Chronobiology by moonlight

Most studies in chronobiology focus on solar cycles (daily and annual). Moonlight and the lunar cycle received considerably less attention by chronobiologists. An exception are rhythms in intertidal species. Terrestrial ecologists long ago acknowledged the effects of moonlight on predation success, and consequently on predation risk, foraging behaviour and habitat use, while marine biologists have focused more on the behaviour and mainly on reproduction synchronization with relation to the Moon phase. Lately, several studies in different animal taxa addressed the role of moonlight in determining activity and studied the underlying mechanisms. In this paper, we review the ecological and behavioural evidence showing the effect of moonlight on activity, discuss the adaptive value of these changes, and describe possible mechanisms underlying this effect. We will also refer to other sources of night-time light (‘light pollution’) and highlight open questions that demand further studies.

[1]  M. Saigusa Entrainment of Tidal and Semilunar Rhythms by Artificial Moonlight Cycles , 1988 .

[2]  M. Gorman,et al.  Circadian entrainment and phase resetting differ markedly under dimly illuminated versus completely dark nights , 2005, Behavioural Brain Research.

[3]  M. Gorman,et al.  Plasticity of Hamster Circadian Entrainment Patterns Depends on Light Intensity , 2003, Chronobiology international.

[4]  S. B. Linhart,et al.  Foraging Behavior of the Common Vampire Bat Related to Moonlight , 1972 .

[5]  G. Boeuf,et al.  Does light have an influence on fish growth , 1999 .

[6]  G. Körtner,et al.  Thermobiology, energetics and activity patterns of the Eastern tube-nosed bat (Nyctimene robinsoni) in the Australian tropics: effect of temperature and lunar cycle , 2010, Journal of Experimental Biology.

[7]  J. Aschoff,et al.  Masking of Circadian Activity Rhythms in Canaries by Light and Dark , 1989, Journal of biological rhythms.

[8]  J. Orton Sea-Temperature, Breeding and Distribution in Marine Animals , 1920, Journal of the Marine Biological Association of the United Kingdom.

[9]  R. Nelson,et al.  Chronic exposure to dim light at night suppresses immune responses in Siberian hamsters , 2011, Biology Letters.

[10]  H. Romijn,et al.  Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway , 1999, The European journal of neuroscience.

[11]  M. Bowers Seed Removal Experiments on Desert Rodents: The Microhabitat by Moonlight Effect , 1988 .

[12]  T. Dayan,et al.  The Effect of the Lunar Cycle on Fecal Cortisol Metabolite Levels and Foraging Ecology of Nocturnally and Diurnally Active Spiny Mice , 2011, PloS one.

[13]  V. Baumans,et al.  Short-term effects of a disturbed light–dark cycle and environmental enrichment on aggression and stress-related parameters in male mice , 2004, Laboratory animals.

[14]  B. Willis,et al.  Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef , 1986 .

[15]  N. Willoughby,et al.  Notes on the biology of the mayfly Povilla adusta in West Africa , 2009 .

[16]  L. Yan,et al.  Nighttime dim light exposure alters the responses of the circadian system , 2010, Neuroscience.

[17]  M. Saigusa Entrainment of a semilunar rhythm by a simulated moonlight cycle in the terrestrial crab, Sesarma haematocheir , 1980, Oecologia.

[18]  Joseph L. Ganey,et al.  Calling Behavior of Spotted Owls in Northern Arizona , 1990 .

[19]  R. Nelson,et al.  The dark side of light at night: physiological, epidemiological, and ecological consequences , 2007, Journal of pineal research.

[20]  G. Falkenberg,et al.  A Lunar Clock Changes Shielding Pigment Transparency in Larval Ocelli of Clunio marinus , 2008, Chronobiology International.

[21]  F. Raible,et al.  Another place, another timer: Marine species and the rhythms of life , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[22]  J. Mohawk,et al.  Circadian dependence of corticosterone release to light exposure in the rat , 2007, Physiology & Behavior.

[23]  R. Babcock,et al.  Self- and cross-fertilization in scleractinian corals , 1986 .

[24]  K. D. Frank,et al.  Impact of outdoor lighting on moths: an assessment , 1988 .

[25]  K. Schmidt,et al.  DAILY PATTERNS AND DURATION OF WOLF ACTIVITY IN THE BIAŁOWIEŻA FOREST, POLAND , 2003 .

[26]  R. Nelson,et al.  Influence of light at night on murine anxiety- and depressive-like responses , 2009, Behavioural Brain Research.

