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Self-feeding behavior of yellowtail, Seriola quinqueradiata, in net cages: diel and seasonal patterns and influences of environmental factors
Aquaculture 220 (2003) 581 – 594 www.elsevier.com/locate/aqua-online
Self-feeding behavior of yellowtail, Seriola quinqueradiata, in net cages: diel and seasonal patterns and influences of environmental factors J. Kohbara a,*, I. Hidaka a, F. Matsuoka a, T. Osada a, K. Furukawa b, M. Yamashita a, M. Tabata c a b
Laboratory of Fish Physiology, Faculty of Bioresources, Mie University, Kamihama, Tsu, Mie 514-8507, Japan Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo 113-8657, Japan c Department of Animal Sciences, Teikyo University of Science and Technology, Uenohara, Yamanashi 409-0193, Japan Received 27 June 2002; received in revised form 1 October 2002; accepted 18 November 2002
Abstract The self-feeding pattern of yellowtail, Seriola quinqueradiata, maintained in floating net cages was examined throughout a year, and the influence of seasonal changes of the photoperiod and water temperature on the feeding pattern was investigated. Two groups of 50 yellowtail (initial mean body weight about 50 and 80 g, respectively) were kept in two experimental net cages (2 3 4 m deep), with a self-feeding device installed on each. It was possible to maintain yellowtail in net cages using a self-feeder throughout almost a year. The number of daily food demands was greatly affected by the seasonal changes in water temperature. Yellowtail showed high self-feeding activity, above 18 jC; depressing water temperatures did not influence the activity when the water temperature was over 18 jC. However, the activity decreased when the water temperature fell below 18 jC. The feeding pattern in a 24-h period was greatly affected by the temporal changes in light intensity. Annual observations revealed that yellowtail showed generally crepuscular plus nocturnal feeding behavior and had two peaks of feeding activity a day. These peaks appeared at dawn and dusk; moreover, a clear association between the most active time of self-feeding and the period of the greatest change in light intensity was observed. The results suggest that a change in light intensity might stimulate the appetite of yellowtail or that there is a light level at which yellowtail prefer to eat. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Light intensity; Net cage; Self-feeding; Seriola quinqueradiata; Water temperature; Yellowtail
* Corresponding author. Tel: +81-59-231-9534; fax: +81-59-231-9523. E-mail address: [email protected] (J. Kohbara). 0044-8486/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0044-8486(02)00642-7
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1. Introduction A self-feeding technique that enables fish to feed on demand has been used in many studies of fish feeding behavior. It has been used, for example, to study the learning ability (Adron et al., 1973; Takahashi et al., 1981a,b, 1984), the diel feeding-pattern (Rozin and Mayer, 1961; Landless, 1976; Boujard and Leatherland, 1992; Sa´nchezVa´zquez et al., 1994), the circadian rhythms of self-feeding (Sa´nchez-Va´zquez et al., 1995, 1996; Sa´nchez-Va´zquez and Tabata, 1998), the regulation of food intake (Boujard and Leatherland, 1992; Alana¨ra¨, 1992a, 1994; Bra¨nna¨s and Alana¨ra¨, 1994), the food preferences (Adron et al., 1973), the nutrient selection for diet design (Sa´nchez-Va´zquez et al., 1998b, 1999; Yamamoto et al., 2000) and the social interaction between individuals (Bra¨nna¨s and Alana¨ra¨, 1993, 1994). The results obtained from these investigations revealed that the technique of self-feeding can be used to investigate a wide variety of research fields relating to fish feeding. In addition, as an aquaculture technique, self-feeding drastically reduces food waste and lowers the environmental impact (Alana¨ra¨, 1992b, 1996; Madrid et al., 1997) because it adjusts the food supply to the appetite of the fish. Research applying self-feeding to aquaculture has been carried out using species of commercial value, such as rainbow trout, Oncorhynchus mykiss (Adron et al., 1973; Landless, 1976; Kindschi, 1984; Tipping et al., 1986; Alana¨ra¨, 1992a,b, 1994, 1996; Boujard and Leatherland, 1992; Bra¨nna¨s and Alana¨ra¨, 1994; Sa´nchez-Va´zquez and Tabata, 1998; Sa´nchez-Va´zquez et al., 1999; Yamamoto et al., 2000), Arctic charr, Salvelinus alpinus (Bra¨nna¨s and Alana¨ra¨, 1993, 1994), lake trout, Salvelinus namaycush (Aloisi, 1994), European sea bass, Dicentrarchus labrax (Sa´nchez-Va´zquez et al., 1994, 1995, 1998a; Boujard et al., 1996; Madrid et al., 1997) and yellowtail, Seriola quinqueradiata (Kohbara et al., 2000, 2001), and the feeding rhythms, growth performances and the rate of feed wastage under the self-feeding condition have been investigated. These practical studies also revealed that the self-feeding pattern of fish could be changeable according to the differences in rearing conditions, even in the same species. For example, rainbow trout showed a feeding peak at dusk and also a high level of nocturnal feeding activity under field conditions on one hand (Landless, 1976) and a clear diurnal pattern synchronizing the given L/D cycle under experimental room conditions on the other (Boujard and Leatherland, 1992). Similarly, European sea bass showed a dualistic feeding behavior, nocturnal and diurnal feeding patterns under the controlled experimental conditions (Sa´nchez-Va´zquez et al., 1995) and a seasonal phase inversion of the diel feeding pattern under field conditions (Sa´nchez-Va´zquez et al., 1998a). We have been studying the self-feeding behavior of the yellowtail, which is one of the most important commercial fish in the aquaculture industry of Japan, and we found that the inversion of the diel feeding pattern also occurred in this species. Specifically, yellowtail in indoor tanks showed a clear diurnal feeding pattern synchronizing to the given photoperiod, whereas those in the outdoor tanks showed a clear nocturnal feeding pattern also synchronizing to the outdoor natural photoperiod (Kohbara et al., 2000). Thus, the findings about changes in feeding pattern mentioned above suggest that exogenous and endogenous factors may influence a pattern of selffeeding behavior (Madrid et al., 2001).
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Most investigations to date have used small tanks up to 500 l, while little is known about self-feeding behavior of fish reared in floating net cages. Therefore, it was considered important to describe the feeding patterns of fish in net cages. The aim of the present experiment was to study the self-feeding pattern of yellowtail maintained in floating net cages throughout a year and to examine the influences of seasonal changes of natural photoperiod and water temperature on these patterns.
2. Materials and methods 2.1. Animals and experimental conditions The experiments were performed from July 1999 to July 2000 at the Fisheries Research Laboratory of Mie University at Wagu (34j16V20WN, 136j48V27WE), Mie Prefecture, Japan. The experimental animals were wild, juvenile yellowtail caught by local fishermen. After being kept in a floating net cage set off from the shore for about a month, they were anesthetized with ethyl m-aminobenzoate methanesulfonate (MS-222, Sigma, St. Louis, MO, USA) for weighing. Individuals whose body weight was approximately 50 g were chosen. Two experimental net cages (2 3 4 m deep), designated as Cage A and Cage B, were established, and the selected yellowtail were then divided into two groups with 50 fish in each net cage. However, for unknown reasons, the fish in Cage B did not actuate the feeder for 2 weeks, so 50 new fish whose body weight was approximately 80 g were selected from a reserve group and were established as a new group in Cage B. Therefore, the mean initial body weights in Cage A and Cage B were 55.1 and 88.5 g, respectively. The experiment was divided into five periods: Period I, from 27 July 1999 in Cage A and 10 August in Cage B to 6 October; Period II, from 7 October to 25 November; Period III, from 26 November to 18 February 2000; Period IV, from 19 February to 2 May; Period V, from 3 May to 12 July. Before and after each experimental period, all fish were removed from their cage, anesthetized and individually weighed to establish an accurate reward level for a certain size of fish. During each experimental period, fish were fed with a recommended size of commercial diet for yellowtail (Hamachi EP Special Nos. 4, 6 and 8, Marubeni Shiryo, Tokyo, Japan) according to the size of the fish. 2.2. Self-feeding device and data acquisition A Touch Feed 990 system (Sterner Products, Leksand, Sweden) was used as the selffeeding apparatus. This system consisted of a trigger, a control unit and a feeder and was useable for larger-scale experiments (Alana¨ra¨, 1992a, 1996). A set consisting of a trigger and a feeder was placed at the center of each net cage. The trigger was stored in a PVC pipe and the feeder was set in a large plastic box with the bottom removed to avoid damage by the salt air or seawater. The trigger was a stainless steel wire type (Sterner Sensor Type 3), and a nylon string that ended in a small plastic ball was attached to the end of the wire. The small plastic ball was located about 10 cm below the surface of the
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seawater. The control unit and the battery were stored in a plastic box and placed on a Styrofoam float of the net cages. The feeder and the control unit were adjusted to deliver a set quantity of pellets when the trigger was actuated by a fish pulling the plastic ball in its mouth. The amount of feed dispensed was calculated every few days from the weight of the feed added and of that remaining in the feeder. The daily food demand was obtained from the number of daily feeder actuations and the actual reward of the day. The time of actuations was stored in a portable data logger (HOBO Event, Onset Computer, MA, USA) and downloaded to a computer. Raw data was summarized as the number of feeder actuations in 10-min segments and translated to a format suitable for the data analysis programs built by Oshima and Ebihara (1987) to draw actograms or periodograms. 2.3. Reward level The reward level, the number of pellets delivered per trigger actuation, was established by dividing 50, the recommended daily amount of feed at a certain temperature for a certain size of fish, by 50. Namely, if the 50 fish actuate a feeder 50 times per day, they obtain the recommended amount of feed indicated in the feeding table provided by the feed manufacturer. 2.4. Environmental factors Light intensity at 1 m depth in the net cage was recorded every 10 min using a data logger (StowAway SLA, Onset Computer). The water temperatures at depth of 0.5 and 4 m were recorded every hour using data loggers (Optic StowAway Temp, Onset Computer) over a 1-year period.
