Abstract
With urbanization expanding into natural areas, it is increasingly important to understand how species subject to human-induced habitat alteration respond to novel opportunities and stressors. A pervasive consequence of urbanization is artificial light at night (ALAN), which previous studies have found introduces both costs and benefits for vertebrates. This understanding, however, primarily reflects findings from laboratory-controlled experiments or comparisons of wild populations in areas with long-standing differences in ALAN regimes. Here, we investigated the short-term costs and benefits for Anolis lizards during the period of initial exposure to ALAN using realistic light levels for urban areas (mean ± SD = 87.9 ± 36.7 lx at a distance of 3 m). As compared to controls, we hypothesized that adding ALAN would result in behavioral and physiological changes over the short term for brown anoles and their arthropod prey. In contrast to predictions, ALAN did not increase arthropod abundance or extend anole activity into the night. Structural habitat and sleep site use changed little in response to ALAN, which exposed about one-third of sleeping anoles in ALAN plots to light at night due to our manipulation. However, this direct light exposure resulted in lizards being more easily roused from sleep compared to lizards sleeping in the dark in control plots or in shadows in ALAN plots. The apparent inability of some anoles to adjust their sleep sites to avoid ALAN exposure may have contributed to their increased responsiveness at night and decreased locomotor endurance in the day. Our study suggests brown anoles can experience higher short-term costs than benefits during initial exposure to ALAN.
Similar content being viewed by others
Data Availability
Data are available from the authors upon request.
References
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bedrosian TA, Fonken LK, Walton JC, Nelson RJ (2011) Chronic exposure to dim light at night suppresses immune responses in Siberian hamsters. Biol Lett 7:468–471. https://doi.org/10.1098/rsbl.2010.1108
Belenky G, Wesensten NJ, Thorne DR, Thomas ML, Sing HC, Redmond DP, Russo MB, Balkin TJ (2003) Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: a sleep dose-response study. J Sleep Res 12:1–12. https://doi.org/10.1046/j.1365-2869.2003.00337.x
Borniger JC, Maurya SK, Periasamy M, Nelson RJ (2014) Acute dim light at night increases body mass, alters metabolism, and shifts core body temperature circadian rhythms. Chronobiol Int 31:917–925. https://doi.org/10.3109/07420528.2014.926911
Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83
Brown TW, Arrivillaga C (2017) Nocturnal activity facilitated by artificial lighting in the diurnal Norops sagrei (Squamata: Dactyloidae) on Isla de Flores, Guatemala. Mesoam Herpetol 4:637–639
Davies TW, Bennie J, Gaston KJ (2012) Street lighting changes the composition of invertebrate communities. Biol Lett 8:764–767. https://doi.org/10.1098/rsbl.2012.0216
de Jong M, Ouyang JQ, Da Silva A, Van Grunsven RHA, Kempenaers B, Visser ME, Spoelstra K (2015) Effects of nocturnal illumination on life-history decisions and fitness in two wild songbird species. Philos Trans R Soc B 370:20140128. https://doi.org/10.1098/rstb.2014.0128
de Jong M, Jeninga L, Ouyang JQ, Van Oers K, 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.2015.12.012
Dominoni DM (2015) The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective. J Ornithol 156:409–418. https://doi.org/10.1007/s10336-015-1196-3
Dominoni DM, Partecke J (2015) Does light pollution alter daylength? A test using light loggers on free-ranging European blackbirds (Turdus merula). Philos Trans R Soc B 370:20140118
