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Characteristics of the circadian activity rhythm in common marmosets (Callithrix j. jacchus)

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American Journal of Primatology 17:271-286 (1989)
Characteristics of the Circadian Activity Rhythm in
Common Marmosets (Callithrix j . jacchus)
HANS G. ERKERT
Institut fur Biologie III, Universitat Tiibingen, Tiibingen, West Germany
The circadian activity rhythm of the common marmoset, Callithrix j .
jacchus was investigated by long-term recording of the locomotor activity
of 15 individuals (5 males, 10 females) from 1.5 to 8 years old, both under
constant illumination and under LD 12:12. The mean period of the
spontaneous circadian rhythm was 23.2 & 0.3 h. Neither sex-specific
differences nor a systematic influence of light intensity on the spontaneous period were observed, but the period was dependent on the duration of
the trial and on the age of the individual. Due to the short spontaneous
period, in LD 12:12 there was a distinct advance of the activity phase with
respect to the light time and a masking of the true onset of activity by the
inhibitory direct effect of low light intensity during the dark time. After an
8 h delay shift of the LD 12:12, re-entrainment of the circadian activity
rhythm required an average of 6.8 0.7 days; the average re-entrainment
time after an 8 h phase advance of the LD cycle was 8.6 +- 1.3 day. This
directional effect is ascribed to characteristics of the phase-response curve.
No ultradian components were observed, either in the LD-entrained or the
free-running circadian activity rhythm.
*
Key words: activity, circadian rhythm, ultradian rhythm, activity pattern,
re-entrainment, CaZZithrix
INTRODUCTION
Callithrix jacchus, the common marmoset, is a small neotropical monkey
which is often thought to have a limited need for living space, and which
reproduces at the high rate of 3-5 offspring per year. For these reasons it has been
considered for years to be a particularly suitable laboratory primate for biomedical
research [Deinhardt et al., 1967; Gengozian, 1969; Poole et al., 19781. As a result,
a wealth of information about the biology of the common marmoset has accumulated. Data are available concerning its behavioral biology and ethology [Epple,
1970; Rothe, 1975; Stevenson & Poole, 1976; Box, 19771, its reproductive biology
and endocrinology [Hearn, 1980,1983; Hearn et al., 1978; Dixson, 1983; Kendrick
& Dixson, 19851, its developmental biology and teratology [Posvillo et al., 1972;
Abbott, 1978; Siddall, 1978; Heger & Neubert, 1983; Moore et al., 19851,
Received for publication August 10, 1988; revision accepted January 11, 1989.
Address reprint requests to Hans G. Erkert, Institut fur Biologie 111, Universitat Tiibingen, Morgenstelle
28, D-7400 Tiibingen, West Germany.
0 1989 Alan R. Liss, Inc.
272 I Erkert
and its physiology [Hawkey et al., 1982; McNees et al., 1982; McIntosh et al., 1985;
Rothwell & Stock, 19851.
By contrast, little is known about the chronobiology of Callithrix jacchus.
Hetherington [19781 found a marked daily variation in rectal temperature in LD
12:12, with an average range from 35/36 to 39°C. Saito et al. [19831showed that in
LD 14:lO marmosets have a daily drinking rhythm, with maximal fluid intake
toward the end of the light phase. Kholkute [1984] demonstrated a marked
bimodal pattern of the plasma androgen level in Callithrix males, with higher
values during the dark phase of an LD 14:lO.
The first recordings of the locomotor activity of marmosets living under
constant environmental conditions in our laboratory revealed a free-running
circadian periodicity of less than 24 h. Furthermore, these recordings showed that
acoustic social contact not only triggers additional activities masking the freerunning endogenous activity rhythm, but also produces variations of the circadian
period length called relative coordination [Erkert et al., 19861. In the experiments
described below additional characteristics of the circadian activity rhythm and of
the endogenous circadian timing system by which it is controlled are presented.
The variability of the spontaneous period is analyzed, and the degree to which the
free-running circadian activity rhythm can be entrained by LD cycles is examined,
together with the re-entrainment of this rhythm after 8 h phase shifts of the
entraining signal.
MATERIALS AND METHODS
The activity recordings were carried out in a total of 15 common marmosets
(5 males and 10 females) aged 1.5-8 years. All the animals were born in captivity.
