Borneo Journal of Marine Science and Aquaculture Volume: 01 | December 2017, 33 - 38
Effect of colored light regimes on the stress response and RNA/DNA ratio of juvenile red sea bream, Pagrus major

Gunzo Kawamura1*, Teodora Uy Bagarinao2, Kazuhiko Anraku3 and Masaru Okamoto3
1Borneo Marine Research Institute, Universiti Malaysia Sabah, 88400, Kota Kinabalu, Sabah, Malaysia 2Aquaculture Department, Southeast Asian Fisheries Development Center, 5021 Tigbauan, Iloilo, Philippines 3Faculty of Fisheries, Kagoshima University, 890-0056 Kagoshima, Japan

*Corresponding author: prof.gunzo@gmail.com

Abstract

We hypothesized that fish with red-sensitive retina would be stressed by red light and thus inhibited in somatic growth. Red sea bream (Pagrus major) juveniles (total length =3 cm) with red-sensitive retina were chosen to test this hypothesis. We examined the effect of different color lights (red with λmax 605 nm; green with λmax 540 nm; blue with λmax at 435 nm; and white with full spectrum) on unfed juveniles in laboratory tanks. Stress level was measured by the plasma cortisol and glucose concentrations, and nutritional status by muscle RNA/DNA ratio. Under red light, plasma cortisol and glucose, and muscle RNA/DNA were significantly higher than under green, blue, or white light. Our hypothesis was partly supported by previous findings on the effects of the color environment and spectral sensitivity of reared fishes. However, the levels of cortisol, glucose, and RNA/DNA in this study were low compared to published values. It seems that hatchery-bred juvenile red sea bream have adapted to red-rich surface light and are able to cope with the stress of living in surface floating cages which is so different from their deep-water habitats.

Keywords: Spectral sensitivity, RNA/DNA ratio, Stress response

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Introduction

tanks of different colors (black, green, red, dark or light blue)

exhibited the lowest cortisol in red tanks (Packer et al.,

Light intensity, spectrum, and photoperiod have all been 1999). The retina of these two species lacks red-sensitive

found to have significant effects on farmed fish. Color elements. The retina of Atlantic cod is dichromatic blue- and

environments affect the stress response of fish (Kawamura green-sensitive (Anthony and Hawkins, 1983; Valen et al.,

et al., 2015) as well as the growth, development, 2014). Summer flounder has a spectral sensitivity with two

malformation, and survival of reared fish (Villamizar et al., peaks at blue (λmax 449 nm) and green (524 nm)

2011). Ambient light in surface waters is richer in longer (Horodysky et al., 2010). It is likely that fish without red-

wavelengths, but becomes blue-dominant with depth (Jerlov, sensitive retina are not negatively affected by red-rich light

1976). The maximum spectral sensitivity of the fish retina is regimes.

closely correlated with the depth of the habitat of the species; the retinal sensitivity shifts toward shorter wavelengths in deeper water (Kobayashi, 1962; Lythgoe and Partridge, 1989). Growout of demersal and benthic fish in floating cages puts them in a full-light pelagic environment that is spectrally different from their natural habitats. This
red-rich surface light is unnatural for deep-dwelling fish and could potentially stress them and compromise their welfare. Blanco-Vives et al. (2011) pointed out the importance of providing the natural underwater photoenvironment in fish farms. For the larvae of European seabass (Dicentrarchus labrax), Senegal sole (Solea senegalensis), and Atlantic cod (Gadus morhua), the use of red light should be avoided given

We hypothesized that fish with red-sensitive retina get stressed and grow slowly in growout floating cages. In the present study, red sea bream (Pagrus major) was used to test this hypothesis. This species has been shown to have red-sensitive tetrachromatic retina. The electroretinogram
of red sea bream has a spectral sensitivity maximum at 470 nm and submaxima at 550 nm and 600 nm (Kobayashi, 1962). Kawamura (1981) recorded a 701 nm sensitive Ctype S-potential, and Miyagi and Kawamura (2000) recorded a 601 nm sensitive L-type S-potential. Red sea bream showed a retinomotor response to 609 nm and 368 nm monochromatic light (Kawamura et al., 1997).

