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p:	The specific effects on vision and body development of turbot ( HYPERLINK "javascript:;" Scophthalmus maximus) larvae caused by different light spectra
Ming Ming Hana, b, d, 1, Xian Lia, b, d,1, Le Le Wua, b, c, Shi Hong Xua, b, d, Yan Feng Wanga, b,d, Jun Lia, b, d, *
a Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China
b Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China
c University of Chinese Academy of Sciences, Beijing, 100049, China
d Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
1. They contributed equally to this work.
* Corresponding authors:  HYPERLINK "mailto:Junli@qdio.ac.cn" Junliww@126.com (Jun Li), Tel: +86 0532 82898718, address: NO.7 Nan Hai Road, Qingdao City, China, post code:266071.
Abstract 
This study was aim to find out the effect of five light spectra (white, LDW; blue, LDB; green, LDG; red, LDR and yellow, LDY) on the visual development and growth performance of turbot (Scophthalmus maximus) larvae. The number (per 100 �m) of cone cells, outer nuclear cells, ganglion cells, the ratio of outer nuclear to cone and ganglion cells, lens diameter and the minimum separable angle were determined. Variations in growth performance in total length, body mass and body color were also examined. The results showed that the LDB group underwent metamorphosis faster than did the other groups and 

attained the greatest total length, body mass and light sensitivity. The LDB group also 
completed the body color variation prior to the other groups. The LDG group exhibited a high mortality rate since 25 dph (days post hatching). We arrived at the conclusions that the spectra could affect the vision and body development of turbot larvae specifically and the blue light had the enhancing efficiency during this process, followed the white and yellow light. The red light imposed an inhibiting effect on these variations. 
Key word: spectra; visual development; growth performance;  HYPERLINK "javascript:;" Scophthalmus maximus
1 Introduction
For vision-dependent species, vision is central to light capture and behaviors such as orientation, prey detection, predator avoidance and communication [1]. Being one kind of the flatfishes, the retina of turbot (Scophthalmus maximus) exhibits protracted development, with the laminate organization emerging in larvae at the same time as yolk sac absorption [2]. The morphogenesis and cell proliferation of the retina of the turbot (Psetta maxima) has been studied thoroughly [3], and found the retina was in an undeveloped state at hatch and the ganglion cells were the first to appear. Studies also found that the retinal surface grew slightly during the larval period, but increased by more than double during metamorphosis [4].
Series of studies have verified that light spectra could affect the hatching [5], performance [6], development [7], survival and welfare [8] of �sh larvae and embryo with species specific characteristics [9]. For turbot (Scophthalmus maximus) larvae, studies have found larvae obtained the highest growth rate in a blue light background when cultured under different monochromatic environments [10]. Recently, Sierra-Flores et al. have found when treated under green (�peak=530nm), blue (�peak=455nm), white (�peak=460nm, 560nm) and red (� peak=640nm) with the intensity of 6.66 � mol/m2/s at the surface of water, the larvae under short light like blue and green light obtained higher dry weight than that under red and white light, and the result was similar in the aspect of eye diameter [11], while there still need more details about the effect of spectra on vision development initiated by different spectra. 
Metamorphosis is crucial for turbot (Scophthalmus maximus) larvae, during which the eye position, body color, retina structure, light sensitivity [5,12,13] and cone type will vary to adapt to the benthic habitats [14]. The mechanism for vision variation during metamorphosis usually including adding or removing cone cell classes [13,15,16], retinal structural reorganization [12,17] and spectral tuning variation [18,19]. In the current study, the effect of different kinds of monochromatic light on retinal development and body growth of turbot larvae will be examined with the aim to explore the plasticity of vision and growth performance under different spectra treatment especially during the metamorphosis.
2 Materials and Methods
2.1 Experimental set up
Light-emitting diodes (LEDs) were used to create the monochromatic light for each experimental group: white (LDW, 450 nm<�<700 nm), blue (LDB, � peak=475 nm), red (LDR, � peak=650 nm), yellow (LDY, � peak =600 nm) and green (LDG, � peak=550 nm). The light period was 24L: 0D, and the replicate for each spectra group was 3. Light intensity was adjusted by tuning the intensity controller which was connected to the LED light to produce the equivalent luminous flux of 1.76 � 0.04 � mol/m2/s at the surface of water. All the experiments were carried out according to U.K. Animals (Scientific Procedures) Act, 1986 and associated guidelines, EU Directive 2010/63/EU for animal experiments. 
2.2 Rearing conditions and sampling
