Basic Processes

Environment, Endogenesis, Entrainment

The matching of the cycle duration of some environmental cycles with that of some biological rhythms might suggest that biological rhythms are mere responses of organisms to the rhythmicity oftheir abiotic environment. Extensive research has clearly established, however, that the relationship between environmental cycles and biological rhythms is much more complex. In some cases, biological rhythms are indeed mere responses to environmental cycles. An example is the tidal rhythm of burrowing in some (but not all) species of crabs. In other cases, biological rhythmicity is endogenously generated and does not respond to environmental cycles. An example is heart beating: the rhythmic activity is endogenously generated by the cardiac pacemaker, which can be modulated by sympathetic and parasympathetic stimulation but is not synchronized by natural environmental cycles. Finally, in some cases, biological rhythmicity is endogen-ously generated and this rhythmicity is modulated (entrained) by environmental cycles. The best-known example is the entrainment of circadian rhythms by the regular alternation of day and night (i.e., the alternation of light and darkness).

In strict sense, only rhythms that are endogenously generated and that can be entrained should receive the circa designation. Laboratory research has documented only four classes of circa rhythms: circatidal, circadian, circalunar, and circannual rhythms. If a given variable does not exhibit circa rhythmicity, or has not been proved to exhibit it, it should be named without the circa designation. Tidal, lunar, and annual are commonly used descriptors. Dian is never used; instead, daily is recommended - although diel and nycthemeral are also used.

It should be pointed out that observation of rhythmic behavior in a natural environment is necessarily insufficient to characterize the nature of the rhythmicity. Whenever a new rhythmic pattern is observed, controlled laboratory investigation is necessary to attribute the rhythmicity to environment, endogenesis, or entrainment. Accurate identification of the modality of rhythmicity is essential for the understanding of ecological and evolutionary significance of the observed rhythmic process.

Rhythmic Variables

Different types of biological rhythmicity may affect the regulation of one or more physiological or behavioral variables. Estrous rhythmicity in rodents, for example, has been shown to affect at least hormonal secretion, behavioral sexual receptivity, the pattern of vaginal discharges, and the amount and temporal organization of locomotor activity. Circadian rhythmicity has been shown to affect locomotor activity, eating and drinking, excretion, learning capability, heart rate, blood pressure, body temperature, hormone secretion, sexual activity, parturition, suicide, susceptibility to heart attack, and many other variables. It is still unclear which of these multiple rhythmic variables are controlled directly by the circadian pacemaker and which are simply caused (masked) by the rhythmicity of variables controlled by the pacemaker. It has been demonstrated that the circadian rhythm of body temperature is not caused by the rhythm of locomotor activity, whereas the rhythm of urea secretion is simply a consequence of the rhythm of food ingestion, but generally very little is known about the inter-relationships among the various rhythms.

Entraining Agents

The circa rhythms can, by definition, be entrained by environmental cycles. Circatidal rhythms are often entrained by the cycle ofinundation, whereas circannual rhythms are often entrained by the seasonal variation in photoperiod (i.e., the fraction of daylight in a day). Circadian rhythms are strongly entrained by the light-dark cycle and less strongly by daily variations in ambient temperature, food availability, and physical exercise. Many environmental cycles that may not entrain a rhythm can nevertheless mask it.

Substrates

Circadian rhythms have been demonstrated in almost ever species ever tested, from bacteria to humans. Although transcriptional/translational loops seem to underlie the intracellular process of generation of circa-dian rhythmicity in all organisms, the specific genes involved are not conserved across domains, kingdoms, or phyla. At the systems level, likewise, the pacemaking structures and the sensory receptors necessary for entrainment vary with the complexity of the organism. In mammals, a major circadian pacemaker is located in the suprachiasmatic nucleus (SCN), a small nucleus in the ventral hypothalamus composed of several thousand neurons. Each neuron in the SCN is an autonomous pacemaker, and the various cells are synchronized mainly through synaptic communication.

