Blackwell Science, LtdOxford, UKFISFisheries Science0919 92682005 Blackwell Publishing Asia Pty Ltd713471478Original ArticleTemperature and the endogenous

rhythmWS Kim et al.

FISHERIES SCIENCE

2005; 71: 471478

Effects of temperature changes on the endogenous rhythm of oxygen consumption in the Japanese ounder Paralichthys olivaceus
Wan Soo KIM,1* Seong-Jin YOON,1 Jong Man KIM,1 Joon Woo GIL2 AND Tae Won LEE3
Marine Living Resources Research Division, Korea Ocean Research and Development Institute, Seoul 425-600, 2Korea Electric Power Research Institute, Yusung-Ku, Taejon 305-380, and 3Department of Oceanography, Chungnam National University, Taejon 305-764, Korea
1

ABSTRACT: The effects of temperature changes on the endogenous rhythm of oxygen consumption in the Japanese ounder Paralichthys olivaceus which were acclimated to 3, 14 or 20C in advance were investigated. The oxygen consumption rate (OCR) of individuals (total length >28 cm) that were acclimated to 3C, maintained a relatively low value of 6.9 2.3 mL (mean SD) O2/kg ww (wet weight)/h till 5.8C, which is considered a minimum rate. Thereafter, the OCR gradually increased up to 18.7 mL O2/kg ww/h at the temperature of 10.6C. The OCR of individuals acclimated to 14C stabilized with 124.2 24.1 mL O2/kg ww/h, when tested at the relatively constant temperature of 14.4 0.17C. Maximum entropy spectral analysis revealed that the peak OCR occurred at 23.9 h intervals, which could be a circadian rhythm. The mean OCR showed a peak at 06.0008.00 hours. For the temperature above 25C in which the sh were acclimated to 20C, the rhythmic patterns of OCR were observed until the experimental temperature reached 26.4C. For the temperature above 28.4C, the metabolic activity rhythm of the OCR was dampened and then the OCR abruptly rose again. It is assumed that the oscillator of the endogenous rhythm lost the governing of normal metabolic activity in Japanese ounders above 28.4C. These results suggest that the temperatures of around 5.8, 26.4 and 28.4C are the lower limit temperature, upper incipient lethal temperature, and the critical thermal maximum, respectively, for the endogenous rhythm of oxygen consumption in the Japanese ounder. KEY WORDS: endogenous rhythm, Japanese ounder, oxygen consumption, Paralichthys olivaceus, temperature.

INTRODUCTION Olive or Japanese ounder Paralichthys olivaceus is widely distributed in the north-western Pacic coastal waters from Kuril Islands, Japan, Korea to the South China Sea.1,2 Many studies have been conducted on its biology and ecology because of its commercial importance in sheries and aquaculture in East Asian countries. In aquaculture practices, the feeding temperature of Japanese ounder has been known to range from 8 to 25C.3,4 The feeding rate of this species has been revealed to decrease abruptly when the temperature drops below 10C and reaches above 25C,4 and its opti-

*Corresponding author: Tel: 82-31-400-6204. Email: waskim@kordi.re.kr Received 20 April 2004. Accepted 11 November 2004.

mal temperature for growth has been reported to be between 15 and 25C.47 These reported data were principally determined by observation of sh behavior. A few studies have been done on the metabolic activity rhythms and thermal limits of this sh. Liu et al.8 reported that the Japanese ounder exhibited a diel rhythm in the oxygen consumption rate (OCR), but their experiments were conducted within a relatively short period of time. To substantiate the thermal limits of the OCR in the Japanese ounder, it is necessary to observe activity rhythms across a wide range of temperatures for a long period of time, which could bring information useful for shery and aquaculture of this species. The use of an automatic intermittentow-respirometer (AIFR) made it possible to observe the metabolic activity rhythm for a longer time (>30 days) and with greater reliability than the

