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Behavioral sleep in the giraffe (Giraffa Camelopardalis) in a zoological garden


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Behavioural sleep was assessed for 152 nights in 5 adult, 2 immature and 1 juvenile giraffes at a zoological garden, using continuous time-lapse video recording. Sleep occurred while the giraffes were standing (SS) and in recumbency (RS). Paradoxical sleep (PS) was recognized by the peculiar positioning of the head on the croup and by phasic events. The 24-h sleep profile had a main bimodal nocturnal sleep period between 20.00 and 07.00 hours, with a trough between 02.00 and 04.00 hours, and several short naps between 12.00 and 16.00 hours. Total sleep time (TST), excluding the juvenile, was 4.6 h, whereby PS comprised only 4.7%. TST was not age dependent, but the lowest amount of RS and the highest amount of SS occurred in the oldest and the two oldest animals, respectively. Sleep was fragmented, as indicated by the predominance of RS episodes lasting less than 11 min. Sleep cycle duration was very variable with most values between 1 and 35 min (when no waking or RS was allowed within PS episodes), or 6-35 min (when the criteria for ending a PS episode allowed 1-2 min interruptions by RS). There were several indications for sleep regulation: (i) RS and SS complemented each other to yield a relatively stable daily value of TST; (ii) sleep was redistributed on nights following a day when the giraffes spent a few hours in an outside enclosure. The first peak of the bimodal sleep profile was absent and RS was more prominent in the second half of the night compared with nights following days spent in the barn; and (iii) napping was followed by a minor reduction of RS and an increase in SS in the subsequent night compared with nights following days without naps.
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J. Sleep Res. (1996) 5, 21–32
Behavioural sleep in the girae(Giraffa camelopardalis)ina
zoological garden
Institute of Pharmacology, University of Zu
¨rich, Zu
¨rich, Switzerland
Accepted 10 January 1996; received 17 November 1995
Behavioural sleep was assessed for 152 nights in 5 adult, 2 immature and 1 juvenile
giraes at a zoological garden, using continuous time-lapse video recording. Sleep
occurred while the giraes were standing (SS) and in recumbency (RS). Paradoxical
sleep (PS) was recognized by the peculiar positioning of the head on the croup and
by phasic events. The 24-h sleep profile had a main bimodal nocturnal sleep period
between 20.00 and 07.00 hours, with a trough between 02.00 and 04.00 hours, and
several short naps between 12.00 and 16.00 hours. Total sleep time (TST), excluding
the juvenile, was 4.6 h, whereby PS comprised only 4.7%. TST was not age dependent,
but the lowest amount of RS and the highest amount of SS occurred in the oldest
and the two oldest animals, respectively. Sleep was fragmented, as indicated by the
predominance of RS episodes lasting less than 11 min. Sleep cycle duration was very
variable with most values between 1 and 35 min (when no waking or RS was allowed
within PS episodes), or 6–35 min (when the criteria for ending a PS episode allowed
1–2 min interruptions by RS).
There were several indications for sleep regulation: (i) RS and SS complemented
each other to yield a relatively stable daily value of TST; (ii) sleep was redistributed
on nights following a day when the giraes spent a few hours in an outside enclosure.
The first peak of the bimodal sleep profile was absent and RS was more prominent
in the second half of the night compared with nights following days spent in the barn;
and (iii) napping was followed by a minor reduction of RS and an increase in SS in
the subsequent night compared with nights following days without naps.
 age, behavioural sleep, girae, nap, sleep regulation
INTRODUCTION sleep quotas are the body mass index, brain weight and
metabolic rate (Zepelin and Rechtschaen 1974; Allison and
Little is known about the sleep behaviour of large herbivores, Cicchetti 1976; Elgar et al. 1988; Zepelin 1994). The amount
especiallythosewhicharenotdomesticated.Zoologicalgardens of sleep decreases as a function of increasing body mass, or
provide an environment where observations of animals in semi- brain weight, but the latter is a better predictor of daily sleep
wild conditions are possible. In addition, modern technology quotas than either body weight or metabolic rate. ‘Danger
allows continuous observation with light-sensitive cameras of variables based on asubjective index consisting ofthe predation
animals in zoo enclosures, so that the animals are undisturbed risk were also found to be better predictors of total sleep time
by the observer or by additional light. thanbody or brain weight(Meddis 1983). Correlationsbetween
Total sleep time exhibits a large species variation (Zepelin the amount of paradoxical sleep (PS) and the danger of
and Rechtschaen 1974; Campbell and Tobler 1984). The predation showed that animals with a small predation index
amount of sleep in ungulates is of special interest because some (e.g. small rodents, large carnivores) exhibit more PS, whereas
of the constitutional variables which correlate best with daily the ungulates, particularly the undomesticated species, exhibit
little PS (Allison and Cicchetti 1976). The domesticated
herbivores seem to have retained this feature as they also
Correspondence: Prof. Irene Tobler Ph.D. Institute of Pharmacology
exhibit little sleep. However, the sleep data of large animals
University of Zu
¨rich Winterthurerstrasse 190 CH-8057 Zu
Switzerland. Tel.: +41/ 1-257-2957; Fax: +41/ 1-257-5707
such as the girae and the elephant (which contribute to
1996 European Sleep Research Society
22 I. Tobler and B. Schwierin
the correlations), are based on direct observations of few ‘deep sleep’ was considered as sleep. Since drowsiness was
individuals and the reliability of the data can be questioned. dicult to define it was not quantified (Immelmann 1958).
The exclusion of large grazing animals considerably weakened A subsequent investigation which comprised 20 nights of
the correlation between body size and total sleep time (Meddis continuous observation and 20 nights of observations until
1983), but was again strong if smaller grazing species were also after midnight, found that adults did not engage in
excluded (Elgar et al. 1988). recumbency during the day, whereas the 4-month old juvenile
Several factors may contribute to the small amounts of sleep lay down 2–3 times at mid-day for 10 min but did not
reported for ungulates. In a zoological garden they are rarely sleep (Immelmann and Gebbing 1962). The adults became
seen sleeping, possibly due to the frequent disturbances by the quiet at this time, either ruminating or standing completely
public. In addition, observations at night, when it is more still.
probable that the animals are sleeping, are influenced by the These observations were complemented by a 3-week
presence of the observer. Wild animals do have the capacity continuous observation of two captive females, 3 y and 9 y
tofurther reduce theirsleep whenthe circumstances areadverse old (the latter was shortly before parturition) in the Bualo
(Hediger 1983, 1985). Zoological Garden (Kristal and Noonan 1979). ‘Deep’ sleep
An additional factor contributing to the short sleep (assumed to correspond to fast-wave sleep) was short (1–10
duration in ungulates (compared, e.g. with carnivores) is the min) and occurred only 1–2 times per night, whereas 3–8
vegetarian diet which necessitates large amounts of food reclining episodes lasting 3–75 min were present, with the
intake. In the wild, an adult girae bull consumes 37kg longer ones later in the night. Cud was chewed during most
of food per day (Moss 1975). Thus a large amount of the of the time spent in recumbency. Most of the reclining time
24h is spent in feeding and ruminating. EEG recordings in was spent with the neck in a vertical position, but occasionally
domesticated herbivores have shown that rumination and S-sleep (assumed to correspond to slow-wave or light sleep),
sleep are not exclusive behaviours. Non-REM sleep, but not occurred in episodes lasting from 5 to 30 min. S-sleep was
PS can occur during rumination (Ruckebusch and Bell 1970; characterized by the absence of cud chewing and a relaxation
Bell and Itabisashi 1972; Ruckebusch and Dougherty 1974). of the neck, which remained in a vertical position. D-sleep
In girae calves, complete rumination, which begins when began only after a long period of reclining rest or S-sleep. In
suckling is ended, occurred at the age of 6–8 months D-sleep the neck and head were lowered until the head rested
(Langman 1977). on the hip or thigh (‘sleeping swan’) and the eyes were closed.