3. Results 3.1. Changes of daily feeding activity The daily food demand (daily food supply) of yellowtail in Cage A and Cage B throughout the experimental periods is shown in Fig. 1. In Cage A, the daily food demand immediately after the beginning of the experiment was about 100 g/day, gradually increasing by November. Feeder actuations were observed almost everyday. The daily food demand became highest, about 1000 g/day, in early November. Afterwards, it gradually decreased until late January, and days without baiting activity were observed frequently from late November through late April. The daily food demand remained at the same low level of around 100 –300 g/day from mid-January through late April. However, days in which the daily feed supply was close to 500 g/day occurred occasionally from late February. In early May, the daily food demand rapidly increased, and it kept increasing until July 12, the end of the experiment. The degree of increment of the daily food demand was remarkable. The changes of daily food demand in Cage B tended to be almost identical to that observed in Cage A (Fig. 1).
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Fig. 1. Changes of the number of daily food demands in Cage A (upper) and Cage B (lower) throughout a 1-year experimental period. The changes of the water temperature (daily average) at the depths of 0.5 m (solid line) and 4 m (dotted line) are superimposed upon each graph.
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3.2. Changes of water temperature The changes in water temperature at 0.5 and 4 m depth of the net cages during the experimental period were superimposed upon both figures of the daily food demand in Cage A and Cage B (Fig. 1). From the beginning of the experiment to late August, the water temperatures both at the surface and at the depth of 4 m increased, and the observed maximum temperature was 29.8 and 29.1jC, respectively. From early September, the water temperature at both observation depths kept falling gradually until mid-December. The water temperature at the surface tended to be higher than that at 4 m depth; however, no difference was observed between them in late September. The water temperature from midDecember to mid-April remained at the same low level of around 13 –14 jC. The lowest was recorded on 25 February, when it was 12.6 jC at the surface and 12.7 jC at 4 m depth. In early March, the water temperature began rising gradually and the water temperature at the surface remained higher than that at 4 m depth from April. It rose rapidly to 18 jC or higher with increasing differences in water temperature between the two depths in late
Fig. 2. An actogram of self-feeding from yellowtail in Cage A (a) and Cage B (b) throughout almost a 1-year observation. Yellowtail in both cages showed a clear crepuscular and nocturnal feeding pattern synchronizing to the natural photoperiod. The data are double plotted (48-h time scale).
J. Kohbara et al. / Aquaculture 220 (2003) 581–594 Fig. 3. Monthly changes of the daily waveform of self-feeding activity in Cage A. The vertical lines in each waveform indicate the average of the daily feeder actuations in 10-min segments. The daily profiles of the photoperiod in each month is indicated the upper part of each waveform. 587
588 J. Kohbara et al. / Aquaculture 220 (2003) 581–594 Fig. 4. Monthly changes of the daily waveform of self-feeding activity in Cage B. The vertical lines in each waveform indicate the average of the daily feeder actuations in 10-min segments. The daily profiles of the photoperiod in each month is indicated the upper part of each waveform.
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April. At the end of the experiment, the water temperatures at the surface and at the depth of 4 m were 27.0 and 25.6 jC, respectively. 3.3. Self-feeding activity The actograms (double-plotted procedure, 48-h time scale) over the year, obtained from Cage A and Cage B, are shown in Fig. 2. The patterns observed in the actograms of Cage A and Cage B are almost identical. The nocturnal feeding activity commenced, seen after the experiments started to around 20 August 1999. The feeding activity showed a tendency to be concentrated particularly at the period of dawn and dusk with less frequent activities both in the daytime and nighttime. From 20 September to late November, the feeding activity during the daytime became much less frequent, being restricted to the nighttime. From late November, the nocturnal feeding continued, but the frequency declined to a level where feeding activity did not occur during the day. From mid-January, the feeding activity was restricted to dusk. From early March, the nighttime feeding activity appeared again, but its frequency was low. Subsequently, the feeding activity increased and was distributed throughout the nighttime by late May. From June through mid-July, the feeding activity occurred particularly at dawn and dusk again. Feeding activity during the daytime was also observed in mid-July. Monthly changes of the daily waveform of self-feeding activity obtained from Cage A and Cage B are shown in Figs. 3 and 4, respectively. The lower waveforms in each figure indicate the average number of daily feeder actuations in 10-min segments. The daily profile of the photoperiod in each month is indicated in the upper part of each waveform. The patterns of daily feeder actuations observed in Cage A and Cage B show a similar tendency. When the experiment started in August, self-feeding of low frequency was unevenly distributed throughout the nighttime. Activity was also observed during the daytime, but its frequency was low. In September, two steep peaks of feeding activity per day were observed, and one of them coincided with the rapid increase of light intensity at dawn and the other with its rapid decrease at dusk. Feeding activity during the daytime and nighttime occurred, but its frequency was low. Similar waveforms possessing two steep peaks at dawn and dusk were also evident from October to December. However, the total number of feeder actuations decreased from January. Low feeding activity during the nighttime with a small peak at dusk was observed, and this situation continued until April. However, the total number of feeder actuations gradually increased, and two steep peaks at dawn and dusk appeared again from May through July. The total number of feeder actuations increased in July, and the feeding activity during the daytime occurred frequently in addition to two peaks of feeding activity at dawn and dusk.
