© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Direct measurement of the swimming speed, tailbeat, and body angle of Japanese flounder (Paralichthys olivaceus)
a Graduate School of Fisheries Sciences, Hokkaido University Minato 3-1-1, Hakodate 041-8611, Japan
b National Institute of Polar Research Kaga 1-9-10, Itabashi, Tokyo 173-8515, Japan
c Field Science Center for the Northern Biosphere, Hokkaido University Minato 3-1-1, Hakodate 041-8611, Japan
*Correspondence to R. Kawabe: tel: +81 95 819 2803; fax: +81 95 819 2799. e-mail: kawabe{at}net.nagasaki-u.ac.jp.
It is well known that flatfish species such as plaice can utilize the selective tidal stream to conduct vertical movements. However, detailed description of actual swimming behaviour is lacking, principally as a result of the difficulties encountered in monitoring the behaviour of flatfish in the open sea. The present study describes the use of a newly developed data-logger in obtaining simultaneous recordings of the swimming speed, depth, tailbeat, and body angle of free-ranging Japanese flounder (Paralichthys olivaceus) in the open sea. Our data indicate that Japanese flounders adopt a tailbeat-and-glide behaviour. They are found to glide downward without tailbeats for propulsion, and only during the ascent phase are tailbeats conducted. Flounders move horizontally at speeds of 0.59–1.23 km d–1 and at a maximum speed of 0.70–0.82 km h–1 in the open sea. Modal flounder swimming speeds are 30–40 cm s–1 (0.57–0.76 and 0.58–0.77 BL s–1), i.e. sometimes lower than the threshold of the speed sensor. In most cases, however, tailbeat oscillations occur at frequencies of 1.2–1.4 Hz. Moreover, flounders travel at a significantly steeper angle during the ascent phase than during the descent phase. In both cases it is believed that flounder optimize the energetic costs of migration, as has been shown for tuna, sharks, and seals.
Keywords: acceleration, beat-and-glide behaviour, body angle, Japanese flounder, swimming speed, tailbeat frequency, vertical movement
Received 16 March 2003; accepted 26 May 2004.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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The Japanese flounder (Paralichthys olivaceus) is widely distributed along the coastal shelf of Japan, where it is a commercially and ecologically important flatfish in the coastal waters of marine ecosystems in this area. In general, both morphological and physical features render flatfish highly adapted to a benthic mode of life (Greer-Walker and Pull, 1975; Webb, 1989). Roundfish such as tuna, which make yearly migrations of thousands of kilometres, are continuous swimmers with numerous specializations required to achieve a high aerobic scope (see review in Korsmeyer et al., 1996). Duthie (1982), however, suggested that the white muscle of flatfish operates anaerobically at moderate speeds, and suggested that flatfish could not swim continuously. Previously, conventional tagging experiments have indicated that Japanese flounders sometimes migrate over long distances, i.e. up to 50–100 km (rarely over 1000 km) (Takeno and Hamanaka, 1994; Minami, 1997; Tominaga and Watanabe, 1998). How, then, can Japanese flounders move over such long distances when their swimming capability has been suggested to be lower than that for some roundfish?
It is well known that aquatic animals use a variety of strategies to reduce the cost of locomotion (Weihs, 1973, 1978; Videler and Weihs, 1982; Holland et al., 1990; Williams et al., 2000). Previous conventional mark–recapture and ultrasonic tagging studies of plaice (Pleuronectes platessa) have indicated the general pattern of adult plaice in the Southern Bight of the North Sea and the English Channel (Harden Jones, 1968; Houghton and Harding, 1976), and that their migrations are made by selective tidal-stream transport in order to maximize energy efficiency (Greer-Walker et al., 1978; Metcalfe et al., 1993; Metcalfe and Arnold, 1997). On the other hand, Weihs (1973) demonstrated, theoretically, that tailbeat-and-glide behaviour in fish with negative buoyancy, such as flatfish and tuna, reduces the energy required for locomotion between two points. In addition, Holland et al. (1990) demonstrated that tuna periodically move in an oscillatory style, consisting of a tailbeat-and-glide pattern. However, because of the difficulties in studying free-ranging fish in the open ocean, a detailed description of the swimming behaviour (swimming speed and body angle) of flatfish during vertical movements has not still to be produced.
