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Electroretinographic analysis of night vision in juvenile Pacific bluefin tuna (Thunnus orientalis).

Introduction

The Pacific bluefin tuna (Thunnus orientalis) is a large pelagic scombrid fish distributed widely in temperate parts of the northern Pacific Ocean (Collette and Smith, 1981). Bluefin tuna (Pacific bluefin tuna, T. orientalis: Atlantic bluefin tuna. T. thynnus; southern bluefin tuna. T. maccoyii) are ofhigh individual value, and their populations are decreasing because of overfishing (Majkowski, 2007). Despite the commercial importance of bluefin tunas, little is known about the behavior, life history, and ecology of these fish because of their extensive lifetime migrations. Physiological studies have been conducted to clarify their sensory mechanisms and predict their behavior and ecology. Tunas possess high-acuity vision (Nakamura, 1968; Kawamura et al., 1981) and an extremely well-developed optic tectum (Kawamura et al., 1981) indicating the importance of vision in these fish. Previous research using archival tags has revealed diurnal vertical migration in Pacific bluefin tuna of 450 to 780 mm fork length (FL); this migration is thought to be a response to changes in ambient light intensity at dawn and dusk (Kitagawa et al., 2004). It has therefore been believed that vision is important in these fish and that visual ability is greater in tunas than in other fishes (Nakamura, 1968; Kawamura et al., 1981). However, relevant information in early juvenile tunas is limited because of the difficulty in capturing smaller juvenile tunas and attaching tags or loggers to them.

Recently, behavioral and physiological studies have been conducted in full-cycle cultured juvenile Pacific bluefin tuna. Visual acuity (Torisawa et al., 2007a), the opsin genes for visual pigments (Miyazaki et al., 2008), and the early development of visual cells (Matsuura et al., 2009) have been investigated. It has been demonstrated that the transition from scotopic to photopic vision occurs at an illuminance of 7.52 lx in juvenile Pacific bluefin tuna of 50.7 to 96.8 mm total length (TL) (Masuma et al., 2001) and at 5.7 to 13 lx in spotted mackerel (Scomber australasicus) (FL 308 to 348 mm) (Kawamura, 1979). The illuminances required for transition in these scombrid fishes are higher than in other fish species (Masuma et al., 2001). Furthermore, the threshold illuminance for schooling behavior of juvenile Pacific bluefin tuna (standard length [SL] 70 to 110 mm) is 0.01 to 0.5 lx, which is higher than that for other species (Torisawa et al., 2007b). In a previous study, we also demonstrated that the scotopic visual threshold for optomotor reactions is at least 40-fold higher in juvenile bluefin tuna than in four marine teleosts (Ishibashi et al., 2009).

One of the biggest problems in seedling production of Pacific bluefin tuna (30 to 60 days post-hatching [dph]) is mass death caused by contact or collisions with the tank or net walls (Miyashita et al., 2000). These mass deaths are thought to be associated with some aspect of the visual function of juvenile Pacific bluefin tuna, since the number of deaths can be reduced by illumination during the night or by using striped, waffled, or polka-dot patterns of white tape placed at intervals of about 0.3 m on the tank or net walls, or both (Ishibashi et al., 2005, 2009; Ishibashi, 2006). Obvious mass deaths caused by contact or collisions have rarely been observed in any cultured fish except tunas--even in juvenile chub mackerel (Scomber japonicus), which, like the Pacific bluefin tuna, is a scombrid fish (Sawada, 2006).

The visual function of juvenile Pacific bluefin tuna thus appears to be inferior to that of other fishes under dim light conditions. However, the details are unclear. We therefore investigated the light sensitivity, spectral sensitivity, and temporal visual resolution of juvenile Pacific bluefin tunas by using an electroretinogram (ERG) technique, and we compared the results with those obtained in chub mackerel (a pelagic scombrid fish) and striped jack (Pseudocaranx dentex), a coastal carangid fish. This is the first study to compare the scotopic visual functions of Pacific bluefin tuna with those of other fishes by ERG.

