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Diurnality and nocturnality in
nonhuman primates: comparative
chronobiological studies in laboratory
and nature
Hans G. Erkert
a
a
University of Tuebingen, Institute for Zoology/Animal Physiology,
Auf der Morgenstelle 28, D-72076, Tuebingen, Germany
Available online: 05 Mar 2008
To cite this article: Hans G. Erkert (2008): Diurnality and nocturnality in nonhuman primates:
comparative chronobiological studies in laboratory and nature, Biological Rhythm Research, 39:3,
229-267
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Biological Rhythm Research
Vol. 39, No. 3, June 2008, 229–267
Diurnality and nocturnality in nonhuman primates: comparative
chronobiological studies in laboratory and nature
Hans G. Erkert*
Downloaded by [University of California Davis] at 18:06 10 November 2011
University of Tuebingen, Institute for Zoology/Animal Physiology, Auf der Morgenstelle 28, D-72076,
Tuebingen, Germany
Looking for differences in circadian clock characteristics of diurnal and nocturnal
nonhuman primates, this article summarizes results of chronobiological studies carried
out in various nocturnal, diurnal, and cathemeral prosimian and anthropoid primate
species under controlled laboratory conditions, under seminatural conditions, and in the
wild. In almost all circadian parameters investigated, no differences were discernible
between the two main chrono-ecotypes, either in circadian period length and the
influence upon it of after-effects, of light intensity, and ambient temperature, or in the
PRC, re-entrainment behavior, rhythm splitting, and internal desynchronization.
Diurnal and nocturnal or cathemeral species differed only in the phase of artificial or
natural LDs to which their circadian activity phase was adjusted as well as in the
characteristics of masking activity upon the rhythms produced by the direct inhibiting
or enhancing effects of light. Pronounced lunar periodicity—observed in the activity
rhythm of nocturnal neotropical owl monkeys, genus Aotus, in seminatural and natural
environments as well as in wild cathemeral Malagasy lemurs, genus Eulemur—is shown
to result from masking effects of moonlight. In captive Eulemur fulvus albifrons, a
change from dark-active over cathemeral to light-active behavior, without concurrently
changing the circadian phase-setting of activity to D, was produced by direct masking
effects of a stepwise reduction of darktime luminosity on an LD 12:12 cycle. Long-term
activity recordings carried out in wild diurnal Malagasy sifakas (Propithecus verreauxi)
and cathemeral redfronted lemurs (Eulemur fulvus rufus), as well as in wild nocturnal
owl monkeys (Aotus a. azarai) of the North Argentinean Chaco, yielded in all species
distinct bimodal long- and short-day activity patterns with pronounced peaks during
dusk and dawn. Applying Pittendrigh’s two-oscillator concept to these results, it is
hypothesized that the differences in chrono-ecotype behavior may result from variations
in internal coupling and external phase-setting of morning and evening oscillators (m, e)
to dawn and dusk, interacting with direct masking effects of light.
Keywords: circadian rhythms; activity patterns; photic and nonphotic entrainment;
phase-response; light masking; lunar periodicity; cathemerality; prosimian and
anthropoid primates
Introduction
Extant mammals are generally assumed to have evolved from small arboreal insectivores
with a nocturnal lifestyle. The diurnality found in a large number of mammalian taxa is
*Email: [email protected]
ISSN 0929-1016 print/ISSN 1744-4179 online
Ó 2008 Taylor & Francis
DOI: 10.1080/09291010701683391
http://www.informaworld.com
Downloaded by [University of California Davis] at 18:06 10 November 2011
230
H.G. Erkert
thought to have developed polyphyletically from nocturnal ancestors (Crompton et al.
1978; Starck 1978). This holds also for nonhuman primates (Charles-Dominique 1975;
Fleagle 1988; Martin 1990). Why and how the transition from the nocturnal to a diurnal
lifestyle might have proceeded in the various taxa is still a matter of speculation (Martin
1990; van Schaik & Kappeler 1996; Smale et al. 2003). While evolutionary biology and
behavioral ecology were mainly concerned with the ultimate factors that might have
caused certain members of an order, family, or genus to remain nocturnal or to adopt a
more diurnal lifestyle, chronobiologists have almost exclusively focused on the
phenomenology and functional analysis of the circadian timing system (CTS) involved
in the temporal regulation of the species’ daily activity and resting phases. But
chronobiologists have often ignored the function of this timing system for the animals’
life and survival in nature (DeCoursey 2004; Marques & Waterhouse 2004; Morgan 2004).
Animal models used for the behavioral, physiological, molecular and moleculargenetical approaches followed thus far in the functional analysis of mammalian circadian
clockwork were only a few nocturnal rodent species such as laboratory rats, mice, and
Syrian hamsters. Corresponding comprehensive studies in other nocturnal or even diurnal
mammalian species have been performed to a much lesser extent (Moore-Ede & Sulzman
1977, 1982; Sulzman et al. 1979; Edgar et al. 1993; Hut et al. 1999a, 1999b; Caldelas et al.
2003). Comparative chronobiological studies in nocturnal and diurnal non-rodent
mammalian species, carried out both under strictly controlled laboratory conditions and
in nature, are rare (DeCoursey & DeCoursey 1964; Erkert 1974, 1976a, 1976b; Erkert &
Groeber 1986; Kappeler & Erkert 2003; Fernandez-Duque & Erkert 2006). For this
reason, not many details of the tissue structure, cellular, molecular, and molecular
genetical mechanisms of the principal central nervous circadian pacemaker located in the
hypothalamic suprachiasmatic nuclei (SCN) are known, except in these few nocturnal
rodent models, and this ignorance extends to an understanding of their afferent and
efferent pathways and the mechanisms of photic and, partly, nonphotic entrainment
(Klein et al. 1991; Weaver 1998; King & Takahashi 2000; Shearman et al. 2000; Zordan
et al. 2000; Moore & Leak 2001; Schwartz et al. 2001; Lee et al. 2003; Meijer & Schwartz
2003). Robust ideas on the chronophysiological and chronoecological basis of mammalian
diurnality and its multiple evolution are still lacking. Another gap in our knowledge
concerns the diversity of circadian characteristics and their functional and/or adaptive
meaning in mammals of different systematic groups, ecotypes and chronotypes. To get a
better idea of the diversity developed in the phylogenetically ancient CTS during their
evolutionary transition from an originally nocturnal to a more diurnal lifestyle and/or
while adapting to changed abiotic and biotic time structures of newly conquered ecological
niches, extensive comparative chronobiological studies are required both under strictly
controlled laboratory conditions and in the natural environment.
In a first attempt to characterize the originally assumed fundamental differences in the
response of the CTS in nocturnal (dark-active) and diurnal (light-active) animals to
changes in light intensiy, Aschoff (1964, 1979) formulated his so-called ‘‘circadian rule’’. It
originally stated that, in nocturnal animals, the circadian spontaneous period t is
positively correlated with light intensity, while total activity and the ratio of activity
time:resting time (a:r) are negatively correlated with it. Diurnal animals should behave in
exactly the opposite manner. As to the circadian effects of ambient temperature, nocturnal
species were thought to behave in a ‘‘cold-active’’, and diurnal ones in a ‘‘warm active’’,
manner. However, while the prediction concerning the light effect on t, nowadays often
cited as ‘‘Aschoff’s rule’’ (Muñoz et al. 2005; Daan 2000), could be substantiated in many
nocturnal mammals, most diurnal species did not follow it (Aschoff 1979). Also,
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Biological Rhythm Research
231
generalizations concerning the temperature effect on circadian rhythmicity could not be
validated in the endothermic mammals.
Since those early years of chronobiological research, no fundamental differences
between the characteristics of the CTS in nocturnal and diurnal mammals could be
established, either in the shape and amplitude of the photic phase response curve essential
for the circadian systems’ phase-setting (entrainment) to the environmental 24-h day
(Pittendrigh & Daan 1976; Daan 2000; Kas & Edgar 2000; Refinetti 2004), the
morphological, immuno-histological, electrophysiological, and metabolic characteristics
of the SCN pacemaker, or its afferent and efferent pathways (for review see Smale et al.
2003). For this reason, it has been assumed that the mechanism or ‘‘swich’’ responsible for
the phase-setting of the diurnal mammals’ active phase to the bright part of the day must
be located downstream from the SCN and/or be a result of direct masking effects due to
light, which were also thought to be mediated independent of the SCN (Mrosovsky 2003;
Smale et al. 2003; Redlin & Mrosovsky 2004; Erkert et al. 2006). However, some recent
findings of nocturnal wheel-running in some diurnal African grass rats, Arvicanthus
niloticus, have been interpreted as indicating fundamental differences in the molecular
mechanism of certain SCN cells in diurnal and nocturnal mammals (Lee 2004; Schwartz
et al. 2004). But since this evidence was obtained from a normally diurnal rodent species, a
few animals of which behave dark-active only when having access to a running wheel,
these results need further substantiation by also analyzing strictly diurnal and nocturnal
species, including non-rodents.
As in rodents, several other mammalian orders are found that are not clearly
nocturnal, diurnal or crepuscular. In primates, for instance, with the exception of the
nocturnal South American owl monkey genus Aotus, all haplorrhine or anthropoid species
are strictly diurnal, while most of the strepsirrhine or prosimian species remained
nocturnal. Only a few Malagasy lemurs such as the indris (Indri indri), sifakas
(Propithecus), ringtailed lemurs (Lemur catta), and ruffed lemurs (Varecia) have adopted
a diurnal lifestyle while some Eulemur and Hapalemur species may be active both during
the day and night. This mode of behavioral activity or chronotype, which is also known
from some other mammalian orders such as Carnivores, Artiodactyla, Perissodactyla, and
Xenarthra, has recently been designated as ‘‘cathemerality’’ (Tattersall 1987, 2006; Curtis
& Rasmussen 2006). Which factors may account for this variability in primate chronoecotypes is still in controversial debate among primatologists, though the debate has
largely taken place without considering relevant chronobiological aspects (van Schaik &
Kappeler 1996; Curtis et al. 1999; Donati et al. 2001; Curtis & Rasmussen 2002; Kirk
2006). Due to this chronotype diversity, nonhuman primates may be of special interest for
the analysis of the chronobiological traits that may have caused or allowed the various
prosimian and simian primate species to become diurnal or cathemeral, or to remain
nocturnal. For these reasons, we have carried out extensive comparative chronobiological/
chronoecological studies in some nocturnal, diurnal, and cathemeral prosimians as well as
in diurnal and nocturnal anthropoid primate species, both under strictly controlled
conditions in the laboratory, under semi-natural conditions in outdoor enclosures within
the species’ habitat, and in the wild. Here we will briefly summarize some of the results
obtained in laboratory settings and present findings from activity recordings obtained
under semi-natural conditions and in the wild. To give an adequate overview of current
knowledge on the characteristics of circadian rhythmicity in nonhuman primates, rather
unconventionally, the results of other authors are integrated into the ‘‘results’’ chapter. A
brief description of the methods used seems necessary because some unpublished results
are presented.
232
H.G. Erkert
Methods
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Laboratory studies
In neotropical haplorrhine (anthropoid) primates, chronobiological experiments under
controlled laboratory conditions were conducted in 12 adult, nocturnal North Colombian owl
monkeys, Aotus lemurinus griseimembra (seven males, five females) as well as in 23 males and
26 females of the strictly diurnal common marmoset, Callithrix j. jacchus. Preliminary
experiments were also carried out in two adult females of the Bolivian owl monkey, A. azarai
boliviensis. Strepsirrhine (prosimian) primates studied under laboratory conditions were the
cathemeral, white-fronted lemur, Eulemur fulvus albifrons (three males, two females), the
nocturnal mouse lemur, Microcebus murinus (six males), and the nocturnal African bush baby
species, Galago senegalensis (five males) and Otolemur garnettii (eight males, one female).
Activity recordings and, in some cases, telemetrical core temperature measurements
were carried out at the Institute for Zoology of the University of Tuebingen, Germany, in
sound-protected and light-proof program-controlled air-conditioned rooms. All experiments were conducted according to German law for animal welfare, with permission and
under control of the relevant veterinary authorities.
Locomotor activity was usually recorded by means of transducer-like microphones
fixed on the wire mesh of the recording cages. If activated by the vibrations which the
animals induced in the wire mesh when moving around, these microphones triggered
electrical pulses via an amplifier. These pulses were counted over 5 min intervals and the
sums printed out and stored on disk by a multiplex counter/PC/printer device. In some
Aotus and Eulemur animals, body temperature was simultaneously measured by means of
intraperitoneally implanted miniature transmitters (MiniMitter, TM disc), whose signal
was picked up and transformed by a LRR-27 multichannel receiver connected to a PCbound DATAQUEST III recording system (MiniMitter). For further details see Rappold
and Erkert (1994) and Rauth-Widmann et al. (1996).
Studies under seminatural conditions
Aotus lemurinus griseimembra
The first activity recordings under semi-natural conditions in a primate’s distribution area
were conducted in 1971–1972 in four owl monkey pairs (A. lemurinus griseimembra) kept in a
field-laboratory shed in the Central Colombian East Andes, in a clearing of the ‘‘cafetal’’ of
Finca Rhenania, El Colegio/Cundinamarca (48350 N, 748270 W), about 1000 m above sea
level. Transparent perspex roofs above a large ventilation space on top of the animals’
rooms and a broad ventilation slot at the bottom of their outer wall, both covered with wire
mesh and flyscreen, ensured that the monkeys were optimally exposed to natural day- and
moonlight as well as to local climatic factors. Rooms were equipped with a sleeping box and
several climbing bars that were suspended from steel spring/microswitch devices connected
to event recorders and electromechanic multiplex counters that printed out the numbers of
closed contacts in 30 min intervals. For further details, see Erkert (1974, 1976).
Ateles geoffroyi
Long-term activity records of spider monkeys (Ateles geoffroy) were collected in
cooperation with Drs. J. Muñoz-Delgado (Instituto Mexicano de Psiquiatrı́a, Mexico
D.F.), M. Corsi-Cabrera (Facultad de Psicologı́a de la Universidad Autonónoma de
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Biological Rhythm Research
233
Mexico) and D. Canales-Espinoza (Instituto de Neuroetologı́a de la Universidad
Veracruzana) at this institute’s ‘‘Parque de la Flora y Fauna Silvestre Tropical Pipiapan’’
(Muñoz et al. 2004). This etho-ecological field station is located in Central Mexico, about
12 km east of Catemaco at 188270 N, 958020 W, 330 m above sea level. It is surrounded by
secondary rainforest, has a tropical climate with a rainy season during the northern long-day
summer months, and a dry season, roughly corresponding to the short-day winter months.
Throughout the first recording period, covering a whole annual cycle, the monkeys
were kept in a large wire mesh outdoor enclosure (126663 m [length6width6height]).
For actimetry, seven subjects of a large social group were provided with Actiwatch1 AW4
accelerometer collars (Cambridge Neurotechnology, UK; http://www.camntech.co.uk).
Those collars were fitted on the monkey’s neck while being anesthetized for about 30 min
with 2.5 mg/kg ketamine-hydrochloride administered via blow-pipe darts. In a later
recording period, some spider monkeys wearing AW4 collars were transferred to a small
forest island of about a quarter hectare surrounded by a high electric fence.
