Animal studies
- The lunar cycle: effects on human and animal behavior and physiology

Insects and lower vertebrates
A study conducted on honeybees showed a 29.5-day rhythm regarding triacyloglycerols and steroids in the hemolymph as well as body weight peaking at the new moon [24]. Studies on fish [37,38,41] demonstrated that fish physiology is infl uenced by lunar periodicity and correlates with hormonal changes. Correlation between hormonal changes in the testis and lunar periodicity was studied in Siganus argenteus, which spawns synchronously around the lastquarter moon [37]. Weekly changes in sperm motility peaked around the last-quarter moon. The pH and osmolarity of the seminal fluid increased and decreased around the same lunar phase, respectively. These results suggest that the testis of this species develop according to the specific lunar phase. Experiments with addition of human chorionic gonadotropin or steroids to testicular fragments led to the conclusion that the lunar cycle clock influences the higher part of the hypothalamus-pituitary-gonadal axis [37].

A study on the golden rabbitfish Siganus guttatus, which spawns synchronously around the first-quarter moon during the reproductive season, showed daily fluctuations of melatonin concentration in the blood, which were low during the day and high at night [41]. In addition, plasma melatonin concentration at the new moon was higher than at full moon. When the fish were exposed to moonlight at midnight of both these moon phases, the melatonin concentration decreased to the control levels. These results show that the fish possibly perceive moonlight intensity and that plasma melatonin fluctuates according to brightness at a certain time of night. Fish kept in constant darkness or light at night did not spawn. It is possible that night conditions are related to synchronous gonadal development and spawning in the golden rabbitfish. The effects of moonlight exposure on plasma melatonin rhythms were also demonstrated in the seagrass rabbitfish Siganus canaliculatus [38]. When the fish were exposed to the four lunar phases, plasma melatonin levels around the new moon were significantly higher than during the first quarter and the full moon. The synchronous rhythmicity of melatonin levels in the plasma supports the hypothesis that the seagrass rabbitfish perceives moonlight intensity and responds with secretion of melatonin into the blood stream.

Reptiles and birds
Reports on the effects of the lunar cycle on the physiology of amphibians and reptiles are lacking. Amphibians [36] and reptiles [27–29] are subject to seasonal changes due to hibernation in winter. In the case of the turtle Mauremys caspica, spring increases cell proliferation in response to mitogens [27–29], and in autumn, proliferation and ADCC- and NK-mediated cytotoxicity [28] demonstrated their lowest values. The increased cell proliferation correlated with low levels of corticosterone and testosterone [29]. In the night-migrating skylark Alauda arvensis, the main nocturnal movements take place during the waxing phase of the moon [15]. The effects of moon phase and age on diurnal rhythms of plasma melatonin and corticosterone in free-living Nazca boobies (Sula granti) on the Galapagos Islands were studied [42]. Nazca boobies showed a diurnal variation with higher concentrations at 00: 00 and 16:00 h. The diurnal variations in melatonin concentrations disappeared during full moon, suggesting that natural light levels at night can suppress melatonin secretion in Nazca boobies. Maximal melatonin concentrations tended to decline in older birds (10–19 years). The birds showed a clear diurnal variation in basal plasma corticosterone, with a peak in the early morning, before the active period begins, and low concentrations throughout the day. As in the case of melatonin, there were no diurnal variations in corticosterone at full moon, which may be due, as the authors suggest, to different activity patterns in response to food availability or changes in the circadian system. No correlation between corticosterone and melatonin levels were found. The authors conclude that the lunar cycle affects the hormone levels in Nazca boobies both directly and indirectly. First, melatonin rhythms can be directly affected by the light intensity associated with the full moon. Second, prey availability may change foraging patterns and can therefore indirectly alter corticosterone secretion in Nazca boobies.

Even in mammals, data on the effects of light/dark, seasonal, and lunar cycles on physiology are scant. Investigations were carried out mostly in rodents. In the Indian palm squirrel Funambulus pennanti, seasonal changes in several immune parameters, such as total blood leukocytes, blastogenic response of blood, and thymus and spleen lymphocytes were studied [11]. The authors found that, in parallel with melatonin, all the parameters increased during the months of April to November. The lowest values occurred during January to March (reproductively active phase). Injection of melatonin during their inactive phase (March) increased all the immune parameters, while pinealectomy during November decreased them signifi cantly. The authors suggest that melatonin is immuno-enhancing for this tropical squirrel. Studying a rat strain with individual differences in the threshold of excitability of the nervous system, researchers found that excitable rats showed rhythmical changes of taste sensitivity to a bitter substance, phenylthiocarbamide, related to the lunar rhythm [32]. Others investigated the influence of light/dark, seasonal, and lunar cycles on serum melatonin levels and synaptic bodies, ultrastructural organelles, of the pineal gland of the rat [23]. The experiment was carried out in winter and repeated in spring. Each season, one group of animals was killed during the new moon and a second group during the full moon days; in addition, half of both groups was studied in the photophase and the other half in the scotophase. The results showed that the number of synaptic ribbons (a type of synaptic body) and serum melatonin levels were higher during scotophases, winter, and full moon days. The synaptic spherules (another type of synaptic body) showed a light predominance during winter, whereas a predominance of intermediate synaptic bodies was found only during scotophases.