In attempting to fill the gap in our knowledge, we made use of recent advances in data-logging technology. These loggers can record body movement and body angle through two accelerometer signals (acceleration data-logger), and are developed and deployed on a variety of free-ranging aquatic animals. Using this acceleration data-logger, Kawabe et al. (2003a) developed a new technique for monitoring the behaviour of free-ranging flatfish. They showed that an acceleration profile could be used to detect fine-scale movements (lying on the seabed, swimming (i.e. tail-beating), gliding, and burying). In this study, the first direct measurement of swimming speed, tailbeat activity, and body angle of free-ranging flatfish using acceleration data-loggers is presented. The results are discussed with respect to the behaviour of flatfish during vertical movement and in relation to their physiological and morphological features.
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Material and methods |
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Field experiment
During October and November 2000, the swimming behaviour of adult Japanese flounder (Paralichthys olivaceus) was studied off the coast of the Tsugaru Strait in the southern part of Hokkaido Island, Japan (Figure 1). In all, 24 flounders were caught in set-nets or by hook in the Kikonai Bay and transferred to the Shiriuchi Fisheries Cooperative Society located on the coast of the Tsugaru Strait. The flounders were then kept in a circular holding tank (5 x 5 m length, 0.5 m depth). Water temperature in the tank was maintained at ambient ocean temperature (approximately 14°C); natural light cycles were also simulated. Ten of the flounders were selected for tagging. The flounders marked with the logger were released on three different occasions: three with a PD2G logger on 21 October, one with a PD2G logger on 28 October, and one with a PD2G logger and five with a PD2GT logger on 11 November 2000 (Figure 1).
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Data-logger
Two types of data-logger (Little Leonard Co. Ltd., Tokyo, Japan) were used on Japanese flounder to illustrate their potential without reference to the type of accelerometers. The PD2G logger (UWE200-PD2G: 20 mm diameter, 120 mm length; 64 g in air and 22 g in seawater) was used to record swimming speed and depth at 1-s intervals, and 2-dimensional acceleration (for determining body movement and body angle) at 1/16-s and 1/4-s intervals. The PD2GT logger (W-190L-PD2GT: 21 mm diameter, 117 mm length; 60 g in air and 22 g in seawater) was used to record swimming speed at 0.5-s intervals, depth at 1-s intervals, 2-dimensional acceleration (for determining body movement and body angle) at 1/16-s and 1/4-s intervals, and temperature at 30-s intervals. The logger uses a two-axis acceleration sensor (PD2G: Model 3031, IC Sensors, Inc., Fairfield, NJ, USA; PD2GT: Model ADXL210, Analog Devices, Inc., Norwood, USA). The sensors can measure both dynamic acceleration (such as propulsive activities) and static acceleration (such as gravity), which means that it can be used as a tilt sensor. The measuring range of the accelerometer (PD2G) is ±39.2 m s–2, with a resolution of 0.02 m s–2; the measuring range of the other sensor (PD2GT) is ±49 m s–2, with a resolution of 0.02 m s–2. Both loggers are cylindrical in shape and have 16 megabytes (PD2G) or 64 megabytes (PD2GT) of flash memory. Depth resolution is 0.05 m; the maximum depth that could be measured was 190 m. Swimming speed, not as ‘over ground’ but ‘through water’, is measured by counting the number of revolutions per second (RPS) of an anteriorly mounted propeller (Tanaka et al., 2001; Kawabe et al., 2003a, b). The stall speeds of the speed sensor were determined experimentally to be 26.5 cm s–1 (PD2G) and 11.0 cm s–1 (PD2GT). Speeds below these values were considered indistinguishable from zero. A regression line was used to relate RPS to swimming speed. To calibrate the speed sensor, we examined the relationship between RPS and flow velocity (cm s–1) in a water tunnel. The relationship was linear from 26.5 to 120.0 cm s–1 for the PD2G logger and from 11.0 to 120.0 cm s–1 for the PD2GT logger; the coefficient of determination (r) for both loggers was greater than 0.99. Previous studies have demonstrated that tailbeat frequency (TBF) can be related to swimming speed (e.g. Bainbridge, 1958). We, too, found that TBF of the flounder was found to increase linearly with increased swimming speed (Kawabe et al., 2003a, b). Using these relationships, we were able to estimate the speed below the threshold.
