Light pollution disrupts sleep in free-living animals

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Raap, Thomas ^a   Pinxten, Rianne ^a   Eens, Marcel ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADVERSE EFFECTS; ANIMAL; ANIMAL BEHAVIOR; BIRD; ILLUMINATION; LIGHT; PATHOPHYSIOLOGY; RADIATION DOSE; RADIATION EXPOSURE; RADIATION RESPONSE; SLEEP; SLEEP WAKE DISORDERS;

ANIMALS; BEHAVIOR, ANIMAL; BIRDS; DOSE-RESPONSE RELATIONSHIP, RADIATION; LIGHT; LIGHTING; RADIATION DOSAGE; RADIATION EXPOSURE; SLEEP; SLEEP WAKE DISORDERS;

EID: 84941006737     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13557     Document Type: Article

References (61)

1. Holker, F., Wolter, C., Perkin, E. K. & Tockner, K. Light pollution as a biodiversity threat. Trends Ecol. Evol. 25, 681-682, doi: 10.1016/j.tree.2010.09.007 (2010).
2. Rich, C. & Longcore, T. Ecological consequences of artificial night lighting. (Island Press, 2005).
3. Dawson, A., King, V. M., Bentley, G. E. & Ball, G. F. Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16, 365-380, doi: 10.1177/074873001129002079 (2001).
4. Bradshaw, W. E. & Holzapfel, C. M. Evolution of animal photoperiodism. Annu. Rev. Ecol. Evol. Syst. 38, 1-25, doi: 10.1146/annurev.ecolsys.37.091305.110115 (2007).
5. Helm, B. et al. Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proc Biol Sci 280, 20130016, doi: 10.1098/rspb.2013.0016 (2013).
6. Cho, J. R., Joo, E. Y., Koo, D. L. & Hong, S. B. Let there be no light: the effect of bedside light on sleep quality and background electroencephalographic rhythms. Sleep Med 14, 1422-1425, doi: 10.1016/j.sleep.2013.09.007 (2013).
7. Navara, K. J. & Nelson, R. J. The dark side of light at night: physiological, epidemiological, and ecological consequences. J. Pineal Res. 43, 215-224, doi: 10.1111/j.1600-079X.2007.00473.x (2007).
8. Bedrosian, T. A., Fonken, L. K., Walton, J. C. & Nelson, R. J. Chronic exposure to dim light at night suppresses immune responses in Siberian hamsters. Biol. Lett. 7, 468-471, doi: 10.1098/rsbl.2010.1108 (2011).
9. Bedrosian, T. A., Galan, A., Vaughn, C. A., Weil, Z. M. & Nelson, R. J. Light at night alters daily patterns of cortisol and clock proteins in female Siberian hamsters. J. Neuroendocrinol. 25, 590-596, doi: 10.1111/jne.12036 (2013).
10. Brainard, G. C., Richardson, B. A., King, T. S. & Reiter, R. J. The influence of different light spectra on the suppression of pineal melatonin content in the Syrian hamster. Brain Res. 294, 333-339, doi: 10.1016/0006-8993(84)91045-X (1984).
11. Shuboni, D. & Yan, L. Nighttime dim light exposure alters the responses of the circadian system. Neuroscience 170, 1172-1178, doi: 10.1016/j.neuroscience.2010.08.009 (2010).
12. Dominoni, D. M., Quetting, M. & Partecke, J. Long-term effects of chronic light pollution on seasonal functions of European blackbirds (Turdus merula). PLoS ONE 8, e85069, doi: 10.1371/journal.pone.0085069 (2013).
13. Rodríguez, A., Rodríguez, B. & Negro, J. J. GPS tracking for mapping seabird mortality induced by light pollution. Sci. Rep. 5, doi: 10.1038/srep10670, http://www.nature.com/srep/2015/150602/srep10670/abs/srep10670.html#supplementary-information (2015).
14. Santhi, N. et al. The spectral composition of evening light and individual differences in the suppression of melatonin and delay of sleep in humans. J. Pineal Res. 53, 47-59, doi: 10.1111/j.1600-079X.2011.00970.x (2012).
15. Dominoni, D. M., Goymann, W., Helm, B. & Partecke, J. Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds. Front Zool 10, 60, doi: 10.1186/1742-9994-10-60 (2013).
16. Dominoni, D., Quetting, M. & Partecke, J. Artificial light at night advances avian reproductive physiology. Proc Biol Sci 280, 20123017, doi: 10.1098/rspb.2012.3017 (2013).
17. Dolgin, E. Deprivation: a wake-up call. Nature 497, S6-7, doi: 10.1038/497S6a (2013).
18. Knutson, K. L., Spiegel, K., Penev, P. & Van Cauter, E. The metabolic consequences of sleep deprivation. Sleep Med Rev 11, 163-178, doi: 10.1016/j.smrv.2007.01.002 (2007).
