Erasing day/night differences in light intensity and spectrum affect biodiversity and the health of mammals by confusing the circadian clock

Zdeňka Bendová 1  and Simona Moravcová 1
  • 1 National Institute of Mental Health, 250 67, Klecany

Abstract

The beneficial effect of sunlight on all forms of life has been well-known to human cultures worldwide throughout history. However, the importance of darkness for survival, successful reproduction and the overall fitness of all organisms is fully appreciated only by physiologists and environmental biologists. Seasonal variations in environmental conditions (i.e., rainfall, temperature, barometric pressure, food availability) significantly affect reproduction and survival but they are of little predictive value. In contrast, daily fluctuations in light levels and the light spectrum are less dramatic in their impact on life, but were highly predictable throughout evolution. Natural selection has thus favored a strategy of monitoring a day’s length as a predictor of changes in external conditions by the development of the molecular circadian clock, which is sensitive to changes in light/darkness during the day and night. Well-synchronized circadian clockwork ensures that behavioral and physiological processes fluctuate with the daily solar cycle and programs the seasonal changes in physiology via the transduction of the photoperiod into hormonal messages. During the last two decades, energy-efficient lighting technology has shifted from “yellow” high-pressure sodium vapor lamps to new “white” light-emitting diodes (LEDs). As a consequence, nighttime light pollution increased, and the sharp difference between day and night has been erased in many parts of the world, which threatens animal ecology and human health. Studies on humans, laboratory mammals and wildlife suggest that the physiological costs of living under artificial light at night (ALAN) may be due to the disruption of circadian and circannual timing. This overview summarizes the recent findings on the effect of the blurred day/night difference on the circadian clock, nighttime melatonin secretion and photoperiodic changes in mammals and suggests that the gradual decline of fitness due to the increasing ALAN measured in the human population may contribute to the changes in mammalian biodiversity in nature.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Al-Naggar R. A. & Anil S., 2016: Artificial light at night and cancer: global study. Asian Pacific Journal of Cancer Prevention, 17: 4661–4664.

  • Aubé M., Roby J. & Kocifaj M., 2013: Evaluating potential spectral impacts of various artificial lights on melatonin suppression, photosynthesis, and star visibility. Public Library of Science One, 8(7): 1–15.

  • Aubrecht G. T., Jenkins R. & Nelson R. J., 2015: Dim light at night increases body mass of female mice. Chronobiology International, 32: 557–560.

  • Azam C., Kerbiriou C., Vernet A., Julien J. F., Bas Y., Plichard L., Maratrat J. & Le Viol I., 2015: Is part-night lighting an effective measure to limit the impacts of artificial lighting on bats? Global Change Biology, 21: 4333–4341.

  • Balsalobre A., 2002: Clock genes in mammalian peripheral tissues. Cell and Tissue Research, 309: 193–199.

  • Barrett P., Ebling F. J. P., Schuhler S., Wilson D., Ross A. W., Warner A., Jethwa P., Boelen A., Visser T. J. & Ozanne D. M., 2007: Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology, 148: 3608–3617.

  • Bartness T. J. & Wade G. N., 1985: Photoperiodic control of seasonal body weight cycles in hamsters. Neuroscience & Biobehavioral Reviews, 9: 599–612.

  • Bauer S. E., Wagner S. E., Burch J., Bayakly R. & Vena J. E., 2013: A case-referent study: light at night and breast cancer risk in Georgia. International Journal of Health Geographics, 12: 1–10.

  • Bedrosian T. A., Weil Z. M. & Nelson R. J., 2013: Chronic dim light at night provokes reversible depression-like phenotype: possible role for TNF. Molecular Psychiatry, 18: 930–936.

  • Berson D. M., Castrucci A. M. & Provencio I., 2010: Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. Journal of Comparative Neurology, 518: 2405–2422.

  • Bellingham J., Chaurasia S. S., Melyan Z., Liu C., Cameron M. A., Tarttelin E. E., Iuvone P. M., Hankins M. W., Tosini G. & Lucas R. J., 2006: Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. Public Library of Science Biology, 4: 1334–1343.

  • Bhadra U., Thakkar N., Das P. & Pal Bhadra M., 2017: Evolution of circadian rhythms: from bacteria to human. Sleep Medicine, 35: 49–61.

  • Blask D. E., 2009: Melatonin, sleep disturbance and cancer risk. Sleep Medicine Reviews, 13: 252–264.

  • Blask D. E., Sauer L. A. & Dauchy R. T., 2002: Melatonin as a chronobiotic/anticancer agent: cellular, biochemical, and molecular mechanisms of action and their implications for circadian-based cancer therapy. Current Topic in Medicinal Chemistry, 2: 113–132.

  • Blask D. E., Dauchy R. T., Sauer L. A., 2005a: Putting cancer to sleep at night: the neuroendocrine/circadian melatonin signal. Endocrine, 27: 179–188.

  • Blask D. E., Brainard G. C., Dauchy R. T., Hanifin J. P., Davidson L. K., Krause J. A., Sauer L. A., Rivera-Bermudez M. A., Dubocovich M. L., Jasser S. A., Lynch D. T., Rollag M. D. & Zalatan F., 2005b: Melatonin-depleted blood from premenopausal women exposed to light at night stimulates growth of human breast cancer xenografts in nude rats. Cancer Research, 65: 11174–11184.

  • Borniger J. C., Maurya S. K., Periasamy M. & Nelson R. J., 2014: Acute dim light at night increases body mass, alters metabolism, and shifts core body temperature circadian rhythms. Chronobiology International, 31: 917–925.

  • Brainard G. C., Richardson B. A., Petterborg L. J. & Reiter R. J., 1982: The effect of different light intensities on pineal melatonin content. Brain Research, 233: 75–81.

  • Brainard G. C., Richardson B. A., Hurlb ut E. C., Steinlechner S., Matthews S. A. & Reiter R. J., 1984a: The influence of various irradiances of artificial light, twilight, and moonlight on the suppression of pineal melatonin content in the Syrian hamster. Journal of Pineal Research, 1: 105–119.

