THE MOON AND LIFE ON EARTH ELFED MORGAN School of Biosciences, University of Birmingham, Edgbaston, Birmingham. UK e-mail: [email protected]

Beliefs . . . in an influence of the Moon on life on Earth are legion. And yet such lunar beliefs are by no means all moonshine. H. Munro Fox, 1928

1. Introduction In 1928, Hector Munro Fox, then professor of Zoology at the University of Birmingham, UK, published a small volume entitled “Selene or Sex and the Moon” The title ensured the book a place on the bookshelves of the “obscene books” sections in the libraries of Post-Victorian England, to the chagrin of the voyeur and the irritation of biologists deprived of a most readable account of the life cycles of shellfish. The book is also concerned with how the application of science to fable and folklore has increased our understanding of the Moon’s influence on life on Earth, and has been the starting point for much of what follows. Deified by the ancients, belief in lunar supernatural powers pre-dates History, and the origins of these beliefs must therefore be speculative. A case can undoubtedly be made for the spiritual inspiration of the Moon (Huxley, 1950), but the phase transitions of the monthly cycle also invite association with earthly changes in the sentient mind. The early Greeks and Romans for example considered sheep’s wool and human hair to grow more rapidly when the Moon was in the ascendant. The belief that the early growth rate of children and cattle was determined by the state of the Moon at birth seems to have been wide-spread (Munro Fox, 1928). A consideration of how some of our perceptions of the Moon’s biological influence have changed over the years thus appears relevant to a discussion of earthmoon relationships. Since these early days, two factors have affected the way we regard the natural world. The first of these was the advent of the empirical philosophy of Francis Bacon in the seventeenth century, when anecdote and superstition made way for hypothesis and experiment under the guidance of Gallileo, Newton and others. The second has been the subsequent “professionalisation” of science during the last century (Rossi, 1968), culminating in the methodology which has given us our understanding of the human genome and taken man to the Moon itself. Together, these changes have placed the onus of proof firmly on the shoulders of Earth, Moon and Planets 85–86: 279–290, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.

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the believers. Consequently, current investigations into the relationship between biological events and the lunar cycle are subject to a number of a priori considerations before they pass muster. The biological process must be quantifiable and the units of measurement clearly defined; the nature of the lunar influence should be identifiable, and its biological impact demonstrated empirically. A constant phase relationship with the Moon should be demonstrated statistically and verified independently. Finally, biologists may wish to add the caveat that the behavioural and physiological process involved should be evolutionarily adaptive.

2. Some Geo-Physical Considerations Before Newton, man knew the Moon only through the sunlight it reflected. Its apparent movement across the night sky is due mainly to the spin of the Earth on its axis. However, the Moon also moves relative to the Earth, so that seen from the Earth, it takes 24.8 h or one lunar day to return to the same point in the night sky on consecutive nights. It takes much longer for the Moon to orbit the Earth, approximately 27.3 days, or one sidereal month (Figure 1). During this time the Earth and Moon move further along their orbit of the Sun, so that the interval between full moons when observed from the Earth is longer. This is the lunar, or synodic, month with a mean duration of 29.5 days. The intensity of illumination changes systematically with changes in the lunar profile over the lunar month. At full moon the Earth lies along a line between the Sun and the Moon, and the latter appears as a complete disc. At new moon, the Moon lies between the Earth and the Sun, and is invisible from the Earth. Quarter moons occur at right angles to the Earth and Sun, so that only part of the face presented to the Earth is illuminated, appearing as a crescent or gibbous Moon. These changes, emanating from a point source in the night sky, provide a potential reference point for orientation in time and space. With the publication of Newton’s “Principia” in 1687 gravity was also recognised as an agent of lunar influence. Its effects are most dramatic in the rise and fall of the tides, for which Newton’s tidal theory remains the basis for our present understanding (e.g., Defant, 1958; Palmer, 1995). In its simplest form this assumes the Earth and Moon to rotate about an axis located within the mass of the Earth. The resulting centrifugal force draws the waters of the Earth towards, and away from the direction of the Moon. Thus, because of the daily rotation of the Earth, the tides rise and fall twice each lunar day, at intervals of approximately 12.4 h. The height of the tides in the open oceans is little more than 76 cm but they may exceed 10 m when amplified by coastal topography. The amplitude of successive tides may also be modulated over a 14–15 day, or semi-lunar cycle, as the Moon orbits the Earth. In the North Atlantic the highest, or spring tides occur when the gravitational pull of the Sun and the Moon are aligned, i.e., at full and new moon,

