Abstract
Artificial light at night is constantly minimizing the span of dark nights from the natural light-dark cycle of earth. Over the past century, the “lightscape” of earth has completely changed owing to technological advancements which subsequently changed the lifestyle of human as well as the nearby animal species. This motivated the present study, wherein we investigated the impact of light at night (LAN) on behavior and physiology of a diurnal passerine finch, baya weaver (Ploceus philippinus). A group of bird (N=10) exposed to 12L:12D photoperiod was initially subjected to dark nights (0 lux) for a period of 1.5 weeks followed by 5 lux, night light for a span of 4 weeks. The first week in LAN served as acute treatment with respect to the fourth week (chronic). The results reveal significant increase in nighttime activity and sleep loss with respect to acute LAN, while significant inclusion of drowsiness behavior during the day in response to chronic LAN. Besides these behavioral alterations, changes in physiological parameters such as reduction in body mass, loss of gradient between pre- and post- prandial blood glucose levels, and elevation in plasma corticosterone levels were more prominent during acute exposure of LAN. Plasma metabolites such as triglycerides, total protein, serum glutamic-oxaloacetic transaminase (SGOT), and creatinine concentrations also hiked in response to acute LAN treatment. Thus, acute exposure of LAN seems to serve as a novel environment for the bird leading to more pronounced impacts on behavioral and physiological observations during the experiment. In chronic exposure, the birds sort of adapted themselves to the prevailing circumstances as evident by decreased nighttime activity, rebound of sleep and corticosterone levels, etc. Thus, the study clearly demonstrates the differential impact of acute and chronic exposure of LAN on behavior and physiology of birds.
Similar content being viewed by others
Data availability
The datasets used and/or analyzed in the present study can be obtained from the corresponding author on request.
References
Aulsebrook AE, Johnsson RD, Lesku JA (2021) Light, sleep and performance in diurnal birds. Clocks Sleep 3(1):115–131. https://doi.org/10.3390/clockssleep3010008
Azzi A, Dallmann R, Casserly A, Rehrauer H, Patrignani Maier AB, Kramer A, Brown SA (2014) Circadian behavior is light-reprogrammed by plastic DNA methylation. Nat Neurosci 17:377–382. https://doi.org/10.1038/nn.3651
Batra T, Malik I, Prabhat A, Bhardwaj SK, Kumar V (2020) Sleep in unnatural times: illuminated night negatively affects sleep and associated hypothalamic gene expressions in diurnal zebra finches. Proc R Soc B 287:20192952. https://doi.org/10.1098/rspb.2019.2952
Behera DP, Sethi APS, Singh C, Singh U, Wadhwa M (2019) Effect of citrus waste on blood parameters of broiler birds with and without cocktail of enzymes. Vet World 12(4):483–488. https://doi.org/10.14202/vetworld.2019.483-488
Bennie J, Davies TW, Cruse D, Inger R, Gaston KJ (2015) Cascading effects of artificial light at night: resource-mediated control of herbivores in a grassland ecosystem. Phil Trans Roy Soc B 370:20140131. https://doi.org/10.1098/rstb.20140.0131
Bennie J, Davies TW, Cruse D, Gaston KJ (2016) Ecological effects of artificial light at night on wild plants. J Ecol 104:611–620. https://doi.org/10.1111/1365-2745.12551
Boonstra R (2004) Coping with changing northern environments: the role of the stress axis in birds and mammals. Integr Comp Biol 44(2):95–108. https://doi.org/10.1093/icb/44.2.95
Cao J, Bian J, Wang Z, Dong Y, Chen Y (2017) Effect of monochromatic light on circadian rhythmic expression of clock genes and arylalkylamine N-acetyltransferase in chick retina. Chronobiol Int 34:1149–1157. https://doi.org/10.1080/07420528.2017.1354013
Cassone VM (2014) Avian circadian organization: a chorus of clocks. Front Neuroendocrinol 35:76–88. https://doi.org/10.1016/j.yfrne.2013.10.002