Recordings in the wild
Malagasy lemurs
The first long-term activity registrations in wild nonhuman primates were conducted in
cooperation with Prof. P. Kappeler (Department of Sociobiology of the German Primate
Center (DPZ), Goettingen), at this institute’s field station in the Kirindy Forest, Western
Madagascar. From September 1998 to March 2003, records lasting several months were
obtained from a total of four adult cathemeral red-fronted lemurs (Eulemur fulvus rufus;
Lemuridae) and eight adult subjects of the considerably larger and strictly diurnal
Verreaux’s sifaka (Propithecus v. verreauxi, Indridae). The study site was a deciduous dry
forest situated 60 km north of Morondava at 448390 E, 208030 S, about 60 m above sea level.
The local climate is characterized by a hot wet season during the summer in the southern
hemisphere from November to March and a cooler dry season from April to October.
Activity data were also collected with AW4 accelerometer collars fixed on the lemur’s
neck after having been captured via blow pipe darting by an experienced Malagasy
technician. For more details, see Kappeler and Erkert (2003) and Erkert and Kappeler (2004).
North Argentinean owl monkeys
The North Argentinean Chaco is the southernmost distribution area of the neotropical
owl monkey, genus Aotus. In the provinces of Formosa and Chaco, Aotus a. azarai mainly
inhabits the gallery forests of the Rio Paraguay and its tributaries. This Aotus subspecies
had been described as showing considerable amounts of activity during the bright portion
of the day (Arditi 1992; Rotundo et al. 2000; Fernandez-Duque 2003). For this reason, it
has been considered to behave cathemerally, like some lemurs (Tattersall 1987, 2006;
Curtis & Rasmussen 2006; Fernandez-Duque 2003). Since the other Aotus species seem,
instead, to behave strictly nocturnally (Moynihan 1964; Erkert 1974; Wright 1978; Garcia
& Braza 1987), those North Argentinean owl monkeys were of special interest with respect
to the diurnality – nocturnality problem.
Together with Dr. E. Fernandez-Duque (Fundación ECO, Formosa, Argentina and
Department of Anthropology, University of Pennsilvania, USA), we also conducted
quantitative long-term activity recordings in wild Aotus a. azarai owl monkeys of the
Argentinean Chaco. The study site was a small gallery forest of the ‘‘Riacho Pilagá’’
234
H.G. Erkert
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situated about 20 km north of Formosa, Argentina at the Estancia Guaycolec (588110 W,
258580 S), about 60 m above sea level. The climate characteristics of this subtropical open
savanna region, with a mosaic of grasslands and dry and gallery forests, are relatively dry
and cold winter months from May–September, with average night-time temperature
minima falling well below 108C and daytime maxima of 21–258C, while the summer
months from October–February are relatively warm and rainy, with average minimum –
maximum temperatures ranging from about 15–30 to 20–378C. Activity recordings for
several months with Actiwatch AW4 accelerometer collars were performed upon a total of
seven male and three female Aotus a. azarai monkeys. For details on the species’ behavior
and ecology, study site, climate conditions, etc., see Fernandez-Duque (2003) and
Fernandez-Duque and Erkert (2006).
Data processing and evaluation
After each of the activity measurements which lasted up to 200 days, the animals wearing
actiwatch collars were recaptured (by the use of a dart) and their collars were replaced or
removed. Activity data were downloaded from the actiwatches to a PC by means of a
reader interface and the commercial Actiwatch-Sleep1 program of Cambridge Neurotechnology. Thereafter, the data files were transformed into another format and analyzed
by an extended periodogram analysis according to Doerrscheidt and Beck (1978). To
obtain comparable data, the individuals’ activity records in five min bins were averaged
over five month periods, covering the long-day and short-day halves of the year. Resulting
activity patterns were then used to calculate average activity and resting times by bestfitting a square wave pattern to them (cf. Figure 8). Then the various parameters of the
two patterns could be determined (cf. Figures 9A, B) and compared within and/or between
species. For statistical comparisions, ANOVA followed by Scheffé tests, or other
parametric or nonparametric tests or correlation analyses, were applied as appropriate. P
values of 50.05 were considered to indicate significant differences or correlations. If not
indicated otherwise, arithmetic means + SD are given.
Results
Laboratory studies
Circadian period and after-effects
Under constant conditions, all primate species studied showed free-running circadian
activity rhythms (CAR). Average periods (t) shorter and longer than 24 h occurred both
in nocturnal and diurnal, as well as in strepsirrhine and haplorrhine, species (Table 1,
Hoban et al. 1985). Thus no clear relationship seems to occur between primate chronoecotypes or systematic affiliation and circadian period length. Whether or not in nocturnal
prosimians there is a tendency to periods shorter than 24 h, as one might be tempted to
infer from Table 1, requires further studies in other species.
Distinct after-effects on t of preceeding photic entrainment to 24 h were observed in
Callithrix, Aotus and Otolemur but not in Eulemur. Callithrix shortened t from 23.6 h to
23.2 h on average (Erkert 1989). In Aotus, in a first trial t lengthened from 24.4 + 0.1 to
25.3 + 0.7 h (Thiemann-Jaeger 1986), while in a second experiment only a minor
lengthening from 24.3 + 0.3 to 24.45 + 0.4 h resulted from exposure to LL 0.1 lux
(Rappold & Erkert 1994). Otolemur shortened t in a first experiment over 60–80 days,
by 1.2 h on average, while extended recordings carried out later revealed much stronger
no
cat
no
no
Strepsirrhini (Prosimii)
Microcebus murinus
Eulemur fulvus albifr.
Galago senegalensis
Otolemur garnettii
di
di
di
di
di
di
Saimiri sciureus
Ateles geoffroyi
Macaca mulatta
Macaca nemestrina
Macaca irus
Pan troglodytes
5
8
4
9
4
4
4
3
3
2
1
6
10
14
6
8
16
30
5
5
9
n
Loc
Loc/Tb
Loc
Loc
Loc
Feed
Tb
Kþ-exc.
Dri
Loc
Feed/Tb
Dri
Loc
Loc
Loc
Loc
Loc
Loc
Feed
Loc
Loc/Tb
Loc
Loc
Parameter
0.002 – 360
0.2
0.1 – 480
0.1 – 430
50.5
1 – 600
1 – 600
1 – 600
0 – 600
0.1 – 400
1 – 300
0 – 600
107
270
0 – 300
0.003 – 100
0.45 – 450
0 – 50
1 – 85
0 – RR
0.1 – 240
0 – 0.1
0 – 0.1
Luminance
range (lux)
24.2
24.4
25.1 + 0.9
24.4 + 0.4
23.3 + 0.3
23.2 + 0.4
23.3 + 0.4a
25.0 + 0.5a
24.9 + 0.6a
25.1 + 0.3a
24.3 + 0.1
25.2 + 0.4
24.8 + 0.3/.1a,b
24.5 + 0.1
23.9 + 0.1
24.0 + 0.3
24.1 + 0.3
23.1 + 0.4
22.5 + 0.6
25.3 + 0.4
23.6 + 0.6
22.6 + 0.7
Average
t (h)
24.2 – 26.2
23.9 – 25.6
22.7 – 24.0
22.5 – 24.2
–
24.3 – 26.3
23.3 – 25.8
20.5 – 29.5
25.7 + 0.3
24.5 – 26.2
25.2/.3 + 0.2/.1a,b
25.6 + 0.1
23.7 – 24.0
23.8 – 24.4
23.8 – 24.9
22.3 – 23.8
22.6 – 25.0
23.7 – 24.6
23.7 – 25.1
20.7 – 23.3
24.1 – 26.5
23.4 – 24.0
21.1 – 23.9
Variation
of t (h)
þ
(þ)
þ
þ
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
n.i.
(þ)
–
(þ)
þþ
Aftereffects
7/þ
n.t.
(þ)
þ
n.t.
–
–
–
–
–
–
–
n.t.
n.t.
–
–
–
–
–
(þ)
n.t.
n.t.
n.t.
Hoban and Sulzman 1985
Aschoff and Tokura 1986
Fuller and Edgar 1986
Ferraro and Sulzman 1988
Muñoz-D et al. 2005
Yellin and Hauty 1971
Martinez 1972
Tokura and Aschoff 1978
Tokura and Aschoff 1983
Hawking and Lobban 1970
Farrer and Ternes 1969
Thiemann-Jaeger 1986
Rappold and Erkert 1994
Erkert 1989
Wechselberger 1995
Glass et al. 2001
Sulzman et al. 1979
Schilling et al. 1999
Erkert and Cramer 2006
Schanz and Erkert 1986
Erkert et al. 2006
Reference
Act: activity type/chrono-ecotype: di: diurnal; no: nocturnal; cat: cathemeral.
Parameter: Loc: locomotor activity; Tb: body temperature; Feed: Feeding, Dri: drinking; Kþ-exc: renal potassium excretion.
After-effects: þþ, þ, (þ): strong, distinct, evidence of after-effects; 7: no after-effects; n.i.: no information.
Light effect on t: þ, (þ), þ/7: is, seems, is only partly consistent; 7: inconsistent with Aschoff’s rule stating for nocturnal species a lengthening and for diurnal species a
shortening of t with increasing light intensity; n.t.: not tested.
RR: constant dim red light; +S.D. or S.E. a; b) The first average corresponds to t in LL 1 lux, the second one to t in LL 300 lux.
di
Callithrix j. jacchus
Haplorrhini (Anthropoidea)
Aotus lemurinus gris.
no
Act.
Light-effect
on t meets
Aschoff’s
rule
Circadian period t, after-effects, and the effect of light intensity on period length in diurnal and nocturnal primates.
Species
Table 1.
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Biological Rhythm Research
235
236
H.G. Erkert
after-effects of Dt ¼ 2.2 h, lasting up to 180 days (Erkert et al. 2006). In Eulemur, no
systematic period changes depending on the duration of constant conditions could be
discerned. Though not checked specifically, the short activity records obtained under
constant conditions (DD, LL 1071 lux) in Microcebus and Galago (Figure 1) seemed to
indicate the presence of distinct after-effects in these two prosimians as well. In
Microcebus, after-effects might have been responsible for the differences between the
relatively long ts obtained in our short LL experiments and the much shorter periods
found by Schilling et al. (1999) in longer lasting DD and dim red light (RR) experiments.
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Parametric light effects on t (Aschoff’s rules)
Clear luminosity-correlated variations in period length, as predicted by Aschoff’s rule,
were not found either in the diurnal marmosets and squirrel monkeys or the nocturnal owl
monkeys (Table 1). In a first study in Callithrix, the effect of LL-luminosity on t within the
range of 0.08–480 lux was a negative correlation of rs ¼ 70.29, one that just missed
Figure 1. Photic entrainment and masking of free-running circadian activity rhythms in
representatives of three nocturnal prosimian species by 12:12 h LD cycles with different light
intensities during the light and dark portions of the LD, as indicated on the right margin. Shaded
areas mark the light portions of the applied LDs. While all animals’ endogenous rhythm was
synchronized both by the LD 102:0 (51077) lux and 102:1071 lux cycles, the LD 1071:0 lux cycle
failed to entrain the two galagos’ free-running activity rhythm, although it produced pronounced
masking effects. Note that the activity level of the LD-entrained rhythm in all species was higher in
LD 102:1071 lux (bottom) than in the LD 102:0 lux (top) cycles.
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statistical significance (Erkert 1989). However, after reducing the LL-luminosity from 430
to 0.3 lux, Wechselberger (1995) found t to lengthen significantly by 22 + 13 min, and to
shorten by 18 + 14 min after increasing LL luminance several months later from 0.3 to
430 lux. Corresponding to Aschoff’s rule, owl monkeys shortened their spontaneous
period from 26.2 + 0.2 h (in LL 240 lux) to 24.3 + 0.1 h (in LL 0.3 lux) but, in LL 0.002
lux, t lengthened again to 24.6 + 0.1 h (Thiemann-Jaeger 1986). Diurnal squirrel
monkeys (Saimiri sciureus) lengthened t of their drinking and activity rhythm significantly
from about 24.3–24.5 h in DD (0 lux) to 25.6–26 h in LL 600 lux (Hoban & Sulzman 1985;
Aschoff & Tokura 1986; Ferraro & Sulzman 1988). Correspondingly, after reducing LL
luminosity from 330 to 1 lux, the period of this species’ body temperature and feeding
rhythm shortened significantly from 25.2 to 24.8 h (Fuller & Edgar 1986). Slight
lenghthening of t at higher LL intensities (600 vs. 60 and 1 lux) was also found in the freerunning circadian rhythms of the squirrel monkeys’ feeding, rectal temperature, and renal
potassium excretion rhythms (Sulzman et al. 1979). Longer periods at higher LL
luminosities also occurred in chimpanzees (Pan troglodytes; Farrer & Ternes 1969) and
some macaques (Macaca nemestrina, M. irus; Tokura & Aschoff 1978, 1983; Hawking &
Lobban 1970), while, in Macaca mulatta, t did not vary uniformely with LL luminosity
(Martinez 1972). Thus, as it had already been realized by Aschoff (1979) himself, (most)
diurnal primates do not follow his rules (Table 1). So in primates at least their central
prediction concerning the parametric light effect on period length t does apply at most for
the nocturnal species. Since in most other diurnal mammals studied thus far the observed
effects of light intensity on t are also inconsistent with that prediction of Aschoff’s rule,
parametric light effects on t cannot be causally connected with mammalian diurnality or
nocturnality, as has originally been assumed by Aschoff.
Characteristics of photic phase response
The phase response curves (PRCs) established in the nocturnal Aotus lemurinus (RauthWidmann et al. 1991; Rappold & Erkert 1994) and the diurnal Callithrix jacchus
(Wechselberger & Erkert 1994) resembled one another as well as those of nocturnal mouse
lemurs (Schilling et al. 1999) and diurnal squirrel monkeys (Hoban & Sulzman 1985). Just
as in nocturnal and diurnal rodents, in primates also, delay shifts were elicited by light
in the late subjective day/early subjective night while advance shifts resulted from
light pulses given in the late subjective night/early subjective day. In the marmosets’ and
mouse lemurs’ PRCs, the delay section was more pronounced (peaks of about 790
and 7150 min, respectively) than the advance section (peak around þ30 min), whereas
the PRCs of squirrel and owl monkeys with longer t’s had a more pronounced advance
than delay section. Thus, in primates as in other animals, no fundamental differences
between nocturnal and diurnal species seem to occur in their photic phase response
characteristics.
Photic entrainment and masking
Entrainment and re-entrainment. As was expected, in all primate species studied, light –
dark cycles were the most potent environmental time cue or Zeitgeber that stably
synchronized the animals’ circadian system with the 24-h time structure in their
environment. In diurnal species, the Zeitgeber phase-set the activity time to coincide
with the light, and in nocturnal species with the dark, portion of the light – dark cycle
(Figure 1; Hoban & Sulzman 1985; Erkert & Thiemann 1983). With respect to some
Zeitgeber parameters, however, marked species-specific differences seemed to exist, and
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H.G. Erkert
these indicate differences in the circadian systems’ susceptibility to this Zeitgeber. While
12:12 h LD cycles of 0.1 lux (full moon luminosity) to 1074 lux or physiological darkness
(about 1076/1077 lux) set the activity phase of the free-running circadian activity – rest
rhythm (CAR) of owl monkeys and mouse lemurs to the dark time (Figure 1 left, Erkert &
Thiemann 1982), such LDs failed to entrain the endogenous rhythm in the two (also
strictly nocturnal) bush baby species, Galago senegalensis and Otolemur garnettii (Figure 1;
Erkert et al. 2006). Thus even in nocturnal primates/prosimians there are distinct species
differences in the circadian systems’ thresholds for photic entrainment. In Otolemur, this
theshold was established in the range of about 3–30 lux, and it has been hypothesized that
such high thesholds for photic entrainment in nocturnal mammals may be an adaptive
trait preventing the circadian mechanism of photic phase-setting of circadian rhythmicity
from being affected by moonlight (Erkert et al. 2006). Unfortunately, in no other primates
have the thresholds for photic entrainment yet been determined, but this is required in
order to find out whether this circadian parameter might be related to diurnal and
nocturnal behavior.