Grzimek (1956) described the sleeping behaviour of four A similar sleep posture was reported for giraes observed in
well-adapted giraes observed for 14 nights in the Frankfurter the wild (Mejia in Moss 1975). During the first two days of its
Zoo, and disproved the common belief that giraes do not life the calf spent 25% of 24 h sleeping with 90% in the D-
sleep at all. The opinion was that animals which are in danger sleep posture (Kristal and Noonan 1979).
of predation must compromise between the need for In the wild, i.e. in Kenya, Zaire, Tanzania and South Africa,
recuperation and avoidance of predators. He published the only day-time activities have been quantified for the girae
first photograph of an adult girae sleeping with its neck bent (Leuthold and Leuthold 1978; Foster; Mejia, Innis, Backhaus,
backwards resting the tip of its head on the ground, behind in Moss 1975). Most of these studies did not include night
the laterally extended hind limb (reproduced in Zepelin 1994; observations or the data were collected on full moon nights.
see also Fig. 1). Earlier, Hediger (1955) had published a photo Often all girae in a herd were seen standing or lying in one
of a young girae in a similar position, where the head tip place, and chewing. Rumination comprised 3–5 h per day. In
rests on the croup and the hind leg is extended towards addition, 2–3 h were spent lying down without chewing (males
the front in parallel with the abdomen. These postures were sometimes during daytime, females usually only at night).
considered typical for ‘deep sleep’, and are not unique to the These animals lay on the brisket, with legs curled under them
girae. Okapi, the closest relative of the girae, antelope and and the neck and head held upright. ‘Deep sleep’, with the
cow also bend their neck backwards, but not only the tip of head resting onthe flank,lasted only about1 min,and occurred
the head but the entire head can be placed on the croup (the for no more than 5–30 min per day. Only this position was
long neck of the adult girae does not allow a positioning on considered to correspond to sleep. Sometime after midnight
the croup). This posture in giraes was later described again, the animals stopped feeding and lay down and ruminated for
being referred to as D-sleep (‘deep’ sleep) and assumed to 2–3 h. At this time they slept for very short intervals. An age
represent fast-wave sleep (Kristal and Noonan 1978). dependence of the amount of time spent lying was observed
Grzimek (1956) reported that adult giraes spent 6.5h (Langman 1977). Time in recumbency decreased from infants
in recumbency with five ‘deep sleep’ episodes lasting 2.5–6 (0–60 d) to juveniles (60d–1.5 y) and was least in theimmature
min (total ‘deep sleep’: 21 min in the adult, 63–70 min in (1.5–3 y female, 1.5–4 y male).
the 4-month old juvenile). The same data analysed later in The aims of this study were to describe and quantify sleep
more detail resulted in 7–9 h per night in recumbency, with behaviour, assess its 24-h pattern and to investigate the eects
2–3 recumbent episodes of 11 min to 3h interrupted by of age and daytime access to an outdoor pen in a group of
1 hour of waking spent in feeding and defaecation. Most
of recumbency was described as a drowsy state and only giraes kept in the Emmen Zoo.
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
Behavioural sleep in the giraffe 23
Table 1 Time of day of main sleep period
Gender Age (y) N Sleep onset Wake onset
(RS or SS)
Twanja f 0.2 juvenile 6 19.00 (7.4) 06.00 (9.3)
Raisa f 2.1 adolescent 25 20.06 (7.7) 06.18 (11.8)
Hans m 2.2 adolescent 25 20.36 (8.6) 05.54 (14.5)
Naomi f 3.4 adult 22 19.30 (10.7) 06.18 (14.1)
Augusta f 3.5 adult 25 20.36 (10.3) 06.12 (8.3)
Tiny f 3.6 adult 18 21.24 (13.2) 06.36 (9.6)
Taos f 13 mother 6 19.54 (14.9) 06.42 (8.7)
Cornelia f 20 adult 25 21.24 (16.7) 06.30 (8.6)
Mean (n=8) 20.18 (18.1) 06.18 (5.9)
Mean (n=7)
20.30 (16.7) 06.24 (6.0)
Time of day is the mean time (±SEM in minutes), over all days per individual or
mean value
excluding Twanja; n=number of animals. RS=recumbent sleep, SS=standing sleep; N=
number of days.
METHODS nights of Group 2, Naomi (7 nights) or Tiny (1 night) remained
inGroup1andcouldnot be assessed. Recordings were obtained
The behaviour of 8 giraes (Giraffa camelopardalis) (age 0.2 for 25d (Group 1) and 6 d (Group 2).
months–20 y; 5 adult females, 2 adolescents, a male and female
and one juvenile female; Table 1) was recorded continuously RESULTS
on two time-lapse video recorders (Panasonic AG-6720 A) for
6–25d during the hours when the animals were in the animal Behavioural states
house of a zoological garden. The recordings were performed Waking was scored when the animals were standing or
with two infrared sensitive cameras (CCD, with automatic recumbent, but moving. Waking behaviour during the night
time-lapse shutter) and infrared illuminators (Sennheiser, SZI consisted largely of feeding. Sleep occurred in a recumbent
1019A, 950 nm), allowing data collection in the undisturbed (RS) and standing posture (SS). SS was scored when the
animals. The cameras were mounted on opposite sides of the animals were motionless(including theears, which wereusually
enclosure (at a height of 8–10m) to ensure that the entire directed backwards), and the neck position was at a narrower
enclosure was visible. The giraes were kept in one of several angle relative to the ground, than was the case during waking.
enclosures (9.60×5.85m) within a barn. When the weather SS usually alternated with short waking episodes, characterized
was mild the animals were allowed to go outside into a large by righting of the neck and head lifting accompanied by ear
park next to the girae house, shared with animals of several movements. SS closely resembled the standing sleep reported
other African species, for 2–6 h between 09.40 and 16.30 hours. earlier in elephants (Tobler 1992). In recumbency the animals
Thereafter they were returned to adjacent pens in the giraecould either be awake or sleeping. The posture in RS was
house, where food was available. An artificial LD cycle typical for ungulates (Fig. 1): lying on the brisket and the
provided light from 06.40 to 18.40 hours; light intensity, 95–110 abdomen or flank with the legs folded under and slightly
lx. In addition several windows provided natural daylight. The displaced to the sides; the neck bent forward at an angle of
recordings were performed in spring (March–April) in Holland
70°from the ground (sometimes even as little as 30°), i.e.
(53°15 min latitude). in a position less vertical than that of waking; and the neck
The video systems simultaneously recorded 24 h of real time and head immobile. The neck angle relative to the ground
on a 3-h tape. The tapes were played back at normal speed could not be determined reliably due to the placement of the
(50 half-frames per second) and the behaviour of the animals cameras above the animals. Therefore, the changes in angle
was visually scored for 1-min epochs. Epochs lasting <30s could not be used for scoring the behavioural states. The
were not considered, whereas epochs lasting between 30 and presence or absence of chewing was not considered a criterion
59s were rounded to 1 min. For scoring of the individual for RS or waking (uninterrupted chewing could occur for long
animals, the two tapes recorded simultaneously from dierent intervals, i.e. 30 min, while no other motor activity was
angles of the barn, were compared. Missing values due to lack evident). PS was scored when in RS the animals suddenly bent
of visibility of the giraes occurred only in one girae (Naomi) the neck backwards and rested the head on the flank of a rear
in 3 of the 22d (missing: 36, 73 and 140 min). leg (Fig. 1). During these PS episodes phasic events were
The giraes were kept in 2 groups: Group 1 consisted of 5 sometimes apparent, consisting of twitches of the ears and
females and 1 male, Group 2 consisted of a mother and her neck.
female juvenile progeny. The two groups were kept in adjacent The transition from locomotion to RS was gradual. Thus
enclosures. Either Group 1 or Group 2 was placed into the
enclosurewherethe cameras were installed. On severalrecorded individuals had a preferred sleeping site within the enclosure
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
24 I. Tobler and B. Schwierin
Figure 1. Behavioural changes leading to postures typical for the vigilance states recumbent sleep (bottom left) and PS (bottom right).
which they would approach several times before finally taking an adult and the immature male, are illustrated in Figs 2 and
3. On several days napping episodes were evident. On mosta recumbent posture. The transition from recumbent
wakefulness to RS could occur several times before a PS days the main sleep period was between 20.00 and 07.00 hours.
episode could be seen. The occurrence of SS was not related
to the subsequent RS. Sleep profile
Sleep rarely occurred outside the barn (our own occasional The mean 24-h sleep profile is illustrated in Fig. 4. It exhibited a
observations and personal communication from the similar bimodal pattern in all the individuals with RS occurring
caretakers). The animals were always returned to the barn between 20.00 and 07.00 hours, with a small trough between
before 17.00 hours, and thereafter spent several hours feeding. 02.00 and 04.00 hours. SS occurred more frequently towards
Sleep onset was defined as the time of day when sleep occurred the end of the sleep period (ANOVA factor interval from 18.00
for at least 3 consecutive minutes. Sleep onset was at 20.18 to 08.00 hours, N=6, d.f.=13, SS F=4.15; RS F=8.54, PS
hours (±18.1 min; N=8) and the end of the sleep period was F=4.12, all vigilance states P<0.0001, except PS/TST which
at 06.18 hours (±5.9 min). The time of day when sleep began was n.s.). In the comparison of the first and second half of the
did not dier between nights following a day with access to night, SS was significantly more abundant in the second half
the outside enclosure (20.6 hours±23.8 min) vs. nights (P<0.02, two-tailed paired t-test). PS was evenly distributed
following days spent inside (20.6 hours±22.0 min).
