Circadian Surfaces and the Diversity of Possible Roles of Circadian Organization in Photoperiodic Induction

Abstract

It is an established fact that circadian rhythmicity is often somehow involved in the physiology of photoperiodic induction. It is shown, however, that there are three possible ways in which such rhythmicity could be involved. For the most part available data are inadequate to discriminate among these three roles, only one of which is covered by "Binning's Hypothesis." Emphasis is given to a previously ignored possibility in which circadian organization is involved in photoperiodism-but not as the clock responsible for the time-measurement. The meaning of circadian surfaces and their bearing on the interpretation of a widely used experimental protocol is developed.The switch from one seasonally appropriate metabolic strategy to another-such as from vegetative growth to flowering, or normal development to developmental arrest (diapause)-is controlled in a great variety of multicellular organisms by the relative duration of light and dark in the daily periodicity of environment: such switches are said to be photoperiodically controlled. This phenomenon of photoperiodism implies that in some sense the organism measures time (the duration of darkness or light), and in recent years it has become fashionable to state the central issue as the nature of the "clock" that effects the photoperiodic time mesurement. The major debate for two decades has been whether the clock that effects the photoperiodic time measured is some sort of "hourglass" or a circadian oscillation of the type known to be utilized as the chronometer used in time-compensated sun orientation and other instances where organisms identify phases of the daily cycle of the external world.The debate is currently in a confusing state in several respects, the full extent of which lies beyond the scope of this brief theoretical note that intends only: (i) to state some general aspects of the complexities not made sufficiently explicit in current discussions; (ii) to draw attention in particular to an additional complication believed to be both significant and not previously recognized; and (iii) to suggest that progress in clarifying currently confounded issues will probably best be made by the measurement of what are here called extended circadian surfaces (or topographies), rather than by traditional experimental protocols that constitute only one transect across such surfaces. Convergent evolution in photoperiodic phenomenaPhotoperiodism itself is by no means the only way in which selection has met the challenge of recognizing the time of year; and what formal similarities there are among those plants and animals that do utilize daylength as a noise-free cue to season may well be no more than that-formal, and in a sense superficial-the product of a convergent evolution that obscures significant differences in the underlying concrete mechanisms involved. Indeed, there is little doubt this is in fact the case, making the search for a unified "theory" founded on facts from different organisms hazardous, at best. Thus, while it is abundantly clear th...

The effect of duration and time of food availability on the photoperiodic response in the male house sparrow, Passer domesticus

“…Light at the beginning of the day entrains the photoperiodic clock, and when the light period is long enough to extend into the photoinducible phase, photoperiodic induction occurs [1,4,11]. The results from several species of birds are consistent with this model of photoperiodic induction called the external coincidence model [6,[12][13][14][15].…”

Photoperiodic Time Measurement in Insects: A Review of Clock Models

“…The hourglass clock is a computerized version of the Megoura clock and is able to generate photoperiodic responses similar to those obtained experimentally with Lees's protocols performed with the mite (Vaz Nunes and Veerman, 1986b). However, in the mite, the positions of the peaks and troughs observed in Nanda-Hamner experiments were not related to the total cycle length (T) as suggested by Pittendrigh (1972); instead, they were re- Pittendrigh et al (1984). a.…”

“…This concept later was called "internal coincidence" (Pittendrigh, 1972) to differentiate it from external coincidence; it suggests that light has a single role (entrainment) and not the dual roles (entrainment and photoinduction) inherent in the latter. Table 1 lists several theoretical versions of internal coincidence: phase relationships between two light-entrainable master oscillators or pacemakers, either coupled in a complex pacemaker (Model 7) or independent of each other (Model 8); phase relationships between a pacemaker and a slave (Model 9); and phase relationships among several slaves driven by the same (or different) pacemaker(s) (Model 10).…”

“…In outlining theoretical differences between external and internal coincidence, Pittendrigh (1972) suggested that the most parsimonious version of the former could be a single circadian oscillation whose phase relationship to photoperiodic cycles involved the illumination or nonillumination of a particular phase (ϕ i ) according to the duration of the photophase. Internal coincidence, on the other hand, incorporated a number of constituent oscillators (at least two) whose mutual (internal) phase relationships varied with season.…”

Ground-roosting in domestic fowl (Gallus gallus domesticus) in The Gambia: the anticipation of night

“…Morris, 1973;Bhatti and Morris, 1978a,b;Brady, 1982;Reebs, 1994), and it has been shown that in birds, the transparency of the skull is sufficient to allow intensities of around 10 lux to reach a photoreceptor in the cerebrum (Hader and Tevini, 1987). It is now generally accepted that photosensitivity (the threshold of an animal's sensitivity to light) is governed by circadian rhythm, but that photoperiodic reactions (the animal's behavioural response to light intensity, such as going to roost) are stimulated only when light coincides with photosensitive periods (Pittendrigh and Morris, 1964;Pittendrigh, 1972;Hader and Tevini, 1987). This theory, known as the 'coincidence model', explains why birds will only be stimulated to go to roost in the evening, even though the environmental conditions (such as light levels) acting as the cues to roosting may occur at other times of the day (Saunders, 1977;Applin and Cloudsley-Thompson, 1982;Brady, 1982).…”