Materials and Methods

Experimental fish

Thunnus orientalis (Temminck and Schlegel) (Pacific bluefin tuna). We used full-cycle cultured Pacific bluefin tuna hatched on 12 July and 2 August 2007 at the Oshima Station of the Kinki University Fisheries Laboratory, Wakayama, Japan. Juvenile growth stages (52 to 64 dph; SL 150 to 175 mm; eye diameter 9 to 10 mm) were used. The cultured fish were maintained in a square indoor tank (length, 5450 mm; width, 5450 mm; height, 1200 mm) containing filtered natural seawater (depth, 800 to 1000 mm; temperature, 25 to 28 [degrees]C; holding period 24 August to 14 September) under sunlight (with shade sheet) during the day and fluorescent bulb illumination at night. The night illumination was needed to prevent fish from colliding with tank wall in dim light (Ishibashi et al., 2005; Ishibashi, 2006). Two wild fish (SL 210 and 240 mm) were also used to compare visual function in wild and cultured fish of the same species. These fish were captured by trolling offshore from Wakayama Prefecture on 21 August 2007. The wild fish were held in a circular tank (diameter 2000 mm) containing natural seawater (depth, 800 to 1000 mm; temperature, 25 to 28 [degrees]C; holding period 21 to 27 August).

Scomber japonicus (Houttuyn) (chub mackerel). We used full-cycle cultured chub mackerel hatched on 1 June 2007 at the Shirahama Station of the Kinki University Fisheries Laboratory, Wakayama, Japan. Five specimens in juvenile growth stages (107 to 109 dph; SL 122 to 150 mm; eye diameter 10 to 12 mm) were used. Before the experiment, the fish were maintained in a circular tank (1000 1) containing filtered natural seawater (28 [degrees]C; holding period 15 to 20 September) under a natural photoperiod.

Pseudocaranx dentex (Bloch and Schneider) (striped jack). The juvenile striped jack specimens used in this experiment were obtained from the Fisheries Laboratory of Kinki University, Shirahama Station. Six juveniles (323 to 334 dph; SL 223 to 246 mm; eye diameter 14 mm) were used. Before the experiment, the fish were maintained in a circular tank (1000 1) containing filtered seawater (temperature 19 to 28 [degrees]C; holding period 14 to 25 November) under a natural photoperiod.

Electroretinogram recordings

Before the experiment, the chub mackerel and striped jack were dark-adapted for at least 1 h in a circular tank (500 1) placed in a light-tight room before their dark adaptation was completed in a light-tight metal box (see below). In contrast, to avoid collision deaths, the bluefin tuna were not dark-adapted in the dark tank before the experiment; their dark-adaptation was instead conducted entirely in the light-tight metal box. Fish were anesthetized by submersion in a solution of 2-phenoxyethanol (0.4 ml/1) and immobilized with an intramuscular injection of gallamine triethiodide (0.4 to 1.4 ml of 2 mg/kg Ringer's solution for the bluefin tuna; 0.4 ml of 50 mg/kg Ringer's solution for the chub mackerel; and 6 to 9 ml of 50 mg/kg Ringer's solution for the striped jack). The optimum amount and concentration of the gallamine triethiodide in Ringer's solution were determined to suit individual fish. The immobilized fish was taken out of the anesthetic solution and placed in the light-tight metal box (length, 37 cm; width, 51 cm; height, 41 cm). Still immobilized, the fish was dark-adapted in the box for either more than 60 min (bluefin tuna) or more than 15 min (the other two species) before the recordings were made. During the ERG recordings, the body of the fish remained out of the water, and the fish was artificially ventilated by pumping aerated seawater over the gills. The water temperature was 25 to 28 [degrees]C for the Pacific bluefin tuna, 28 [degrees]C for the chub mackerel, and 19 to 21 [degrees]C for the striped jack.

ERGs were recorded in the box by using two silver-wire electrodes (0.3-mm diameter). The recording electrode was inserted through a small hole in the cornea so that it rested on the retina. The top 3 mm of the recording electrode was bent manually into a U-shape to prevent damage to the retina. The reference electrode was a silver wire (sharpened to hold its position) placed into the skin of the cranium. The electrodes were positioned by using a micromanipulator (MN-153; Narishige, Tokyo, Japan). Electrical signals were amplified with a differential amplifier (MEG-5100; Nihon Kohden, Tokyo, Japan) using a band-pass of 0.5-300 Hz for temporal resolution and 0.5-100 Hz for other recordings. Amplified signals were transmitted simultaneously to a digital oscilloscope (DS1M12; USB Instruments, Glasgow. UK) and a laboratory computer.