Crino OL, Prather CT, Driscoll SC, Good JM, Breuner CW (2014) Developmental stress increases reproductive success in male zebra finches. Proc R Soc B 281:20141266. https://doi.org/10.1098/rspb.2014.1266
Cuesta M, Clesse D, Pevet P, Challet E (2009) From daily behavior to hormonal and neurotransmitters rhythms: comparison between diurnal and nocturnal rat species. Horm Behav 55(2):338–347. https://doi.org/10.1016/j.yhbeh.2008.100.015
De Jong M, Jeninga L, Ouyang JQ, Oers VK, Spoelstra K, Visser ME (2016) Dose-dependent responses of avian daily rhythms to artificial light at night. Physiol Behav 155:172–179. https://doi.org/10.1016/j.physbeh.2015.120.012
De Jong M, Caro SP, Gienapp P, Spoelstra K, Visser ME (2017) Early birds by light at night: effects of light color and intensity on daily activity patterns in blue tits. J Biol Rhythm 32:323–333. https://doi.org/10.1177/0748730417719168
Dominoni DM, Quetting M, Partecke J (2013) Artificial light at night advances avian reproductive physiology. Proc R Soc B 280:20123017. https://doi.org/10.1098/rspb.2012.3017
Falcón J, Torriglia A, Attia D, Viénot F, Gronfier C, Behar-Cohen F, Martinsons C, Hicks D (2020) Exposure to artificial light at night and the consequences for flora, fauna, & ecosystems. Front Neurosci 14:602796. https://doi.org/10.3389/fnins.2020.602796
Ferretti A, Rattenborg NC, Ruf T, McWilliams SR, Cardinale M, Fusani L (2019) Sleeping unsafely tucked in to conserve energy in a nocturnal migratory songbird. Curr Biol 29:2766–2772. https://doi.org/10.1016/j.cub.20190.070.028
Foster RG, Kreitzman L (2005) Rhythms of life: the biological clocks that control the daily lives of every living thing. Yale University Press, New Haven, Connecticut ISBN: 0 300 10574 6. 2004
Fuchs T, Haney A, Jechura TJ, Moore FR, Bingman VP (2006) Daytime naps in night migrating birds: behavioural adaptation to seasonal sleep deprivation in the Swainson’s thrush, Catharus ustulatus. Anim Behav 72:951–958. https://doi.org/10.1016/j.anbehav.20060.030.008
Halford S, Pires SS, Turton M, Zheng L, Gonzalez-Menendez I, Davies WL, Peirson SN, Garcia-Fernandez JM, Hankins MW, Foster RG (2009) VA opsin-based photoreceptors in the hypothalamus of birds. Curr Biol 19:1396–1402. https://doi.org/10.1016/j.cub.2009.06.066
Jain N, Kumar V (1995) Changes in food intake, body weight, gonads and plasma concentration of thyroxine, luteinizing hormone and testosterone in captive male buntings exposed to natural daylengths at 29° N. J Biosci 20:417–426. https://doi.org/10.1007/BF02703845
Khandia R, Pathe CS, Vishwakarma P, Dhama K, Munjal A (2020) Evaluation of the ameliorative effects of Phyllanthus niruri on the deleterious insecticide imidacloprid in the vital organs of chicken embryos. J Ayurveda Integr Med 11(4):495–501. https://doi.org/10.1016/j.jaim.20190.030.003
Kumar V (1997) Photoperiodism in higher vertebrates: an adaptive strategy in temporal environment. Indian J Exp Biol 35(5):427–437
Kumar V, Singh S, Misra M, Malik S (2001) Effects of duration and time of food availability on photoperiodic responses in the migratory male blackheaded bunting (Emberiza melanocephala). J Exp Biol 204:2843–2848
Kumar J, Malik S, Bhardwaj SK, Rani S (2018) Bright light at night alters the perception of daylength in Indian weaver bird (Ploceus philippinus). J Exp Zool Part A: Ecol Integ Physiol 329:488–496. https://doi.org/10.1002/jez.2201
Kyba CCM, Kuester T, Sanchez de Miguel A, Baugh K, Jechow A, Holker F, Bennie J, Elvidge CD, Gaston KJ, Guanter L (2017) Artificially lit surface of Earth at night increasing in radiance and extent. Sci Adv 3:e1701528. https://doi.org/10.1126/sciadv.1701528
Lieske CL, Ziccardi MH, Mazet JAK, Newman SH, Gardner IA (2002) Evaluation of 4 hand held blood glucose monitors for use in seabird rehabilitation. J Avian Med Surg 16(4):277–285
Lobban K, Downs CT, Brown M (2010) Diel variations in plasma glucose concentration in some South African avian frugivores. Emu-Austral Ornithol 110(1):66–70. https://doi.org/10.1071/MU09088
Longcore T (2010) Sensory ecology: night lights alter reproductive behavior of blue tits. Curr Biol 20:R893–R895. https://doi.org/10.1016/j.cub.20100.090.011