Durrant J, Michaelides EB, Rupasinghe T, Tull D, Green MP, Jones TM (2015) Constant illumination reduces circulating melatonin and impairs immune function in the cricket Teleogryllus commodus. PeerJ 3:e1075. https://doi.org/10.7717/peerj.1075
Eisenbeis G (2006) Artificial night lighting and insects: attraction of insects to streetlamps in a rural setting in Germany. In: Rich C, Longcore T (eds) Ecological consequences of artificial night lighting. Island Press, Washington, pp 281–304
Falchi F, Cinzano P, Duriscoe D, Kyba C M, Elvidge CD, Baugh K, Portnov B, Rybnikova NA, Furgoni R (2016) Supplement to the New World atlas of artificial night sky brightness. V. 1.1. GFZ Data Services. https://doi.org/10.5880/GFZ.1.4.2016.001
Farnworth B, Innes J, Kelly C, Littler R, Waas JR (2018) Photons and foraging: artificial light at night generates avoidance behaviour in male, but not female, New Zealand weta. Environ Pollut 236:82–90
Fite KV, Lister BC (1981) Bifoveal vision in Anolis lizards. Brain Behav Evol 19:144–154. https://doi.org/10.1159/000121639
Fleishman LJ, Bowman M, Saunders D, Miller WE, Rury MJ, Loew ER (1997) The visual ecology of Puerto Rican anoline lizards: habitat light and spectral sensitivity. J Comp Physiol A 181:446–460
Fonken LK, Nelson RJ (2013) Dim light at night increases depressive-like responses in male C3H/HeNHsd mice. Behav Brain Res 243:74–78
Forman RTT (2014) Urban ecology: science of cities. Cambridge University Press, Cambridge
Garber SD (1978) Opportunistic feeding behavior of Anolis cristatellus (Iguanidae: Reptilia) in Puerto Rico. Trans Kans Acad Sci 81:79–80
Gaston KJ, Duffy JP, Gaston S, Bennie J, Davies TW (2014) Human alteration of natural light cycles: causes and ecological consequences. Oecologia 176:917–931. https://doi.org/10.1007/s00442-014-3088-2
Gaston KJ, Visser ME, Holker F (2015) The biological impacts of artificial light at night: the research challenge. Proc R Soc B 370:20140133
Hamilton WJ (1982) Baboon sleeping site preferences and relationships to primate grouping patterns. Am J Primatol 3:41–53
Justice MJ, Justice TC (2016) Attraction of insects to incandescent, compact fluorescent, halogen, and LED lamps in a light trap: implications of light pollution and urban ecologies. Entomol News 125:315–326
Kolbe JJ, Glor RE, Rodriguez-Schettino L, Chamizo-Lara A, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181
Kolbe JJ, VanMiddlesworth P, Battles AC, Stroud JT, Buffum B, Forman RTT, Losos JB (2016) Determinants of spread in an urban landscape by an introduced lizard. Landscape Ecology 31:1795–1813
Kolbe JJ, Ehrenberger JC, Moniz HA, Angilletta MJ (2014) Physiological variation among invasive populations of the Brown Anole (Anolis sagrei). Physiological and Biochemical Zoology 87:92–104
Knop E, Zoller L, Ryser R, Gerpe C, Hörler M, Fontaine C (2017) Artificial light at night as a new threat to pollination. Nature 548:206–209. https://doi.org/10.1038/nature23288
Kurvers RHJM, Drägestein J, Hölker F, Jechow A, Krause J, Bierbach D (2018) Artificial light at night affects emergence from a refuge and space use in guppies. Sci Rep 8:14131. https://doi.org/10.1038/s41598-018-32466-3
Kyba CCM, Kuester T, Sánchez De Miguel A et al (2017) Artificially lit surface of earth at night increasing in radiance and extent. Sci Adv 3:e1701528. https://doi.org/10.1126/sciadv.1701528
Lapiedra O, Chejanovski Z, Kolbe JJ (2017) Urbanization and biological invasion shape animal personalities. Global Change Biology 23:592–603
Lapiedra O (2018) Urban behavioral ecology: lessons from Anolis lizards. Integr Comp Biol 58:939–947
Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723–736
Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, Berkeley