Besides the variability of t (including its dependence on light intensity) and the PRC,
the range of photic entrainment and the time needed for re-entrainment (tr) after phase
shifts of an entraining Zeitgeber may also be used to estimate the degree of plasticity of a
species’ circadian system. Ranges of photic entrainment have been determined in the
neotropical anthropoids, Callithrix jacchus and Aotus lemurinus, as well as in the
prosimian species, Galago senegalensis, Otolemur garnettii, and Eulemur fulvus. In female
marmosets, Haerter and Erkert (1993) found the range of entrainment for LDs of 345:0.03
lux with corresponding L and D times between 22/23 and 26/27 h. In Aotus lemurinus, for
LDs of 240:0.3 lux, the lower limit of photic entrainment was established at about 20–22 h
and the upper one around 30 h (Thiemann-Jaeger 1986). For LD cycles with only 3 h L of
100 lux and 20–23 h D of 0.2 lux, Rappold and Erkert (1994) determined the range of
entrainment between 23/23.5 and 25.5/26 h (LD 3:20 to LD 3:23). Relatively short
synchronization experiments with LDs of about 100:0.1 lux yielded in Galago senegalensis
a range of entrainment between 22/23 and 26/28 h and, in Otolemur garnettii, of 20/22 to
25/28 h (Erkert 1984). It is still unknown, however, whether or not, at the limits of the
range of photic entrainment of those species studied, forced internal desynchronization
between the activity rhythm and other circadian functions might occur, as has been found
in squirrel monkeys (Moore-Ede et al. 1982).
Both single light pulse photoperiods and various skeleton photoperiods entrained the
free-running CAR to 24 h in diurnal Callithrix and nocturnal Aotus. Phase positions of the
entrained rhythms always corresponded to those expected from a knowledge of the
respective spontaneous periods and PRCs (Rauth-Widmann et al. 1991; Wechselberger
1995).
The time needed for re-entrainment (tr) after sudden phase-shifts of synchronizing LD
cycles may differ depending on species, circadian parameter, direction (advance or delay)
and amount of shift, as well as on the L:D luminance and time relationship, i.e. the
Zeitgeber strength. In Table 2 this is documented for some nocturnal and diurnal primate
species. For instance, after 8-h advances and delays (DF þ/7 8 h) of an LD 12:12 cycle
(56:0.07 lux), nocturnal Galago senegalensis re-entrained on average within about 9.2 and 5
days, respectively, while they took about 7.4 and 5.6 transient cycles to re-adapt to
corresponding shifts of an LD 8:16 cycle. Otolemur garnettii showed an opposite direction
effect in re-entrainment. The subjects required less transient cycles to re-adapt to an 8-h
advance than to compensate for an 8-h delay of the LD 12:12 (Schanz & Erkert 1987). In
A. lemurinus griseimembra, re-entrainment times of 5.3 and 2.7 days were determined after
5
3
no
no
Galago senegalensis
Otolemur garnettii
di
Saimiri sciureus
6
4
4
5
14
12:12 (60:0)
Tb
A, F, D,Tb 12:12 (n.i.)
K, Na, UV 12:12 (n.i.)
Tb
12.3:11.7 (500:0.001)
12:12 (60:0)
12:12 (410:0.2)
LA-end
LA
12:12 (280:0.2)
12:12 (280: 0.2)
12:12 (410:0.2)
12:12 (243:0.3)
8:16 (243:0.3)
3:21 (100:0.2)
12:12 (56:0.07)
8:16 (56:0.07)
12:12 (56:0.07)
12:12 (140:0.1)
12:12 (100:0)
L:D cycle
h (lux)
LA-on
LA-end
LA-on
LA
LA
LA
LA
LA
LA
LA
Parameter
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
Shift
DF (h)
3.8 + 0.7
5.2 + 0.5a
6.6 + 0.9
6.8 + 0.7
5.4 + 1.5
(4.8 + 1.6)
6.8 + 0.8
(6.0 + 1.2)
5.8 + 1.2a
5.3 + 0.6
11.0 + 1.0
10.2 + 1.9
9.2 + 1.6
7.4 + 0.8
6.3 + 1.5
7
8
tr after DF þ
(advance; d)
4.1 + 0.5a
2–6
6 – 12
5.4 + 1.0
2.9 + 0.9a
6.4 + 0.7
8.6 + 1.3
2.7 + 0.6
5.0 + 1.0
7.6 + 1.8
5.0 + 0.7
5.6 + 0.5
10.0 + 1.0
3.7
3.7
tr after
DF 7 (delay; d)
Erkert 1987
Erkert 1987
Erkert 1987
Erkert,
Erkert,
Boulos et al. 1996
Moore-Ede et al. 1977
Wexler and
Moore-Ede 1986
Fischer and Erkert,
unpub.1
Rappold and Erkert
1994
Erkert 1989
Thiemann-Jaeger 1986
Schanz and
unpub.
Schanz and
unpub.
Schanz and
Schanz and
Schanz and
Reference
Act: activity type: di: diurnal; no: nocturnal; cat: cathemeral.
Parameter: LA: locomotor activity; A: motor activity, Tb: body temperature; F: Feeding; D: drinking; K, Na: renal potassium and sodium excretion; UV: urine volume. tr:
aithmetic means + S.D. or S.E.a.
1
tr after one single dose of 50 ml 10% ethanol without and with (in brackets) 250 mg melatonin administered orally (in mealworms) 3 h before lights-off on the first 8-h advanced
LD cycle.
di
Callithrix j. jacchus
5
5
8
5
cat
Eulemur fulvus albifr.
Haplorrhini (Anthropoidea)
Aotus lemurinus gris.
no
6
no
Strepsirrhini (Prosimii)
Microcebus murinus
n
Act.
Species
Table 2. Re-entrainment behaviour of circadian rhythms in diurnal and nocturnal primates. Times needed for re-entrainment (tr) after advance and delay
shifts (DFþ/7) of synchronizing light – dark cycles.
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H.G. Erkert
8-h advance and delay shifts of an LD 12:12 (240:0.3 lux) cycle, respectively, and times of
11 + 1 and 5 + 1 d after corresponding shifts of an LD 8:16 (240:0.3 lux) cycle
(Thiemann-Jaeger 1986). To 8-h advance and delay shifts of an LD 3:21 (100:0.2 lux)
cycle, they adjusted within 10.2 and 7.6 d, respectively (Rappold & Erkert 1994). In
diurnal marmosets, tr for activity onset was slightly different from that of the end of
activity, both after 8-h advance and delay shifts of an LD 12:12 (280:0.2 lux) cycle (Table
2, Erkert 1989).
Different re-entrainment times for the onset (evening) and end (morning) component
of the activity pattern were observed in an Otolemur garnetti. Following a 6-h delay of an
LD 12:12 (450:0.3 lux) cycle, the activity onset component of the CAR re-entrained
orthodromically (by delaying) while the offset component adjusted antidromically, in this
latter case taking as long as about 40 days (Erkert 2006).
In chair-restrained squirrel monkeys, the circadian rhythms of activity, feeding,
drinking, and body temperature were found to re-entrain significantly faster after an 8-h
delay shift of an LD-Zeitgeber than the rhythms of urinary K and Na excretion and urine
volume (Moore-Ede et al. 1977). After 8-h advance and delay shifts of an LD 12:12 (60:0
lux) cycle, the squirrel monkeys’ body temperature (Tb) rhythm was found to re-entrain
within about five and four days, respectively, while the activity rhythm needed about six
and three days (Wexler & Moore-Ede 1986). In both cases, differing tr’s of the recorded
circadian parameters indicated transient internal desynchronization. After 8-h advance
and delay shifts of an LD 12:12 (500:0.001 lux) cycle, with and without interposed twilight,
Boulos et al. (1996) found a significant dependence of tr in the Tb-rhythm of Saimiri on
the direction of the Zeitgeber shift but not on the presence or absence of twilight.
Thus, in all primates tested so far, more or less pronounced direction effects occurred
in the times needed for re-entrainment after advance and delay shifts of LD cycles
(Table 2). Only in part of the species the direction effect was related to the circadian period
(t5/424 h). In the others the phase-response characteristics might have played a more
crucial role for the circadian system’s re-entrainment behavior, which did not differ
between diurnal and nocturnal species (c.f. Table 2).
Masking direct effects of light. In all primate species studied thus far, pronounced direct
inhibitory or enhancing effects of high or low light intensities, respectively, have been
shown that masked free-running and/or entrained circadian functions such as the
activity – rest or body temperature rhythm (Figures 2–4; Aschoff et al. 1982; Gander &
Moore-Ede 1983; Erkert & Groeber 1986; Rappold & Erkert 1994; Erkert et al. 2006). In
diurnal species, the magnitude of the inhibitory (negative) photic masking effects on the
circadianly programmed activity level is usually negatively correlated with light intensity.
Nocturnal primates, however, often show strong negative light masking both at high and
very low luminosities. For instance, in Aotus lemurinus, an optimum function for the
dependence of total daily activity on darktime luminosity (with an LD 12:12 cycle with
about 100 lux in L and stepwise reductions on D-time luminosities) was established
(Figure 5). The luminosity of about 0.1–0.5 lux, at which highest activity level occurred,
corresponded to full moonlight (Erkert 1976b). Due to this strong dependence of the
locomotor activity on darktime luminosity in Aotus, all kinds of activity patterns could be
produced in a predictable manner, simply by providing adequate patterns of darktime
luminosity (Erkert & Groeber 1986). Since the inhibitory effect of short-term reductions of
luminosity during the night seems to depend to a small degree on the circadian phase, it
may be concluded that primates might also show some circadian modulation of their
susceptibility to the inhibitory effects of low light intensities (cf. Mrosovsky 1999).
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Biological Rhythm Research
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Figure 2. Averaged patterns (n ¼ 10 d each) of the free-running circadian body temperature
rhythm in four owl monkeys (Aotus lemurinus griseimembra) kept in LL of 0.1 lux at constant
ambient temperatures of 30 and 208C (upper and lower curves, respectively). Note that the lower Ta
not only led to a generally lower Tb level but, in three animals, also to a distinct ultradian
modulation of the circadian Tb pattern.
Largely in parallel with the light-induced variation of the activity pattern, the owl
monkeys’ core temperature rhythm was also modulated. Though this may largely be
attributed to the inhibitory effects of light on motor activity and muscle tone, additional
masking direct effects of low light intensities on the circadian level of Tb seem to occur
(Erkert & Groeber 1986). Studying the impact of continuous 2:2 h short-term LD cycles of
60:0 lux on the activity and body temperature rhythm of diurnal squirrel monkeys, Gander
and Moore-Ede (1983) came to a similar conclusion. However, since they could
demonstrate that these LD-related short-term modulations in both circadian functions
occurred during the monkeys’ resting time also, though to a lesser extent, the relatively
dim light of 60 lux in this case did not merely have a permissive effect but also exerted an
enhancing direct effect, i.e. positive masking. Analyzing the effect of short-term light –
dark cycles (LD 2:2; 200:0 lux) on circadian functions in Saimiri, Robinson and Fuller
(1999) showed not only that the circadian Tb rhythm but also the patterns of heat
production and heat loss (both of which contribute to a determination of the Tb rhythm)
were negatively masked by darkness.
Figure 1 shows that, in these three nocturnal prosimians also, due to a strong negative
masking effect of very low light intensities, the darktime activity level in the LD 12:12
(100:0.1 lux) cycle is considerably higher (bottom) than in LDs with physiological (total)
darkness in the dark (top). In Galago and Otolemur, the same holds for the free-running
CAR, as shown in an LD 12:12 cycle with phsiological darkness in D and dim light of 0.1
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242
H.G. Erkert
Figure 3. Upper panel: Average activity pattern of Eulemur fulvus albifrons (n ¼ 5) in an LD 12:12
(140:0.1 lux) cycle. Shaded areas indicate the light time. Lower panel: changing activity pattern of an
E. fulvus albifrons pair in an LD 12:12 cycle with 140 lux in L and stepwise reductions in luminosity
during the dark phase, as indicated on the right margin. Note that the lemurs behaved as dark-active
with 0.1 lux and light-active with physiological darkness in the D phase, and that, in the subsequent
constant dim light of 0.1 lux, the rhythm’s activity phase started to free-run from the dark portion of
the preceding LD cycle. For further information, see text. From Erkert HG, Cramer B: Folia
Primatol 2006; 77: 87–103, S. Karger AG, Basel.
lux in L (Figure 1, middle), which, for these species, is well below the threshold for photic
entrainment. The fact that in Otolemur the period of the free-running CAR, despite the
strong masking effects of the LD 12:12 (0.1:0 lux) cycle, does not normally show any
variation, that is, a sign of relative coordination, indicates that masking by light, at least in
this case, is not mediated via the circadian pacemaker in the SCN but at some point
downstream from it (Erkert et al. 2006).
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Figure 4. Left: Spontaneous splitting of the free-running circadian activity rhythm in a male owl
monkey (Aotus lemurinus griseimembra) in LL of 0.1 lux (upper panel) and averaged activity patterns
of the unsplit (middle, t ¼ 24.9 h) and split parts of this rhythm (lower panel, t ¼ 23.7 h). Note the
1808 phase relationship of the two activity peaks in the split rhythm. Right: internally desynchronized and split free-running circadian activity rhythm in another male Aotus living in LL0.1 lux.
Particularly strong direct inhibitory effects of low dark-time luminosities that totally
masked the animals’ CAR occurred in the white-fronted lemur Eulemur fulvus albifrons
(Figure 3; Erkert & Cramer 2006). In nature, the cathemeral E. f. rufus and E. f.
mayottensis are much more active throughout the day than the night (Donati et al. 2001;
Kappeler and Erkert 2003). Under laboratory conditions (LD 12:12 of 145:0.15 lux,
ambient temperature ¼ 238C, 60% relative humidity, food and water ad libitum),
however, E. f. albifrons became dark-active and developed, on average, 81.8 + 5.5% of its
daily total activity during the dark time (Figure 3, top). Reduction of dark-time luminosity
to 0.002 or 0.0002 lux caused the animals to become ‘‘cathemeral’’, in that they now
developed an average of around 40–60% of total daily activity during the light. With 1075
lux or physiological darkness in the dark, the animals became light-active, showing up to
90% of their total daily activity in the light phase. Despite this, on a subsequent LL 0.15
lux regimen, their circadian activity phase started free-running from the previous dark
phase. This indicates that activity had remained in phase with the dark time of the LD
cycle (Figure 3, bottom). Corresponding results were obtained in another trial in which the
dark-time luminosity (of 0.15 lux) of an LD 12:12 cycle was suddenly switched off for two
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H.G. Erkert
Figure 5. Owl monkey activity patterns under semi-natural conditions, in laboratory settings and in
the wild. Left panel: lunar periodicity of nocturnal activity in an Aotus lemurinus griseimembra pair
kept under semi-natural conditions in Central Colombia. Hourly activity counts every other day over
a period of about two months. Second column: lower panel: average activity patterns of another A.
lemurinus pair (n ¼ 13 months) at four phases of the moon (new, waxing, full and waning moon; +1 d
each) and time course of night-time luminosity (curves) measured during corresponding nights during
one lunar cycle (from Erkert 1974). Upper panel: effect of dark-time luminosity of an LD 12:12 cycle
with about 100 lux in L on the total daily activity of two A. lemurinus pairs (from Erkert 1976). Third
column: average activity patterns of A. lemurinus (n ¼ 7) in rectangular LD cycles simulating the
nocturnal lighting conditions at the four phases of the moon, as indicated by the curves on top
(luminosity is indicated by the y-axes at the top right of the diagrams; pd ¼ physiological darkness
assumed below 1076/77 lux). From Erkert and Groeber 1986. Right panel: activity rhythm in a wild
female A. azarai owl monkey of the Argentinean Chaco showing similar lunar periodicity as
A.lemurinus (30 min counts of 100–1000 impulses are plotted). For more details, see text.
weeks and the lemurs thereafter were subjected to LL 0.15 lux for some days (Erkert &
Cramer 2006). In parallel to the light-induced phase reversal of the lemurs’ activity – rest
rhythm, the two peaks of their Tb rhythm were only slightly phase-delayed and advanced,
respectively. When starting to free-run in the subsequent LL 0.15 lux protocol, the two
temperature peaks immediately re-adopted their former phase position.