4. Discussion The present study revealed that it is possible to cultivate yellowtail in net cages throughout the year using self-feeders. Moreover, it demonstrated that environmental factors, such as water temperature and light intensity, have a great influence on the self-
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feeding behavior of yellowtail. Namely, the seasonal changes of water temperature influenced the number of daily food demands, and the temporal changes in light intensity greatly influenced the feeding pattern in a 24-h period. In the relationship between the changes of water temperature and the number of daily food demands, the daily food demand increased day by day from September to November in spite of the decreasing water temperature. Thus, a rise or fall in water temperature is not always consistent with an increase or decrease in the daily food demand of yellowtail. In many fish species, such as brown trout, Salmo trutta (Brown, 1946), sockeye salmon, Oncorhynchus nerka (Brett and Higges, 1970), goldfish, Carassius auratus (Rozin and Mayer, 1961) and bluegill, Lepomis macrochirus (Lagler et al., 1977), the food intake is closely adjusted to changes in water temperature, whereas yellowtail is recognized to be a fish species that can increase daily food intake in spite of decreasing water temperature. The food intake of yellowtail is apparently regulated on an annual basis, somewhat independent of water temperature changes, especially when the water temperature is above 18 jC. Yellowtail show a particular high growth rate in their juvenile stage, and this might encourage them to eat as much as they can. Therefore, the influence of water temperature on the food intake may be different for 2-year-old and older yellowtail. Similarly, food intake was independent of water temperature changes in pike, Esox lucius (Johnson, 1966). Contrary to the phenomena described above, low water temperature, less than 18 jC, had a great influence on the food demand of yellowtail. When the water temperature fell to less than 18 jC in November, a decrease of food demand occurred simultaneously, and when it rose to more than 18 jC in May the following year, a marked increase of food demand occurred simultaneously. This suggests the existence of a marginal temperature at which yellowtail can maintain high feeding activity, and it must be around 18 jC. Minamisawa and Sakai (1969) mentioned the relationship between water temperature and the feeding activity in yellowtail in culture conditions. They observed that at less than 11 jC, no feeding activity occurred; at 13– 17 jC, feeding activity was observed but its frequency was low; 18– 27 jC was a suitable temperature range for feeding; 24 – 26 jC was the best temperature range for feeding; and above 28 jC, feeding activity decreased due to too high water temperature for yellowtail. Interestingly, the present self-feeding experiments showed clearly that the daily food demand rapidly decreased when the water temperature fell below 18 jC and rapidly increased when it rose over 18 jC. So, the present result agrees with the findings of Minamisawa and Sakai (1969) and, further, indicates that self-feeding is a technique that can straightforwardly show the relationship between an external factor, such as water temperature, and the feeding activity of fishes. Based on Minamisawa and Sakai’s descriptions, the water temperature of the present study from September to the middle of November was kept above 18 jC and within the appropriate range for yellowtail feeding, so this seemed to be a reason yellowtail increased their food demand in spite of the water temperature being lower. The low feeding activity from late November to early May at 12 – 17 jC was also consistent with their description. In early March, an abrupt increase in feed intake was observed occasionally, corresponding well with transitory increases in water temperature at the end of winter. The daily profile of self-feeding activity changed, especially during the early period of the experiments (Fig. 2). Just after the experiments started, the feeding activity was observed mostly during the nighttime. This scotophase feeding lasted for 25 days in Cage
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A and 10 days in Cage B, and it may mainly be due to an avoidance of high light intensity during the daytime. The same scotophase feeding was observed in the experiment with outdoor tanks (Kohbara et al., 2000). Also, this period may be related to learning the process of self-feeding since the frequency of feeding activity was very low and fluctuating. The period from start to onset of self-feeding has been reported to be within 1– 3 days in rainbow trout (Landless, 1976; Boujard and Leatherland, 1992), Arctic charr (Bra¨nna¨s and Alana¨ra¨, 1993), European sea bass (Sa´nchez-Va´zquez et al., 1994) and yellowtail (Kohbara et al., 2000, 2001). However, it took much longer for the food demand to reach a suitable level. For example, rainbow trout required a further 8– 11 days to reach a stable level of self-feeding (Boujard and Leatherland, 1992). In European sea bass, it took 22 days to reach the maximum amount of food that could be delivered per day (Sa´nchez-Va´zquez et al., 1994). In yellowtail, we reported in the previous papers that it required 11– 15 days to reach a stable level of self-feeding in the experiments using 200-l tanks (Kohbara et al., 2000, 2001). Although the reason the first group of yellowtail in Cage B did not start self-feeding is unknown, the other two groups in net cages started self-feeding immediately. However, they might require a much longer time to reach a stable level of self-feeding as was observed in the experimental tanks. Lower stocking density in tanks or cages may have some effect and prolong the learning period for self-feeding. After a period of learning, feeding occurred during both daytime and nighttime with small peaks at dawn and dusk. The continuous feeding throughout the whole day might be necessary for young yellowtail to grow rapidly in a short period. Observations of the swimming behavior revealed that young yellowtail have a tendency to swim at the surface of the net cages, and this might reflect the habit of juvenile yellowtail hiding under floating seaweed (Anraku and Azeta, 1965, 1967). Additionally, the tip of the sensor, a pellet-like knob, was located about 10 cm below the surface of seawater. Therefore, these three factors, i.e., the rapid growth, the habit of swimming at the surface and the surface location of the sensor tip, might be implicated in feeding throughout the whole day. Later, yellowtail had a tendency to swim at the lower area in the net cages during the daytime. It is uncertain whether this behavioral change is based on avoidance of high light intensity or natural predators, such as birds, but it might accompany an increasing size. Interestingly, this behavioral change in swimming depth was concurrent with the disappearance of the difference in water temperature between the surface layer and 4 m depth. This environmental change could be a trigger that lets yellowtail swim at a deeper level. Also, the behavioral change of swimming at a deeper level and the surface location of the sensor tip may be the cause of a decreased feeding activity during the daytime. Subsequently, yellowtail began high feeding activity at dawn and dusk. The two peaks appeared at the time period of the greatest change in light intensity and followed perfectly the seasonal change of photoperiod (Figs. 3 and 4). This synchronization may suggest that a significant change in light intensity stimulates the appetite of yellowtail or there is a light level where yellowtail prefer to eat. The evocation of the feeding activity by a significant change in light intensity has not been reported in the indoor self-feeding experiments because a simple electric timer without a dimmer function has often been used. Moreover, the fundamental interest of researchers was put on the relationship between the diel feeding pattern and the given photoperiod. In outdoor experiments under the natural light conditions, however, a high self-feeding
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activity was observed at dawn and/or dusk in some species. Landless (1976) reported an evident correlation between the time of feeding peaks and sunset in rainbow trout. Also, a feeding peak around dawn was observed in the daily pattern of self-feeding activity in European sea bass (Azzaydi et al., 1999). These peaks followed the seasonal change in sunrise and/or sunset time, as was observed in the present experiment. Therefore, rainbow trout and European sea bass also naturally adjust feeding activity according to a significant change of light intensity. Kadri et al. (1991) observed the swimming and feeding behavior of Atlantic salmon, Salmo salar, in sea cages using an underwater video camera and reported that both appetite and swimming speed also showed a marked daily rhythm, being highest in early morning and evening. They reported that time of day had a far greater influence on swimming and feeding activity than the state of the tide. In addition, Blyth et al. (1993) investigated the feeding behavior of Atlantic salmon in sea cages using an adaptive feeding system, which automatically feed fish by regulating feed input based on the levels of waste food detected beneath a feeding zone, and reported that Atlantic salmon display a diel feeding pattern, preferring to feed in just after dawn and just before dusk. These two distinct feeding peaks of Atlantic salmon closely related to the significant change of light conditions at dawn and dusk, as was observed in the present study in yellowtail. Moreover, Anraku and Azeta (1967) reported that the prey content in the stomach of larvae and juvenile yellowtail showed active feeding at around sunrise and sunset. Also, Hatanaka et al. (1958) observed that young yellowtail started to feed actively a little before sunrise, that the activity seemed to be low in the daytime and that they then started to eat again vigorously at sunset. Mitani (1958) categorized adult yellowtail as a nocturnal feeder in nature since fish caught in the morning had a higher prey content in the stomach than those caught in the evening. All these results coincided well with the present result of the selffeeding study. In general, fishermen know from experience that the feeding activity of fishes during the time period of dawn and dusk is much higher than usual since the crepuscular period is a good fishing time. It is very interesting that self-feeding technique could experimentally confirm the phenomenon that is experienced by fishermen. Acknowledgements We thank Mr. H. Nakamura for his help in transporting the experimental animals and Dr. S. Kimura for his help during our stay at the Fisheries Research Laboratory, Faculty of Bioresources, Mie University. Thanks are also due to Dr. I. Oshima, Aburabi Laboratory, Shionogi & Co., for providing the data acquisition software. This work was partly supported by a Grant-in-Aid for Scientific Research (Nos. 08556033 and 11356006) from the Ministry of Education, Science, Sports and Culture of Japan. A part of this work was conducted as ‘‘A project for the development of a feed wastage reduction system in marine fish culture’’ by Marinoforum 21. References Adron, J.W., Grant, P.T., Cowey, C.B., 1973. A system for the quantitative study for the learning capacity of rainbow trout and its application to the study of food preferences and behaviour. J. Fish Biol. 5, 625 – 636.