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Figure 1. Diagram to illustrate changes in the Sun–Earth–Moon configuration during the passage of one lunar month. At time A the Moon lies directly between the Sun and the Earth, as it does at new moon. At B, 27.3 days or one sidereal month later, the Moon will have returned to the same point overhead relative to the Earth, but does not regain it’s position on the line between the Earth and the Sun for another 2.2 days, i.e., after 29.5 days or one synodic month (redrawn from Rackham, 1968).

and the lowest, or neap tides, at the moons quarters when these gravitational forces are at right angles to each other. The Moon’s gravitational effect is not confined to the oceans. Tidal movements in the atmosphere and in the Earth’s crust follow a similar pattern (Palmer, 1995), and it is conceivable that the former may modulate the number of charged particles entering the atmosphere. In addition the transient atmosphere generated at the Moon’s surface by the solar wind may be diverted by gravity to focus on the Earth around the time of the new moon (Mendillo, 2001).

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3. Biological Evidence of Lunar Influence From a biological standpoint the rhythmic nature of the Moon’s influence is as significant as its physical manifestations. The regular environmental changes that accompany the Moon’s passage across the night sky mark out a time-scale different from that of the Sun. Because of the greater length of the lunar day, changes in the Moon’s gravitational influence occur progressively later in each 24-h cycle of light and darkness, and a greater range of ecological niche becomes available through time. This is most obvious in the region between tidemarks, and a comparison of the two time-scales is shown in Table I. Given the antiquity of the Earth–Moon relationship, the diversity of morphological and physiological adaptations shown by marine littoral organisms is to be expected, but it is through their behaviour patterns that the influence of the Moon is most clearly manifest. These provide an immediate and flexible response to a periodically changing environment. Under such conditions it could be advantageous for animals to confine their activities to the most beneficial stage of the environmental cycle, and it is reasonable to expect such behaviour to be favoured by natural selection. Tidal, semi-lunar and lunar variations in the behaviour of marine and inter-tidal animals have long been recognised by fishermen and naturalists, and there is now considerable empirical evidence from species as diverse as shore-crabs, fishes, annelid worms and gastropod molluscs to support these observations (see references below). Moreover, these behaviour patterns have proved amenable to manipulation in the laboratory, enabling the nature of the lunar influence to be investigated experimentally. The demonstration during the latter half of the 20th century, that an internal clock may regulate the lives of sea-shore animals has been especially significant in this respect. At first approximation this assertion seems more akin to the fables of yester-year than to scientific scrutiny, and a consideration of some of the evidence on which it is founded is appropriate here.

4. Tidal or Lunar Day Phenomena The basic experimental protocol used in the study of tidal and lunar rhythms is essentially that employed by Gamble and Keeble (1904) to investigate the periodic migration of Convoluta roscoffensis. This small flatworm rises to the surface of the sand in large numbers at low water, but burrows again in anticipation of the hazards of the incoming tide. Remarkably, the same behaviour was observed in animals newly transferred to the laboratory, away from the rise and fall of the tides (Keeble, 1910), and similar rhythms have been reported subsequently for a number of different inter-tidal species studied under constant conditions (Naylor, 1988, 2001; Morgan, 1991; Palmer, 1995). As with circadian clocks, the circa-tidal oscillators only approximate to the period of the natural cycle that they follow, and gradually drift out of phase with the 12.4 h cycle that prevails at the site of collec-

