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Effects of different light conditions on the retinal microstructure and ultrastructure of Dicentrarchus labrax larvae

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Abstract

Light is a key environmental parameter known to influence fish throughout various stages of their life, from embryonic development to sexually mature adults. In a recent study, the effects of different light conditions on the growth of Dicentrarchus labrax larvae were investigated using light-emitting diodes (LEDs) as a light source. Here, pathological examinations were carried out to assess whether variations in light affected the visual system of the larvae, including any negative impacts on the retina or the growth rate. Although light did not affect the total thickness (TT) of the retina, the thickness of the retinal pigment epithelium layer (PRE), photoreceptor layer (PRos/is), outer nuclear layer (ONL), and inner nuclear layer (INL), and the PRE/TT and ONL/TT ratios were all significantly higher in larvae exposed to blue light than in larvae exposed to white light. Additionally, the thickness of PRE and the outer nuclear layer and the RPE/TT and ONL/TT ratios of larvae exposed to 2.0 W m−2 were significantly lower than in larvae exposed to 0.3 W m−2. By contrast, the INL/TT ratio in larvae exposed to 2.0 W m−2 was significantly higher than in larvae exposed to 0.3 W m−2. Additionally, the INL and ganglion cell layer nuclei density of larvae exposed to 2.0 W m−2 were significantly higher than in those exposed to 0.3 W m−2 (p < 0.05). Transmission electron microscopy revealed different levels of abnormalities in the photoreceptor layers in all treatment groups. Considering the growth of the larvae, the results of the study suggest that continuous LED exposure induced damage to photoreceptor cells but was not relevant to the growth performance of D. labrax larvae. Moreover, the results obtained here also support the high plasticity of retinal development in response to altered environmental light conditions.

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References

  • Aksnes DL, Giske J (1993) A theoretical model of aquatic visual feeding. Ecol Model 67:233–250

    Google Scholar 

  • Allen DM, Hallows TE (1997) Solar pruning of retinal rods in albino rainbow trout. Vis Neurosci 14:589–600

    CAS  PubMed  Google Scholar 

  • Allison WT, Hallows TE, Johnson T, Hawryshyn CW, Allen DM (2006) Photic history modifies susceptibility to retinal damage in albino trout. Vis Neurosci 23:25–34

    PubMed  Google Scholar 

  • Behar-Cohen F, Martinsons C, Viénot F, Zissis G, Barlier-Salsi A, Cesarine JP, Enouf O, Garcia M, Picaud S, Attia D (2011a) Light-emitting diodes (LED) for domestic lighting: Any risks for the eye? Prog Retin Eye Res 30(4):239–257

    CAS  PubMed  Google Scholar 

  • Bapary MAJ, Amin MN, Takeuchi Y, Takemura A (2011) The stimulatory effects of long wavelengths of light on the ovarian development in the tropical damselfish, Chrysiptera cyanea. Aquaculture 314:188–192

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Beatty S, Koh H, Henson D, Boulton M (2000) The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 45:115–134

    CAS  PubMed  Google Scholar 

  • Begtashi I, Rodríguez L, Moles G, Zanuy S, Carrillo M (2004) Long-term exposure to continuous light inhibits precocity in juvenile male European sea bass (Dicentrarchus labrax, L.). I. morphological aspects. Aquaculture 241:539–559

    Google Scholar 

  • Behar-Cohen F, Martinsons C, Viénot F, Zissis G, Barlier-Salsi A, Cesarini JP, Enouf O, Garcia M, Picaud S, Attia D (2011b) Light-emitting diodes (LED) for domestic lighting: any risks for the eye? Pro Retin Eye Res 30:239–257

    CAS  Google Scholar 

  • Bejarano-Escobar R, Blasco M, Martín-Partido G, Francisco-Morcillo J (2012) Light-induced degeneration and microglial response in the retina of an epibenthonic pigmented teleost: age-dependent photoreceptor susceptibility to cell death. J Exp Biol 215:3799–3812

    PubMed  Google Scholar 

  • Bernardos RL, Barthel LK, Meyers JR, Raymond PA (2007) Late stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 27:7028–7040

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blaxter J, Staines ME (1971) Food searching potential in marine fish larvae. In: Crisp DJ (ed) Fourth European marine biology symposium. Cambridge University Press, Cambridge, pp 467–485