Thevigilancestateson8consecutivedaysfortwoindividuals, across the entire night.
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
Behavioural sleep in the giraffe 25
Figure 2. Vigilance states of an individual adult female girae (Augusta, age 3.5 years) recorded for eight consecutive nights. W=waking while
in locomotion or moving, WR=waking recumbent, SS=standing sleep, RS=recumbent sleep, PS=paradoxical sleep.
The mean 24-h-values of the vigilance states are presented unchanged when the data were restricted to days when the
animals were not allowed Table 2 and Fig. 5. Total sleep time expressed as a percentage
of24 h varied between 14.4and 22.4% with sleep ina recumbent
position between 6.4 and 20.4% of 24h. A one-way ANOVA Sleep episode duration
factor ‘age’, for the amount of each of the vigilance states was The PS episodes were short, with 24% lasting less than 1
significant for all stages including TST (d.f.=7, SS F=21.31, min (Fig. 6, Table 3). The longest PS episodes occurred in the
RS F=20.72, PS F=8.41, TST F=7.37, all vigilance states juvenile, which exhibited also the largest variability in PS
P<0.0001). While no age relationship was evident for TST in duration. The inclusion of a maximum interruption criterion
the post-hoc analysis, the lowest amount of RS was present in of 2 min RS to interrupt PS did not have a large eect on the
the oldest girae and SS was most prominent in the oldest two duration of PS episodes (mean duration in minutes: 4.3±0.3,
giraes (comprising 7.5% of 24 h; Fig. 5, Duncan multiple N=8; 4.1±0.23, N=7; Table 3). The mean duration of RS
range test, P<0.05). The juvenile never exhibited SS. An age episodes (excluding PS) varied between 8.1 and 13.2 min,
dependence became evident for the total time in recumbency, although single RS episodes could last for up to 100 min. Of
irrespective of whether the animals were asleep or in all RS episodes 58.7%±2.4 (N=7) were shorter than 11 min
wakefulness (Table 2). The oldest animal exhibited the lowest (data not shown). No evident age relationship was present for
amount and the youngest the highest amount of recumbency
(Duncan multiple range test, P<0.05). This result was episode duration of any vigilance state, with the exception
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
26 I. Tobler and B. Schwierin
Figure 3. Vigilance states of an individual immature male girae (Hans, age 2.2y) recorded for eight consecuitve nights. W=waking while in
locomotion or moving, WR=waking recumbent, SS=standing sleep, RS=recumbent sleep, PS=paradoxical sleep.
that the juvenile exhibited the shortest RS episodes (Duncan Access to outdoor pen
multiple range test, P<0.05; N=8). Only Group 1 had access to the outdoor pen (mean duration
of time spent outdoors 5.0 h±1.4 min, N=5; range 2.1–6.7 h;
Sleep cycle duration on N=10d the entire group remained inside due to bad
weather, and the male (Hans) was outside on only two of the
A PS cycle was defined as the interval between the onset of 24 d and was excluded from the analysis). Since the juvenile
two consecutive PS episodes. When no interruptions of the female (Twanja) was still too young to be allowed outside in
cycle were allowed by other vigilance states, there was a large the early spring weather, the mother (Taos) and the juvenile
peak of PS cycles of 1–5 min duration and an even distribution always remained inside the barn. The comparison of the sleep
of cycles of 6–35 min duration (Fig. 7, top left). The inclusion states and their distribution on nights (18.00–08.00 hours)
ofacriterion allowing <5 min of wakingassingle or consecutive following a day spent outdoors with nights following upon
1-min epochs within a PS cycle did not have a major eect on days when the animals remained in the barn resulted in a
this distribution (Fig. 7, top right). Allowing 1 or 2 min RS significant redistribution of TST (Fig. 8; ANOVA factor
within a PS episode with or without the waking criterion interaction ‘condition interval’ for 1-h intervals, d.f.=13,
reduced the frequency of PS cycles Ζ5 min, whereas the
distribution of cycles between 6 and 35 min remained similar. F=2.43, P<0.007). The biphasic sleep pattern was less
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
Behavioural sleep in the giraffe 27
compriseatleast 5 min between 08.00 and17.00 hours. Daytime
sleep was usually seen between 12.00 and 16.00 hours in some
of the giraes (Figs 2, 3, 4, Table 2). The total duration of
daytime sleep is illustrated in the frequency histogram (Fig. 9).
The amount of daytime sleep was small since most naps
were short, comprising 5–50 min, but occasionally reaching a
cumulative value of 50–90 min.
The comparison of sleep duration in the nights following a
day with or without daytime sleep (N=3–15 vs. N=10d with
daytime sleep in 4 giraes; daytime sleep < than 10 min was
excluded from this analysis) resulted in a significantly lower
RS value (48.1 min) after daytime sleep and an increase in
SS (15.2 min; P<0.04, two-tailed paired t-test); whereas TST
remained unchanged. The results were not aected when the
exclusion criterion of <10 min for daytime sleep was eliminated
(N=1–17 vs. N=4–10 days with daytime sleep, in 5 giraes).
The duration of all daytime sleep episodes did not correlate
significantly with TST on the subsequent night, or with the
amount of RS alone (r
=0.06 for TST and for RS).
The animals obtained a relatively low amount of sleep per
24h, although we did include SS, which previously has never
been quantified in giraes, and RS which due to the frequent
rumination bouts was not considered as sleep. However, the
4.6 h are more than usually reported for the girae, since most
other studies were influenced by the notion that girae sleep
only in the ‘deep sleep’ posture, which corresponds to the
behavioural PS scored in our study. Kristal andNoonan (1979)
did describe S-sleep (behavioural sleep in recumbency), but did
not report its amount in the adults. In contrast to their study
we chose to exclude chewing in recumbency as a criterion for
waking. EEG recordings in cattle and sheep have shown that
nonREM sleep occurs during cud chewing (Ruckebusch et al.
Figure 4. Daily distribution of the vigilance states. The lines connect
1974; Bell and Itabisashi 1993).
mean hourly values. Top panel: mean values per hour (N=6
giraes) recorded for 18–25d, middle panel: a 13-y old female,
SS has also been observed in the elephant (Tobler 1992), the
mother of the juvenile female (3-month old, lower panel). The
behaviour during this state being very similar in elephants and
mother and the juvenile were simultaneously recorded for 6d. Black
giraes. However, in the giraes it did not precede RS as was
area, paradoxical sleep (PS), dashed area, recumbent sleep (RS),
often the case in the elephants, and is was not interrupted by
white area, standing sleep (SS). Total area under the curve represents
total sleep time.
short waking bouts characterized by swaying movements of
the body and head (and flapping the ears) as in the elephants.
It has been shown on the basis of EEG recordings for many
ungulates that sleep can occur in a standing position (e.g.
prominent when the animals had been outside, since the lower Ruckebusch and Bell 1970). On the basis of such data it can
values between 02.00 and 04.00 hours were absent. While be assumed that the behaviourobserved in the standing giraes,
TST over the entire night or the 24h was unaected, it was scored here as SS, could indeed be considered sleep. The
significantly decreased in the second half of the night following inclusion of SS did not have a large eect on the TST reported
an indoor day vs. a day with access to the outside enclosure here since SS comprised only 47 min of 24 h. In general, RS
(mean values in minutes after days: inside 131.2±5.4, outdoors episodes were short (58.7% RS episodes were shorter than 10
150.3±3.2; N=5; P<0.008, two-tailed paired t-test). min; in the juvenile over 70% were shorter than 10 min). Thus
sleep in girae is very fragmented. Possibly the long legs and
Effect of daytime sleep neck contribute to a dicult recumbent sleeping posture which
does not allow quick fleeing as a response to external stimuli.
