Friday, January 20, 2006

Circadian Rhythms, or Not, in Arctic Reindeer

There are two main hypotheses - not mutually exclusive - for the adaptive value of having a circadian clock. One is the Internal Synchronization hypothesis, stating that the circadian clock serves to synchronize biochemical and physiological processes within the body. The second is the External Synchronization hypothesis, stating that the circadian clock serves to syncronize the physiology and behavior to the natural environment.

The prediction from the Internal Hypothesis is that circadian rhythms in various physiological parameters - for instance body temperature, release of various hormones, cell division - will persist in organisms that live in non-rhythmic environments, e.g., in caves, underground or in the depths of the ocean. Measuring such parameters, especially in the wild, is difficult and expensive, though, so not much work has been done. Work in the laboratory, mostly in fruitflies and hamsters, brings indirect support for this hypothesis.

The predicition from the External Hypothesis is that circadian rhythms of behavior will not persist in organisms that live in arrhythmic environments. This has been shown in a number of fossorial animals in the field.

A research group from Norway has recently published a short paper in Nature (I saw these data on a poster at a meeting in 1999 - just goes to show how long it takes to publish in Nature!), looking at an animal that lives in an environment that is sometimes rhythmic, sometimes not - the Arctic. They have monitored, for a whole year, the gross locomotor activity of 12 reindeer. Six of those were in Svaldbard (78 degrees North) and the other six were of another subspecies in northern Norway (70 degrees North).
In the Arctic, for several months during the winter there is only darkness - it is the long polar night. Likewise, it is one continuous day through the months of summer. However, for a few weeks in spring and again in fall, there is a clear light-dark cycle in the environment.

What the group discovered was that, in both subspecies, there was no detectable rhythm during the one long day of summer. This is consistent with the data in a number of laboratory animals - constant bright light tends to supress circadian rhythmicity. Reindeer, like most ruminants, have ultradian rhythms of activity, i.e., tend to roam and forage in bursts.

During spring and fall, both subspecies entrained to the external light-dark cycle, although the rhythm in Norway deer appeared much more robust. It is unclear if the apparent rhythms in the more Northern population were entrained circadian rhythms or masking effects (i.e., direct effects of light on activity) of the LD cycle.

During the winter, though, the Norway reindeer exhibited a freerunning rhythm of activity, but the Svaldbard deer were again not showing any rhythms. An absence of a freerunning rhythm in constant darkness is a rare finding in animal chronobiology, and the data strongly support the External Synchronization hypothesis.
On the left - Norway deer, on the right - Svaldbard deer. Every black dot is a bout of activity and white dot a bout of inactivity. X-axis is a double-plotted 24-hour day. Y-axis (going from top to bottom) shows one day of the year in each row.

However, people from the same group (mostly Karl-Arne Stokkan) have shown before that Svaldbard reindeer (as well as Svaldbard ptarmigan, a gallinaceous bird, which is also behaviorally arrhythmic in a similar experiment) have no rhythm of melatonin secretion during the long polar night in winter either, something that contradicts the Internal Synchronization hypothesis to some extent. On the other hand, people and seals living at the same latitudes have circadian rhythms in melatonin release.

Circadian pacemakers in the suprachiasmatic nuclei signal time of day using various neural and hormonal mechanisms. One of the mechanisms involves rhythmic stimuulation of melatonin release from the pineal gland. Other hormones may be Arginine Vasopressing, Cortisol, brain peptides, etc. It is possible that melatonin signal acts on brain centers that drive various behaviors, while other neural and humoral signals drive rhythms in biochemistry and physiology of various internal organs. It is, thus, possible that animals in arrhythmic environments have no rhythms in melatonn release or behavior but still retain rhythms in physiology - something that can be tested by, for instance, continuous monitoring of body temperature in the field - hard and expensive, but not impossible to do. If this is the case, that both Internal and External Synchronization hypotheses will be supported.

Circadian clocks are so ubiqutous, it is difficult to come up with a conclusive evidence for their adaptive function. Finding animals, like reindeer, that are not rhythmic in constant natural environments but exhibit rhythms when the environment is rhythmic, add some strength to the notion that the biological clocks are evolved adaptations.

And of course, not being sleepy on the night of December 25th certainly helps Rudolf, Prancer and friends work more efficiently in delivering presents.

van Oort BE, Tyler NJ, Gerkema MP, Folkow L, Blix AS, Stokkan KA. Circadian organization in reindeer. Nature. 2005 Dec 22;438(7071):1095-6.


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