MATERIALS AND METHODS
The fish used in this study were all
juveniles of the 'jewel fish' or 'Yellow-tail
Demoiselle', Microspathodon chrysurus.
Individuals ranged from 3 tO 5 cm standard
length. They were kept isolated in aquaria of
approximately 200 L capacity, these being
bisected by an opaque PVC partition in which was
set an L-shaped tube 4 cm in diameter, attached
to a clear glass boule 8 X 3 cm in size on the
other side of the partition. The tube and bottle
were set in the middle of the partition about1/3
of the way up from the substrate.
The aquaria were floored with gravel and sand
and had a group of corals and rocks in each
half. Mater temperature was kept at 28° C
with heaters regulated by a thermostat and
lighting was by 'Day-Glo' strip lamps set on a
12 hour continuous light schedule from 0800 to
2000 hrs. Subsurface illumination was found to
range from 5500 to 6000 Lux with the lights on.
pH was kept at 8.2 to 8.4 Aeration was by means
of sub-sand filters and air-stones and surplus
protein in the water was eliminated by means of
a 'foamer'. Fish grazed the algae present on the
aquarium walls and were also provided with
supplementary protein fed in the form of
hydrated freezedried Artemia or chopped mussel
flesh once daily at midday. Beliaviour was
recorded with an Esterline Angus 20-channel
event recorder and observations were made with
the observer sitting as quietly as possible
about 11/2 m from the aquarium.
DESCRIPTION OF YAWNING AND ITS DIURNAL
RHYTHMICITY
The behaviour pattern yawning was usually
preceded by the fish swimining rather slowly
with a sculling movement of the pectoral fins
and in a head-up position. The forward motion
then ceased and the fish raised the median fins
maximally, spread the caudal fin and pelvic fins
and momentarily stopped the sculling motion of
the pectorals. At the same time the mouth was
opened, the opercles flared, the hyoid apparatus
depressed and the premaxillae projected forward
to their maximal extent. During this period of
stretch all forward motion stopped and the
animal sank slightly in the water. This is
probably because the fin motion supporting the
body had ceased and the animal is denser than
seawater, hence sinks slightly before fin motion
is recommenced. The rigid position of the body
maintained during a yawn indicates that the
lateral musculature is also contracted during
its performance, but no external signs of such
contraction were evident.
Many variations in the degree of these fin
and mouth stretching occur, the culmination of
which is the true "yawn", where both median fins
and mouth are maximally extended simultaneously.
This simultaneous stretch of fin and mouth
musculture was the only behaviour recorded as a
yawn since the variability in the uncoordinated
or weaker fin and mouth stretchings made them
difficult to quantify exactly.
Fish were found to have preferred yawning
sites, each individual selecting a particular
area of the aquarium in which yawns were most
frequently performed. The yawning site selected
differed between individuals and bore no
relation to any particular stationary object in
the aquarium. The reasons for the selection of
such yawning sites are not known.
In addition to the preference for yawning in
a particular place in the aquarium, the animals
also showed a difference in the frequency of
yawns performed at different times of the day.
Five individuals were observed for10 mn in each
half hour starting at 0600 h, when they were
still asleep, to 2030 hrs, half an hour after
the timed light cycle had ended (the fishes
could still be seen as silhouette). Totals were
averaged for each hour, starting at the time
general (swimming etc.) activity was first
recorded i.e. 0630 + 0700 h etc. The
observations were repeated, making a total of 10
observations for 5 individals. The results
obtained are shown in Fig 1. These data show
that yawns gradually increase in frequency
during the morning, reaching a peak at 1100 h
and then decrease rapidly and remain low in
frequency for the remainder of the day. All
individuals showed the same general cycle with
only slight variation.
THE INITIATION OF YAWNING BY ENDOGENOUS
FACTORS
The apparatus described ni the Materials and
Methods section was designed to simulate
conditions pertaining during territorial
borderline fights. When an antagonist was
present on the opposite side of the partition,
the experiniental fish learned rapidly to
negotiate the maze and enter the boule in order
to engage in a display fight with this
individual. A definite appetence for such
agressive encounters was proved (RASA,
1971).