Acceleration data analysis
We attached the PD2G, which includes a Model 3031, IC Sensors accelerometer, or the PD2GT logger, with an accelerometer Model ADXL210, Analog Devices, to free-ranging adult flounders in order to record movements in two directions: surging acceleration (body angle) along the longitudinal body axis of the flounder (forward and backward) and heaving acceleration (tailbeat) along the axis crossing the fish's body from the eyed (upward facing) side to the blind (downward facing) side (Figure 2).
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= angle of ascent/descent.Heaving acceleration often contained low-frequency variations that were assumed to be the result of various turning and rolling movements. These variations were separated using a 0.1-Hz highpass filter (IFDL Version 3.1; WaveMetrics, Inc., Lake Oswego, OR, USA). The remaining peaks and troughs with absolute amplitudes greater than 0.5 m s–2 were considered to be tailbeats and used in analyses. Peak–trough and trough–peak duration corresponds to one tailbeat stroke (i.e. upward-to-downward and downward-to-upward; see Kawabe et al. 2003a, b, for detailed information). The acceleration sensor along the longitudinal axis of the body measured surging acceleration, which is affected by both the forward movements of the animal and gravity (Tanaka et al., 2001; Yoda et al., 2001; Sato et al., 2003). High-frequency variations in surging acceleration are believed to be caused by body movements and were filtered out using a 0.1-Hz low-pass filter (IFDL Version 3.1; WaveMetrics, Inc., Lake Oswego, OR, USA). As described by Tanaka et al. (2001), when the animal is still or moving at a constant speed, the gravity vector will change in response to body angle. Together, these vectors were used to calculate the body angle. Figure 2 shows the direction of the surging acceleration recorded by a PD2G or PD2GT logger attached to the back of a flounder. A descending flounder would have surging accelerations and body angles represented as negative values. Body angles and surging accelerations during ascent were positive. To re-adjust the horizontal level, we corrected the values of body angle recorded in the holding tank to 0° when the instrumented flounder lay on the bottom of the holding tank.
After retrieving the logger, the data were downloaded onto a laptop computer and analyzed using Igor Pro 3.1.4 software (WaveMetrics, Lake Oswego, OR, USA). The data were analyzed to statistical significance using StatView 4.5 software (SAS Institute, Cary, NC, USA). All values are presented as mean ± standard deviation (s.d.) and p < 0.05 was used to indicate statistically significant differences.
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Results |
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General behaviour of the flounder
Two tagged flounders (Flounder #A with PD2G logger and Flounder #B with PD2GT logger) were retrieved by commercial fishers. They had been caught in a trapnet. One flounder (Flounder #A) was recaptured close to the seabed, the other (Flounder #B) close to the surface (see Figure 1). Flounder #A was recaptured within about 1 km of the release point, while Flounder #B was recaptured about 6 km away from the release point. Table 1 gives the length, weight, recording duration, swimming speed, and tailbeat frequency for each of the two recaptured fish.