The light sources used as stimuli consisted of 12 light-emitting diodes (LEDs), each of which had a different peak emission, ranging from 369 to 652 nm. The light sources have been described previously (Matsumoto et al., 2009). One of the LEDs was used as a narrow-band stimulator. The stimulating LED was selected by means of a rotary switch (one pole, 12 position). The LEDs rotated with the rotary switch. Light intensity of the stimulus was controlled by placing neutral-density filters in the light path. The attenuated light was positioned such that the light was projected onto the entire pupil of the experimental fish. The stimulus light system itself was placed outside the box. The intensities of the stimulus lights were measured at the same position as the fish eye with a radiometer sensitive to UV and visible wavelengths (USB-4000; Ocean Optics, Florida) and then converted to quanta [cm.sup.-2] [s.sup.-1], integrated over wavelengths from 300 to 750 nm. We used only dim red light while setting up the electrodes on the body of the dark-adapted fish. This light (peak emission wavelength, 654 nm; light intensity 4.9 X [10.sup.12] quanta [cm.sup.-2] [s.sup.-1] [1.1 1x] at a distance of 50 cm) was emitted from an LED worn on the researcher's head. The experimental recording apparatus and stimulus light sources have been described previously (Matsumoto et al., 2009).

Spectral sensitivity

In each recording session, ERGs were recorded in response to narrow-band stimuli of increasing intensity; each flash for 500 ms. The number of stimuli was different in each session. To maintain the dark-adapted state, at least 20 s separated the stimulus presentations. Twelve sessions were conducted--one for each wavelength. Standard responses to a 503-nm, equal-intensity light stimulus were recorded between each session for correcting the change of ERG voltage with time.

To determine retinal sensitivity, we measured the b-wave amplitude. Response versus light intensity curves were constructed for the different wavelengths, and these curves were then used to interpolate the threshold of incident light intensity required to generate criterion responses of 180 or 300 [micro]V in the Pacific bluefin tuna (n = 6) and 200, 450, or 500 [micro]V in the striped jack (n = 4). The criterion responses were determined for each fish by selecting values above the baseline recording of responses; this was done because of the variation in ERG voltage among species and individuals, and the narrow intensity ranges of stimuli among some LEDs for a detectable ERG voltage. Relative spectral sensitivity was calculated by using the inverse ratio of the threshold light intensity.

To estimate the spectral sensitivity peak wavelength from our ERG data, we fitted a template (Stavenga et al., 1993) to the averaged relative sensitivity. The parameter values were determined by a least-squares fit.

Light sensitivity

We recorded ERG responses to 503-nm light stimuli of increasing intensity for each 500-ms flash from the 503-nm LED. These data of response (V) versus light intensity (I) were plotted on V/log I curves for each fish. These curves were then fitted with the modified Naka-Rushton equation (Naka and Rushton, 1966a, b) by using a least-squares fit:

V/[V.sub.max] = [I.sup.max]/([I.sup.m] + [K.sup.m])

Where I = light intensity of stimulus (quanta [cm.sup.-2] [s.sup.-1]), V = response amplitude at intensity I, [V.sub.max] = maximum response amplitude, m = slope of the linear part of the V/log I curve, and K = light intensity of stimulus (quanta [cm.sup.-2] [s.sup.-1]) eliciting a half-maximum (1/2 [V.sub.max]) response. The values of K and m were used to compare light sensitivity and sensitivity to contrast and changing light intensities. Furthermore, to compare light sensitivities, we defined a 0.05[I.sub.503] value as the intensity of the 503-nm lights at 5% of the maximum ERG voltage. The 0.05[I.sub.max] value was corrected from the 0.05[I.sub.503] value by using our spectral sensitivity curve results and calculated as follows:

0.05[I.sub.max] = ([[Ic.sub.max]/[Ic.sub.503]]) X 0.05[I.sub.503]

= [R.sub.503] X 0.05[I.sub.503]

[R.sub.503] = [[Ic.sub.max]/[Ic.sub.503]]

Where [Ic.sub.max] is the light intensity at which the criterion ERG responds to a light stimulus at the peak sensitivity wavelength; [Ic.sub.503] is the light intensity at which the criterion ERG responds to a light stimulus at a wavelength of 503 nm; and [R.sub.503] is the relative spectral sensitivity at 503 nm calculated from the spectral sensitivity curve by using the template of Stavenga et al. (1993). The 0.05[I.sub.max] values are indicative of light sensitivity if the wavelengths of the narrow-band light stimuli peak at the spectral sensitivity peak of each species that we investigated.