From these results, it may be concluded that, although the lemurs became cathemeral
or even light-active, their circadian systems’ phase-setting mechanism behaved like that of
a ‘‘nocturnal’’ species. Hence the observed ‘‘cathemeral’’ and ‘‘diurnal’’ behavior in these
lemurs resulted mainly from strong, direct activity-inhibiting effects of low light intensities,
presumably in combination with higher tolerance of and/or a greater activity-enhancing
effect of the higher luminosity during the light phase. That is, it seems to have been the
result of extreme ‘‘light masking’’ (Erkert & Cramer 2006).
Nonphotic entrainment and masking
Ambient temperature (Ta). The daily variations of Ta and relative humidity generally
provide much more imprecise and unpredictable time cues for circadian systems than the
light – dark cycle. Since Ta rhythms, in addition, often have considerably smaller
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245
amplitudes and may vary substantially with the habitat’s latitude, altitude, geographic and
geomorphologic characteristics, as well as with vegetation, they are a priori less suitable to
become reliable Zeitgebers for circadian entrainment in endothermic mammals. In
primates, the effects of constant Tas and temperature cycles (TCs) on the parameters of
circadian rhythmicity have been studied in Macaca nemestrina, Saimiri sciureus, Callithrix
jacchus and Aotus lemurinus (Tokura & Aschoff 1983; Aschoff & Tokura 1986; Erkert
1991; Pálkova et al. 1999).
No significant Ta effects on t were found in owl monkeys (Figure 2) and common
marmosets (tested in the range 20–308C; Erkert 1991; Pálkova et al. 1999) as well as in
squirrel monkeys (range 15–328C; Aschoff & Tokura 1986). In the much larger pigtailed
macaque, however, in LL of 100 and 450 lux, t was significantly longer at 328C than at
178C, while, at lower LL luminosities, no significant temperature effect on t could be
established (Tokura & Aschoff 1983).
Trapezoidal TCs of 20–308C failed to entrain the free-running circadian activity and
Tb rhythms in owl monkeys or to modulate their period length, while, in some
marmosets, it led to entrainment and in others to period changes indicating relative
coordination (Erkert 1991; Pálkova et al. 1999). Squirrel monkeys and pig-tailed
macaques responded similarly to 24 h TCs of 17–328C. Most individuals showed more
or less pronounced relative coordination while a few others were entrained (Aschoff &
Tokura 1986; Tokura & Aschoff 1983). While in TC-entrained marmosets and macaques
the animals’ active phase was set to coincide with the warm fraction of the external
temperature cycle, it coincided with the cold fraction in the TC-entrained squirrel
monkeys. According to the species’ average t (of mainly less or more than 24 h), in
Callithrix and Macaca, the entrained activity time, a, adopted a more positive phase
relationship (advance) to the warm fraction (Pálkova et al. 1999; Tokura & Aschoff
1983) and, in Saimiri, a more negative one (delay) to the cold fraction of the temperature
cycle (Aschoff & Tokura 1986).
Except for Macaca nemestrina, all other primate species studied showed more or less
strong direct masking effects of Ta on locomotor activity. Lower ambient temperature
usually caused higher activity levels, both with constant Ta and with TCs. In Aotus
monkeys, the Tb level also varied with changing Tas, but, despite higher activity at 208C
than at 308C, it was higher at 308C (Figure 2). Though the ts of the activity and Tb
rhythms were not influenced by the applied TC of 20–308C, both circadian functions were
strongly masked by it: activity increased and core temperature decreased as soon as, and
for as long as, the circadian activity phase coincided with the cold fraction of the TC. In
some animals at 208C, the circadian Tb rhythm showed pronounced short-term variations
(Figure 2, left) which were not obseved in the activity rhythm. This observation, and that
showing that ultradian modulations of Tb also occurred during the cold fraction of the
applied TC 20–308C, points to their thermoregulatory origin.
Other environmental factors
Social entrainment by daily periodic contact with conspecifics has been evidenced in the
diurnal common marmoset Callithrix jacchus (Erkert & Schardt 1991). Acoustic social
contact produced entrainment in a few animals, while, in others, both acoustic and visual
social contact merely led to rather weak relative coordination, and full social contact was
required for real entrainment. Thus, daily periodic social cues exert, at best, a very weak
Zeitgeber effect on marmoset/primate circadian systems.
By inducing locomotor activity and/or increased arousal—by presenting 2-h playbacks
of agitated vocalizations of conspecifics in combination with a mirror—Wechselberger
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H.G. Erkert
(1994, 1995) was able to elicit phase responses and to entrain the marmosets’ free-running
CAR in LL of 430 lux. Phase responses and entrainment—by 1-h activity pulses
stimulated by agitation of the cages and intermittent sprinkling with water (while lights
were off)—were also obtained in Callithrix monkeys kept isolated in dim LL of less than
0.1 lux that obviously had strong inhibiting effects on these monkeys’ spontaneous
locomotor activity (Glass et al. 2001). In contrast to the marmosets living in LL 430 lux,
however, in those kept in dim light, induced activity led to phase responses and
entrainment characteristics corresponding to those produced in nocturnal hamsters by
social stimuli and cage agitation (Reebs & Mrosovsky 1989). The discrepancy between the
results obtained in the two settings may be attributed to the fact that in Wechselberger’s
experiment, with high LL luminosity, the phase-shifting light effects may have dominated
those of induced activity and/or arousal.
Evidence for social masking was found in the free-running circadian activity and Tb
rhythm in a pair of the gregarious Eulemur fulvus albifrons when living in LL 0.15 lux,
either in isolation or with different kinds of social contact with each other and/or a
neighboring family group of conspecifics (Erkert & Cramer 2006).
Entraining effects of time-restricted food availability (eating and fasting, EF cycles)
have been tested repeatedly in diurnal squirrel monkeys, with inconsistent results. In
chair-restrained animals, Sulzman et al. (1977, 1978) found that the colonic temperature, drinking and urinary excretion rhytms became synchronized to a 24-h EF cycle
with 3 h of food availability. Aschoff and von Goetz (1986), however, observed that
EF cycles induced in Saimiri, at most, weak relative coordination, while Boulos et al.
(1989) found entrainment to an EF cycle in only one of 10 monkeys, and relative
coordination in one other. In both studies, the EF cycle produced distinct masking
effects. Taken together, EF cycles may exert, at most, a very weak Zeitgeber effect on the
monkeys’ CTS.
Splitting and internal desynchronization
Circadian phenomena pointing to the existence of a two- or multi-oscillator system
underlying circadian rhythmicity, such as rhythm splitting and internal desynchronization,
have been described both in nocturnal and diurnal primates. Splitting occurred in the
activity and Tb rhythm of Aotus lemurinus (cf. Figure 4, Rappold & Erkert 1994) as well as
in the activity rhythm of Otolemur garnettii (Erkert et al. 2006) and Callithrix jacchus
(Schardt et al. 1989; Wechselberger 1995; Palkova et al. 1999). Long-lasting spontaneous
internal desynchronization of the circadian activity and feeding rhythm has been
documented in a male Aotus (Erkert 2000). In another Aotus, internal desynchronization
was observed between two activity components which had periods of 23.75 and 24.75 h
(Figure 4). Spontaneous, forced, and transient internal desynchronization of various
physiological and behavioral parameters occurred in up to about 25% of the diurnal
squirrel monkeys studied by Moore-Ede and Sulzman (1977), Sulzman et al. (1977b) and
Hoban and Sulzman (1985).
Activity rhythms under seminatural conditions
Aotus lemurinus griseimembra
Continuous activity recordings lasting 6–13 months and carried out 1971–1972 in Central
Colombia in four pairs of the North Colombian owl monkey species, Aotus lemurinus
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griseimembra (Karyotype II-IV, 2n ¼ 52–54 chromosomes), clearly proved this species to
behave strictly nocturnally. Its mostly bimodal activity pattern, with peaks during dusk
and dawn, showed pronounced lunar periodic variations (Figure 5). Around the new
moon, the owl monkeys largely limited their locomotor activity to the twilight periods.
With the waxing moon, their nocturnal activity time extended in parallel to the moonlit
fraction of the night until, at the full moon, it finally covered the whole night. With the
waning moon, the animals’ active phase shortened in parallel to the gradual reduction of
the nocturnal moonlight. The largely coincident time course of activity and night-time
luminosity at the four phases of the lunar cycle indicated that this pronounced lunar
variation of the owl monkeys’ activity rhythm was mainly an effect of masking by light
(Figure 5, Erkert 1974). This hypothesis was substantiated by laboratory results showing
in Aotus a darktime luminosity-dependent activity optimum at about 0.1 lux, which
corresponds to the luminance on cloudless nights with a full moon (Figure 5, Erkert
1976b). Furthermore, by simulating the nightly time course of luminosity at the four
phases of the lunar cycle with corresponding rectangular light cycles, similar activity
patterns as observed under semi-natural conditions could be produced (Figure 5, Erkert &
Groeber 1986).
In addition to the variation of the owl monkeys’ activity pattern, significant lunar
variations also occurred in the phase position of the onset (Co) and end (Ce) of activity in
relation to sunset and sunrise, respectively. Around the new moon, the monkeys began
their locomotor activity earliest (average Co ¼ þ43 min) and terminated it latest
(Ce ¼ þ7 min), while, on nights with a full moon, they became active latest (Co ¼ þ13
min) and entered the resting phase earliest (Ce ¼ þ23 min). For further details, see Erkert
(1976a).
Ateles geoffroyi
Quantitative long-term activity recordings carried out in seven Ateles geoffroyi kept under
semi-natural conditions in the Central Mexican tropics clearly showed that this large
neotropical anthropoid behaves strictly diurnally (Figure 6, Muñoz-Delgado et al. 2004).
Throughout the half of the year associated with short daylengths, the spider monkeys
developed, on average, 91 + 1.5% and, throughout the half of the year associated with
long daylengths, 93.5 + 3.5% of their total daily activity during the light phase
(t12 ¼ 71.41, p ¼ 0.18). Almost all animals had bimodal activity patterns with a first
activity peak (in the morning) more than twice the size of the second peak (Figure 6). Peak
activity height remained largely constant throughout the year, averaging 1.41 + 0.62% of
daily total activity/5 min during the short-day months and 1.36 + 0.62%/5 min during
the long-day months. The average trough of the bimodal activity phase amounted to
0.43 + 0.11%/5 min in the short day and 0.34 + 0.08%/5 min during the long day half
of the year (t11 ¼ 1.5, p ¼ 0.16).
Activity time changed with day length and amounted, on average, to 11.6 + 0.4 h
throughout half of the year with short days and 13.4 + 0.7 h during the half with long
days (t12 ¼ 6.2, p 5 0.001). Accordingly, the mean activity:resting time ratio (a:r) was
significantly larger during the summer than the winter months (1.27 + 0.16 vs
0.94 + 0.06; t12 ¼ 75.3, p 5 0.001). Mean peak-to peak intervals (PPI) amounted to
5.63 + 0.92 h during the short days and to 7.61 + 0.52 h during the long days
(t12 ¼ 74.87, p 5 0.001).
After the transition from winter to summer time, and vice versa, gradual advance and
delay shifts, respectively, of about 1-h in the first activity peak were observed. From these
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248
H.G. Erkert
Figure 6. Upper panel: activity rhythm of a female diurnal spider monkey (Ateles geoffroyi) kept in
a small forest island in Cental Mexico (double-plotted original recording over two months; 5-min
bins, each of 5–200 counts). Lower panel: mean activity pattern as averaged over this two-month
record (5-min values expressed as % of average total daily activity) and activity time calculated by a
best-fitting rectangular pattern (dotted).
observations, it has been deduced that the relatively late occurrence of the morning
activity peak mainly resulted from the late feeding times which reflected this artificial 1-h
shift in the animals’ environment (Muñoz-Delgado et al. 2004). Individual ratios between
the trough values of a and r, which in species with bimodal activity patterns may be used
as an additional indicator for the degree of diurnality, varied from 11–30 in the short-day
fraction of the year and from 10–39 throughout the long-day fraction (average 18.5 + 6.3
vs. 22.4 + 12.9, p 4 0.05).
The transfer of some animals from the wire-mesh enclosure to a small forest island
enclosure resulted in a slight extension of their activity time, a, and a more pronounced
evening activity peak (Figure 6). From this result, an even more pronounced bimodality of
activity, in combination with an earlier morning activity peak, would be expected to occur
in wild Ateles.
Biological Rhythm Research
249
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Long-term activity recordings in the wild
As a further example of the efficiency of comparatively long-term activity recordings with
an actiwatch in wild diurnal and nocturnal primates, Figure 7 shows (double plotted) 150day records in one Malagasy Verreaux’s sifaka and red-fronted lemur as well as in an
Aotus a. azarai owl monkey of the North Argentinean Chaco. These original data, and
the mean activity patterns, obtained by averaging over the whole registration period
(Figure 8), provide evidence that the three species represent different chrono-ecotypes.
A common trait in their activity patterns is a distinct bimodal time course with very
pronounced peaks during dawn/early morning and late afternoon/dusk.
Propithecus undoubtedly behaved strictly diurnally. Throughout the short-day period,
the sifakas exhibited, on average, 85.4 + 2.5% of their total daily activity within the light
portion of the day and, throughout the long-day period, 91.5 + 1.4%. The average a
amounted to 11.1 + 0.7 h during the short-day months and to 14.8 + 0.4 h during the
long day months (t11 ¼ 711.72, p 5 0.001). Correspondingly, the average a:r-ratio
differed significantly between the two halfs of the year (t11 ¼ 712.73, p 5 0.001; cf.
Figure 10). Statistically significant differences between the two half-year periods occurred
also in the amplitudes of the morning and evening activity peaks, the trough between
them, and in the time of the evening peak, but not in that of the morning peak or the time
of the trough (Figures 9A, B). Analyzing the monthly averages of those parameters for
annual variations by ANOVA yielded consonant results (cf. Erkert & Kappeler 2004, p.
180, Table 3).
Eulemur fulvus rufus also showed most of its total daily activity during the light portion
of the natural light – dark cycle. During the short-day period, the lemurs developed, on
Table 3. Comparision of average activity pattern parameters between the wild Malagasy lemur
species Propithecus v. verreauxi (P; diurnal) and Eulemur f. fulvus (E; cathemeral) and the North
Argentinean owl monkey Aotus a. azarai (A; nocturnal) by post-hoc ANOVA and Scheffé tests.
