The results gained from laboratory experiments, together with observations in nature, can give us insights into how Gonyaulax populations behave under the natural conditions of their environment in the ocean. During the day, they rise to the surface to capture light, which they need to produce energy and sugar molecules.3 However, the upward urge turned out to have nothing to do with light.4 If we offer the cells light from the side in the laboratory, they still swim upward during the day, showing that this part of their behavior is guided purely by gravity. But under these artificial conditions, the cells also show a clear light orientation, even though it changes over the course of twenty-four hours. While the cells carefully choose their position in a light gradient during the day (neither too bright nor too dim), they behave like moths at night: they will always swim toward light—even if it is so bright that they die. These experiments showed that the orientation behavior of Gonyaulax consists of two components—one using gravity (gravitaxis), the other using light (phototaxis). Both of these behavioral components are controlled by the cells’ circadian timing system. The phototaxis is “choosy” during the day and mothlike during the night, and the gravitaxis is negative during the day (swimming upward) and positive during the night (sinking). The switch between swimming up and sinking is thrown two hours before the sun sets. But why do the cells sink to such considerable depths?5 It could be exhausting to swim upward, but that is probably the easiest challenge for these little creatures. Although the surface offers a lot of energy in the form of light, the building blocks for making sugar, as well as other nutrients essential for their survival, are practically absent in surface waters.6 Nutrients are released primarily by dead organisms, which are usually heavier than water and, therefore, sink to the bottom or are caught by a thermocline. That is why organisms that need light to photosynthesize but also other nutrients to proliferate face a dilemma. To get everything they need, they often engage in long, vertical journeys in the ocean; and to change their orientation at the right time, they need an internal clock.7
The “decision” to leave the surface toward the evening and wander off to get nutrients is an easy one because photosynthesis doesn’t work in darkness. Deciding when to rise to the surface again while looking for nutrients in the depths of the ocean is more difficult. Let’s assume that a swarm of Gonyaulax has harvested enough energy and sugar during the day at the surface. To proliferate, it needs the additional resources present only at lower depths—so, it sinks. But what happens if it doesn’t find those vital other building blocks? Should the algae stay at depth until they eventually find the necessary goodies? Or should they rise to the surface because they are losing energy during every minute of their search? It is the circadian system of these cells that makes these difficult decisions. Depending on the internal time of day, nutrients such as nitrate will delay the internal clock and thereby prevent the cells from rising. But if a cell hasn’t found nutrients all night and then, at last, encounters a source of them close to or even after dawn, lingering even longer at great depth could be lethal because the cell may run out of energy no matter how many nutrients it might assimilate. So, if nutrients are only found at the end of the night, they do not delay the internal time, and the circadian clock will throw the switch that lets the cells rise back to the surface. Only cells with a precise internal timing system can perform optimally in this game involving space, time, and nutrients, and only these can actually occupy this difficult ecological niche where resources are separated by long distances in addition to being available (as is the case with light) only at certain hours of the day.
To understand the complexity of circadian systems, it is advantageous to monitor more than one “hand” of the internal clock. Recall the results from human bunker experiments in which the activity–rest rhythm adopted a different period from the body temperature rhythm. The internal desynchronization of these two rhythms would not have been discovered if at least two different outputs of the circadian system had not been recorded. In the case of Gonyaulax, the clock was investigated for decades predominantly by recording bio-luminescence. With the discovery of the behavior rhythm, it was possible to do long-term recordings of both rhythms simultaneously. Under certain light conditions in the laboratory, we noticed that the rhythms of bioluminescence and behavior showed internal desynchrony—like some humans did in the Andechs bunker. This result indicates that the circadian system can consist of more than one internal timer, whether in complex creatures like us or in single-cell organisms. In bioluminescent algae, one of them appears to be dedicated to optimizing the cell’s responses to light, and the other seems to be responsible for coordinating the acquisition of nutrients. One of them is linked to photosynthesis and phototaxis, the other to nutrient uptake and vertical migration.
How advantageous it is to have an optimally tuned internal timing system was elegantly shown by Carl Johnson. He performed experiments with an even simpler organism than Gonyaulax, namely the blue-green alga Synechococcus elongatus.8 These very simple single-cell organisms also have an excellent circadian clock. Like Gonyaulax, they get their energy via photosynthesis. Johnson took advantage of mutant strains that show very different free-running periods, one of them much shorter than twenty-four hours and the other much longer. When he cultured populations of these mutants in cycles of twelve hours of light and twelve hours of darkness in separate flasks, each one of them grew at about the same rate. He then mixed the two cultures in one flask so that the two genetically different strains were now competing for the same resources. This permitted him to ask whether one strain would outcompete the other. When he cultured them in constant light, both strains still grew with the same rate, neither outgrowing the other. However, when he grew them in a cycle of ten hours of light and ten hours of darkness (adding up to a twenty-hour day), the short-period mutant outgrew the long-period mutant. When he grew the mixture in a cycle of fourteen hours of light and fourteen hours of darkness (adding up to a twenty-eight-hour day), the long-period mutant won the growth race. Thus, when two strains compete for the same resources, the strain with an internal timing system that is most adapted to its temporal environment has the greatest advantage. Carl Johnson later also tested strains that had a dysfunctional circadian clock and found that they grew even slightly better than all other strains in constant light. In light–dark cycles, however, they didn’t stand a chance against strains with a functional clock. These examples make it quite obvious how advantageous an internal timing system is for organisms that have to cope with a rhythmic environment in which resources are not constantly available.
