TIDAL RHYTHMS: THE CLOCK CONTROL OF THE RHYTHMIC PHYSIOLOGY OF MARINE ORGANISMS

Summary 1. A great number of vital processes are rhythmic and the rhythms quite often persist in constant conditions. The best‐known rhythms are circadian; much less is known about circalunadian rhythms, and this review was prepared in an attempt to rectify this deficiency. All through the article comparisons are drawn between circalunadian and circacian rhythms. 2. Activity rhythms. ( a ) The activity patterns of 28 intertidal animals are discussed. All describe a periodicity with a basic component of 24.8 hours, and this approximate period persists in the laboratory in constant light and temperature and in the absence of the tides. The duration of persistence ranges from a few cycles to months, and is a function of the species studied, the conditions imposed, and individual tenacity. ( b ) In those few cases where relatively long‐term observations have been made, there is a trend for the period of the rhythm to become circatidal, or better, circalunadian. ( c ) The ‘desired’ phase relationship between rhythm and tidal cycle is species‐specific. Geographical translocation experiments have shown that the phase is set by the local tides. ( d ) In some cases the amplitude of the persistent rhythm mimics the semidiurnal inequality of the tides. ( e ) In about a third of the species discussed, a circadian component has been found combined with the tidal component. Many of the other studies were of such short duration that a low‐amplitude circadian component would have gone unnoticed. (f) The tidal rhythm is innate. However, the rhythm is (i) sometimes lacking in organisms living in non‐tidal habitats, or (ii) fades after a spell of incarceration in constant conditions. Various treatments — some aperiodic — can induce the expression of the missing tidal rhythm. ( g ) In the green crab, removal of the eyestalks destroys the activity rhythm. 3. Vertical migration rhythms. ( a ) A rather surprisingly large number of intertidal animals have been found to undergo migration rhythms between the upper layers of the substratum and its surface. The movements are synchronized with the tides in nature, but most species have either been shown to be diurnal in constant conditions, or in cases where adequate testing has not been done, suspected of being so. ( b ) In only one species has confirming work shown that the fundamental frequency is truly tidal. This finding is especially important as it shows that tidal rhythms need only the single‐cell level of organization for expression. Even at this level there appears to be a dictatorial override by a circadian clock. 4. Colour change. Low‐amplitude tidal rhythms in colour change — superimposed on a more dominant circadian change — have been reported to be intrinsic in four species and inducible in a fifth. 5. Oxygen consumption. Tidal rhythms in oxygen consumption have been described for seven invertebrates and one alga; six of the species have superimposed solar‐day rhythmic components also. 6. Translocation. A total of five geographical translocation experiments, in which the organisms were maintained in constant conditions throughout, have been tried. Unequivocally in one case, and possibly in a second, the test organisms rephased spontaneously to the times commensurate with local tidal conditions. In two other cases, the pretranslocation phase was retained. The fifth experiment has not been reproducible. 7. Determination of phase. ( a ) The tidal cycle on the home shoreline sets the phase of the inhabitant's rhythms. Even the location of a crab's burrow on the beach incline can play a determining role. ( b ) Paradoxically, the periodic wetting by inundation is not an important entraining factor for most intertidal organisms. Instead, the effective portions of the tidal cycle include one or more of the following. (i) Mechanical agitation, especially for animals living in an uprush zone where they are periodically subjected to the pounding surf, (ii) Temperature cycles, though they have not yet been systematically investigated, have very pronounced entraining roles in crabs. (iii) Pressure is probably not a generally important entraining agent for most intertidal organisms, but it is so for the green crab. (c) Light‐dark cycles in general, whether daily or tidal in length, have no effect on the entrainment or phase setting of many tidal rhythms. There are two exceptions: (i) a 24‐hour light‐dark cycle is known to keep a tidal locomotor rhythm (one that becomes circalunadian in constant conditions) at a strict tidal frequency. (ii) In rhythms with both daily and tidal components, when the former is shifted by light stimuli, the latter is affected in a nearly identical manner. 8. Temperature. ( a ) The role of temperature on tidal rhythms is compared with its role on circadian rhythms. ( b ) The effects of different constant temperatures have so far been studied on only four tidal rhythms. All studies indicate a lack of any permanent change in period, which is not so with most circadian rhythms; the latter having temperature coefficients around 1.1. In two of the studies the rhythms under test temperatures were followed for less than a day, and a third study cannot be repeated. ( c ) Short exposure to very cold temperature pulses produced a response that may be interpreted as a temporary stoppage of the clock. Exposure to relatively less‐cold pulses appear simply to reset the hands of the clock. The same responses have been demonstrated with circadian rhythms. ( d ) In the case of green crabs, which had become arrhythmic during prolongued captivity in the laboratory, a tidal rhythm could be reinitiated by a single short cold treatment. The cold pulse also set the phase of the rhythm. ( e ) A few superficial studies employing temperature steps or pulses have produced results which suggest that a phase‐change sensitivity rhythm — just like that found associated with circadian rhythms — may underlie tidal rhythms. Certainly a determined search for this rhythm should be made in the near future. 9. Clock control of rhythms. ( a ) An argument is constructed claiming that tidal rhythms have a basic period of about 24–8 hours rather than the more expected tidal interval of 12.4 hours. In constant conditions, a circalunadian period is usually displayed. ( b ) After speculating that a frequency‐transforming coupler may function between the clock and the overt rhythm, reasons are given that lead to the further speculation that both circadian and circalunadian rhythms could be generated by a single clock, via specific coupling mechanisms. ( c ) Two current hypotheses concerning the nature of the clockworks are reviewed and discussed. ( d ) Suggestions are made for future investigations.