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© 2005 Nature Publishing Group
Vol 438|22/29 December 2005
1095
Circadian organization in reindeer
These Arctic animals abandon their daily rhythms when it is dark all day or light all night.
The light/dark cycle of day and night synchro-
nizes an internal ‘biological clock’ that governs
daily rhythms in behaviour, but this form of
regulation is denied to polar animals for most
of the year. Here we demonstrate that the con-
tinuous lighting conditions of summer and of
winter at high latitudes cause a loss in daily
rhythmic activity in reindeer living far above
the Arctic Circle. This seasonal absence of
circadian rhythmicity may be a ubiquitous
trait among resident polar vertebrates.
Circadian oscillators are present in all
organisms on our rotating planet (see ref. 1, for
example). These ‘biological clocks’ govern the
temporal organization of physiological func-
tions and behaviour, and enable plants and
animals to anticipate and prepare for daily
events such as sunrise and sunset2. A convinc-
ing argument for the internal nature of circa-
dian regulation is the persistence of temporal
organization under constant environmental
conditions. This was first described in the plant
Mimos a pudica by the French astronomer Jean
de Mairan in 1729 (ref. 3), and persistence,
under constant conditions, of rhythms with
periods deviating slightly from 24 h remains
a prerequisite for the identification of circa-
dian control.
Few plants and animals experience constant
conditions in the wild. But at high latitudes,
where the Sun neither sets in summer nor rises
in winter, resident polar organisms experience
the distinct changes in light intensity that
result from a day/night cycle for just a few
weeks each year — in spring and in autumn.
We recorded daily patterns of activity contin-
uously for one year in two subspecies of rein-
deer: Rangifer tarandus platyrhynchus (5 or 6
animals; Fig. 1a, b) living at 78 N in the high
Arctic archipelago of Svalbard, and R. t. taran-
dus (6 animals) living in northern Norway
at 70 N. The animals ranged freely in their
natural habitat. (For methods, see supplemen-
tary information.)
All animals showed alternating bouts of
activity and inactivity typical of ruminants4;
these cycles were substantially shorter than
24 hours (ultradian) and persisted throughout
the year. Plots of activity over time (acto-
grams) reveal a complete absence of circadian
organization of this behaviour in both sub-
species in summer and in Svalbard reindeer in
winter (Fig. 1c, d). Evidently, the changes in
light intensity that occur across the day at
these times are not sufficient to synchronize
BRIEF COMMUNICATIONS
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c d
Figure 1 |Activity patterns in reindeer under
polar light conditions. a, b, Polar light
conditions: mixed groups of Svalbard reindeer
Rangifer tarandus platyrhynchus at 7 8 N,
at a, midnight in late June, and b, midday in
mid-February. c, d, Sample actograms showing
patterns of activity over one year in sub-adult
reindeer in c, northern Norway (R. t. tarandus,
70 N; n1), and d,Svalbard (R. t. platy-
rhynchus, 78 N; n1). Data, recorded
continuously using small activity-loggers,
are presented as double-plot actograms in
which each row represents two consecutive
days; time of day is indicated. Bouts of activity
(black bars) are interspersed with bouts of
inactivity (white spaces). Grey region, data
missing. Lines indicating the beginning and
end of civil twilight (when light intensity is
10 lux, orange) and sunrise and sunset
(yellow) are superimposed on each
actogram. Rhythmicity in the actograms
was determined by F-periodogram analysis
(see supplementary information).
22.12 brief comms MH 15/12/05 5:37 PM Page 1095
Nature Publishing Group
© 2005
© 2005 Nature Publishing Group
BRIEF COMMUNICATIONS NATURE|Vol 438|22/29 December 2005
One of the most striking predictions of Ein-
stein’s special theory of relativity is also per-
haps the best known formula in all of science:
Emc2. If this equation were found to be even
slightly incorrect, the impact would be enor-
mous — given the degree to which special
relativity is woven into the theoretical fabric of
modern physics and into everyday applica-
tions such as global positioning systems. Here
we test this mass–energy relationship directly
by combining very accurate measurements of
atomic-mass difference, m, and of -ray
wavelengths to determine E, the nuclear bind-
ing energy, for isotopes of silicon and sulphur.
Einstein’s relationship is separately confirmed
in two tests, which yield a combined result of
1mc2/E(1.44.4)107, indicating
that it holds to a level of at least 0.00004%. To
our knowledge, this is the most precise direct
test of the famous equation yet described.
Our direct test is based on the prediction
that when a nucleus captures a neutron and
emits a -ray, the mass difference mbetween
the initial (including unbound neutron) and
final nuclear states, multiplied by c2 (where c is
the speed of light), should equal the energy of
the emitted -ray(s), as determined from
Planck’s relation Ehf (where h is Planck’s
constant and fis frequency).
The total energy of the -rays emitted as
the daughter nucleus
decays to the ground-
state was determined
by summing the indi-
vidual -ray energies.
These were obtained
by wavelength mea-
surement using crystal
Bragg spectroscopy.
The mass difference
mis measured by
simultaneous compar -
isons of the cyclotron
frequencies (inversely
proportional to the
mass) of ions of the
initial and final iso-
topes confined over a
period of weeks in a
Penning trap.