  • Brainard G. C., Richardson B. A., King T. S. & Reiter R. J., 1984b: The influence of different light spectra on the suppression of pineal melatonin content in the Syrian hamster. Brain Research, 294: 333–339.

  • Brainard G. C., Hanifin J. P., Greeson J. M., Byrne B., Glickman G., Gerner E. W. & Rollag M. D., 2001: Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. Journal of Neuroscience, 21: 6405–6412.

  • Brainard G. C., Sliney D., Hanifin J. P., Glickman G., Byrne B., Greeson J. M., Jasser S., Gerner E. & Rollag M. D., 2008: Sensitivity of the human circadian system to short-wavelength (420-nm) light. Journal of Biological Rhythms, 23: 379–386.

  • Brown G. M., 1994: Light, melatonin and the sleep-wake cycle. Journal of Psychiatry and Neuroscience, 19: 345–353.

  • Brüning A., Hölker F., Franke S., Kleiner W. & Kloas W., 2016: Impact of different colours of artificial light at night on melatonin rhythm and gene expression of gonadotropins in European perch. Science of the Total Environment, 543: 214–222.

  • Cabrera-Cruz S. A., Smolinsky J. A. & Buler J. J., 2018: Light pollution is greatest within migration passage areas for nocturnally-migrating birds around the world. Scientific Reports, 8: 1–8.

  • Cajochen C., Münch M., Kobialka S., Kräuchi K., Steiner R., Oelhafen P., Orgül S. & Wirz-Justice A., 2005: High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light. Journal of Clinical Endocrinology & Metabolism, 90: 1311–1316.

  • Carlson D. E. & Chiu W. C., 2008: The absence of circadian cues during recovery from sepsis modifies pituitary-adrenocortical function and impairs survival. Shock, 29: 127–132.

  • Carrill o-Vico A., Lardone P. J., Alv arez-Sánchez N., Rodríguez-Rodríguez A. & Guerrero J. M., 2013: Melatonin: buffering the immune system. International Journal of Molecular Sciences, 14: 8638–8683.

  • Castanon-Cervantes O., Wu M., Ehlen J. C., Paul K., Gamble K. L., Johnson R. L., Besing R. C., Menaker M., Gewirtz A. T. & Davidson A. J., 2010: Dysregulation of inflammatory responses by chronic circadian disruption. Journal of Immunology, 185: 5796–5805.

  • Chang A. M., Scheer F. A. & Czeisler C. A., 2011: The human circadian system adapts to prior photic history. Journal of Physiology, 589: 1095–1102.

  • Cho Y., Ryu S. H., Lee B. R., Kim K. H., Lee E. & Choi J., 2015: Effects of artificial light at night on human health: A literature review of observational and experimental studies applied to exposure assessment. Chronobiology International, 32: 1294–1310.

  • Cipoll a-Neto J., Amaral F. G., Afeche S. C., Tan D. X., Reiter R. J., 2014: Melatonin, energy metabolism, and obesity: a review. Journal of Pineal Research, 56: 371–381.

  • Coomans C. P., van den Berg S. A., Houben T., van Klinken J. B., van den Berg R., Pronk A. C., Havekes L. M., Romijn J. A., van Dijk K. W., Biermasz N. R. & Meijer J. H., 2013: Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. The Federation of American Societies for Experimental Biology Journal, 27: 1721–1732.

  • Cos S., Mediavill a D., Martínez-Campa C., González A., Alonso-González C. & Sánchez-Barceló E. J., 2006: Exposure to light-at-night increases the growth of DMBA-induced mammary adenocarcinomas in rats. Cancer Letters, 235: 266–271.

  • Cravens Z. M. & Boyles J. G., 2018: Illuminating the physiological implications of artificial light on an insectivorous bat community. Oecologia, 189: 69–77.

  • Csaba G. & Barath P., 1975: Morphological changes of thymus and the thyroid gland after postnatal extirpation of pineal body. Endocrinologia Experimentalis, 9: 59–67.

  • Cutty G. B., Goldman B. D., Doherty P. & Bartke A., 1981: Melatonin prevents decrease in plasma PRL and LH levels in male hamsters exposed to a short photoperiod. International Journal of Andrology, 4: 281–290.

  • Czeisler C.-A., All an J. S., Strogatz S. H., Ronda J. M., Sánchez R., Ríos C. D., Freitag W. O., Richardson G. S. & Kronauer R. E., 1986: Bright light resets the human circadian pacemaker independent of the timing of the sleep-wake cycle. Science, 233: 667–671.

  • Dardente H., Wyse C. A., Birnie M. J., Dupré S. M., Loudon A. S., Lincoln G. A. & Hazlerigg D. G., 2010: A molecular switch for photoperiod responsiveness in mammals. Current Biology, 20: 2193–2198.

  • Dauchy R. T., Sauer L. A., Blask D. E. & Vaughan G. M., 1997: Light contamination during the dark phase in “photoperiodically controlled” animal rooms: effect on tumor growth and metabolism in rats. Laboratory Animal Science, 47: 511–518.

  • De Jong M., Ouyang J. Q., Da Silv a A., van Grunsven R. H., Kempenaers B., Visser M. E. & Spoelstra K., 2015: Effects of nocturnal illumination on life-history decisions and fitness in two wild songbird species. Philosophical Transactions of the Royal Society B, Biological Sciences, 370: 1–8.

  • de Jong M., Lamers K. P., Eugster M., Ouyang J. Q., Da Silv a A., Mateman A. C., van Grunsven R. H. A., Visser M. E. & Spoelstra K., 2018: Effects of experimental light at night on extra-pair paternity in a songbird. Journal of Experimental Zoology, Part A, Ecological and Integrative Physiology, 329: 441–448.

  • De Molenaar J. G., Sanders M. E. & Jonkers D. A., 2006: Roadway lighting and grassland birds: local influences of road lighting on a black-tailed godwit population. Pp.: 114–136. In: Rich C. & Longcore T. (eds.): Ecological Consequences of Artificial Night Lighting, Island Press, Washington, DC, 480 pp.

  • Dibner C., Schibler U. & Albrecht U., 2010: The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72: 517–549.