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Alana¨ra¨, A., 1992a. Demand feeding as a self-regulating feeding system for rainbow trout (Oncorhynchus mykiss) in net-pens. Aquaculture 108, 347 – 356. Alana¨ra¨, A., 1992b. The effect of time-restricted demand feeding on feeding activity, growth and feed conversion in rainbow trout (Oncorhynchus mykiss). Aquaculture 108, 357 – 368. Alana¨ra¨, A., 1994. The effect of temperature, dietary energy content and reward level on the demand feeding activity of rainbow trout (Oncorhynchus mykiss). Aquaculture 126, 349 – 359. Alana¨ra¨, A., 1996. The use of self-feeders in rainbow trout (Oncorhynchus mykiss) production. Aquaculture 145, 1 – 20. Aloisi, D.B., 1994. Growth of hatchery-reared lake trout fed by demand feeders. Prog. Fish-Cult. 56, 40 – 43. Anraku, M., Azeta, M., 1965. The feeding habits of larvae and juveniles of the yellowtail, Seriola quinqueradiata Temminck et Schlegel, associated with floating seaweeds. Bull. Seikai Reg. Fish. Res. Lab. 33, 15 – 45 (in Japanese, with English abstract). Anraku, M., Azeta, M., 1967. The feeding activities of yellowtail larvae, Seriola quinqueradiata Temminck et Schlegel, associated with floating seaweeds. Bull. Seikai Reg. Fish. Res. Lab. 35, 41 – 50 (in Japanese, with English abstract). Azzaydi, M., Martı´nez, F.J., Zamora, S., Sa´nchez-Va´zquez, F.J., Madrid, J.A., 1999. Effect of meal size modulation on growth performance and feeding rhythms in European sea bass (Dicentrarchus labrax L.). Aquaculture 170, 253 – 266. Blyth, P.J., Purser, G.J., Russell, J.F., 1993. Detection of feeding rhythms in seacaged Atlantic salmon using new feeder technology. In: Reinertsen, H., Dahle, L.A., Jørgensen, L., Tvinnereim, K. (Eds.), Fish Farming Technology. Proceedings of the First International Conference on Fish Farming Technology, 9 – 12 August 1993, Trondheim, Norway. A.A. Balkema, Rotterdam, pp. 209 – 216. Boujard, T., Leatherland, J.F., 1992. Demand-feeding behaviour and diel pattern of feeding activity in Oncorhynchus mykiss held under different photoperiod regimes. J. Fish Biol. 40, 535 – 544. Boujard, T., Jourdan, M., Kentouri, M., Divanach, P., 1996. Diel feeding activity and effect of time-restricted selffeeding on growth and feed conversion in European sea bass. Aquaculture 139, 117 – 127. Bra¨nna¨s, E., Alana¨ra¨, A., 1993. Monitoring the feeding activity of individual fish with a demand feeding system. J. Fish Biol. 42, 209 – 215. Bra¨nna¨s, E., Alana¨ra¨, A., 1994. Effect of reward level on individual variability in demand feeding activity and growth rate in Arctic charr and rainbow trout. J. Fish Biol. 45, 423 – 434. Brett, J.R., Higges, D.A., 1970. Effect of temperature on the rate of gastric digestion in fingerling sockeye salmon Oncorhynchus nerka. J. Fish. Res. Board Can. 27, 1767 – 1779. Brown, M.E., 1946. The growth of brown trout (Salmo trutta Linn.): III. The effect of temperature on the growth of two-year-old trout. J. Exp. Biol. 22, 145 – 155. Hatanaka, M., Takahashi, M., Murakawa, G., 1958. Experimental studies on the feeding habits of amber-fish, Seriola quinqueradiata T. et S. Bull. Jpn. Soc. Sci. Fish. 24, 251 – 255 (in Japanese, with English abstract). Johnson, L., 1966. Experimental determination of food consumption of pike, Esox lucius, for growth and maintenance. J. Fish. Res. Board Can. 23, 1495 – 1505. Kadri, S., Metcalfe, N.B., Huntingford, F.A., Thorpe, J.E., 1991. Effect of meal size on feeding rhythms in Atlantic salmon in sea cages. Aquaculture 92, 219 – 224. Kindschi, G.A., 1984. Notes on two feed types and methods for steelhead trout production. Prog. Fish-Cult. 46, 44 – 47. Kohbara, J., Hidaka, I., Kuriyama, I., Yamashita, M., Ichikawa, M., Furukawa, K., Aida, K., Sa´nchez-Va´zquez, F.J., Tabata, M., 2000. Nocturnal/diurnal demand-feeding pattern of yellowtail Seriola quinqueradiata under different keeping conditions. Fish. Sci. 66, 955 – 962. Kohbara, J., Hidaka, I., Yamashita, M., Ichikawa, M., Furukawa, K., Aida, K., Tabata, M., 2001. Effect of reward level on the number of food demands in yellowtail Seriola quinqueradiata. Fish. Sci. 67, 660 – 666. Lagler, K.F., Bardach, J.E., Miller, R.R., Passino, D.R.M., 1977. Ichthyology, 2nd ed. Wiley, New York. 506 pp. Landless, P.J., 1976. Demand feeding behaviour of rainbow trout. Aquaculture 7, 11 – 25. Madrid, J.A., Azzaydi, M., Zamora, S., Sa´nchez-Va´zquez, F.J., 1997. Continuous recording of uneaten food pellets and demand-feeding activity: a new approach to studying feeding rhythms in fish. Physiol. Behav. 62, 689 – 695.
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Madrid, J.A., Boujard, T., Sa´nchez-Va´zquez, F.J., 2001. Feeding rhythms. In: Houlihan, D., Boujard, T., Jobling, M. (Eds.), Food Intake in Fish. Blackwell Science, Oxford, pp. 189 – 215. Minamisawa, A., Sakai, H., 1969. Cultivation of a yellowtail (Seriola quinqueradiata Temminck & Schlegel). Aquaculture Series 18. Japan Fisheries Resource Conservation Association, Tokyo. 56 pp., in Japanese. Mitani, F., 1958. Feeding habits of the yellow-tail, Seriola quinqueradiata T. & S., caught in Wakasa Bay, the Japan Sea, based on its stomach contents: II. Daily change of feeding activity and variation in feeding activity with its growth. Bull. Jpn. Soc. Sci. Fish. 24, 182 – 185 (in Japanese, with English abstract). Oshima, I., Ebihara, S., 1987. The measurement and analysis of circadian locomotor activity and body temperature rhythms by a computer-based system. Physiol. Behav. 43, 115 – 119. Rozin, P., Mayer, J., 1961. Regulation of food intake in the goldfish. Am. J. Physiol. 201, 968 – 974. Sa´nchez-Va´zquez, F.J., Tabata, M., 1998. Circadian rhythms of demand-feeding and locomotor activity in rainbow trout. J. Fish Biol. 52, 255 – 267. Sa´nchez-Va´zquez, F.J., Martı´nez, M., Zamora, S., Madrid, J.A., 1994. Design and performance of an accurate demand feeder for the study of feeding behaviour in sea bass, Dicentrarchus labrax L. Physiol. Behav. 56, 789 – 794. Sa´nchez-Va´zquez, F.J., Madrid, J.A., Zamora, S., 1995. Circadian rhythms of feeding activity in sea bass, Dicentrarchus labrax L.: dual phasing capacity of diel demand-feeding pattern. J. Biol. Rhythms 10, 256 – 266. Sa´nchez-Va´zquez, F.J., Madrid, J.A., Zamora, S., Iigo, M., Tabata, M., 1996. Demand feeding and locomotor circadian rhythms in the goldfish, Carassius auratus: dual and independent phasing. Physiol. Behav. 60, 665 – 674. Sa´nchez-Va´zquez, F.J., Azzaydi, M., Martinez, F.J., Zamora, S., Madrid, J.A., 1998a. Annual rhythms of demand-feeding activity in sea bass: evidence of a seasonal phase inversion of the diel feeding pattern. Chronobiol. Int. 15, 607 – 622. Sa´nchez-Va´zquez, F.J., Yamamoto, T., Akiyama, T., Madrid, J.A., Tabata, M., 1998b. Selection of macronutrients by goldfish operating self-feeders. Physiol. Behav. 65, 211 – 218. Sa´nchez-Va´zquez, F.J., Yamamoto, T., Akiyama, T., Madrid, J.A., Tabata, M., 1999. Macronutrient self-selection through demand-feeders in rainbow trout. Physiol. Behav. 66, 45 – 51. Takahashi, M., Murachi, S., Moriwaki, S., 1981a. A feeding device for fishes designed for experimental use. Bull. Jpn. Soc. Sci. Fish. 47, 1131 – 1134. Takahashi, M., Murachi, S., Sekitani, T., Moriwaki, S., Ogawa, T., 1981b. Formation of the ‘‘bobber up thrust response’’ for food-obtaining in bluegill sunfish Lepomis macrochirus. Bull. Jpn. Soc. Sci. Fish. 47, 1135 – 1140. Takahashi, M., Murachi, S., Moriwaki, S., Ogawa, S., 1984. The response level of bluegill sunfish, Lepomis macrochirus, to a demand feeder. Bull. Jpn. Soc. Sci. Fish. 50, 1475 – 1480. Tipping, J.M., Rathvon, R.L., Moore, S.T., 1986. Use of demand feeders in large steelhead rearing ponds. Prog. Fish-Cult. 48, 303 – 304. Yamamoto, T., Shima, T., Furuita, H., Shiraishi, M., Sa´nchez-Va´zquez, F.J., Tabata, M., 2000. Self-selection of diets with different amino acid profiles by rainbow trout (Oncorhynchus mykiss). Aquaculture 187, 375 – 386.