that these benthic species clearly perform better under

The red sea bream is an important aquaculture

shorter blue-green wavelengths (Villamizar et al., 2011).

species in Japan, commonly stocked as juveniles (>30 mm

However, the demersal Atlantic cod juveniles reared in metal halide light (λmax 593 nm), green cathode light (λmax 546 nm) or white light (λmax 614 nm) showed no significant difference in stress levels (Cowan et al., 2011). Similarly, summer flounder (Paralichthys dentatus) larvae reared in

total length TL) in floating gravity cages that are 4–5 m deep from the sea surface. At this stocking size, the red sea bream has already achieved retinal changes adaptive to benthic habitats. In the wild, the pelagic larvae metamorphose and settle at 12–18 mm TL and the juveniles and adults are

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Borneo Journal of Marine Science and Aquaculture Volume: 01 | December 2017, 33 - 38

demersal thereafter, usually inhabiting the seafloor 150 m deep or more (Mitsunaga, 2000). Rods and twin cones are formed in the retina during metamorphosis; the rod density increases and the visual axis shifts from temporal to ventrotemporal at 30 mm TL (Kawamura et al., 1984). A ventrotemporal visual axis is common among demersal fish (Boehlert, 1978; Shand, 1994).
In this paper, we describe the effect of light spectrum on juvenile red sea bream in white tanks in terms of the stress response (indicated by plasma cortisol and plasma glucose levels) and the nutritional status (by
RNA/DNA ratio).
Materials and Methods
Juvenile red sea bream and husbandry Hatchery bred and reared juveniles of the red sea bream (7.5–11.7 cm body length, 13.2–44.2 g body weight) were obtained from the Kagoshima Fish Farming Association (Tarumizu Station) and used in the experiment at the Kamoike Marine Production Laboratory of the Faculty of Fisheries, Kagoshima University, Japan. Four white highdensity polyethylene circular tanks (60 cm diameter, 75 cm high) were covered with either white, red, green, or blue plastic sheets and arranged as independent compartments in an indoor concrete tank. Seawater was pumped directly from the Kagoshima bay, sand-filtered, aerated to maintain the dissolved oxygen near 100% saturation, and supplied to each tank at a flow-through rate of 1.4 L min-1. Water temperature ranged 27.5–31.0oC.
Fifteen specimens of the fish were stocked in each tank and held without food for 8 days (plus a day without food during transport). All the fish survived during these 9 days of food deprivation. Trial on 15 specimens was made for the reason that earlier studies suggested large individual variations in the RNA/DNA ratio during ontogenetic development (Clemmesen, 1987; Raae et al., 1988; Richard et al., 1991). Fish were starved to reduce variability in the RNA/DNA turnover as reported by Raae et al. (1988) and Richard et al., 1991).
The handling of the fish for trials was in compliance with the guidelines of the Animal Care and Use Committee of Kagoshima University and with the regulations for the care and use of laboratory animals in Japan.
Color treatments Color treatments of the fish were decided on the basis of information established earlier. This was considered essential for success of the experiment in generating new knowledge. The baseline information used was: duplex retina of the red sea bream with rods and cones, and particularly a regular cone mosaic with twin cones, a central single cone, and additional single cones (Kawamura et al., 1984), color vision capability (Kawamura, 1981), sensitivity to ultraviolet light (Miyagi and Kawamura, 2000), spectral sensitivity of retina with peak wavelength λmax at 470 nm (sensitivity