  • Dimovski A. M. & Robert K. A., 2018: Artificial light pollution: Shifting spectral wavelengths to mitigate physiological and health consequences in a nocturnal marsupial mammal. Journal of Experimental Zoology, Part A, Ecological and Integrative Physiology, 329: 497–505.

  • Dominoni D. M. & Partecke J., 2015: Does light pollution alter daylength? A test using light loggers on free-ranging European blackbirds (Turdus merula). Philosophical Transactions of the Royal Society B, Biological Sciences, 370: 1–8.

  • Dominoni D., Quetting M. & Partecke J., 2013: Artificial light at night advances avian reproductive physiology. Proceedings of the Royal Society B, Biological Sciences, 280: 1–8.

  • Ebl ing F. J. P., 2014: On the value of seasonal mammals for identifying mechanisms underlying the control of food intake and body weight. Hormones and Behavior, 66: 56–65.

  • Eisenbeis G., 2006: Artificial night lighting and insects: attraction of insects to streetlamps in a rural setting in Germany. Pp.: 281–304. In: Rich C. & Longcore T. (eds.): Ecological Consequences of Artificial Night Lighting. Island Press, Washington, DC, 480 pp.

  • Falchi F., Cinzano P., Duriscoe D., Kyba C. C. M., Elv idge C. D., Baugh K., Portnov B. A., Rybnikova N. A. & Furgoni R., 2016: The new world atlas of artificial night sky brightness. Science Advances, 2: 1–25.

  • Favero G., Franceschetti L., Bonomini F., Rodella L. F. & Rezzani R., 2017: Melatonin as an antiinflammatory agent modulating inflammasome activation. International Journal of Endocrinology, 2017: 1–13.

  • Figueiro M. G., 2017: Disruption of circadian rhythms by light during day and night. Current Sleep Medicine Reports, 3: 76–84.

  • Firebaugh A. & Haynes K. J., 2016: Experimental tests of light-pollution impacts on nocturnal insect courtship and dispersal. Oecologia, 182: 1203–1211.

  • Fonken L. K. & Nelson R. J., 2013: Dim light at night increases depressive-like responses in male C3H/HeNHsd mice. Behavioural Brain Research, 243: 74–78.

  • Fonken L. K., Kitsmiller E., Smale L. & Nelson R. J., 2012: Dim nighttime light impairs cognition and provokes depressive-like responses in a diurnal rodent. Journal of Biological Rhythms, 27: 319–327.

  • Fonken L. K., Aubrecht T. G., Meléndez-Fernandés O. H., Weil Z. M. & Nelson R. J., 2013: Dim light at night disrupts molecular circadian rhythms and increases body weight. Journal of Biological Rhythms, 28: 262–271.

  • Frank K. D., 2006: Effects of artificial night lighting on moths. Pp.: 305–344. In: Rich C. & Longcore T. (eds.): Ecological Consequences of Artificial Night Lighting. Island Press, Washington, DC, 480 pp.

  • Freeman D. A., Teubner B. J., Smith C. D. & Prendergast B. J., 2007: Exogenous T3 mimics long day lengths in Siberian hamsters. American Journal of Physiology, Regulatory Integrative and Comparative Physiology, 292: R2368–R2372.

  • Freitas J. R., Bennie J., Mantovani W., Gaston K. J., 2017: Exposure of tropical ecosystems to artificial light at night: Brazil as a case study. Public Library of Science One, 12: 1–12.

  • Full er G., Raghanti M. A., Dennis P. M., Kuhar C. W., Will is M. A., Schook M. W. & Lukas K. E., 2016: A comparison of nocturnal primate behavior in exhibits illuminated with red and blue light. Applied Animal Behaviour Science, 184: 126–134.

  • Gauthreaux S. A. & Belser C. G., 2006: Effects of artificial night lighting on migrating birds. Pp.: 67–93. In: Rich C. & Longcore T. (eds.): Ecological Consequences of Artificial Night Lighting. Island Press, Washington, DC, 480 pp.

  • Giudice A., Crispo A., Grimaldi M., Polo A., Bimonte S., Capunzo M., Amore A., D’Arena G., Cerino P., Budillon A., Botti G., Costantini S. & Montella M., 2018: The effect of light exposure at night (LAN) on carcinogenesis via decreased nocturnal melatonin synthesis. Molecules, 23: 1–14.

  • Golombek D. A. & Rosenstein R. E., 2010: Physiology of circadian entrainment. Physiological Reviews, 90: 1063–1102.

  • Golombek D. A., Pandi-Perumal S. R., Brown G. M. & Cardinali D. P., 2015: Some implications of melatonin use in chronopharmacology of insomnia. European Journal of Pharmacology, 762: 42–48.

  • Gooley J. J., Lu J., Fischer D. & Saper C. B., 2003: A broad role for melanopsin in nonvisual photoreception. Journal of Neuroscience, 23: 7093–7106.

  • Grubisic M., van Grunsven R. H. A., Manfrin A., Monaghan M. T. & Hölker F., 2018: A transition to white LED increases ecological impacts of nocturnal illumination on aquatic primary producers in a lowland agricultural drainage ditch. Environmental Pollution, 240: 630–638.

  • Haim A. & Zubidat A. E., 2015: Artificial light at night: melatonin as a mediator between the environment and epigenome. Philosophical Transactions of the Royal Society B, Biological Sciences, 370: 1–7.

  • Hannibal J., Hindersson P., Knudsen S. M., Georg B. & Fahrenkrug J., 2002a: The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. Journal of Neuroscience, 22: 1–7.

  • Hannibal J., Hindersson P., Nevo E. & Fahrenkrug J., 2002b: The circadian photopigment melanopsin is expressed in the blind subterranean mole rat, Spalax. Neuroreport, 13: 1411–1414.

  • Hannibal J., Kankipati L., Strang C. E., Peterson B. B., Dacey D. & Gamlin P. D., 2014: Central projections of intrinsically photosensitive retinal ganglion cells in the macaque monkey. Journal of Comparative Neurology, 522: 2231–2248.