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short-term measurements of respiration using closed systems.9 The development of laboratory techniques for long-term measurement of metabolic response has made it possible to determine the effects of environmental factors, such as temperature and salinity, on the endogenous rhythm of marine animals.1012 However, few data are available on the relationship between thermal limits and metabolic activity rhythms in shes. When sh are exposed to low/high temperature extremes within lethal limits, their metabolic activities decrease/increase as per a typical response in poikilothermic animals. These thermal changes have been reported to bring shifts in locomotive activity,1 swimming speed,13 osmotic balance,14 growth rate,15,16 as well as the OCR.17 The upper boundary of the thermal resistance for survival, which has been often called critical thermal maximum (CTM) is determined by exposing sh to increasing water temperatures at a dened rate until they lose equilibrium, and has been known to be a key factor in the distribution and growth of shes.18,19 For example, the CTM ranges have been demonstrated to range from 39.5 to 44.5C for seven estuarine shes,20 and from 26 to 39C for 14 species of marine sh.21 Although the effects of temperature changes on the OCR of sh, irrespective of whether they are with or without thermal acclimation in advance are well documented15,2226 and endogenous rhythms of the OCR in marine organisms have been studied extensively,27,28 information on the thermal limits of the endogenous rhythm of the OCR is very limited. Because the Japanese ounder is one of the most important sh species cultured in north-east Asia,29 the determination of its thermal limits could be of practical importance in wintering and summering sh in aquaculture. The purpose of this study was to determine the thermal limits of the endogenous rhythm of the OCR in Japanese ounder, P . olivaceus, exposed to a wide range of temperatures and to offer informa-

tion inevitably necessary for reliable production of this sh. MATERIALS AND METHODS A total of 18 adult Japanese ounders were used in this study. They were 31.9 1.9 cm (mean SD) in total length and 354.7 88.8 g in wet weight (ww). They were kept together in a circular indoor tank (2000 L) for 2 weeks in which well-aerated fresh seawater was continuously supplied. They were then transferred into three smaller tanks (500 L) of three different temperatures for acclimation (at 3, 14 and 20C) in laboratory conditions (indoor, 12 hour light/dark cycle). At each temperature, ve, eight and ve individuals, respectively, were kept for an additional 2 weeks prior to the beginning of experiments as the initial temperature has been known to inuence the OCR of the sh.30 Fish were fed with a commercial pellet once a day throughout the acclimation periods except for 48 h prior to and during the experiment to ensure a postabsorptive digestive state before their introduction into a test chamber.31 Test sh were held in water at the salinity of 30.333.9 psu. Their OCR were then measured as the temperature increased from these initial acclimation temperatures: to 10.6C in 3C acclimated sh and 29.4C in 20C acclimated sh with the rate of 0.050.15C/h, whereas 14C acclimated sh were kept at almost the same temperature of 14C continuously. The OCR of a pair of individuals were monitored simultaneously by placing a sh in each Plexiglas incubator chamber in a semicirculatory system (Table 1). At the end of the measurement, individuals were isolated from the chambers and weighed. The OCR was measured over 18220 h by the AIFR following the procedures described by Kim et al.9,11,12 The limitations imposed by earlier procedures were alleviated by new techniques which allowed non-invasive monitoring of certain rate processes in selected animals using computer-

Table 1 Experimental conditions for different experiments on adult Japanese ounder Paralichthys olivaceus under various temperature ranges Temperature acclimated Mean total length of sh (cm) Mean wet weight of sh (g) Number of points measured Salinity (psu) Levels of oxygen saturation (%) Duration (h) of the experiment Number of experiments (n) Total number of sh (Tn) 3C 32.8 3.1 393 21.4 18932974 31.333.0 85.694.5 92120 5 5 14C 33.4 2.3 448 37.9 23863942 31.533.3 85.494.5 120288 8 8 20C 34.3 1.3 415 10.8 21563530 31.533.7 85.794.8 144220 5 5

Length and weight are expressed as mean standard deviation.