Manfrin A, Singer G, Larsen S, Weiß N, van Grunsven RHA, Weiß NS, Wohlfahrt S, Monaghan MT, Hölker F (2017) Artificial light at night affects organism flux across ecosystem boundaries and drives community structure in the recipient ecosystem. Front Environ Sci 5:61. https://doi.org/10.3389/fenvs.2017.00061
Maurer AS, Thawley CJ, Fireman AL, Giery ST, Stroud JT (2019) Nocturnal activity of Antiguan lizards under artificial light. Herpetol Conserv Biol 14:105–110
Meshaka J, Walter E, Butterfield BP, Hauge JB (2004) The exotic amphibians and reptiles of Florida. Krieger Publishing Company, Malabar
Miller MW (2006) Apparent effects of light pollution on singing behavior of American robins. Condor 108:130–139
Moore AF, Menaker M (2011) The effect of light on melatonin secretion in the cultured pineal glands of Anolis lizards. Comp Biochem Physiol A 160:301–308
Moore AF, Menaker M (2012) Photic resetting of the circadian clock is correlated with photic habitat in Anolis lizards. J Comp Physiol A 198:375–387
Moore AF, Kawasaki M, Menaker M (2012) Photic induction of locomotor activity is correlated with photic habitat in Anolis lizards. J Comp Physiol A 198:193–201
Navara KJ, Nelson RJ (2007) The dark side of light at night: physiological, epidemiological, and ecological consequences. J Pineal Res 43:215–224. https://doi.org/10.1111/j.1600-079X.2007.00473.x
Oliver SJ, Costa RJS, Laing SJ, Bilzon JLJ, Walsh NP (2009) One night of sleep deprivation decreases treadmill endurance performance. Eur J Appl Physiol 107:155–161. https://doi.org/10.1007/s00421-009-1103-9
Ouyang JQ, de Jong M, Van Grunsven RHA et al (2017) Restless roosts: light pollution affects behavior, sleep, and physiology in a free-living songbird. Glob Chang Biol 23:4987–4994. https://doi.org/10.1111/gcb.13756
Ouyang JQ, Davies S, Dominoni D (2018) Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function. J Exp biol 221:jeb156893. https://doi.org/10.1242/jeb.156893
Owens ACS, Lewis SM (2018) The impact of artificial light at night on nocturnal insects: a review and synthesis. Ecol Evol 8:11337–11358. https://doi.org/10.1002/ece3.4557
Perry G, Fisher RN (2006) Night lights and reptiles: observed and potential effects. In: Ecological consequences of artificial night lighting. (eds Rich C, Longcore T). Island Press, Washington, pp 281–304
Perry G, Lazell J (2000) Liophis portoricensis anegadae. Night-light hunting. Herpetol Rev 31:247
Petren K, Bolger DT, Case TJ (1993) Mechanisms in the competitive success of an invading sexual gecko over an asexual native. Science 259:354–358
Petren K, Case TJ (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118–132
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2020) nlme: linear and nonlinear mixed effects models. R package version 3.1–148, https://CRAN.R-project.org/package=nlme
Prugh LR, Golden CD (2014) Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles. J Anim Ecol 83:504–514. https://doi.org/10.1111/1365-2656.12148
R Core Team (2015). R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. URL https://www.R-project.org
Rich C, Longcore T (eds) (2006) Ecological consequences of artificial night lighting. Washington, DC, Island Press
Rizwan AM, Dennis LYC, Liu C (2008) A review on the generation, determination and mitigation of urban Heat Island. J Environ Sci 20:120–128. https://doi.org/10.1016/S1001-0742(08)60019-4
Robert KA, Lesku JA, Partecke J, Chambers B (2015) Artificial light at night desynchronizes strictly seasonal reproduction in a wild mammal. Proc R Soc B 282:20151745
Ruibal R (1961) Thermal relations of five species of tropical lizards. Evolution 15:98–111
Russ A, Ruger A, Klenke R (2014) Seize the night: European blackbirds (Turdus merula) extend their foraging activity under artificial illumination. J Ornithol 156:123–131. https://doi.org/10.1007/s10336-014-1105-1