10,000 fertilized eggs were stocked in each tank of 1.4�103 L3. The fertilized eggs were supplied by a local breeder (Weihai Sheng Hang Aquatic Science and Technology Co. Ltd, China, Weihai). Temperature was maintained at 21 � 0.5! until 20 dph (days post hatching) and was reduced to 17 � 0.5! from 20 dph to the end. The dissolved oxygen, salinity and pH was determined and maintained of 7.0-8.5mg/L, 30-32� and 7.7-8.0 respectively. According to Al-maghazachi and Gibson [20], the larvae were fed with rotifers from 0�20 dph, Artemia nauplii from 21�34 dph and with a mixed diet of Artemia nauplii and commercial feed (Kai Do, San Tong Bio-engineering CO., Ltd, Weifang, China) since 35 dph. 
From 1 to 60 dph, each six tail of larvae were sampled from each tank every day and were anesthetized in 0.1% MS-222 prior to fixation with Bouin's fluid overnight, and then stored in 70% alcohol for histological analysis (for further details see section 2.3). Prior to fixation, data relating to growth parameters, such as total length and body mass were recorded, and photographs of skin color were also taken (see section 2.5)
Morphological analysis with optical microscope
   Larva samples collected at 1, 2, 5, 10, 18, 20, 25, 30, 35, 40, 50 and 60 dph from the five experimental groups were stored in 70% alcohol and were prepared for histological analysis. Cross sections were cut into 5 �m thickness on a standard microtome (Leica-Microsystems, Germany, Wetzlar). Photographs were taken with a light microscope (DS-Ri2; Nikon, Japan, Tokyo) and the contrast and brightness of the photomicrographs were adjusted using Photo paint Software (Corel Corporation, Canada, Ottawa). The number of cone cells (C.), ganglion cells (G.) and the outer nuclear layer (O.N.) per 100 �m unit length of the retina were counted with the method described by Blaxter and Janes [21]; the ratio of O.N. to C. and O.N. to G. were also caculated; the statistics of the diameter of the lens and the minimum separable angle were done with the formula supplied by Tamura and Wisbey [22].
2.4 Transmission electron microscope (TEM) analysis
The whole eyes of larvae at 14, 21 and 52dph of LDW were removed and cut into pieces less than 1cm3 in volume and immersed into the 2.5% glutaraldehyde solution for TEM observing. The experiment was done by the lab of Medical College of Qing Dao University where the images were taken with a transmission electron microscope (Mic JEM-1200EX, Japan).
2.5 Growth and development measurement
The total length of each 20 tails of larvae at 1, 10, 20, 30, 40, 50 and 60 dph from each spectra treatment was measured. Prior to 20 dph, measurement was performed with a stereo microscope (Nikon, SMZ1000, Japan, Tokyo). A digital caliper was used after 20 dph. An electronic scale (OHAUS, ARN14CN, USA, New Jersey) was used to measure body weight. Photographs of the larvae were taken for body color development analysis under the same light conditions as the room with a camera (Sony ILCE-5100, Japan, Tokyo).  
2.6 Statistics
All data were analyzed using SPSS 17.0 (IBM, Armonk, NY, USA) and were expressed as the mean � standard error of the mean (SEM). Statistical differences in variations of visual and body parameters were determined by one-way analysis of variance (ANOVA). Tukey�s HSD test was used for multiple pairwise comparisons to identify significant differences between experimental groups. A significance level of d"5% was accepted for all tests.
3 Results
3.1 Retinal development 
The retina was undeveloped at hatching, only outer nuclear cells (O.N.), inner nuclear cells and the ganglion cell (G.) layers were observed, with no photoreceptor layer found (Fig. 2a). The pigment epithelium layer appeared at 2 dph (Fig. 2b). Later in the development process, a multi-layer retinal structure was formed, which included photoreceptor layer, outer limiting membrane, outer nuclear layer, outer plexiform layer, inner nuclear layer, inner plexiform layer, ganglion cell layer and nerve fiber layer (Fig 2(a-c)). During the whole experiment period, among all the groups, the number of O.N. increased while G. decreased (per 100 �m). Significant differences in retinal structures mainly emerged during metamorphosis, even early since 18 dph (Fig. 2q). According to Fig 4, when before metamorphosis, the photoreceptors were mainly composed of cone cells, while around metamorphosis, the rod cells increased and became the main component of photoreceptors during the post-metamorphosis.   
The LDB group varied faster in the number of O.N., C. and G. (Table 1, Fig. 2(c-o)) during the metamorphosis than other groups. After metamorphosis, this phenomenon disappeared gradually. By the end of the experiment, the LDR group had a significantly lower O.N./G. ratio than did the other experimental groups (Table 2). The LDG group seemed development abnormally in O.N. and C. with fewer number than other treatment groups with a high mortality since 25dph (Table 1).
Newly hatched larvae from all five experimental groups were hatched with one layer of horizontal cells, three layers of amacrine cells and two layers of bipolar cells (Fig. 2a). During the experiment the first two kinds of cells remained unchanged, only the bipolar cell layer varied significantly. For all groups, there was an obvious increase in the number of bipolar cell layers from 25 dph. At 50 dph, the bipolar cell layer of the LDW and LDR groups was composed of five layers, while for the LDB and LDY groups it contained three layers of cells. (Fig. 2).



