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aided data acquisition and storage systems. Experimental water was ltered free of bacteria through sterile membrane lters (two Sartorius capsule lters, Sartobran PH, Sartorius, Gttingen, Germany; input 0.2 mm and output 0.07 mm). The probe voltage for polarization was observed for a 20-min period in order to ascertain whether it had deviated from the gauge voltage in the beginning of the experiment. Oxygen levels in the Plexiglas experimental chamber (diameter, 38 cm; height, 8 cm; volume, 9.6 L) were maintained by changing the water between 80% (lowest) and 95% (highest) saturation to avoid any physiological stress caused by hypoxic condition. When the oxygen level dropped below the predetermined limit, a magnetic drive gear pump and three-way actuator valve (TX 3501 DA-1/2, Ilyoung, Seoul, Korea) supplied the system with saturated seawater until the selected oxygen level (95% saturation) was reached. No measurements were made while refreshing the chamber water with oxygen-saturated water from a storage tank (20 L) to restore the oxygen saturation level to 95%. After each experiment, the chamber was rinsed with oxygen-saturated water and the probe voltage was examined to ascertain whether it had deviated from the gauge voltage at the beginning of the experiment. The oxygen probe (M-100, Eschweiler, Kiel, Germany) was calibrated before each experiment, and if the water temperature or air pressure were increased or decreased in real time, then determination of the OCR was automatically recalculated every second by computer program. The total water volume of the respirometer system was c. 30 L. The magnetic drive gear pump (MS-Z, Ismatec Sa, Switzerland) produced horizontal water ow rates of 1400 mL/min. Measurements were conducted in a constantly dark BOD incubator (VS1203P5 N, Vison Co., Seoul, Korea), which got the experimental sh to avoid any visual contact with other sh and not to suffer from any disturbances. The water temperature was controlled with a temperature-control (thermostat) system which is internally built in the BOD incubator. Using a custom software, actual oxygen levels were monitored by a digital controlling unit through a picoammeter. Mean oxygen consumption rates (mOCR) of the test animals were calculated at 90-s intervals, and all data were graphically displayed in real time. Data readings, including local and experimental time, temperature (C), air pressure (hPa), oxygen consumption rate (mL O2/ h), and oxygen levels (%) in the ambient water, were stored directly onto a hard disk for future analysis. The OCR was calculated from changes in the oxygen saturation level in the test chamber over time. The oxygen saturation concentration KO2 (mL/L) was calculated for standard conditions

(atmospheric pressure Patm = 1 atm = 1013 hPa) as a function of temperature and salinity using the formula of Weiss32 as follows: ln KO2 = A1 + A2(100/T) + A3ln(T/100) + A4(T/100) + S([B1 + B2(T/100) + B3(T/100)2]) where, T is temperature (K), S is salinity (psu) at the time of the measurement, and A and B are the following constants: A1 = -173.4292; A2 = 249.6339; A3 = 143.3483; A4 = -21.8492; B1 = -0.033096; B2 = 0.014259; B3 = -0.0017000. To obtain concentration in mg/L, we used the following conversion of gas volume under standard conditions (Vstd) into gas volume under measured conditions (VR): VR = VStd(1013 hPa/Patm)(T/273.15 K) where, T (K) and Patm (hPa) were taken at the time of measurement.15 Following this, KO2 (mg/L) was calculated as follows:33 KO2(mg/L) = KO2(mL/L) 1.429 More detailed descriptions of AIFR, including the location of the probe and a schematic of the apparatus, are provided by Kim et al. and Yoon et al.9,3436 The OCR was analyzed using the weighted smooth curve procedure at 2% individual error. To plot a best-t smooth curve through the center of the data, we used the locally weighted least squares error method (KaleidaGraphy custom program for Macintosh, Synergy Software, Essex Junction, VT, USA). The values of 2% and 5% individual error obtained from the repeated tests yielded the bestt curve. Statistical values were computed for each batch from the data points measured (Table 1). Signicant differences of mean values were examined by Students t-test. Maximum entropy spectral analysis (MESA) was used to estimate the dominant periodicity peaks in the oxygen consumption time series.37 The effects of a change in temperature on the OCR are expressed as rate/temperature or RT curves (Q10) approximation38 which is the factor showing the velocity of a rate process in increased metabolism for a rise in temperature of 10C. RESULTS The mOCR of a ounder acclimated to 3C being exposed to low temperatures of 3.410.6C, with an increasing temperature rate of 0.1C/h for 69 h, are shown in Fig. 1. The ounder maintained a low uptake of oxygen with a mOCR of 6.9 2.3 mL O2/ kg ww/h without showing the rhythmicity of the OCR until the temperature reached 5.8C (Fig. 1 A). The sh appeared to resume a normal metabolic rhythm at 5.8C or higher (Fig. 1 X). The

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Fig. 1 Time series of oxygen consumption by a single fasted Japanese ounder Paralichthys olivaceus (33.7 cm, 390 g wet weight) acclimated to 3C in advance during a gradual temperature increase from 3.4 to 10.6C over 69 h. The sh was kept in water at 80.394.9% oxygen saturation levels (solid line). The arrow X at 5.8C indicates the lower limit temperature for maintaining the endogenous rhythm. Curves of mean oxygen consumption rate and temperature (dotted line) are tted to a weighted smooth curve of 5%. A and B represent different patterns displayed by the Japanese ounder during the experiments, that is, constant pattern and rhythmicity pattern, respectively. A single dot represents the mean oxygen consumption rate at 90-s intervals.