Russ A, Reitemeier S, Weissmann A, Gottschalk J, Einspanier A, Klenke R (2015) Seasonal and urban effects on the endocrinology of a wild passerine. Ecol Evol 5:5698–5710. https://doi.org/10.1002/ece3.1820
Russart KLG, Nelson RJ (2018) Artificial light at night alters behavior in laboratory and wild animals. J Exp Zool A 329:401–408. https://doi.org/10.1002/jez.2173
Rydell J (1992) Exploitation of insects around streetlamps by bats in Sweden. Funct Ecol 6:744–750. https://doi.org/10.2307/2389972
Sanders D, Kehoe R, Cruse D, van Veen FJ, Gaston KJ (2018) Low levels of artificial light at night strengthen top-down control in insect food web. Curr Biol 28:2474–2478. https://doi.org/10.1016/j.cub.2018.05.078
Schwartz A, Henderson RW (1991) Amphibians and reptiles of the West Indies: descriptions, distributions, and natural history. University Press of Florida, Gainesville
Silva E, Marco A, Da Graça J et al (2017) Light pollution affects nesting behavior of loggerhead turtles and predation risk of nests and hatchlings. J Photochem Photobiol B 173:240–249. https://doi.org/10.1016/j.jphotobiol.2017.06.006
Singhal S, Johnson MA, Ladner JT (2007) The behavioral ecology of sleep: natural sleeping site choice in three Anolis lizard species. Behaviour 144:1033–1052
Spiller DA, Piovia-Scott J, Wright AN, Yang LH, Takimoto G, Schoener TW, Iwata T (2010) Marine subsidies have multiple effects on coastal food webs. Ecology 91:1424–1434
Thawley CJ, Kolbe JJ (2020) Artificial light at night increases growth and reproductive output in Anolis lizards. Proc R Soc B 287:20191682
Yorzinski JL, Chisholm S, Byerley S, Coy JR, Aziz AB, Wolf JA, Gnerlich A (2015) Artificial light pollution increases nocturnal vigilance in peahens. PeerJ 3: e1174
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. https://doi.org/10.3389/fevo.2017.00055
Acknowledgments
This study was conducted at Montgomery Botanical Center and we thank Patrick Griffith for permission to collect lizards on plants at MBC. We thank Carl Lewis of Fairchild Tropical Botanic Garden, and Ken Feeley and James Stroud of Florida International University for logistical support. We are grateful for the assistance of Shelby Rinehart and Malcom Moniz with fieldwork. Eily Sullivan assisted with insect identification and data collection. Haley Moniz was a Coastal Fellow at URI while conducting this research. Oriol Lapiedra was supported by a Beatriu de Pinós postdoctoral fellowship 2014 BP-A 00116 from the AGAUR.
Funding
This work was supported by funds from the University of Rhode Island and a grant from the National Geographic Society.
Author information
Authors and Affiliations
Contributions
JJK and HAM conceived of this study and conducted the field work; all authors contributed to data analysis and interpretation; JJK wrote the first draft of the manuscript; all authors contributed to manuscript revisions and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
The University of Rhode Island Institutional Animal Care and Use Committee approved protocols for use of live animals in this study (AN11–09-005).
Consent for publication
The authors consent to the terms for publication as stated by the journal and its publisher.
Competing interests
The authors have no conflicts of interest to declare.
Supplementary Information
ESM 1
(DOCX 6803 kb)
Rights and permissions
About this article
Cite this article
Kolbe, J.J., Moniz, H.A., Lapiedra, O. et al. Bright lights, big city: an experimental assessment of short-term behavioral and performance effects of artificial light at night on Anolis lizards. Urban Ecosyst 24, 1035–1045 (2021). https://doi.org/10.1007/s11252-021-01098-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11252-021-01098-3