When the animal's aggressive tendencies were
not allowed expression by removal of the
antagonist, the frequency of yawning was found
to increase markedly during the first few davs
of isolation. The effect isolation for a 10 day
period had on yawning frequency is given in Fig.
2, this being, the average frequency observed
for io individuals. These data are derived from
3 half hour readings during each of the days in
question, readings being taken at 1100, 1400 and
1700 hrs to compensate for diurnal rhythm
effects. On day o another fish was present on
the opposite side of the partition. A few yawns
occurred in the glass tube itself on occasions
wlich the antagonist, although visible, did not
come to fight. The majority of yawns occurred in
the aquarium when the experimental fish could
enter the tube, but did not.
At the same time as this change in frequency
of yawning was observed, a change in the colour
pattern of the animal took place. The normal
colour of M. chrysurus is dark blue-black with a
paler throat, the 'jewels" appearing as
dark-ringed light patches against the dark
background. During the isolation period, four
classes of colour pattern were distingtilshable:
'all dark', which was as described above but
with or without the paler throat region present;
1/2 light, in which the animal was pale blue up
to the level of the pectoral fins; 3/4 light,
where the animal had a pale undersurface in
addition to the pale front and 'all light'', in
which the animal was completely pale in colour.
These differences in colour pattern are
illustrated in fig 3.
Darkening in colour could be produced by any
type ot external stimulation: feeding; the
observer approaching the aquarium; switching the
light on and off; increasing the speed of water
circulation: introducing an antagonist:
frightening the animal etc. It was therefore
considered to be an indicator of the (general)
excitement level of the animal, this being
congruent to the psychological term 'arousal'.
To quantify this varlable for any particular
time interval, the following formula was used
and termed the 'colour index'(C.J.):
CI= (secs all dark*100 + secs1/2 light*50 +
secs3/4light*25 + secs all light*10)/100
To determine the colour index for different
days of isolation, 5 individuals were observed
for half hour intervals at 1100, 1400 and 1700
hrs on each of the days of isolation, the colour
indices for individuals being averaged for each
day. The results obtained are shown in Fig. 4,
the variations being deviations from the mean
for individuals on each of the days in question.
These results show that the peak in frequency of
yawning observed coincides with the highest
level of excitement as indicated by the colour
index.
Concurrent with this change in colour
pattern, a change in the activity of the animals
also took place. As a measure of their kinetic
activity level, the number of turns of 90°
or more performed during the same observation
periods as given above for colour index were
determined for each day of isolation. Frequency
of turning was selected as the most accurate
measure of the kinetic activity in this species.
Turns were used as most Pomacentrids perform a
"dance" when they are very excited. This is a
zig-zag, up and down, rapid swimming action
performed at the focal point of the territon,
with a large number of rapid angular dashes to
and from the focal point. Normal swimming is
rather slow with much fewer turns. Since the
territory was physically delineated by the
aquarium walls, the restriction on swimrning
speed was even more rigidly enforced than would
be the case in nature. The results obtained for
the change in kinetic activity with isolation
time are shown in Fig. 5, the results being the
average frequency of turns for 3 individuals
with maximum and minimum deviations from the
mean.
The increase in frequency of yawning observed
under isolation conditions therefore coincides
with not only a marked increase in colour index
i.e. increase in excitement level as evidenced
by the darkening in colour, but also a marked
decrease in kinetic activity.
To determine whether the changes observed in
these variables during isolation could be some
of the causal factors of yawning, the following
experiment was conducted. Five animals were
observed for one hour each on the first day of
isolation, readings being taken at 1000 and 1400
hrs and the experimental series then repeated
for each individual making a total of 20
observations in all. The same procedure was
followed in a second series of experiments, but
these were conducted under conditions of high
water turbulence, so that the fish were kept
swimming actively for the duration of the
observation. A strong pump which extracted and
retumed the aquarium water at a rate of 2000
l/hr was used to maintain this high rate of
water flow. The results obtained are shown in
Fig. 6. These data show that, when kinetic
activity is maintained at a high level
concurrent with high excitement level, yawning
is rarely performed.
