Natural light vs artificial light. Effects of light pollution on the bioluminescence of dinoflagellate Pyrocystis lunula
DOI:
https://doi.org/10.15359/revmar.16-2.5Keywords:
bioluminescence, color, intensity, light pollution, light sourceAbstract
Although there are thousands of marine bioluminescent species, very little is known about the effects of artificial light at night (ALAN) on these organisms, particularly those living near the sea surface, such as dinoflagellates. These organisms have a circadian clock that influences their rhythmic physiology, including processes like photosynthesis and nitrogen metabolism, which help regulate marine carbon and nitrogen cycles, respectively. The purpose of this study is to partially address this knowledge gap and research the effects of light pollution on the bioluminescent dinoflagellate Pyrocystis lunula through a series of experiments aimed at verifying the consequences due to changes in the normal day-night circadian cycle and exposure to different types of light source, colors, and light intensities. The response variable was the Corrected Total Algal Bioluminescence, which was recorded with a digital camera and then calculated with the ImageJ software. Results show that dinoflagellates do not appear to be susceptible to slight changes in the light/dark cycle. However, a total absence of light and darkness leads to a drastic inhibition of their bioluminescence, particularly under white LED or incandescent artificial light and with a light intensity of 100 lux or higher.
References
Arroyo, H. L., Abascal, A., Degen, T., Aubé, M., Espey, B. R., Gyuk, G., ... & Kyba, C. C. M. (2024). Monitoring, trends and impacts of light pollution. Nat. Rev. Earth Environ., 5, 417-430. https://doi.org/10.1038/s43017-024-00555-9
Bhovichitra, M. & Swift, E. (1977). Light and dark uptake of nitrate and ammonium by large oceanic dinoflagellates: Pyrocystis lunula, Pyrocystis fusiformis, and Dissodinium lunula. Limnol. Oceanogr., 22(1), 73-83. https://doi.org/10.4319/lo.1977.22.1.0073
Bialevich, V., Zachleder, V. & Bišova, K. (2022). The Effect of Variable Light Source and Light Intensity on the Growth of Three Algal Species. Cells, 11(8), 1293. https://doi.org/10.3390/cells11081293
Claes, J. M., Haddock, S. H. D., Coubris, C. & Mallefet, J. (2024). Systematic Distribution of Bioluminescence in Marine Animals: A Species-Level Inventory. Life, 14(4), 432. https://doi.org/10.3390/life14040432
Cohen, N. R., McIlvin, M. R., Moran, D. M., Held, N. A., Saunders, J. K., Hawco, N. J., ... & Saito, M. A. (2021). Dinoflagellates alter their carbon and nutrient metabolic strategies across environmental gradients in the central Pacific Ocean. Nat. Microbiol., 6(2), 173-186. https://doi.org/10.1038/s41564-020-00814-7
Colepicolo, P., Roenneberg, T., Morse, D., Taylor, W. & Hastings, J. W. (1993). Circadian regulation of bioluminescence in the dinoflagellate Pyrocystis lunula. J. Phycol., 29(2), 173-179. https://doi.org/10.1111/j.0022-3646.1993.00173.x
Corfitsen, M. T. (1996). Enhanced tiredness among young impaired male nighttime drivers. Accid. Anal. Prev., 28(2), 155-162. https://doi.org/10.1016/0001-4575(95)00042-9
Costin, K. J. & Boulton, A. M. (2016). A field experiment on the effect of introduced light pollution on fireflies (Coleoptera: Lampyridae) in the Piedmont Region of Maryland. The Coleopt. Bull., 70(1), 84-86. https://doi.org/10.1649/072.070.0110
Craig, J. M., Klerks, P. L., Heimann, K. & Waits, J. L. (2003). Effects of salinity, pH and temperature on the re-establishment of bioluminescence and copper or SDS toxicity in the marine dinoflagellate Pyrocystis lunula using bioluminescence as an endpoint. Environ. Pollut., 125(2), 267-275. https://doi.org/10.1016/S0269-7491(03)00059-9