The mammalian circadian system relies exclusively on the eyes to acquire photic information necessary for entrainment, although other vertebrates and invertebrates possess a variety of additional photosensitive structures. Both classic photoreceptors (rods and cones) and photo-responsive ganglion cells in the retina of the eyes provide photic information to the mammalian circadian system. Very little is known about how the circadian pacemaker acquires the information about temperature and nutritional state that is needed for nonphotic entrainment. Temperature signals are available from cold- and warmsensitive cells on the skin and in the body core. Hunger and satiety signals are available from the blood concentration of nutrients, taste and smell of the food being ingested, gastric distension, gastric contents, and blood levels of various hormones secreted by the stomach, by the intestines, and by fat cells.

The efferent pathways responsible for communication of circadian rhythmicity to the various organs are not well known but seem to involve neural as well as humoral mechanisms. One mammalian efferent pathway has been described in detail: the control of rhythmic melatonin secretion by the pineal gland is achieved through a tortuous pathway from the SCN to the paraventricular nucleus of the hypothalamus, to the intermediolateral column of the thoracic spinal cord, to the superior cervical sympathetic ganglion, and finally to the pineal gland.

Ecological Aspects

Evolutionary Advantage

Because extant bacteria exhibit circadian rhythmicity, it is usually assumed that endogenous rhythmicity was present already in the earliest life forms and was retained in all divergent branches along the evolutionary tree. In the absence of fossil evidence, however, it is equally possible that circadian rhythmicity evolved de novo multiple times in various taxonomic groups. Early life forms exposed to sunlight had to deal with the conflict between obtaining life-sustaining energy from solar radiation and being damaged by the Sun's strong ultraviolet emissions. Resolution of this conflict - in the form of daily vertical migration in the ocean - may have been the driving force for the evolution of circadian rhythmicity.

In general terms, it is often assumed that endogenous rhythmicity evolved as a mechanism that allowed organisms to prepare for predictable daily changes in the environment. For instance, photosynthetic plants could wait for sunlight each day, but those with an innate mechanism capable of anticipating sunrise would get an early start by initiating preparatory adjustments during the last part of the night. Similarly, nocturnal rodents could wait for the darkness of the night before getting ready to leave their burrows, but those with an innate mechanism capable of anticipating sunset would prepare in advance for the rigors of foraging. On a limited scale, experimental research has demonstrated enhanced reproductive fitness or survival in normal organisms as compared to organisms with deficient circadian systems.

Diurnality and Nocturnality Phenomenology

Perhaps the most fundamental ecological issue in circa-dian physiology is an organism's adoption of a nocturnal niche or a diurnal niche. Evolutionarily, it is not certain whether the choice of a temporal niche was relevant to early life forms. If the first organisms were photoauto-trophic and relied on energy from the Sun, then the choice of a diurnal niche would certainly have been important. However, if the first organisms were chemoau-totrophic and relied on geothermal energy from deep-ocean vents, then the alternation of day and night on Earth's surface would have been of very little importance. Millions of years later, when living beings - particularly heterotrophic ones, such as animals - abandoned the ocean and colonized terrestrial environments, the choice of a nocturnal niche was probably necessary as a means of preventing desiccation. Thus, invasion of the diurnal niche likely became possible only after the evolution of integuments capable of preventing water loss.

Although many organisms today can be classified as either nocturnal (night-active) or diurnal (day-active), many others defy classification. Representative activity records for five mammalian species are shown in Figure 1. Under a light-dark cycle with 12 h of light and 12 h of darkness per day, Syrian hamsters (Mesocricetus auratus) are exclusively nocturnal. Domestic mice (Mus musculus) are predominantly nocturnal, but their active phase is quite long and extends slightly into the light portion of the light-dark cycle. Rabbits (Oryctolagus cuniculus) are not clearly nocturnal or diurnal. Horses (Equus caballus) are predominantly diurnal but have a long active phase that extends into the dark portion of the light-dark cycle. Finally, Nile grass rats (Arvicanthis niloticus) are almost exclusively diurnal.