Although turbulence in the water was not
equal throughout the aquarium owing to
mechanical obstructions such as coral heads,
filters etc., the frequency of yawning in these
more protected locations was no higher than that
in the high turbulence areas. The increase in
kinetic activity instigated by the moving water
is thought to be the factor inhibiting yawns as,
under high excitement with low kinetic activity
(slack water on day 1 of isolation) the
frequencv of yawning increases. Only when the
kinetic activity level is artificially raised
during this period of isolation by keeping the
water moving does the frequency of yawning
decrease markedly.
The increase in exitement observed during the
first days of isolation has been shown to be the
result of frustration of the learned behaviour
for aggression (RASA. 1971). Delius (1967) found
that, in the Herring Gull, several areas of the
forebrain and brainstem, when stimulated
electrically via electrodes, elicited vawnim- in
addition to a series of other behaviours whIch
culminated in sleep. These behaviours were all
frequently performed by the animals as
'displacement activities' and he suggested, from
this finding, that a homeostatic process must be
operant in the brain to cancel the arousal
increment generated by conditions such as
conflict, thwarting and frustration. To
determine whether the behaviour pattern
'yawning' in fish initiated by frustration of
fighting could be attributed a 'dearousing'
function, the colour pattern of the animal was
recorded concurrent with the behaviour. A change
in colour within 2 seconds of performance of the
behaviour was considered as being associated
with it, as colour change in these animals is
very rapid. Darkening in colour takes less than
a second to become evident and lightening a
little longer, but not more than 2 seconds.
Yawns occurring in the 'all dark' colour phase
were discarded to prevent bias to the data, as
the level of excitement could not be accurately
determined. The darkening might differ in
intensity and such differences would not be
clearly evident to the obser~-er.
Five different fish were observed for a total
of 10 hours. Of the 34 yawns recorded which were
not performed in the 'all dark' phace~ 7 (20,5%)
were associated with a darking in colour after
their performance; 26 ( 76,5%) had no colour
change associated with their performance and
only1 (2,9%) was associated with a paling in
colour pattern. These data indicate that there
is no evidence that yawning in fish can be
attributed a 'dearotising' function.
Since the darkening in colour associated
witli frustration during the first few days of
isolation was thought to be hormonally as well
as neurally initiated, experiments were
conducted with the 'stress' hormone ACTH
(adrenocorticotropin) to determine whether the
change in colour and behaviour observed during
this period could be associated with increased
secretion level of this hormone. A solution
which would yield a concentration of 0,030 ppm
in the aquarium water was introducecl by means
of a polythene tube inserted into the outlet
pipe of the sub-sand filter. This was to prevent
water disturbance and bubbles resulting from
introduction of the hormone from having an
effect on the experimental animal, any such
disturbance being masked by the normal bubbles
and water flow from the filter. Five animals
were isolated for 10 days, observed for 10
minutes, the hormone solution added to the water
and the observation continued, for a further
half hour. Darkening in colour appeared within 3
to 5 minutes after hormone introduction, this
probably being due to the direct effect of the
hormone on the skin, as ACTH has the property of
causing melanophore pigment dispersion in vitro.
The results obtained for the influence of this
hormone on the frequencv of performance of
yawning are given in Fig, 7, the data being
averaged for each five minute intenal of the
observation period.
These results show that a gradual increase in
the frequency of performance of yawn starts
approximately 10 minutes after hormone
introduction. Yawning reaches a peak between15
and 20 minutes and then shows a marked decrease.
This decrease can probably be attributed to the
fact that ACTH, being a short chain amino acid,
is rapidly removed from the water, not only by
cohesion with colloidal particles but also by
the action of the 'foamer' which is designed the
remove surplus protein.
The results of these experiments indicate,
therefore, that the behaviour pattern 'yawning'
in fish can be initiated not only by conditions
of endogenous high excitement instigated by
frustration, but also by artificially increased
levels of the hormone ACTH when kinetic activity
is low in both cases.