Davies, T. W., Duffy, J. P., Bennie, J. & Gaston, K. J. (2014). The nature, extent, and ecological implications of marine light pollution. Front. Ecol. Environ., 12(6), 347-355. https://doi.org/10.1890/130281
Davies, T. W. & Smith, T. (2018). Why artificial light at night should be a focus for global change research in the 21st century. Glob. Chang. Biol., 24(3), 872-882. https://doi.org/10.1111/gcb.13927
Depledge, M., Gordard-Codding, C. A. J. & Bowen, R. E. (2010). Light pollution in the sea. Mar. Pollut., 60(9), 1383-1385. https://doi.org/10.1016/j.marpolbul.2010.08.002
Di Bari, D. (2023). Effects of artificial light at night on the mobility of the sea urchin Paracentrotus lividus. Mar. Fish. Sci., 37(1), 41-52. https://doi.org/10.47193/mafis.3712024010106
Diamantopoulou, C., Christoforou, E., Dominoni, D. M., Kaiserli, E., Czyzewski, J., Mirzai, N. & Spatharis, S. (2021). Wavelength-dependent effects of artificial light at night on phytoplankton growth and community structure. Proc. R. Soc. B., 288, 20210525. https://doi.org/10.1098/rspb.2021.0525
Dunlap, J. C. & Hastings, J. W. (1981). The biological clock in Gonyaulax control luciferase activity by regulating turnover. J. Biol. Chem., 256(20), 10509-10518. https://doi.org/10.1016/S0021-9258(19)68651-5
Enright, J. T. (1977). Copepods in a hurry sustained high speed upward migration, Limnol. Oceanogr., 22(1), 118-125. https://doi.org/10.4319/LO.1977.22.1.0118
Esaias, W. E. & Curl, H. C. (1972). Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limn. Oceanogr., 17(6), 901–906. https://doi.org/10.4319/lo.1972.17.6.0901
Fajardo, C., De Donato, C., Rodulfo, H., Martínez-Rodríguez, G., Costas, B., Mancera, J. M. & Fernández-Acero, F. J. (2020). New Perspectives Related to the Bioluminescent System in Dinoflagellates: Pyrocystis lunula, a Case Study. Int. J. Mol. Sci., 21(5), 1784. https://doi.org/10.3390/ijms21051784
Falchi, F., Cinzano, P., Elvidge, C. D., Keith, D. M. & Haim, A. (2011). Limiting the impact of light pollution on human health, environment and stellar visibility. J. Environ. Manage., 92(10), 2714-2722. https://doi.org/10.1016/j.jenvman.2011.06.029
Falchi, F., Cinzano, P., Duriscoe, D., Kyba, C. C., Elvidge, C. D., Baugh, K., ... & Furgoni, R. (2016). The new world atlas of artificial night sky brightness. Sci. Adv., 2(6), e1600377. https://doi.org/10.1126/sciadv.1600377
Firebaugh, A. & Haynes, K. J. (2019). Light pollution may create demographic traps for nocturnal insects. Basic Appl. Ecol., 34, 118-125. https://doi.org/10.1016/j.baae.2018.07.005
Fobert, E. K., Burke da Silva, K. & Swearer, S. E. (2019). Artificial light at night causes reproductive failure in clownfish. Biol. Lett., 15(7), 20190272. https://doi.org/10.1098/rsbl.2019.0272
Garratt, M. J., Jenkins, S. R. & Davies, T. W. (2019). Mapping the consequences of artificial light at night for intertidal ecosystems. Sci. Total Environ., 691, 760-768. https://doi.org/10.1016/j.scitotenv.2019.07.156
Gaston, K. J., Davies, T. W., Bennie J. & Hopkins J. (2012). Reducing the ecological consequences of nighttime light pollution: Options and developments. J. Appl. Ecol. 49(6), 1256-1266. https://doi.org/10.1111/j.1365-2664.2012.02212.x
Gaston, K. J., Gaston, S., Bennie, J. & Hopkins, J. (2015). Benefits and costs of artificial nighttime lighting of the environment. Environ. Rev., 23(1), 14-23. https://doi.org/10.1139/er-2014-0041
Guillard, R. L. L. (1975). Culture of phytoplankton for feeding marine invertebrates. In W. L. Smith & M. H. Chanley (Eds.), Culture of Marine Invertebrate Animals (pp. 29-60). USA: Springer.