[27]  T. Dayan,et al.  Effect of artificial night lighting on temporally partitioned spiny mice , 2011 .

[28]  M. G. Oehmke Lunar periodicity in flight activity of honey bees , 1973 .

[29]  R. Nelson,et al.  Illuminating the deleterious effects of light at night , 2011, F1000 medicine reports.

[30]  J. Rydell,et al.  Exploitation of Insects around Streetlamps by Bats in Sweden , 1992 .

[31]  Uwe Redlin,et al.  NEURAL BASIS AND BIOLOGICAL FUNCTION OF MASKING BY LIGHT IN MAMMALS: SUPPRESSION OF MELATONIN AND LOCOMOTOR ACTIVITY , 2001, Chronobiology international.

[32]  S. Gursky Lunar Philia in a Nocturnal Primate , 2003, International Journal of Primatology.

[33]  P. Hardin,et al.  Nocturnal Male Sex Drive in Drosophila , 2007, Current Biology.

[34]  J. Woodley,et al.  Timing of reproduction in Montastraea annularis: relationship to environmental variables , 2002 .

[35]  J. Richardson,et al.  The effect of artificial light on male breeding-season behaviour in green frogs, Rana clamitans melanota , 2006 .

[36]  P. Kappeler,et al.  Nocturnal activity in the cathemeral red‐fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse , 2001, American journal of primatology.

[37]  H. Erkert,et al.  Chronobiological Background to Cathemerality: Circadian Rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea) , 2006, Folia Primatologica.

[38]  N. Mrosovsky,et al.  Impaired Masking Responses to Light in Melanopsin‐Knockout Mice , 2003, Chronobiology International.

[39]  R. A. Fuchs,et al.  Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning , 2004, Neurobiology of Learning and Memory.

[40]  T. Milsom,et al.  Activity patterns of Lapwings Vanellus vanellus in relation to the lunar cycle , 1990 .

[41]  M. Ciechanowski,et al.  Spatiotemporal variation in activity of bat species differing in hunting tactics: effects of weather, moonlight, food abundance, and structural clutter , 2007 .

[42]  R. Vásquez Assessment of predation risk via illumination level: facultative central place foraging in the cricetid rodent Phyllotis darwini , 1994, Behavioral Ecology and Sociobiology.

[43]  T. Dayan,et al.  Light Masking in the Field: An Experiment with Nocturnal and Diurnal Spiny Mice Under Semi-natural Field Conditions , 2011, Chronobiology international.

[44]  C. Patrick Doncaster,et al.  Jaguar and puma activity patterns in relation to their main prey , 2011 .

[45]  D. Neumann The Timing of Reproduction to Distinct Spring Tide Situations in the Intertidal Insect Clunio , 1988 .

[46]  Charalambos P. Kyriacou,et al.  Unexpected features of Drosophila circadian behavioural rhythms under natural conditions , 2012, Nature.

[47]  P. Falkowski,et al.  Photoreceptors in the cnidarian hosts allow symbiotic corals to sense blue moonlight , 2002 .

[48]  R. Sapolsky,et al.  Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy , 2008, Proceedings of the National Academy of Sciences.

[49]  Randy J. Nelson,et al.  Dim Nighttime Light Impairs Cognition and Provokes Depressive-Like Responses in a Diurnal Rodent , 2012, Journal of biological rhythms.

[50]  T. Dayan,et al.  TEMPORAL PARTITIONING: AN EXPERIMENT WITH TWO SPECIES OF SPINY MICE , 2005 .

[51]  J. Theuerkauf,et al.  Daily and seasonal variation in wolf activity in the Bieszczady Mountains, SE Poland , 2009 .

[52]  W. Jetz,et al.  Effects of light and prey availability on nocturnal, lunar and seasonal activity of tropical nightjars , 2003 .

[53]  K. V. Orsdol Foraging behaviour and hunting success of lions in Queen Elizabeth National Park, Uganda , 1984 .

[54]  J. Clarke Moonlight's influence on predator/prey interactions between short-eared owls (Asio flammeus) and deermice (Peromyscus maniculatus) , 1983, Behavioral Ecology and Sociobiology.

[55]  H. L. Stolov Further investigations of a variation of geomagnetic activity with lunar phase. , 1965 .

[56]  Effects of Simulated Moonlight on Activity in the Desert Nightsnake (Hypsiglena chlorophaea) , 2011 .

[57]  P. Pinet,et al.  Celestial Moderation of Tropical Seabird Behavior , 2011, PloS one.