Self-feeding behavior of yellowtail, Seriola quinqueradiata, in net cages: diel and seasonal patterns and influences of environmental factors J. Kohbara a,*, I. Hidaka a, F. Matsuoka a, T. Osada a, K. Furukawa b, M. Yamashita a, M. Tabata c a b
Laboratory of Fish Physiology, Faculty of Bioresources, Mie University, Kamihama, Tsu, Mie 514-8507, Japan Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo 113-8657, Japan c Department of Animal Sciences, Teikyo University of Science and Technology, Uenohara, Yamanashi 409-0193, Japan Received 27 June 2002; received in revised form 1 October 2002; accepted 18 November 2002
Abstract The self-feeding pattern of yellowtail, Seriola quinqueradiata, maintained in floating net cages was examined throughout a year, and the influence of seasonal changes of the photoperiod and water temperature on the feeding pattern was investigated. Two groups of 50 yellowtail (initial mean body weight about 50 and 80 g, respectively) were kept in two experimental net cages (2 3 4 m deep), with a self-feeding device installed on each. It was possible to maintain yellowtail in net cages using a self-feeder throughout almost a year. The number of daily food demands was greatly affected by the seasonal changes in water temperature. Yellowtail showed high self-feeding activity, above 18 jC; depressing water temperatures did not influence the activity when the water temperature was over 18 jC. However, the activity decreased when the water temperature fell below 18 jC. The feeding pattern in a 24-h period was greatly affected by the temporal changes in light intensity. Annual observations revealed that yellowtail showed generally crepuscular plus nocturnal feeding behavior and had two peaks of feeding activity a day. These peaks appeared at dawn and dusk; moreover, a clear association between the most active time of self-feeding and the period of the greatest change in light intensity was observed. The results suggest that a change in light intensity might stimulate the appetite of yellowtail or that there is a light level at which yellowtail prefer to eat. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Light intensity; Net cage; Self-feeding; Seriola quinqueradiata; Water temperature; Yellowtail
* Corresponding author. Tel: +81-59-231-9534; fax: +81-59-231-9523. E-mail address: [email protected] (J. Kohbara). 0044-8486/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0044-8486(02)00642-7
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1. Introduction A self-feeding technique that enables fish to feed on demand has been used in many studies of fish feeding behavior. It has been used, for example, to study the learning ability (Adron et al., 1973; Takahashi et al., 1981a,b, 1984), the diel feeding-pattern (Rozin and Mayer, 1961; Landless, 1976; Boujard and Leatherland, 1992; Sa´nchezVa´zquez et al., 1994), the circadian rhythms of self-feeding (Sa´nchez-Va´zquez et al., 1995, 1996; Sa´nchez-Va´zquez and Tabata, 1998), the regulation of food intake (Boujard and Leatherland, 1992; Alana¨ra¨, 1992a, 1994; Bra¨nna¨s and Alana¨ra¨, 1994), the food preferences (Adron et al., 1973), the nutrient selection for diet design (Sa´nchez-Va´zquez et al., 1998b, 1999; Yamamoto et al., 2000) and the social interaction between individuals (Bra¨nna¨s and Alana¨ra¨, 1993, 1994). The results obtained from these investigations revealed that the technique of self-feeding can be used to investigate a wide variety of research fields relating to fish feeding. In addition, as an aquaculture technique, self-feeding drastically reduces food waste and lowers the environmental impact (Alana¨ra¨, 1992b, 1996; Madrid et al., 1997) because it adjusts the food supply to the appetite of the fish. Research applying self-feeding to aquaculture has been carried out using species of commercial value, such as rainbow trout, Oncorhynchus mykiss (Adron et al., 1973; Landless, 1976; Kindschi, 1984; Tipping et al., 1986; Alana¨ra¨, 1992a,b, 1994, 1996; Boujard and Leatherland, 1992; Bra¨nna¨s and Alana¨ra¨, 1994; Sa´nchez-Va´zquez and Tabata, 1998; Sa´nchez-Va´zquez et al., 1999; Yamamoto et al., 2000), Arctic charr, Salvelinus alpinus (Bra¨nna¨s and Alana¨ra¨, 1993, 1994), lake trout, Salvelinus namaycush (Aloisi, 1994), European sea bass, Dicentrarchus labrax (Sa´nchez-Va´zquez et al., 1994, 1995, 1998a; Boujard et al., 1996; Madrid et al., 1997) and yellowtail, Seriola quinqueradiata (Kohbara et al., 2000, 2001), and the feeding rhythms, growth performances and the rate of feed wastage under the self-feeding condition have been investigated. These practical studies also revealed that the self-feeding pattern of fish could be changeable according to the differences in rearing conditions, even in the same species. For example, rainbow trout showed a feeding peak at dusk and also a high level of nocturnal feeding activity under field conditions on one hand (Landless, 1976) and a clear diurnal pattern synchronizing the given L/D cycle under experimental room conditions on the other (Boujard and Leatherland, 1992). Similarly, European sea bass showed a dualistic feeding behavior, nocturnal and diurnal feeding patterns under the controlled experimental conditions (Sa´nchez-Va´zquez et al., 1995) and a seasonal phase inversion of the diel feeding pattern under field conditions (Sa´nchez-Va´zquez et al., 1998a). We have been studying the self-feeding behavior of the yellowtail, which is one of the most important commercial fish in the aquaculture industry of Japan, and we found that the inversion of the diel feeding pattern also occurred in this species. Specifically, yellowtail in indoor tanks showed a clear diurnal feeding pattern synchronizing to the given photoperiod, whereas those in the outdoor tanks showed a clear nocturnal feeding pattern also synchronizing to the outdoor natural photoperiod (Kohbara et al., 2000). Thus, the findings about changes in feeding pattern mentioned above suggest that exogenous and endogenous factors may influence a pattern of selffeeding behavior (Madrid et al., 2001).
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Most investigations to date have used small tanks up to 500 l, while little is known about self-feeding behavior of fish reared in floating net cages. Therefore, it was considered important to describe the feeding patterns of fish in net cages. The aim of the present experiment was to study the self-feeding pattern of yellowtail maintained in floating net cages throughout a year and to examine the influences of seasonal changes of natural photoperiod and water temperature on these patterns.
2. Materials and methods 2.1. Animals and experimental conditions The experiments were performed from July 1999 to July 2000 at the Fisheries Research Laboratory of Mie University at Wagu (34j16V20WN, 136j48V27WE), Mie Prefecture, Japan. The experimental animals were wild, juvenile yellowtail caught by local fishermen. After being kept in a floating net cage set off from the shore for about a month, they were anesthetized with ethyl m-aminobenzoate methanesulfonate (MS-222, Sigma, St. Louis, MO, USA) for weighing. Individuals whose body weight was approximately 50 g were chosen. Two experimental net cages (2 3 4 m deep), designated as Cage A and Cage B, were established, and the selected yellowtail were then divided into two groups with 50 fish in each net cage. However, for unknown reasons, the fish in Cage B did not actuate the feeder for 2 weeks, so 50 new fish whose body weight was approximately 80 g were selected from a reserve group and were established as a new group in Cage B. Therefore, the mean initial body weights in Cage A and Cage B were 55.1 and 88.5 g, respectively. The experiment was divided into five periods: Period I, from 27 July 1999 in Cage A and 10 August in Cage B to 6 October; Period II, from 7 October to 25 November; Period III, from 26 November to 18 February 2000; Period IV, from 19 February to 2 May; Period V, from 3 May to 12 July. Before and after each experimental period, all fish were removed from their cage, anesthetized and individually weighed to establish an accurate reward level for a certain size of fish. During each experimental period, fish were fed with a recommended size of commercial diet for yellowtail (Hamachi EP Special Nos. 4, 6 and 8, Marubeni Shiryo, Tokyo, Japan) according to the size of the fish. 2.2. Self-feeding device and data acquisition A Touch Feed 990 system (Sterner Products, Leksand, Sweden) was used as the selffeeding apparatus. This system consisted of a trigger, a control unit and a feeder and was useable for larger-scale experiments (Alana¨ra¨, 1992a, 1996). A set consisting of a trigger and a feeder was placed at the center of each net cage. The trigger was stored in a PVC pipe and the feeder was set in a large plastic box with the bottom removed to avoid damage by the salt air or seawater. The trigger was a stainless steel wire type (Sterner Sensor Type 3), and a nylon string that ended in a small plastic ball was attached to the end of the wire. The small plastic ball was located about 10 cm below the surface of the
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seawater. The control unit and the battery were stored in a plastic box and placed on a Styrofoam float of the net cages. The feeder and the control unit were adjusted to deliver a set quantity of pellets when the trigger was actuated by a fish pulling the plastic ball in its mouth. The amount of feed dispensed was calculated every few days from the weight of the feed added and of that remaining in the feeder. The daily food demand was obtained from the number of daily feeder actuations and the actual reward of the day. The time of actuations was stored in a portable data logger (HOBO Event, Onset Computer, MA, USA) and downloaded to a computer. Raw data was summarized as the number of feeder actuations in 10-min segments and translated to a format suitable for the data analysis programs built by Oshima and Ebihara (1987) to draw actograms or periodograms. 2.3. Reward level The reward level, the number of pellets delivered per trigger actuation, was established by dividing 50, the recommended daily amount of feed at a certain temperature for a certain size of fish, by 50. Namely, if the 50 fish actuate a feeder 50 times per day, they obtain the recommended amount of feed indicated in the feeding table provided by the feed manufacturer. 2.4. Environmental factors Light intensity at 1 m depth in the net cage was recorded every 10 min using a data logger (StowAway SLA, Onset Computer). The water temperatures at depth of 0.5 and 4 m were recorded every hour using data loggers (Optic StowAway Temp, Onset Computer) over a 1-year period.