For an atom X with
a mass number of A
WORLD YEAR OF PHYSICS
A direct test of Emc2
the pattern of activity in reindeer. However,
the daily pattern was modified when there was
a distinct light/dark cycle, and reindeer in
northern Norway, in particular, displayed a
significant rhythm of exactly 24 hours
throughout autumn, winter and spring (see
supplementary information).
Free-living reindeer do not therefore show
evidence of the classical prerequisite for
circadian organization— persistence under
constant conditions. Seasonal absence of
rhythmicity in the circadian range has been
recorded in the daily activity of the Svalbard
ptarmigan (L agopus mutus hyperboreus)5, and
in circulating levels of the hormone melatonin
in ptarmigan6and in reindeer7, indicating that
the expression of an internal clock is reduced
in both Arctic species under constant light
conditions. We therefore suggest that seasonal
absence of circadian rhythmicity is a ubiqui-
tous trait among resident polar vertebrates.
Reduced circadian organization may
enhance animals’ responsiveness and speed
of phase adaptation to the light/dark cycle, as
proposed for migrating birds8and mammals
emerging from hibernation9. And for herbi-
vores in polar regions, there can be little
selective advantage in maintaining strong
internal clocks in an effectively non-rhythmic
environment.
Bob E. H. van Oort*, Nicholas J. C. Tyler†,
Menno P. Gerkema‡, Lars Folkow*,
Arnoldus Schytte Blix*, Karl-Arne Stokkan*
*Department of Arctic Biology and Institute of
Medical Biology, †Centre for Sámi Studies,
University of Tromsø, 9037 Tromsø, Norway
e-mail: karlarne@fagmed.uit.no
‡Department of Chronobiology, University of
undergoing this nuclear reaction, the com-
parison is expressed in terms of measured
quantities as
Mc2M[AX]M[A1X]M[D]M[H])c2
103NAh(fA1fD) mol AMU kg1(1)
where the Avogadro constant NArelates the
measured mass M[X] in unified atomic mass
units (AMU) to its mass in kilograms m[X].
We made comparisons for A1X29Si and
A1X33S. The mass of the neutron M[n] is
determined from the masses1of hydrogen M[H]
and deuterium M[D] combined with fD, the
frequency of the -ray corresponding to the
deuteron binding energy2. The molar Planck
constant is NAh3.990312716(27)1010 Js
mol1; numbers in parentheses indicate uncer-
tainty on the last digits. This figure has been
independently confirmed at about the 5108
level by a range of experiments through its rela-
tionship with the fine-structure constant1.
The -ray frequencies on the righthand side
of equation (1) have been measured using the
GAMS4 crystal-diffraction facility at the
Laue–Langevin Institute in Grenoble3. The
-rays emitted from sources located near the
high-flux reactor core are diffracted by two
nearly perfect, flat crystals whose lattice spac-
ing, d, has been determined in metres4. The
diffraction angles,
, are measured with angle
interferometers calibrated using a precision
optical polygon (Fig. 1a). Wavelengths are
determined from the Bragg equation
2dsin
and were measured for the 3.5-
MeV and 4.9-MeV transitions in 29Si, for the
0.8-MeV, 2.4-MeV and 5.4-MeV transitions in
33S, and for the 2.2-MeV transition in deu-
terium 2H (see supplementary information).
Because the diffraction angle for a 5-MeV
-ray by a low-order silicon reflection is less
than 0.1, our binding-energy determinations
were limited by our ability to measure the dif-
fraction angles of the highest-energy -rays
with fractional accuracy better than about
Groningen, 9750 AA Haren, The Netherlands
1. Lowrey, P. L. & Takahashi, J. S. Annu. Rev. Genom. Hum.
Genet. 4, 407–441 (2004).
2. Daan, S. & Aschoff, J. in Circadian Clocks (eds Takahashi, J. S.
et al.) 7–43 (Plenum, New York, 2001).
3. de Mairan, J. J. in Histoire de l´Académie Royale des Sciences
35–36 (Paris, 1729).
4. Gerkema, M. P. in Biological Rhythms (ed. Kumar, V.)
207–215 (Narosa, New Dehli, 2002).
5. Stokkan, K. A., Mortensen, A. & Blix, A. S. Am. J. Physiol.
251, 264–267 (1986).
6. Reierth, E., van’t Hof, T. & Stokkan, K. A. J. Biol. Rhyth. 14,
314–319 (1999).
7. Stokkan, K. A., Tyler, N. J. C. & Reiter, R. J. Can. J. Zool. 72,
904–909 (1994).
8. Hau, M. & Gwinner, E. Physiol. Behav. 58, 89–95 (1995).
9. Hut, R. A., Van der Zee, E. A., Jansen, K., Gerkema, M. P. &
Daan, S. J. Comp. Physiol. B172, 59–70 (2002).
Supplementary information accompanies this
communication on Nature’s website.
Competing financial interests: declared none.
doi:10.1038/4381095a
Albert Einstein: father
of the famous formula.
BETTMANN/CORBIS
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