely of fixed
action patterns which, for the stretching
behavior, often achieve a high degree of
complexity. The yawning and stretching
activities of man are also composed of a set of
basic motor patterns, but his behavior appears
frequently flexible and modulated by many
individual idiosyncrasies. Yawning and
stretching are described as phenomena associated
with fatigue. The behavior is blocked as long as
the organism breathes regularly and sufficiently
deeply and fully exercises its muscles during
the periods of activity. Thus, yawning and
stretching characteristically appear at the end
and at the begining of activity cycles, i.e.,
their occurrence is correlated with periods of
rest and sleep.
Yawning in
birds
Maintenance activities are common among all
vertebrates, and yawning and stretching are
general behavioral attributes of the
homeotherms. Among birds, as well as among
mammals. yawning is so wide-spread that it is
difficult to understand why it has not become
better known. Maintenance behavior in birds is
easily observed: particularly when the ontogeny
of an organism and its behavioral systems are
carefully studied, one has no difficulty in
identifying the patterns of maintenance
behavior. However, students of bird behavior are
commonly more interested in other behavior
patterns, such as social behavior or migration,
and the establishment of ethograms, the complete
behavioral catalogues for individual species, is
badly neglected. The organic and physiological
bases of bird behavior are usually overlooked
and also largely unknown. However, a knowledge
of these underlying mechanisms is required for a
full understanding of maintenance behavior and
as a basis for experimental analysis of such
behavior.
There is still another reason why yawning is
not better known in birds. When Heinroth (1930)
focused his attention on species-specific
behavior in birds, he compared homologous action
patterns in groups of related species. Noting
the value of this stereotyped behavior for
taxonomic studies, he introduced the use of
genetically fixed action patterns in the study
of phylogenetic relationships between species.
With his superb knowledge of bird behavior and
his outstanding contributions to the biology of
so many species of birds, Heinroth programmed
and influenced for decades the development of
the science of ethology in Europe. So
authoritative were his views on bird behavior
that his statement that birds do not yawn was
accepted without question, and it was even
treated as dogma. Once a discussion of ours of
yawning, in warblers of the genus Sylvia though
documented by photographs and many observations,
did not pass the first editorial critique for
this very reason. and remained unpublished. As
recently as 1963 Konrad Lorenz stated that birds
and reptiles do not yawn, which he considered a
finding of taxonomic importance unknown to any
zoologist before Heinroth (-"Das Vögel und
Reptilien nicht gähnen, zum Beispiel, ist
eine taxonomisch wichtige Festellung, die vor
Heinroth kein Zoologe gemacht hat": Lorenz,
1963; 153)
In their recent AUK review of aspects of
avian field ethology, Ficken and Ficken ( 1966)
note the importance of maintenance activities to
the survival of the bird and as phylogenetically
important components of display behavior.
Following closely the traditional concept,
procedure, classification. and selection of
exemples, the authors did not mention yawning.
This is not surprising. but il seems desirable
to point out that yawning does exist in birds
and to note its importance as regulatory
behavior and its potential as social releaser in
gregarious species.
Methods
In this paper yawning and some related
behavior patterns are described for the South
African Ostrich : Struthio camelus australis. We
also discuss painting open-mouthed threat
gestures to illustrate differences in
superficially similar behavioral expressions; a
complete account of the maintenance activities
and social behavior of the Ostrich will be
published elsewhere. The descriptions are based
onobservations of the Ostrich in South West
Africa in 1957-1958 and 1964. For further
information see Sauer and Sauer, 1959, 1966.
Still and motion picture photography and tape
recordings were used to supplement the direct
observations. The field studies pertained to
wild birds of all age groups and covered all
phases of their daily and annual activity
cycles. The main study was performed in the
inner Namib desert in the Erongo Mointains at
Etosha Pan, and in the Omaheke district of the
Kalahari region; occasionnal observations were
made trhoughout the country.