THE INITIATION OF YAWING BY EXTERNAL
STIMULI
Apart from being endogenously triggered by
conditions of high excitement and low kinetic
activity, yawning was also observed to occur
when the animal was presetited by visual
stimuli. To test the effect of presentation of
such stimuli on the frequency of yawning, two
models were used to deterinine whether the type
of visual stimulus presented would affect the
frequency of yawning after presentation. One
model was a fish model, constructed from a dried
specimen of M.chrysurus 4 cm in length and
painted to appear as natural as possible. This
was considered specifically aggression releasing
in function and the experimental fish would
usually come and display aggressively towards it
on its appearance at the front pane of the
aquarium. The second model used was the ball
model, a sphere of grey 'Nakiplast' 5 mm in
diameter which was considered as a non-specific
visual stimulus. This elicited approach by the
fish on its appearance, but no aggressive
display as was seen with the fish model. The
fish model was held steady at the center of the
front pane, but the ball model was moved up and
down over approximately 5 cm distance, as it was
found that, after preliminary investigation, a
stationary ball evoked no further interest, but
a stationary fish model alwavs elicited
prolonged response. To keep the two stimulus
situations as comparable as possible therefore,
the ball model was kept in motion during its
presentation.
Ten different individuals were kept isolated
for 4 days and the two models presented in two
different experimental series, for 0 (control)
5, 10, 20, 30 and 60 seconds. The frequency of
yawning was recorded for each five minute
interval following model presentation. The
results obtained are given in Fig. 8.
These data indicate that there is no marked
difference in the frequency of yawning elicited
by stimuli influencing specific motivations and
those with general arousal properties. The
correlation coefficients obtained were +0.76 (p
= 0.02) for the fish model and +0,95 o.9,3
(p<0,001) for the ball. Both models increase
the frequency of yawning the longer they have
been presented to the animal.
It was noticed that, after yawning, the
frequency of performance of other behaviours
observed ni the experimental situation tendecy
to increase. The behaviours concerned were 'in
boule', the learned appetitive behaviour for
aggression, where the animal negotiated the maze
and entered the attached bottle in an attempt to
instigite a fight; snap, a bite directed towards
inanimate objects in the aquarium; pebble
carrying, holding a small stone in the mouth and
swimming with it; twitch, a convulsive shaking
movement of the whole body and chafe, a
scratching of the body against objects in the
aquarium. To determine what effect prescntation
of a visual stimulus had on yawning and the
frequency of performance of these behaviours
following it, the following experiment was
conducted.
Five fish were isolated for 10 days, observed
for 10 minutes, the ball model presented for 10
seconds and the observation continued for a
further 10 minutes, the colour pattern being
recorded simultaneously with the behaviour. 12
observations were made on each individual and
the data obtained grouped in 20 second intervals
for the whole observation period. The colour
pattern index was calculated for each individual
for each 20 second interval and the results
averaged. The data obtained are shown in Fig.
9.
These results demonstrate that presentation
of the model results in a tenfold increase in
the frequency of yawning in the 20 second
interval following, concurrent with an increase
in colour index to almost maximum. Practically
no other behaviours occur during this 20 second
interval, the few snaps and twitches recorded
nearly all being observed in instances in which
no yawn was elicited. The decline in yawning
frequency coincides with that of colour index
over the next 40 seconds. After this peak in
yawning, the other behaviours show increases in
performance level, the degree of increase and
the time taken before increase occurred being
illustrated schematically in Fig10.
These data therefore confirm the observation
that other behaviours increase in frequcncy of
performance after the animal has yawned. Yawning
elicited by external stimuli is also associated
with an increase in excitement level, as shown
by the increase ni colour index observed. A
similar darkening in colour was noticed in the
experinients with the fish and ball models, but
was not quantified. As colour index decreases,
so does yawning frequency but, from the results
obtained previously on the relationship between
this bellaviour and colour change after its
performance, yawning itself cannot be the causal
factor for this decrease. A more logical
explanation would be that as excitement level
decreases, so does the frequency of yawning.
The fact that these experiments were
conducted on day 10 of isolation when kinetic
activity is extremely low suggests that induced
by external stimulation might have the same
relationship with excitement and kinetic
activity as yawning initiated by endogenous
factors. To prove this hypothesis, the fish
model was presented to individuals which had
been isolated for 8 days, one series of
experinients being conducted in calm water and
one in turbulent water as described previously.
20 observations were made with 5 individuals in
each experimental series. Fish were observed for
30 mn, the model presented for 30 s and the
observation continued for a further 30 mn. Data
were averaged for each 5 mn interval and the
results obtained are given in Fig11.