Some were placed at our disposal from the German Primate Center in Gottingen;
others were obtained from Dr. H. Rothe in Gottingen, from Dr. Ch. Welker in
Kassel, and the rest from our own colony. During the experiments the monkeys
lived in wire mesh cages measuring 85 x 85 x 155 cm or 75 x 105 x 95 cm; 7
animals were kept singly, 4 as pairs, and 4 others both singly and as pairs (Table
I). Data from animals kept as pairs were treated as a unit. The recording cages
were equipped with a sleeping box and sitting board mounted on the rear as well
as with several climbing sticks attached to the wire mesh of the two sides. In the
first series of experiments the marmosets were isolated from one another visually,
but not acoustically or olfactorily, in a 21 m2 room under constant conditions.
Later, to improve the acoustic isolation, the cages of the single animals were placed
within thick-walled (10 cm) wooden boxes measuring 130 x 130 x 160 cm, which
greatly attenuated external sound. The top of each box was covered with a 30
cm-high light box comprising 7 fluorescent tubes (Osram 40 W/25) and two
light-scattering matt plates. The ambient temperature in all experiments was
25°C 2 1"C, and the relative humidity was 60% -t- 5%.
All the animals were fed ad libitum with a protein-rich rice-flake porridge and
mixed fruit as described elsewhere [Erkert et al., 19861. Normally the porridge was
provided shortly after the onset of activity of the marmosets, and the mixed-fruit
meal 4-6 h later. During the constant-condition (LL) experiments the mush and
fruit meals often coincided and were given at randomly varying phases of the
circadian cycle with the exception of the last 2 h of rest time and activity time,
during which the animals' circadian activity rhythm has been shown to be very
susceptible to disturbances.
The locomotor activity of the marmosets was recorded by an electroacoustic
method, whereby the vibrations (sounds in solids) of the wire mesh of the cage
generated by the various activities of the animals (e.g., moving around, intense
Circadian Activity Rhythm in Marmosets I 273
TABLE I. Summary of the Conditions of the Constant-LightExperiments in This Paper
(LLrLL8) Showing the Light Levels, Durations, Numbers of Animals (n), and the
Individuals Used in Each Experiment*
Illumination intensity (lux)
Experiment
ir
* SD
88 % 11
64 ? 35
2.6 1.9
340 ? 160
0.16 lr 0.07
280 ? 80
280 ? 80
420 ? 120
350 % 80
*
Minimum-maximum
78- 100
12- 100
0.4- 5.1
160- 480
0.08-0.23
160- 350
160- 350
240- 500
200- 410
Test animals
Duration
(days)
nl/nz
Individuals
20
20
35
65
20
51
170
150
210150
313
414
414
414
514
915
915
414
616
Fi;Mo;Li
Fi;Mo;Li;To
Fi;Mo;Li;To
Fi;Mo;Li;To
Fi;Mo;To;T/A;(Chi)
AnlBe;DilCl;T/A;GllGr;Mo
An/Be;Di/Cl;T/A;Gl/Gr;Mo
T;A;Di;Cl
G1;Gr;Em;Na;Mo;Ki
*The intensity variation within a given experiment is due to differences in illuminance among the various
recording cages. Under “Test Animals,” the first figure (nl) gives the total No. of individuals, and the second (n,)
gives the No. of recording units. Where the two differ, some of the animals were kept as pairs. Under the
“Individuals,” each of the individual test animals which joined in the respective trial is identified by the first
(two) letter(s) of its name. Names divided by a diagonal stroke mark the individuals which were kept and
recorded together. Further characterizations of the individual test animals are as follows: F i = ym; Mo= of;
Li=of;To=om;Di=om; Cl=of; An=of; Be=om;T=ym;A=yf; Gl=yf; Gr=yf;Em=yEKi=yf; Na=yf, where
ym = young male; yf = young female (53 years); om = old male; of = old female ( 2 4 years).
scratching, scent marking) were picked up by a transducer-like special microphone
(Merula TVJ-XL, Holthausen) that is highly sensitive t o sounds in solids and very
insensitive to sounds propagated by air. Therefore, it was very rarely activated by
the marmosets’ vocalizations. The electrical signals of the microphone were then
amplified to trigger a series of constant-frequency square wave pulses that were
added by electronic counters (Demel V224). The count was sampled at 1-min
intervals by an Apple II+ PC, totaled every 5 min, with the sum then stored on
disk; hard copy was produced by an Epson MX 100 matrix printer. In addition, the
half-hour values were printed out every 24 h. For further analysis the data were
transferred, via Kermit program, to an IBM-compatibleOlivetti PC M-24 with two
floppy disks, a 10 megabyte hard disk, and attached plotter (HP 7475 A). The
period length, T , of the free-running circadian activity rhythm was calculated by
periodogram analyses [Dorrscheidt & Beck, 19751of the consecutive 30 min values
(cf. Fig. 3). Data from four animals were also tested for the presence of an ultradian
periodicity by applying both periodogram analysis and the maximum entropy
spectrum analysis of Marple [1980] t o the consecutive 5 min values. The latter,
according to Leonard [19841, is a particularly suitable method for the analysis of
biological time series.