Maintenance
behavior in the Ostrich
Yawning : soon after hatching, having rested
and recovered from their tiring attempts to rid
themselves of the egg shell and membranes, the
chicks yawned for the first time. This indicated
that they had either been disturbed wile resting
or that they were about to begin a nex phase of
activity. The first yawn, with or without a
stretching movement of the neck, appeared in the
complete form characteristic throughout the life
of an Ostrich. No changes in its expression and
motor coordination were noticeable that
suggested any postnatal maturation of this
behavior. It appeared at the beginning and at
the end of the many activity cycles during the
day, in the functional context mentioned in our
introduction and further outfined below.
When uncovered, the dozing nestlings drowsily
yawned. A group of chicks exploring the
surroundings of the nest quickly became tired
from their walk: a few meters from the nest they
paused for a rest, squatted, gave deep yawns
which were often associated with stretching and
then closed their eyes for a nap. Commonly the
chicks yawned deeply: the gular part of the
mouth was lowered maximally, and the tongue was
withdrawn during the long phase of inhaling. The
chicks yawned and might stretch either the neck
or the whole body at the same time. The yawning
was terminated with a relaxation of the body
which began with the short phase of exhaling.
Occasionally, a yawn consisted of a short phase
of inhaling followed by a long phase of
exhaling.
The chick's yawn lasted for about seven to
eight seconds, during which it usually erected
its head feathers for some two seconds when it
was about to have its beak maximally opened.
Drowsy chicks frequently kept their eyes closed
while they yawned, provided they were not
aroused by some environmental event. When a
chick was affected by an external stimulus, such
as a restless sibling, the call from another
chick, or the call of a parent, it might open
its eyes slighty or fully during yawning. The
act of yawning, however, was not oriented toward
the source of disturbance or attraction, but
remained directed as always in the mid-sagittal
body plane. When terminating a yawn, a chick
might return to the same resting posture or
quite commonly, change the position of the head
and neck slighty. The latter indicated some
discomfort or fatigue from the earlier resting
posture.
Yawning appeared in Ostriches of all age
classes in the very same context as described
for the young chick: just before falling asleep
or beginning to rest, when a rest was
interrupted and again when the bird awoke and
initiated a new phase of activity. Typically a
bird that yawned had been immobile for some
time, either resting on the ground or standig.
Quite commonly a flock or herd of Ostriches,
coming to a halt in their communal area near a
water hole, crowded and rested before they would
approach the water. Many of these birds.
enjoying safety and protection in the group and
having come a long way from their "family"
territories might begin to preen and rest or
sleep. Those that appeared exhausted from their
long walks might immediately reveal their
tirednes with a few deep yawns: then they would
nod a few times in the manner familiar to
everybody of one who falls asleep would slowly
tilt its head downward and, after a while, jerk
it up just to droop it again. Nodding in this
manner a few more times, and often giving a few
moreyawns, the bird in the end dozes off,
holding its neck typically locked in the sigmoid
resting posture. When after some time an ostrich
would come into action usually with a deep yawn,
often associated with a stretching of the neck
and followed, or sometimes preceded, by a
complete stretch. Birds that slept and rested
with their necks and headslying on the sand
yawned when waking even without lifting their
heads.
In general, yawning was seen in the communal
areas when the birds rested or waited their
turns at the water holes and in their
territories when they garded their nests, when
they incubated their eggs or brooded chicks,
when they settled for their night's sleep or
awake from it during a disturbance in the night
or in the morning or when they were disturbed
during any of their short resting and sleeping
periods in daytime. It never occurred when the
birds were very active and alert. The periodoc
appearance of yawning was observed in individual
birds studied over long periods of time. A hen,
for example, temporarily remained on the nest
and incubated for several days and nights in a
row. Quite regularly she began to yawn
extensively in the late afternoon at the time
when her mate formerly appeared to relieve her.
The deserted hen then yawned several times every
half hour and toward the evening more
frequently, until she finally fell asleep for
the night after several deep and long drawn
yawns.
In the evening about sunset, and regularly up
to some 40 minutes thereafter, solitary, and
flocking Ostriches, having gathered the last
bits of food, arrived at their individual
sleeping places for the night, commonly the
birds of flock stood for a while before
squatting: they would look around, listen, turn
their backs up the wind, and began to preen.