These data show that, when the model is
presented under conditions of high kinetic
activity, a peak in yawning frequency after its
appearance no longer occurs. External stimuli
therefore cause no increase in the frequency of
yawning when the kinetic activity of the animal
is maintained at a high level, while under
conditions of low kinetic activity, they elicit
a marked increase in the number of yawns
performed.
DISCUSSION
The results of these experiments have shown
that the behaviour pattern 'yawning' in fish is
associated with increased excitement level,
either endogenously or exogenously produced and
low levels of kinetic activity. The reciprocal
relationship between this behaviour and kinetic
activity suggests that it may function as a
means ot increasing this variable, and activity
in general has been shown to increase after the
performance of a yawn. The behavior pattern yawn
itself is merely a state of maximal stretch of
the body musculature. An animal which is not in
a state of endogenously produced high excitement
or aroused by the appearance of a stimulus
object could be considered as maintaining a low
input-output transfer between the central
nervous system and the body musculature. When
sensory input is greatly increased as, for
example, by the appearance of a novel stimulus
object, this is registered as an increase in
excitement level in the central nervous sytem
This would result in a discrepancy between
input-output transfer between it and the budy
musculature, the raised excitement level causing
the transmission of a high output signal to the
latter, which would manifest itself in strong
contraction ie a maximal stretch which would be
similar to the behaviour pattern 'yawn'. A
simplified schema illustrating the mechanisms
physiologically underlying such an exogenously
produced yawn according to this hypothesis is
given in Fig. 12.
Muscle contraction is known to increase blood
flow to the muscle fibres, oxygen transfer and
heat expenditure, these facilitatilig tension
and thus 'priming' the muscle for further
action. In addition, a high spike potential in
the nerve fibre would facilitate motor end-plate
transmission. Such strong muscular contraction
would thus not only facilitate the effector, but
also its activator. One would therefore expect
that, after strong muscle contraction, such as
is evident in a yawn, the animal would be
physically more capable of performing other
behaviours. This appears to be true as an
increase in the frequency of performance of
other behaviours after yawning has been shown to
occur.
Yawning in fish can therefore be considered
as a behaviour by which the animal is able to
regulate discrepancies between central nervous
system excitation and body musculature tonus.
Its performance would result in an increase in
muscle tonus and therefore aids in preparing the
animal for action. This would be of especial
advantage in the case of exogenously instigated
yawning as the animals would, after performing
this behaviour, be able to respond more rapidly
to the stimulus object. As has been
demonstrated, the type of stimulus appears
unimportant a, far as the initiation of the
bebaviour is concerned. Yawning probably serves
as general bodily activator, hence the animal
should, after its performance, be facilitated in
its response to the incoming stimulus. The type
of response made would depend on the specific
motivation-activating properties of the stimulus
object concerned.
This theory of the causality and function of
yawning in fish can be applied to explain the
instances previously mentioned of its occurrence
in other species. Morris (1958) stated that it
occurred when Pygosteus was unoccupied, i.e. in
a state of low kinetic activity, but he does not
mention under what conditions this unoccupation
occurs. thus the excitement level of the animal
is unknown. TUGENDHAT (1960) stated that it
occurred most frequently in Gasterosteus when
the learned behaviour pattern for feeding is
thwarted, the longer the period of feeding
interruption, the greater the likelihood that
the fish will yawn, a thwarting situation giving
rise to increased excitement level without an
associated increase in kinetic activity. BARLOW
(1964) stated that yawning occurred more
frequently in Badis badis under low levels of
kinetic activity as evidenced by the decrease in
fanning tempo. The excitement level of the
animal can only be inferred in this case, but is
probably high, fanning possibly being the result
of an approach - withdrawal conflict (SEVENSTFR,
1961) and any motivational conflict usually
results in raised excitement level. Thwarting of
migration together with reduced swimming
activity, as the fish were held in pens, also
restuts in an increase in yawning as mentioned
by HOAR for Oncorhynchus. It therefore appears
that several cases of thwarting or conflict of
motivational variables other than aggression,
the motivatory variable in this study in
conjunction with decreased kinetic activity can
result in yawning or an increase in its
frequency of performance.
The increase in yawning frequency observed in
Cottus gobio by MORRIS (1954) and in Chromis
multilineata by MYRBERG could be attributed to
exogenously induced excitement caused by the
appearance of the female in both instances.