100%) and sub-maxima at 550 nm (50%) and 600 nm (20%) (Kobayashi, 1962).
This study tested four color regimes (white, blue, green and red, all fully visible to red sea bream) in four tanks with 15 fish each. Normal white light was produced with a 17 W fluorescent lamp with full spectrum (Matsushita, model L20S·N·EDL). Color regimes were produced with 17 W fluorescent lamps (Toshiba, model Neoball): blue (Toshiba, model EFG14EBG with λmax at 435 nm); green (Toshiba, model EFG14EGG with λmax 540 nm); and red (Toshiba, model EFG14EREG with λmax 605 nm). Lamps were covered with cellophane filters of the respective colors and suspended 55 cm above the water surface of the four tanks. The red and green filters cut the short wavelengths emitted by the red and green lamps, respectively. The blue filter cuts out the 550 nm emission from the blue lamp. The spectral irradiance of the four fluorescent lamps and the transmittance of the three color cellophane filters were recorded with a spectroradiometer (HSR-8100, Maki Manufacturing Co., Ltd., Hamamatsu, Japan) over the wavelength band from 400 nm to 750 nm (Figure 1).
Figure 1. Irradiance spectra for four fluorescent lamps (bold lines) and transmittance spectra of three color cellophane filters
Taking the spectral sensitivity of the eye with a maximum in blue, sub-maxima in green and of less-redsensitive eye of red sea bream (Kobayashi, 1962) into consideration, light intensity (photon flux density) transmitted through the cellophane filters was as follows: white, 0.167 μmol m-2 s-1; blue, 0.201 μmol m-2 s-1; green, 0.292 μmol m-2 s-1; red, 0.498 μmol m-2 s-1. Photoperiod in the tanks was set at 12L:12D, i.e., the fish were exposed to their respective color regimes for 12 h, then the lamps were turned off for a complete darkness for 12 h. Histological examination of the retinae showed that the fish in the four color regimes were all light-adapted in daytime.

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Borneo Journal of Marine Science and Aquaculture Volume: 01 | December 2017, 33 - 38

Assays of plasma cortisol, plasma glucose, and muscle RNA/DNA. Test specimens of the fish were deprived of food. After 8 days of exposure to the four color regimes, the fish were all taken out from the tanks and euthanized in 0.2% phenoxyethanol. Blood was collected from the caudal vein of each fish into haematocrit capillary tubes, centrifuged at 12000 rpm for 10 min, and frozen at –80°C. Plasma samples from three fish were combined for five replicate assays of plasma cortisol (Cortisol ELISA Kit, Neogen Corporation, K.Y., U.S.A.) and glucose (glucose-oxidase kit, Iatro-chrome GLULQ, Iatron Laboratories Co., Tokyo, Japan). Muscle samples (about 1 g) were collected from the trunk of each fish and frozen at −80°C until determination of the quantity of RNA and DNA according to the method of Nakano (1988).
Statistical analysis One-way ANOVA was used for statistical analysis. Where significant differences were found, the mean of each treatment and among treatments were compared using Tukey's test of multiple comparison. Significance was accepted at P < 0.05.
Results and Discussion
The cortisol level in the fish from the red light treatment was 3.0 ± 0.2 ng mL-1. No cortisol was detected (below the sensitivity of the method used) in fish from the other treatments. It has been established that under conditions of stress, the hormones cortisol and catecholamines are released into the bloodstream (Randall and Perry, 1992), and consequently plasma glucose increases (Begg and Pankhurst, 2004). Cortisol and glucose are good initial stress indicators (Martínez-Porchas et al., 2009). Plasma glucose 54 ± 18.5 mg dL-1 was significantly higher in fish under red light, but not different among fish under green, blue, and white light exposures (P > 0.05) (Figure 2a).
Mean RNA/DNA ratio was 0.16 ± 0.05 in fish under red light, significantly higher than 0.06 ± 0.02 under green; 0.08 ± 0.03 under blue; and 0.09 ± 0.03 under white (P < 0.05) (Figure 2b).
A characteristic behavioral response to stress in fish is known to be reduction in food intake (Wendelaar Bonga, 1997; Bernier, 2006). In this experiment the fish were not fed and the growth may have been compromised due to starvation. This is reflected in the RNA/DNA ratio which has been shown to be a sensitive indicator of instantaneous nutritional status (Clemmesen, 1987) and growth rate (Tong et al., 2010).
The visible light spectrum is an important factor for red sea bream and should be considered in efforts to optimize growth and production in floating cage farms. The present study showed that starved red sea bream was significantly stressed (highest plasma cortisol and glucose) under red light but not under green, blue, or white light. The 3.0 ± 0.2 ng mL-1 cortisol detected in red sea bream in this study was similar to the 3.0 ± 0.3 ng mL-1 cortisol in stressed pallid sturgeon,