In order to both evaluate the recording method and ascertain the time course
of several behavioral activities such as feeding and drinking, monitoring, locomotion, scent marking, play, and grooming, as a pilot study we also carried out
certain video observations and tapings of single test animals lasting 12-14 h each.
By using an infrared-sensitive low-light camera (GRUNDIG FAE 70) it was also
possible to check the marmosets’ behavior before the beginning of light time of the
light-dark cycle.
To determine the spontaneous period in various constant light levels and for
different durations of exposure to constant conditions, the marmosets were kept in
constant light (LL)with illumination intensities between 0.1 and 500 lux, for times
ranging from 20 t o 210 days. Table I summarizes the conditions in the successive
constant-light trials such as LL light intensities, duration of experiment, number
274 I Erkert
of test animals, and individuals used. The light intensity in each case was
measured with a Tektronix J 16 digital photometer with a cosine-corrected
photocell (56511). In all measurements the sensor was positioned in the middle of
the recording cage, pointing vertically toward the illuminated matt plates of the
light box. Between consecutive experiments the animals were kept for several
months in LD 12:12 (102:10p1lux), to allow full entrainment and recuperation. In
order to keep the influence of the after effects of entrainment [Pittendrigh & Daan,
1976; Aschoff, 19791 as nearly constant as possible in the evaluation of the
influence of light intensity on the spontaneous period, only the data from the first
20 days of the LL conditions subsequent to an LD 12:12 were used.
RESULTS
Activity Pattern
Common marmosets are strictly diurnal animals. In artificial LD cycles with
>lo0 lux in the light time and light intensities in the dark time ranging from
physiological darkness (<lop6 lux) t o full-moon brightness (0.3 lux), their daily
activity was confined entirely to the light time. As determined by video observation, the monkeys awakened some time before the beginning of the light time and
remained in their sleeping box monitoring the surroundings until the light had
been turned on. Then they immediately began locomotor activity. Activity was
usually terminated 1-2 h before the onset of darkness. As a result, in LD 12:12 the
average duration of activity time was 11.1 2 0.7 h (n = 12 individuals; n’ = 20 days
in each case), and there was a positive overall phase angle difference of the
entrained circadian activity rhythm with respect to the center of the light time of
the LD cycle.
The time course of activity during the light phase varied from one animal to
another. Often there was distinct intra-individual variation, although some
individuals maintained an extremely constant activity pattern for a long time.
Typical examples are shown in Figure 1. The individual patterns found by
averaging the corresponding 30 min counts over a long time (>20 days) in LD
12:12 can be unimodal, bimodal, or trimodal. Accordingly, when several such
individual patterns are averaged, the resulting “species actogram” can be purely
unimodal or tend to have two or three peaks, depending on the composition and
size of the sample population, and on the current andlor preceding environmental
conditions. This complexity is demonstrated by the patterns in Figure 2, which
were obtained from the data for several individuals in three different experiments
with LD 12:12 (200-400:0.2 lux). The top diagram represents the mean individual
patterns (each of which was an average over 20 days) of 5 old marmosets (2 males,
3 females; >5 yr) kept singly and isolated from one another visually but not
acoustically. The middle diagram is based on 4 pairs of old animals ( 2 5 yr), and the
one at the bottom is the average pattern of 5 females, 4 young (<3 yr) and one old
(>4 yr), which 3 months before had completed a long-term free-running session
under constant conditions (LL8) in complete isolation. Since that time they had
been in full acoustical contact with occasional direct mutual visual contact.
The standard deviations given by the vertical lines in Figure 2 differ greatly
from one another. The largest values (i.e., the largest interindividual or betweenpairs differences in activity pattern) are found for the animals kept singly (top and
bottom diagrams). Obviously such animals have less influence on the activity of
others than do pairs of marmosets on other pairs.