  • Hardeland R., Cardinali D. P., Brown G. M. & Pandi-Perumal S. R., 2015: Melatonin and brain inflammaging. Progress in Neurobiology, 127–128: 46–63.

  • Hatori M. & Panda S., 2010: The emerging roles of melanopsin in behavioral adaptation to light. Trends in Molecular Medicine, 16: 435–446.

  • Hatori M., Gronfier C., Van Gelder R. N., Bernstein P. S., Carreras J., Panda S., Marks F., Sliney D., Hunt C. E., Hirota T., Furukawa T. & Tsubota K., 2017: Global rise of potential health hazards caused by blue light-induced circadian disruption in modern aging societies. Nature Partner Journals, Aging and Mechanisms of Disease, 3: 1–3.

  • Hattar S., Liao H. W., Takao M., Berson D. M. & Yau K. W., 2002: Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science, 295: 1065–1070.

  • Hazlerigg D. & Loudon A., 2008: New insights into ancient seasonal life timers. Current Biology, 18: R795–R804.

  • Hébert M., Martin S. K., Lee C. & Eastman C. I., 2002: The effects of prior light history on the suppression of melatonin by light in humans. Journal of Pineal Research, 33: 198–203.

  • Helm B., Ben-Shlomo R., Sheriff M. J., Hut R. A., Foster R., Barnes B. M. & Dominoni D., 2013: Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proceedings of the Royal Society B, Biological Sciences, 280: 1–10.

  • Henningsen J. B., Gauer F. & Simonneaux V., 2016: RFRP Neurons – The doorway to understanding seasonal reproduction in mammals. Frontiers in Endocrinology, 7(36): 1–10.

  • Hoffmann K., 1979: Photoperiod, pineal, melatonin and reproduction in hamster. Pp.: 397–415. In: Ariëns-Kappers & Pevet P. (eds.): The Pineal Gland of Vertebrates Including Man. Progress in Brain Research 52. Elsevier & North Holland Biomedical Press, Amsterdam, 562 pp.

  • Hoffmann K., Illnerová H. & Vanĕček J., 1981: Effect of photoperiod and of one minute light at nighttime on the pineal rhythm on N-acetyltransferase activity in the Djungarian hamster Phodopus sungorus. Biology of Reproduction, 24: 551–556.

  • Hoffmann K., Illnerová H. & Vanĕček J., 1986: Change in duration of the nighttime melatonin peak may be a signal driving photoperiodic responses in the Djungarian hamster (Phodopus sungorus). Neuroscience Letters, 67: 68–72.

  • Hölker F., Wolter C., Perkin E. K. & Tockner K., 2010: Light pollution as a biodiversity threat. Trends in Ecology & Evolution, 25: 681–682.

  • Hurley S., Goldberg D., Nelson D., Hertz A., Horn-Ross P. L., Bernstein L. & Reynolds P., 2014: Light at night and breast cancer risk among California teachers. Epidemiology, 25: 697–706.

  • Ikegami K. & Yoshimura T., 2012: Circadian clocks and the measurement of daylength in seasonal reproduction. Molecular and Cellular Endocrinology, 349: 76–81.

  • Ikeno T., Numata H., Goto S. G. & Shiga S., 2014: Involvement of the brain region containing pigmentdispersing factor-immunoreactive neurons in the photoperiodic response of the bean bug, Riptortus pedestris. Journal of Experimental Biology, 217: 453–462.

  • Illnerová H. & Vanĕček J., 1979: Response of rat pineal serotonin N-acetyltransferase to one min light pulse at different night times. Brain Research, 167: 431–434.

  • Illnerová H. & Vaněček J., 1980: Pineal rhythm in N-acetyltransferase activity in rats under different artificial photoperiods and in natural daylight in the course of a year. Neuroendocrinology, 31: 321–326.

  • Illnerová H., Vanĕček J., Křeček J., Wetterberg L. & Sääf J., 1979: Effect of one minute exposure to light at night on rat pineal serotonin N-acetyltransferase and melatonin. Journal of Neurochemistry, 32: 673–675.

  • Jeong M. J. & Jeon C. J., 2015: Localization of melanopsin-immunoreactive cells in the Mongolian gerbil retina. Neuroscience Research, 100: 6–16.

  • Jeong M. J., Kim H. G. & Jeon C. J., 2018: The organization of melanopsin-immunoreactive cells in microbat retina. Public Library of Science One, 13(1): 1–21.

  • Joshi D. S. & Chandrashekaran M. K., 1984: Bright light flashes of 0.5 msec reset the circadian clock of a michrochiropteran bat. Journal of Experimental Zoology, 230: 325–328.

  • Joshi D. S. & Chandrashekaran M. K., 1985: Light flashes of different durations phase shift the circadian flight activity of a bat. Journal of Experimental Zoology, 233: 187–192.

  • Jusuf P. R., Lee S. C., Hannibal J. & GrÜnert U., 2007: Characterization and synaptic connectivity of melanopsincontaining ganglion cells in the primate retina. European Journal of Neuroscience, 26: 2906–2921.

  • Kalsbeek A., Bruinstroop E., Yi C. X., Klieverik L. P., La Fleur S. E. & Fliers E., 2010: Hypothalamic control of energy metabolism via the autonomic nervous system. Annals of the New York Academy of Science, 1212: 114–129.

  • Kalsbeek A., Yi C. X., Cailotto C., la Fleur S. E., Fliers E. & Buijs R. M., 2011: Mammalian clock output mechanisms. Essays in Biochemistry, 49: 137–151.

  • Kempenaers B., Borgström P., Loës P., Schlicht E. & Valcu M., 2010: Artificial night lighting affects dawn song, extra-pair siring success, and lay date in songbirds. Current Biology, 20: 1735–1739.

  • Keshet-Sitton A., Or-Chen K., Huber E. & Haim A., 2017: Illuminating a risk for breast cancer: A preliminary ecological study on the association between streetlight and breast cancer. Integrative Cancer Therapies, 16: 451–463.

  • Kim Y. J., Lee E., Lee H. S., Kim M. & Park M. S., 2015: High prevalence of breast cancer in light polluted areas in urban and rural regions of South Korea: An ecologic study on the treatment prevalence of female cancers based on National Health Insurance data. Chronobiology International, 32: 657–667.

