For centuries it was believed that biological periodicities were cuused 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 (p. 5) —-continue to fold and unfold in a 24-hour cycle that was previously thought to be in response to daylight. 10
The idea that the circadian movements of plants are indepmdent of the daily light-dark cycle was confirmed by a series of experiments performed by the Oerman botanist, Wilhelm F.P. Pfeffer (1845-1920),6,11 (p. 61-2) in the late 1800s12 and early 1900s.13 As Reinberg and Smolensky note, however, it was not until the 1950s “that Pfeffer’s findings were clearly understood and appreciated.”6
It was another Oerman botanist, Erwin Bihming, University of Ttibingen, 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. Bunning 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 Phaseolus14 and the fruit fly Drosophila, 15 even though generation after generation had been raised in environments completely lacking cues to the passage of time.6,11 (p. 146-8) The 1936 paper on fruit flies has been cited over 180 times, according to the Science Citation Index (SCI). A Citation Classic, 16 it is the most-cited paper ever published by Berichte der Deutschen Botanischen Gesellschaft, the journal of the German Society of Botanists. Bunning’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 Bunning’s work in this area, entitled Die physiologische Uhr (The Physiological Clock), 17 was originally published in 1958 and reprinted in 1963. Using the 1955-1964 SCI, 18 we determined that the former has received about 100 citations. The reprint has been cited at least 120 times. An English translation appeared in 196419 and has been reprinted twice since then. The various editions have been explicitly cited in almost 700 publications, making The Physiological Clock a Citation Classic.20
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 Jurgen Aschoff, professor of physiology and director, Max Planck Institute for Behavioral Physiology, Seewiesen uber Starnberg, Federal Republic of Gemany,21 and Franz Halberg, University of Minnesota Medical School, Minneapolis, and Cambridge State School and Hospital, Minnesota, and colleagues22 independently and almost simultaneously developed an explanation of the role that environmental factors play in the functioning of internal clocks.6
These environmentai factors -- such as light and dark, ambient temperature, noise, and even interactions with other members of the same species6 -- act to keep biological cycles in phase with periodic fluctuations in the environment. in the absence of such cues (which owurs when plants and anirnais 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.23-25 One of these papers, entitled’ ‘Exogenous and endogenous components in circadian rhythms,’ “24 is Aschoff’s most-cited paper; published in 1960, this Citation Classic has been cited over 470 times.
To describe the environmental cues from which biological rhythms are derived, Aschoff coined the word ‘‘Zeitgeber, ” meaning “time giver. “21 Colin S. Pittendrigh, Stanford University, California, later introduced the term “entraining agent” ;26 still later, Halberg and colleagues proposed the word “synchronizer.’ ’27 Although these authors each give a somewhat different definition of their terms, it has become common practice in the field to use them interchangeably.6
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