Skip to main content

Influence of light intensity and spectral composition of artificial light at night on melatonin rhythm and mRNA expression of gonadotropins in roach Rutilus rutilus

Abstract

In this study we investigated the influence of artificial light at night (ALAN) of different intensities (0, 1, 10, 100 lx) and different colours (blue, green, red) on the daily melatonin rhythm and mRNA expression of gonadotropins in roach Rutilus rutilus, a ubiquitous cyprinid, which occur in standing and moderately flowing freshwater habitats of central Europe. Melatonin concentrations were significantly lowered under nocturnal white light already at 1 lx. Low intensity blue, green and red ALAN lowered the melatonin levels significantly in comparison to a dark control. We conclude that ALAN can disturb melatonin rhythms in roach at very low intensities and at different wavelengths and thus light pollution in urban waters has the potential to impact biological rhythms in fish. However, mRNA expression of gonadotropins was not affected by ALAN during the period of the experiments. Thus, suspected implications of ALAN on reproduction of roach could not be substantiated.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Alvarado MV, Carrillo M, Felip A (2015) Melatonin-induced changes in kiss/gnrh gene expression patterns in the brain of male sea bass during spermatogenesis. Comp Biochem Phys A 185:69–79. doi:10.1016/j.cbpa.2015.03.010

    CAS  Article  Google Scholar 

  2. Amano M, Iigo M, Ikuta K, Kitamura S, Yamada H, Yamamori K (2000) Roles of melatonin in gonadal maturation of underyearling precocious male masu salmon. Gen Comp Endocrinol 120:190–197. doi:10.1006/gcen.2000.7547

    CAS  PubMed  Article  Google Scholar 

  3. Anisimov VN (2006) Light pollution, reproductive function and cancer risk. Neuro Endocrinol Lett 27:35–52

    CAS  PubMed  Google Scholar 

  4. Baker BJ, Richardson JML (2006) The effect of artificial light on male breeding-season behaviour in green frogs, Rana clamitans melanota. Can J Zool 84:1528–1532. doi:10.1139/z06-142

    Article  Google Scholar 

  5. Bayarri MJ, Madrid JA, Sánchez-Vázquez FJ (2002) Influence of light intensity, spectrum and orientation on sea bass plasma and ocular melatonin. J Pineal Res 32:34–40. doi:10.1034/j.1600-079x.2002.10806.x

    CAS  PubMed  Article  Google Scholar 

  6. Bayarri MJ, Rodríguez L, Zanuy S, Madrid JA, Sánchez-Vázquez FJ, Kagawa H, Okuzawa K, Carrillo M (2004) Effect of photoperiod manipulation on the daily rhythms of melatonin and reproductive hormones in caged European sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 136:72–81. doi:10.1016/j.ygcen.2003.12.004

    CAS  PubMed  Article  Google Scholar 

  7. Becker A, Whitfield AK, Cowley PD, Järnegren J, Næsje TF (2013) Potential effects of artificial light associated with anthropogenic infrastructure on the abundance and foraging behaviour of estuary-associated fishes. J Appl Ecol 50:43–50. doi:10.1111/1365-2664.12024

    Article  Google Scholar 

  8. Bird BL, Branch LC, Miller DL (2004) Effects of coastal lighting on foraging behavior of beach mice. Efectos del Alumbrado Costero sobre el Comportamiento de Forrajeo de Ratones de Playa. Conserv Biol 18:1435–1439. doi:10.1111/j.1523-1739.2004.00349.x

    Article  Google Scholar 

  9. Biswas AK, Seoka M, Inoue Y, Takii K, Kumai H (2005) Photoperiod influences the growth, food intake, feed efficiency and digestibility of red sea bream (Pagrus major). Aquaculture 250:666–673. doi:10.1016/j.aquaculture.2005.04.047

    Article  Google Scholar 

  10. Brüning A, Hölker F, Preuer T, Kloas W (submitted) Influence of artificially induced light pollution on the hormone system of perch and roach in a rural habitat. Aquat Sci