19. Titulaer, M., Spoelstra, K., Lange, C. Y. & Visser, M. E. Activity patterns during food provisioning are affected by artificial light in free living great tits (Parus major). PLoS ONE 7, e37377, doi: 10.1371/journal.pone.0037377 (2012).
20. Schlicht, L., Valcu, M., Loes, P., Girg, A. & Kempenaers, B. No relationship between female emergence time from the roosting place and extrapair paternity. Behav. Ecol. 25, 650-659, doi: 10.1093/beheco/aru035 (2014).
21. de Jong, M. et al. Effects of nocturnal illumination on life-history decisions and fitness in two wild songbird species. Phil. Trans. R. Soc. B. 370, doi: 10.1098/rstb.2014.0128 (2015).
22. Molenaar de J. G., J. D. A. & Sanders, M. E. Wegverlichting en Natuur III. Lokale invloed van wegverlichting op een gruttopopulatie (Road lighting and nature III; Local influence of road lighting on a population of godwits). Vol. 064 (Alterra, 2000).
23. Poot, H. et al. Green Light for Nocturnally Migrating Birds. Ecol. Soc. 13 (2008).
24. Rodríguez, A. et al. Fatal Attraction of Short-Tailed Shearwaters to Artificial Lights. PLoS ONE 9, e110114, doi: 10.1371/journal. pone.0110114 (2014).
25. Da Silva, A., Samplonius, J. M., Schlicht, E., Valcu, M. & Kempenaers, B. Artificial night lighting rather than traffic noise affects the daily timing of dawn and dusk singing in common European songbirds. Behav. Ecol. 25, 1037-1047, doi: 10.1093/beheco/aru103 (2014).
26. Kempenaers, B., Borgstrom, P., Loes, P., Schlicht, E. & Valcu, M. Artificial night lighting affects dawn song, extra-pair siring success, and lay date in songbirds. Curr. Biol. 20, 1735-1739, doi: 10.1016/j.cub.2010.08.028 (2010).
27. Dominoni, D. M., Carmona-Wagner, E. O., Hofmann, M., Kranstauber, B. & Partecke, J. Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds. J. Anim. Ecol. 83, 681-962, doi: 10.1111/1365-2656.12150 (2013).
28. Dominoni, D. M., Helm, B., Lehmann, M., Dowse, H. B. & Partecke, J. Clocks for the city: circadian differences between forest and city songbirds. Proc Biol Sci 280, 20130593, doi: 10.1098/rspb.2013.0593 (2013).
29. Nordt, A. & Klenke, R. Sleepless in Town-Drivers of the Temporal Shift in Dawn Song in Urban European Blackbirds. PLoS ONE 8, e71476, doi: 10.1371/journal.pone.0071476 (2013).
30. Steinmeyer, C., Schielzeth, H., Mueller, J. C. & Kempenaers, B. Variation in sleep behaviour in free-living blue tits, Cyanistes caeruleus: effects of sex, age and environment. Anim. Behav. 80, 853-864, doi: 10.1016/j.anbehav.2010.08.005 (2010).
31. Russ, A., Rüger, A. & Klenke, R. Seize the night: European Blackbirds (Turdus merula) extend their foraging activity under artificial illumination. Journal of Ornithology 156, 123-131, doi: 10.1007/s10336-014-1105-1 (2015).
32. Rattenborg, N. C. et al. Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). PLoS Biol. 2, E212, doi: 10.1371/journal.pbio.0020212 (2004).
33. Cirelli, C. & Tononi, G. Is sleep essential? PLoS Biol. 6, e216, doi: 10.1371/journal.pbio.0060216 (2008).
34. Siegel, J. M. Do all animals sleep? Trends Neurosci. 31, 208-213, doi: 10.1016/j.tins.2008.02.001 (2008).
35. Siegel, J. M. Sleep viewed as a state of adaptive inactivity. Nat. Rev. Neurosci. 10, 747-753, doi: 10.1038/nrn2697 (2009).
36. Weljie, A. M. et al. Oxalic acid and diacylglycerol 36:3 are cross-species markers of sleep debt. Proc. Natl. Acad. Sci. USA 112, 2569-2574, doi: 10.1073/pnas.1417432112 (2015).
37. Lesku, J. A. & Rattenborg, N. C. Avian sleep. Curr. Biol. 24, R12-14, doi: 10.1016/j.cub.2013.10.005 (2014).
38. Roth, T. C., 2nd, Lesku, J. A., Amlaner, C. J. & Lima, S. L. A phylogenetic analysis of the correlates of sleep in birds. J. Sleep Res. 15, 395-402, doi: 10.1111/j.1365-2869.2006.00559.x (2006).
39. Roth, T. C., 2nd, Rattenborg, N. C. & Pravosudov, V. V. The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation. Phil. Trans. R. Soc. B. 365, 945-959, doi: 10.1098/rstb.2009.0209 (2010).