3. Results 3.1. Changes of daily feeding activity The daily food demand (daily food supply) of yellowtail in Cage A and Cage B throughout the experimental periods is shown in Fig. 1. In Cage A, the daily food demand immediately after the beginning of the experiment was about 100 g/day, gradually increasing by November. Feeder actuations were observed almost everyday. The daily food demand became highest, about 1000 g/day, in early November. Afterwards, it gradually decreased until late January, and days without baiting activity were observed frequently from late November through late April. The daily food demand remained at the same low level of around 100 –300 g/day from mid-January through late April. However, days in which the daily feed supply was close to 500 g/day occurred occasionally from late February. In early May, the daily food demand rapidly increased, and it kept increasing until July 12, the end of the experiment. The degree of increment of the daily food demand was remarkable. The changes of daily food demand in Cage B tended to be almost identical to that observed in Cage A (Fig. 1).
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Fig. 1. Changes of the number of daily food demands in Cage A (upper) and Cage B (lower) throughout a 1-year experimental period. The changes of the water temperature (daily average) at the depths of 0.5 m (solid line) and 4 m (dotted line) are superimposed upon each graph.
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3.2. Changes of water temperature The changes in water temperature at 0.5 and 4 m depth of the net cages during the experimental period were superimposed upon both figures of the daily food demand in Cage A and Cage B (Fig. 1). From the beginning of the experiment to late August, the water temperatures both at the surface and at the depth of 4 m increased, and the observed maximum temperature was 29.8 and 29.1jC, respectively. From early September, the water temperature at both observation depths kept falling gradually until mid-December. The water temperature at the surface tended to be higher than that at 4 m depth; however, no difference was observed between them in late September. The water temperature from midDecember to mid-April remained at the same low level of around 13 –14 jC. The lowest was recorded on 25 February, when it was 12.6 jC at the surface and 12.7 jC at 4 m depth. In early March, the water temperature began rising gradually and the water temperature at the surface remained higher than that at 4 m depth from April. It rose rapidly to 18 jC or higher with increasing differences in water temperature between the two depths in late
Fig. 2. An actogram of self-feeding from yellowtail in Cage A (a) and Cage B (b) throughout almost a 1-year observation. Yellowtail in both cages showed a clear crepuscular and nocturnal feeding pattern synchronizing to the natural photoperiod. The data are double plotted (48-h time scale).
J. Kohbara et al. / Aquaculture 220 (2003) 581–594 Fig. 3. Monthly changes of the daily waveform of self-feeding activity in Cage A. The vertical lines in each waveform indicate the average of the daily feeder actuations in 10-min segments. The daily profiles of the photoperiod in each month is indicated the upper part of each waveform. 587
588 J. Kohbara et al. / Aquaculture 220 (2003) 581–594 Fig. 4. Monthly changes of the daily waveform of self-feeding activity in Cage B. The vertical lines in each waveform indicate the average of the daily feeder actuations in 10-min segments. The daily profiles of the photoperiod in each month is indicated the upper part of each waveform.
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April. At the end of the experiment, the water temperatures at the surface and at the depth of 4 m were 27.0 and 25.6 jC, respectively. 3.3. Self-feeding activity The actograms (double-plotted procedure, 48-h time scale) over the year, obtained from Cage A and Cage B, are shown in Fig. 2. The patterns observed in the actograms of Cage A and Cage B are almost identical. The nocturnal feeding activity commenced, seen after the experiments started to around 20 August 1999. The feeding activity showed a tendency to be concentrated particularly at the period of dawn and dusk with less frequent activities both in the daytime and nighttime. From 20 September to late November, the feeding activity during the daytime became much less frequent, being restricted to the nighttime. From late November, the nocturnal feeding continued, but the frequency declined to a level where feeding activity did not occur during the day. From mid-January, the feeding activity was restricted to dusk. From early March, the nighttime feeding activity appeared again, but its frequency was low. Subsequently, the feeding activity increased and was distributed throughout the nighttime by late May. From June through mid-July, the feeding activity occurred particularly at dawn and dusk again. Feeding activity during the daytime was also observed in mid-July. Monthly changes of the daily waveform of self-feeding activity obtained from Cage A and Cage B are shown in Figs. 3 and 4, respectively. The lower waveforms in each figure indicate the average number of daily feeder actuations in 10-min segments. The daily profile of the photoperiod in each month is indicated in the upper part of each waveform. The patterns of daily feeder actuations observed in Cage A and Cage B show a similar tendency. When the experiment started in August, self-feeding of low frequency was unevenly distributed throughout the nighttime. Activity was also observed during the daytime, but its frequency was low. In September, two steep peaks of feeding activity per day were observed, and one of them coincided with the rapid increase of light intensity at dawn and the other with its rapid decrease at dusk. Feeding activity during the daytime and nighttime occurred, but its frequency was low. Similar waveforms possessing two steep peaks at dawn and dusk were also evident from October to December. However, the total number of feeder actuations decreased from January. Low feeding activity during the nighttime with a small peak at dusk was observed, and this situation continued until April. However, the total number of feeder actuations gradually increased, and two steep peaks at dawn and dusk appeared again from May through July. The total number of feeder actuations increased in July, and the feeding activity during the daytime occurred frequently in addition to two peaks of feeding activity at dawn and dusk.