  11. Brüning A, Hölker F, Wolter C (2011) Artificial light at night: implications for early life stages development in four temperate freshwater fish species. Aquat Sci 73:143–152. doi:10.1007/s00027-010-0167-2

    Article  Google Scholar 

  12. Brüning A, Hölker F, Franke S, Preuer T, Kloas W (2015) Spotlight on fish: light pollution affects circadian rhythms of European perch but does not cause stress. Sci Total Environ 511:516–522. doi:10.1016/j.scitotenv.2014.12.094

    PubMed  Article  CAS  Google Scholar 

  13. 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(Part A):214–222. doi:10.1016/j.scitotenv.2015.11.023

    PubMed  Article  CAS  Google Scholar 

  14. Buchanan BW (1993) Effects of enhanced lighting on the behaviour of nocturnal frogs. Anim Behav 45:893–899. doi:10.1006/anbe.1993.1109

    Article  Google Scholar 

  15. Cameron NE (1982) The photopic spectral sensitivity of a dichromatic teleost fish (Perca fluviatilis). Vis Res 22:1341–1348. doi:10.1016/0042-6989(82)90223-1

    CAS  PubMed  Article  Google Scholar 

  16. Carnevali O, Gioacchini G, Maradonna F, Olivotto I, Migliarini B (2011) Melatonin induces follicle maturation in Danio rerio. PLoS One 6:e19978. doi:10.1371/journal.pone.0019978

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. Chepesiuk R (2009) Missing the dark: health effects of light pollution. Environ Health Perspect 117:A20–A27

    PubMed  PubMed Central  Article  Google Scholar 

  18. Cowing JA, Poopalasundaram S, Wilkie SE, Bowmaker JK, Hunt DM (2002) Spectral tuning and evolution of short wave-sensitive cone pigments in Cottoid fish from Lake Baikal†. Biochemistry 41:6019–6025. doi:10.1021/bi025656e

    CAS  PubMed  Article  Google Scholar 

  19. Davie A, Mazorra de Quero C, Bromage N, Treasurer J, Migaud H (2007) Inhibition of sexual maturation in tank reared haddock (Melanogrammus aeglefinus) through the use of constant light photoperiods. Aquaculture 270:379–389. doi:10.1016/j.aquaculture.2007.04.052

    Article  Google Scholar 

  20. Davies TW, Bennie J, Gaston KJ (2012) Street lighting changes the composition of invertebrate communities. Biol Lett 8:764–767. doi:10.1098/rsbl.2012.0216

    PubMed  PubMed Central  Article  Google Scholar 

  21. Davies TW, Bennie J, Inger R, de Ibarra NH, Gaston KJ (2013) Artificial light pollution: are shifting spectral signatures changing the balance of species interactions? Glob Chang Biol 19:1417–1423. doi:10.1111/gcb.12166

    PubMed  PubMed Central  Article  Google Scholar 

  22. Douglas RH (1986) Photopic spectral sensitivity of a teleost fish, the roach (Rutilus rutilus), with special reference to its ultraviolet sensitivity. J Comp Physiol 159:415–421. doi:10.1007/bf00603986

    CAS  Article  Google Scholar 

  23. Duray M, Kohno H (1988) Effects of continuous lighting on growth and survival of first-feeding larval rabbitfish, Siganus guttatus. Aquaculture 72:73–79. doi:10.1016/0044-8486(88)90147-0

    Article  Google Scholar 

  24. Ekström P, Meissl H (1997) The pineal organ of teleost fishes. Rev Fish Biol Fish 7:199–284. doi:10.1023/A:1018483627058

    Article  Google Scholar 

  25. Ekström P, Meissl H (2010) Pineal photoreception and temporal physiology in fish. In: Biological clock in fish. Science Publishers, pp 35–70. doi:10.1201/b10170-4