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The instrumented flounder began swimming down to the seabed immediately after being released into the sea. Figure 3a shows the entire swimming speed, tailbeat frequency, body angle, and depth data for Flounder #B in the open sea, as well as a 26-min sequence from that record shown on an expanded time scale (Figure 3b). Kawabe et al. (2003a) showed that the acceleration data-loggers can distinguish between "active" (tail-beating and burying) and "inactive" behaviour (gliding and lying on the seabed), using acceleration, speed, and depth data (see Kawabe et al., 2003a, Figure 4, for detailed information). Using this method, we estimated that the flounder spent most of the time of recording (Flounder #A, 95.3%; Flounder #B, 97.5%) on the seabed. Although rare, 208 swimming behaviour events were recorded in total from two flounders off the seabed. According to the tailbeat profile (as shown in Figure 3b), the flounders adopted "tailbeat-and-glide" behaviour throughout their vertical movements (n = 71). Their tailbeats were only substantial during ascent, gliding from peak of depth profile through their descent until reaching a given depth or the seabed (Figure 3b). This beat-and-glide behaviour is defined by intermittent strokes and corresponding fluctuations in swimming speed. On the other hand, an example of the typical profiles of "only beat" (continuous tailbeat) of the instrumented flounder is demonstrated by the data recorded from Flounder #A (Figure 3c; n = 137). Tailbeats were substantial until the flounder reached the seabed (Figure 3c). Flounder moved horizontally in the open sea at mean speeds of 0.59–1.23 km d–1 (Table 1) and had a maximum speed of 0.70–0.82 km h–1.
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Frequency distributions of swimming speed for two of the instrumented flounders are shown in Figure 4. Modal swimming speeds of two flounders were 30–40 cm s–1 (0.57–0.76 and 0.58–0.77 BL s–1, where BL is body length), which sometimes moved below the threshold of the speed sensor (Table 1). Mean swimming speeds for two instrumented flounders ranged from 30.3 ± 12.7 to 31.6 ± 15.3 cm s–1 (0.58 ± 0.24 to 0.61 ± 0.30 BL s–1). The distribution of swimming speeds showed a broad peak, suggesting that the flounders had two ranges of preferred speeds, namely 30–40 cm s–1 and below 20 cm s–1. However, distributions of tailbeat frequency for two of the instrumented flounders showed a narrow peak, suggesting that the flounders had a narrow range of preferred tailbeat frequencies of 1.2–1.4 Hz (Figure 5). Mean tailbeat frequencies for two instrumented flounders ranged from 1.47 ± 0.34 Hz to 1.49 ± 0.30 Hz. The flounders rarely swam at frequencies greater than 4.0 Hz.
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In general, the flounders maintained their body axis within an angle of between –20° and +40°. The frequency distribution of body angle for two instrumented flounders is shown in Figure 6 and clearly shows a bimodal distribution having two peaks on the negative and positive side, with two modal ranges of –4° to –6° and +4° to +10°. The negative side of the distribution was steeper than the positive side, although the positive side was relatively smooth.
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Comparison between the descent and ascent phases
To facilitate our analysis, data sets were chosen for which changes in depth during ascent and descent, after swimming up from the seabed, were greater than 2 m (as shown in Figure 3b). A total of 139 ascents and descents were recorded from two instrumented flounders. Table 2 summarizes duration, vertical rate, swimming speed, tailbeat frequency, and body angle of the ascents and descents for both recaptured flounders. There were significant differences in all of these behavioural variables between the ascent and descent phases (Mann–Whitney U test). The duration during ascents (45.5 ± 34.6 s for Flounder A and 38.5 ± 28.0 s for Flounder B) was significantly longer and swimming speeds (35.4 ± 7.5 cm s–1 for Flounder A and 34.1 ± 8.0 cm s–1 for Flounder B) significantly faster than for descents (12.4 ± 10.5 s for Flounder A and 22.5 ± 25.9 s for Flounder B; 34.1 ± 8.1 cm s–1 for Flounder A and 26.5 ± 7.6 cm s–1 for Flounder B). Moreover, flounders swam at a significantly steeper angle during ascent (12.9 ± 6.5° for Flounder A and 12.7 ± 7.6° for Flounder B) than during descent (–5.5 ± 4.9° for Flounder A and –5.8 ± 3.0° for Flounder B). However, the vertical descent rate (11.9 ± 6.9 cm s–1 for Flounder A and 8.4 ± 2.1 cm s–1 for Flounder B) was significantly faster than the vertical ascent phase (6.7 ± 3.6 cm s–1 for Flounder A and 7.5 ± 2.9 cm s–1 for Flounder B).