Haddock, S. H. D., Moline, M. A. & Case, J. F. (2010). Bioluminescence in the Sea. Annu. Rev. Mar. Sci., 2(1), 443-493. https://doi.org/10.1146/annurev-marine-120308-081028
Hanley, K. A. & Widder, E. A. (2017). Bioluminescence in Dinoflagellates: Evidence that the Adaptive Value of Bioluminescence in Dinoflagellates is Concentration Dependent. Photochem. Photobiol., 93(2), 519-530. https://doi.org/10.1111/php.12713
Hastings, J. W. (2007). The Gonyaulax Clock at 50: Translational Control of Circadian Expression. Cold Spring Harb. Symp. Quant. Biol., 72(1), 141-144. https://doi.org/10.1101/sqb.2007.72.026
Hastings, J. W. (2013). Circadian rhythms in dinoflagellates: What is the purpose of synthesis and destruction of proteins? Microorganisms, 1(1), 26-32. https://doi.org/10.3390/microorganisms1010026
Heisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., Dennison, W. C., ... & Suddleson, M. (2008). Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae, 8(1), 3-13. https://doi.org/10.1016/j.hal.2008.08.006
Hickman, A. E., Holligan, P. M., Moore, C. M., Sharples, J., Krivtsov, V. & Palmer, M. R. (2009). Distribution and chromatic adaptation of phytoplankton within a shelf sea thermocline. Limn. Oceanogr., 54(2), 525-536. https://doi.org/10.4319/lo.2009.54.2.0525
Hölker, F., Wolter, C., Perkin, E. K. & Tockner, K. (2010a). Light pollution as a biodiversity threat. Trends Ecol. Evol., 25(12), 681-682. https://doi.org/10.1016/j.tree.2010.09.007
Hölker F., Moss R., Griefahn B., Kloas W., Voigt C. C., Henckel D., ... & Tockner K. (2010b). The dark side of light: a transdisciplinary research agenda for light pollution policy. Ecol. Soc., 15(4), 13. http://doi.org/10.5751/ES-03685-150413
International Energy Agency. (2006). Light’s labour’s lost: policies for energy efficient lighting. France. OECD/IEA. https://doi.org/10.1787/19900694
Jadhav, D. B., Sriramkumar, Y. & Roy, S. (2022). The enigmatic clock of dinoflagellates, is it unique? Front. Microbiol., 13, 1004074. https://doi.org/10.3389%2Ffmicb.2022.1004074
Jeong, H. J., Lee, K. H., Yoo, Y. D., Kang, N. S., Song, J. Y., Kim, T. H., ... & Potvin, E. (2018). Effects of light intensity, temperature, and salinity on the growth and ingestion rates of the red-tide mixotrophic dinoflagellate Paragymnodinium shiwhaense. Harmful Algae, 80, 46-54. https://doi.org/10.1016/j.hal.2018.09.005
Johnson, C. H., Roeber, J. & Hastings, J. W. (1984). Circadian changes in enzyme concentration account from rhythm of enzyme activity in Gonyaulax. Science, 223(4643), 1428-1430. https://doi.org/10.1126/science.223.4643.1428
Kaniewska, P., Alon, S., Kariko-Lampert, S., Hoegh-Guldberg, O. & Levy, O. (2015). Signaling cascades and the importance of moonlight in coral broadcast mass spawning. eLife, 4, e09991. https://doi.org/10.7554/elife.09991
Kivelä, L., Elgert, C., Lehtonen, T. K. & Candolin, U. (2023). The color of artificial light affects mate attraction in the common glow-worm. Sci. Total Environ., 857(3), 159451. https://doi.org/10.1016/j.scitotenv.2022.159451
Knaust, R., Urbig, T., Li, L., Taylor, W. & Hastings, J. W. (1998). The circadian rhythm of bioluminescence in Pyrocystis is not due to differences in the amount of luciferase: A comparative study of three bioluminescent marine dinoflagellates. J. Phycol., 34(1), 167-172. https://doi.org/10.1046/j.1529-8817.1998.340167.x
Lambrechts, D., Roeffaers, M., Goossens, K., Hofkens, J., Vande Velte, G., Van de Putte, T., ... & Van Oosterwyck, H. (2014). A causal relation between bioluminescence and oxygen to quantify the cell niche. PLoS One, 19, 9(5), e97572. https://doi.org/10.1371/journal.pone.0097572