Temporal resolution

We recorded the flicker ERG responses of fish to a square pulse of 503-nm light with a constant 50% duty cycle. Waveform examples are shown in Figure 1. The frequencies of the flicker stimulations were varied from 2 Hz to 40 Hz, with each frequency presented for 5 s, and with an interval of at least 1 min between different frequencies; the resulting responses were averaged. Light intensities of flicker stimuli were adjusted to 4.43, 36.1, and 503 X [10.sup.11] quanta [cm.sup.-2] [s.sup.-1] (corresponding to 0.56, 4.54, and 62.5 lx, respectively). The responses were plotted against frequency and the resulting curves fitted to the exponential function y = a X [e.sup.-bx]; this is the function that shows the best fit to the flicker ERG in dark-adapted rats (Sauve et al., 2006).

[FIGURE 1 OMITTED]

The temporal resolution of the eye was evaluated by determining the values of the slope of the exponential function, slope b, by least-squares fit, instead of using the critical flicker fusion frequency (CFFF). The frequency at which the amplitude becomes 5% of the amplitude at 2 Hz (0.05F[A.sub.2Hz]) was also defined in order to investigate the nature of the flicker ERG in fish. Although CFFF is an index commonly used for evaluating temporal resolution, it is very difficult to definitively determine the CFFF from the record of flicker ERG (Tamura and Hanyu, 1959). This difficulty arises from the fact that CFFF changes with background noise, which is not always constant in any given locality.

Data analysis

The light sensitivity and temporal resolution data were analyized by using Tukey's multiple comparison test with equal sample variances or the Steel-Dwass test with unequal sample variances. The degree of correlation between two variables was determined by using Pearson's correlation test.

Results

Spectral sensitivity

The correlation coefficients between the raw data and curve-fitted values were more than 0.95 (Pearson's correlation test). Spectral sensitivity peaks of dark-adapted fish, as estimated by fitting a function of the template of Stavenga et al. (1993), were observed at approximately 479 nm in bluefin tuna, 482 nm in chub mackerel (Matsumoto et al., 2009), and 512 nm in striped jack (Fig. 2a, b, c).

[FIGURE 2 OMITTED]

Light sensitivity

The V/log I curves for all fish in the study were fitted to the Naka-Rushton equation (Fig. 3). The correlation coefficients between the raw data and curve-fitted values were more than 0.95 (Pearson's correlation test). Table 1 lists the parameters of the Naka-Rushton equation and the related indices on the V/log I curves for 503-nm light stimuli in bluefin tuna, chub mackerel, and striped jack.

[FIGURE 3 OMITTED]
Table 1

Parameters of the Naka-Rushton fitting equations

                                          Species

Parameter              Thunnus orientalis         Scomber japonicus

log K                12.0 [+ or -] 0.202 (a)   12.1 [+ or -] 0.230 (a)

m                   0.724 [+ or -] 0.117 (a)  0.657 [+ or -] 0.0699
                                              (ab)

log                  10.2 [+ or -] 0.475 (a)   10.2 [+ or -] 0.330 (a)
(0.05[I.sub.503])

log                  10.0 [+ or -] 0.475 (a)   10.0 [+ or -] 0.330 (a)
(0.05[I.sub.max])

n                             9                         10

                                            Species

Parameter                 Pseudocaranx dentex     T. orientalis (wild)

log K                   11.7 [+ or -] 0.146 (b)     12.0, 12.1 (ab)

m                      0.566 [+ or -] 0.0657 (b)   0.621, 0.798 (ab)

log (0.05[I.sub.503])   9.43 [+ or -] 0.298 (b)     9.90, 10.5 (ab)

log (0.05[I.sub.max])   9.42 [+ or -] 0.298 (b)     9.75, 10.3 * (ab)

n                                5                        2

Values with different letters in the same column are significantly
different (P < 0.05).

* Calculated from the spectral sensitivity curve for cultured tuna.


The variable K, which is the irradiance required to generate a half response of [V.sub.max], was used as an indicator of relative sensitivity in fish; this variable has previously been used for insects (Eguchi and Horikoshi, 1984) and crustaceans (Frank, 2003). The values of log K for the bluefin tuna and chub mackerel were not significantly different from each other; however, both of these log K values were significantly larger than that for the striped jack. The light intensities for K for the bluefin tuna, chub mackerel, and striped jack were 1.38, 1.86, and 0.69 lx, respectively.