Scaphirhynchus albus (Barton, 2002), but much lower than the 60 ng mL-1cortisol in air-exposed red sea bream larvae (Ji et al., 2009). The 54 ± 18.5 mg dL-1 glucose in red sea bream in this study was similar to 55 mg dL-1in pre-stressed red sea bream larvae but much lower than the 172.1 mg dL-1 in airexposed stressed larvae (Ji et al., 2009). Thus, it is not clear from the data if cortisol and glucose levels indicate actual stress, but it is clear that the red light regime elicits higher levels of both. These results support our hypothesis.
Figure 2. (A) Plasma glucose concentrations and (B) muscle RNA/DNA ratio in juvenile red sea bream under four different color treatments. Values are means ± SE of 15 fish specimens. Mean values with different letter superscripts are significantly different (p < 0.05, Tukey's multiple comparison test)
Higher stress response under red light was also reported for four other species: gilthead sea bream (Sparus aurata), common carp (Cyprinus carpio), rainbow trout (Oncorhynchus mykiss) and beluga (Huso huso) (Table 1). In contrast, the Atlantic cod, the summer flounder, and the red porgy (Pagrus pagrus) were not stressed or were even destressed under a red environment, and the European eel (Anguilla Anguilla) showed highest survival in a red tank (Table 1). These latter four species lack red-sensitive retina (Table 1).
We expected that somatic growth of red sea bream would be inhibited under a stressful red-light environment. Indeed, these red sea bream had RNA/DNA ratios < 0.16, much lower than the 3.7–4.2 reported for red sea bream larvae (Kato et al., 2012). The low RNA/DNA ratios in the present study can be attributed less to stress under red light and more to lack of food for 9 d. However, the effect of starvation seems less under red light.
High stress does not necessarily result in poor growth in fish. Higher stress with better growth performance under red light or tank was also observed in rainbow trout, summer flounder, and Asian seabass (Lates calcarifer), all three species with red sensitive retina (Table 1). Inhibited growth under red light was reported for seven species: gilthead sea bream, common carp, beluga, barfin flounder (Verasper moseri), thin lip mullet (Liza ramada), striped trumpeter (Latris lineata) and Nile tilapia (Oreochromis
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Borneo Journal of Marine Science and Aquaculture Volume: 01 | December 2017, 33 - 38

Table 1. Effects of colors of light or tank on growth, survival, and stress response of fish. Visual spectral sensitivity of fish is also shown

Fish and stage

Species name

Color of tank or light (λmax, nm)

Stress response

Fishes negatively affected by red color of light or tank

Red sea bream

Pagrus major

Light: red (605), green (540), blue (435)

Highest plasma
cortisol and glucose in red

Gilthead

Sparus

seabream (30 g) aurata

Light: blue (480), red (605), white

Increased dopaminergic activity in red

Common carp juveniles

Cyprinus carpio

Tank: white, black, red, Highest cortisol

blue, yellow

in red

Rainbow trout (145 g)
Beluga juveniles

Oncorhynchus mykiss
Huso huso

Light: blue, red, white
Light: blue, green, red, white

High glucose level in blue
and red Elevated cortisol and
glucose in red

Barfin flounder juveniles

Verasper moseri

Tank: blue, green, red, white

Thinlip mullet larvae

Liza ramada

Tank: white, black, red, green, yellow, blue

Striped
trumpeter larvae

Latris lineata

Tank: black, blue,
green, red, white, mottled

Nile tilapia juveniles

Oreochromis niloticus

Light: blue, green, yellow, red

Fishes not negatively affected by red colour of light or tank

Atlantic cod juveniles

Gadus morhua

Light: green (546),
metal halide (593), white (614)