Short-day period
Parameter
F14
A/a
a/50
a/r
a:r
a-a/50
a-r/50
a-a:A/50
a-r:A/50
a-a:a-r/50
p1-a
p2-a
tr-a
tr-r
pt1-a
pt2-a
trt-a
Trt-r
0.45
0.46
55.08
30.37
1.41
9.78
122.28
16.37
66.86
6.70
1.89
58.31
4.06
370.86
653.82
52.91
16.65
p - sign.
0.654
0.644
50.001
50.001
0.282
0.003
50.001
50.001
50.001
0.011
0.193
50.001
0.045
50.001
50.001
50.001
50.001
7
7
þþþ
þþþ
7
þþ
þþþ
þþþ
þþþ
þ
7
þþþ
þ
þþþ
þþþ
þþþ
þþþ
Scheffé-Test
sign.
P-E; P-A; E-A
P-A; E-A
P-E; E-A
P-E; P-A
P-E; P-A; E-A
P-E; P-A
E-A
P-E; P-A
P-A
P-A; E-A
P-E; P-A; E-A
P-A; E-A
P-A; E-A
Long-day period
F16
p - sign.
6.29
11.27
3.33
3.51
9.86
27.51
39.28
35.90
40.94
30.65
15.86
4.92
6.85
597.52
1253.79
546.85
57.59
0.012 þ
0.001 þþþ
0.066 (7)
0.058 (7)
0.002 þþ
50.001 þþþ
50.001 þþþ
50.001 þþþ
50.001 þþþ
50.001 þþþ
50.001 þþþ
0.024 þ
p.008 þþ
50.001 þþþ
50.001 þþþ
50.001 þþþ
50.001 þþþ
Scheffé-Test
sign.
E-A
P-A; E-A
P-A; E-A
P-E; E-A
P-E; P-A
P-E; P-A; E-A
P-E; P-A
P-A; E-A
P-A; E-A
E-A
E-A
P-E; P-A; E-A
P-E; P-A; E-A
P-A; E-A
P-E; P-A; E-A
For parameter abbreviations see legend to Figure 9B; p: probability of error; sign.: significance: 7, (7), þ, þþ,
þþþ: not, just not, just, highly, very highly significant.
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250
H.G. Erkert
Figure 7. Double-ploted, original long-term activity records from one wild Verreaux’s sifaka
(Propithecus v. verreauxi), one red-fronted lemur (Eulemur fulvus rufus) and one Argentinean owl
monkey (Aotus a. azarai). Records obtained by Actiwatch1 actimetry (5-min counts) throughout a
five month period during the long-day half of the Austral year. Note the pronounced bimodal
pattern in all species, that Propithecus and Eulemur behave mainly diurnally while Aotus shows most
activity during the night, and that, in both Eulemur and Aotus, a distinct lunar periodic component
occurs with lowest activity during the nights of the new moon (indicated by closed circles at the right
margin) and highest activity around the time of the full moon.
average, 69.4 + 5.3% and, during the long-day period, 80.2 + 4.1% of their total daily
activity during a (t7 ¼ 73.47, p ¼ 0.001). Statistically significant differences between the
two halves of the year were also present in daily total activity, the activity and resting
times, the a:t-ratio, the amplitude and time of the evening activity peak, the trough
between the two activity peaks, and in the activity level throughout a (cf. Figures 9A, B).
Because the lemurs also developed considerable amounts of locomotor activity during
the brighter moonlit parts of the night (Figure 5 right, Figure 7), the ratio between their
activity level (% of daily total activity/h) throughout the day/twilight span from 05:00 to
20:00 and the dark night hours from 20:00 to 05:00 varied with a lunar periodicity. Over
the course of a year, this ratio amouted to 2.72 on nights with a new moon and to only
1.46 on nights with a full moon (long-day months: 3.32:1.73; short-day months: 2.19:1.21;
Kappeler & Erkert 2003). Such relationships between the activity levels during day and
night may justify the classification of Eulemur fulvus as a cathemeral species.
Aotus azarai monkeys of the North Argentinean Chaco were noticeably more active
throughout the night than the day, but their nocturnal activity usually showed a much
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Biological Rhythm Research
251
Figure 8. Bimodal, long-day activity patterns in Propithecus verreauxi, Eulemur fulvus, and Aotus
azarai, obtained by averaging the 5-min activity records shown in Figure 8. Ordinate values are given
as % of average total daily activity. Dotted rectangles indicate calculated average activity and resting
times (a, r). Note the generally low night-time activity level in the clearly diurnal Propithecus and the
relatively high night-time activity of Eulemur, the peak of which surpasses the daytime trough at
noon. That the Aotus’ morning activity bout extends far into the morning hours is due mainly to a
compensatory lengthening of a around the time of the new moon (cf. Figure 7). Since Argentinean
official time is one hour phase-advanced in relation to local time, the owl monkey activity pattern
must be correspondingly advanced in order to become directly comparable with the other two
patterns. It then becomes clearer that all three patterns might have been derived originally from more
crepuscular patterns.
more pronounced lunar periodicity than that observed in the red-fronted lemurs (Figure 7,
Fernandez-Duque & Erkert 2006). Throughout the short-day period, the Aotus developed,
on average, 83.6 + 7.2% and, during the long-day period, 86.3 + 2.7% of the total daily
activity within the activity time (t8 ¼ 70.77, p ¼ 0.46), which, around the new moon,
usually extended into the late morning hours. Average relationships between the activity
levels during a and r were 40.6 + 9.9:15.9 + 4.5 and 37.6 + 9.5:0.1 + 2.3 counts/5 min
during the short- and long-day halves of the year, respectively (Figure 9A). Significant
differences between the parameters of the average activity patterns from the two halves of
the year were found only in the amplitude of the evening peak, the trough between the two
activity peaks, and in the times of peaks (Figures 9A, B).
From Figure 9(A, B), which compares relevant parameters of the three species’
bimodal activity patterns during the short-day and long-day period of the year, it can also
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252
H.G. Erkert
Figure 9A.
be seen that, between the two halves of the year in the owl monkeys, some of the
parameters, such as total activity/day, a, r, and a:t, and activity levels during activity and
resting time (a-a and a-r/5min), varied in opposite directions to those values seen in the
two Malagasy lemurid species. These results also suggest the characteristics of the owl
monkeys’ CAR more in keeping with a nocturnal response. On the other hand, the highest
activity levels during the resting time and the lowest quotients between the activity levels
during a and r indicate that Eulemur actually exhibited the most cathemeral behavior of
the three species when studied quantitatively in the wild.
Table 3 summarizes the results of statistical comparisions (using ANOVA followed by
Scheffé tests) of the individual parameters of the averaged activity patterns in the three
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253
Figure 9B. Comparison of various parameters of the bimodal short day (sd) and long day (ld) activity
patterns in wild Malagasy lemurids (Propithecus v. verreauxi:P.v., n ¼ 6/7; Eulemur fulvus rufus:E.f.,
n ¼ 4/5) and North Argentinean Aotus a. azarai owl monkeys (A.a., n ¼ 5). Arithmetic means + SE.
Panel A: A/d: total activity/day (kc ¼ kilo [1000] counts); a-a: percentage of daily total activity
occurring during calculated activity times; alpha (a): calculated activity time; rho (r): calculated resting
time; a-a/50 :average activity level during a (counts/5 min); a-r: average activity level during r (counts/
5 min); a-a:A/50 : activity level during a related to the overall mean of activity/5 min; a-r:A/50 : resting
time activity level related to the 5-min overall activity level. Panel B: a:r:activity time:resting time
quotient; a-a:a-r/50 : relationship between the activity levels during a and r; p1-a, p2-a: height of the first
and second activity peaks (as % of average total activity/day); tr-a, tr-r: height of activity minimum
(trough) during activity and resting time; pt1-a, pt2-a: time of first and second activity peak of the
bimodal activity patterns; trt-a, trt-r: daytimes of lowest activity levels during activity and resting time.
Note that peak numbering refers to the diurnal and nocturnal activity pattern rather than to morning
and evening.
254
H.G. Erkert
species for the short-day and long-day period. In almost all cases there were significant
species differences. For both the short- and long-day halves of the year, the differences
were least between Propithecus and Eulemur (n ¼ 7); on the other hand, during the shortday periods, the largest differences were found between Eulemur and Aotus (n ¼ 13) and,
during the long-day periods, between Propithecus and Aotus (n ¼ 11 parameters).
Discussion
Laboratory studies
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Functional characteristics of primate circadian systems as compared to those of rodents
Primate circadian systems do not differ fundamentally from those of rodents. From lesion
experiments carried out in rhesus and squirrel monkeys, the hypothalamic suprachiasmatic nuclei (SCN) have also been identified as the main central nervous pacemaker
(Reppert et al. 1981; Fuller et al. 1981; Moore-Ede et al. 1982; Albers et al. 1982, 1984a,
1984b; Edgar et al. 1993). The location and appearance of the monkeys’ SCN (Macaca,
Saimiri, Callithrix), as well as the neurotransmitters present, largely resemble those of
nocturnal rodents. Retinal afferents from the retino-hypothalamic tract (RHT) also
terminate in the ventral part of the SCN but, other than in rodents, most RHT fibers stem
from the ipsilateral retina. Furthermore, the monkeys’ intergeniculate leaflet (IGL), which
also receives retinal input and projects back to the SCN via geniculo-hypothalamic tract
(GHT) fibers, is described as being a much larger component of the geniculate complex
than in rodents, and the efferent projections of the SCN seem more widely distributed
(Lydic et al. 1981; Reppert et al. 1987; Murakami & Fuller 1990; Moore 1993; Costa et al.
1998). Since comparative immuno-histological studies in other primate species, especially
in nocturnal prosimians, are still lacking, it is not yet clear whether or not these differences
are specific to primates in general and may be of functional significance for the CTS.
Rhythmic clock gene expression (Bmal1, Cry, Per1), documented in the adrenal gland of
Macaca mulatta, indicates that non-human primates have a similar set of clock genes as do
rodents and that the adrenal gland may possess an intrinsic circadian clock (Lemos et al.
2006).
Taken together, the response characteristics of primate circadian systems, such as
period variability, shape and amplitude of PRCs, re-entrainment behavior after phase
shifts of LD-Zeitgebers, and ranges of entrainment, do not differ substantially from those
described in rodents. The exception to this general statement might be the large deviation
of the circadian period from 24 h that is found in the nocturnal prosimians Microcebus
murinus (Schilling et al. 1999) and Otolemur garnettii (Erkert et al. 2006). Compared with
the large species-specific variation in the plasticity of the CTS response characteristics
established in nocturnal chiroptera (cf. Erkert 1982), we may state that non-human
primates generally possess a well-developed and relatively precise circadian system of
medium plasticity.
Circadian response characteristics in diurnal and nocturnal species
Comparisions of the response characteristics of the various circadian parameters in
prosimian and simian, as well as in diurnal and nocturnal, species reveal no fundamental
differences, either between the two primate suborders or the two chrono-ecotypes. Both
groups comprise species/subspecies with periods longer and shorter than 24 h, though all
three nocturnal prosimians studied had relatively short spontaneous periods. As in most
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other diurnal mammals, parametric light effects on t in anthropoid primates do not follow
‘‘Aschoff’s rule’’, except in Callithrix (Aschoff 1964, 1979; Wechselberger 1995). Being
valid only for (most) nocturnal mammals (Aschoff 1979), this rule has not achieved the
discriminatory power originally hoped for. Therefore, the parametric light effects on t are
as unsuitable as the PRC for evaluating if a given species’ CTS shows genuine diurnal or
nocturnal response characteristics; the best method for this still remains to carry out
photic entrainment/re-entrainment experiments (cf. Refinetti 2006). These strictures also
apply to the rather weak and unpredictable (often even lacking) parametric and entraining
effects of Ta and TCs on the CTS of diurnal and nocturnal species.
In non-human primates, diurnal or nocturnal behavior, i.e. photic phase-setting of the
active phase to the bright or dark portion of the day, can be explained by the PRC no
more satisfactorily than in rodents (cf. Smale et al. 2003; Refinetti 2004). Between primate
and rodent representatives of those two chrono-ecotypes studied so far, no real substantial
differences seem to exist with respect to shape and amplitude of the photic PRC. It is also
difficult to imagine that the small differences between the PRCs of nocturnal and diurnal
mammals, found by Daan (2000) when comparing averaged curves of a number of diurnal
and nocturnal mammalian species (mostly rodents), might account for the opposite phasesetting in diurnal and nocturnal species of the active phase of the endogenous rhythms to
day or night. Whether additional photic period responses may produce such phase
differences seems just as doubtful. Furthermore, no obvious differences between diurnal
and nocturnal primates are discernible thus far concerning the species-specific variations
of circadian paramaters that are indicative of the CTS’ degree of plasticity and
adaptability—such as period variability, range of photic entrainment, or re-entrainment
time. Whether or not there are characteristic differences between the thresholds for photic
entrainment in diurnal and nocturnal primates remains to be tested. From the relatively
large threshold differences found in nocturnal primates (50.1 lux in Microcebus and Aotus
as compared to 43–30 lux in Otolemur), it is impossible to give a firm estimate for the
thresholds to be expected in diurnal primate species.
Masking direct effects of light
Masking of circadian rhythms by direct activity-inhibiting and activity-enhancing/
disinhibitory effects of high or low environmental luminosity seems to be much more
pronounced in primates than in most other mammalian species (cf. Figures 1, 3, 5, 7). This
result might, at least partly, be related to the fact that primates in general are more visually
oriented than most other mammals. Most of them live and move (climb/jump) in a threedimensional world, in which effective visual long-distance detection of suitable food (such
as ripe fruits, blossoms or young leaves), of potential social partners or competitors, and
of dangerous aereal or terrestrial/arboreal predators may be an essential prerequisite for
survival and thus of selection benefit. Impaired vision at reduced ambient luminosity
might therefore, a priori, be expected to also have negative, i.e. inhibitory, consequences
on these animals’ locomotion and muscle activity or tone, and, in turn, also upon heat
production and the body temperature rhythm. But the fact that both diurnal and
nocturnal prosimian and simian primates are equally affected by low luminances in their
familiar cages indicates that a more basic mechanism is also involved in the strong
masking effects of light in primates.
While inhibitory masking effects of light in diurnal primates are usually negatively
correlated with ambient luminosity and increase with decreasing light intensity, in
nocturnal species they often obey an optimum (‘‘inverted U’’) function (Figure 5).
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H.G. Erkert
Luminances above and below a certain value, which may correspond to full moonlight at
about 0.1–0.5 lux, as in Aotus, or be below that, as in Galago, Otolemur, or Microcebus,
produce increasing inhibition of behavioral activities. Comparable functions in masking
effects of ambient luminosity, though with maxima at different luminance levels, are also
known to exist in some nocturnal rodents, a few bat species, and owls (Erkert 1982;
Aschoff 1988; Mrosovsky 1994, 1999). However, speaking here of ‘‘paradoxical positive or
negative masking’’, as proposed by Mrosovsky (1999), seems inappropriate. None of these
terms has been unequivocally defined. Instead, they refer to comparisions between quite
variable stages of activity that inhibit or enhance/disinhibit effects of given ambient
factors—such as luminance or temperature—on the circadianly pre-set activity level of an
animal or species. For instance, Aotus monkeys usually show maximal spontaneous
locomotor activity in the dark with luminosities of about 0.1–0.5 lux that correspond to
full moonlight (Figure 5). Both rising and lowering luminosity in the dark cause increasing
inhibition of activity, i.e. ‘‘negative masking’’ according to some authors (Aschoff et al.