[58]  Marcel E. Visser,et al.  Activity Patterns during Food Provisioning Are Affected by Artificial Light in Free Living Great Tits (Parus major) , 2012, PloS one.

[59]  Alexa Mills The influence of moonlight on the behavior of goatsuckers (Caprimulgidae) , 1986 .

[60]  Thomas A. Bass,et al.  Effects of Moonlight on Microhabitat Use by Desert Rodents , 1984 .

[61]  T. Halliday,et al.  The lunar cycle: a cue for amphibian reproductive phenology? , 2009, Animal Behaviour.

[62]  Sunggu Yang,et al.  Aberrant light directly impairs mood and learning through melanopsin-expressing neurons , 2012, Nature.

[63]  V. C. Moran,et al.  The solar-day activity rhythm of myrmeleontid larvae , 1969 .

[64]  D. W. Morrison Lunar phobia in a neotropical fruit bat, Artibevs jamaicensis (Chiroptera: Phyllostomidae) , 1978, Animal Behaviour.

[65]  G. Körtner,et al.  Metabolism: Winter torpor in a large bird , 2000, Nature.

[66]  P. Jokiel,et al.  Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis , 1985 .

[67]  D. Macdonald,et al.  Masking of the zeitgeber: African wild dogs mitigate persecution by balancing time , 2012 .

[68]  N. Mrosovsky,et al.  Masking of locomotor activity in hamsters , 1999, Journal of Comparative Physiology A.

[69]  M. Gorman,et al.  Potent Circadian Effects of Dim Illumination at Night in Hamsters , 2006, Chronobiology international.

[70]  J. Clarke,et al.  The effect of moonlight on activity patterns of adult and juvenile prairie rattlesnakes (Crotalus viridis viridis) , 1996 .

[71]  S. Harris,et al.  Street Lighting Disturbs Commuting Bats , 2009, Current Biology.

[72]  R. Brigham,et al.  Common Poorwill activity and calling behavior in relation to moonlight and predation , 2008 .

[73]  Travis Longcore,et al.  Ecological consequences of artificial night lighting , 2006 .

[74]  R. Cooper RELATIVE ABUNDANCE OF GEORGIA CAPRIMULGIDS BASED ON CALL-COUNTS , 1981 .

[75]  Travis Longcore,et al.  Ecological light pollution , 2004 .

[76]  M. Ryan,et al.  Light Levels Influence Female Choice in Túngara Frogs: Predation Risk Assessment?@@@Light Levels Influence Female Choice in Tungara Frogs: Predation Risk Assessment? , 1997 .

[77]  Kwang-Soo Kim,et al.  Anxiogenic-like effect of chronic corticosterone in the light-dark emergence task in mice. , 2006, Behavioral neuroscience.

[78]  Uwe Redlin,et al.  The circadian Clock mutant mouse: impaired masking response to light , 2004, Journal of Comparative Physiology A.

[79]  C. Simpson,et al.  Mass spawning of corals on a high latitude coral reef , 1994, Coral Reefs.

[80]  A. Castrucci,et al.  Effects of continuous exposure to light on behavioral dopaminergic supersensitivity , 1999, Biological Psychiatry.

[81]  S. Boldogh,et al.  The effects of the illumination of buildings on house-dwelling bats and its conservation consequences , 2007 .

[82]  Till Roenneberg,et al.  IS LIGHT-AT-NIGHT A HEALTH RISK FACTOR OR A HEALTH RISK PREDICTOR? , 2009, Chronobiology international.

[83]  R. Pettifor,et al.  Lunar-related reproductive behaviour in the badger (Meles meles) , 2006, acta ethologica.

[84]  H. O. de la Iglesia,et al.  Moonstruck Primates: Owl Monkeys (Aotus) Need Moonlight for Nocturnal Activity in Their Natural Environment , 2010, PloS one.

[85]  Joel s. Brown,et al.  Vigilance, patch use and habitat selection: Foraging under predation risk , 1999 .

[86]  Hans G. Erkert,et al.  Diurnality and nocturnality in nonhuman primates: comparative chronobiological studies in laboratory and nature , 2008 .

[87]  P. Pyle,et al.  You have printed the following article : The Effects of Weather and Lunar Cycle on Nocturnal Migration of Landbirds at Southeast Farallon Island , California , 2007 .

[88]  M. Willig,et al.  The Effect of Lunar Illumination on Movement and Activity of the Red Fig‐eating Bat (Stenodema rufum) , 1997 .

[89]  Burt P. Kotler,et al.  Factors Affecting Gerbil Foraging Behavior and Rates of Owl Predation , 1991 .