Latz, M. I., Juhl, A. R., Ahmed, A. M., Elghobashi, S. E. & Rohr, J. (2004). Hydrodynamic stimulation of dinoflagellate bioluminescence: A computational and experimental study. J. Exp. Biol., 207(11), 1941-1951. https://doi.org/10.1242/jeb.00973
Latz, M. I. & Rohr, J. (2005). Glowing with the flow. Opt. Photonics News, 16(10), 40-45. http://doi.org/10.1364/OPN.16.10.000040
Lindström, J., Grebner, W., Rigby, K. & Selander, E. (2017). Effects of predator lipids on dinoflagellate defense mechanisms – increased bioluminescence capacity. Sci. Rep., 7(1), 13104. https://doi.org/10.1038/s41598-017-13293-4
Love, A. C. & Prescher, J. A. (2020). Seeing (and Using) the Light: Recent Developments in Bioluminescence Technology. Cell Chem. Biol., 27(8), 904-920. https://doi.org/10.1016/j.chembiol.2020.07.022
Luarte, T., Bonta, C. C., Silva-Rodríguez, 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. Environ. Pollut., 218, 1147-1153. https://doi.org/10.1016/j.envpol.2016.08.068
Ludvigsen, M., Berge, J., Geoffroy, M., Cohen, J. H., De La Torre, P. R., Nornes, S. M., ... & Johnsen, G. (2018). Use of an Autonomous Surface Vehicle reveals small-scale diel vertical migrations of zooplankton and susceptibility to light pollution under low solar irradiance. Sci. Adv., 4(1), eaap9887. https://doi.org/10.1126/sciadv.aap9887
Luijendijk, A., Hagenaars, G., Raasinghe, R., Baart, F., Donchyts, G. & Aarninkhof, S. (2018). The State of the World’s Beaches. Sci. Rep., 8(1), 6641. https://doi.org/10.1038/s41598-018-24630-6
Mandal, G., Bauri, J. & Choudhary, R. B. (2024). Conjugated polymeric nanocomposite-based light-generating active materials for OLED applications: A review. Mater. Sci. Eng. B, 303, 117271. https://doi.org/10.1016/j.mseb.2024.117271
Manríquez, P. H., Jara, M. E., González, C. P., Seguel, M., Quijón, P. A., Widdicombe, S., ... & Duarte, C. (2021). Effects of artificial light at night and predation cues on foraging and predator avoidance in the keystone inshore mollusc Concholepas concholepas. Environ. Pollut., 280, 116895. https://doi.org/10.1016/j.envpol.2021.116895
Morin, J. G. (1983). Coastal bioluminescence: patterns and functions. Bull. Mar. Sci., 33(4), 787-817.
Nemade, L. P. (2023). Review on Thermal Analysis of LED Heat Power Dissipation and Efficiency Analysis. Int. J. Res. Appl. Sci. Eng. Technol., 11(11), 1284-1287. https://doi.org/10.22214/ijraset.2023.56685
Neun, S., Hintz, N. H., Schröder, M. & Striebel, M. (2022). Phytoplankton Response to Different Light Colors and Fluctuation Frequencies. Front. Mar. Sci., 9, 824624. https://doi.org/10.3389/fmars.2022.824624
Owens, A. C. S. & Lewis, S. M. (2021). Effects of artificial light on growth, development, and dispersal of two North American fireflies (Coleoptera: Lampyridae). J. Insect Physiol., 130, 104200. https://doi.org/10.1016/j.jinsphys.2021.104200
Owens, A. C. S., Van der Broeck, M., De Cock, R. & Lewis, S. M. (2022). Behavioral responses of bioluminescent fireflies to artificial light at night. Front. Ecol. Evol., 10, 946640. https://doi.org/10.3389/fevo.2022.946640
Park, S. A., Jeong, H. J., Ok, J. H., Kang, H. C., You, J. H., Eom, S. H., ... & Lee, M. J. (2024). Effect of salinity on the bioluminescence intensity of the heterotrophic dinoflagellates Noctiluca scintillans and Polykrikos kofoidii and the autotrophic dinoflagellate Alexandrium mediterraneum. Mar. Biol., 171, 126. https://doi.org/10.1007/s00227-024-04440-3
Price, J. T., Drye, B., Domangue, R. J. & Paladino, F. V. (2018). Exploring the role of artificial lighting in loggerhead turtle (Caretta caretta) nest-site selection and hatchling disorientation. Herpetol. Conserv. Biol., 13(2), 415-422.