1982; Aschoff 1988; Mrosovsky 1994, 1999). In the case of entrainment by an LD 12:12
cycle of about 100:0.0001 lux, for instance, interposed dim light of 0.001 or 0.01 lux during
the dark phase would immediately induce increased activity. According to Mrosovsky’s
(1999) specified masking terminology, in both cases, the direct activity-enhancing or, more
probably, disinhibiting effects of light would have to be called ‘‘paradoxical positive
masking’’. In an LD cycle with 0.1 lux in D, however, the pronounced immediate drop of
activity caused by temporarily lowering the D-time luminosity to 0.01 or 0.001 lux would
have to be called ‘‘paradoxical negative masking’’. Thus, depending on the starting
conditions, identical luminance levels in one case would produce ‘‘paradoxical positive’’
and in the other ‘‘paradoxical negative’’ masking. This is unsatisfactory and quite
confusing. Such terminology appears inadequate and should not be adopted, not even in
chronobiology with its ‘‘clock-centered’’ approach. Aschoff et al. (1982) introduced the
term ‘‘masking’’ for all non-circadianly mediated direct (acute) effects of physical and
biotic environmental factors on circadianly (co-)regulated behavioral and physiological
functions. However, many or even most of such direct effects of environmental factors on
physiology and behavior, i.e. on the various effector systems, though not mediated by the
body clock, do in fact represent a further (probably even primary) regulatory mechanism.
This mechanism may be as important as the CTS for an organism’s optimal time-niche
occupation and adaptation to the manifold challenges of its physically and biotically timestructured environment. We should not ignore its role in most of life’s timing processes in
diurnal and nocturnal mammals by considering it merely as ‘‘masking’’ of circadian
rhythms, i.e. as some kind of white noise, which has to be removed or minimized
(‘‘purified’’, Minors et al. 1966) before a chosen marker rhythm may be chronobiologically
studied adequately. That’s why we, like Rensing (1989), who also asked ‘‘Is masking an
appropriate term?’’, generally prefer to speak of ‘‘direct effects’’, of ‘‘rhythm-masking
direct effects’’ or, probably the best, of circadian and non-circadian effects of light,
ambient temperature, etc. (Haeussler & Erkert 1978; Erkert & Groeber 1986). For
ecologists, behaviorists, sensory physiologists and non-chronobiologic neuroscientists
who, for many decades, have been familiar with this phenomenon, a less clock-centered
but more generally applicable term would be more intelligible.
Activity rhythms under seminatural conditions and in the wild
During the past two decades, numerous field studies have been carried out on behavioral
ecology and sociobiology in diurnal and nocturnal mammals, including primates. Many of
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those studies, besides analyzing the species’ time budgets, also dealt in detail with the
timing and daily patterns of their various behavioral activities. Findings of such studies on
Malagasy Eulemur and Hapalemur species led to the differentiation of a further activity
type in addition to the generally distinguished chrono-ecotypes of diurnal, nocturnal,
crepuscular, and non-circadian (arrhythmic or ultradian) species: the ‘‘cathemeral’’
animals (Tattersall 1987, 2006; Colquhoun 1998; Curtis & Rasmussen 2002, 2006; Curtis
et al. 1999; van Schaik & Kappeler 1996; Donati et al. 2001; Donati & Borgognini-Tarli
2006; Fernandez-Duque 2003). These animals are neither arrythmic nor do they show a
regular ultradian periodicity, but they develop a clear diel rhythm (Halle 2006) regulated
by a strong CTS (Erkert & Cramer 2006). The cathemeral species differ from diurnal,
nocturnal, and crepuscular species in that they do not restrict daily activity to the bright or
dark portion of the day but extend it, in addition to the twilight periods in which usually
pronounced peaks occur, variably into large amounts of the day and night hours (Figures
7–9). Chronobiologists may tend to assign this activity pattern observed in nature to the
crepuscular chronotype rather than to any other, or to create a new category of activity.
However, its introduction in primatology has been of great heuristic value in that it has
stimulated further field work on related species as well as an intense discussion on
nocturnality and diurnality and their evolution in non-human primates (for review see
Curtis & Rasmussen 2006).
Nevertheless, due to methodological restrictions, many of these observational field
studies were of only limited value to chronobiology. For reasons of practicality, it is
impossible to conduct in nature the uninterrupted long-term behavioral observations that
are required to produce chronobiologically relevant datasets. Even so, the use of
actiwatches has proved to be a suitable tool for obtaining such long-term activity
recordings in wild, medium-sized and larger mammals (Erkert 2003). It is advisable,
however, to carry out these recordings in collaboration with experienced field workers of
behavioral ecology (cf. Kappeler & Erkert 2003; Fernandez-Duque & Erkert 2006), who
have access to suitable study sites and animal groups and know their species’ behavior and
ecology in detail. Such field workers are usually not fully familiar with the data-collection
and data-evaluation methods of chronobiology, nor with its relevant theories, specific
approaches and results.
The comparative studies carried out in captive diurnal and nocturnal primates under
controlled laboratory conditions and in semi-natural environments, as well as in wildliving subjects in their natural habitat, show that all three approaches yield essential results
that complement and explain each other and contribute to a better understanding of
behavioural, ecological, and evolutionary aspects of biological timing processes in nature,
including underlying mechanisms. From the good correspondence between the results
obtained in Aotus lemurinus kept under seminatural conditions and those obtained from
the wild A. azarai of the Argentinean Chaco (cf. Figure 5, left and right panels), it may be
inferred that recordings made under semi-natural conditions can also provide reliable data
on a species’ CAR in nature and its response to changing physical and biotic
environmental factors. Furthermore these environments offer the opportunity for simple
experimentation, such as to check the role of food abundance, quality or dispersal on
activity patterns as well as influences from other environmental factors.
Aotus
The most prominent feature of the owl monkeys’ activity rhythm is its pronounced lunar
periodicity, found in A. lemurinus under semi-natural lighting and climate conditions as
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258
H.G. Erkert
well as in the wild A. azarai of the Argentinean Chaco (Erkert 1974, 1976; FernandezDuque 2003; Fernandez-Duque & Erkert 2006). Since indications of lunar periodicity in
behavioral activities have also been observed in other Aotus (sub)species (Wright 1978,
1989), the strong dependence of the owl monkeys’ nocturnal activity on moonlight may be
considered a genus-specific characteristic. Thus it seems justified to assume, further, that
the laboratory finding that the pronounced activity inhibiting direct effect of low light
intensities (50.1 lux) on the activity level of A. lemurinus, which is thought to be mainly
responsible for the lunar variation of these monkeys’ activity rhythm (Figure 5, Erkert
1974; Erkert & Groeber 1986), would apply to the whole genus.
Despite the pronounced lunar periodicity under natural lighting conditions, in
laboratory studies no evidence of an endogenous lunadian or lunar, i.e. circalunadian or
circalunar component, has been found. At most, the apparently internally desynchronized
and split free-running CAR of the male A. lemurinus, shown in Figure 4 (right panel), may
intuitively be interpreted to indicate that an approximately lunadian component of 24.75 h
(the lunar period is 24.8 h) might have been superimposed upon a main circadian
component of 23.75 h. However, since no other clues were found pointing to a
circalunadian or circalunar component in the owl monkeys’ activity rhythm—either in
the free-running CAR in LL or in rhythms entrained by single light pulse, skeleton, or
complete photoperiods—this still isolated result should not be over-interpreted. A circasemilunar rhythm of peak total daily activity, with an average period of 14.0 + 2.3 d,
shown to be present in the activity rhythms of five adult Aotus females while free-running
in LL 0.1 lux or entrained by skeleton photoperiods, has been interpreted as an effect of
oestrous (Rauth-Widmann et al. 1996) because its period corresponded approximately to
the species’ endocrinologically-determined ovarian cycle length of 15.5 + 0.6 d (Bonney
et al. 1980).
Recent neurobiological studies have shown that, in cases of behavioral rhythm
splitting, either the left and right SCN or ‘‘core-like’’ and ‘‘shell-like’’ neuron populations
of the SCN may oscillate circadianly and in antiphase to one another (de la Iglesia et al.
2000; Yan et al. 2005). These antiphase rhythms have been associated with the morning
(m) and evening (e) oscillators (Jagota et al. 2000; Daan et al. 2001; Yan et al. 2005),
hypothesized long ago to underlie bimodal circadian activity patterns, rhythm splitting
under constant conditions, and photoperiodic time measurement (Pittendrigh & Daan
1976). Taking this into account, from the pure phenomenology of the owl monkeys’ lunarmodulated activity rhythm under natural conditions, one might be tempted to speculate
that this conspicious phenomenon might also probably (co-)result from separate,
decoupled oscillators of the bilaterally organized circadian pacemaker system in the
SCN, these oscillators being differentially entrained by sunlight and moonlight. Such an
assumption would also explain both the desynchonized split activity rhythm shown in
Figure 4 (right panel) and the temporary extension of activity into the later morning hours
around the new moon (cf. Figures 5, right, and 7, lower panel). However, the experimental
results render this quite improbable (Erkert & Groeber 1986); the most reasonable and
parsimonious hypothesis is still the assumption of a photically entrained circadian activity
rhythm which shows lunadian masking due to strong inhibitory effects of low night-time
luminance. Significant falls in activity at the time of the full moon, observed during lunar
eclipses (Fernandez-Duque et al., in preparation), support this hypothesis.
Both the increased late morning activity around the new moon and the irregular bouts of
daytime activity observed throughout the year in the Aotus azarai of the Argentinean Chaco
(Fernandez-Duque 2003; Fernandez-Duque & Erkert 2006) might best be interpreted as
compensatory responses to detrimental nightly lighting, temperature and/or foraging
Biological Rhythm Research
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conditions, presumably ‘‘allowed’’ by an evolutionarily-acquired increased (day)light
tolerance in conjunction with a reduced predator pressure in those southernmost Aotus
habitats (Wright 1989; Fernandez-Duque 2003; Fernandez-Duque & Erkert 2006).
Eulemur
The cathemeral wild red-fronted lemurs’ activity rhythm differed considerably from that
recorded in E. fulvus albifrons under laboratory conditions. E. f. rufus showed most
activity during the day/twilight period as well as a distinct lunar variation in nocturnal
activity throughout the year (Figure 7, Kappeler & Erkert 2003) while, depending on
luminosity during the dark phase, E. f. albifrons changed from showing dark-active,
through cathemeral, to light-active behavior (Figure 3). Since the circadian activity
remained in phase with the dark, this phenotypical phase-reversal was interpreted as a
compensatory response to the increasing inhibitory masking effects due to stepwise
reductions of D-time luminosity (Erkert & Cramer 2006). The minor delays and advances,
respectively, observed in the two peaks of a male’s and female’s Tb rhythms—while their
activity rhythm was inverted after switching off D-lighting of 0.1 lux, and two weeks later
after switching it on again—agree with this interpretation. But the results may also provide
some indication of the underlying mechanism. Starting from Pittendrigh’s two-oscillator
concept (Pittendrigh & Daan 1976) of coupled m and e oscillator systems phase-set to
dawn and dusk, respectively, the minor phase shifts of the two Tb-peaks may be
interpreted as due to opposite phase-shifts of m and e. Together with the characteristics of
direct activity-inhibiting and/or activity-enhancing masking effects of low and high light
intensities, such opposite shifts of m and e oscillators and of the activity bouts coupled to
them may have resulted in the light activity observed in these lemurs. Figure 10 illustrates
this in a simple diagram.
Figure 10. Rough sketch illustrating how minor opposite phase shifts of putative morning (m) and
evening (e) oscillator-coupled activity components would lead to a phase reversal from a more ‘‘dark
active’’ (nocturnal) to a more ‘‘light active’’ (diurnal) bimodal activity pattern (middle and lower row
of triangles, respectively). The black and white bar on top indicates the LD cycle to which the two
oscillators are phase-set. Considering further the specific activity-inhibiting and activity-enhancing
(disinhibiting) non-circadian direct effects of light, the observed luminosity during the dark phase
induced an inversion of the lemurs’ activity pattern (Figure 2), in spite of there being a lack of phasereversal in the underlying circadian rhythmicity.
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H.G. Erkert
Direct activity-inhibiting effects of low light intensities may also be assumed to be
responsible for the lunar activity component of the otherwise predominantly diurnal
activity pattern shown in nature in the subspecies E. f. rufus (Figures 7 and 8). In addition,
their cathemeral behavior may also be interpreted to result from similar ‘‘negative masking
effects’’ of low night-time luminances and/or from disinhibition of nocturnal activity by
moonlight. Though yet to be established, it is assumed that the lemurs’ CTS also indicates
behavior of a genuinely nocturnal species, in that their ‘‘circadian activity phase’’ in nature
is also phase-set to the dark fraction of the 24-h day, in spite of predominantly behaving as
diurnal animals.
A common feature of the three species’ activity rhythms in nature is a very pronounced
bimodal activity pattern (Figure 8). Considering that the study sites in Madagascar and
South America were located at almost equal latitudes and that Argentinean official time is
advanced about one hour in relation to local time, the morning activity peak occurred
earliest in nocturnal Aotus, later in the cathemeral Eulemur, and latest in the diurnal
Propithecus—while the sequence of evening peak times was reversed, and daytime troughs
coincided around noon (Figure 9B). Applying Pittendrigh’s two-oscillator model
(Pittendrigh & Daan 1976) to these species activity patterns, one might hypothesize that
only minor differences in the phase-setting of the m and e oscillators to dawn and dusk
may ultimately be responsible for the differences in crepuscular peak times, and thus, in
conjunction with the species’ characteristics of masking by light, also for their more
nocturnal, cathemeral, or diurnal behavior in nature, in spite of a generally ‘‘nocturnal’’
phase-setting characteristic of the CTS. An internally-coupled dual circadian oscillator
system with oscillators set to dawn and dusk might not only be a suitable tool for the
time measurement underlying photoperiodic regulation of annual events such as
reproduction (which also occurs in lemurs, van Horn & Eaton 1979), migration and
hibernation, but also for the induction of annual activity phase reversals as described
in various vertebrates including microtine rodents (Erkinaro 1969; Pittendrigh & Daan
1976, Halle 1995). It might also provide the substrate for the species’ evolutionarilyacquired nocturnal (mainly), diurnal, crepuscular, or ‘‘cathemeral’’ behavior. In that case,
the lemurs’ cathemerality, which seems closest related to a crepuscular lifestyle, might
indeed be considered rather to represent an original trait than being derived from
nocturnal or diurnal ancestors, as has recently been proposed by Curtis and Rasmussen
(2006).
Evolutionary aspects
Without adequate answers to the yet unsettled question of how, i.e. by which central
nervous mechanism(s), diurnality may be produced or enabled in the various mammalian
taxa, chronobiology will hardly be able to contribute substantially to the problem of
‘‘why’’ given species may have changed from nocturnality to diurnality and cathemerality
or vice versa. Thus the evolutionary background of chronotype differentiation, i.e the
question of the ultimate factors that may have caused or allowed the various mammalian
taxa including primates to adopt and/or maintain a more or less strictly nocturnal,
diurnal, crepuscular, or cathemeral lifestyle, cannot be cleared up by a pure
chronobiological approach. However, systematic extension of long-term activity recordings in wild-living primates to certain closely related species and to other mammalian taxa
of different chrono-ecotypes would provide both a better overview of chronotype diversity
and clearer indications of the underlying evolutionary processes and their adaptive value.