  26. Enright Jennifer M, Toomey Matthew B, S-y S, Temple Shelby E, Allen James R, Fujiwara R, Kramlinger Valerie M, Nagy Leslie D, Johnson Kevin M, Xiao Y, How Martin J, Johnson Stephen L, Roberts Nicholas W, Kefalov Vladimir J, Guengerich FP, Corbo Joseph C (2015) Cyp27c1 red-shifts the spectral sensitivity of photoreceptors by converting vitamin A1 into A2. Curr Biol 25:3048–3057. doi:10.1016/j.cub.2015.10.018

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Falcón J, Meissl H (1981) The photosensory function of the pineal organ of the pike (Esox lucius L.) correlation between structure and function. J Comp Physiol 144:127–137. doi:10.1007/bf00612806

    Article  Google Scholar 

  28. Falcón J, Tanabe J (1983) Early receptor potential of pineal organ and lateral eye of the pike. Naturwissenschaften 70:149–150. doi:10.1007/bf00401607

    PubMed  Article  Google Scholar 

  29. Falcón J, Besseau L, Boeuf G (2006) Molecular and cellular regulation of pineal organ responses. In: Hara T, Zielinski B (eds) Fish physiology: sensory systems neuroscience, vol 25. Academic Press, Elsevier, pp 243–306

    Chapter  Google Scholar 

  30. Falcón J, Besseau L, Fuentès M, Sauzet S, Magnanou E, Boeuf G (2009) Structural and functional evolution of the pineal melatonin system in vertebrates. Ann N Y Acad Sci 1163:101–111

    PubMed  Article  CAS  Google Scholar 

  31. Falcón J, Migaud H, Munoz-Cueto JA, Carrillo M (2010) Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165:469–482. doi:10.1016/j.ygcen.2009.04.026

    PubMed  Article  CAS  Google Scholar 

  32. Falcón J, Besseau L, Magnanou E, Herrero MJ, Nagai M, Boeuf G (2011) Melatonin, the time keeper: biosynthesis and effects in fish. Cybium 35:3–18

    Google Scholar 

  33. Felip A, Zanuy S, Muriach B, Cerdá-Reverter JM, Carrillo M (2008) Reduction of sexual maturation in male Dicentrarchus labrax by continuous light both before and during gametogenesis. Aquaculture 275:347–355. doi:10.1016/j.aquaculture.2008.01.020

    Article  Google Scholar 

  34. Fernandes António M, Fero K, Arrenberg Aristides B, Bergeron Sadie A, Driever W, Burgess Harold A (2012) Deep brain photoreceptors control light-seeking behavior in zebrafish larvae. Curr Biol 22:2042–2047. doi:10.1016/j.cub.2012.08.016

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. Fleige S, Pfaffl MW (2006) RNA integrity and the effect on the real-time qRT-PCR performance. Mol Asp Med 27:126–139. doi:10.1016/j.mam.2005.12.003

    CAS  Article  Google Scholar 

  36. Franke S, Brüning A, Hölker F, Kloas W (2013) Study of biological action of light on fish. J Light Vis Environ 37

  37. Gaildrat P, Falcon J (1999) Expression of melatonin receptors and 2-[(125)I]iodomelatonin binding sites in the pituitary of a teleost fish. Adv Exp Med Biol 460:61–72

    CAS  PubMed  Article  Google Scholar 

  38. García-López Á, Pascual E, Sarasquete C, Martínez-Rodríguez G (2006) Disruption of gonadal maturation in cultured Senegalese sole Solea senegalensis Kaup by continuous light and/or constant temperature regimes. Aquaculture 261:789–798. doi:10.1016/j.aquaculture.2006.09.005

    Article  Google Scholar 

  39. Gaston KJ (2013) Sustainability: a green light for efficiency. Nature 497:560–561. doi:10.1038/497560a

    CAS  PubMed  Article  Google Scholar 

  40. Gaston KJ, Davies TW, Bennie J, Hopkins J (2012) 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

    PubMed  PubMed Central  Article  Google Scholar 

  41. Gaston KJ, Bennie J, Davies TW, Hopkins J (2013) The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol Rev 88:912–927. doi:10.1111/brv.12036