3.3 Lens development 
The diameter of the lens increased as grew. The LDB and LDG groups increased early from 10 dph than the other groups. Since 30 dph, all groups enlarged rapidly, especially the LDB group(P<0.05). The minimum separable angle kept decreasing throughout the experiment in all the groups. The slowest decrease was observed in the LDG group. By 60 dph, the LDY group obtained the largest minimum separable angle (Table 3).


3.3 Body growth and skin color variation
Before 20 dph, the LDG groups achieved longer total length than other groups. Since then, all groups increased rapidly, by 60 dph, the LDB group obtained the highest value for total length, followed by the LDW group, LDR group and LDY group (Table 4 a). Results for body weight were similar, with a rapid increase occurring between 20 and 30 dph. At 60 dph, the LDB group had attained the highest body weight, followed by the LDY group, the LDW group and the LDR group, with significant differences among the groups (Table 4(b)). 
Differences in body color development were also found. Up to 20 dph, body color changed from dark black to light or even non-black with no significant differences among the groups. The LDB group had completed its color variation by 30 dph, and the LDW and LDY groups finished this by 60 dph. It took even longer for the LDR group to complete this process (Fig. 5).





 
 
4 Discussion
The current study revealed that different light spectra could cause different effects on visual development and growth of turbot larvae, specifically during metamorphosis. Compared with other groups, the LDB group began and completed metamorphosis earlier and with better light sensitivity. These results implied that the blue light could accelerate metamorphosis in turbot larvae. Similar findings were reported for Senegal sole, where light spectrum could influence the timing of eye migration [7]. The larvae of LDG group exhibited a high mortality rate prior to metamorphosis. We presumed that the abnormally developed retina contributed to this. Further evidence was needed to confirm this point. The mortal effect of green light may be stage-dependent, because at later stages of development, larvae at 90 dph exhibited high selectivity for green light (unpublished results). 
Throughout the current study, the specific effect of spectra on the vision and body development could occur at two stages: embryo and metamorphosis. In turbot (Psetta maxima) the emergence of the retinal phenotype is delayed until hatching [3], and its color vision is developed with the absorbance of yolk sac [2,23, 24]. Based on our experiments, and according to recent findings, the non-vision opsins and circadian rhythm system should play an important role in controlling the development of retina, including the production of cone cell classes, though the concrete details were not clear [25,26]. For the other stage of metamorphosis, in wild environment, the turbot larvae will adapt to the beneath habitat where the short spectra stay predominant. After long years of evolution, the short wavelength light become the optimizing condition for the larvae, this may explain why the blue light could enhance the process of metamorphosis and the larvae under blue light treatment could obtain the better performance than other groups in our experiment. The spectra affect the metamorphosis through changing the number, types and arrangement of cone cells during  HYPERLINK \l "/javascript:;" metamorphosis and pigment [12,17,18,27]. This