[90]  Z. Dubinsky,et al.  Photobehavior of stony corals: responses to light spectra and intensity , 2003, Journal of Experimental Biology.

[91]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[92]  J. Clarke,et al.  Microhabitat Use by Brown Treesnakes (Boiga irregularis): Effects of Moonlight and Prey , 2008 .

[93]  V. Penteriani,et al.  Individual status, foraging effort and need for conspicuousness shape behavioural responses of a predator to moon phases , 2011, Animal Behaviour.

[94]  Yun-Wei A Hsu,et al.  Biological clocks and rhythms in intertidal crustaceans. , 2010, Frontiers in bioscience.

[95]  J. Hirsh,et al.  Roles of Dopamine in Circadian Rhythmicity and Extreme Light Sensitivity of Circadian Entrainment , 2010, Current Biology.

[96]  M. Ryan,et al.  Light Levels Influence Female Choice in Tiingara Frogs: Predation Risk Assessment? , 1997 .

[97]  L. S. Mills,et al.  Mortality by moonlight: predation risk and the snowshoe hare , 2005 .

[98]  G. H. Parker Tierbau und Tierleben , 1915 .

[99]  V. Bretagnolle,et al.  Predation risk and moonlight avoidance in nocturnal seabirds , 2000 .

[100]  J. Millar,et al.  The effects of moonlight on nocturnal activity in bushy-tailed wood rats (Neotoma cinerea) , 1999 .

[101]  H. D. Jackson ASPECTS OF THE BREEDING BIOLOGY OF THE FIERYNECKED NIGHTJAR , 1985 .

[102]  I. Meinertzhagen,et al.  The Extraretinal Eyelet of Drosophila: Development, Ultrastructure, and Putative Circadian Function , 2002, The Journal of Neuroscience.

[103]  P. Corbet Lunar Periodicity of Aquatic Insects in Lake Victoria , 1958, Nature.

[104]  R. Ben-Shlomo,et al.  Annual rhythms that underlie phenology: biological time-keeping meets environmental change , 2013, Proceedings of the Royal Society B: Biological Sciences.

[105]  Deborah L. Miller,et al.  Effects of Coastal Lighting on Foraging Behaviorof Beach Mice , 2004 .

[106]  Menna E. Jones,et al.  COEXISTENCE OF TEMPORALLY PARTITIONED SPINY MICE: ROLES OF HABITAT STRUCTURE AND FORAGING BEHAVIOR , 2001 .

[107]  Dina K. N. Dechmann,et al.  Activity levels of bats and katydids in relation to the lunar cycle , 2005, Oecologia.

[108]  N. Høiby,et al.  Summary and Perspectives , 2011 .

[109]  J. Aschoff,et al.  Exogenous and endogenous components in circadian rhythms. , 1960, Cold Spring Harbor symposia on quantitative biology.

[110]  B. Bell,et al.  Dependence of the lunar modulation of geomagnetic activity on the celestial latitude of the Moon , 1966 .

[111]  J. Aschoff,et al.  Masking of circadian activity rhythms in hamsters by darkness , 1988, Journal of Comparative Physiology A.

[112]  G. Tsujimoto,et al.  Light activates the adrenal gland: timing of gene expression and glucocorticoid release. , 2005, Cell metabolism.

[113]  R. Brigham,et al.  Does Moonlight Change Vertical Stratification of Activity by Forest-Dwelling Insectivorous Bats? , 1999 .

[114]  Angelika Scheideler,et al.  Seasonal Variation of Temporal Niche in Wild Owl Monkeys (Aotus azarai azarai) of the Argentinean Chaco: A Matter of Masking? , 2012, Chronobiology international.

[115]  Darren J. Bender,et al.  Lunar Condition Influences Coyote (Canis latrans) Howling , 1996 .

[116]  C. Helfrich-Förster,et al.  Moonlight shifts the endogenous clock of Drosophila melanogaster , 2007, Proceedings of the National Academy of Sciences.

[117]  F. Brischoux,et al.  Is it better in the moonlight? Nocturnal activity of insular cottonmouth snakes increases with lunar light levels , 2012 .

[118]  R. Brigham,et al.  Lunar Influence on Foraging and Nesting Activity of Common Poorwills (Phalaenoptilus Nuttallii) , 1992 .

[119]  Lucia F. Jacobs,et al.  Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami , 1992, Animal Behaviour.

[120]  P. Harrison,et al.  Reproduction, dispersal and recruitment of scleractinian corals , 1990 .