You may have asked yourself why Gonyaulax cells glow at night. Scientists have thought of several advantages for bioluminescence, especially if the cells produce bright flashes when they are bumped into. Most marine biologists favor the “startle-your-enemy” hypothesis along with the “burglar alarm” hypothesis, presuming that the algae’s enemies don’t like it when they become literally visible to their own enemies by microscopic floodlights. I have an additional explanation that doesn’t contradict the deterrent hypotheses. Many animals use bioluminescence for communicating with other members of their species. Think of fireflies flashing. For organisms that produce offspring by sexual reproduction, it is utterly important either to stay together as a population or to evolve some kind of communication to find others of their kind. Gonyaulax obviously belongs to the former and not the latter group. When they shed their winter coats (cysts) after having spent the cold season wrapped in ocean mud, they go through a transition for sexual reproduction. It is, therefore, imperative that they stay together—a lonesome Gony will not be able to exchange its DNA. The strange, mothlike affinity to light at night, when there is usually only the light they produce themselves, suggests that they may use bioluminescence to stay together.
The American clock researcher Mary Harrington was so taken by these algae and their temporal ecology that she wrote a poem about the clock-controlled life of Gonyaulax polyedra.9 It is th
e only poem that has been published to date in the Journal of Biological Rhythms and perhaps the only poem ever published in an otherwise purely scientific journal.
FEEDBACK*
If the lazy dinoflagellate
should lay abed
refuse to photosynthesize,
realize:
the clock will not slow
but it will grow faint
weaker
weaker
barely whispering at the end
“rise”
“rise”
to little effect.
The recalcitrant Gonyaulax
arms crossed
snorts
“No longer will
they call my life
(my life!)
‘just hands’.
I am sticking to the sea bed!”
* After reading Roenneberg T, Merrow M (1999) Circadian systems and metabolism. J Biol Rhythms 14:449–459.
11
Wait until Dark
Someone always tended the fire in the center of the great cave. The clan had some kind of arrangement as to whose turn it was to watch the fire, but these arrangements were only for emergencies—just in the rare case that nobody was awake. Normally, someone would be awake at all times during the night and would come to sit around the fire to chat or just add some wood. No one was able to sleep through the entire stretch of a night’s darkness, except for the few short midsummer nights. Most members of the clan retired shortly after dusk: some earlier, some later—the youngest adults usually were the last to go.
Mrk, the clan’s chief, had gone to his small, private side cave around dusk and had fallen asleep immediately. After some time he woke up, but not fully—entering a state between sleep and wakefulness. The clan’s storyteller had once told him that this was the time when he developed his best tales. He claimed that, during these half-awake spells, he was able to see into worlds much stranger than their own. After lying in the dark half-conscious for a while, Mrk went back to a deep sleep, only to wake up later—this time fully. He got up and joined other clan members who sat around the fire in the big cave. The older Mrk got, the longer he found himself sitting around the fire. He had woken up during the night all his life but usually felt tired after a short while and spent the rest of the night sleeping on his mat.
As Mrk watched the dancing flames, his thoughts wandered off to the dark forest. While they were safe in the cave labyrinth, Urf, the man of his daughter and the current leader of the night-hunters, was out in the dark forest together with three others. Around sunrise, the night-hunters returned from their outing with their prey. The older members of the clan were already up and started to cut the large prey into smaller parts with handheld polished stone axes and flint knives while the hunters lay down to recover their lost sleep.
In this chapter, we return to my favorite animal—our own species. I promised in the introduction that the facts concerning the internal timing system underlying all stories in this book were sound. With regard to the preceding narrative, however, I hope you won’t mind my taking a few creative liberties concerning the history of human life in the Stone Age. My aim is to take you back to our not-too-ancient history and try to imagine what life was like when humans were almost completely dependent on night and day, dark and light, cold and warm.