The light intensity during the dark time of an artificial LD cycle seems to have
relatively little influence on either the activity pattern or the phase position of the
Circadian Activity Rhythm in Marmosets I 275
~~
2
8 %
4-
0
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4 -
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1 5 h 3
.Duplicate
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31
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Days
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Degrees(360:‘f)
Fig. 1. Intra-individual and interindividual variation of the activity pattern of Cullithrix j. jucchus. Mean
actograms are shown for 4 young females ( 5 3 yr; G L K I ) and one old female ( 2 4 yr; NA) in 3 consecutive 20
day segments (left to right) of the entrained circadian activity rhythm in LD 12:12 (420: 0.2 lux).
Fig. 2. Mean actograms of common marmosets kept in LD 1212 (200-500: 0.2 lux) under various social
conditions (x & SD). Top: Old animals (24yr) kept singly with acoustic contact (n = 5; n’ = 20 days). Middle:
Old animals (24yr) kept a s pairs in acoustic contact with other groups (n = 4 pairs; n‘ = 20 days). Bottom: Four
young and 1 old animals (data from the 2nd column of Fig. 1) kept singly with acoustic social contact.
Fig. 3. Free-running circadian activity rhythm of a female Callzthrix jacchus living under constant ambient
conditions (LL 340 lux). Left: Double plot of the original data. Right: Evaluation mode, shown for the data on
the left. Top: Results of the periodogram analysis to determine spontaneous period. The curve peak marks the
most probable period contained in the time series, and the thin straight line delimits the region above which the
probability of chance is P 5 0.01.Middle: Total amount of activity in consecutive circadian cycles. Bottom:
Mean actogram of the free-running circadian activity rhythm, obtained by averaging over the calculated
spontaneous period 7 = 23.2 h.
276 I Erkert
25
-
20
-
15
-
10
-
5 -
0 22.5
23.0
23.5
24.0 Z ( h )
Fig. 4. Frequency distribution of periods of the free-running circadian activity rhythm of 15 common
marmosets for a total of 167 decades (LL 0.2-500 lux).
entrained CAR with respect to the LD entraining signal. Of the eight individuals
tested in this regard, none noticeably altered its activity rhythm when the dark
illuminance was increased from physiological darkness to 0.1-0.5 lux (full-moon
brightness).
Circadian Period
Under constant environmental conditions in the laboratory the marmosets
generated a free-running circadian activity rhythm (Fig. 3) that remained stable
for a long time (>200 days in tests so far). The period length of this endogenous
rhythm was almost always distinctly shorter than 24 h. Among the 15 individuals
studied to date, the spontaneous period in LL from 0.1 t o 480 lux varied from 22.7
to 24.0 h. The histogram in Figure 4 shows the distribution of the period lengths
as calculated from 167 10 day segments (decades) of the free-running rhythm of
these monkeys while living under constant conditions for several months. The
overall average of the spontaneous period calculated from these data is q , L = 23.3
2 0.3 h. However, the true mean, i.e., the average calculated from the data of the
decades following the 40th day under constant conditions, is slightly shorter (23.2
2 0.3 h; n = 90 decades of experiments LLB and LL,.,). This is due to the fact that
the data of Figure 4 include all the decades of each experiment, and the period
during the first 2-4 decades under constant conditions is usually longer than
subsequent periods (see below and Fig. 6 ) .
There were no differences attributable to the sex of the animals. The average
spontaneous period of the ten females in the study was 23.2 0.3 h, identical with
the 23.3
0.3 h found for the five males. Young marmosets had a somewhat
shorter circadian period in LL than did older animals. On the basis of decade
values (79 for the young and 69 for the old animals) the average T L L of individuals
less than 3 years old was 23.2 L 0.3 h, and that of those over 4 years old was 23.4
2 0.3 h (Mann-Whitney U-test: u = -2.98; P <0.01).
Despite a slight negative correlation between the period length and the
logarithm of LL light intensity (Fig. 5 ) the circadian spontaneous period does not
depend on light intensity. The Spearman rank-correlation analysis of the 7 values
found for the illuminance range from 0.08 to 480 lux showed no significant
correlation between light level and period length (r, = - 0.29; P>0.05). As with all
the other diurnal primates studied so far as well as certain other diurnal
*
Circadian Activity Rhythm in Marmosets I 277
25
f
5
Callithrix jacchus
-..
*. .
.. .
.. .
*:-
23
4
22
I
2
I
1
I
I
3
1
1
22.6
1
2
3
4
5
6
mammals, Callithrix jacchus seems not to obey Aschoff's circadian rule, which
postulates a negative correlation of period length with illumination intensity for
diurnal species in general [Aschoff, 19791.