A laboratory study involving seven species of small rodents revealed a gradient of temporal niches running from predominantly diurnal species to predominantly nocturnal species with many chronotypes in between, including species exhibiting wide intraspecies gradients of temporal niche (Figure 2). Domestic mice (Mus mus-culus), laboratory rats (Rattus norvegicus), Syrian hamsters

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Figure 1 Representative activity records of five mammalian species. In all cases, data were collected in a controlled laboratory environment where the light-dark cycle (indicated by the hatched and clear boxes) was the only prominent 24-h environmental cycle. The ordinates in each graph are set in arbitrary units to facilitate comparison between different species. Notice the differences in diurnality/nocturnality among the five species. Original figure from data collected in the laboratories of the author and his research collaborators.

Figure 1 Representative activity records of five mammalian species. In all cases, data were collected in a controlled laboratory environment where the light-dark cycle (indicated by the hatched and clear boxes) was the only prominent 24-h environmental cycle. The ordinates in each graph are set in arbitrary units to facilitate comparison between different species. Notice the differences in diurnality/nocturnality among the five species. Original figure from data collected in the laboratories of the author and his research collaborators.

Grass rat Gerbil-D Degu-D Gerbil-N Degu-N Rat Siberian Mouse Syrian

Diurnality index

Figure 2 Mean diurnality scores of nine groups of small rodents. The diurnality score was computed as the ratio of the number of activity-wheel revolutions during the light portion of the light-dark cycle and the number of wheel revolutions during the whole day, so that larger scores reflect greater diurnality. The dashed line indicates the theoretical separation between nocturnal and diurnal animals (i.e., equal amounts of activity during the light and dark portions of the light-dark cycle). Notice the gradient from predominant nocturnality to predominant diurnality. Adapted from Refinetti R (2006) Variability of diurnality in laboratory rodents. Journal of Comparative Physiology A 192: 701-714.

Diurnality index

Figure 2 Mean diurnality scores of nine groups of small rodents. The diurnality score was computed as the ratio of the number of activity-wheel revolutions during the light portion of the light-dark cycle and the number of wheel revolutions during the whole day, so that larger scores reflect greater diurnality. The dashed line indicates the theoretical separation between nocturnal and diurnal animals (i.e., equal amounts of activity during the light and dark portions of the light-dark cycle). Notice the gradient from predominant nocturnality to predominant diurnality. Adapted from Refinetti R (2006) Variability of diurnality in laboratory rodents. Journal of Comparative Physiology A 192: 701-714.

(Mesocricetus auratus), and Siberian hamsters (Phodopus sungorus) were found to be predominantly nocturnal, with small intra- and interspecies variability. Nile grass rats (Arvicanthis niloticus) were found to be predominantly diurnal, again with small intraspecies variability. Curiously, degus (Octodon degus) and Mongolian gerbils (Meriones unguiculatus) were found to be naturally distributed into two distinct groups - one predominantly diurnal and one predominantly nocturnal - so that a downward gradient of diurnality was observed from Mongolian gerbils classified as diurnal, degus classified as diurnal, gerbils classified as nocturnal, and degus classified as nocturnal.

Great intraspecies variability in diurnality, with some individuals showing predominantly diurnal activity patterns and others showing predominantly nocturnal activity patterns, has been described in other species as well. In goldfish (Carassius auratus), about 80% of individuals tested in the laboratory were found to be diurnal, whereas 10% were nocturnal, and 10% displayed very weak rhythmicity. In carpenter ants (Camponotus compres-sus), approximately 70% of individually tested animals were found to be nocturnal, whereas 30% were diurnal. Likewise, in subterranean mole-rats of various species, some members of the species were found to be diurnal and some were found to be nocturnal. Even some instances of intraindividual variability (i.e., the same individual being diurnal under some circumstances and nocturnal under other circumstances) have been reported. For instance, wolves (Canis lupus) are normally nocturnal; however, when traveling over long distances, they travel during the day. Conversely, migratory birds are normally diurnal, but they do most of their migratory flight at night.

Some authors have used the term cathemerality to refer to activity patterns that are not clearly diurnal or nocturnal. It has been suggested that cathemerality (lack of circadian rhythmicity) may be an adaptive feature that allows animals to optimally exploit the available resources without the temporal restrictions imposed by circadian rhythms. Of course, this reasoning is the very opposite of that used to explain the existence of circadian rhythmicity, but it is not absurd to assume that circadian rhythmicity provided selective advantage to some species and not to others.