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TABLE I Calendar of periodic environmental changes in the inter-tidal zone Period

Name

Cause/consequence

12.4/24.7 h

Tidal

24 h

Diel

14 day 28 day

Semi-lunar } Lunar }

365 day

Annual

Earth rotates Moon, tidal rise and fall Earth rotates Sun, light/dark cycles Moon orbits Earth, spring/neap tides, full/new moon Earth orbits Sun, seasons, photoperiod

tion. They are also relatively short lived. Only about 8 cycles of vertical migration are shown by C. roscoffensis before the activity pattern becomes arrhythmic, but the clock may be re-set by returning the animals to the shore and exposing them again to the cycle of the tide. In more recent years the different environmental factors which make up the semi-diurnal tide have been simulated in laboratory experiments. Tidal cycles of inundation and exposure, temperature, pressure, salinity and wave action have all been shown to be potential mediators of the Moon’s influence, acting independently or in combination (Morgan, 1991). Paradoxically, Keeble and Gamble rejected a control mechanism involving a “tidal memory” with its implied time measurement suggested by Bohn (1904) (Keeble, 1910), but the rhythm characteristics they described for C. roscoffensis subsequently formed the cornerstones of the argument for endogenous, or internal clock control (Pittendrigh, 1960). An activity rhythm driven by environmental cycles of tidal period not controlled for in the experiments, such as barometric pressure or electro-magnetic radiation described above would be expected to retain its integrity and also keep phase with the twice-daily gravitational tides. The Moon does not act alone however. The behaviour patterns of many inter-tidal animals also show evidence of solar day effects (Naylor, 1958; Petpiroon and Morgan, 1983), suggesting that clocks of differing periods may be involved and the exact nature of the controlling mechanism is a matter of debate.

5. Lunar or Semilunar Monthly Phenomena Environmental changes of lunar and semi-lunar monthly period are more complicated, and both moonlight and gravitational factors prevail. Their influence during

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the lunar monthly orbit is reflected in cycles of reproductive and migratory behaviour, as well as in a semi-lunar modulation of locomotor activity cycles associated with the semi-diurnal tide. Early maritime people were well aware of the relationship between the gastronomic qualities of shellfish and the stage of the lunar cycle. Aristotle was probably expressing the scientific opinion of his time when he said that the correlation was clearest in sea-urchins, whose roe was largest at the time of the full moon. About 2,300 years later Munro Fox saw in this statement a testable hypothesis. By counting the number of urchins with mature gonads he was able to show a periodic reproductive cycle, with spawning at the time of the full moon (Munro Fox, 1923). Other studies, involving a diversity of species have been largely supportive of these observations (see reviews by Palmer, 1995; Naylor, 2001; Bentley et al, 2001), although not invariably so (Lessios, 1991). The nature of lunar intervention in these spawning cycles is not always clear, and both moonlight and gravitational factors are implicated. Away from the shore the least equivocal examples of lunar influence are those in which animal behaviour changes in direct response to moonlight. For example the banner-tailed kangaroo rat, Dipodomys spectabilis, is strictly nocturnal during the winter, except on bright, moonlit nights when it does not venture above ground, perhaps to avoid predation (Lockhard, 1978). The predatory larvae of the lion ant Myrmeleon sp. on the other hand, excavate larger pitfall traps at the time of the full moon, presumably to exploit the less cautious (Youthed and Moran, 1969). As a species we are equally susceptable to the cyclic changes in moonlight intensity. In 1776 Mathew Boulton, industrialist and entrepreneur, wrote to his friend and business partner, James Watt: Prey remember that ye celebration of ye 3rd full moon will be on Sunday March 3rd. Darwin and Keir will both be at Soho. I then propose to make many motions to the members respecting new laws and regulations, such as will tend to prevent the decline of a society which I hope will be long lasting. Darwin was of course Erasmus Darwin, grandfather of Charles, and the society referred to was the Lunar Society of Birmingham, an informal group of highly intelligent men who met regularly to enjoy the intellectual stimulus of each others’ company. The meetings were timed to coincide with the full moon simply to ensure enough light for a safe passage home. The changes Boulton had in mind were never implemented and no records were kept, but the consequences of the industrial revolution, ushered in around the table at Soho House, have been considerable. Ironically, one of these has been the reduction of the importance of moonlight as a source of nocturnal illumination in urban societies, although in some rural areas crops were harvested by the light of the Moon as recently as the middle of the last century. Claims for lunar intervention in other aspects of human biology are more contentious, and mental health and fertility have attracted particular attention.