mOCR increased markedly (P < 0.01) from 6.9 2.3 to 18.7 4.5 mL O2/kg ww/h with the temperature increase from 5.8 to 10.6C (Fig. 1 B). The other four replicate experiments with varying duration (92120 h) yielded results similar to that presented in Fig. 1 (data not shown). The mOCR of a sh acclimated to 14C was stabilized at 124.2 24.1 mL O2/kg ww/h when tested at a medium temperature of 14.4 0.17C in constant darkness for 164 h (Fig. 2a). Seven replicate experiments revealed similar trends (data not shown). The mOCR ranged from 44 to 207 mL O2/kg ww/h. Seven cycles assuming a circadian rhythm were observed during the 164 h (6.8 days) period. The OCR peaked in the early morning (06.0008.00 hours), corresponding to 1 or 2 h after sunrise (Fig. 2b) and lowered during the day in all experiments. MESA spectra analysis indicated that OCR peaked at 23.9-h intervals (Fig. 3) and was independent of the uctuating oxygen levels ranging from 85.7 to 94.9% of saturation. Figure 4 showed the mOCR of a sh acclimated to 20C in the course of the temperature increase experiment. Similar trends were observed in another four replicates (data not shown). The sh showed a relatively constant OCR (96.7 mL O2/kg ww/h) with a circadian rhythmicity until the temperature reached 25.0C (Fig. 4 A). The OCR of ounder increased continuously with temperature increases above 25.0C (Fig. 4 X1). The rhythmic patterns of the OCR were observed until the experimental temperature reached 26.4C (Fig. 4 X2). The OCR above 26.4C, however, was slightly

dampened and then abruptly rose disturbing the rhythmicity (Fig. 4 B). The mOCR at 28.4C rose approximately 1.5-fold over that at 25.0C. For the temperature above 28.4C, the OCR abruptly rose again (Fig. 4 Y). DISCUSSION Adult ounders acclimated to 3C exhibited a constant low oxygen uptake of <10 mL O2/kg ww/h when exposed to temperatures below 5.8C, and the sh held above 5.8C exhibited increased oxygen uptake rates showing rhythmicity in the OCR. Therefore, the temperature of c. 5.8C could be referred to as the lower limit temperature (LLT) for the rhythmicity of the OCR in the Japanese ounder. Under the LLT the sh are inactive and failed to learn to swim, and appeared to lose some metabolic regulatory ability.39,40 At temperatures over 5.8C, the OCR increased with the increasing temperature and showed a circadian rhythm up to 10.6C. The mean OCR of individuals acclimated to 14C was stabilized c. 124 mL O2/kg ww/h showing a circadian rhythm at the constant temperature of 14C, whereas c. 97 mL O2/kg ww/h at the temperature from 20 to 25C in sh acclimated at 20C. The mOCR between 14C and 2025C did not differ signicantly (P > 0.05). Similar mOCR have been reported for the Japanese ounder by Liu et al.8 and Kubosho,4 and those of other sh species including at sh have been also documented in detail by Kubosho.4

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Fig. 2 (a) Patterns of the oxygen consumption rate by a single fasted Japanese ounder Paralichthys olivaceus (30.7 cm, 370 g wet weight) acclimated to 14C in advance during the period of 160 h held at 14.4 0.07C (mean SD) for 160 h. (b) Enlargement of a region of the upper panel was drawn for 1618 January 2002.

Fig. 3 Maximum entropy spectral analysis (MESA) spectra for data presented in Fig. 2. The period length (h) corresponding to the dominant peaks in the MESA plots is given in parentheses.