plasticity of vision development could be found in many species. South American cichlid fish Aequidens pulcher, whose outer segment lengths of cone cells, spectral cone ratios, cone synaptic dynamics, cone-specific horizontal cell connectivity and spectral responses, as well as visual behavior could change after long-term exposure to manipulated visual environments [28]. Juvenile salmon living in freshwater, have ultraviolet-sensitive (UVS)cones in the entire retina. During smoltification, i.e. the physiological changes preparing for life in saltwater, UVS cones disappear from large retinal regions and reappear in the same positions in the cone mosaic in adult salmon [29]. 
The plasticity can also be reflected in the network on the retina for signal delivery and brain areas for color vision with the opponent processing [19,30]. The neural signal from a certain kind of cone cell is delivered to the inner nuclear layer [31,32] in a parallel and convergent way [33], and finally reaches the corresponding ganglion cell type [31,32,34,35,36]. Besides these, a periodic variation in lighting conditions the daily light-dark, lunar (moonlight and tides) and annual cycles (seasons) cycle may also cause the substantial modifications in structure and function of retina [27]. 
Acknowledgements
This work was supported by the National Key R&D Program of China [grant numbers 2017YFD0404000]; the Key R&D Program of Shandong Province [grant numbers 2018GHY115031]; the Scientific and Technologic Development Program of Weihai [grant numbers 2017GNS05]; and China Agriculture Research System [ grant numbers CARS-47]. We were also grateful to the industry of Weihai Sheng Hang Aquatic Science and Technology Co., LTD, which supplied the equipment and place for our study.

Conflict of Interest statement:
The authors declare that they have no conflict of interest.
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Table caption






















Figure legend






























 1 LED: Light-emitting diodes; 2: TEM: transmission electron microscope









PAGE   \* MERGEFORMAT2



Fig 1. The transverse section of the retina of turbot larvae at different developmental stages in five experimental groups exposed to different light spectra. Photographs were taken under a microscope (Nikon DS-Ri2, 100�). Photographs were taken at 1 dph (a), 2 dph (b), 25 dph (c-g), 35 dph (h-k) and 50 dph (l-o). GC: ganglion cell layer; IN: inner nuclear layer; IP: inner plexiform; OF: optic nerve fibers layer; ON: outer nuclear layer; PE: pigment epithelium; PR: photoreceptors. The smaller images in the upper left corner are the ganglion cell layers which could not be shown in a single image due to size limitation. Bars=10 �m.

Fig 2. The transverse section of the retina of turbot larvae at 18 dph which instructed the different speed in metamorphosis of five spectra treatment groups, especially the variation of eye position. (10�).

Fig 3. The variation of retinal structure of LDW during the metamorphosis taken by TEM (Transmission Electron Microscope) (Mic JEM-1200EX, Japan). A-c were the photoreceptors of 14dph(pre-metamorphosis) turbot larvae. The magnification for a, b and c was 3000�, 10000� and 30000� respectively. D-f were the structure of photoreceptors at 21dph(metamorphosis). The magnification for d, e and f was 2000�, 30000� and 10000� respectively. G-h were the photoreceptors of 52dph (post- metamorphosis). The magnification for g was 20000�, for h was 8000� and for i was 6000�.