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Garzino (1982) has critically reviewed studies prior to 1982. More recent contributions are discussed by Raison et al. (1999), and elsewhere in the present volume (Zanchin, 2001; Strestik, 2001; De Antonio, 2001). In contrast to the animal studies in which data have been collected over a linear time-series, the basic approach here has been demographic. Attempts have been made to relate data from medical records to the stages of the Moon, although the objectives and methods of analysis have been diverse. Different authors have used different criteria to define the same biological variables, and the lunar stages with which they are correlated have not always been determined in the same way. The use of different statistical tools further complicates the interpretation of the results. The overall picture is thus confusing or contradictory and the demonstration of lunar rhythmicity often lacks conviction, with one notable exception. The human fertility cycle is clearly periodic. At issue here is if, and how it is related to the Moon. This problem was addressed by the Swedish chemist and polymath, Svante Arrhenius in 1898. He found, as other studies have confirmed (e.g., Folin et al., 2001), the mean period to be 27.32 days, two days shorter than the synodic cycle of Moon. Menstruation and childbirth followed the sidereal cycle more closely and should change their phase relative to the cycle of the full moon. There was however a significant correlation with electro-magnetic fluctuations in the fluctuations in atmosphere, which also followed a sidereal cycle (Arrhenius,1898).

6. Lunar Influence on Orientation and Navigation Students of animal migration frequently testify to a lunar influence on the movements of animal populations. In coastal waters tidal currents offer economic transport for those animals that are able to take advantage of them. One such is the estuarine amphipod, Corophium volutator (Holmström and Morgan, 1983; Morgan and Harris, 1986). Enticed to leave its burrow by the rising water level, it is transported landward while feeding on the surface of the substratum at the edge of the tide. Increased swimming, initiated by an internal clock and falling pressure early during the ebb, keeps the animal in the water column as the tide retreats, and ensures its return to the burrowing zone (Figure 2). Surf-migrant crustaceans show similar behaviour patterns on sandy beaches (Naylor, 2001), and inshore fish may use the tidal currents in much the same way. For example the North Sea flatfish Pleuronectes platessa, migrating between spawning and feeding grounds, rises into the tidal water current when it flows in the migratory direction, but remains on the bottom during the counter-flow, thus reducing the energy cost significantly (Metcalfe et al. 1992; Arnold and Metcalfe, 1996; Page, 1998). The influence of moonlight is more subtle and diverse. The full moon illuminates the Earth to 1.5 × 10−5 lumens per cm2 , sufficient for the visual recognition of topographic cues, and a number of field and laboratory studies have reported changes in migratory and other activity at this time (e.g., Hain, 1977; James et

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Figure 2. The tidal migration of the estuarine amphipod Corophium volutator. Animals are induced to leave their burrows by the rising tide, and may be transported passively up the shore on the flood tide. As the tide turns they leave the substratum and swim up into the water column to facilitate their transportation back dowm the shore. The onset of increased swimming in response to the animals’ body clock, derived from laboratory experiment, is shown in the polar plot (from Morgan and Harris, 1986, after Holmström, 1981).