    PubMed  Article  Google Scholar 

  42. Gaston KJ, Visser ME, Hölker F (2015) The biological impacts of artificial light at night: the research challenge. Philos Trans R Soc Lond B Biol Sci 370 doi:10.1098/rstb.2014.0133

  43. Hölker F, Breckling B (2005) A spatiotemporal individual-based fish model to investigate emergent properties at the organismal and the population level. Ecol Model 186:406–426. doi:10.1016/j.ecolmodel.2005.02.010

    Article  Google Scholar 

  44. Hölker F, Dörner H, Schulze T, Haertel-Borer SS, Peacor SD, Mehner T (2007) Species-specific responses of planktivorous fish to the introduction of a new piscivore: implications for prey fitness. Freshw Biol 52:1793–1806. doi:10.1111/j.1365-2427.2007.01810.x

    Article  Google Scholar 

  45. Hölker F, Moss T, Griefahn B, Kloas W, Voigt CC, Henckel D, Hänel A, Kappeler PM, Völker S, Schwope A, Franke S, Uhrlandt D, Fischer J, Klenke R, Wolter C, Tockner K (2010a) The dark side of light: a transdisciplinary research agenda for light pollution policy. Ecol Soc 15:13

    Article  Google Scholar 

  46. Hölker F, Wolter C, Perkin EK, Tockner K (2010b) Light pollution as a biodiversity threat. Trends Ecol Evol 25:681–682. doi:10.1016/j.tree.2010.09.007

    PubMed  Article  Google Scholar 

  47. Hölker F, Wurzbacher C, Weißenborn C, Monaghan MT, Holzhauer SIJ, Premke K (2015) Microbial diversity and community respiration in freshwater sediments influenced by artificial light at night. Philos Trans R Soc Lond B Biol Sci 370 doi:10.1098/rstb.2014.0130

  48. Imsland AK, Folkvord A, Stefansson SO (1995) Growth, oxygen consumption and activity of juvenile turbot (Scophthalmus maximus L.) reared under different temperatures and photoperiods. Neth J Sea Res 34:149–159. doi:10.1016/0077-7579(95)90023-3

    Article  Google Scholar 

  49. Imsland AK, Handeland S, Stefansson S (2014) Photoperiod and temperature effects on growth and maturation of pre- and post-smolt Atlantic salmon. Aquac Int 22:1331–1345. doi:10.1007/s10499-014-9750-1

    Article  Google Scholar 

  50. Isobe SI, Hamamura S (2000) Light pollution and its energy loss. Astrophys Space Sci 273:289–294. doi:10.1023/a:1002719404278

    Article  Google Scholar 

  51. Jamet J-L, Desmolles F (1994) Growth, reproduction and condition of roach (Rutilus rutilus (L.)), perch (Perca fluviatilis, L.) and Ruffe (Gymnocephalus cernuus (L.)) in eutrophic Lake Aydat (France). Int Rev Gesamten Hydrobiol Hydrogr 79:305–322. doi:10.1002/iroh.19940790216

    Article  Google Scholar 

  52. Jones TM, Durrant J, Michaelides EB, Green MP (2015) Melatonin: a possible link between the presence of artificial light at night and reductions in biological fitness Philos Trans R Soc Lond B Biol Sci 370 10.1098/Rstb.2014.0122

  53. 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. doi:10.1016/j.physbeh.2015.12.012

    PubMed  Article  CAS  Google Scholar 

  54. Juell J-E, Fosseidengen JE (2004) Use of artificial light to control swimming depth and fish density of Atlantic salmon (Salmo salar) in production cages. Aquaculture 233:269–282. doi:10.1016/j.aquaculture.2003.10.026