While writing about the Stone Age, I found myself using, and then rejecting, expressions like “several hours later.” The concept of hours is of course inappropriate for that era, but it’s an issue in our era, too. Not so long ago I was approached by a younger colleague, who inquired whether we had developed a different chronotype questionnaire for the “third world.”1 His girlfriend was researching human behavior in Madagascan villages that have no contact with modern civilization. Thus, asking inhabitants at what “time” they went to bed or got up was pretty useless. So far we haven’t produced a chronotype questionnaire for these populations because it is difficult to exchange the useful time conventions of hours and minutes that we are so used to with another, equally measurable time frame. Sunrise, sunset, and possibly midday are natural markers for time of day. But in order to develop a finer time frame by using references from the environment, we would need to understand the daily routines of the population under investigation. Are there natural time markers, such as the appearance of birds, the opening and closing of flowers, shadows (cast by mountains), or specific odors during the night?2
How did our present-day culture of sleeping develop over the course of our evolution? Few animals actually sleep and are awake in a consolidated way over long stretches of time—many of them are episodic sleepers. Although they do sleep more at night than during the day (if they are day-active creatures), they tend to sleep whenever they have nothing to do (hunt, graze, or whatever). The description of humans gathering around the fire at night is not my ad hoc invention. Anthropologists and human ethologists reported this nocturnal behavior after returning from expeditions to populations not in contact with modern civilization.3 Nights are usually much longer than we require for sleep. Near the equator, nights are about twelve hours long throughout the year. The farther we travel from the equator, the shorter the summer nights and the longer the winter ones. What did our ancestors do in winter when they had no light to fake a longer day? Even before the invention of the light bulb, light was commonly available at night. Night lights existed from the moment we were able to manage fire in a small container or in the form of a lit candle or torch. In a way, the central fire in the great cave was the beginning of light at night.
But even now that we have become completely independent of the night’s darkness, we sleep and are awake for very long stretches of time—on average, eight and sixteen hours, respectively. We have already covered the main factors that determine when we fall asleep: internal timing and the amount of sleep pressure we have built up over the time we are awake. The largest decrease of this sleep pressure occurs during the first half of our sleep, so that we are relatively close to the wake-up threshold throughout the second half. We know from experience that the closer we are to our usual end of sleep when we wake up, the harder it is to fall asleep again. Charles A. Czeisler, a clock and sleep researcher at Harvard University, developed a theory about why we are able to sleep and be awake for such relatively long stretches of time. Alertness and sleepiness are controlled by centers in our brain, which obviously have to be able to record how long we have been awake. They also receive an input from the SCN to incorporate internal time. There is, however, another factor that has an impact on how sleepy we feel: our body temperature, specifically, the temperature of our brain.4 Our wakefulness is highest in a narrow temperature range around 37°C. We get very sleepy when we have a fever, and reports of polar expeditions state that freezing to death resembles falling asleep. We feel tired when our brain cools down, and we feel awake when our brain warms up (if it doesn’t become too hot). Czeisler’s hypothesis is based on the fact that our body temperature reaches an all-day low during the second half of our sleep and thereby enables us to continue sleeping for another couple of hours despite most of our sleep pressure having been relieved.
This hypothesis could explain why we are able to sleep for such a long time, but we still need an explanation for why we can stay awake for an even longer stretch. While the first half of sleep is the most effective in reducing our sleep pressure, we build up most of our sleep pressure during the first half of our wake period, so that we are already quite sleepy around lunchtime—even if we don’t eat a midday meal (if we do, the lunchtime dip is even deeper). Depending on how well and how long we slept during the preceding night, we can either fight this lunchtime dip or, if we cannot muster any resistance, doze off—at least for a power nap. Light helps to win the battle for wakefulness while darkness fights with great success on the other side. I have often witnessed colleagues dozing off into a deep sleep in the middle of an interesting lunchtime seminar, especially in former days when the seminar room had to be sufficientl
y dark to see the slides projected by an old-fashioned slide projector. Once we have survived this lunchtime dip, the likelihood that we will fall asleep declines again. Czeisler argues that this is because the body clock cranks up our body temperature again. According to his theory our consolidated sleep and wake times are supported by the circadian temperature rhythm, making us colder in the second half of the night and making us warmer in the second half of the day.
Mediterranean culture has developed the nap into a full-blown siesta. The mechanisms behind this second daily sleep episode involve heat, darkness, and nocturnal sleep deprivation. In the Mediterranean summer, it is too hot for farmers to work outside for many hours around midday. The amount of work per day is, however, the same compared to that of farmers living in more temperate regions who can work throughout the entire day—except perhaps on some exceptional days during the summer. The quandary of the Mediterranean farmer was solved by starting to work very early in the morning and working until very late at night, but not around the hottest hours of the day. Starting early and finishing late shortens sleep at night, leading to considerable sleep pressure during the day. The most natural reaction to the heat of the midday sun is to go into a cool place, which was always a dark space before the use of air conditioners. The combination of accumulated sleep pressure and darkness can easily induce sleep, especially if we lie down at a time when most of us experience a lunchtime dip.
Internal Time: Chronotypes, Social Jet Lag, and Why You’re So Tired Page 9