Table 1. The number of outer nuclear cells (O.N.), cone cells (C.) and ganglion cells (G.) per 100 ?@Z[op���������������						�	�	�	



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Table 2. The ratio of O.N. to C. and G. per 100 �m in the retina of turbot larvae from 1-60 dph in experimental groups exposed to different light spectra. Different letters indicate a significant difference at the same developmental stage between the experimental groups ( P<0.05).


Table 3. The lens diameter and the minimum separable angle of turbot larvae during early development. Different letters indicate a significant difference at the same developmental stage between the experimental groups (P<0.05).

Table 4(a). Total length of turbot larvae during early development (mm).

Table 4(a, b). Growth performance of turbot larvae during early development. Different letters indicate significant differences at same stage among all spectra (P<0.05).


Table 4(b). Body mass of turbot larvae during early development (mg).


Fig 4. A comparison of skin color development of turbot larvae grown under different light spectra treatments at three different stages: pre-metamorphosis (20 dph), metamorphosis (30 dph) and post- metamorphosis (35, 60 dph). Please note the photographs are only used to examine skin color and are not to scale.

Table 1. The number of outer nuclear cells (O.N.), cone cells (C.) and ganglion cells (G.) per 100 �m in the retina of turbot larvae from 1 60 dph in experimental groups exposed to different light spectra. Different letters indicate a significant difference at the same developmental stage between the experimental groups (P<0.05). 


Table 2. The ratio of O.N. to C. and G. per 100 �m in the retina of turbot larvae from 1-60 dph in experimental groups exposed to different light spectra. Different letters indicate a significant difference at the same developmental stage between the experimental groups (P<0.05).


Table 3. The lens diameter and the minimum separable angle of turbot larvae during early development. Different letters indicate a significant difference at the same developmental stage between the experimental groups (P<0.05).

Table 4(a). Total length of turbot larvae during early development (mm).

Table 4(b). Body mass of turbot larvae during early development (mg).


Table 4(a, b). Growth performance of turbot larvae during early development. Different letters indicate significant differences at same stage among all spectra (P<0.05).


Fig 1. The transverse section of the retina of turbot larvae at different developmental stages in five experimental groups exposed to different light spectra. Photographs were taken under a microscope (Nikon DS-Ri2, 100�). Photographs were taken at 1 dph (a), 2 dph (b), 25 dph (c-g), 35 dph (h-k) and 50 dph (l-o). GC: ganglion cell layer; IN: inner nuclear layer; IP: inner plexiform; OF: optic nerve fibers layer; ON: outer nuclear layer; PE: pigment epithelium; PR: photoreceptors. The smaller images in the upper left corner are the ganglion cell layers which could not be shown in a single image due to size limitation. Bars=10 �m.

Fig 2. The transverse section of the retina of turbot larvae at 18 dph which instructed the different speed in metamorphosis of five spectra treatment groups, especially the variation of eye position. (10�).

Fig 3. The variation of retinal structure of LDW during the metamorphosis taken by TEM (Transmission Electron Microscope) (Mic JEM-1200EX, Japan). A-c were the photoreceptors of 14dph(pre-metamorphosis) turbot larvae. The magnification for a, b and c was 3000�, 10000� and 30000� respectively. D-f were the structure of photoreceptors at 21dph(metamorphosis). The magnification for d, e and f was 2000�, 30000� and 10000� respectively. G-h were the photoreceptors of 52dph (post- metamorphosis). The magnification for g was 20000�, for h was 8000� and for i was 6000�.


Fig 4. A comparison of skin color development of turbot larvae grown under different light spectra treatments at three different stages: pre-metamorphosis (20 dph), metamorphosis (30 dph) and post- metamorphosis (35, 60 dph). Please note the photographs are only used to examine skin color and are not to scale.



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