Napping (SS, RS and PS) was scored on those days when the
animals remained indoors. A daytime sleep episode had to The diculties in raising from the ground could contribute to
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28 I. Tobler and B. Schwierin
Table 2 Duration of vigilance states, recumbency and daytime sleep
Twanja 0.2 5 0.0 (0.0) 15.0 (0.6) 1.4 (0.3) 16.4 (0.4) 8.6 (1.8) 16.4 (0.4) 1 0.6 40.7 (1.6)
Raisa 2.1 25 1.5 (0.4) 17.3 (1.0) 0.7 (0.1) 18.1 (1.0) 3.7 (0.4) 19.6 (0.9) 3 1.0 (0.3) 25.2 (1.1)
Hans 2.2 25 0.8 (0.2) 18.3 (1.0) 1.3 (0.1) 19.6 (1.0) 7.0 (0.8) 20.4 (1.0) 17 1.9 (0.3) 30.7 (0.8)
Naomi 3.4 22 0.9 (0.4) 20.4 (1.0) 1.1 (0.1) 21.5 (1.1) 4.9 (0.5) 22.4 (1.1) 6 4.0 (0.5) 32.0 (1.2)
Augusta 3.5 25 2.1 (0.4) 17.5 (0.9) 1.1 (0.1) 18.6 (0.9) 5.6 (0.6) 20.7 (0.8) 7 1.0 (0.2) 26.7 (0.9)
Tiny 3.6 18 2.9 (0.6) 12.2 (0.9) 0.8 (0.1) 13.0 (1.0) 4.9 (0.5) 16.0 (0.9) 0 0.0 (0.0) 18.4 (1.2)
Taos 13 6 7.5 (2.0) 11.8 (2.1) 0.7 (0.2) 12.5 (2.1) 3.4 (0.9) 20.1 (0.7) 0 0.0 (0.0) 16.4 (2.7)
Cornelia 20 25 7.5 (0.8) 6.4 (1.0) 0.4 (0.1) 6.9 (1.1) 3.1 (0.7) 14.4 (1.1) 0 0.0 (0.0) 11.1 (1.5)
Mean (n=8) 2.9 (1.1) 14.9 (1.6) 1.0 (0.1) 15.8 (1.7) 5.1 (0.7) 18.7 (1.0) 25.1 (3.4)
Mean (n=7)
3.3 (1.1) 14.9 (1.8) 0.9 (0.1) 15.7 (1.9) 4.7 (0.5) 19.1 (1.1) 22.9 (3.0)
Sleep was subdivided into standing (SS), recumbent (RS) and paradoxical sleep (PS). REC=total time spent in recumbency. Total sleep (TST)
includes the three subdivisions of sleep. Mean values in percentage of 24h (±SEM) except for PS/TST; age in years; n=number of animals;
N=number of days or number of days with daytime sleep; Nap=TST between 12:00 and 16:00 hours;
mean value excluding Twanja.
Figure 5. Vigilance states represented as a
function of age. The bars represent mean
values±s.e.m. as percentage of 24h for total
sleep, standing sleep and recumbent sleep, and as
percentage of total sleep time for paradoxical
sleep (note the dierent scale for paradoxical
sleep). The age of the animals is indicated below
the bars.
the short duration of sleep and maybe to the development of that PS is less abundant and of shorter duration in animals
with a large predatory index (Allison and Cicchetti 1976). Thethe capacity to obtain sleep in a standing posture. Elephants
havediculties in rising easily fromrecumbency,also; however, question remains open as to whether the PS described here
(which others have quantified as ‘deep sleep’) corresponds tothe mean duration of their RS (which included PS) was 61–77
min (Tobler 1992). It is probable that elephants are less REMsleep found in othermammals; this needsto beconfirmed
by electroencephalography. The remarkable posture, thesusceptible to predation than girae.
The PS episodes were brief, usually below 3 min and they concomitant phasic events and the EEG findings in species
such as horse, cattle, sheep and piglets showing that PS isonly amounted to 13 min per 24h or 4.7% of TST. These
values are similar to those for ‘deep sleep’ episodes which attained only when in recumbency and the head can be rested
(Ruckebusch et al. 1974), are a strong indication that thelasted 1–10 min in 1–2 episodes per night reported by Kristal
and Noonan (1979) and the 2.5–6 min-episodes found by behavioural PS defined in the girae is a correlate of PS as
described by EEG patterns in other mammals. In summary,Grzimek (1956). Thus the present data support the hypothesis
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
Behavioural sleep in the giraffe 29
min in a 4-month old, but similar to the 21 min in the adults
(Grzimek 1956). Although no age eect was found for PS, the
juvenile did exhibit the largest variation in the duration of PS
episodes, but as in many other species PS/TST was most
prominent in the youngest animal. In addition, RS episodes
were shortest in the juvenile, indicating that her sleep was the
most fragmented. SS was never observed in this animal, which
is reminiscent of the late appearance of SS in the developing
young elephant (Tobler 1992).
An additional factor which may explain the larger dierence
between young and adults in both elephants and giraes is
that young giraes have only a weak bond with their mother
except during the first few days after birth, in contrast to the
strong bond lasting for several years in the elephant. However,
Langman (1977) who investigated the cow–calf relationship in
giraes observed cases of a strong relationship between the
girae cow and calf which lasted until the cow’s next calving.
Girae calf usually suckle only until approx. one month of
age, but up to one year has been seen, whereas elephants suckle
3–4 years. A girae calf stays with its mother till 16–18 months
(usually in a ‘kindergarten’, i.e. nursery) when it becomes
independent. Sexual maturation is reached at 4 years. Our
Figure 6. Frequency distribution of paradoxical sleep episodes. Bars
juvenile was never observed suckling, which indicates a
represent mean values±s.e.m. computed for 10-min bins of N=7
relatively large independence from the mother.
giraes (top panel) and the single juvenile female (bottom panel).
An age dependence in the amount of time spent lying was
Data are expressed as percentage of the total amount of episodes for
seen in giraes in the wild, but no details are given (Langman
each individual. Note the dierent scale of the top and the lower
1977). The adult male was seen only once sleeping for 10 min
motionless in a standing position with his eyes closed. In the
zoo total time spent in recumbency (7–9h) did not dier
between the adults and the single juvenile (Grzimek 1956).
the present data suggest that sleep duration in the girae has The juvenile did get up more frequently but returned into
been underestimated. recumbency more rapidly than the adults. In the present study
It is well known that for many mammalian species the the juvenile exhibited the largest amount of total recumbency
amounts of each sleep stage depends on the age and level of and the oldest girae the smallest amount (Table 2). Also,
development at birth (rat, cat, guinea pig: Jouvet-Mounier et another ungulate exhibited an age-dependent amount of time
al. 1969; piglet: Kuipers and Whatson 1979). Due to the age spent in recumbency: foals (7.1% of 24 h), stallion (2.4%), and
distribution in our giraes such aspects could be addressed. mares (3.6%) (Bubenik 1978). The oldest giraes exhibited the
However, the 3-month old juvenile borders on to the next age lowest amount of RS and largest amount of SS. Assuming that
category of ‘immature’, and cannot be expected to reflect the the reclining position involves considerable eort (Fig. 1), it
sleep states of a young animal. The amount of PS in the 3-
month old female was 20 min which was less than the 63–72 could explain why these older animals obtained less RS and
Table 3 Duration of vigilance state
Age (y) PS N RS N SS N
Twanja 0.2 5.6 (1.0) 18 8.1 (0.4) 152 0.0 (0.0) 0
Raisa 2.1 2.9 (0.2) 94 13.2 (0.5) 473 5.7 (0.6) 94
Hans 2.2 4.9 (0.2) 99 11.1 (0.4) 591 5.4 (0.7) 53
Naomi 3.4 3.8 (0.3) 92 12.0 (0.5) 536 5.3 (0.9) 52
Augusta 3.5 3.5 (0.2) 118 10.9 (0.4) 578 6.7 (0.6) 112
Tiny 3.6 3.8 (0.4) 54 10.0 (0.5) 316 6.9 (0.6) 111
Taos 13 3.2 (0.4) 19 11.4 (1.1) 90 6.0 (0.5) 109
Cornelia 20 4.2 (0.4) 38 9.9 (0.6) 234 5.2 (0.2) 517
Mean (n=8) 4.0 (0.3) 10.8 (0.5) 5.1 (0.8)
Mean (n=7)
3.7 (0.3) 11.2 (0.4) 5.9 (0.3)
Mean values in min (±SEM) of all days separately for each animal and over dierent groups
of animals. N=total number of episodes per girae; n=number of animals;
mean value
excluding Twanja.
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
30 I. Tobler and B. Schwierin
Figure 7. Frequency distribution of PS-cycle
duration in 1-min bins. The frequency of each
bin was expressed as percentage of the total
number of PS cycles per individual. The bars
represent mean values±s.e.m. (N=7, i.e.
excluding the juvenile). Left panels: no waking
was allowed within the cycle. Right panels:
waking <5 min as single or consecutive 1-min
epochs was allowed within a cycle. Top panels:
no interruption of PS episodes was allowed.
Bottom panels: a maximum of 2 single or
consecutive 1-min RS epochs (but no waking)
was allowed within a PS episode.
Figure 9. Frequency distribution of total duration of the cumulated
daytime sleep episodes within single days. Bars represent the
frequency of daytime sleep duration classified into 5-min bins for
N=6 giraes.