  • Kim Y. J., Park M. S., Lee E. & Choi J. W., 2016: High incidence of breast cancer in light-polluted areas with spatial effects in Korea. Asian Pacific Journal of Cancer Prevention, 17: 361–367.

  • Kim K. Y., Lee E., Kim Y. J. & Kim J., 2017: The association between artificial light at night and prostate cancer in Gwangju City and South Jeolla Province of South Korea. Chronobiology International, 34: 203–211.

  • Klein D. C. & Weller J. L, 1970: Indole metabolism in the pineal gland: a circadian rhythm in N-acetyltransferase. Science, 169: 1093–1095.

  • Klein D. C., Sugden D. & Well er J. L., 1983: Postsynaptic alpha-adrenergic receptors potentiate the beta-adrenergic stimulation of pineal serotonin N-acetyltransferase. Proceedings of the National Academy of Sciences of the United States of America, 80: 599–603.

  • Klein D. C., 1985: Photoneural regulation of the mammalian pineal gland. Pp.: 38–56. In: Evered D. & Clark S. (eds.): Photoperiodism, Melatonin and the Pineal. Ciba Foundation Symposium 117. Pitman, London, 320 pp.

  • Kloog I., Haim A., Stevens R. G. & Portnov B. A., 2009: Global co-distribution of light at night (LAN) and cancers of prostate, colon, and lung in men. Chronobiology International, 26: 108–125.

  • Kyba C. C. M., Ruhtz T., Fischer J. & Hölker F., 2012: Red is the new black: how the colour of urban skyglow varies with cloud cover. Monthly Notices of the Royal Astronomical Society, 425: 701–708.

  • Kyba C. C. M. & Hölker F., 2013: Do artificially illuminated skies affect biodiversity in nocturnal landscapes? Landscape Ecology, 28: 1637–1640.

  • Kyba C. C. M., Kuester T., Sánchez de Miguel A., Baugh K., Jechow A., Hölker F., Bennie J., Elv idge C. D., Gaston K. J. & Guanter L., 2017: Artificially lit surface of Earth at night increasing in radiance and extent. Science Advances, 3(11): 1–8.

  • La Sorte F. A., Fink D., Buler J. J., Farnsworth A. & Cabrera-Cruz S. A., 2017: Seasonalassociations with urban light pollution for nocturnally migrating bird populations. Global Change Biology, 23: 4609–4619.

  • Lacoeuilhe A., Machon N., Julien J. F., Le Bocq A. & Kerbiriou C., 2014: The influence of low intensities of light pollution on bat communities in a semi-natural context. Public Library of Science One, 9(10): 1–8.

  • Langel J. L., Smale L., Esquiva G. & Hannibal J., 2015: Central melanopsin projections in the diurnal rodent, Arvicanthis niloticus. Frontiers in Neuroanatomy, 9(93): 1–17.

  • Le Tallec T., Théry M. & Perret M., 2016: Melatonin concentrations and timing of seasonal reproduction in male mouse lemurs (Microcebus murinus) exposed to light pollution. Journal of Mammalogy, 97: 753–760.

  • Leliavski A., Dumbell R., Ott V. Oster H., 2015: Adrenal clocks and the role of adrenal hormones in the regulation of circadian physiology. Journal of Biological Rhythms, 30: 20–34.

  • Lerchl A., 1995: Sustained response of pineal melatonin synthesis to a single one-minute light pulse during night in Djungarian hamsters (Phodopus sungorus). Neuroscience Letters, 198: 65–67.

  • Lewis P. D., Perry G. C., Morris T. R. & English J., 2001: Supplementary dim light differentially influences sexual maturity, oviposition time, and melatonin rhythms in pullets. Poultry Science, 80: 1723–1728.

  • Li S. & Zhang L., 2015: Circadian control of global transcription. BioMed Research International, 2015(18780): 1–8.

  • Li Y., Li S., Zhou Y., Meng X., Zhang J. J., Xu D. P. & Li H. B., 2017: Melatonin for the prevention and treatment of cancer. Oncotarget, 8: 39896–39921.

  • Lincoln G. A., 1994: Effects of placing micro-implants of melatonin in the pars tuberalis, pars distalis and the lateral septum of the forebrain on the secretion of FSH and prolactin, and testicular size in rams. Journal of Neuroendocrinology, 142: 267–276.

  • Lockley S. W., Brainard G. C. & Czeisler C. A., 2003: High sensitivity of the human circadian melatonin rhythm to resetting by short wavelength light. Journal of Clinical Endocrinology and Metabolism, 88: 4502–4505.

  • Longcore T. & Rich C., 2004: Ecological Light Pollution. Frontiers in Ecology and the Environment, 2: 191–198.

  • Luarte T., Bonta C. C., Silv a-Rodriguez E. A., Quijón P. A., Miranda C., Farias A. A. & Duarte C., 2016: Light pollution reduces activity, food consumption and growth rates in a sandy beach invertebrate. Environmental Pollution, 218: 1147–1153.

  • Lucassen E. A., Coomans C. P., van Putten M., de Kreij S. R., van Genugten J. H. L. T., Sutorius R. P. M., de Rooij K. E., van der Velde M., Verhoeve S. L., Smit J. W. A., Löwik C. W. G. M., Smits H. H., Guigas B., Aartsma-Rus A. M. & Meijer J. H., 2016: Environmental 24-hr cycles are essential for health. Current Biology, 26: 1843–1853.

  • Lunn R. M., Blask D. E., Coogan A. N., Figueiro M. G., Gorman M. R., Hall J. E., Hansen J., Nelson R. J., Panda S., Smolensky M. H., Stevens R. G., Turek F. W., Vermeulen R., Carreón T., Caruso C. C., Lawson C. C., Thayer K. A., Twery M. J., Ewens A. D., Garner S. C., Schwingl P. J., Boyd W. A., 2017: Health consequences of electric lighting practices in the modern world: A report on the National Toxicology Program’s workshop on shift work at night, artificial light at night, and circadian disruption. Science of the Total Environment, 607–608: 1073–1084.