The circadian period gradually shortened for some time after the beginning of
the LL regimen. Figure 6 shows the average spontaneous periods of 11marmosets
in the first six consecutive 10 day segments of a several-month session under
constant conditions (LL 200-400 lux) following a prolonged stable entrainment by
LD 12:12. The downward trend at the left of the graph indicates that these
aftereffects [Pittendrigh & Daan, 19761 of the preceding 24 h rhythm in Callithrix
jacchus can persist an average of 20-40 days. This influence of duration of
constant conditions on the period of the free-running circadian activity rhythm
was confirmed statistically (Friedman test: P<O .01). Wilcoxon tests showed that
the spontaneous periods of the first decade were significantly longer than those of
decades 3-4 (P <0.01) and 6 (P <0.05), and comparison of the second decade period
values with those of the fourth to sixth decades gave the same result (P<0.05). It
follows that fairly constant period lengths, i.e., a steady state of the free-running
circadian activity rhythm are not reached before the 30th-50th day of constant
conditions. Shorter LL experiments can therefore lead to incorrect results.
The average duration of the activity time of the free-running circadian
rhythm, (YLL, was 11.3 ? 0.4 h, which did not differ from the value found under
entrainment by LD 12:12 (Wilcoxon test: P>>0.05). Because the free-running
period is always shorter than 24 h, the proportion of the circadian cycle occupied by
a was somewhat larger under constant conditions than in LD 12:12 (48.5% 2 1.8%
as compared with 46.5% k 4.1%). However, the difference was not statistically
significant (Wilcoxon test: P >0.05).
Entrainment and Re-Entrainment
The main entraining signal, by which the endogenous rhythm of Callithrix
jacchus (averaging 23.3 h) is synchronized with the external 24 h day, is the
278 / Erkert
0
10
20
30
40
50
60
70
DAYS
I
9
I
I
15
I
I
21
I
I
3
I
]
9
I
I
15
I
I
21
I
I
I
3
h[CET1
]
Fig. 7. Entrainment of the circadian activity rhythm of a n old female Callzthrix. Originally free-running in LL
a t 280 lux, the circadian activity rhythm is first entrained by LD 12:12 (280:0.2 lux), then re-entrained after a
6 h delay shift of the LD signal, and finally returned to free-running in LL a t 280 lux. The shaded areas mark
the dark phase of the LD 12:12.
alternation between light and darkness-as it is for other animals. The entraining
effect of the LD alternation on the free-running circadian activity rhythm is
illustrated in Figure 7 by activity recordings in an old female. In this experiment,
after changing the constant LL on day 21 to LD 12:12 (240:0.3 lux), it took only
five lengthened transient cycles to bring the circadian rhythm into stable synchrony with the light phase of the LD. On the 40th day of the experiment the LD
was phase-delayed 6 h by extending the duration of darkness. After this abrupt
shift, the activity rhythm of the animal became re-entrained within 6 days. That
this phenomenon is true entrainment in the sense of phase-setting, and not just
light-induced masking, is demonstrated by the timing of the onset of activity when
constant conditions were again imposed. On the first free-running day (LL 240 lux,
beginning on day 62; T = 23.1 h) activity began at nearly the same time as it had
Circadian Activity Rhythm in Marmosets I 279
CALLITHRIX
JACCHUS
[TtA)
0
10
20
30
40
50
60
70
Fig. 8. Re-entrainment of the circadian activity rhythm of a Callithrix pair after an 8 h phase delay (day 19)
and advance shift (day 55) of the synchronizing LD 12:lZ (350:O.Zlux).
under the preceding LD 12:12 conditions, and then gradually drifted further out of
phase. On the other hand, the immediate 2.5 h phase advance of the activity on the
first day of LL indicates that masking is also involved. Under the preceding LD
conditions the activity time would have begun earlier, if it had not been inhibited
by the low dark illuminance.
Re-entrainment after a phase shift of the entraining signal was studied in a
total of 14 marmosets, 12 kept as pairs and 2 singly. In these experiments the
entraining LD 12:12 (280: 0.16 lux) was first phase delayed 8 h by a single
lengthening of the L-phase, and 35 days later a corresponding phase advance (by
an 8 h shortening of the D-phase) restored the original situation. Figure 8 shows
the course of re-entrainment for a pair of marmosets. In this case, after the 8 h
delay shift of the LD the animals’ circadian activity rhythm needed seven
lengthened transient cycles before the onset and end of activity matched their
280 I Erkert
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Fig. 9. Lack of ultradian components in the LD-entrained (above) and free-running (LLs; see Table I) circadian
activity rhythm of a female Callithrixjacchus (n = 30 days in each case). Results of a periodogram analysis (left)
and of a maximum entropy spectrum analysis (right). All the peaks in the periodogram-analysis plot which
exceed the significance limit, P 5 0.01, are fractions of the circadian period and therefore do not indicate
ultradian periodicity.