Interruption of ongoing activities by the
appearance of such a stimulating object could
initiate a yawn, especially if the general
muscle, tonus of the animal is low at the time
of its appearance.
The findings of McCUTCHEON (1962), that
ywaning causes a compensatory swimbladder
compression to maintain neutral bouyancy
suggests that, ni Lagodon rhomboides, yawning
has an additional function to raising general
motor activity in this species. As yawning
causes both isotonic and isometric contraction
of the body musculature, it is not unlikely that
the muscles controlling swimbladder volume would
also be activated. In M. chrysurus, however, it
cannot be stated that yawning functions to
maintain neutral bouyancy since the fish have
been observed to sink slightly in the water
during its performance.
It is thought unlikely that the function of
the behaviour pattern yawning in fish is exactly
the same as yawning in birds and mammals from
three point of view. Firsthly as SAUER
& SAUER ( 1967) have mentioned, one of
the functions of yawning in the Ostrich is to
relax tension in a group and sleepiness. In M.
Chrysurus however, its performance appears to
have exactly the opposite effect, as the
frequency of all other behaviours increases
after the performance of a yawn, thus it must
have more of an arousing effect than a
sleep-inducing one. One would expect that, if
yawning were associated with a readiness to
sleep in fish, its frequency of performance
would increase towards evening, but this is not
the case (see Fig. 1), the highest peak in
yawning occurring at approximately mid-day. Its
frequence of performance i, the evening is very
low compared to that of the morning. An
association between yawning and sleepiness is
therefore thought to be lacking in fish.
Secondly, it has been shown by DUMPERT
(1929), SELBACH & SELBACH (1953) and PEIPER
(1963) that in mammals, yawning is associated
with deep inhalation and exhalation, there being
a homeostatic mechanism between the
extrapyramidal motor system and the neural
center for breathing. This is activated by
insufficient oxygen in the brain arterial system
or a surplus of carbon dioxide. The performance
of a yawn in mammals is associated with the
regulation of the oxygen/carbon dioxide ratio in
the brain by means of such deep breathing
movements. In fish, yawning, if anything, should
result in less oxygen being taken in through the
gill filaments. Even though the mouth is opened,
the hypid apparatus depressed and the opercles
flared (resulting in a larger volume of water
prescrit in the oral cavity) all pumping action
of water over the gills ceases. In addition,
since the animal usually remains motionless
while yawning, even passive water movement over
the gills caused by the fishs forward swimming
movements does not occur. These observations
suggest that yawning is unlikely to be
associated with breathing in fish and does not
act as a mechanism for correcting the
oxygen/carbon dioxide ratio in the fish
brain.
Thirdly, yawning in fish does not appear to
have the infectious quality noted for the
behaviour of the same name in birds and mammals.
Apart from HOAR's observation that large numbers
of the salmon smolts might be yawning
simultaneously, no evidence is available from
aquarium or field observations on Pomacentrids
to substantiate that it has infectious qualities
in this family of fish at least. One individual
may yawn up to three times in rapid succession,
but this does not appear to be communicated to
other individuals in the area. Most of the
species studied to date have either been kept
isolated in aquaria or are naturally solitary or
territorial species. Further observations on
schooling and social fish are necessary to
support HOAP's observation that many of the
salmon smolts were simultaneously, since this
might be coincidental as the frequency of
yawning was so high. Until further evidence is
forthcoming, this behaviour must be considered
as non infectious in fish.
In conclusion, it appears that the
behaviour pattern yawning in fish is unlikely to
be completely analogous to the behaviour of the
same name in birds and mammals. In fish it
serves asa mechanism to equate discrepancies
between increased excitement level and lowered
kinetic activity, raising the latter variable by
its performance. It is, as has stated, simply a
stretching movement and appears to be
unassociated with breathing. In all vertebrates,
however, it appears to be triggered by
environmental stimuli and can also occur under
the influence of endogenous factors, as stated
above. It is likely that yawning may basically
have the same causation in other vertebrate
groups as has been demonstrated here for fish,
but has developed secondary functions in the
higher vertebrates, especially in social species
where it acts as a signal in addition to being
physiological regulatory mechanism.