Between the acclimation temperatures of 3 and 14C, the OCR increases with a Q10 of 13.8, which is exceptionally high, especially when compared to the direct temperature effects during short period exposure between 3.4 and 10.6C (Q10 = 4). This is probably because the OCR for the Japanese ounder acclimated to 3C was abnormally restricted to the minimum at the water temperature of 5.8C or

lower comparing the normal OCR shown at 14C. In contrast, a relatively higher value of Q10 = 4 than a normal, physiological range (e.q. 23)38 may reect that the metabolic recovery rate increase more rapidly than the rate of increases in water temperature. Therefore, the results from this study suggest that it is difcult to compare metabolic activity data obtained through a certain period under the experimental condition of increasing water temperature with those obtained under the experimental condition of a steady state. The OCR of ounders increased continuously as the temperature increased beyond 25.0C. However, the rhythmic pattern of the OCR was only maintained below 26.4C. These facts suggest that the Japanese ounders were stressed at the temperature above 26.4C. We then considered that the temperature of 26.4C could be called the upper incipient lethal temperature (UILT). Above 26.4C, the rhythmic pattern was disturbed and the OCR abruptly increased until 28.4C. In addition, Japanese ounders could no longer maintain their endogenous rhythm above 28.4C. This suggests that the oscillator lost the governing of normal metabolic activity in Japanese ounders at this temperature. Thus, we dened this temperature as

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Fig. 4 Patterns of the oxygen consumption rate by a single fasted Japanese ounder Paralichthys olivaceus (35.4 cm, 415 g wet weight) acclimated to 20C in advance during a temperature increase from 20.4 to 29.5C (1C/24 h) over 220 h. X1 (25.0C), X2 (26.4C) and Y (28.4C) indicate the optimal, the upper incipient lethal temperature and the critical thermal maximum, respectively, for maintaining the endogenous rhythm of oxygen consumption.

critical thermal maximum (CTM). Because the CTM has been dened so far to be an upper border temperature causing muscle spasms or loss of equilibrium,41 the temperature obtained as the CTM in the present study for Japanese ounder could not be always identical to that based on the previous denition. However, there have been no studies determining the CTM through the longterm monitoring of the OCR, and the CTM through the physiological bases was rst demonstrated in the present study. The UILT and the CTM of the sh estimated from our laboratory experiments may differ from the actual values due to variation in the response of test sh to experimental conditions. Many earlier studies did not provide individual data points,30 probably because of difculties in plotting the range of values obtained in respiratory experiments. Therefore, it is difcult to compare results obtained in these early studies15,17,18 with those detailed in this study. Also, many earlier studies used a group of sh, and this could result in different tolerance limits. Fish in large schools may feel less stressed as a result of visual contact with conspecics, which may reduce their OCR. In contrast, an isolated sh, as in our study, or sh in a small group, may be more stressed and, therefore, may exhibit a higher rate of the OCR.42 The tolerance limits may also be dependent upon age, as it is well known that juveniles can survive at higher temperatures than older sh.43 Our test sh were not fed during the experiment, and our estimated CTM could be slightly underestimated compared to normally feeding sh. The CTM may also be affected by body size44 and

physiological conditions45 of the test organisms. Woiwode and Adelman45 reported that the CTM of starved hybrid bass (Morone saxatilis x M. chrysops) averaged 0.35C lower than that of satiated hybrid bass. In addition, environmental conditions of habitat also appear to affect the level of the CTM.19,20 The CTM range from 39.5 to 44.5C in estuarine shes,19 is higher than those of marine shes (2639C).20 Lee and Rinne conrmed a signicant linear relationship between the CTM and acclimation temperature in each individual species.17 The CTM may vary due to the initial acclimation temperatures25 and the rate of temperature increase as well, as similarly discussed above on difference of Q10 values. If the initial acclimation temperature is low and the experiment is made over a wide range of temperatures, the CTM is underestimated at the high temperature.30 Cox also found different CTM values in bluegill (Lepomis macrochirus) when sh of various sizes were subjected to different rates of temperature increase (0.1, 0.5 and 1.0C/min), and observed signicantly lower CTM values at the slower heating rate (0.1C/min) than at the faster heating rate (0.5 and 1.0C/min).30 To minimize the effect of the mentioned experimental variables, the ounders in our experiments were acclimated to three different temperatures and exposed to a slower rate of temperature increase (1C/24 h increase from 20.4 to 29.5C). In conclusion, it was claried through the present study that the temperatures of around 5.8, 26.4 and 28.4C are the lower limit temperature, upper incipient lethal temperature, and the criti-

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cal thermal maximum, respectively, for the endogenous rhythm of oxygen consumption in Japanese ounder.

14.

ACKNOWLEDGMENTS The authors wish to thank Mr T. Stewart for helpful comments on an earlier draft of this manuscript. This study was supported in part by the Ministry of Science and Technology Korea under a project of the National Research Laboratory (2000-N-NL-01C-16) and Marine Ranching Program of Korea.

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