original phase position to the entraining signal. After the advance shift, 6 (activity
onset) and 9-11 (activity end) transient cycles were required. The average
re-entrainment times of all the marmosets tested were 6.6 0.9 (activity onset)
and 6.8 2 0.7 (activity end) days for the delay shift, and 6.4 2 0.7 (onset) and 8.6
1.3 (end of activity) days for the advance shift of the LD. If the end of activity is
taken as the reference phase (because in these animals end of activity is less
subjected to masking effects than the onset of activity), the marmosets are found to
be re-entrained more slowly after an 8 h advance of the LD 12:12 than after an 8
h delay shift (Wilcoxon test: P >0.05). Whereas there was no difference between
the times needed for re-entrainment of onset and end of activity following a delay
shift, the advance shift produced a statistically significant difference in the rate of
re-entrainment of these two phases of the circadian activity rhythm (Wilcoxon test;
P <0.05). However, the activity records in Figure 8 indicate that this difference is
at least partly an artifact of masking the onset of activity by an activity inhibiting
effect of darkness.
*
*
Lack of Ultradian Components
Additional analyses were carried out to determine whether the circadian
activity rhythm of Callithrix is modulated by a superimposed ultradian rhythm. In
four adult females the activity data obtained from a 30-day free-running segment
(LL 350 lux) and an entrained segment (LD 12:12;350: 0.16 lux) of the same length
were analyzed by an expanded periodogram analysis and by maximum entropy
analysis. In no case was there evidence of an ultradian component (Fig. 9).
Similarly, spectrum analysis of all data from a 210 day free-running experiment
revealed no periodicity other than that of the circadian activity rhythm in any of
the animals. The secondary peaks in the periodogram-analysis plots coincide
exclusively with integral fractions of the calculated circadian period. Hence they
represent computational artifacts of the circadian rhythmicity.
The circadian activity rhythm of Callithrix exhibits no ultradian components.
Circadian Activity Rhythm in Marmosets i 281
But since only the gross locomotor activity was monitored, rather than particular
forms of behavior, the results do not rule out the possibility that certain elements
or sequences of behavior may be repeated with an ultradian periodicity within the
circadian cycle.
DISCUSSION
The currently available data from chronobiological studies on four prosimian
and seven simian species are summarized in Table 11. Nonhuman primates
constitute a relatively homogeneous group with respect to the period length of the
free-running circadian rhythm under constant environmental conditions. Neither
the mean nor the range of variation of the spontaneous period differ characteristically between prosimians and simians, or between the diurnal and the nocturnal
species. With a period spectrum ranging from 22.3 to 26.3 h over all the species, the
intraspecific range of variation of period lies between 0.9 h in Macaca irus
[Hawking & Lobban, 19701 and 2.7 h in Galago senegalensis [Erkert et al., 19841.
The range of spontaneous periods found here for Callithrix, 1.3 h, is close to the
overall average of 1.6 i. 0.5 h for all the primate species studied thus far.
Furthermore, Callithrix is not unique in having the period consistently shorter
than 24 h, as the same appears to be true for the nocturnal Galago garnettii [Erkert
et al., 19841 and the diurnal Macaca nemestrina [Tokura & Aschoff, 19831.
On the basis of the relation between the spontaneous circadian period and the
phase position of the entrained rhythm with respect to the LD signal found for
other vertebrate species [Aschoff & Pohl, 19781, the positive overall phase-angle
difference of the entrained marmoset rhythm in LD 12:12 can be ascribed to its
relatively short period (7 << 24 h) combined with the characteristics of the phase
response curve. As a result of the short endogenous rhythm the marmosets
ordinarily awake before the end of the dark phase of the LD 12:12. This true onset
of activity, i.e., the onset preprogrammed by the circadian timing system, then is
evidently masked by a direct inhibitory effect of the low D illuminance (0.1 lux) on
the motor system. Such masking effects by the direct action of light [Aschoff et al.,
1982; Erkert & Grober, 19861 are particularly clear during re-entrainment of the
circadian activity rhythm following phase shifts of the LD entraining signal.