No clear effect

Summer

Paralichthys

flounder larvae dentatus

Red porgy (372 g)
Asian seabass juveniles

Pagrus pagrus
Lates calcarifer

Tank: Black, green, red, dark and light blue
Tank: white, red
Tank: blue, green, yellow, red

Lowest cortisol in red
No difference in cortisol level after handling stress

European eel larvae

Anguilla anguilla

Light: blue, green, red, white

Growth and survival
Highest RNA/DNA ratio in red Reduced growth in red Lower final body weight in red and black Best growth in red
Negative impact on growth in red
Growth best in blue, lowest in red Retarded growth in red, black, green and blue Worst jaw malformation, and lowest growth in red Growth better in blue, lowest in red
Highest weight gain in red
Highest growth in red
Best survival in red

Author for color test
Present study
Karakatsouli et al. (2007)
Ebrahimi (2011)
Karakatsouli et al. (2008) Banan et al. (2011)
Yamanome et al. (2009)
El-Sayed and ElGhobashy (2011)
Cobcroft and Battaglene (2009)
Elnwishy et al. (2012)
Boehlert (1978)
McLean et al. (2008)
van der Salm et al. (2006)
Ullman et al. (2011)
Polis et al. (2014)

Spectral sensitivity (λmax, nm)
UV-, blue-, green-, redsensitive
Unknown
blue-, green-, red-sensitive
UV-, blue-, green-, redsensitive
Blue-, green-, red-sensitive
UV-, Blue-, green-, redsensitive opsin genes
Blue-, greenred-sensitive
Unknown
Violet-, blue-, green-, redsensitive
Blue-, greensensitive; lack red-sensitive element 449, 524 nm; lack redsensitive element Blue-, greensensitive; lack red-sensitive element 472, 580, 595; low-redsensitivity 434, 525 nm; lack redsensitive element

Author for spectral sensitivity
Kobayashi (1962); Kawamura (1981); Kawamura et al. (1997)
Kaneko and Tachibana (1985) Anderson et al. (2010) Govardovskii et al. (1992)
Kasagi et al. (2015)
Tamura and Niwa (1967)
Lisney et al. (2010)
Anthony and Hawkins (1983); Valen et al. (2014)
Horodysky et al. (2010)
Munz (1971)
Ullman et al. (2011)
Damjanović et al. (2005)

niloticus) (Table 1). All these species have red-sensitive retina except the gilthead sea bream and striped trumpeter which have unknown spectral sensitivity (Table 1).
The juvenile red sea bream used in this study, just like the specimens stocked in commercial marine cages, came from hatcheries and shallow-water rearing facilities and have probably adapted to the red-rich light different from that in their natural habitat. Such acclimatization allows the hatchery-bred red sea bream to grow reasonably well in surface cages despite the stress due to the red sensitivity of the retina. Nevertheless, the results of this study argue against the use of red light in Pagrus major rearing facilities such as hatcheries and roofed tanks. Fish can adapt to stress for a period of time; they look and act normal. However, energy reserves are eventually depleted, hormone imbalance occurs, the immune system is suppressed, and susceptibility to infectious diseases increases (Fevolden et al., 1992; Rottmann et al., 1992). Recently, it has been established that

stress can be reduced or suppressed by adding L-tryptophan to the fish diet (Winberg et al., 2001; Hosseini and Hoseini, 2013; Wolkers et al., 2014).
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