  • Maeda K., Mori Y., Sawasaki T. & Kano Y., 1984: Diurnal changes in peripheral melatonin concentration in goats and effects of light or dark interruption. Nihon Juigaku Zasshi, 46: 837–842.

  • Marseglia L., D’Angelo G., Manti S., Salpietro C., Arrigo T., Barberi I., Reiter R. J. & Gitto E., 2014: Melatonin and atopy: role in atopic dermatitis and asthma. International Journal of Molecular Sciences, 15: 13482–13493.

  • Martinez-Nicolas A., Madrid J. A. & Rol M. A., 2014: Day-night contrast as source of health for the human circadian system. Chronobiology International, 31: 382–393.

  • McFadden E., Jones M. E., Schoemaker M. J., Ashworth A. & Swerdlow A. J., 2014: The relationship between obesity and exposure to light at night: cross-sectional analyses of over 100,000 women in the Breakthrough Generations Study. Americal Journal of Epidemiology, 180: 245–250.

  • Min J. Y. & Min K. B., 2017: Outdoor light at night and the prevalence of depressive symptoms and suicidal behaviors: A cross-sectional study in a nationally representative sample of Korean adults. Journal of Affective Disorders, 227: 199–205.

  • Montevecchi W. A., 2006: Influences of artificial light on marine birds. Pp.: 94–113. In: Rich C. & Longcore T. (eds.): Ecological Consequences of Artificial Night Lighting. Island Press, Washington, D.C., 480 pp.

  • Münch M., Nowozin C., Regente J., Bes F., De Zeeuw J., Hädel S., Wahnschaffe A. & Kunz D., 2016: Blue-enriched morning light as a countermeasure to light at the wrong time: effects on cognition, sleepiness, sleep, and circadian phase. Neuropsychobiology, 74: 207–218.

  • Navara K. J. & Nelson R. J., 2007: The dark side of light at night: physiological, epidemiological, and ecological consequences. Journal of Pineal Research, 43: 215–224.

  • Navarro-Barranco C. & Hughes L. E., 2015: Effects of light pollution on the emergent fauna of shallow marine ecosystems: Amphipods as a case study. Marine Pollution Bulletin, 94: 235–240.

  • Nelson R. J. & Chbeir S., 2018: Dark matters: effects of light at night on metabolism. Proceedings of the Nutrition Society, 77: 223–229.

  • Nozaki M., Tsushima M. & Mori Y., 1990: Diurnal changes in serum melatonin concentrations under indoor and outdoor environments and light suppression of nighttime melatonin secretion in the female Japanese monkey. Journal of Pineal Research, 9: 221–230.

  • Obayashi K., Saeki K. & Kurumatani N., 2018: Bedroom light exposure at night and the incidence of depressive symptoms: A Longitudinal Study of the HEIJO-KYO Cohort. American Journal of Epidemiology, 187: 427–434.

  • Ohta H., Yamazaki S. & McMahon D. G., 2005: Constant light desynchronizes mammalian clock neurons. Nature Neuroscience, 8: 267–269.

  • Oishi K., Shibusawa K., Kakazu H., Kuriyama T., Ohkura N. & Machida K., 2006: Extended light exposure suppresses nocturnal increases in cytotoxic activity of splenic natural killer cells in rats. Biological Rhythm Research, 37: 21–35.

  • Oliveira C., Ortega A., López-Olmeda J. F., Vera L. M. & Sánchez-Vázquez F. J., 2007: Influence of constant light and darkness, light intensity, and light spectrum on plasma melatonin rhythms in senegal sole. Chronobiology International, 24: 615–627.

  • Ouyang J. Q., de Jong M., van Grunsven R. H. A., Matson K. D., Haussmann M. F., Meerlo P., Visser M. E. & Spoelstra K., 2017: Restless roosts: Light pollution affects behavior, sleep, and physiology in a free-living songbird. Global Change Biology, 23: 4987–4994.

  • Panda S., Sato T. K., Castrucci A. M., Rollag M. D., DeGrip W. J., Hogenesch J. B., Provencio I. & Kay S. A., 2002: Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science, 298: 2213–2216.

  • Perreau-Lenz S., Kalsbeek A., Garidou M. L., Wortel J., Van Der Vliet J., Van Heijningen C., Simonneaux V., Pévet P. & Buijs R. M., 2003: Suprachiasmatic control of melatonin synthesis in rats: inhibitory and stimulatory mechanisms. European Journal of Neuroscience, 17: 221–228.

  • Perreau-Lenz S., Kalsbeek A., Pévet P. & Buijs R. M., 2004: Glutamatergic clock output stimulates melatonin synthesis at night. European Journal of Neuroscience, 19: 318–324.

  • Perry G., Buchanan B. W., Fisher R. N., Salmon M. & Wise S. E., 2008: Effects of artificial night lighting on amphibians and reptiles in urban environments. Herpetological Conservation, 3: 239–256.

  • Pevet P., 2014: The internal time-giver role of melatonin: A key for our health. Revue Neurologique, 170: 646–652.

  • Poza J. J., Pujol M., Ortega-Albás J. J. & Romero O., 2018: Melatonin in sleep disorders. Neurologia (in press). Preslock J. P., 1976: Regulation of pineal enzymes by photoperiod, gonadal hormones and melatonin in Coturnix quail. Hormone Research, 7: 108–117.

  • Provencio I., Rodriguez I. R., Jiang G., Hayes W. P., Moreira E. F. & Rollag M. D.., 2000: A novel human opsin in the inner retina. Journal of Neuroscience, 20: 600–605.

  • Raap T., Pinxten R. & Eens M., 2015: Light pollution disrupts sleep in free-living animals. Scientific Reports, 5(13557): 1–8.

  • Raap T., Sun J., Pinxten R. & Eens M., 2017: Disruptive effects of light pollution on sleep in free-living birds: Season and/or light intensity-dependent? Behavioural Processes, 144: 13–19.

  • Reiter R. J., 2002: Potential biological consequences of excessive light exposure: melatonin suppression, DNA damage, cancer and neurodegenerative diseases. Neuro Endocrinology Letters, 2: 9–13.