    Article  Google Scholar 

  55. Kissil GW, Lupatsch I, Elizur A, Zohar Y (2001) Long photoperiod delayed spawning and increased somatic growth in gilthead seabream (Sparus aurata). Aquaculture 200:363–379. doi:10.1016/S0044-8486(01)00527-0

    Article  Google Scholar 

  56. Kojima D, Mano H, Fukada Y (2000) Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci 20:2845–2851

    CAS  PubMed  Google Scholar 

  57. Kolkovski S, Dabrowski K (1998) Off-season spawning of yellow perch. Prog Fish Cult 60:133–136. doi:10.1577/1548-8640(1998)060<0133:ossoyp>2.0.co;2

    Article  Google Scholar 

  58. Kurvers RHJM, Hölker F (2014) Bright nights and social interactions: a neglected issue. Behav Ecol. doi:10.1093/beheco/aru223

  59. Kyba C, Hänel A, Hölker F (2014) Redefining efficiency for outdoor lighting. Energy Environ Sci 7:1806–1809

    Article  Google Scholar 

  60. van Langevelde F, Ettema JA, Donners M, WallisDeVries MF, Groenendijk D (2011) Effect of spectral composition of artificial light on the attraction of moths. Biol Conserv 144:2274–2281. doi:10.1016/j.biocon.2011.06.004

    Article  Google Scholar 

  61. Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198. doi:10.1890/1540-9295(2004)002[0191:elp]2.0.co;2

    Article  Google Scholar 

  62. Macquarrie DW, Vanstone WE, Markert JR (1979) Photoperiod induced off-season spawning of pink salmon (Oncorhynchus gorbuscha). Aquaculture 18:289–302. doi:10.1016/0044-8486(79)90033-4

    Article  Google Scholar 

  63. Maitra SK, Chattoraj A, Mukherjee S, Moniruzzaman M (2013) Melatonin: a potent candidate in the regulation of fish oocyte growth and maturation. Gen Comp Endocrinol 181:215–222. doi:10.1016/j.ygcen.2012.09.015

    CAS  PubMed  Article  Google Scholar 

  64. Marchesan M, Spoto M, Verginella L, Ferrero EA (2005) Behavioural effects of artificial light on fish species of commercial interest. Fish Res 73:171–185. doi:10.1016/j.fishres.2004.12.009

    Article  Google Scholar 

  65. Migaud H, Taylor JF, Taranger GL, Davie A, Cerdá-Reverter JM, Carrillo M, Hansen T, Bromage NR (2006a) A comparative ex vivo and in vivo study of day and night perception in teleosts species using the melatonin rhythm. J Pineal Res 41:42–52. doi:10.1111/j.1600-079X.2006.00330.x

    CAS  PubMed  Article  Google Scholar 

  66. Migaud H, Wang N, Gardeur J-N, Fontaine P (2006b) Influence of photoperiod on reproductive performances in Eurasian perch Perca fluviatilis. Aquaculture 252:385–393. doi:10.1016/j.aquaculture.2005.07.029

    Article  Google Scholar 

  67. Migaud H, Cowan M, Taylor J, Ferguson HW (2007) The effect of spectral composition and light intensity on melatonin, stress and retinal damage in post-smolt Atlantic salmon, Salmo salar. Aquaculture 270:390–404. doi:10.1016/j.aquaculture.2007.04.064

    CAS  Article  Google Scholar 

  68. Migaud H, Davie A, Taylor JF (2010) Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol 76:27–68. doi:10.1111/j.1095-8649.2009.02500.x

    CAS  PubMed  Article  Google Scholar 

  69. Miller MW (2006) Apparent effects of light pollution on singing behavior of American Robins. Condor 108:130–139. doi:10.1650/0010-5422(2006)108[0130:aeolpo]2.0.co;2

    Article  Google Scholar 

  70. Mylonas CC, Fostier A, Zanuy S (2010) Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 165:516–534. doi:10.1016/j.ygcen.2009.03.007