40. Gobes, S. M., Zandbergen, M. A. & Bolhuis, J. J. Memory in the making: localized brain activation related to song learning in young songbirds. Proc Biol Sci 277, 3343-3351, doi: 10.1098/rspb.2010.0870 (2010).
41. Vorster, A. P. & Born, J. Sleep and memory in mammals, birds and invertebrates. Neurosci. Biobehav. Rev. 50, 103-119, doi: http://dx.doi.org/10.1016/j.neubiorev.2014.09.020 (2015).
42. Steinmeyer, C., Mueller, J. C. & Kempenaers, B. Individual variation in sleep behaviour in blue tits Cyanistes caeruleus: assortative mating and associations with fitness-related traits. J. Avian Biol. 44, 159-168, doi: 10.1111/j.1600-048X.2012.05750.x (2013).
43. Lesku, J. A. et al. Adaptive Sleep Loss in Polygynous Pectoral Sandpipers. Science 337, 1654-1658, doi: 10.1126/science.1220939 (2012).
44. Greives, T. J. et al. Costs of sleeping in: circadian rhythms influence cuckoldry risk in a songbird. Funct. Ecol., doi: 10.1111/1365-2435.12440 (2015).
45. Snyder, J. M., Molk, D. M. & Treuting, P. M. Increased Mortality in a Colony of Zebra Finches Exposed to Continuous Light. J Am Assoc Lab Anim Sci. 52, 301-307 (2013).
46. Van Duyse, E., Pinxten, R., Snoeijs, T. & Eens, M. Simultaneous treatment with an aromatase inhibitor and an anti-androgen decreases the likelihood of dawn song in free-living male great tits, Parus major. Horm. Behav. 48, 243-251 (2005).
47. Hart, N. S. The visual ecology of avian photoreceptors. Prog Retin Eye Res 20, 675-703, doi: 10.1016/S1350-9462(01)00009-X (2001).
48. Gaston, K. J., Bennie, J., Davies, T. W. & Hopkins, J. The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol. Rev. Camb. Philos. Soc. 88, 912-927, doi: 10.1111/brv.12036 (2013).
49. Davies, T. W., Bennie, J., Inger, R., de Ibarra, N. H. & Gaston, K. J. Artificial light pollution: are shifting spectral signatures changing the balance of species interactions? Glob Chang Biol 19, 1417-1423, doi: 10.1111/gcb.12166 (2013).
50. Schubert, E. F. & Kim, J. K. Solid-state light sources getting smart. Science 308, 1274-1278, doi: 10.1126/science.1108712 (2005).
51. R: A language and environment for statistical computing (Vienna, Austria, 2013).
52. lme4: Linear mixed-effects models using Eigen and S4 v. R package version 1.0-4 (2013).
53. Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom J 50, 346-363, doi: 10.1002/bimj.200810425 (2008).
54. Byrkjedal. I., Lislevand. T. & Vogler. S. Do passerine birds utilise artificial light to prolong their diurnal activity during winter at northern latitudes? Ornis Nor. 35, 37-42 (2012).
55. Dominoni, D. M. & Partecke, J. Does light pollution alter daylength? A test using light loggers on free-ranging European blackbirds (Turdus merula). Phil. Trans. R. Soc. B 370, doi: 10.1098/rstb.2014.0118 (2015).
56. Gaston, K. J., Davies, T. W., Bennie, J. & Hopkins, J. Reducing the ecological consequences of night-time light pollution: options and developments. J. Appl. Ecol. 49, 1256-1266, doi: 10.1111/j.1365-2664.2012.02212.x (2012).
57. Christe, P., Richner, H. & Oppliger, A. Of great tits and fleas: Sleep baby sleep. Anim. Behav. 52, 1087-1092, doi: 10.1006/anbe.1996.0256 (1996).
58. Rattenborg, N. C., Martinez-Gonzalez, D., Roth, T. C. & Pravosudov, V. V. Hippocampal memory consolidation during sleep: a comparison of mammals and birds. Biological Reviews 86, 658-691, doi: 10.1111/j.1469-185X.2010.00165.x (2011).
59. Lesku, J. A., Vyssotski, A. L., Martinez-Gonzalez, D., Wilzeck, C. & Rattenborg, N. C. Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds? Proc. R. Soc. B 278, 2419-2428, doi: 10.1098/rspb.2010.2316 (2011).
60. Rattenborg, N. & Martinez-Gonzalez, D. Avian Versus Mammalian Sleep: the Fruits of Comparing Apples and Oranges. Current Sleep Medicine Reports 1, 55-63, doi: 10.1007/s40675-014-0001-9 (2015).
61. Lima, S. L., Rattenborg, N. C., Lesku, J. A. & Amlaner, C. J. Sleeping under the risk of predation. Anim. Behav. 70, 723-736, doi: 10.1016/j.anbehav.2005.01.008 (2005).