Meyer U, Kampen MV, Isovich E, Flugge G, Fuchs E (2001) Chronic psychosocial stress regulated the expression of both GR and MR mRNA in the hippocampal formation of tree shrews. Hippocampus 11:329–336
Miller MW (2006) Apparent effects of light pollution on singing behavior of American robins. Condor. 108:130–139. https://doi.org/10.1650/0010.5422(2006)108[0130:AEOLPO]2.0.CO;2
Miller WL, Tyrrell JB (1995) The adrenal cortex. In: Felig P, Baxter JD, Frohman LA (eds) Endocrinol meta. McGraw-Hill Inc., New York, pp 555–711
Mishra I, Singh D, Kumar V (2017) Daily levels and rhythm in circulating corticosterone and insulin are altered with photostimulated seasonal states in night-migratory blackheaded buntings. Horm Behav 94:114–123. https://doi.org/10.1016/j.yhbeh.20170.070.004
Ouyang JQ, De Jong M, Hau M, Visser ME, Van Grunsven RHA, Spoelstra K (2015) Stressful colors: corticosterone concentrations in a free-living songbird vary with the spectral composition of experimental illumination. Biol Lett 11:20150517. https://doi.org/10.1098/rsbl.20150.0517
Ouyang JQ, de Jong M, Van Grunsven RHA, Matson KD, Haussmann MF, Meerlo P, Visser ME, Spoelstra K (2017) Restless roosts: light pollution affects behavior, sleep, & physiology in a free-living songbird. Glob Chang Biol 23:4987–4994. https://doi.org/10.1111/gcb.13756
Raap T (2018) Effects of artificial light at night on the behaviour and physiology of free-living songbirds. In: Faculteit Wetenschappen Departement Biologie. Universiteit Antwerpen, Antwerpen, p 275
Raap T, Pinxten R, Eens M (2015) Light pollution disrupts sleep in free-living animals. Sci Rep 5:13557. https://doi.org/10.1038/srep13557
Raap T, Casasole G, Costantini D, Abd Elgawad H, Asard H, Pinxten R et al (2016a) Artificial light at night affects body mass but not oxidative status in free-living nestling songbirds: an experimental study. Sci Rep 6:35626. https://doi.org/10.1038/srep35626
Raap T, Pinxten R, Eens M (2016b) Artificial light at night disrupts sleep in female great tits (Parus major) during the nestling period, & is followed by a sleep rebound. Environ Pollut 215:125–134. https://doi.org/10.1016/j.envpol.20160.04.100
Rezende EL, Gomes FR, Chappell MA, Garland T Jr (2009) Running behavior and its energy cost in mice selectively bred for high voluntary locomotor activity. Physiol Biochem Zool 82(6):662–679. https://doi.org/10.1086/605917
Risser AC (1971) A technique for performing laparotomy on small birds. Condor 73:376–379
Roby J, Aubé M, Morin-Paulhus A, Beauchesne W, Cyr L-O, Laflèche C (2021) Lamp spectral power distribution database (n.d.). https://lspdd.org/app/en/lamps/2768
Rodriguez A, Dann P, Chiaradia A (2017) Reducing light-induced mortality of seabirds: high pressure sodium lights decrease the fatal attraction of shearwaters. J Nat Conserv 39:68–72. https://doi.org/10.1016/j.jnc.20170.070.001
Roenneberg T, Kumar CJ, Merrow M (2007) The human circadian clock entrains to sun time. Curr Biol 7:R44–R45. https://doi.org/10.1016/j.cub.2006.120.011
Ronconi RA, Allard KA, Taylor PD (2015) Bird interactions with offshore oil and gas platforms: review of impacts and monitoring techniques. J Env Manag 147:34–45. https://doi.org/10.1016/j.jenvman.20140.070.031
Russart KL, Nelson RJ (2018) Light at night as an environmental endocrine disruptor. Physiol Behav 190:82–89. https://doi.org/10.1016/j.physbeh.20170.080.029
Schoech SJ, Bowman R, Hahn TP, Goymann W, Schwabl I, Bridge ES (2013) The effects of low levels of light at night upon the endocrine physiology of western scrub-jays (Aphelocoma californica). J Exp Zool A: Ecol Integr Physiol 319:527–538. https://doi.org/10.1002/jez.1816
Shivaprasad HN, Gopalakrishna S, Mariyanna B, Thekkoot M, Reddy R, Tippeswamy BS (2014) Effect of Coleus forskohlii extract on cafeteria diet-induced obesity in rats. Pharm Res 6(1):42–45. https://doi.org/10.4103/0974-8490.122916
Singh J, Rani S, Kumar V (2012) Functional similarity in relation to the external environment between circadian behavioral and melatonin rhythms in the subtropical Indian weaver bird. Horm Behav 61(4):527–534. https://doi.org/10.1016/j.yhbeh.20120.010.015