[121]  J. Partecke,et al.  Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences? , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[122]  R. Young,et al.  A note on the effect of the full moon on the activity of wild maned wolves, Chrysocyon brachyurus , 2006, Behavioural Processes.

[123]  Karrigan S Börk Lunar phobia in the greater fishing bat Noctilio leporinus (Chiroptera: Noctilionidae). , 2006, Revista de biologia tropical.

[124]  B. Smit,et al.  Torpor in Dark Times: Patterns of Heterothermy Are Associated with the Lunar Cycle in a Nocturnal Bird , 2011, Journal of biological rhythms.

[125]  W. Kerfoot The lunar periodicity of Sphecodogastra texana, a nocturnal bee (Hymenoptera: Halictidae). , 1967, Animal behaviour.

[126]  C. Darwin The Descent of Man and Selection in Relation to Sex: INDEX , 1871 .

[127]  C. Helfrich-Förster,et al.  The Nocturnal Activity of Fruit Flies Exposed to Artificial Moonlight Is Partly Caused by Direct Light Effects on the Activity Level That Bypass the Endogenous Clock , 2009, Chronobiology international.

[128]  C. Helfrich-Förster,et al.  The Fruit Fly Drosophila melanogaster Favors Dim Light and Times Its Activity Peaks to Early Dawn and Late Dusk , 2007, Journal of biological rhythms.

[129]  C. Simpson,et al.  Destruction of corals and other reef animals by coral spawn slicks on Ningaloo Reef, Western Australia , 1993, Coral Reefs.

[130]  S. L. Lima,et al.  Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs , 2009, Hormones and Behavior.

[131]  D. Heckel,et al.  Genetic Architecture of Local Adaptation in Lunar and Diurnal Emergence Times of the Marine Midge Clunio marinus (Chironomidae, Diptera) , 2012, PloS one.

[132]  M. Gorman,et al.  Dim nocturnal illumination alters coupling of circadian pacemakers in Siberian hamsters, Phodopus sungorus , 2004, Journal of Comparative Physiology A.

[133]  D. Dominoni,et al.  Artificial light at night advances avian reproductive physiology , 2013, Proceedings of the Royal Society B: Biological Sciences.

[134]  B. Kempenaers,et al.  Artificial Night Lighting Affects Dawn Song, Extra-Pair Siring Success, and Lay Date in Songbirds , 2010, Current Biology.

[135]  H. Caspers Spawning periodicity and habitat of the palolo worm Eunice viridis (Polychaeta: Eunicidae) in the Samoan Islands , 1984 .

[136]  A. Szmant Reproductive ecology of Caribbean reef corals , 1986, Coral Reefs.

[137]  D. Hayward,et al.  Light-Responsive Cryptochromes from a Simple Multicellular Animal, the Coral Acropora millepora , 2007, Science.

[138]  Foraging Behaviour in Relation to the Lunar Cycle by Australian Owlet-nightjars Aegotheles cristatus , 1999 .

[139]  C. Bost,et al.  Corticosterone and foraging behavior in a diving seabird: the Adélie penguin, Pygoscelis adeliae. , 2008, General and comparative endocrinology.

[140]  C. Helfrich-Förster,et al.  Drosophila timeless2 Is Required for Chromosome Stability and Circadian Photoreception , 2010, Current Biology.

[141]  Randy J. Nelson,et al.  Light at night increases body mass by shifting the time of food intake , 2010, Proceedings of the National Academy of Sciences.

[142]  Hsu Yw,et al.  Biological clocks and rhythms in intertidal crustaceans. , 2010 .

[143]  V. Penteriani,et al.  Moonlight Makes Owls More Chatty , 2010, PloS one.

[144]  M. V. Price,et al.  Direct Observations of Owls and Heteromyid Rodents: Can Predation Risk Explain Microhabitat Use? , 1991 .

[145]  B. Willis,et al.  Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984 , 1985 .

[146]  M. Ryan,et al.  Evasive behaviour of a frog in response to bat predation , 1982, Animal Behaviour.

[147]  P. Pye-Smith The Descent of Man, and Selection in Relation to Sex , 1871, Nature.

[148]  B. Willis,et al.  Mass Spawning in Tropical Reef Corals , 1984, Science.

[149]  Mark W. Miller Apparent Effects of Light Pollution on Singing Behavior of American Robins , 2006 .

[150]  J. Szyndler,et al.  The effects of acute corticosterone administration on anxiety, endogenous corticosterone, and c-Fos expression in the rat brain , 2007, Hormones and Behavior.