Whenever part of the daily activity coincides with the dark phase of the delayed or
advanced LD 12:12, the level of activity is drastically reduced as long as the
darkness continues (Figs. 7, 8). Accordingly, the 2-2Y2 h advance of the activity
onset observed immediately after either a sudden advance of the light phase of an
LD or a sudden transition from LD 12:12 to LL can be explained, at least in part,
by the abrupt cessation of the activity-inhibiting action of the low D illuminance
(Fig. 7).
The spontaneous period produced by the circadian timing system in Callithrix
seems neither to be systematically influenced by the light intensity, nor to depend
on the sex of the animal, though an effect of age was observed. The finding that
young marmosets have a somewhat shorter free-running period than the older
animals is inconsistent with the results of Pittendrigh and Daan [19741, who
demonstrated a shortening of T with increasing age in three rodent species. On the
other hand, Haussler [1987] found that in the neotropical bat M. molossus, in
which spontaneous periods shorter than 24 h predominate, individuals over 2 years
old had larger 7 values than did the young animals. It might be that these
contradictory findings in different mammalian species are due in part to aftereffects of prior entrainment in one case or another, and they may indicate an
age-dependence of aftereffects rather than a genuine age-dependence of the
circadian period. Thus the present results demonstrate that generalizations in
*di
=
diurnal; no
=
nocturnal; loc.
di
di
di
Macaca nemestrina
Macaca irus
Pan troglodytes
= gross locomotor
4
4
3
2
1
=
1-85
0150
SD
=
- T
,,,
(h)
22.7-24.0
24.5-26.2
24.3-26.3
23.3-25.8
23.8-24.4
23.8-24.9
22.3-23.8
23.7-24.6
23.7-25.1
24.2-26.2
23.5-25.2
22.8-24.6
22.8-25.5
22.4-23.7
7,in
T
Standard
lux).
Yellin & Hauty 119713
Martinez [1972l
Tokura & Aschoff [1978, 19831
Hawking & Lobban [19701
Farrer & Ternes [1961]
Present paper
Aschoff & Tokura [ 19861
Sulzman e t al. [1979]
Thiemann-Jager [19861
Erkert et al. [1984]
Erkert e t al. [1984]
Erkert e t al. [19841
Erkert e t al. [19841
Authors
2
care temperature; pD = physiological darkness ( 5
23.32 0.3
25.22 0.4
25.02 0.5
24.92 0.6
24.0k 0.3
24.1-r- 0.3
23.12 0.4
24.2
25.12 0.9
24.52 0.6
23.72 0.5
23.8k 0.6
23.1-r- 0.5
T 2
Period length,
feeding; temp.
270
0/0.4-1300
0.003-100
0.1-400
0.1-400
1-600
0.1-360
0.1-240
pD-0.1
pD-0.1
pD-0.1
Range
illumination
intensityhx
activity; feed.
loc.
loc.
feed.
temp
loc.
loc.
loc.
loc.
feed.
14
8
di
di
di
loc.
6
no
loc.
loc.
loc.
loc.
3
5
6
5
n
no/di
no
no
no
diho
Macaca mulatta
Prosimiae
Lemur fulvus
Microcebus murinus
Galago senegalensis
Galago garnettii
Simiae
Aotus lemurinus
griseimembra
Callithrix jacchus
Saimiri sciureus
Parameter
TABLE 11. Summary of the Spontaneous Periods Found Thus Far in Nonhuman Primates (Means T
Deviation and Overall Range of Variation) *
Circadian Activity Rhythm in Marmosets I 283
chronobiology should be based on extensive comparative studies on many species
of diverse systematic groups.
Unexpectedly, in view of the short spontaneous period and the marked positive
phase angle difference between the entrained circadian period and the LD cycle,
the circadian activity rhythm of Callithrix becomes re-entrained more slowly after
an 8 h advance shift of the LD 12:12 than after an 8 h delay shift (Fig. 8). It
appears, therefore, that this “directional effect” [Erkert & Grober, 1986; “asymmetry effect” according to Aschoff, 19781 in re-entrainment after shifting of the
entraining signal is unrelated-or at least has no direct causal relationshipto
the period length. The alternative possibility suggested by Aschoff [1978] and also
considered likely by Schanz and Erkert [19871, is that the magnitude of the
directional effect may be determined primarily by characteristics of the phase
response of the circadian timing system to changes in light intensity.