Rabha, M. M., Sharma, U. & Barua, A. G. (2021). Light from a firefly at temperatures considerably higher and lower than normal. Sci. Rep., 11, 12498. https://doi.org/10.1038/s41598-021-91839-3
Ritchie, R. J. & Sma-Air, S. (2023). Microalgae grown under different light sources. J. Appl. Phycol., 35(2), 1-16. https://doi.org/10.1007/s10811-023-02917-0
Rodríguez, 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.2017.07.001
Roenneberg, T. & Morse, D. (1993). Two circadian oscillators in one cell. Nature, 362(6418), 362-364. https://doi.org/10.1038/362362a0
Sathish, K., Saraswat, S. & Anusha, B. S. (2023). Light pollution and the impacts on biodiversity: the dark side of light. Biodiversity, 24(4), 194-199. https://doi.org/10.1080/14888386.2023.2244920
Satthong, S., Saego, K., Kitrungloadjanaporn, P., Nuttavut, N., Amornsamankul, S. & Triampo, W. (2019). Modeling the effects of light sources on the growth of algae. Adv. Differ. Equ., 170(1). 1-6. https://doi.org/10.1186/s13662-019-2112-6
Sherr, E. B. & Sherr B. F. (2007). Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar. Ecol. Prog. Ser., 352, 187-197. https://doi.org/10.3354/meps07161
Stomp, M., van Dijk, M. A., van Overzee, H. M. J., Wortel, M. T., Sigon, C. A. M., Egas, M., … & Huisman, J. (2008). The timescale of phenotypic plasticity and its impact on competition in fluctuating environments. Am. Nat., 172(8), 169-185. https://doi.org/10.1086/591680
Swift, E. & Meunier, V. (1976). Effects of light intensity on division rate, stimulable bioluminescence and cell size of the oceanic dinoflagellates Dissodinium lunula, Pyrocystis fusiformis and P. noctiluca. J. Phycol., 12(1), 14-22. https://doi.org/10.1111/j.1529-8817.1976.tb02819.x
Talanda, J., Maszczyk, P., Babkiewicz, E., Rutkowska, K. & Ślusarczyk, M. (2022). The short-term effects of planktivorous fish foraging in the presence of artificial light at night on lake zooplankton. J. Plankton Res., 44(6), 942-946. https://doi.org/10.1093/plankt/fbac046
Valiadi, M. & Iglesias-Rodríguez, D. (2013). Understanding Bioluminescence in Dinoflagellates – How Far Have We Come? Microorganisms, 1(1), 3-25. https://doi.org/10.3390/microorganisms1010003
Vitaterna, M. H., Takahashi, J. S. & Turek, F. W. (2001). Overview of Circadian Rhythms. Alcohol Res. Health, 25(2), 85-93.
Wang, L. (2018). Microbial control of the carbon cycle in the ocean. Natl. Sci. Rev., 5(2), 287-291. https://doi.org/10.1093/nsr/nwy023
Watanabe, Y. & Tanaka, Y. (2011). Bioluminescence-based imaging technique for pressure measurement in water. Exp. Fluids, 51, 225-236. https://doi.org/10.1007/s00348-011-1043-0
Zou, S. J., Shen, Y., Xie, F. M., Chen, J., Li, Y. & Tang, J. (2020). Recent Advances in Organic Light-Emitting Diodes: Toward Smart Lighting and Displays. Mater. Chem. Front., 4(3), 788-820. https://doi.org/10.1039/C9QM00716D
Downloads
Published
How to Cite
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
General terms and conditions
Revista Ciencias Marinas y Costeras by Universidad Nacional is located under a Licencia Creative Commons Atribución-NoComercial-SinDerivadas 3.0 Costa Rica.
The journal is hosted in open-access repositories such as the Repositorio Institucional de la Universidad Nacional, the Repositorio Kimuk de Costa Rica and la Referencia.
The editorial source of the journal must be acknowledged. For this purpose, use the doi identifier of the publication.
Self-archiving policy: The journal allows the self-archiving of articles in their refereed version, edited and approved by the Editorial Board of the Journal so that they are available in Open Access through the Internet. More information at the following link: https://v2.sherpa.ac.uk/id/publication/28915