The variable m, which is the slope of the V/log I curve, tended to be higher in bluefin tuna than in the chub mackerel and striped jack, and a significant difference was observed between bluefin tuna and striped jack (Table 1). The steeper slope for bluefin tuna may indicate higher sensitivity to a difference in light intensity and contrast sensitivity. The values of K and m were not obviously different between wild and cultured bluefin tuna; however, since the sample size of wild fish was very small, this result should be considered as indicative only.

The values log(0.05[I.sub.503]) and log(0.05[I.sub.max])--the indices of light sensitivity at a wavelength of 503 nm and the spectral sensitivity peak for each fish, respectively--revealed that the striped jack was more light-sensitive than either the bluefin tuna or chub mackerel. The values of relative sensitivity to the 503-nm light ([R.sub.503]) used were 0.709 in juvenile Pacific bluefin tuna, 0.773 in chub mackerel (calculated from Matsumoto et al., 2009). and 0.968 in striped jack. No obvious differences in the light sensitivities of wild and cultured juvenile Pacific bluefin tuna were detected (Table 1). However, considering the small sample size of the wild fish, further investigations in wild-caught bluefin tuna are required.

Temporal resolution

All the data obtained were well fitted to the exponential function. The correlation coefficients between the raw data and curve-fitted values were more than 0.95 (Pearson's correlation test). Figure 4 gives examples of flicker ERGs at a light intensity of 4.43 X [10.sup.11] quanta [cm.sup.-2] [s.sup.-1]. The parameters of the temporal functions are shown in Table 2. The chub mackerel exhibited significantly lower b values and higher 0.05[FA.sup.2Hz] than the other two species. The temporal resolution of chub mackerel was significantly higher than that of bluefin tuna and striped jack for any of the measured parameters at a light intensity of 4.43 X [10.sup.11] quanta [cm.sup.-2] [s.sup.-1] (0.56 lx). and was significantly higher than that of striped jack at 3.61 X [10.sup.11] quanta [cm.sup.-2] [s.sup.-1] (4.54 lx).

[FIGURE 4 OMITTED]
Table 2

Indices of temporal resolution in flicker ERG responses

                                                 Species Scomber
Index         Light intensity    Thunnus            japonicus
                 (quanta        orientalis
                [cm.sup.-2]
                [s.sup.-1]

b             4.43 X           0.184 [+ or -]  0.118 [+ or -] 0.0184
              [10.sup.11]      0.0381 (a)      (b)

0.05                           18.8 [+ or -]   28.0 [+ or -] 4.12 (b)
[FA.sub.2Hz]                   3.27 (a)

n                              5               5

b             36.1 X           0 211 [+ or -]  0.149 [+ or -] 0.0114
              [10.sup.11]      0.0637(ab)      (a)

0.05                           18.3 [+ or -]   22.0 [+ or -] 1.71 (a)
[FA.sub.2Hz]                   5.96 (ab)

n                              5               5

b             503 X            0.269.167       0.151 [+ or -] 0.0382
              [10.sup.11]

0.05                           13.1, 19.9      22.2 [+ or -] 4.67
[FA.sub.2Hz]

n                              2               5

                                               Species

Index               Light intensity       Pseudocaranx dentex
                  (quanta [cm.sup.-2]
                      [s.sup.-1]

b                 4.43 X [10.sup.11]   0.200 [+ or -] 0.0327 (a)

0.05[FA.sub.2Hz]                         17.4 [+ or -] 2.43 (a)

n                                               5

b                 364 X [10.sup.11]    0.273 [+ or -] 0.712 (b)

0.05[FA.sub.2Hz]                         13.6 [+ or -] 2.71 (b)

n                                               5

b                 503 X [10.sup.11]            0.199

0.05[FA.sub.2Hz]                              16.4

n                                               1

Values with different letters in the same row are significantly
different (P < 0.05).


Discussion

Light sensitivity

The estimated values for the parameters log K, log(0.05[I.sub.503]), and log(0.05[I.sub.max]) indicated that the light sensitivity of bluefin tuna was comparable to that of chub mackerel. The striped jack, however, was significantly more sensitive to light than both the tuna and mackerel (Table 1). The light intensity at which light adaptation takes place is higher in juvenile Pacific bluefin tuna (Masuma et al., 2001) and spotted mackerel (Kawamura, 1979) than in other fish species. Thus, scombrid fishes are less sensitive to dim light. Further investigations of many species are needed to clarify this point.