4. Discussion The present study revealed that it is possible to cultivate yellowtail in net cages throughout the year using self-feeders. Moreover, it demonstrated that environmental factors, such as water temperature and light intensity, have a great influence on the self-
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feeding behavior of yellowtail. Namely, the seasonal changes of water temperature influenced the number of daily food demands, and the temporal changes in light intensity greatly influenced the feeding pattern in a 24-h period. In the relationship between the changes of water temperature and the number of daily food demands, the daily food demand increased day by day from September to November in spite of the decreasing water temperature. Thus, a rise or fall in water temperature is not always consistent with an increase or decrease in the daily food demand of yellowtail. In many fish species, such as brown trout, Salmo trutta (Brown, 1946), sockeye salmon, Oncorhynchus nerka (Brett and Higges, 1970), goldfish, Carassius auratus (Rozin and Mayer, 1961) and bluegill, Lepomis macrochirus (Lagler et al., 1977), the food intake is closely adjusted to changes in water temperature, whereas yellowtail is recognized to be a fish species that can increase daily food intake in spite of decreasing water temperature. The food intake of yellowtail is apparently regulated on an annual basis, somewhat independent of water temperature changes, especially when the water temperature is above 18 jC. Yellowtail show a particular high growth rate in their juvenile stage, and this might encourage them to eat as much as they can. Therefore, the influence of water temperature on the food intake may be different for 2-year-old and older yellowtail. Similarly, food intake was independent of water temperature changes in pike, Esox lucius (Johnson, 1966). Contrary to the phenomena described above, low water temperature, less than 18 jC, had a great influence on the food demand of yellowtail. When the water temperature fell to less than 18 jC in November, a decrease of food demand occurred simultaneously, and when it rose to more than 18 jC in May the following year, a marked increase of food demand occurred simultaneously. This suggests the existence of a marginal temperature at which yellowtail can maintain high feeding activity, and it must be around 18 jC. Minamisawa and Sakai (1969) mentioned the relationship between water temperature and the feeding activity in yellowtail in culture conditions. They observed that at less than 11 jC, no feeding activity occurred; at 13– 17 jC, feeding activity was observed but its frequency was low; 18– 27 jC was a suitable temperature range for feeding; 24 – 26 jC was the best temperature range for feeding; and above 28 jC, feeding activity decreased due to too high water temperature for yellowtail. Interestingly, the present self-feeding experiments showed clearly that the daily food demand rapidly decreased when the water temperature fell below 18 jC and rapidly increased when it rose over 18 jC. So, the present result agrees with the findings of Minamisawa and Sakai (1969) and, further, indicates that self-feeding is a technique that can straightforwardly show the relationship between an external factor, such as water temperature, and the feeding activity of fishes. Based on Minamisawa and Sakai’s descriptions, the water temperature of the present study from September to the middle of November was kept above 18 jC and within the appropriate range for yellowtail feeding, so this seemed to be a reason yellowtail increased their food demand in spite of the water temperature being lower. The low feeding activity from late November to early May at 12 – 17 jC was also consistent with their description. In early March, an abrupt increase in feed intake was observed occasionally, corresponding well with transitory increases in water temperature at the end of winter. The daily profile of self-feeding activity changed, especially during the early period of the experiments (Fig. 2). Just after the experiments started, the feeding activity was observed mostly during the nighttime. This scotophase feeding lasted for 25 days in Cage
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A and 10 days in Cage B, and it may mainly be due to an avoidance of high light intensity during the daytime. The same scotophase feeding was observed in the experiment with outdoor tanks (Kohbara et al., 2000). Also, this period may be related to learning the process of self-feeding since the frequency of feeding activity was very low and fluctuating. The period from start to onset of self-feeding has been reported to be within 1– 3 days in rainbow trout (Landless, 1976; Boujard and Leatherland, 1992), Arctic charr (Bra¨nna¨s and Alana¨ra¨, 1993), European sea bass (Sa´nchez-Va´zquez et al., 1994) and yellowtail (Kohbara et al., 2000, 2001). However, it took much longer for the food demand to reach a suitable level. For example, rainbow trout required a further 8– 11 days to reach a stable level of self-feeding (Boujard and Leatherland, 1992). In European sea bass, it took 22 days to reach the maximum amount of food that could be delivered per day (Sa´nchez-Va´zquez et al., 1994). In yellowtail, we reported in the previous papers that it required 11– 15 days to reach a stable level of self-feeding in the experiments using 200-l tanks (Kohbara et al., 2000, 2001). Although the reason the first group of yellowtail in Cage B did not start self-feeding is unknown, the other two groups in net cages started self-feeding immediately. However, they might require a much longer time to reach a stable level of self-feeding as was observed in the experimental tanks. Lower stocking density in tanks or cages may have some effect and prolong the learning period for self-feeding. After a period of learning, feeding occurred during both daytime and nighttime with small peaks at dawn and dusk. The continuous feeding throughout the whole day might be necessary for young yellowtail to grow rapidly in a short period. Observations of the swimming behavior revealed that young yellowtail have a tendency to swim at the surface of the net cages, and this might reflect the habit of juvenile yellowtail hiding under floating seaweed (Anraku and Azeta, 1965, 1967). Additionally, the tip of the sensor, a pellet-like knob, was located about 10 cm below the surface of seawater. Therefore, these three factors, i.e., the rapid growth, the habit of swimming at the surface and the surface location of the sensor tip, might be implicated in feeding throughout the whole day. Later, yellowtail had a tendency to swim at the lower area in the net cages during the daytime. It is uncertain whether this behavioral change is based on avoidance of high light intensity or natural predators, such as birds, but it might accompany an increasing size. Interestingly, this behavioral change in swimming depth was concurrent with the disappearance of the difference in water temperature between the surface layer and 4 m depth. This environmental change could be a trigger that lets yellowtail swim at a deeper level. Also, the behavioral change of swimming at a deeper level and the surface location of the sensor tip may be the cause of a decreased feeding activity during the daytime. Subsequently, yellowtail began high feeding activity at dawn and dusk. The two peaks appeared at the time period of the greatest change in light intensity and followed perfectly the seasonal change of photoperiod (Figs. 3 and 4). This synchronization may suggest that a significant change in light intensity stimulates the appetite of yellowtail or there is a light level where yellowtail prefer to eat. The evocation of the feeding activity by a significant change in light intensity has not been reported in the indoor self-feeding experiments because a simple electric timer without a dimmer function has often been used. Moreover, the fundamental interest of researchers was put on the relationship between the diel feeding pattern and the given photoperiod. In outdoor experiments under the natural light conditions, however, a high self-feeding
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activity was observed at dawn and/or dusk in some species. Landless (1976) reported an evident correlation between the time of feeding peaks and sunset in rainbow trout. Also, a feeding peak around dawn was observed in the daily pattern of self-feeding activity in European sea bass (Azzaydi et al., 1999). These peaks followed the seasonal change in sunrise and/or sunset time, as was observed in the present experiment. Therefore, rainbow trout and European sea bass also naturally adjust feeding activity according to a significant change of light intensity. Kadri et al. (1991) observed the swimming and feeding behavior of Atlantic salmon, Salmo salar, in sea cages using an underwater video camera and reported that both appetite and swimming speed also showed a marked daily rhythm, being highest in early morning and evening. They reported that time of day had a far greater influence on swimming and feeding activity than the state of the tide. In addition, Blyth et al. (1993) investigated the feeding behavior of Atlantic salmon in sea cages using an adaptive feeding system, which automatically feed fish by regulating feed input based on the levels of waste food detected beneath a feeding zone, and reported that Atlantic salmon display a diel feeding pattern, preferring to feed in just after dawn and just before dusk. These two distinct feeding peaks of Atlantic salmon closely related to the significant change of light conditions at dawn and dusk, as was observed in the present study in yellowtail. Moreover, Anraku and Azeta (1967) reported that the prey content in the stomach of larvae and juvenile yellowtail showed active feeding at around sunrise and sunset. Also, Hatanaka et al. (1958) observed that young yellowtail started to feed actively a little before sunrise, that the activity seemed to be low in the daytime and that they then started to eat again vigorously at sunset. Mitani (1958) categorized adult yellowtail as a nocturnal feeder in nature since fish caught in the morning had a higher prey content in the stomach than those caught in the evening. All these results coincided well with the present result of the selffeeding study. In general, fishermen know from experience that the feeding activity of fishes during the time period of dawn and dusk is much higher than usual since the crepuscular period is a good fishing time. It is very interesting that self-feeding technique could experimentally confirm the phenomenon that is experienced by fishermen. Acknowledgements We thank Mr. H. Nakamura for his help in transporting the experimental animals and Dr. S. Kimura for his help during our stay at the Fisheries Research Laboratory, Faculty of Bioresources, Mie University. Thanks are also due to Dr. I. Oshima, Aburabi Laboratory, Shionogi & Co., for providing the data acquisition software. This work was partly supported by a Grant-in-Aid for Scientific Research (Nos. 08556033 and 11356006) from the Ministry of Education, Science, Sports and Culture of Japan. A part of this work was conducted as ‘‘A project for the development of a feed wastage reduction system in marine fish culture’’ by Marinoforum 21. References Adron, J.W., Grant, P.T., Cowey, C.B., 1973. A system for the quantitative study for the learning capacity of rainbow trout and its application to the study of food preferences and behaviour. J. Fish Biol. 5, 625 – 636.