Singh D, Trivedi N, Malik S, Rani S, Kumar V (2016) Timed food availability affects circadian behavior but not the neuropeptide Y expression in Indian weaverbirds exposed to atypical light environment. Physiol Behav 161:81–89. https://doi.org/10.1016/j.physbeh.20160.040.017
Soper DS (2013) F-value and p-value calculator for multiple regression [online software]. Available at: http://www.danielsoper.com/statcalc
Stracey CM, Wynn B, Robinson SK (2014) Light pollution allows the northern mockingbird (Mimus polyglottos) to feed nestlings after dark. Wilson J Ornithol. 126:366–369
Van Doren BM, Horton KG, Dokter AM, Klinck H, Elbin SB, Farnsworth A (2017) High-intensity urban light installation dramatically alters nocturnal bird migration. Proc Nat Acad Sci USA 114(42):11175–11180. https://doi.org/10.1073/pnas.1708574114
Webster JC, Cidlowski JA (1994) Downregulation of the glucocorticoid receptor: a mechanism for physiological adaptation to hormones. Ann N Y Acad Sci 746:216–220
Welbers AAMH, van Dis NE, Kolvoort AM, Ouyang J, Visser ME, Spoelstra K, Dominoni DM (2017) Artificial light at night reduces daily energy expenditure in breeding great tits (Parus major). Front Ecol Evol 5:1–10
West AC, Bechtold DA (2015) The cost of circadian desynchrony: evidence, insights and open questions. BioEssays 37(7):777–788. https://doi.org/10.1002/bies.201400173
Williams TD, Ternan SP (1999) Food intake, locomotor activity, & egg laying in zebra finches: contributions to reproductive energy demand? Physiol Biochem Zool 72(1):19–27. https://doi.org/10.1086/316639
Wright KP, McHill AW, Birks BR, Griffin BR, Rusterholz T, Chinoy ED (2013) Entrainment of the human circadian clock to the natural light-dark cycle. Curr Biol 23(16):1554–1558. https://doi.org/10.1016/j.cub.20130.060.039
Wyse CA, Selman C, Page MM, Coogan AN, Hazlerigg DG (2011) Circadian desynchrony and metabolic dysfunction; did light pollution make us fat? Med Hypotheses 77(6):1139–1144. https://doi.org/10.1016/j.mehy.20110.090.023
Yadav A, Kumar R, Tiwari J, Kumar V, Rani S (2017) Sleep in birds: lying on the continuum of activity and rest. Biol Rhythm Res 48(5):805–814. https://doi.org/10.1080/09291016.2017.1346850
Yadav A, Tiwari J, Vaish V, Malik S, Rani S (2021) Migration gives sleepless nights to the birds: a study on a Palaearctic–Indian migrant, Emberiza bruniceps. J Ornithol 162:77–87. https://doi.org/10.1007/s10336-020-01829-x
Funding
The financial support by DBT (Department of Biotechnology) Research Project (BT/PR4984/MED/30/752/2012) to SR and UGC-BSR (Fellowship ID 25-1/2014-2015(BSR)/7-109/2007(BSR) to AY, Department of Zoology, University of Lucknow, Lucknow, is highly acknowledged.
Author information
Authors and Affiliations
Contributions
Conceptualization and study design: AY, SR, and SM; study conducted by AY, RK, JT, VV; statistical analyses: AY; result interpretation: AY and SR; manuscript writing: AY and SR. All authors contributed critically to the draft and gave final approval for publication.
Corresponding author
Ethics declarations
Ethical approval
The experiments were performed as per approval of Institutional Animal Ethics Committee of University of Lucknow, Lucknow India. Protocol number: LU/ZOOL/IAEC/08/17/07 (ii).
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Figure 1
: Rhythmic profile of different sleep behaviors under LAN. Mean ±SEM values of different sleep behaviors of baya weaver bird during different times of day (ZT- 4, 8, 12, 16, 20, 24) and in different treatment phases of experiment. (PPTX 1808 kb)
ESM 2
(PPTX 18249 kb)
(MP4 28233 kb)
(MP4 16555 kb)
(MP4 15899 kb)
Rights and permissions
About this article
Cite this article
Yadav, A., Kumar, R., Tiwari, J. et al. Effect of artificial light at night on sleep and metabolism in weaver birds. Environ Sci Pollut Res 29, 80422–80435 (2022). https://doi.org/10.1007/s11356-022-20875-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-20875-x