With regard to our data presented above, of special interest would be comparative studies
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of some of the more nocturnal northern owl monkey species as well as of some other
Malagasy lemurids such as the nocturnal indriid Avahi, the cathemeral Hapalemur and the
diurnal Lemur catta and Varecia, which have also been reported to show some night-time
activity temporarily (Tattersall 1987; Curtis & Rasmussen 2006).
As indicated by the variability of the activity patterns in the wild owl monkeys and
lemurs, or, more conspiciously, by the well-known examples of wild boars and roe deers
(which, according to local hunting pressure, may be either diurnal or nocturnal),
mammalian chrono-ecotypes are obviously not to be regarded as fixed and rigid clockdriven systems squeezed once and permanently into a certain temporal niche. They
represent, rather, relatively flexible open systems whose behavioral activities are, by means
of their photically entrained CTS and the various direct effects of abiotic and biotic
environmental factors, roughly phase-positioned (but, in relation to their needs and given
environmental conditions in their habitat, nevertheless, optimally so) within the
continuum of accidental and regularly recurring, and more or less beneficial and/or
detrimental, external conditions and events. Of course, as recently shown by DeCoursey
(2003, 2004) in SCN-lesioned fossorial sciurid rodents, a functioning circadian clock might
be beneficial for an individual’s survival in nature, and should thus not be neglected in
mammalian behavioral ecology. However, on account of the very small number of animals
involved in this study and of the possibility, therefore, of a non-representative outcome,
further studies with sufficiently large numbers of test animals should be performed before
one may generalize these results and ascribe to the mammalian CTS a really crucial role
for the animals’, and hence also the species’, survival in nature. Besides their crucial
function in coordinating internal timing processes, mammalian circadian clocks are
certainly also essential tools for the timing of annual events (such as reproduction,
hibernation, or migration), for the timing of day-time related behavioral activities (such as
onset and offset of activity and resting times, especially for cave dwelling and fossorial
species) and for the time – place learning ability (necessary to avoid or visit particular
places at a certain time of day, in order to reduce or rise the chance of predator, prey, rival
or mate encounter, or to re-visit certain nectar sources, offered from many flowers only
throughout certain time windows during the day—e.g. for humming birds—or night—e.g.
nectarivorous bats). Despite this, however, their importance for the development or
modification of a certain chrono-ecotype type behavior should not be overestimated.
Driving forces and limiting factors for the transition to another temporal lifestyle, such
as that from nocturnality or crepuscularity to cathemerality or diurnality (as shown in
extant Malagasy lemuriform primates and other mammalian taxa) or vice versa (as has
been assumed in Aotus, Wright (1989), Martin (1990)) have to be looked for primarily
among relevant ecological and fitness factors, like food availability and competition,
predation pressure, general and extreme climate conditions, metabolic, thermoregulatory,
sensory, and motor capacities, etc. As compared to these factors, circadian clock
characteristics and mechanisms seem of secondary significance. Speculations about the
evolution of a certain chrono-ecotype observed in nature (Horton 2001) will have to
consider that this usually requires a whole bundle of co-evolutionary changes, some of
which may really be essential while others may be only permissive for the adopted
temporal lifestyle, or merely tolerated by it. Finally, the controversial discussion in
primatology as to which one of the various proposed factors might have caused lemurs to
become cathemeral (for review see Curtis & Rasmussen 2006) may be pointless, because
each of the facors may have contributed to a greater or lesser extent. Benefits and
constraints associated with chrono-ecotype transition will have to be analyzed separately
in each species.
262
H.G. Erkert
Acknowledgements
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I am very grateful to my colleagues Drs. Peter Kappeler (German Primate Center), Eduardo
Fernandez-Duque (Fundación Eco, Argentina), Jairo Muñoz-Delgado (Instituto Mexicano de
Psiquiatrı́a, Mexico), and Domingo Canales (Universidad Veracruzana, Mexico) for quite a pleasant
and highly productive cooperation in carrying out long-term activity recordings in wild lemurs and
owl monkeys, as well as in spider monkeys kept under seminatural conditions. Many thanks also to
Angelika Scheideler (Maximilian University, Munich) for her help with the statistics and diagram
production. Furthermore, I would like to thank Drs. Jim Waterhouse and Roberto Refinetti for their
invitation to contribute to this special issue of Biological Rhythm Research and for kindly reviewing
and improving the manuscript. Last but not least, I’m very much obliged to all my students for their
highly appreciated contributions to our comparative approach in primate chronobiology. All studies
were supported by grants from the Deutsche Forschungsgemeinschaft.
References
Albers HE, Lydic R, Gander PH. 1982. Gradual decay of circdadian drinking organization
following lesions of the suprachiasmatic nuclei in primates. Neuros Lett. 27:119–124.
Albers HE, Lydic R, Moore-Ede MC. 1984a. Role of the suprachiasmatic nuclei in the circadian
timing system of the squirrel monkey. I. The generation of rhythmicity. Brain Res. 300:275–
284.
Albers HE, Lydic R, Moore-Ede MC. 1984b. Role of the suprachiasmatic nuclei in the circadian
timing system of the squirrel monkey. II. Light-dark cycle entrainment. Brain Res. 300:285–
293.
Arditi SI. 1992. Variaciones estacionales en la actividad y dieta de Aotus azarai y Alouatta caraya en
Formosa, Argentina. Boletin Primatológico Latinoamericano. 3:11–30.
Aschoff J. 1964. Die Tagesperiodik licht- und dunkelaktiver Tiere. Rev Susse Zool. 71:528–558.
Aschoff J. 1979. Circadian rhythms:influences of internal and external factors on the period
measured in constant conditions. Z Tierpsychol. 49:225–249.
Aschoff J, Daan S, Honma K-I. 1982. Vertebrate circadian systems – structure and physiology. New
York: Springer-Verlag, Heidelberg. Zeitgebers, entrainment, and masking:some unsettled
questions. p. 13–24.
Aschoff J, Tokura H. 1986. Circadian activity rhythms in squirrel monkeys:entrainment by
temperature cycles. J Biol Rhythms. 2:91–99.
Aschoff J, von Goetz C. 1986. Effects of feeding cycles on circadian rhythms in squirrel monkeys. J
Biol Rhythms. 1:267–276.
Bonney RC, Dixson AF, Fleming D. 1980. Plasma concentration of oestradiol-17b, oestrone,
progesterone and testosterone during ovarian cycle of the owl monkey (Aotus trivirgatus). J
Reprod Fert. 60:101–107.
Boulos Z, Frim DM, Dewey LK, Moore-Ede MC. 1989. Effects of feeding schedules on circadian
organization in squirrel monkeys. Physiol Behav. 45:507–515.
Boulos Z, Machi M, Terman M. 1996. Effects of twilights on circadian entrainment patterns and
reentrainment rates in squirrel monkeys. J Comp Physiol A. 179:687–694.
Caldelas I, Poirel V-J, Sicard B, Pevet P, Challet E. 2003. Circadian profile and photic regulation of
clock genes in the suprachiasmatic nucleus of a diurnal mammal (Arvicanthus ansorgei).
Neuroscience 116:583–591.
Charles-Dominique P. 1975. Phylogeny of primates. New York: Plenum Press. p. 69–90.
Nocturnality and diurnality. An ecological interptetation of these two modes of life by an
analysis of the higher vertebrate fauna in tropical forest ecosystems.
Colguhoun IC. 1998. Cathemeral behaviour of Eulemur macaco macaco at Ambato Massif,
Madagascar. Folia Primatol. 69:22–34.
Costa MSMO, Moreira LF, Alones V, Lu J, Santee UR, Cavalcante JS, Moraes PRA, Britto LRG,
Menaker M. 1998. Characterization of the circadian system of monkey (Callithrix jacchus):Immunohistochemical analysis and retinal projections. Biol Rhytm Res. 29:510–520.
Downloaded by [University of California Davis] at 18:06 10 November 2011
Biological Rhythm Research
263
Crompton AW, Taylor CR, Jagger JA. 1978. Evolution of homeothermy in mammals. Nature.
272:333–336.
Curtis DJ, Zaramody A, Martin RD. 1999. Cathemerality in the mongoose lemur, Eulemur mongoz.
Am J Primatol. 47:279–298.
Curtis DJ, Rasmussen MA. 2006. The evolution of cathemerality in primates and other mammals:a
comparative and chronoecological approach. Folia Primatol. 77:178–193.
Curtis DJ, Zaramody A, Martin D. 1999. Cathemerality in the mongoose lemur, Eulemur mongoz.
Am J Primatol. 47:279–298.
Daan S. 2000. Colin Pittendrigh, Jürgen Aschoff, and the natural entrainment of circadian systems. J
Biol Rhythms. 15:195–207.
Daan S, Albrecht U, van der Horst GT, Illnerova H, Roenneberg T, Wehr TA, Schwartz WJ. 2001.
Assembling a clock for all seasons:are there M and E oscillators in the genes? J Biol Rhythms.
16:105–116.
DeCoursey PJ. 2003. Chronobiology: Biological timekeeping. Sunderland (MA): Sinauer Associates,
Inc.. p. 144–178. The behavioral ecology and evolution of biological timing systems.
DeCoursey PJ. 2004. Diversity of function of SCN pacemakers in behavior and ecology of three
species of sciurid rodents. Biol Rhythm Res. 35:13–33.
DeCoursey PJ, DeCoursey G. 1964. Adaptive aspects of activity rhythms in bats. Biol Bull. 126:14–
27.
De la Iglesia HO, Meyer J, Carpino A, Jr., Schwartz WJ. 2000. Antiphase oscillation of the left and
right suprachiasmatic nuclei. Science. 290:799–801.
Doerrscheidt GJ, Beck L. 1975. Advanced method for evaluating characteristic parameters (tau,
alpha, rho) of circadian rhythms. J Math Biol. 2:107–121.
Donati G, Borgognini-Tarli SM. 2006. Influence of abiotic factors on cathemeral activity:
a case of Eulemur fulvus collaris in the littoral forest of Madagascar. Folia Primatol. 77:104–
122.
Donati G, Lunardini A, Kappeler PM, Borgonini Tarli S. 2001. Nocturnal activity in the cathemeral
red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse. Am J
Primatol. 53:69–78.
Edgar DM, Dement WC, Fuller CA. 1993. Effects of SCN lesions on sleep in squirrel
monkeys:Evidence for opponent processes in sleep-wake regulation. J Neurosci. 13:1065–1079.
Erkert HG. 1974. Der Einfluss des Mondlichtes auf die Aktivitaetsperiodik nachtaktiver Saeugetiere.
Oecologia. 14:269–287.
Erkert HG. 1976a. Lunarperiodic variation of the phase-angle difference in nocturnal animals under
natural Zeitgeber conditions near the equator. Int J Chronobiol. 4:125–138.
Erkert HG. 1976b. Beleuchtungsabhaengiges Aktivitaetsoptimum bei Nachtaffen (Aotus trivirgatus).
Folia Primatol. 25:186–192.
Erkert HG. 1982. Ecology of bats. New York, London: Plenum Press. p. 201–242. Ecological aspects
of bat activity rhythms.
Erkert HG. 1989. Characteristics of the circadian activity rhythm in common marmosets (Callithrix
j. jacchus). Am J Primatol. 17:271–286.
Erkert HG. 1991. Primatology today. Amsterdam, New York, Oxford: Elsevier Science Publishers.
p. 435–438. Influence of ambient temperature on circadian rhythms in Colombian owl monkeys,
Aotus lemurinus griseimembra.
Erkert HG. 2003. Field and laboratory methods in primatology. Cambridge: Cambridge University
Press. p. 252–270. Chronobiological aspects of primate research.
Erkert HG, Cramer B. 2006. Chronobiological background to cathemerality:circadian rhythms in
Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea). Folia Primatol.
77:87–103.
Erkert HG, Gburek V, Scheideler A. 2006. Photic entrainment and masking of prosimian circadian
rhythms (Otolemur garnettii, Primates). Physiol Behav. 88:39–46.
Erkert HG, Groeber J. 1986. Direct modulation of activity and body temperature of owl monkeys
(Aotus lemurinus griseimembra) by low light intensities. Folia Primatol. 47:171–188.
Downloaded by [University of California Davis] at 18:06 10 November 2011
264
H.G. Erkert
Erkert HG, Kappeler PM. 2004. Arrived in the light:diel and seasonal activity patterns in wild
Verreaux’s sifakas (Propithecus v. verreauxi, Primates:Indriidae). Behav Ecol Sociobiol. 57:174–
186.
Erkert HG, Schardt U. 1991. Social entrainment of circadian activity rhythms in common
marmosets, Callithrix j. jacchus (Primates). Ethology. 87:189–202.
Erkert HG, Thiemann A. 1983. Dark switch in the entrainment of circadian activity rhythms in night
monkeys, Aotus trivirgatus HUMBOLDT. Comp Biochem Physiol. 74A:307–310.
Erkinaro E. 1969. Der Phasenwechsel der lokomotorischen Aktivitaet bei Microtus agrestis (L.), M.
arvalis (Pall.) und M. oeconomicus (Pall.). Aquilo Ser Zool. 13:1–31.
Farrer DN, Ternes JW. 1969. Circadian rhythms in nonhuman primates. Basel: S. Karger. p. 1–7.
Bibl Primat 9, Illumination intensity and behavioural circadian rhythms.
Fernandez-Duque EF. 2003. Influences of moonlight, ambient temperature and food availablility on
the diurnal and nocturnal activity of owl monkeys (Aotus azarai). Behav Ecol Sociobiol. 54:431–
440.
Fernandez-Duque EF, Erkert HG. 2006. Cathemerality and lunar periodicity of activity rhythms in
owl monkeys of the Argentinean chaco. Folia Primatol. 77:123–138.
Ferraro JE, Sulzman FM. 1988. The effects of feedback lighting on the circadian drinking rhythm in
the diurnal new world primate Saimiri sciureus. Am J Primatol. 15:143–155.
Fleagle JG. 1988. Primate adaptation and evolution. San Diego, New York: Academic Press, Inc.. p.
474.
Fuller CA, Edgar DM. 1986. Effects of light intensity on the circadian temperature and feeding
rhythms in the squirrel monkey. Physiol Behav. 36:687–691.
Fuller CA, Lydic R, Sulzman FM, Albers HE, Tepper B, Moore-Ede MC. 1981. Circadian rhythm
of body temperature persists after suprachiasmatic lesions in the squirrel monkey. Am J Physiol.
241:R385–R391.
Gander PH, Moore-Ede MC. 1983. Light-dark masking of circadian temperature and activity
rhythm in squirrel monkeys. Am J Physiol. 245:R927–R934.
Garcia JE, Braza. 1987. Activity rhythms and use of space of a group of Aotus azarae in Bolivia
during the rainy season. Primates. 28:337–342.
Glass JD, Tardiff SD, Clements R, Mrosovsky N. 2001. Photic and nonphotic circadian phase
resetting in a diurnal primate, the common marmoset. Am J Physiol. 280:R191–R197.
Haerter L, Erkert HG. 1993. Alteration of circadian period length does not influence the ovarian
cycle length in common marmosets, Callithrix j. jacchus (Primates). Chronobiol Int. 10:165–
175.
Haeussler U, Erkert HG. 1978. Different direct effects of light intensity on the entrained activity
rhythm in neotropical bats (Chiroptera, Phyllostomidae). Behav Proc. 3:223–239.
Halle S. 1995. Diel patterns of locomotor activity in populations of root voles, Microtus
oeconomicus. J Biol Rhythms. 10:211–224.