    CAS  PubMed  Article  Google Scholar 

  71. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, Uesaka M, Kimijima M, Hashimoto R, Arai N, Suga T, Kosuge K, Abe T, Maeda R, Senga T, Amiya N, Azuma T, Amano M, Abe H, Yamamoto N, Yoshimura T (2013) The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun 4 doi:10.1038/ncomms3108

  72. Newman RC, Ellis T, Davison PI, Ives MJ, Thomas RJ, Griffiths SW, Riley WD (2015) Using novel methodologies to examine the impact of artificial light at night on the cortisol stress response in dispersing Atlantic salmon (Salmo salar L.) fry. Conserv Physiol 3:cov051. doi:10.1093/conphys/cov051

    PubMed  PubMed Central  Article  Google Scholar 

  73. Okun N, Mehner T (2005) Distribution and feeding of juvenile fish on invertebrates in littoral reed (Phragmites) stands. Ecol Freshw Fish 14:139–149. doi:10.1111/j.1600-0633.2005.00087.x

    Article  Google Scholar 

  74. Oliveira C, Ortega A, López-Olmeda JF, Vera LM, Sánchez-Vázquez FJ (2007) Influence of constant light and darkness, light intensity, and light Spectrum on plasma melatonin rhythms in Senegal sole. Chronobiol Int 24:615–627. doi:10.1080/07420520701534657

    CAS  PubMed  Article  Google Scholar 

  75. Oliveira C, Duncan NJ, Pousão-Ferreira P, Mañanós E, Sánchez-Vázquez FJ (2010) Influence of the lunar cycle on plasma melatonin, vitellogenin and sex steroids rhythms in Senegal sole, Solea senegalensis. Aquaculture 306:343–347. doi:10.1016/j.aquaculture.2010.05.003

    CAS  Article  Google Scholar 

  76. Oppedal F, Lasse Taranger G, Juell J-E, Fosseidengen JE, Hansen T (1997) Light intensity affects growth and sexual maturation of Atlantic salmon (Salmo salar) postsmolts in sea cages. Aquat Living Resour 10:351–357

    Article  Google Scholar 

  77. Pankhurst NW, Porter MJR (2003) Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiol Biochem 28:385–389. doi:10.1023/b:fish.0000030602.51939.50

    CAS  Article  Google Scholar 

  78. Pauley SM (2004) Lighting for the human circadian clock: recent research indicates that lighting has become a public health issue. Med Hypotheses 63:588–596. doi:10.1016/j.mehy.2004.03.020

    PubMed  Article  Google Scholar 

  79. Peirson SN, Halford S, Foster RG (2009) The evolution of irradiance detection: melanopsin and the non-visual opsins. Philos Trans R Soc London B Biol Sci 364:2849–2865

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  80. Perkin EK, Hölker F, Richardson JS, Sadler JP, Wolter C, Tockner K (2011) The influence of artificial light on stream and riparian ecosystems: questions, challenges, and perspectives ecosphere 2:art122 doi:10.1890/es11-00241.1

  81. Perkin EK, Hölker F, Heller S, Berghahn R (2014a) Artificial light and nocturnal activity in gammarids. Peer J 2:e279

    PubMed  PubMed Central  Article  Google Scholar 

  82. Perkin EK, Hölker F, Tockner K (2014b) The effects of artificial lighting on adult aquatic and terrestrial insects. Freshw Biol 59:368–377. doi:10.1111/fwb.12270

    Article  Google Scholar 

  83. Perkin EK, Hölker F, Tockner K, Richardson JS (2014c) Artificial light as a disturbance to light-naïve streams. Freshw Biol 59:2235–2244. doi:10.1111/fwb.12426

    Article  Google Scholar 

  84. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. Philp AR, Garcia-Fernandez JM, Soni BG, Lucas RJ, Bellingham J, Foster RG (2000) Vertebrate ancient (VA) opsin and extraretinal photoreception in the Atlantic salmon (Salmo salar). J Exp Biol 203:1925–1936