Variations in the magnitude of the immune response in laboratory animals remain mostly unexplained. Thus, evaluation of the immunotropic effects of various compounds may be not conclusive. The author’s studies on the regulation of the humoral immune response to a synthetic B cell-dependent antigen, polyvinylpyrrolidone (PVP), by prostaglandins (PG) showed 12-week cycles of high and low responsiveness [50]. Peaks in the number of cells forming antibodies to PVP in culture occurred every third full moon (Figure 1).

It is unlikely that this was due to periodic changes in sex hormones since male mice were used. Moreover, the mice were used at the same age (six weeks), which rules out the possibility that these changes were the result of biological rhythms of a single individual undergoing its development. The immune response to PVP in vivo underwent changes similar to the antibody response to another B-dependent antigen, DNP-fi coll [50]. Interestingly, in the period of low antibody response, PG inhibitors enhanced the immune response, but inhibited it in the period of high immune response. The application of PG inhibitors during the lowest level of antibody production (close to background levels) was ineffective in enhancing the immune response. The effects of the lunar cycle on the antibody response to a T-dependent antigen, sheep erythrocytes (SRBCs), was also analyzed [52] and showed a regular cycle (13 peaks in the year, corresponding to 13 lunar months, with peak responses around the full moon days) (Figure 2). In addition, two distinct peaks in the anti-SRBC response in mice were registered in March and October [53].

Acceptance of the existence of such immune response variability has important implications. When interpreting experimental data, investigators should be aware of the magnitude of the control immune response on a given day. In particular, the immunoregulatory character of some compounds may be verified only after performing a series of experiments over a longer time period [46] and it strictly depends on the control immune response on the given day, resulting in stimulation, no effect, or suppression. Even the immunosuppresory effects of cyclosporine A are dependent on variability in the humoral and cellular immune response [54].

At this stage of investigation, the exact mechanism of the lunar effect on the immune response is hard to explain. The prime candidates to exert regulatory function on the immune response are melatonin and steroids, whose levels are affected by the moon cycle. Functional and pharmacological inhibition of melatonin synthesis resulted in depressed immune function in vivo [20]. Exogenous, evening administration of melatonin enhanced antibody formation and was also antagonized by the opioid receptor blocker naltrexone, indicating that the neurohormone regulates the immune response via opioid peptides [21]. Exogenous melatonin also completely counteracts the effect of acuteanxiety- restraint stress on thymus weight and antibody response to SRBC [22]. Melatonin treatment increased, in addition, the affinity and decreased the density of glucocorticoid and progestin receptors in non-immunized mice [34]. There is also evidence that the rise in corticosterone levels decreases T-dependent antibody response [13]. It is therefore tempting to speculate that the biorhythm observed in the antibody response to SRBC [52] could be due to lower levels of endogenous steroids around the full-moon days. On the other hand, the response to PVP was not affected by changes in steroid levels [13] which makes interpretation of the biorhythm in the immune response to PVP difficult. It is, however, possible that in this case, T-suppressor cells controlling the anti-PVP response are affected [51]. Although the immunostimulatory action of melatonin is well documented, it does not explain the peak responses at full-moon days when melatonin levels are low [18,38,41,42]. No direct correlation exists between melatonin and endogenous steroid levels, either [42]. Whereas a direct effect of lunar light may have significance in the fluctuation of physiological processes in free-living animals, it is unlikely that laboratory animals, kept in an isolated place (an animal facility) with a 12/12 h light/dark cycle, could also be subject to such effects. Other types of the moon‘s activity suggested by some authors, such as electromagnetic radiation [8] and the gravitational pull [43], would more likely be the primary causes of the described rhythms. It is also likely that laboratory animals which do not perceive lunar light, in contrast to free-living animals, have elevated concentrations of melatonin during full-moon days, as was shown in laboratory rats [23]. In such a case, the elevated antibody response in murine models could be explained [50,52]. There are indications that the cycling moon initiates neurohormonal activity in the hypothalamus and the pituitary gland [28]. Surprisingly, however, moon-induced cyclic changes in the steroid levels can also be observed in the honeybee, whose nervous system is much less complex [16].

In summary, the exact mechanism by which the moon affects behavior and physiology still has to be clarifi ed. The hitherto accumulated data indicate that knowledge of the rhythms elicited by the lunar cycle may be helpful in police surveillance, hospital practice, and animal laboratory research.

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