While preening would frequently be interronpted
by yawning, the birds would continue their
toilet behavior for some time after having
settled on the ground. The preening was then
interrupted more often and for longer intervals
during which the tired birds repeatedly yawned
or simply stared without moving. Finally
preening ceased altogether; the more alert birds
in the flock would close its eyes and nod its
head. Then their necks and heads were lowered to
the ground; individual birds would blink a few
times, yawn once or several times, and fall
asleep. The Ostriches commonly maintained a wide
field of view and open space at least to one
side of their sleeping places and, therefore,
made it easy for us to observe this
characteristic sequence of behavior daily after
sunset. In the morning, ususally up to 40
minutes before sunrise, the walkening birds
would yawn, get up and strectch themselves a few
times, excrete and preen briefly, and shortly
begin to graze and leave the sleeping place very
quickly.
Behavior associtaed with yawning : no other
behavior was obligatorily associated with
yawning, but a number of activities were
performed before, after, or at the same time as
a yawn. Yawning was sometimes begun during from
time to time jerked their heads laterally to
shake off excess mucus from the nasal cavity and
some times from the mouth. This head-jerking was
frequently followed by yawn before the birds
dozed or slept again. A dozing Ostrich suddendly
disturbed by a passing companion or stranger
would initiate an open-mouth threat, and,
becoming aware of the harmlessness of the
situation, switch directly into a deep yawn
before closing his mouth and his eyes again.
This is a spontaneous displacement of the
open-mouthed threat gesture through yawning,
both of which, in part, make use of the same
motor patterns.
Various acts of streching were associated
with yawning. Most frequently a stretching of
the neck or the body was synchronised with
yawning, while the unilateral stretching of wing
and leg quite often immediatly followed, but
migt also precede, the act of yawning.
Panting : in the open and arid vels, heat
dissipation by panting was of common occurence
in Ostriches of all age groups. Small chicks
sought shelter from solar radiation by standing
or walking in the shadow cast by the bodies of
the guarding hen and cock. Standing in the open
with young chicks, adult Ostriches enlarged
their shadows, providing thereby increased heat
dissipation for themeselves, by lowering the
wings and holding them away from the body. The
hen was also seen to signal her brood to
assemble under her when the group was disturbed,
for example, by a group of noisy Burchell's
zebras (Equus burchelli) passing nearby. The hen
signaled with a rhythmic beating of her wings
while she called the young and held her head
near the ground. Upon perceiving the signal the
resting chicks interrupted their panting and
gathered immediately in the shade of her body,
where they remained clustered while the group
walked slowly to a new resting place. Families
with offspring occasionally stood in the shade
of trees or large bushes, but every so often the
parents did not share with their brood. Chicks
were also seen crouching in the shade of low
bushes or more depression in the ground. Many
tests at the nests and in the open veld
indicated that chicks sought very actively any
avaible shade-producing object, even our
research equipment and the human observer
himself.
These observations reveal the chicks need for
shade, but the older Ostriches seldom sought
shade, and on the vast Namib flats many of them
had none. There they habitually rested and did
everything in the open and remained fulIy
exposed to the intense sunlight and heat even
during the noon hours. They were, however, very
inactive at noon, which prevented accumulation
of excessive body heat, and ther panting was
almost continous when the birds were not engaged
in minor activities such as preening.
While panting, but not when yawning, both
young and old Ostriches exposed the triangular
submalar apteria: it is reasonable to assume
that this aide heat dissipiation. When panting
the Ostriches held their heads horizontally or
tilted slightly upward, which assured maximum
air ventilation and a maximum distension of the
submalar region. When an Ostrich changed from
panting to yawning, the former was usually
terminated with a swalling motion, followed by a
yawn.
Open mouthed threat compared with
yawning
Open mouthed threat gesture of Ostrich : to
show the differences between yawning and
superficially similar behavior, panting was
descrobed above, and now the gesture of the
open-mouthed threat is briefly noted. This form
of social defense and agression was given in
encounters of Ostriches with conspecific
partners, birds of other species, and with any
sizeable mammal or reptile. During this threat
an Ostrich might give a variety of threat calls.