    CAS  PubMed  Google Scholar 

  86. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. Springer, New York

    Book  Google Scholar 

  87. Planas JV, Swanson P (2008) Physiological function of gonadotropins in fish. In: Rocha MJ, Arukwe A, Kapoor BG (eds) Fish reproduction. CRC Press, Boca Raton, pp 37–66

    Google Scholar 

  88. Porter MJR, Duncan NJ, Mitchell D, Bromagea NR (1999) The use of cage lighting to reduce plasma melatonin in Atlantic salmon (Salmo salar) and its effects on the inhibition of grilsing. Aquaculture 176:237–244. doi:10.1016/S0044-8486(99)00113-1

    CAS  Article  Google Scholar 

  89. Redlin U (2001) Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity. Chronobiol Int 18:737–758. doi:10.1081/cbi-100107511

    CAS  PubMed  Article  Google Scholar 

  90. Renuka K, Joshi BN (2010) Melatonin-induced changes in ovarian function in the freshwater fish Channa punctatus (Bloch) held in long days and continuous light. Gen Comp Endocrinol 165:42–46. doi:10.1016/j.ygcen.2009.05.020

    CAS  PubMed  Article  Google Scholar 

  91. Riegel KW (1973) Light pollution: outdoor lighting is a growing threat to astronomy. Science 179:1285–1291. doi:10.1126/science.179.4080.1285

    CAS  PubMed  Article  Google Scholar 

  92. Riley WD, Davison PI, Maxwell DL, Newman RC, Ives MJ (2015) A laboratory experiment to determine the dispersal response of Atlantic salmon (Salmo salar) fry to street light intensity. Freshw Biol 60:1016–1028. doi:10.1111/fwb.12568

    Article  Google Scholar 

  93. Rodríguez R, Felip A, Cerqueira V, Hala E, Zanuy S, Carrillo M (2012) Identification of a photolabile period for reducing sexual maturation in juvenile male sea bass (Dicentrarchus labrax) by means of a continuous light regime. Aquacult Int 20:1071–1083. doi:10.1007/s10499-012-9510-z

    Article  CAS  Google Scholar 

  94. Swanson P, Dickey JT, Campbell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:53–59. doi:10.1023/b:fish.0000030476.73360.07

    CAS  Article  Google Scholar 

  95. Takemura A, Ueda S, Hiyakawa N, Nikaido Y (2006) A direct influence of moonlight intensity on changes in melatonin production by cultured pineal glands of the golden rabbitfish Siganus guttatus. J Pineal Res 40:236–241. doi:10.1111/j.1600-079X.2005.00306.x

    CAS  PubMed  Article  Google Scholar 

  96. Taranger GL, Aardal L, Hansen T, Kjesbu OS (2006) Continuous light delays sexual maturation and increases growth of Atlantic cod (Gadus morhua L.) in sea cages. ICES J Mar Sci 63:365–375. doi:10.1016/j.icesjms.2005.10.014

    Article  Google Scholar 

  97. Thrush MA, Duncan NJ, Bromage NR (1994) The use of photoperiod in the production of out-of-season Atlantic salmon (Salmo salar) smolts. Aquaculture 121:29–44. doi:10.1016/0044-8486(94)90005-1

    Article  Google Scholar 

  98. Titulaer M, Spoelstra K, Lange CYMJG, Visser ME (2012) 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. Trubiroha A, Kroupova H, Wuertz S, Kloas W (2012) Up-regulation of gonadotropin mRNA-expression at the onset of gametogenesis in the roach (Rutilus rutilus): evidence for an important role of brain-type aromatase (cyp19a1b) in the pituitary. Gen Comp Endocrinol 178:529–538. doi:10.1016/j.ygcen.2012.07.002

    CAS  PubMed  Article  Google Scholar 

  100. Tsuneki K (1992) A systematic survey of the occurrence of the hypothalamic saccus vasculosus in teleost fish. Acta Zool 73:67–77. doi:10.1111/j.1463-6395.1992.tb00950.x

