An Overview of Monthly Rhythms and Clocks

Abstract

Organisms have evolved to cope with geophysical cycles of different period lengths. In this review, we focus on the adaptations of animals to the lunar cycle, specifically, on the occurrence of biological rhythms with monthly (circalunar) or semi-monthly (circasemilunar) period lengths. Systematic experimental investigation, starting in the early twentieth century, has allowed scientists to distinguish between mythological belief and scientific facts concerning the influence of the lunar cycle on animals. These studies revealed that marine animals of various taxa exhibit circalunar or circasemilunar reproductive rhythms. Some of these rely on endogenous oscillators (circalunar or circasemilunar clocks), whereas others are directly driven by external cues, such as the changes in nocturnal illuminance. We review current insight in the molecular and cellular mechanisms involved in circalunar rhythms, focusing on recent work in corals, annelid worms, midges, and fishes. In several of these model systems, the transcript levels of some core circadian clock genes are affected by both light and endogenous circalunar oscillations. How these and other molecular changes relate to the changes in physiology or behavior over the lunar cycle remains to be determined. We further review the possible relevance of circalunar rhythms for terrestrial species, with a particular focus on mammalian reproduction. Studies on circalunar rhythms of conception or birth rates extend to humans, where the lunar cycle was suggested to also affect sleep and mental health. While these reports remain controversial, factors like the increase in "light pollution" by artificial light might contribute to discrepancies between studies. We finally discuss the existence of circalunar oscillations in mammalian physiology. We speculate that these oscillations could be the remnant of ancient circalunar oscillators that were secondarily uncoupled from a natural entrainment mechanism, but still maintained relevance for structuring the timing of reproduction or physiology. The analysis and comparison of circalunar rhythms and clocks are currently challenging due to the heterogeneity of samples concerning species diversity, environmental conditions, and chronobiological conditions. We suggest that future research will benefit from the development of standardized experimental paradigms, and common principles for recording and reporting environmental conditions, especially light spectra and intensities.

Keywords: circadian; circalunar; light; marine; mood; moon; reproduction; sleep.

Figure 1

Circalunar and circasemilunar rhythms and clocks/oscillators are widely present in the animal kingdom. (A) Common biological rhythms linked to the moon cycle can be classified into circalunar and circasemilunar rhythms based on their periodicity, reflecting the re-occurrence of specific events/states once or twice, respectively, during the lunar month. Note that these events/states can be matched with any of the lunar phases, with the example showing synchrony with the full/new moon. (B) Circalunar/circasemilunar rhythms are found in a broad range of animals, as demonstrated by the phylogenetic position of individual animal groups in which reproductive cycles have been linked to the lunar phase (see text). (C) Biological rhythms either reflect direct response of an organism to changes in the respective environmental stimulus, such as nocturnal light (top; “Stimulus-controlled”); or they are driven by endogenous clocks that are entrained/set by a particular state of the environmental stimulus (bottom; “Clock-controlled”). As the environmental stimulus is not required for an endogenous clock to continue, a clock-mediated biological rhythm also “free-runs” if the environmental stimulus is experimentally removed.

Figure 2

Levels and spectra of artificial light compared to natural light sources. (A) The graph summarizes published values on the illuminance caused by celestial bodies (up) (top), and of various sources of artificial light (bottom), expressed in lux, plotted on a logarithmic scale. All displayed artificial light sources cause intensities that exceed maximal moon light intensities (approximately 0.25 lx at a clear full moon night) by at least two orders of magnitude. This indicates that artificial light is highly likely to interfere with any natural response to moonlight. (B) In addition to light intensities, artificial lights also have various distinct spectra. Top: Photon flux (expressed as micromoles per square meter per second photons) across the light spectrum (in nanometers), measured for sunlight (on noon of a summer’s day, Vienna, Austria); bottom: spectrum of a Philips compact fluorescent lamp (14 W); depending on the specific light receptors affected, the effect of artificial light at night can be aggravated or reduced by changing its spectral composition. Data in panel (A) compiled from Ref. (52, 53) and an online version of the Handbook published by the Illuminating Engineering Society (https://www.archtoolbox.com/materials-systems/electrical/recommended-lighting-levels-in-buildings.html); spectra in panel (B) schematized based on published values (54).