Figure 8. Eect of access to an outdoor pen during the day on sleep
distribution in the subsequent night. The lines connect mean hourly
values of total sleep time (±s.e.m., N=5), after days with (outdoor)
and without (indoor) access to an outdoor pen. Comparison of 1-h
(Zepelin and Rechtschaen 1974; Allison and Cichetti 1976).
intervals outdoor vs. indoor, ∗∗P<0.007, P<0.02, two-tailed paired
The daily sleep quota cited by Zepelin (1994) for the Asiatic
elephant was 3.9h (African elephant 3.3 h) and for giraes
1.9h, which contrasts with both our TST values in elephants
(circus without sleep ad lib: 3.5h; zoo – summer 5.9 h, winter
6.7h; Tobler 1992) and in giraes, at 4.6 h (evenexcluding SS,compensated with an increase in SS. Also in the elephants the
oldest cow exhibited the least RS (Tobler 1992). which is arbitrary and could be considered as drowsiness this
would give values of: girae: 3.8h, elephants: circus 3.3h, zooIn summary, the smaller amount of sleep and the shorter
duration of RS and PS episodes in giraes may be a summer 3.7 h, winter 4.5 h).
It has been shown for many species that sleep is regulatedconsequence of a larger predatory risk, but this does not
confirm the negative correlation withbody size or brain weight as a function of prior wakefulness (reviewed by Borbe
´ly 1994).
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
Behavioural sleep in the giraffe 31
In particular, sleep intensity is increased after prolonged the two conditions were responsible for the redistribution of
sleep and its increase in the second half of the night.
wakefulnessorreduced in the night following anappingepisode In conclusion, this study demonstrates that behavioural
(Feinberg 1982; Werth et al. 1996). In several species TST is observations in undisturbed animals can contribute to our
increased and motor activity during sleep is decreased after a understanding of sleep mechanisms inspecies where performing
period of sleep deprivation (reviewed by Tobler 1985; Deboer EEG recordings is more dicult.
et al. 1994). Sleep regulation has been little investigated in
ungulates. Ruckebusch (Ruckebusch and Bell 1970;
Ruckebusch et al. 1974; Ruckebusch 1975) performed selective ACKNOWLEDGEMENTS
deprivation of REM sleep and partial sleep deprivation in cows The study was supported by the Swiss National Science
by preventing recumbency for 14–22h per day for 2–4 weeks. Foundation, grant 31.32574.91 and 3100.042500.94. The
Both nonREM sleep and REM sleep were significantly recordings were obtained in the Dierepark Emmen, Holland
increasedduringrecovery.During recovery,drowsiness, defined with the permission of H. Hiddingh. We thank Mr H. Scheeve
as a wakefulness with a mixture of high and low voltage and the caretakers of the giraes for their cooperation and for
synchronized EEG activity, usually encompassing about 30% the daily changing of the video tapes, Mr K. Wu
¨thrich for
of wakefulness, was not aected. Similarly, cattle deprived technical assistance and P. Achermann and A.A. Borbe
´ly for
from lying for 3h increased the duration of lying in the critical reading of the manuscript.
subsequent recovery period (Metz et al. 1984/1995). Data from
the present study reflect several aspects of sleep regulation in
the girae. Whereas experimental manipulations such as sleep REFERENCES
deprivation in wild animals in a zoo are not without risks the
Adams, J. and Berg, J.K. Behavior of female African elephants
continuousobservationof animals does allow one toinvestigate
(Loxodonta africana) in captivity. Appl. Anim. Ethol., 1980, 6:
the eects of napping episodes on the subsequent night. The
Allison, T. and Cicchetti, D.V. Sleep in mammals: ecological and
frequent occurrence of napping allowed the analysis of nights
constitutional correlates. Science, 1976, 194: 732–734.
following naps vs. nights not preceded by napping. If sleep in
Balch, C.C. Sleep in ruminants. Nature Lond., 1955, 175: 940–941.
the girae is finely regulated and if SS is a less intense sleep
Bell, F.R. and Itabisashi, T. The electroencephalogram of sheep and
stage than RS we would expect a decrease of RS in the nights
goats with special reference to rumination. Physiol. Behav., 1973,
11: 503–514.
following daytime naps. A significant reduction of RS was
Benedict, F.G. The Physiology of the Elephant. Carnegie Institution of
present, while SS was not aected. These results may be similar
Washington, Washington, 1936.
to the reduction of EEG slow-wave activity in humans on the
´ly, A.A. Sleep homeostasis and models of sleep regulation. In:
night following a napping episode (Feinberg 1982; Werth et al.
M.H. Kryger, T. Roth, and W.C. Dement (Eds) Principles and
Practice of Sleep Medicine, 2nd edn. Saunders, Philadelphia, 1994:
It is dicult to establish the relationship of SS to RS in the
Campbell, S.S. and Tobler, I. Animal sleep: a review of sleep duration
absence of EEG recordings. Thus it is not clear whether SS is
across phylogeny. Neurosci. Biobehav. Rev., 1984, 8: 269–300.
a less intense sleep state than RS. The relationship between SS
Dallaire, A. Rest behavior. Vet. clin. north. amer. (Equine Pract.), 1986,
and drowsiness as defined by the EEG by Ruckebusch (1972)
2: 591–607.
is also not clear. There are several indications that SS is a form
Dallaire, A., Toutain, P.L. and Ruckebusch, Y. Sur la pe
sommeil paradoxal: faites et hypothe
`ses. Physiol. Behav., 1974, 13:
of ‘light’ sleep. Moreover, the present results show that these
two sleep states were finely regulated. Thus both SS and RS
Deboer, T., Franken, P. and Tobler, I. Sleep and cortical temperature
showed a prominent intra- and inter-individual variation, but
in the Djungarian hamster under baseline conditions and after sleep
complemented each other, resulting in a relatively constant
deprivation. J. Comp. Physiol. A., 1994, 174: 145–155.
value for TST. This feature has also been observedin elephants
Deboer, T. and Tobler, I. Shortening of the photoperiod aects sleep
distribution, EEG and cortical temperature. J. Comp. Physiol. A.,
(Tobler 1992). A remarkable stability of TST hasbeen reported
in press.
for other species on the basis of EEG recordings, e.g. under
Elgar, M.A., Pagel, M.D. and Harvey, P.H. Sleep in mammals. Anim.
shortand long photoperiods. Despite themarked redistribution
Behav., 1988, 36: 1407–1419.
of sleep in the two photoperiods, TST remained constant (rat:
Feinberg,I., March, J.D., Floyd,T.C.,Jimison,R., Bossom-Demitrack,
Franken et al. 1995; Djungarian hamster: Deboer and Tobler
L. and Katz, P.H. Homeostatic changes during post-nap sleep
maintain baseline levels of delta EEG. Electroenceph. Clin.
Neurophysiol., 1985, 61: 134–137.
Furthermore, the access to the outdoor pen aected the sleep
Franken, P., Tobler, I. and Borbe
´ly, A.A. Varying the photoperiod in
profile in the subsequent night. Thus the bimodal sleep pattern
the laboratory rat: profound eect on the 24-h sleep pattern but no
was less prominent and TST significantly enhanced in the
eect on sleep homeostasis. Am. J. Physiol., 1995, 269: R691–R701.
second half of the night, on nights following access to the
Grzimek, B. Schlaf von Giraen und Okapi. Naturwiss., 1956, 17: 406.
Hediger, H. Tiere im Schlaf, 2. Documenta Geigy, J.R. Geigy S.A.
outdoor enclosure. Since sleep onset was not aected, and TST
Basel, 1955: 1–9.
in the first part of the night did not dier between nights after
Hediger, H. Wie Tiere schlafen. Med. Klin., 1959, 20: 938–946.
hours outside vs. nights spent indoors, it is improbable that
Hediger, H. Comparative observations on sleep. Proc. R. Soc. Med.,
the result was a consequence of the activities in the outside
1969, 62: 153–156.
Hediger, H. Natural sleep behaviour in vertebrates. In: M. Monnier
enclosure. It is possible that dierent feeding patterns under
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
32 I. Tobler and B. Schwierin
and M. Meulders (Eds) Functions of the Nervous System. Elsevier, Ruckebusch, Y. Sleep deprivation in cattle. Brain Res., 1974, 78:
Amsterdam, 1983: 105–130. Ruckebusch, Y. and Toutain, P.L. La phyloge
`se du sommeil.
Hediger, H. Schlafsto
¨rungen. In: V. Faust (Ed.), Compendium Confront. Psychiat., 1977, 15: 9–48.