    Article  Google Scholar 

  101. Tuxbury SM, Salmon M (2005) Competitive interactions between artificial lighting and natural cues during seafinding by hatchling marine turtles. Biol Conserv 121:311–316. doi:10.1016/j.biocon.2004.04.022

    Article  Google Scholar 

  102. Underwood H (1989) The pineal and melatonin: regulators of circadian function in lower vertebrates. Experientia 45:914–922. doi:10.1007/bf01953048

    CAS  Article  Google Scholar 

  103. Vera LM, López-Olmeda JF, Bayarri MJ, Madrid JA, Sánchez-Vázquez FJ (2005) Influence of light intensity on plasma melatonin and locomotor activity rhythms in tench. Chronobiol Int 22:67–78. doi:10.1081/CBI-200038157

    CAS  PubMed  Article  Google Scholar 

  104. Vera LM, Davie A, Taylor JF, Migaud H (2010) Differential light intensity and spectral sensitivities of Atlantic salmon, European sea bass and Atlantic cod pineal glands ex vivo. Gen Comp Endocrinol 165:25–33. doi:10.1016/j.ygcen.2009.05.021

    CAS  PubMed  Article  Google Scholar 

  105. Veras GC, Murgas LDS, Rosa PV, Zangeronimo MG, Ferreira MSS, Leon JAS-D (2013) Effect of photoperiod on locomotor activity, growth, feed efficiency and gonadal development of Nile tilapia. Rev Bras Zootec 42:844–849

    Article  Google Scholar 

  106. Villamizar N, García-Alcazar A, Sánchez-Vázquez FJ (2009) Effect of light spectrum and photoperiod on the growth, development and survival of European sea bass (Dicentrarchus labrax) larvae. Aquaculture 292:80–86. doi:10.1016/j.aquaculture.2009.03.045

    Article  Google Scholar 

  107. Volpato GL, Barreto RE (2001) Environmental blue light prevents stress in the fish Nile tilapia. Braz J Med Biol Res 34:1041–1045

    CAS  PubMed  Article  Google Scholar 

  108. Wetzel RG (2001) Light in inland waters. In: Wetzel RG (ed) Limnology, Third edn. Academic Press, San Diego, pp 49–69. doi:10.1016/B978-0-08-057439-4.50009-5

    Chapter  Google Scholar 

  109. Witherington BE, Bjorndal KA (1991) Influences of artificial lighting on the seaward orientation of hatchling loggerhead turtles Caretta caretta. Biol Conserv 55:139–149. doi:10.1016/0006-3207(91)90053-C

    Article  Google Scholar 

  110. Zakes Z, Szczepkowski M (2004) Induction of out-of-season spawning of pikeperch, Sander lucioperca (L). Aquac Int 12:11–18. doi:10.1023/B:AQUI.0000017183.40691.7d

    CAS  Article  Google Scholar 

  111. Ziv L, Tovin A, Strasser D, Gothilf Y (2007) Spectral sensitivity of melatonin suppression in the zebrafish pineal gland. Exp Eye Res 84:92–99. doi:10.1016/j.exer.2006.09.004

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

The authors like to thank Matthias Kunow and students at Leibniz-Institute of Freshwater Ecology and Inland Fisheries for technical support. Funding was provided by the “Verlust der Nacht” project (Federal Ministry of Education and Research, Germany, BMBF-033L038A).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Anika Brüning.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Brüning, A., Hölker, F., Franke, S. et al. Influence of light intensity and spectral composition of artificial light at night on melatonin rhythm and mRNA expression of gonadotropins in roach Rutilus rutilus . Fish Physiol Biochem 44, 1–12 (2018). https://doi.org/10.1007/s10695-017-0408-6

Download citation

Keywords

  • Light pollution
  • Fish
  • Reproduction
  • Biological rhythms
  • Light colour
  • Light intensity