al., 1999). However, the Moon is a capricious reference point for orientation and navigation. Frequently hidden by low cloud cover, its position in the sky also changes throughout the night. Moreover, as it rises 50 minutes later each night its position at any given hour will change from night to night. Animal navigators must compensate for these positional changes if they are to remain on course, and to this requires measurement of the passage of time on a lunar, as well as a solar time-scale. Evidence for a time-compensated moon-compass of this sort is often contradictory and indirect, as studies on sand-hoppers have shown (Enright, 1972). Talitrus saltator is a small amphipod crustacean that lives near high water mark on sandy beaches. At night it emerges from the sand and, in mediterranean populations, migrates landward on short foraging excursions, returning to the burrowing

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Figure 3. Results from different experiments showing the orientation of sand-hoppers before and after the apparent position of the Moon was changed through 1800 by reflection in a mirror. The initial direction of orientation is shown by the downward arrows in each case. The upward arrows show the expected orientation to the reflected Moon. The closed circles indicate the actual orientation to the mirror shown by animals in individual experiments. In Figure 3B the orientation to the Moon itself, and to it’s reflection is indicated by arrows 1–3, and 4–6 respectively. Figures A and B show significant orientation in the expected direction, consistent with the Moon compass hypothesis; those in C show no significant preference for any direction while in D the animals are significantly orientated in a direction apparently unrelated to the Moon (after Enright, 1972).

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zone before sunrise. It is the return journey that provides the best evidence of lunar orientation. Papi and Pardi (1959) found that when captive animals were allowed to move freely in a glass flask, they gathered in the direction of the sea, but only if the Moon was visible. On moonless nights they showed no directional preference, but when the Moon was reflected from a mirror, the animals re-orientated accordingly. These observations were confirmed by Enright (1972), who also showed that the angle of lunar orientation varied with the passage of the Moon, which suggested the involvement of a lunar clock. The results were not always clearly defined however. In some experiments the observed orientation deviated significantly from the expected, in others the animals were dispersed generally in the flask (Figure 3) This led Enright (1972) to conclude that although the Moon Compass hypothesis offered the best explanation for the available data, it was unlikely that the Moon was the only factor involved. Studies on the use of a possible Moon compass by migratory birds have come to the same general conclusion (see Baker 1984), and one possible navigational aid may be provided by the geo-magnetic field. This is known to influence the orientation of many organisms, including perhaps our own (Baker, 1984). Moreover, in a number of species the orientation has been found to vary over the lunar cycle. For example the sea-slug, Tritonia diomedea showed significant orientation in the geo-magnetic field when tested at full moon, but were randomly distributed at the new (Lohman and Willows, 1987). When the magnetic field was reversed using an induction coil, the inverse relationship was observed. Here the Moon appears to provide a time cue for the directional change, rather than acting on the geo-magnetic field itself, and it has been suggested that the re-orientation would facilitate onshore migration during the reproductive period.

7. Conclusion The geo-physical changes effected by the Moon are qualitatively very different. Some are self evident, such as moonlight or the ocean tides while others, such as barometric pressure or electro-magnetic radiation are more subtle. Reported manifestations of the influence of these changes on animal behaviour and physiology are correspondingly diverse, and carry different degrees of conviction. The robust regulation of animal behaviour by the ocean tides contrasts sharply with the evidence for periodic lunar intervention in human behaviour and physiology. This may reflect the different methodology employed in the two areas of study, but the controversial nature of the evidence presented in the literature implies that the effect of the Moon is less imperative on land than in the inter-tidal habitat. To some extent investigations of the Moon’s influence on human biology find an interesting parallel in animal navigation studies. Here the unpredictability of a significant lunar effect has led to the suggestion that the Moon may not be the only factor involved. This being so, the influence of the Moon may be moderated by other

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environmental variables, and by the physiological state of the animal itself. Some of the difficulties in obtaining unequivocal verification of Moon-related phenomena reported in the literature could be explained in this way. Alternatively, the statistical analyses in some of the earlier studies may be misleading. Either way the argument for further empirical study of the Moon’s influence on life on Earth (Garzino, 1982) is substantiated.

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