  • Reiter R. J. & Peters J. F., 1984: Non-suppressibility by room light of pineal N-acetyltransferase activity and melatonin levels in two diurnally active rodents, the Mexican ground squirrel (Spermophilus mexicanus) and the eastern chipmunk (Tamias striatus). Endocrine Research, 10: 113–121.

  • Reiter R. J., Vriend J., Brainard G. C., Matthews S. A. & Craft C. M., 1982: Reduced pineal and plasma melatonin levels and gonadal atrophy in old hamsters kept under winter photoperiods. Experimental Aging Research, 8: 27–30.

  • Reiter R. J., Steinlechner S., Richardson B. A. & King T. S. 1983: Differential response of pineal melatonin levels to light at night in laboratory-raised and wild-captured 13-lined ground squirrels (Spermophilus tridecemlineatus). Life Sciences, 32: 2625–2629.

  • Reiter R. J., Bhaskar N. J., Heinzeller T. & Nujrnberger F., 1986: A single 1- or 5-second light pulse at night inhibits hamster pineal melatonin. Endocrinology, 118: 1906–1909.

  • Reiter R. J., Tan D. X. & Galano A., 2014: Melatonin: exceeding expectations. Physiology, 29: 325–333.

  • Reppert S. M., Perlow M. J., Tamarkin L., Orloff D. & Klein D. C., 1981: The effects of environmental lighting on the daily melatonin rhythm in primate cerebrospinal fluid. Brain Research, 223: 313–323.

  • Revel F. G., Saboureau M., Pevet P., Mikkelsen J. D. & Simonneaux V., 2006: Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology, 147: 4680–4687.

  • Robert K. A., Lesku J. A., Partecke J. & Chambers B., 2015: Artificial light at night desynchronizes strictly seasonal reproduction in a wild mammal. Proceedings of the Royal Society B, Biological Sciences, 282: 1–7.

  • Rodríguez A., Rodríguez B. & Negro J. J., 2015: GPS tracking for mapping seabird mortality induced by light pollution. Scientific Reports, 5(10670): 1–11.

  • Romeo S., Viaggi C., Di Camillo D., Willis A. W., Lozzi L., Rocchi C., Capannolo M., Aloisi G., Vaglini F., Maccarone R., Caleo M., Missale C., Racette B. A., Corsini G. U. & Maggio R., 2013: Bright light exposure reduces TH-positive dopamine neurons: implications of light pollution in Parkinson’s disease epidemiology. Scientific Reports, 3(1395): 1–9.

  • Rowan W., 1938: London starlings and seasonal reproduction in birds. Proceedings of the Zoological Society of London, 1938: 51–78.

  • Russ A., Reitemeier S., Weissmann A., Gottschalk J., Einspanier A. & Klenke R., 2015: Seasonal and urban effects on the endocrinology of a wild passerine. Ecology and Evolution, 5(23): 5690–5710.

  • Rybnikova N. A., Haim A. & Portnov B. A., 2016: Does artificial light-at-night exposure contribute to the worldwide obesity pandemic? International Journal of Obesity, 40: 815–823.

  • Saboureau M., Vivien-Roels B. & Pevet P., 1991: Pineal melatonin concentrations during day and night in the adult hedgehog: effect of a light pulse at night and superior cervical ganglionectomy. Journal of Pineal Research, 11: 92–98.

  • Sakamoto K., Nagase T., Fukui H., Horikawa K., Okada T., Tanaka H., Sato K., Miyake Y., Ohara O., Kako K. & Ishida N., 1998: Multitissue circadian expression of rat period homolog (rPer2) mRNA is governed by the mammalian circadian clock, the suprachiasmatic nucleus in the brain. Journal of Biological Chemistry, 273: 27039–27042.

  • Sanders D. & Gaston K. J., 2018: How ecological communities respond to artificial light at night. Journal of Experimental Zoology, Part A, Ecological and Integrative Physiology, 329: 394–400.

  • Sarlak G., Jenwitheesuk A., Chetsawang B. & Govitrapong P., 2013: Effects of melatonin on nervous system aging: neurogenesis and neurodegeneration. Journal of Pharmacological Sciences, 123: 9–24.

  • Schibler U., Gotic I., Saini C., Gos P., Curie T., Emmenegger Y., Sinturel F., Gosselin P., Gerber A., Fleury-Olela F., Rando G., Demarque M. & Franken P., 2015: Clock-Talk: Interactions between central and peripheral circadian oscillators in mammals. Cold Spring Harbor Symposia on Quantitative Biology, 80: 223–232.

  • Schoech S. J., Bowman R., Hahn T. P., Goymann W., Schwabl I. & Bridge E. S., 2013: The effects of low levels of light at night upon the endocrine physiology of western scrub-jays (Aphelocoma californica). Journal of Experimental Zoology, Part A, Ecological and Integrative Physiology, 319: 527–538.

  • Smith K. A., Schoen M. W. & Czeisler C. A., 2004: Adaptation of human pineal melatonin suppression by recent photic history. Journal of Clinical Endocrinology and Metabolism, 89: 3610–3614 (Erratum in: Journal of Clinical Endocrinology and Metabolism, 90[2005]: 1370).

  • Spoelstra K., Ramakers J. J. C., van Dis N. E. & Visser M. E., 2018: No effect of artificial light of different colors on commuting Daubenton’s bats (Myotis daubentonii) in a choice experiment. Journal of Experimental Zoology, Part A, Ecological and Integrative Physiology, 329: 506–510.

  • Su S. C., Hsieh M. J., Yang W. E., Chung W. H., Reiter R. J. & Yang S. F., 2017: Cancer metastasis: Mechanisms of inhibition by melatonin. Journal of Pineal Research, 62: 1–11.

  • Sulli G., Manoogian E. N. C., Taub P. R. & Panda S., 2018: Training the circadian clock, clocking the drugs, and drugging the clock to prevent, manage, and treat chronic diseases. Trends in Pharmacological Sciences, 39: 812–827.