    Google Scholar 

  • Boeuf G, Le Bail PY (1999) Does light have an influence on fish growth? Aquaculture 177:129–152

    Google Scholar 

  • Bonvini E, Parma L, Gatta PP, Mandrioli L, Sirri R, Martelli G, Nannoni E, Mordenti A, Bonaldo A (2016) Effects of light intensity on growth, feeding activity and development in common sole (Solea solea L.) larvae in relation to sensory organ ontogeny. Aquac Res 47:1809–1819

    Google Scholar 

  • Braisted JE, Raymond PA (1992) Regeneration of dopaminergic neurons in goldfish retina. Development 114:913–919

    CAS  PubMed  Google Scholar 

  • Braisted JE, Essman TF, Raymond PA (1994) Selective regeneration of photoreceptors in goldfish retina. Development 120:2409–2419

    CAS  PubMed  Google Scholar 

  • Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197:63–98

    CAS  Google Scholar 

  • Bush RA, Remé CE, Malnoë A (1991) Light damage in the rat retina: the effect of dietary deprivation of N-3 fatty acids on acute structural alterations. Exp Eye Res 53:741–752

    CAS  PubMed  Google Scholar 

  • Cadet J, Douki T, Ravanat J (2010) Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 49:9–21

    CAS  PubMed  Google Scholar 

  • Carrillo M, Zanuy S, Prat F, Mañanós E, Cerdá J, Bromage N, Ramos J, Kah O (1995) Nutritional and photoperiodic effects on hormonal cycles and quality of spawning in sea bass (Diceatrarchus Labrax L.). Neth J Zool 45:204–209

    Google Scholar 

  • Chi L, Li X, Liu Q, Liu Y (2017) Photoperiod regulate gonad development via kisspeptin/kissr in hypothalamus and saccus vasculosus of Atlantic salmon (Salmo salar). PloS One 12:e0169569

    PubMed  PubMed Central  Google Scholar 

  • Dalton BE, Lu J, Leips J, Cronin TW, Carleton KL (2015) Variable light environments induce plastic spectral tuning by regional opsin coexpression in the African cichlid fish, Metriaclima zebra. Mol Ecol 24:4193–4204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Debose JL, Lema SC, Nevitt GA (2008) Dimethylsulfoniopropionate as a foraging cue for reef fishes. Science 319:1356–1356

    CAS  PubMed  Google Scholar 

  • Delori FC, Webb RH, Sliney DH (2007) Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices. J Opt Soc Am A Opt Image Sci Vis 24:1250–1265

    PubMed  Google Scholar 

  • Downing G, Litvak MK (1999) The Influence of light intensity on growth of larval haddock. N Am J Aquacult 61:135–140

    Google Scholar 

  • Downing G, Litvak MK (2001) The effect of light intensity and spectrum on the incidence of first feeding by larval haddock. J Fish Biol 59:1566–1578

    Google Scholar 

  • Fausett BV, Goldman D (2006) A role for α1 tubulin-expressing Müller glia in regeneration of the injured zebrafish retina. J Neurosci 26(23):6303–6313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernald RD (1985) Growth of the teleost eye: novel solutions to complex constraints. Environ Biol Fish 13:113–123

    Google Scholar 

  • Fimbel SM, Montgomery JE, Burket CT, Hyde DR (2007) Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J Neurosci 27:1712–1724

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fuller RC, Carleton KL, Fadool JM, Spady TC, Travis J (2005) Genetic and environmental variation in the visual properties of bluefin killifish, Lucania goodei. J Evol Biol 18:516–523

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Heil K, Pearson D, Carell T (2011) Chemical investigation of light induced DNA bipyrimidine damage and repair. Chem Soc Rev 40:4271–4278

    CAS  PubMed  Google Scholar 

  • Hitchcock P, Ochocinska M, Sieh A, Otteson D (2004) Persistent and injury-induced neurogenesis in the vertebrate retina. Prog Retin Eye Res 23:183–194

    PubMed  Google Scholar 

  • Hofmann CM, O'Quin KE, Smith AR, Carleton KL (2010) Plasticity of opsin gene expression in cichlids from Lake Malawi. Mol Ecol 19:2064–2074

    PubMed  Google Scholar 

  • Humphrey JD (2007) Systemic pathology of fish: A text and atlas of normal tissue in teleosts and their responses in disease. J Fish Dis 30:381–382