Psychiatricum. Hippokrates, Stuttgart, 1985: 48–54. Ruckebusch, Y. and Morel, M.T. Etude polygraphique du sommeil
Immelmann, K. Vom Schlaf der Girae. Umschau, 1958, 12: 356–357. chez le porc, C.R. Acad. Sci. Paris, 1968, 1346–1354.
Immelmann, K. and Gebbing, H. Schlaf bei Giraden. Z. Tierpsychol., Ruckebusch, Y. The relevance of drowsiness in the circadian cycle of
1962, 19: 84–92. farm animals. Anim. Behav., 1972, 20: 637–643.
Jouvet-Mounier, D., Astic, L. and Lacote, D. Ontogenesis of the states Ruckebusch, Y. The hypnogram as an index of adaptation of farm
of sleep in the rat, cat, and guinea pig during the first post-natal animals to changes in their environment. Appl. Anim. Ethol., 1975,
month. Devel. Psychobiol., 1969, 2: 216–239. 2: 3–18.
Kristal,M.B.andNoonan,M.Noteonsleepincaptivegiraes(GiraaRuckebusch, Y., Dougherty, R.W. and Cook, H.M. Jaw movements
camelopardalis reticulata). S. Afr. J. Zool., 1979, 14: 108. and rumen motility as criteria for measurement of deep sleep in
Kuipers, M. and Whatson, T.S. Sleep in piglets:an observational study. cattle. A.J. Vet. Res., 1974, 35: 1309–1312.
Appl. Anim. Ethol., 1979, 5: 145–151. Tobler, I. Deprivation of sleep and rest in vertebrates and invertebrates.
Langman, V.A. Cow-calf relationships in girae (GiraaIn: S. Inoue
´and A.A. Borbe
´ly (Eds) Endogenous Sleep Substances
camelopardalis giraa). Z. Tierpsychol., 1977, 43: 264–286. and Sleep Regulation. VNU Science Press BV, Utrecht (Taniguchi
McKay, G.M. Behavior and ecology of the asiatic elephant in Symposia, Series no. 8), 1985: 57–66.
southeastern Ceylon. Smithson. Contr. Zool., 1973, 125: 1–113. Tobler, I. Napping and polyphasic sleep in mammals. In: D. Dinges
Meddis,R. The evolutionofsleep. In: A.Mayes(Ed.) Sleep Mechanisms and R. Broughton (Eds) Napping: Biological, Psychological, and
and Functions in Humans and Animals: an evolutionary perspective. Medical Aspects. Raven Press, 1990: 9–30.
Van Nostrand Reinhold press (UK), Berkshire 1983: 57–106. Wert, E., Dijk, D.J., Achermann, P. and Borbe
´ly, A.A. Dynamics of
Metz, J.H.M. The reaction of cows to a short-term deprivation of the sleep EEG after an early evening nap: experimental data and
lying. Appl. Animal Behav. Sci., 1984/85, 13: 301–307. simulations. A. J. Physiol., in press.
Moss, C. Portraits in the Wild. Houghton Miin Co., Boston, 1975: Zepelin, H. and Rechtschaen, A. Mammalian sleep, longevity, and
39–61. energy metabolism. Brain Behav. Evol., 1974, 10: 425–470.
Ruckebusch, Y. and Bell, F.R. Etude polygraphique et Zepelin, H. Mammalian sleep. In: M.H. Kryger, T. Roth, and W.C.
comportementale des e
´tats de veille et de sommeil chez la vache Dement (Eds) Principles and Practice of Sleep Medicine. WB
Saunders Company, 1989: 30–49.(Bos taurus). Ann. Rech. ve
´r., 1970, 1: 41–62.
1996 European Sleep Research Society, J. Sleep Res.,5, 21–32
... Although much of what is known about sleep has been gleaned from the study of rodents and primates [1,7,8], studies of other mammals and birds have revealed striking differences in sleep. For example, ruminants and other large mammals can sleep while standing [9][10][11], marine mammals can sleep while swimming [12,13], some seabirds can sleep while flying [14], and monotremes and ostriches exhibit a mixed SWS-REM sleep state [15][16][17][18]. In this way, the study of "nontraditional" animals has resulted in new insight into conserved, and evolutionarily derived, features and phenotypes of sleep [19,20]. ...
... Shivering-like activity occurred during the day and night, in all four antechinus, and during most, but not all, SWS episodes. In either case, the EEG was characterized by high amplitude slow-waves and sleep spindles (7)(8)(9)(10)(11)(12)(13). SWS would most often give way to REM sleep, characterized by wake-like brain waves, neck muscle hypotonia, intermittent twitching (visible only on the ear and leg), and a cessation of shivering-like movements (Figure 2b). ...
... SWS-related thalamocortical spindles and REM sleeprelated hippocampal theta are common features of sleep in eutherian mammals. Sleep spindles have also been observed across diverse marsupials, including the common opossum (8)(9)(10)(11) [51], North American opossum (10-14 Hz) [56], white-eared opossum (Didelphis albiventris) (10-16 Hz) [66], little water opossum [53], and long-nosed potoroo [67]. Sleep spindles (7)(8)(9)(10)(11)(12)(13) were also found in dusky antechinus, notably, but not exclusively, at SWS-REM sleep transitions. ...
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Study Objectives In this study, we (1) describe sleep behaviour and architecture, and (2) explore how sleep is regulated in dusky antechinus (Antechinus swainsonii), a small insectivorous marsupial. Our aim is to provide the first investigation into sleep homeostasis in a marsupial. Methods Wild-caught male dusky antechinus (n = 4) were individually housed in large indoor cages under a natural photoperiod of 10.5 h light / 13.5 h dark. Continuous recordings of EEG, EMG, and tri-axial accelerometry were performed under baseline conditions and following 4-h of extended wakefulness. Results Antechinus engage in SWS and REM sleep. Some aspects of these states are mammal-like, including a high amount (23%) of REM sleep, but other features are reminiscent of birds, notably, hundreds of short sleep episodes (SWS mean: 34 s; REM sleep: 10 s). Antechinus are cathemeral and sleep equally during the night and day. Immediately after the sleep deprivation ended, the animals engaged in more SWS, longer SWS episodes, and greater SWS SWA. The animals did not recover lost REM sleep. Conclusions Sleep architecture in dusky antechinus was broadly similar to that observed in eutherian and marsupial mammals, but with interesting peculiarities. We also provided the first evidence of SWS homeostasis in a marsupial mammal.
... Resting increased after 20:00 on both event nights and non-event nights. This likely reflects their usual resting patterns and activity [44]. ...
... During our observations, the giraffe did not have access to their outside paddock. Limiting the giraffe's access to the outside enclosure is part of standard winter management practices and best practice recommendations (due to the cold, wet weather conditions in northwest England from November to February) [44,45]. This likely reduced the exposure of the giraffe to the event and any possible stressors the event may have presented. ...
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It is important to examine the animal welfare implications of all aspects of zoo operations, including out-of-hours public events. Research to date has indicated variable responses across species and event types. The current research aimed to understand and quantify the impact of a Christmas lights event. Four species of ungulates: Rothschild giraffe (Giraffa camelopardalis rothschildi; n = 2) in one exhibit and capybara (Hydrochoerus hydrochaeris; n = 4), lowland tapir (Tapirus terrestris; n = 3) and vicuña (Lama vicugna; n = 5) in a mixed species exhibit were observed. Data were collected from 16:00–20:00 between 28 October 2021 and 11 January 2022. The event ran from mid-November to the end of December 2021. Five-minute behavioural observations were undertaken once per hour using instantaneous scan sampling with a one-minute inter-scan interval. A further six days of 12 h observations were conducted to enable a more detailed investigation post-event. Data collected were compared on non-event and event days using Mann–Whitney U tests (event vs. non-event) and Kruskal–Wallis tests (pre-event, event, post-event periods). Kruskal–Wallis tests and one-way ANOVAs were undertaken to compare behaviours during three time periods (12:00–16:00, 16:00–20:00, 20:00–00:00) over 12 h. Mixed behavioural responses were seen across the study species. Capybara spent more time in their house from 16:00–20:00 on event nights compared to non-event nights (p < 0.001) and tapir only engaged in vigilant behaviour from 16:00–20:00 when the event was held, (p = 0.044). There were no differences in frequency of behaviour between pre-event, event, and post-event observation periods, with the exception of capybara, who spent more time OOS in the pre-event period than during (p < 0.001) or after the event (p < 0.001). The results of the project, undertaken as part of an evidence-based management programme, highlighted that the event did not have any overtly negative impacts on the ungulates studied. Except for the giraffe, all individuals had free access to inside and outside environments, and it is believed this choice enabled animals to be active in managing their response to the event. It is recommended that future work observe animals over 24 h to understand whether events lead to behavioural changes the day after events or if animals reverted to normal activity once the event ended.