  • Surbhi T. & Kumar V., 2015: Avian photoreceptors and their role in the regulation of daily and seasonal physiology. General and Comparative Endocrinology, 220: 13–22.

  • Takahashi J. S., 2016: Molecular architecture of the circadian clock in mammals. Pp.: 13–24. In: Sassone-Corsi P. & Christen Y. (eds.): A Time for Metabolism and Hormones. Springer, Cham.

  • Tamarkin L., Westrom W. K., Hamill A. I. & Goldman B. D., 1976: Effect of melatonin on the reproductive systems of male and female Syrian hamsters: a diurnal rhythm in sensitivity to melatonin. Endocrinology, 99: 1534–1541.

  • Tan D. X., Manchester L. C., Esteban-Zubero E., Zhou Z. & Reiter R. J., 2015: Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules, 20: 18886–18906.

  • Thiele G., Holtorf A., Steinlechner S. & Reiter R. J., 1983: The influence of different light irradiances on pineal N-acetyltransferase activity and melatonin levels in the cotton rat, Sigmodon hispidus. Life Sciences, 33: 1543–1547.

  • Touitou Y., 2015: Light at night pollution of the internal clock, a public health issue. Bulletin de lAcadémie Nationale de Medicine, 199: 1081–1098.

  • Touitou Y., Reinberg A. & Touitou D., 2017: Association between light at night, melatonin secretion, sleep deprivation, and the internal clock: Health impacts and mechanisms of circadian disruption. Life Sciences, 173: 94–106.

  • Turek F. W., Desjardins C. & Menaker M., 1975: Melatonin: antigonadal and progonadal effects in male golden hamsters. Science, 190: 280–282.

  • Tuxbury S. M. & Salmon M., 2005: Competitive interactions between artificial lighting and natural cues during seafinding by hatchling marine turtles. Biological Conservation, 121: 311–316.

  • Uth K. & Sleigh R., 2014a: Deregulation of the circadian clock constitutes a significant factor in tumorigenesis: a clockwork cancer. Part I: clocks and clocking machinery. Biotechnology & Biotechnological Equipment, 28: 176–183.

  • Uth K. & Sleigh R., 2014b: Deregulation of the circadian clock constitutes a significant factor in tumorigenesis: a clockwork cancer. Part II. In vivo studies. Biotechnology & Biotechnological Equipment, 28: 379–386.

  • Vanĕček J. & Illnerová H., 1982: Effect of light at night on the pineal rhythm in N-acetyltransferase activity in the Syrian hamster Mesocricetus auratus. Experientia, 38: 513–514.

  • Vera L. M., Davie A., Taylor J. F. & Migaud H., 2010: Differential light intensity and spectral sensitivities of Atlantic salmon, European sea bass and Atlantic cod pineal glands ex vivo. General and Comparative Endocrinology, 165: 25–33.

  • Vivien-Roels B., Arendt J. & Bradtke J., 1979: Circadian and circannual fluctuations of pineal indoleamines (serotonin and melatonin) in Testudo hermanni Gmelin (Reptilia, Chelonia). I. Under natural conditions of photoperiod and temperature. General and Comparative Endocrinology, 37: 197–210.

  • Vollrath L. & Huesgen A., 1988: Response of pineal serotonin N-acetyltransferase activity in male guinea pigs exposed to light pulses at night. Journal of Neural Transmission, 72: 55–66.

  • Walsh C.M., Prendergast R.L., Sheridan J.T., Murphy B.A., 2013: Blue light from light-emitting diodes directed at a single eye elicits a dose-dependent suppression of melatonin in horses. Veterinary Journal, 196: 231–235.

  • Watanabe M., Yasuo S., Watanabe T., Yamamura T., Nakao N., Ebihara S. & Yoshimura T., 2004: Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology, 145: 1546–1549.

  • Watanabe T., Yamamura T., Watanabe M., Yasuo S., Nakao N., Dawson A., Ebihara S. & Yoshimura T., 2007: Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals. American Journal of Physiology, Regulatory Integrative and Comparative Physiology, 292: R568–R572.

  • Wood S. & Loudon A., 2014: Clocks for all seasons: unwinding the roles and mechanisms of circadian and interval timers in the hypothalamus and pituitary. Journal of Endocrinology, 222: R39–R59.

  • Wood S. & Loudon A., 2018: The pars tuberalis: The site of the circannual clock in mammals? General and Comparative Endocrinology, 258: 222–235.

  • Wright H. R., Lack L. C. & Kennaway D. J., 2004: Differential effects of light wavelength in phase advancing the melatonin rhythm. Journal of Pineal Research, 36: 140–144.

  • Yamazaki S., Numano R., Abe M., Hida A., Takahashi R., Ueda M., Block G. D., Sakaki Y., Menaker M. & Tei H., 2000: Resetting central and peripheral circadian oscillators in transgenic rats. Science, 288: 682–685.

  • Yasuo S., Yoshimura T., Ebihara S. & Korf H. W., 2007: Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology, 148: 4385–4392.

  • Yoshimura T., Yasuo S., Watanabe M., Iigo M., Yamamura T., Hirunagi K. & Ebihara S., 2003: Lightinduced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature, 426: 178–181.

  • Zhang R., Lahens N. F., Ballance H. I., Hughes M. E. & Hogenesch J. B., 2014: A circadian gene expression atlas in mammals: implications for biology and medicine. Proceedings of the National Academy of Sciences of the United States of America, 111: 16219–16224.

  • Ziv L., Tovin A., Strasser D. & Gothilf Y., 2007: Spectral sensitivity of melatonin suppression in the zebrafish pineal gland. Experimental Eye Research, 84: 92–99.

  • Zubidat A. E. & Haim A., 2017: Artificial light-at-night – a novel lifestyle risk factor for metabolic disorder and cancer morbidity. Journal of Basic and Clinical Physiology and Pharmacology, 28: 295–313.

  • Zubidat A. E., Nelson R. J. & Haim A., 2011: Spectral and duration sensitivity to light-at-night in ‘blind’ and sighted rodent species. Journal of Experimental Biology, 214: 3206–3217.

OPEN ACCESS

Journal + Issues

Search