    Google Scholar 

  • Johns PR, Easter SS (1977) Growth of the adult goldfish eye. II. Increase in retinal cell number. J Comp Neur 176:331–341

    CAS  PubMed  Google Scholar 

  • Julian D, Ennis K, Korenbrot JI (1998) Birth and fate of proliferative cells in the inner nuclear layer of the mature fish retina. J Comp Neurol 394:271–282

    CAS  PubMed  Google Scholar 

  • Kröger RHH, Bowmaker JK, Wagner HJ (1999) Morphological changes in the retina of Aequidens pulcher (Cichlidae) after rearing in monochromatic light. Vision Res 39:2441–2448

    PubMed  Google Scholar 

  • Kusmic C, Gualtieri P (2000) Morphology and spectral sensitivities of retinal and extraretinal photoreceptors in freshwater teleosts. Micron 31:183–200

    CAS  PubMed  Google Scholar 

  • Lee JSF, Poretsky RS, Cook MA, Reyes-Tomassini JJ, Berejikian BA, Goetz FW (2016) Dimethylsulfoniopropionate (DMSP) increases survival of larval sablefish, Anoplopoma fimbria. J Chem Ecol 42:533–536

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JSF, Britt LL, Cook MA, Wade TH, Berejikian BA, Goetz FW (2017) Effect of light intensity and feed density on feeding behaviour, growth and survival of larval sablefish Anoplopoma fimbria. Aquac Res 48:4438–4448

    Google Scholar 

  • Marotte LR, Wye-Dvorak J, Mark RF (1979) Retinotectal reorganization in goldfish—II. Effects of partial tectal ablation and constant light on the retina. Neuroscience 4:803–810

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Monk J, Puvanendran V, Brown JA (2006) Do different light regimes affect the foraging behaviour, growth and survival of larval cod (Gadus morhua L.)? Aquaculture 257:287–293

    Google Scholar 

  • Morris AC, Scholz TL, Brockerhoff SE, Fadool JM (2008) Genetic dissection reveals two separate pathways for rod and cone regeneration in the teleost retina. Develop Neurobiol 68:605–619

    Google Scholar 

  • Negishi K, Teranishi T, Kato S, Nakamura Y (1987) Paradoxical induction of dopaminergic cells following intravitreal injection of high doses of 6-hydroxydopamine in juvenile carp retina. Dev Brain Res 33:67–79

    CAS  Google Scholar 

  • Organisciak DT, Vaughan DK (2010) Retinal light damage: Mechanisms and protection. Prog Retin Eye Res 29:113–134

    PubMed  Google Scholar 

  • Otteson DC, Hitchcock PF (2003) Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 43:927–936

    CAS  PubMed  Google Scholar 

  • Puvanendran V, Brown JA (2002) Foraging, growth and survival of Atlantic cod larvae reared in different light intensities and photoperiods. Aquaculture 214:131–151

    Google Scholar 

  • Raymond PA, Reifler MJ, Rivlin PK (1988) Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol 19:431–463

    CAS  PubMed  Google Scholar 

  • Remé CE (2005) The dark side of light: rhodopsin and the silent death of vision the proctor lecture. Invest Ophthalmol Vis Sci 46:2671–2682

    PubMed  Google Scholar 

  • Roehlecke C, Schumann U, Ader M, Knels L, Funk RHW (2011) Influence of blue light on photoreceptors in a live retinal explant system. Mol Vis 17:876–884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rozanowska MB (2012) Light-Induced damage to the retina: current understanding of the mechanisms and unresolved questions: a symposium-in-print. Photochem Photobiol 88:1303–1308

    CAS  PubMed  Google Scholar 

  • Saka S, Firat K, Süzer C (2001) Effects of light intensity on early life development of gilthead sea bream Sparus aurata Larvae. Isr J Aquac 53:139–146

    Google Scholar 

  • Sanyal S, Zeilmaker GH (1988) Retinal damage by constant light in chimaeric mice: implications for the protective role of melanin. Exp Eye Res 46:731–743

    CAS  PubMed  Google Scholar 

  • Shand J, Davies WL, Thomas N, Balmer L, Cowing KA, Pointer M, Carvalho LS, Trezise AE, Collin SP, Beazley LD, Hunt DM (2008) The infuence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, Acanthopagrus butcheri. J Exp Biol 211:1495–1503