Causality

Very little is known about the causes of temporal niche selection beyond the obvious fact that some species inherit a diurnal preference while others inherit a nocturnal preference or no preference at all. In animals, eyes specialized for day vision (i.e., eyes possessing retinal cones in addition to retinal rods) evidently facilitate adaptation to a diurnal niche, but image-forming photo-reception is not essential for circadian entrainment because the photosensitive ganglion cells can provide sufficient photic input to the SCN. Researchers who have tried to identify the mechanisms responsible for diurnality or nocturnality have generally found that there is no clear difference between diurnal and nocturnal organisms except for the obvious difference in the phase angles of entrainment - that is, diurnal animals are diurnal because they are active during the day, and nocturnal animals are nocturnal because they are active at night.

Although we do not know why diurnal organisms differ from nocturnal ones, we do know that temporal niche selection depends on the interplay of two basic mechanisms: entrainment and masking. Entrainment results from the resetting of the pacemaker by photic stimulation at the appropriate time of the circadian cycle, whereas masking refers to the inhibition (negative masking) or disinhibition (positive masking) of behavioral activity without a direct effect on the pacemaker. Resetting of the pacemaker follows species-specific phase-response curves that do not differ between diurnal and nocturnal organisms except for the fact that diurnal organisms are responsive to light during their inactive phase, whereas nocturnal organisms are responsive to light during their active phase (i.e., both diurnal and nocturnal organisms are responsive to light at night). Similarly, the masking effects of light are equivalent in diurnal and nocturnal organisms except that light generally causes positive masking in diurnal organisms and negative masking in nocturnal organisms.

Naturally, entrainment and masking need not be restricted to photic stimuli. Outside the controlled conditions of the laboratory, organisms are subject not only to a light-dark cycle but also to rhythmic and nonrhythmic variations in food availability, ambient temperature, and intra- and interspecies competition. One case of interspe-cies competition that has been relatively well studied is that involving mice of the genus Acomys. In natural settings in rocky deserts of the Middle East, common spiny mice (A. cahirinus) share a foraging microhabitat with golden spiny mice (A. russatus). Normally, common spiny mice are nocturnal, whereas golden spiny mice are diurnal. However, if the common spiny mice are removed from the area, the golden spiny mice become nocturnal. This suggests that the golden spiny mice are normally forced into the diurnal niche by the competition for resources. Indeed, when golden spiny mice are trapped in the field and immediately tested individually in the laboratory, they exhibit a nocturnal pattern of activity. Thus, the phase reversal in spiny mice is quite interesting from an ecological point of view. It shows how masking mechanisms may supplant entrainment mechanisms in the determination of the temporal niche of species in the wild.

Seasonal Adjustments

Much research has dealt with the interaction between annual rhythms and circadian rhythms. Except at the equator, nights are longer in the winter and shorter in the summer, and it is well known that this seasonal variation in photoperiod causes a temporal compression or expansion of circadian rhythms. The phenomenon has been observed in natural settings (where the change in photoperiod is accompanied by changes in temperature and food availability) as well as in the laboratory (where only the photoperiod is changed). An example of expansion of the active phase (a) of a mouse under long nights in the laboratory is shown in Figure 3. Notice that the expansion of a is accompanied by a reduction in exertion at each time point, so that the overall amount of activity (number of wheel revolutions, in this case) is conserved. As it would be expected, a is expanded under long nights in nocturnal organisms but under long days in diurnal organisms. As a rule, wintertime is associated

Days

Figure 3 Three-day segments of the records of running-wheel activity of a domestic mouse housed in the laboratory under a light-dark cycle with 8 h of darkness per day (top) or 16 h of darkness per day (bottom). The white and black horizontal bars denote the light and dark portions of the light-dark cycle, respectively. Notice that the active phase of the activity rhythm is longer when the nights are longer. Original figure from data collected in the author's laboratory.