... In this way, the great interspecific variation observed in the timing, duration, and composition of sleep reflects the optimal sleep architecture for that species in that environment. For example, large herbivorous mammals sleep very little in barns, zoos, and in the wild, just a handful of hours per 24-h day [17][18][19][20][21] . Shortsleeping mammals favour being awake, perhaps because their nutritionally impoverished diet demands voluminous consumption achieved through time-intensive foraging 22 . ...
... Using this criterion, the elephants slept an average of 2 h per 24-h day 21 ; 2 -3 times less than that reported for captive, female Asian elephants (Elephas maximus) video recorded for ten months 18 . Most sleep occurred while the animals were standing, similar to behavioural work on giraffes (Giraffa camelopardalis) 19 , and EEG-based research on horses (Equus ferus caballus) and ...
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Sleep serves many important functions. And yet, emerging studies over the last decade indicate that some species routinely sleep little, or can temporarily restrict their sleep to low levels, seemingly without costs. Taken together, these systems challenge the prevalent view of sleep as an essential state on which waking performance depends. Here, we review diverse case-studies, including elephant matriarchs, post-partum cetaceans, seawater sleeping fur seals, soaring seabirds, birds breeding in the high Arctic, captive cavefish, and sexually-aroused fruit flies. We evaluate the likelihood of mechanisms that might allow more sleep than is presently appreciated. But even then, it appears these species are indeed performing well on little sleep. The costs, if any, remain unclear. Either these species have evolved a (yet undescribed) ability to supplant sleep need, or they endure a (yet undescribed) cost. In both cases, there is urgent need for the study of non-traditional species so we can fully appreciate the extent, causes, and consequences of ecological sleep loss.
... In particular, the sleeping behavior of many ungulates is poorly studied (Lyamin et al., 2021). On the other hand, the nocturnal behavior of very prominent ungulates like giraffes (Grzimek, 1956;Tobler and Schwierin, 1996;Seeber et al., 2012;Sicks, 2016;Burger et al., 2021), elephants (Gravett et al., 2017), or farm animals like cattle (Ruckebusch, 1972;Ternman et al., 2014;Fukasawa et al., 2018) is well studied. However, there are, to the best of our knowledge, many other ungulates whose nocturnal behavior has not been analyzed currently (Campbell and Tobler, 1984;Lesku et al. 2008). ...
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Introduction The nocturnal behavior of many ungulate species has currently not been sufficiently studied. However, the behavioral patterns of large herbivores vary greatly between day and night, and knowledge about species’ behavior is not only scientifically interesting, but also required for successful animal management and husbandry. Material and methods In the current study, the nocturnal behavior of 196 individuals of 19 ungulate species in 20 European zoos is studied, providing the first description of the nocturnal behavior of some of the species. The importance of a wide range of possible factors influencing nocturnal behavior is discussed. Specifically, the behavioral states of standing and lying were analyzed, evaluating the proportion and number of phases in each behavior. The underlying data consist of 101,629 h of video material from 9,239 nights. A deep learning-based software package named Behavioral Observations by Videos and Images Using Deep-Learning Software (BOVIDS) was used to analyze the recordings. The analysis of the influencing factors was based on random forest regression and Shapley additive explanation (SHAP) analysis. Results The results indicate that age, body size, and feeding type are the most important factors influencing nocturnal behavior across all species. There are strong differences between the zebra species and the observed Cetartiodactyla as well as white rhinos. The main difference is that zebras spend significantly less time in a lying position than Cetartiodactyla. Discussion Overall, the results fit well into the sparse existing literature and the data can be considered a valid reference for further research and might help to assess animal's welfare in zoos.
... Although accelerometer data alone cannot discriminate between sleep phases, the association of this method with other remote assessed physiological measures, such as heart rate or body temperature [29,30], could make this technology a reliable tool to assess sleep quantity and quality (e.g., sleep fragmentation or reduced sleeping times). Another option would be to associate accelerometer measures with recordings of specific behavioural events that happened during sleep; for example, cows (Bos taurus), giraffes (Giraffa camelopardalis), elephants (Loxodonta africana) and horses (Equus caballus) all need to lay down in lateral recumbency to achieve REM sleep [31][32][33][34]. ...
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Sleep is a physiological process that has been shown to impact both physical and psychological heath of individuals when compromised; hence, it has the potential to be used as an indicator of animal welfare. Nonetheless, evaluating sleep in non-human species normally involves manipulation of the subjects (i.e., placement of electrodes on the cranium), and most studies are conducted in a laboratory setting, which limits the generalisability of information obtained, and the species investigated. In this study, we evaluated an alternative method of assessing sleep behaviour in domestic dogs, using a wearable sensor, and compared the measurements obtained to behavioural observations to evaluate accuracy. Differences between methods ranged from 0.13% to 59.3% for diurnal observations and 0.1% to 95.9% for nocturnal observations for point-by-point observations. Comparisons between methods showed significant differences in certain behaviours, such as inactivity and activity for diurnal recordings. However, total activity and total sleep recorded did not differ statistically between methods. Overall, the wearable technology tested was found to be a useful, and a less-time consuming, tool in comparison to direct behavioural observations for the evaluation of behaviours and their indication of wellbeing in dogs. The agreement between the wearable technology and directly observed data ranged from 75% to 99% for recorded behaviours, and these results are similar to previous findings in the literature. Keywords: sleep; PetpaceTM collar; physiology; wellbeing
... By making use of a mobile stretcher and with the assistance of a few people, the head and upper neck should be elevated to prevent passive regurgitation [2]. Under normal circumstances, even when sleeping, giraffes do not lay down with their heads flat on the ground [37]. By elevating the head and neck slightly, it therefore may aid in blood pressure management, as well as assisting with the veterinary monitoring of the animal. ...
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One of the highest occurrences of mortalities among giraffes (Giraffa camelopardalis) takes place during immobilisations, captures and translocations. Common mistakes, human error, unforeseen risks, the awkward anatomy and the sheer size of the animal are leading factors for giraffes’ mortalities during these operations. Many risks can be circumvented but some risks are unpreventable, often due to terrain characteristics (rivers, deep ditches, holes and rocky terrain). From 2011 to 2021, seventy-five giraffes were successfully immobilised and captured to collect biological and physiological data from eight different study areas across South Africa. A 0% mortality and injury rate was achieved and, therefore, the techniques described in this paper are testimony to the advances and improvements of capture techniques and drugs. Biological information and capture experiences were noted for 75 immobilised giraffes, of which, knockdown time data were recorded for 43 individuals. Effective and safe immobilisation requires a competent team, proper planning, skill and knowledge. In this manuscript, we address procedures, techniques, ethical compliance, welfare and safety of the study animals. General experiences and lessons learned are also shared and should benefit future captures and immobilisations by limiting the risks involved. The sharing of experiences and information could influence and improve critical assessments of different capture techniques and can likely contribute to the success rate of immobilisation and translocation success for giraffes in the future.
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Since the analysis of animal behavior is a central element of ethology and ecology, it is not surprising that a great deal of research has been conducted describing the behavior of various ungulates. Most studies were conducted during the daylight hours, thus much less is known about nocturnal behavior. Detailed analyses of nocturnal behavior have only been conducted for very prominent ungulates such as giraffes, elephants, or livestock, and the nocturnal rhythms exhibited by many ungulates remain unknown. In the present study, the nocturnal rhythms of 192 individuals of 18 ungulate species from 20 European zoos are studied with respect to the behavioral positions standing, lying - head up, and lying - head down (the typical REM sleep position). Differences between species of the orders Perissodactyla and Cetartiodactyla, as well as between individuals of different age were found. However, no differences with respect to the sex were seen. Most species showed a significant increase in the proportion of lying during the night. In addition, the time between two events of “lying down” was studied in detail. A high degree of rhythmicity with respect to this quantity was found in all species. The proportion of lying in such a period was greater in Cetartidactyla than in Perissodactyla, and greater in juveniles than in adults.