    CAS  PubMed  Google Scholar 

  • Stefansson SO, Nilsen TO, Ebbesson LOE, Wargelius A, Madsen SS, Björnsson BT, McCormick SD (2007) Molecular mechanisms of continuous light inhibition of Atlantic salmon parr–smolt transformation. Aquaculture 273:235–245

    CAS  Google Scholar 

  • Stuart KR (2013) The effect of light on larval rearing in marine finfish. In: Qin JG (ed) Larval fish aquaculture. Nova Science Publisher Inc, New York, pp 25–40

    Google Scholar 

  • Taylor JF, North BP, Porter MJR, Bromage NR, Migaud H (2006) Photoperiod can be used to enhance growth and improve feeding efficiency in farmed rainbow trout, Oncorhynchus mykiss. Aquaculture 256:216–234

    Google Scholar 

  • Thummel R, Kassen SC, Enright JM, Nelson CM, Montgomery JE, Hyde DR (2008a) Characterization of Müller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp Eye Res 87:433–444

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thummel R, Kassen SC, Montgomery JE, Enright JM, Hyde DR (2008b) Inhibition of Müller glial cell division blocks regeneration of the light-damaged zebrafish retina. Dev Neurobiol 68:392–408

    PubMed  PubMed Central  Google Scholar 

  • Vaughan DK, Nemke JL, Fliesler SJ, Darrow RM, Organisciak DT (2002) Evidence for a circadian rhythm of susceptibility to retinal light damage. Photochem Photobiol 75:547–553

    CAS  PubMed  Google Scholar 

  • Vera LM, Migaud H (2009) Continuous high light intensity can induce retinal degeneration in Atlantic salmon, Atlantic cod and European sea bass. Aquaculture 296:150–158

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Vihtelic TS, Hyde DR (2000) Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol 44:289–307

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Villamizar N, Blanco-vives B, Migaud H, Davie A, Carboni S, Sánchez-vázquez FJ (2011) Effects of light during early larval development of some aquacultured teleosts: a review. Aquaculture 315:86–94

    Google Scholar 

  • 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  Google Scholar 

  • Wagner HJ (1990) Retinal structure of fishes. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 109–157

    Google Scholar 

  • Wagner HJ, Fröhlich E, Negishi K, Collin SP (1998) The eyes of deep-sea fish II. Functional morphology of the retina. Prog Retin Eye Res 17:637–685

    CAS  PubMed  Google Scholar 

  • Wagner HJ, Kröger RHH (2000) Effects of long-term spectral deprivation on the morphological organization of the outer retina of the blue acara (Aequidens pulcher). Philos Trans R Soc Lond B Biol Sci 355:1249–1252

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner HJ, Kröger RHH (2005) Adaptive plasticity during the development of colour vision. Prog Retin Eye Res 24:521–536

    PubMed  Google Scholar 

  • Wu J, Seregard S, Algvere PV (2006) Photochemical damage of the retina. Surv Ophthalmol 51:461–481

    PubMed  Google Scholar 

  • Yamanome T, Mizusawa K, Hasegawa E, Takahashi A (2009) Green light stimulates somatic growth in the barfin flounder Verasper moseri. J Exp Zool A Ecol Genet Physiol 311:73–79

    PubMed  Google Scholar 

  • Young RW (1976) Visual cells and the concept of renewal. Invest Ophthalmol Vis Sci 15:700–725

    CAS  PubMed  Google Scholar 

  • Youssef PN, Sheibani N, Albert DM (2011) Retinal light toxicity. Eye 25:1–14

    CAS  PubMed  Google Scholar 

  • Yu DY, Cringle SJ (2005) Retinal degeneration and local oxygen metabolism. Exp Eye Res 80:745–751

    CAS  PubMed  Google Scholar 

  • Yurco P, Cameron DA (2005) Responses of Müller glia to retinal injury in adult zebrafish. Vision Res 45:991–1002

    PubMed  Google Scholar 

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This research was supported by the National Key R&D Program of China (2017YFB0404000).

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Yan, H., Liu, Q., Shen, X. et al. Effects of different light conditions on the retinal microstructure and ultrastructure of Dicentrarchus labrax larvae. Fish Physiol Biochem 46, 613–628 (2020). https://doi.org/10.1007/s10695-019-00735-1

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