Sexual Satellites, Moonlight and the Nuptial Dances of Worms: The Influence of the Moon on the Reproduction of Marine Animals

Abstract

The evidence that the moon has a profound effect on the timing of reproductive activities of marine animals is compelling. Some moon phase related spawning events are revealed by the constant phase relationship between the timing of “once per year” spawning events and the lunar phase as in the highly synchronised breeding of the palolo worm Palola viridis, and the Japanese crinoid Comanthus japonicus. In other cases there is a repeated lunar cycle of reproductive activity and again the marine worms provide many good examples. The breeding of the palolo worm involves the highly synchronised release of what are in effect detached sexual satellites and the timing of this has annual (solar year), lunar, daily and tidal rhythm components. In a similar way, the onset of sexual maturation and participation in the nuptial dance of Platynereis dumerilli has strong lunar components. Sexual reproduction is the culmination of a process of sexual maturation that takes many months for completion and the mechanisms by which moon phase relationships are imposed on this process must have been selected for by mechanisms relating to reproductive success. The polychaetes provide excellent models for investigation of both the selective advantage and the physiological processes involved in reproductive synchrony. We have recently shown that the spawning of the lugworm Arenicola marina has lunar components and we conclude that an interaction between solar and lunar signals is widespread in the timing of reproduction in marine animals. Carl Hauenschild was the first to demonstrate the existence of a free-running circa-lunar rhythm in marine animals using captive populations of Platynereis dumerilli. His experiments also provided clear evidence for the influence of moonlight (light at night) as the zeitgeber for this rhythm. This implies a high level of sensitivity to light, and the operation of appropriate endogenous biological rhythms. Using Nereis virens we have demonstrated a high level of sensitivity to low intensity solar light signals in relation to rhythmic processes with the properties similar to the circadian and photoperiodic mechanisms of terrestrial organisms. The spawning of N. virens is also believed to have lunar components reflecting the complex influences of the sun and the moon in the marine domain, where influences of the moon and sun are more equal. We suggest that evolution of biological rhythmicity that can be entrained to either lunar or solar systems arose in the marine domain. Recent advances in understanding the molecular components of the circadian clock system suggest that a search for a common molecular mechanism for both lunar and solar related biological rhythms in marine organisms might be very fruitful.