Environmental Influences on Biological Rhythms
LECTION 3.
Chronobiology: An Internal Clock for All Seasons
Living organisms exhibit myriad cycles. Annually, the leaves of deciduous trees in the temperate zones turn brilliant hues of yellow, orange, and red as the days shorten and winter approaches. Each year, animals go through cycles related to reproduction; most of those in the temperate zones also experience rhythms that prepare them for the period of inactivity that comes with winter.
Cycles that take less than a year to complete are also plentiful. Daily rhythms include the folding and unfolding of the leaves of certain plants, such as the “sensitive plant” (Mimosa pudicd) and the tamarind tree (Tamarindus indicus), and the rise and fall of the body temperature of animals (including humans). Numerous organisms inhabiting the earth’s tidal zones, from plankton and diatoms to crabs and seabirds, exhibit cycles of physical and behavioral change ranging from 12 hours to two weeks to a month in length, matching the complex, interacting effects of the sun and the moon on the tides. In fact, even cells exhibit some type of periodicity in their activities, often in cycles lasting fractions of a second.
The importance of rhythms in nature has been appreciated for thousands of years: people plant their crops in tune with the cycle of the seasons and eat and sleep according to the daily rise and fall of the sun. Indeed, so familiar are these rhythms that, according to pharmacologists Joseph S. Takahashi and Martin Zatz, Laboratory of Clinical Science, National Institute of Mental Health, Bethesda, Maryland, they did not elicit systematic, scholarly investigation until the 1700s. Since that time, however, the study of these biological rhythms has slowly coalesced into the science of chronobiology.
Some of the foundations of chronobiology were laid in the 1930s. But as the first part of this essay shows, activity in this Field remained fairly constant at a relatively low level until the 1950s and 1960s. Since then, according to a review by Alain Reinberg, director of research, National Center of Scientific Research, Paris, France, and Michael H. Smolensky, associate professor of environmental sciences, University of Texas Health Sciences Center, Houston, chronobiology has been an active, rapidly growing, multidisciplinary field. The second part of this essay focuses on the latest research in this dynamic science.
Biological Rhythms and Their Significance
A vast array of periodicities in functions or activities are exhibited by virtually every organism, from single-celled plants and animals to such complex creatures as human beings.8 These rhythms are intrinsic to the organism and enable it to measure the passage of time. For many organisms, the most important interval measured by their internal clocks is the 24-hour cycle of light and dark. Rhythms that coincide with this cycle are called “circadian,” from the Latin circa (about) and dies (day).
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Other important biological periodicities include “circatidal” rhythms, matching the period of daily high and low tides, and “circasyzygic” rhythms, which match the cycle of unusually high and low tides occurring each fortnight, when the sun and moon are in the proper alignment. “Circalunar” rhythms are synchronized with the monthly waxing and waning of the moon. “Circannual” periodicities are cycles of about a year. It should be noted, however, that circannual rhythms are not the end of the story; for example, the 7-year and 17-year locusts that emerge from their long pupal incubation in the ground are cycles that span longer periods.
An innate ability to measure the passage of time has adaptive significance. A sense of time helps birds to accurately use the sun, moon, and stars as navigational aids during migration. Internal clocks also enable organisms to synchronize their breeding behaviors with one another as well as with the most favorable environmental conditions for raising young. In fact, biological rhythms help organisms match a number of activities to the times when those activities can be carried out most effectively. For example, as noted by zoologist David S. Saunders, University of Edinburgh, Scotland, circadian rhythms allow animals of different species to share the same food sources without direct competition because some animals are active only during hours of darkness (i.e., they are nocturnal) while others are active only during the day (diurnal). The advantage to having a built-in method of responding to light and darkness, rather than relying on actual changes in light as a cue, is that, in effect, the organism is prevented from “sleeping late” and missing the optimal time of day for foraging.
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Environmental Influences on Biological Rhythms
For centuries it was believed that biological periodicities were caused by the environmental rhythms with which they were synchronized.6 But in 1729 French astronomer Jean Jacques d’Ortous de Mairan (1678-1771) conducted an experiment showing that, even in total darkness, the leaves of a “sensitive heliotropic plant”—probably Mimosa pudica1— continue to fold and unfold in a 24-hour cycle that was previously thought to be in response to daylight.
The idea that the circadian movements of plants are independent of the daily light-dark cycle was confirmed by a series of experiments performed by the German botanist, Wilhelm F.P. Pfeffer (1845-1920), in the late 1800s and early 1900s. As Reinberg and Smolensky note, however, it was not until the 1950s “that Pfeffer’s findings were clearly understood and appreciated.”
It was another German botanist, Erwin Bünning, University of Tübingen, who first conclusively established the accepted foundations of chronobiology: that organisms use their biological rhythms to measure the passage of time and that these rhythms are inherent to the organism. Bünning proved the genetic origin of biological rhythms in the mid-1930s while working at the Botanical Institute of the University of Jena. He found that circadian rhythms persisted in the bean plant Phaseolus and the fruit fly Drosophila, even though generation after generation had been raised in environments completely lacking cues to the passage of time. The 1936 paper on fruit flies has been cited over 180 times, according to the Science Citation Index® (SCI®).
Bünning’s work with Drosophila eventually led him to conclude that the fruit fly “knew” when to emerge from the pupal stage of its development because its circadian rhythm had cycled a given number of times, indicating that a season had passed.
His work has been extensively cited. A definitive, German-language edition of Bünning’s work in this area, entitled Die physiologische Uhr (The Physiological Clock), was originally published in 1958 and reprinted in 1963.
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Although biological rhythms are innate, they nevertheless function to keep organisms in tune with their environment and are thus responsive to various environmental, or exogenous, cues. In 1954 Jürgen Aschoff, professor of physiology and director, Max Planck Institute for Behavioral Physiology, Seewiesen über Starnberg, Federal Republic of Germany, and Franz Halberg, University of Minnesota Medical School, Minneapolis, and Cambridge State School and Hospital, Minnesota, and colleagues independently and almost simultaneously developed an explanation of the role that environmental factors play in the functioning of internal clocks.
These environmental factors—such as light and dark, ambient temperature, noise, and even interactions with other members of the same species—act to keep biological cycles in phase with periodic fluctuations in the environment. In the absence of such cues (which occurs when plants and animals are removed to controlled laboratory conditions), the cycles continue but begin to drift out of phase with clock time and become ‘ ‘free-running. ’ ’ Within their own free-running cycles, though, they are remarkably resistant to perturbation.6 In fact, several studies by Aschoff demonstrated that, beyond certain narrow limits, the presence or lack of environmental cues has no effect on biological rhythms.
To describe the environmental cues from which biological rhythms are derived, Aschoff coined the word “Zeitgeber,” meaning “time giver.” Colin S. Pittendrigh, Stanford University, California, later introduced the term “entraining agent”; still later, Halberg and colleagues proposed the word “synchronizer.” Although these authors each give a somewhat different definition of their terms, it has become common practice in the field to use them interchangeably.
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