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Alana¨ra¨, A., 1992a. Demand feeding as a self-regulating feeding system for rainbow trout (Oncorhynchus mykiss) in net-pens. Aquaculture 108, 347 – 356. Alana¨ra¨, A., 1992b. The effect of time-restricted demand feeding on feeding activity, growth and feed conversion in rainbow trout (Oncorhynchus mykiss). Aquaculture 108, 357 – 368. Alana¨ra¨, A., 1994. The effect of temperature, dietary energy content and reward level on the demand feeding activity of rainbow trout (Oncorhynchus mykiss). Aquaculture 126, 349 – 359. Alana¨ra¨, A., 1996. The use of self-feeders in rainbow trout (Oncorhynchus mykiss) production. Aquaculture 145, 1 – 20. Aloisi, D.B., 1994. Growth of hatchery-reared lake trout fed by demand feeders. Prog. Fish-Cult. 56, 40 – 43. Anraku, M., Azeta, M., 1965. The feeding habits of larvae and juveniles of the yellowtail, Seriola quinqueradiata Temminck et Schlegel, associated with floating seaweeds. Bull. Seikai Reg. Fish. Res. Lab. 33, 15 – 45 (in Japanese, with English abstract). Anraku, M., Azeta, M., 1967. The feeding activities of yellowtail larvae, Seriola quinqueradiata Temminck et Schlegel, associated with floating seaweeds. Bull. Seikai Reg. Fish. Res. Lab. 35, 41 – 50 (in Japanese, with English abstract). Azzaydi, M., Martı´nez, F.J., Zamora, S., Sa´nchez-Va´zquez, F.J., Madrid, J.A., 1999. Effect of meal size modulation on growth performance and feeding rhythms in European sea bass (Dicentrarchus labrax L.). Aquaculture 170, 253 – 266. Blyth, P.J., Purser, G.J., Russell, J.F., 1993. Detection of feeding rhythms in seacaged Atlantic salmon using new feeder technology. In: Reinertsen, H., Dahle, L.A., Jørgensen, L., Tvinnereim, K. (Eds.), Fish Farming Technology. Proceedings of the First International Conference on Fish Farming Technology, 9 – 12 August 1993, Trondheim, Norway. A.A. Balkema, Rotterdam, pp. 209 – 216. Boujard, T., Leatherland, J.F., 1992. Demand-feeding behaviour and diel pattern of feeding activity in Oncorhynchus mykiss held under different photoperiod regimes. J. Fish Biol. 40, 535 – 544. Boujard, T., Jourdan, M., Kentouri, M., Divanach, P., 1996. Diel feeding activity and effect of time-restricted selffeeding on growth and feed conversion in European sea bass. Aquaculture 139, 117 – 127. Bra¨nna¨s, E., Alana¨ra¨, A., 1993. Monitoring the feeding activity of individual fish with a demand feeding system. J. Fish Biol. 42, 209 – 215. Bra¨nna¨s, E., Alana¨ra¨, A., 1994. Effect of reward level on individual variability in demand feeding activity and growth rate in Arctic charr and rainbow trout. J. Fish Biol. 45, 423 – 434. Brett, J.R., Higges, D.A., 1970. Effect of temperature on the rate of gastric digestion in fingerling sockeye salmon Oncorhynchus nerka. J. Fish. Res. Board Can. 27, 1767 – 1779. Brown, M.E., 1946. The growth of brown trout (Salmo trutta Linn.): III. The effect of temperature on the growth of two-year-old trout. J. Exp. Biol. 22, 145 – 155. Hatanaka, M., Takahashi, M., Murakawa, G., 1958. Experimental studies on the feeding habits of amber-fish, Seriola quinqueradiata T. et S. Bull. Jpn. Soc. Sci. Fish. 24, 251 – 255 (in Japanese, with English abstract). Johnson, L., 1966. Experimental determination of food consumption of pike, Esox lucius, for growth and maintenance. J. Fish. Res. Board Can. 23, 1495 – 1505. Kadri, S., Metcalfe, N.B., Huntingford, F.A., Thorpe, J.E., 1991. Effect of meal size on feeding rhythms in Atlantic salmon in sea cages. Aquaculture 92, 219 – 224. Kindschi, G.A., 1984. Notes on two feed types and methods for steelhead trout production. Prog. Fish-Cult. 46, 44 – 47. Kohbara, J., Hidaka, I., Kuriyama, I., Yamashita, M., Ichikawa, M., Furukawa, K., Aida, K., Sa´nchez-Va´zquez, F.J., Tabata, M., 2000. Nocturnal/diurnal demand-feeding pattern of yellowtail Seriola quinqueradiata under different keeping conditions. Fish. Sci. 66, 955 – 962. Kohbara, J., Hidaka, I., Yamashita, M., Ichikawa, M., Furukawa, K., Aida, K., Tabata, M., 2001. Effect of reward level on the number of food demands in yellowtail Seriola quinqueradiata. Fish. Sci. 67, 660 – 666. Lagler, K.F., Bardach, J.E., Miller, R.R., Passino, D.R.M., 1977. Ichthyology, 2nd ed. Wiley, New York. 506 pp. Landless, P.J., 1976. Demand feeding behaviour of rainbow trout. Aquaculture 7, 11 – 25. Madrid, J.A., Azzaydi, M., Zamora, S., Sa´nchez-Va´zquez, F.J., 1997. Continuous recording of uneaten food pellets and demand-feeding activity: a new approach to studying feeding rhythms in fish. Physiol. Behav. 62, 689 – 695.
594
J. Kohbara et al. / Aquaculture 220 (2003) 581–594
Madrid, J.A., Boujard, T., Sa´nchez-Va´zquez, F.J., 2001. Feeding rhythms. In: Houlihan, D., Boujard, T., Jobling, M. (Eds.), Food Intake in Fish. Blackwell Science, Oxford, pp. 189 – 215. Minamisawa, A., Sakai, H., 1969. Cultivation of a yellowtail (Seriola quinqueradiata Temminck & Schlegel). Aquaculture Series 18. Japan Fisheries Resource Conservation Association, Tokyo. 56 pp., in Japanese. Mitani, F., 1958. Feeding habits of the yellow-tail, Seriola quinqueradiata T. & S., caught in Wakasa Bay, the Japan Sea, based on its stomach contents: II. Daily change of feeding activity and variation in feeding activity with its growth. Bull. Jpn. Soc. Sci. Fish. 24, 182 – 185 (in Japanese, with English abstract). Oshima, I., Ebihara, S., 1987. The measurement and analysis of circadian locomotor activity and body temperature rhythms by a computer-based system. Physiol. Behav. 43, 115 – 119. Rozin, P., Mayer, J., 1961. Regulation of food intake in the goldfish. Am. J. Physiol. 201, 968 – 974. Sa´nchez-Va´zquez, F.J., Tabata, M., 1998. Circadian rhythms of demand-feeding and locomotor activity in rainbow trout. J. Fish Biol. 52, 255 – 267. Sa´nchez-Va´zquez, F.J., Martı´nez, M., Zamora, S., Madrid, J.A., 1994. Design and performance of an accurate demand feeder for the study of feeding behaviour in sea bass, Dicentrarchus labrax L. Physiol. Behav. 56, 789 – 794. Sa´nchez-Va´zquez, F.J., Madrid, J.A., Zamora, S., 1995. Circadian rhythms of feeding activity in sea bass, Dicentrarchus labrax L.: dual phasing capacity of diel demand-feeding pattern. J. Biol. Rhythms 10, 256 – 266. Sa´nchez-Va´zquez, F.J., Madrid, J.A., Zamora, S., Iigo, M., Tabata, M., 1996. Demand feeding and locomotor circadian rhythms in the goldfish, Carassius auratus: dual and independent phasing. Physiol. Behav. 60, 665 – 674. Sa´nchez-Va´zquez, F.J., Azzaydi, M., Martinez, F.J., Zamora, S., Madrid, J.A., 1998a. Annual rhythms of demand-feeding activity in sea bass: evidence of a seasonal phase inversion of the diel feeding pattern. Chronobiol. Int. 15, 607 – 622. Sa´nchez-Va´zquez, F.J., Yamamoto, T., Akiyama, T., Madrid, J.A., Tabata, M., 1998b. Selection of macronutrients by goldfish operating self-feeders. Physiol. Behav. 65, 211 – 218. Sa´nchez-Va´zquez, F.J., Yamamoto, T., Akiyama, T., Madrid, J.A., Tabata, M., 1999. Macronutrient self-selection through demand-feeders in rainbow trout. Physiol. Behav. 66, 45 – 51. Takahashi, M., Murachi, S., Moriwaki, S., 1981a. A feeding device for fishes designed for experimental use. Bull. Jpn. Soc. Sci. Fish. 47, 1131 – 1134. Takahashi, M., Murachi, S., Sekitani, T., Moriwaki, S., Ogawa, T., 1981b. Formation of the ‘‘bobber up thrust response’’ for food-obtaining in bluegill sunfish Lepomis macrochirus. Bull. Jpn. Soc. Sci. Fish. 47, 1135 – 1140. Takahashi, M., Murachi, S., Moriwaki, S., Ogawa, S., 1984. The response level of bluegill sunfish, Lepomis macrochirus, to a demand feeder. Bull. Jpn. Soc. Sci. Fish. 50, 1475 – 1480. Tipping, J.M., Rathvon, R.L., Moore, S.T., 1986. Use of demand feeders in large steelhead rearing ponds. Prog. Fish-Cult. 48, 303 – 304. Yamamoto, T., Shima, T., Furuita, H., Shiraishi, M., Sa´nchez-Va´zquez, F.J., Tabata, M., 2000. Self-selection of diets with different amino acid profiles by rainbow trout (Oncorhynchus mykiss). Aquaculture 187, 375 – 386.