A hissing note was most commonly associated with
the slight threat of a defensive bird. The voice
of an agressive Ostrich, however, changed
rapidly with increasing excitement, from hissing
to loud and harsh snorting and to one and two
syllabled calls with pronounced tonal
qualities.
During the open-mouthed threat the gular
tissue is pressed upward, quite in contrast to
its maximally lowered state during a yawn.
Further, the tongue is thrust upward and slighty
forward. These characters remain the same
regardless of the degree of the opening of the
beak and the intensity and quality of the
threat. The open mouthed threat gesture,
therefore, cannot be mistaken for yawning, even
when a bird faces danger with an immadiate
threat at the momoent af awaking from sleep when
one expects the bird to yawn.
Discussion
The primary function of maintenance behavior
: maintenance of the organism through
homeostasis is commonly based on both
physiological and behavioral mechanisms.
Yawning, stretching, and panting are described
as examples of maintenance or economic behavior
in the Ostrich. While Cannon (1932) introduced
in biology the term homeostasis to designate
primarily feedback and regulatory mechanisms of
humoral and visceral processes that maintain
constancy of internal body conditions, Jacob von
Uexküll in 1909 had already applied clearly
the principle of homeostasis to behavioral
activities. The priciple was later emphasized by
Richter (1942) in his analysis of animal and
human behavior. Though it is now generally
understood that maintenance behavior that
regulates various economic requirements of an
organism is activated by homeostatic needs,
quantitative analyses of all but the few known
kinds of maintenance activities, such eating and
breathing have been hampered by a lack of
qualitative description and analysis of the
associated behavior. Yawning has not yet become
well known in birds. Using the Ostrich as an
example, this preliminary report emphasizes its
existence as well as the importance of this
behavior in these homeotherms. It should be
noted once more that yawning in birds is by no
means restricted to the Ostriches with their
large bulk, but that it occurs in small birds as
well, and we have noticed it in many bird
species of very different taxonomic position
where it occurs in the same functional context,
correlated with periodic fatigue. We have seen
it also in lizards and geckoes, and it is common
in the Florida gopher tortoise. Indeed the
"so-called yawning" in fish may be true yawning.
triggered for the same common reason and
serving, the same purpose. It is conceivable
that yawning is a phylogenetically old behavior
pattern among vertebrates and common to most if
not all of them.
Yawning as a social stimulus : while yawning
serves primarily as a regulator of physiological
conditions, its secondary function as an
involuntarily presented social stimulus becomes
obvious when it is studied in a group of
Ostriches. A bird that yawns quite often makes
one or several neighboring birds yawn too, and
yawning in an Ostrich herd can spread out like a
"snowball-effect".
Yawning in the Ostrich is not given as a
signal for the purpose of social communication:
it is not a social display. The effect that it
exerts on the conspecific partner is not easily
assessed. because the latter commonly responds
only with a minute change in expression posture,
or with an intention movement. A clear
identification and evaluation of this requires a
profound knowledge of the action system of the
species. Some of the important social functions
are as follows. At the beginning of a period of
rest it assures members of a group of momentary
safety or absence of danger. This is
particularly sigificant in view of the fact that
the socially higher-ranking birds customarily
relax and yawn before the lower-ranking and more
nervous birds calm down to rest. Thus, yawning
dotes induce a general relaxation of tension in
a group and trigger sleepiness. This prevents a
scattering of the flock and disturbance of the
group lifte, which is easily caused by
lower-ranking birds that are not assured of
safety by their dominant companions. Indeed,
nervous Ostriches run from many a harmless event
if they are not assured of safety. The calming
effect functions whether tension had been
buiding up by either intre or interspecific
contacts. Further, after any disturbance during
a resting period, yawning does again assure
nervous birds that danger has passed and
stimulate them to continue their rest or sleep.
At the end of a pariod, yawning would
stir up the group. It initiates and even helps
to synchronize the new activity cycle that birds
share with one another. The latter function
becomes particularly significant after a long
rest or sleep on the ground, whereby preening
behavior, too, aids, in synchronizing the bird's
activity before they depart as a group from the
place of rest.
Pandiculation:
the comparative phenomenon of systematic
stretching AF Fraser
Derived
activities: their causation; biological
signifiance, origin and emancipation during
evolution