The variability of the average actograms obtained under identical physical
environmental conditions in the laboratory makes it difficult to decide whether the
basic activity pattern of Callithrix jacchus is primarily unimodal, bimodal, or
multimodal. Since no ultradian periodicity was found, however, a regular multimodal actogram can be excluded. The data in Fig. 2 suggest that in the normal
case, i.e., in animals with complete social contact, bimodal activity patterns
predominate. This assumption is supported by the findings of Saito et al. 119831
that feeding and drinking activity in Callithrix jacchus do have a bimodal time
course as well. Common marmosets are relatively small mammals. Therefore their
body temperature rhythm should be expected to run in parallel to locomotor
activity. The more unimodal temperature pattern described by Hetherington
[1978] seems to be inconsistent with this deduction. However, since Hetherington
measured rectal temperature while handling the marmosets, the basic circadian
pattern could have been masked by handling-induced rises in core temperature.
Actual comparable data can be obtained only by telemetric measurements in
undisturbed animals.
The proportions of time spent in different activities and the diurnal patterns of
these behaviors are generally accepted to be important in primate behavior and
ecology [Harrison, 19851. But in spite of this, field studies in which such data were
established in a systematic manner and over an adequate time span are still
lacking. From field observations lasting only a few days, of a group of Callithrix
jacchus inhabiting a small woodland a t a university campus in Brazil, Maier et al.
[1982] reported the activity pattern to vary considerably from day to day. By
radiotagging single members of two groups of common marmosets inhabiting the
same forest area, Hubrecht [19851proved as well that the pattern of activity levels
differed markedly between groups. These observations made in the natural habitat
coincide quite well with the variability of the activity pattern found in the present
study under controlled laboratory conditions. Maier et al. [1982] also reported that
the animals started locomotor activity about 15-35 min after sunrise and returned
to their sleeping site about 1 h before sunset. From these data, a positive overall
phase-angle difference of the marmoset’s circadian activity rhythm to the entraining natural light dark cycle can be deduced. This is consistent with the results
obtained here in an artificial light-dark cycle and can therefore also be traced back
to the short circadian period underlying the activity rhythm in Callithrix jacchus.
Similar times of onset and end of activity (30-60 min after sunrise and 1-2 h before
sunset, respectively) have also been reported for a wild group of the tassel-ear
marmoset, Callithrix humeralifer, inhabiting an evergreen dryland forest in the
State of Mato Gross0 in Brazil [Rylands, 19861. Proceeding from this observation
284 I Erkert
one should expect the activity rhythm of this marmoset species to be based on an
endogenous circadian rhythm with a period length of less than 24 h as well.
CONCLUSIONS
1. The activity patterns of common marmosets living in artificial light-dark
cycles (LD 12:12) reveal marked intra-individual and interindividual variation. In
animals with full social contact, bimodal patterns predominate.
2. The daily-periodic activity rhythm of the marmosets is controlled by an
endogenous timing system which generates an average circadian spontaneous
period of 23.2 5 0.3 h. The period length of the free-running circadian activity
rhythm does not seem to be influenced systematically by the illumination
intensity or by the sex of the animal, but it does vary slightly with age, and is
dependent on the duration of trial. Due to such aftereffects a steady state of the
spontaneously free-running rhythm is not reached before at least 30-40 days spent
under constant conditions.
3. The light-dark cycle acts as a potent entraining signal which synchronizes
the marmoset’s endogenous rhythm with the environmental 24-h periodicity. The
positive overall phase-angle difference of the entrained activity rhythm with
respect to the LD cycle, as observed under artificial and under natural lighting
conditions, can be attributed to the very short circadian spontaneous period.
4. After sudden 8 h delay shifts of an entraining LD 12:12 the circadian
activity rhythm of Callithrix jacchus resynchronizes more quickly than after 8-h
advance shifts. This directional effect in resynchronization is ascribed t o characteristics of the phase response of the circadian system t o changing light intensities.
5. Neither the free-running nor the entrained circadian activity rhythm of
Callithrix jacchus contains ultradian components.
ACKNOWLEDGMENTS
I am very grateful to Prof. Dr. H.-J. Kuhn and Dr. W. Kaumanns, of the
German Primate Center in Gottingen, as well as to Prof. Dr. C. Vogel and Dr. H.
Rothe, Gottingen, and to Dr. C. Welker, Kassel, for providing me with some of the
marmosets used here. I thank Mrs. Birgit Brodbeck-Vater for carefully tending the
animals, and for much-appreciated technical assistance in carrying out and
evaluating the experiments. Many thanks are also due to Ms. Ursula Schardt and
Ms. Ingrid Wilhelm, who made available to me certain data from their experiments under constant conditions. This work was supported by the Deutsche
Forschungsgemeinschaft (Er 59/10).
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