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In the “Two-Process” model, Process C controls circadian distribution of sleep/wake behaviors, whereas Process S regulates daily sleep amount/depth through the waxing (during waking) and waning (during sleep) of sleep need to maintain sleep-wake homeostasis1,2. Besides baseline sleep regulation, acute sleep deprivation leads to subsequent increase of sleep amount and depth, called recovery sleep³⁻⁵. However, the central regulators and mechanisms that govern Process S in mammals remain unclear. Here, we report that induction of constitutively active calcineurin–a Ca²⁺/calmodulin-dependent serine/threonine phosphatase⁶–in mouse brain neurons markedly increases daily amount (to ~18-h/day) and delta power–an index of sleep need–of non-rapid eye movement sleep (NREMS). Adult brain neuron-specific knockout of calcineurin diminishes basal NREMS amount (to ~4-h/day) and delta power, but also recovery NREMS after sleep deprivation. Consistent with neuronal activation of calcineurin during sleep deprivation, simulation of Process S in calcineurin knockout mice reveals an essential role of calcineurin in the accumulation of homeostatic sleep need. Moreover, calcineurin promotes daily NREMS by antagonizing protein kinase A (PKA) and activating salt-inducible kinase SIK3 via S551 dephosphorylation. Together, these results establish calcineurin as a NREMS-promoting phosphatase and a central regulator of Process S that governs sleep homeostasis under both baseline and sleep-deprived conditions in mice.
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This study analyzed the nocturnal behavior of 196 individuals of 19 ungulate species in 20 zoos in Germany and the Netherlands. To the best of our knowledge, this is the first description of nocturnal behavior for some of the species. The importance of a wide range of possible factors influencing nocturnal behavior is discussed. Specifically, the behavioral states of standing and lying were analyzed, evaluating the proportion and number of phases in each behavior. The underlying data consists of 101,629 hours of video material from 9,239 nights. BOVIDS, a deep learning-based software package, was used to analyze the recordings. The analysis of the influencing factors was based on a random forest regression and a SHAP analysis. The results indicate that age, body size and feeding type are the most important factors influencing nocturnal behavior across all species. There are strong differences between the zebra species and the observed Cetartiodactyla as well as White Rhinos. The main difference is that zebras spend significantly less time in a lying position than Cetartiodactyla.
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Most living organisms have evolved to synchronize their biological activities with the earth's rotation, a daily regulation of biology and behaviour controlled by an evolutionary conserved molecular machinery known as the circadian clock. For most animals, circadian mechanisms are meant to maximize their exposure to positive activities (e.g.: social interactions, mating, feeding - generally during the day) and minimize their exposure to peril (e.g.: predation, weather, darkness - generally during the night). On top of circadian regulation, some behaviours also feature a second layer of homeostatic control acting as a fail-safe to ensure important activities are not ignored. Sleep is one of these behaviours: largely controlled by the circadian clock for its baseline appearance, it is at the same time modulated by a - poorly understood - homeostatic regulator ensuring animals obey their species-specific amount of daily sleep. An evolutionary conserved homeostatic control is often considered the main evidence for a core biological function of sleep beyond the trivial one (that is: keeping us out of trouble by limiting our energy expenditure and exposure to danger) and it is hypothesized that sleep evolved around this mysterious basic biological function. Here we characterize sleep regulation in a group of seven species of the Drosophila genus at key evolutionary distances and representing a variety of ecological niche adaptations. We show that the spontaneous circadian-driven aspects of sleep are conserved among all species but the homeostatic regulation, unexpectedly, is not. We uncover differences in the behavioural, cell-biological and neuro-pharmacological aspects of sleep and suggest that, in Drosophilids, sleep primarily evolved to satisfy a circadian role, keeping animals immobile during dangerous hours of the day. The homeostatic functions of sleep evolved independently, in a species-specific fashion, and are not conserved.
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The duration and intensity of the cow‐calf bond during lying out, calving pools and nursery herds has been analysed in a wild population of giraffe (Giraffa camelopardalis giraffa). Field behaviour observations were made on naturally marked and radio‐collared giraffe. Radio‐tracking was used to follow and observe giraffe of a known age for up to 1½ years. The giraffe calf participates in various calf sub‐groups while the cow travels to browse and water. A strong maternal bond exists between the giraffe cow and calf until the cow's next calving. Zusammenfassung Die Entwicklung der Mutter‐Kind‐Beziehung bei Giraffen (Giraffa camelopardalis giraffa) von der Geburt bis zur Trennung von Mutter und Kind wurde beobachtet und in 3 Entwicklungsabschnitte unterteilt: 1. Absonderung des ruhenden Kalbes während der ersten bis dritten Woche nach der Geburt; 2. Säugegruppen, Geburtsgruppen und Gruppen abgesondert ruhender Kälber; 3. Trennung von Mutter und Kalb vor der nächsten Geburt. Entwöhnt werden Giraffen mit 6–8 Monaten; die Kuh‐Kalb‐Beziehungen dauern 14–16 Monate. Der durchschnittliche Anteil von Liegen (78%), Fressen (19%) und Säugen (2%) an der Gesamtaktivität ganz junger Giraffen unterschied diese von halbwüchsigen Giraffen, welche 80% ihrer täglichen Aktivität mit Fressen, 19% mit Liegen und 1% mit Säugen verbrachten.
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Habschr. Zürich (Austausch beschränkt).
Based on data for 53 mammalian species reported in the literature, statistical analyses revealed that daily sleep quotas correlate positively with metabolic rate and negatively with maximum life span and brain weight. Sleep cycle length correlates positively with life span and brain weight and negatively with metabolic rate. Paradoxical sleep figures in these intercorrelations only by virtue of its positive correlation with slow wave sleep. The correlation between sleep time and metabolic rate suggests that sleep has the function of enforcing rest and limiting metabolic requirements, although some inconsistent findings are noted. Strong correlations of cycle length with brain weight and metabolic rate suggest that the significance of cycle length has not been sufficiently explored.
The duration of the REM-sleep was studied in three domestic species with body weights ranging from 40 to 450 kg. The results (goat: 19.2 min; pony: 15.5 min; cow: 15.8 min) lie within a close range. The results and values published for other mammalian species are compared and a parallel drawn between sleep cycle length and the evolutionary level of the species.
The degree of vigilance of an animal is a useful parameter for measuring its behavioural integration with the surroundings. Each species has a particular hypnogram which is very sensitive to variations in the environment and reflects the adaptive response of the animal. Four species, horses, cattle, sheep and pigs were used to study the responsiveness of the different components of the hypnogram to changes in physical environment, social context and diet. Standardized conditions provided a base for measuring the time taken for an animal to revert to its previous hypnogram or to exhibit a stable compensatory mechanism. Depending on the species and the experimental situation, either the number, or the duration of sleep episodes, or both were ersponsive and exhibited progressive adaptation with time. The relevance of the components of the hypnogram as a subtle index of adaptation of the animal to changes in its surroundings is discussed.
The purpose of this research was to ascertain the repertoire of behavior of female African elephants (Loxodonta africana) in captivity. Seven female African elephants were observed for 558 hours and 22 minutes for a period of one year. This paper gives a detailed description of the activities of the elephants maintained in a relatively restricted environment. Twenty one different kinds of behaviors were observed, 14 of which were considered unique to elephants. The most frequently occurring behavior was the placement of the trunk of one elephant into or near the mouth of another elephant. The activities were discussed in terms of: (1) social behaviors; (2) individual behaviors; (3) biological behaviors; (4) dominance hierarchy; (5) four factors derived by statistical factor analysis.
Quiet sleep (QS) was correlated with a different set of constitutional variables from those associated with active sleep (AS), in a sample of 69 species of mammals. The time spent in quiet sleep was negatively correlated with body size and basal metabolic rate. The latter relationship remained even after controlling for the effects of body weight. Neither the total time spent in active sleep, nor active sleep as a percentage of total sleep time was significantly correlated with body weight or metabolic rate. Altricial species spend more time in active sleep than do precocial species. The time between the onset of successive episodes of active sleep, the AS-QS cycle length, was positively correlated with body weight. For their body sizes, species that live in temperate regions have shorter AS-QS cycles than those living in tropical or sub-tropical regions. Correlations between patterns of sleep and adult brain weight probably result from the confounding effects of body weight. These findings were used to evaluate several explanations for interspecific differences in patterns of sleep among mammals.
The development of sleep was examined in 16 piglets during their first 5 weeks of life. Each piglet was observed for one 90 min period each week and a record of the duration of lying, non-REM-sleep and REM-sleep was made. Sleeping position was also recorded. The amount of time spent sleeping and lying did not change systematically over the 5 weeks and neither did the duration of a sleeping episode. However, the duration of REM-sleep decreased from Week 1 to Week 5. REM-sleep could readily be divided into bouts and whereas the median bout length, number of bursts of REM-sleep per bout and duration of each burst remained constant, the mean number of bouts per observation period showed a marked decline with age. REM-sleep was seen to occur more frequently in the crouch position (all 4 legs folded under the body) than in any other position. It was concluded that the development of sleep follows a similar pattern to other precocious and non-precocious species and that piglets are probably not sleep-deprived.