Slope m of the V/log I curve for bluefin tuna tended to be sleeper than that for chub mackerel and striped jack (Table 1). This suggests that juvenile Pacific bluefin tuna are more sensitive to changing light intensity.

Temporal resolution

Temporal resolution at a light intensity of 4.43 X [10.sup.11] quanta [cm.sup.-2] [s.sup.-1] (= 0.56 lx; Table 2) was significantly greater in chub mackerel than in either bluefin tuna or striped jack. No significant difference in temporal resolution was observed between bluefin tuna and striped jack. However, since temporal resolution tends to increase with increasing water temperature (Fritsches et al., 2005), the striped jack, which was studied at a lower water temperature, might have exhibited a greater temporal resolution than the bluefin tuna if the two had been studied at the same water temperature.

Pacific bluefin tuna exhibited a lower temporal resolution than chub mackerel, although the light sensitivity in these two species was comparable. Visual temporal resolution is analogous to the shutter lime or integration lime of a camera (Lythgoe. 1979; Warrant, 1999), indicating that there is a trade-off relationship between temporal resolution and light sensitivity. Low visual temporal resolution (motion detection) in the juvenile Pacific bluefin tuna may be advantageous for increasing light sensitivity to achieve a level comparable to that of chub mackerel.

Although CFFF is commonly used as an index of temporal resolution, it is affected by individual differences in ERG potential and background noise. Consequently, it is difficult to make comparisons among different studies with respect to this index. In an attempt to solve this problem, we defined the frequency at which the amplitude of flicker ERG becomes 5% of the amplitude at 2 Hz as an index of temporal resolution. Our results demonstrated that the exponential curve-fitting method was suitable for describing the amplitude-frequency relationship for flicker ERG in our dark-adapted fish, as has previously been demonstrated in dark-adapted rats (Sauve et al., 2006).

Spectral sensitivity

The spectral sensitivity of the eyes of dark-adapted blue-fin tuna peaked at approximately 479 nm (Fig. 2a), which is comparable to the 483 nm reported for yellowfin tuna (Loew et al., 2002). The spectral sensitivity of chub mackerel peaked at approximately 482 nm (Fig. 2b; Matsumoto et al., 2009), whereas that of striped jack peaked at approximately 512 nm (Fig. 2c). Thus, the sensitivity peak wavelengths of the scombrid fishes were shorter than that of the striped jack. This difference in spectral sensitivity may be attributable to the different habitats of these species: the bluefin tuna and chub mackerel are pelagic fishes (Collette and Nauen, 1983), whereas the striped jack is a reef-associated fish (Masuda and Tsukamoto, 1999). Generally, the spectral sensitivity of an organism is thought to be related to the light environment of its habitat and to its behavior (Kobayashi, 1962; Munz and McFarland, 1977). For example, oceanic and deep-water fishes tend to be sensitive to blue light, whereas freshwater and shallow marine fishes tend to be sensitive to green light (Munz and McFarland, 1977).

Visual function in dark-adapted Pacific bluefin tuna

It was suggested that the scombrid fishes are less sensitive to dim light, since both the tuna and mackerel were significantly less sensitive than striped jack to light (Table 1). Moreover, Pacific bluefin tuna exhibited a lower temporal resolution than chub mackerel, although the light sensitivity in these two species was comparable. Therefore, our results demonstrated that the dark-adapted visual function of Pacific bluefin tuna is inferior to that of chub mackerel and striped jack. The scotopic visual threshold of juvenile Pacific bluefin tuna for optomotor reactions was at least 40-fold inferior to the threshold of four marine teleosts: grouper (Epinephelus septemfasciatus), purplish amberjack (Seriola dumerili), ocellate puffer (Takifugu rubripes), and red sea bream (Pagrus major) (Ishibashi et al., 2009). The light intensity threshold for schooling in juvenile Pacific bluefin tuna has been demonstrated to range from 0.01 to 0.5 lx (Torisawa et al., 2007b); this is higher than in Atlantic mackerel (Scomber scombrus) (315 to 341 mm: [10.sup.-5] 1x; Glass et al., 1986) and juvenile striped jack (5 x [10.sup.-4] lx: TL = 120 mm; Miyazaki et al., 2000). The findings of these previous studies are consistent with our present results of a low temporal resolution and poor light sensitivity in this species.