Halle S. 2006. Polyphasic activity patterns in small mammals. Folia Primatol. 77:15–26.
Hawking F, Lobban MC. 1970. Circadian rhythms in macaca monkeys (physical activity,
temperature, urine and microfilarial levels). J Interdisc Cycle Res. 1:267–290.
Hoban TM, Levine AH, Shane RB, Sulzman FM. 1985. Circadian rhythms of drinking and body
temperature rhythms in night monkeys, Aotus trivirgatus HUMBOLDT. Comp Biochem
Physiol. 74A:307–310.
Hoban TM, Sulzman FM. 1985. Light effects on the circadian timing system of a diurnal primate,
the squirrel monkey. Am J Physiol. 249:R274–280.
Horton TH. 2001. Handbook of Neurobiology 12:Circadian clocks. New York: Kluwer Academic
Press/Plenum Publishers. p. 45–57. Conceptual issues in the ecology and evolution of circadian
rhythms.
Hut RA, van Oort BEH, Daan S. 1999a. Natural entrainment without dawn and dusk: The case of
the European ground squirrel. J Biol Rhythms. 14:290–299.
Hut RA, Mrosovsky N, Daan S. 1999b. Nonphotic entrainment in a diurnal mammal, the European
ground squirrel (Spermophilus citellus). J Biol Rhythms. 14:409–419.
Downloaded by [University of California Davis] at 18:06 10 November 2011
Biological Rhythm Research
265
Jagota A, de la Iglesia HO, Schwartz WJ. 2000. Morning and evening circadian oscillations in the
suprachiasmatic nucleus in vitro. Nat Neurosci. 3:372–376.
Kappeler PM, Erkert HG. 2003. On the move around the clock:correlates and determinants of
cathemeral activity in wild redfronted lemurs (Eulemur fulvus fulvus). Behav Ecol Sociobiol.
54:359–369.
Kas MJH, Edgar DM. 2000. Photic phase response curve in Octodon degus:assessment as a function
of activity phase preference. Am J Physiol. 278:R1385–R1389.
King DP, Takahashi JS. 2000. Molecular genetics of circadian rhythms in mammals. Ann Rev
Neurosci. 23:713–742.
Kirk EC. 2006. Eye morphology in cathemeral lemurids and other mammals. Folia Primatol. 77:27–
49.
Klein DC, Moore RY, Reppert SM. editors. 1991. Suprachiasmatic nucleus. The mind’s clock. New
York (Oxford): Oxford University Press. p. 467.
Lee HS, Billings HJ, Lehman MN. 2003. The suprachiasmatic nucleus:a clock of multiple
components. J Biol Rhythms. 18:435–449.
Lee TM. 2004. Growing evidence that some aspects of SCN function differ in nocturnal and diurnal
rodents. Am J Phsiol Regul Integr Comp Physiol. 286:R814–R815.
Lemos DR, Downs JL, Urbanski HF. 2006. Twenty-four-hour rhythmic gene expression in the
rhesus macaque adrenal gland. Mol Endocrinol. 20:1164–1176.
Lydic R, Albers HE, Tepper B, Moore-Ede MC. 1981. Three-dimensional structure of mammalian
suprachiasmatic nuclei:a comparative study of five species. J Comp Neurol. 204:225–237.
Marques MD, Waterhouse J. 2004. Rhythms and Ecology – do chronobiologists still remember
nature? Biol Rhythm Res. 35:1–2.
Martin RD. 1990. Primate origins and evolution. London: Chapman and Hall.
Martinez JL. 1972. Effects of selected illumination levels on circadian periodicity in the rhesus
monkey (Macaca mulatta). J Interdisc Cycle Res. 3:47–59.
Meijer JH, Schwartz WJ. 2003. In search of the pathways for light-induced pacemaker resetting the
suprachiasmatic nucleus. J Biol Rhythms. 18:235–249.
Minors D, Waterhouse J, Rietveld W. 1996. Constant routine and ‘‘purification’’ methods:do they
measure the same thing? Biol Rhythm Res. 27:166–174.
Moore RY. 1993. Organization of the primate circadian system. J Biol Rhythms. 8(Suppl):3–9.
Moore RY, Leak RK. 2001. Suprachiasmatic nucleus. In: Takahashi JS, Turek FW, Moore RY,
editors. Handbook of behavioral neurobiology, Vol. 12:Circadian clocks. New York: Kluwer
Academic/Plenum Publishers. p. 141–179.
Moore-Ede MC, Sulzman FM. 1977. The physiological basis of circadian timekeeping in primates.
Physiologist. 20:17–25.
Moore-Ede MC, Kass DA, Herd JA. 1977. Transient circadian internal desynchronization after
light-dark shifts in monkeys. Am J Physiol. 232:R31–37.
Moore-Ede MC, Sulzman FM, Fuller. 1982. The clock that time us. Physiology of the circadian
system. Cambridge Mass and London: Harvard University Press. p. 448.
Morgan E. 2004. Ecological significance of biological clocks. Biol Rhythm Res. 2004:3–12.
Moynihan M. 1964. Some behavior patterns of platyrrhine monkeys. I. The night monkey (Aotus
trivirgatus). Smithsonian Misc Coll. 146:1–84.
Mrosovsky N. 1994. In prais of masking:behavioral responses of retinally degenerate mice to dim
light. Chronobiol Int. 11:343–348.
Mrosovsky N. 1999. Masking:History, definitions, and measurement. Chronobiol Int. 16:415–429.
Mrosovsky N. 2003. Beyond the suprachiasmatic nucleus. Chronobiol Int. 20:1–8.
Muñoz M, Peirson SN, Hankins MW, Foster RG. 2005. Long-term constant light induces
constitutive elevated expression of mPER2 protein in the murine SCN:A molecular basis for
Aschoff’s rule? J Biol Rhythms. 20:3–14.
Muñoz-Delgado J, Corsi-Cabrera M, Canales-Espinoza D, Santillán-Doherty AM, Erkert HG.
2004. Astronomicl and meteorological parameters and rest-activity rhythm in the spider monkey
Ateles geoffroyi. Physiol Behav. 83:107–117.
Downloaded by [University of California Davis] at 18:06 10 November 2011
266
H.G. Erkert
Muñoz-Delgado J, Fuentes-Pardo B, Euler Baum A, Lanzagorta N, Arenas-Rosas R, SantillanDoherty AM, Guevara MA, Corsi-Cabrera M. 2005. Presence of a circadian rhythm in the
spider monkey’s (Ateles geoffroyi) motor activity. Biol Rhythm Res. 36:115–121.
Murakami DM, Fuller CA. 1990. The retinohypothalamic projection and oxidative metabolism in
the suprachiasmatic nucleus of primates and tree shrews. Brain Behav Evol. 35:302–312.
Pálkova M, Sigmund L, Erkert HG. 1999. Effect of ambient temperature on the circadian
activity rhythm in common marmosets, Callithrix j. jacchus (Primates). Chronobiol Int. 16:149–
161.
Pittendrigh CS, Daan S. 1976. A functional analysis of circadian pacemakers in nocturnal rodents.
V. Pacemaker structure:a clock for all seasons. J Comp Physiol. 106:333–355.
Rappold I, Erkert HG. 1994. Re-entrainment, phase-response and range of entrainment of
circadian rhythms in owl monkeys (Aotus lemurinus g.) of different age. Biol Rhythm Res.
25:133–152.
Rauth-Widmann B, Fuchs E, Erkert HG. 1996. Infradian alteration of circadian rhythms in owl
monkeys (Aotus lemurinus griseimembra):An effect of estrous? Physiol Behav. 59:11–18.
Rauth-Widmann B, Thiemann-Jäger A, Erkert HG. 1991. Significance of nonparametric light effects
in entrainment of circadian rhythms in owl monkeys (Aotus lemurinus griseimembra) by lightdark cycles. Chronobiol Int. 8:251–266.
Redlin U, Mrosovsky N. 2004. Nocturnal activity in a diurnal rodent (Arvicanthis niloticus):The
importance of masking. J Biol Rhythms. 19:58–67.
Refinetti R. 2004. Parameters of photic resetting of the circadian system of a diurnal rodent, the nile
grass rat. Acta Sci Vet. 32:1–7.
Refinetti R. 2006. Variability of diurnality in laboratory rodents. J Comp Physiol A. 192:701–
714.
Reebs SG, Mrosovsky N. 1989. Effects of induced wheel running on the circadian activity rhythms of
Syrian hamsters:entrainment and phase response curve. J Biol Rhythms. 4:39–48.
Rensing L. 1989. Is ‘‘masking’’ an appropriate term? Chronobiol Int. 6:297–300.
Reppert SM, Perlow MJ, Ungerleider LG, Mishkin M, Tamarkin L, Orloff DG, Hoffman HJ, Klein
DC. 1981. Effects of damage to the suprachiasmatic area of the anterior hypothalamus on the
daily melatonin and cortisol rhythms in the rhesus monkey. J Neurosci. 1:1414–1425.
Reppert S, Schwartz W, Uhl G. 1987. Arginine vasopressin:A novel peptide rhythm in cerebrospinal
fluid. Trends Neurosci. 10:76–80.
Robinson EL, Fuller CA. 1999. Light masking of circadian rhythms of heat production, heat loss,
and body temperature in squirrel monkeys. Am J Physiol. 276:R298–R307.
Rotundo M, Sloan C, Fernandez-Duque E. 2000. Cambios estacionales en el ritmo de actividad del
mono mirikiná (Aotus azarai) en Formosa Argentina. In: Cabrera E, Mércolli C, Resquin R
(eds.) Manejo de fauna silvestre en Amazonia y Latinoamerica, pp. 413–417. Asunción,
Fundación Moisés Bertoni.
Schanz F, Erkert HG. 1987. Resynchronisationsverhalten der Aktivitaetsperiodik von Galagos
(Galago senegalensis, Galago crassicaudatus garnettii). Z Saeugetierk. 52:218–226.
Schardt U, Wilhelm I, Erkert HG. 1989. Splitting of the circadian activity rhythm in common
marmosets (Callithrix j.jacchus; Primates). Experientia. 45:1112–1115.
Schilling A, Richard J-P, Servière J. 1999. Duration of activity and period of circadian activity-rest
rhythm in a photoperiod-dependent primate, Microcebus murinus. CR Acad Sci Paris, Life Sci.
322:759–770.
Schwartz MD, Nunez AA, Smale L. 2004. Differences in the suprachisamatic nucleus and lower
subparaventricular zone of diurnal and nocturnal rodents. Neusoscience. 127:13–23.
Schwartz WJ, de la Iglesia HO, Zlomanczuk P, Illnerova H. 2001. Encoding le quattro stagioni
within the mammalian brain: Photoperiodic orchestration through the suprachiasmatic nucleus.
J Biol Rhythms. 16:302–311.
Shearman LP, Siriam S, Weaver DR, Maywood ES, Chavez I, Zheng B, Kume K, Lee CC, van der
Horst GTJ, Hastings MH, Reppert SM. 2000. Interacting molecular loops in the mammalian
circadian clock. Science. 288:1013–1019.
Downloaded by [University of California Davis] at 18:06 10 November 2011
Biological Rhythm Research
267
Smale L, Lee T, Nunez AA. 2003. Mammalian diurnality:some facts and gaps. J Biol Rhythms.
18:356–366.
Starck D. 1978. Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage. Vol.
1:Theoretische Grundlagen, Stammesgeschichte und Systematik unter Beruecksichtigung der
niederen Chordata. Berlin, Heidelberg, New York: Springer-Verlag. p. 274.
Sulzman FM, Fuller CA, Moore-Ede MC. 1977a. Feeding time synchronizes primate circadian
rhythms. Physiol Behav. 18:775–779.
Sulzman FM, Fuller CA, Moore-Ede MC. 1977b. Spontaneous internal desynchronization of
circadian rhythms in the squirrel monkey. Comp Biochem Physiol. 58A:63–67.
Sulzman FM, Fuller FA, Moore-Ede MC. 1978. Comparison of synchronization of primate
circadian rhythms by light and food. Am J Physiol. 234:R130–R135.
Sulzman FM, Fuller CA, Moore-Ede. 1979. Tonic effects of light on the circadian system of the
squirrel monkey. J Comp Physiol. 129:43–50.
Tattersall I. 1987. Cathemeral activity in primates:a definition. Folia Primatol. 49:200–202.
Tattersall I. 1979. Patterns of activity in the Mayotte lemur. J Mammal. 60:314–323.
Tattersall I. 2006. The concept of cathemerality: history and definition. Folia Primatol. 77:7–14.
Thiemann-Jaeger A. 1986. Charakteristika der circadianen Aktivitaetsperiodik von Nachtaffen (Aotus
trivirgatus, HUMBOLDT 1811). Germany: University of Tuebingen. p. 79. Doctoral thesis.
Tokura H, Aschoff J. 1978. Circadian activity rhythms of the pig-tailed macaque, Macaca
nemestrina, under constant conditions. Pfluegers Archiv. 376:241–243.
Tokura H, Aschoff J. 1983. Effects of temperature on the circadian rhythm of pig-tailed macaques,
Macaca nemestrina. Am J Physiol. 245:R800–804.
Van Horn RN, Eaton GG. 1979. The Study of prosimian behaviour. New York: Academic Press. p.
79–122. Reproductive physiology and behavior in prosimians.
Van Schaik CP, Kappeler PM. 1996. The social systems of gregarious lemurs:lack of convergence
with anthropoids due to evolutionary disequilibrium? Ethology. 102:915–941.
Weaver DR. 1998. The suprachiasmatic nucleus:a 25-year retrospective. J Biol Rhythms. 13:100–
112.
Wechselberger E. 1994. Current Primatology Vol. III. Strasbourg: Université Louis Pasteur. p. 223–
226. Phase-shifting effects of arousal on circadian rhythms in Callithrix j. jacchus.
Wechselberger E. 1995. Charakteristik und Mechanismen der Synchronisation der Circadianperiodik des Weissbuesschelaeffchens, Callithrix j. jacchus. Germany: University of Tuebingen. p.
113. Doctoral thesis.
Wechselberger E, Erkert HG. 1994. Characteristics of the light-induced phase response of circadian
activity rhythms in common marmosets, Callithrix j. jacchus [Primates-Cebidae]. Chronobiol Int.
11:275–284.
Wexler DB, Moore-Ede MC. 1985. Circadian sleep-wake cycle organization in squirrel monkeys.
Am J Physiol. 248:R353–R362.
Wexler DB, Moore-Ede MC. 1986. Resynchronization of circadian sleep-wake and temperature
cycles in the squirrel monkey following phase shifts of the environmental light-dark cycle. Aviat
Space Environ Med. 57:1144–1149.
Wright PC. 1978. Home range, activity patterns, and agonistic encounters of a group of night
monkeys (Aotus trivirgatus) in Perú. Folia Primatol. 29:43–55.
Wright PC. 1989. The nocturnal primate niche in the New World. J Hum Evol. 18:635–658.
Yan L, Foley NC, Bobula JM, Kriegsfeld LJ, Silver R. 2005. Two antiphase oscillations
occur in each suprachiasmatic nucleus of behaviorally split hamsters. J Neurosci. 28:9017–
9026.
Yellin AM, Hauty GT. 1971. Activity cycles of the rhesus monkey (Macaca mulatta) under several
experimental conditions both in isolation and in a group situation. J Interdiscipl Cycle Res.
2:475–490.
Zordan M, Costa R, Macino G, Fukuhara C, Tosini G. 2000. Circadian clocks: what makes them
tick? Chronobiol Int. 17:433–451.