Days

Figure 3 Three-day segments of the records of running-wheel activity of a domestic mouse housed in the laboratory under a light-dark cycle with 8 h of darkness per day (top) or 16 h of darkness per day (bottom). The white and black horizontal bars denote the light and dark portions of the light-dark cycle, respectively. Notice that the active phase of the activity rhythm is longer when the nights are longer. Original figure from data collected in the author's laboratory.

with rhythm compression in diurnal animals and rhythm expansion in nocturnal animals, whereas summertime is associated with rhythm expansion in diurnal animals and rhythm compression in nocturnal animals. A full-year record of feeding activity of a mouflon sheep ( Ovis musimon) housed outdoors in Germany is shown in Figure 4. This diurnal animal spent many more hours grazing during the summer than during the winter.

Seasonal variations have also been documented in other parameters of circadian rhythms, such as phase, amplitude, and period. An interesting seasonal modulation of rhythm amplitude is observed in beavers (Castor canadensis). During the winter, in Canada and northern United States, beavers remain essentially sequestered in their lodges or underneath the ice cover, so that their daily rhythm of activity is almost flat, whereas robust rhythmicity is present in the summer.

Figure 4 The daily feeding rhythm of a mouflon sheep (Ovis musimon) maintained outdoors in Germany for a full year. Notice the gradual contraction - and later expansion - of the feeding rhythm as the days become shorter in the winter - and longer again in the summer. Adapted from Berger A, Scheibe KM, Michaelis S, and Streich WJ (2003) Evaluation of living conditions of free-ranging animals by automated chronobiological analysis of behavior. Behavior Research Methods, Instruments, and Computers 35: 458-466.

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Figure 4 The daily feeding rhythm of a mouflon sheep (Ovis musimon) maintained outdoors in Germany for a full year. Notice the gradual contraction - and later expansion - of the feeding rhythm as the days become shorter in the winter - and longer again in the summer. Adapted from Berger A, Scheibe KM, Michaelis S, and Streich WJ (2003) Evaluation of living conditions of free-ranging animals by automated chronobiological analysis of behavior. Behavior Research Methods, Instruments, and Computers 35: 458-466.

The interaction between annual and circadian rhythms occurs also in the opposite direction, as circadian rhythmicity can affect annual rhythms. Perhaps the best example of this interaction is the circadian modulation of entry into and arousal from hibernation. Studies conducted on several species of squirrels and hamsters have generally shown that entry into torpor is restricted to a narrow segment of the day (and, therefore, is modulated by the circadian system), although there is disagreement about the circadian modulation of arousal. Figure 5 shows the results of a study conducted on European hamsters (Cricetus cricetus). The animals were kept in the laboratory under simulated winter conditions of short photoperiod (8 h of light per day) and low ambient temperature (8 ° C). Each dot in the figure corresponds to an episode of entry into or arousal from a deep hibernation bout. Although the temporal distribution of entries into torpor is not very tight, almost all entries occurred between 18.00 and 06.00. Arousals from torpor were scattered all over the day in this study. Some investigators have found that arousal from hibernation is restricted to a narrow segment of the day (and, therefore, is modulated by the circadian system), whereas others have not. Because the conflicting findings have been obtained in different species, they may be explained by species differences. The central question is whether the circadian system

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Figure 5 Distributions of the times of entry into and arousal from deep hibernation bouts of eight European hamsters (Cricetus cricetus) maintained in the laboratory under simulated winter conditions (80C, 8 h of light per day). Notice that the distribution for entry into torpor is clustered around the late evening and early morning. Adapted from WaBmer T and Wollnik F (1997) Timing of torpor bouts during hibernation in European hamsters. Journal of Comparative Physiology B 167: 270-279.

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Figure 5 Distributions of the times of entry into and arousal from deep hibernation bouts of eight European hamsters (Cricetus cricetus) maintained in the laboratory under simulated winter conditions (80C, 8 h of light per day). Notice that the distribution for entry into torpor is clustered around the late evening and early morning. Adapted from WaBmer T and Wollnik F (1997) Timing of torpor bouts during hibernation in European hamsters. Journal of Comparative Physiology B 167: 270-279.

remains functional during hibernation, as a functional clock is required for the timing of arousal. Some researchers have observed circadian rhythmicity of body temperature (with very small amplitude) during hibernation, whereas others have not. A study of metabolic activity of various brain areas identified high activity in the site of the master circadian pacemaker (SCN) during hibernation, which constitutes evidence that the circadian system remains functional during the maintenance stage of hibernation.

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