Nocturnal feeding behavior has not been observed in larval (TL 2.28 to 14.6 mm; Uotani et al., 1990) and juvenile (FL 450 to 780 mm) Pacific bluefin tuna (Kitagawa et al., 2004). Sleeping behavior at the water surface has also been observed in juvenile Pacific bluefin tuna (TL around 20 to 50 mm; Ishibashi et al., 2009). Therefore, unlike typical schooling fishes such as the Atlantic mackerel (Glass et al., 1986) and striped jack (Miyazaki et al., 2000), the juvenile Pacific bluefin tuna may not need to detect motion in order to follow schooling mates, even in dim light. The juvenile bluefin tuna may be able to avoid predators by a greater swimming speed, although its ability to detect approaching predators is inferior to that of other species. The high-burst swimming speed (19.1 to 34.1 SL/s in 50 to 300 mm SL) has been reported by Miyashita (2002).

Mass death

Mass death is a characteristic phenomenon of cultured juvenile Pacific bluefin tunas after about 30 dph (TL around 50 mm). This phenomenon is associated with contact or collisions with tank or net pen walls; consequently, the fish die of trauma (Ishibashi et al., 2009). In contrast, mass death has rarely been observed in the chub mackerel, although this species belongs to the same family (Scombridae) as the tunas (Sawada, 2006).

The swimming speed of the Pacific bluefin tuna (SL 80 to 300 mm) is about 3 to 4 SL/s during normal swimming (Miyashita, 2002). In contrast, chub mackerel (SL 139 mm) swim at about 2.2 SL/s during normal swimming (Suzuki, 2006). Therefore, juvenile Pacific bluefin tuna have a higher risk of collision- or contact-induced mass death than chub mackerel.

We previously hypothesized that mass deaths are caused by contact or collisions because of low visibility under dark and dim light conditions, since artificial lighting prevents high nighttime mortality of juvenile Pacific bluefin tuna (Ishibashi et al., 2005, 2009). For juveniles of this species kept in culture systems, low visual temporal resolution is likely to inhibit perception of the net wall as they approach it. Our results therefore suggest that mass deaths can be attributed to the low temporal resolution and poor light sensitivity of juvenile Pacific bluefin tuna under dim light.

In conclusion, dark-adapted juvenile Pacific bluefin tuna exhibited low temporal resolution and light sensitivity although it had been generally believed that the visual ability of the species was higher than that of other fishes. The Pacific bluefin tuna may not need high visual function under dim light conditions in its natural habitat because it is a diurnal species. However, in artificial culture, mass deaths through contact or collisions with the net walls probably occur because of a relatively poor visual ability to perceive the nets on approach.

Acknowledgments

We thank Prof. Osamu Murata, Mr. Shinji Yamamoto, and the staffs of the Shirahama and Oshima Experiment Stations of the Fisheries Laboratory of Kinki University for providing the specimens for our study. We also thank Dr. Hiroshi Kobayashi for his advice regarding the ERG. This research was supported by the 21st Century and Global Centers of Excellence Program of the Ministry of Education, Science, Sports and Culture of Japan.

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TARO MATSUMOTO (1), HIROSHI IHARA (1), YOSHINARI ISHIDA (2), TOKIHIKO OKADA (3), MICHIO KURATA (3),YOSHIFUMI SAWADA (3),AND YASUNORI ISHIBASHI (1) *

(1) Department of Fisheries, School of Agriculture, Kinki University, Naka-machi, Nara 631-8505, Japan;

(2) Osaka School of Communication Arts, Shinmachi, Nishi-ku, Osaka 550-0013, Japan: and

(3) Ohshima Experiment Station, Fisheries Laboratory, Kinki University, 1790-4, Oshima, Kushimoto, Wakayama 649-3633, Japan

Received 28 April 2009; accepted 12 June 2009.

* To whom correspondence should be addressed. E-mail: isibasi@nara.kindai.ac.jp

Abbreviations: CFFF. critical flicker fusion frequency; dph. days post-hatching: FL, fork length: SL, standard length: TL, total length.
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Author:Matsumoto, Taro; Ihara, Hiroshi; Ishida, Yoshinari; Okada, Tokihiko; Kurata, Michio; Sawada, Yoshifu
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:9JAPA
Date:Oct 1, 2009
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