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Discussion |
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First, we briefly comment on the behaviour and locomotion of swimming individuals and the effects of data-logger attachment. Tag attachments can adversely affect fish, thus biasing the field data of their movement and behaviour. In particular, the attachment of external devices to fish and other marine vertebrates can affect their swimming speed because of increased hydrodynamic drag (Mellas and Haynes, 1985; Bannasch et al., 1994). We had to use the external attachment because our data-logger included a speed sensor. However, we could detect no differences in swimming speed and tailbeat frequency between instrumented and uninstrumented individuals (Kawabe et al., 2003a). Tanaka et al. (2001) suggested that migrating adult chum salmon fitted with the data-logger, using the external attachment, retain their homing motivation and maintain horizontal movement. It is therefore likely that our instrumented flounders retain their swimming performance and behaviour in the open sea.
Our results show that the mean ascent duration of two retrieved flounders after swimming up from the seabed was about 40 s. In previous studies of flatfish and other fish using data storage tags, the tags were programmed to measure over 5 min (Metcalfe and Arnold, 1997; Righton and Metcalfe, 2002; Solmundsson et al., 2003). We could not monitor ascent duration and rate, tailbeat frequency, or body angle since we were to adopt a lower sampling rate by the acceleration data-logger. Thus, high-frequency sampling using the acceleration data-logger is necessary if the vertical movement of Japanese flounder and other fish is to be quantified accurately. Our results may not help us to understand the general behaviour of Japanese flounder because of being based on just two individuals over a brief time period.
Williams et al. (2000) demonstrated that the energy-conservation strategy (prolonged gliding behaviour) allows diving marine mammals to increase aerobic dive duration and achieve remarkable depths despite limited oxygen availability when submerged. Moreover, Greer-Walker et al. (1978) demonstrated that plaice swam off the seabed, moved downstream with the tide in midwater, and returned to the seabed at the next slack water. Metcalfe et al. (1990) suggested, theoretically, that selective tidal-stream transport of plaice appeared to be energetically one of the most effective mechanisms of fish migration. Although Japanese flounder also made vertical movements, we could not examine whether they used the selective tidal stream or not. However, we believe our study on Paralichthys olivaceus to be the first to demonstrate a precise tailbeat profile that flatfish adopt during intermittent swimming (tailbeat-and-glide) behaviour in open sea, by using electronic tagging technology.
Previous calculations of the cost of locomotion on flatfish have indicated that the most economical speeds might occur at higher than the critical speeds (above 0.95–1.50 BL s–1) (Priede and Holliday, 1980; Duthie, 1982). However, the modal range of swimming speeds of two Japanese flounders in our results was lower (0.57–0.77 BL s–1) than the economical speed. How could our flounder swim at lower speeds than the sustained, and the optimum and maximum sustained speed that Duthie (1982) calculated? There are two possible reasons. Duthie (1982) reported that the elevated lactic acid levels in flounder white muscle indicated that it was operating anaerobically at moderate speeds (0.5 BL s–1). This suggests that flounder might need to avoid lactic acid accumulation as far as possible, with the exception of burst swimming associated with prey capture and escape. Another reason could be that flounder prefer swimming speeds lower than the maximum sustained speeds that have been recorded in some experimental flumes (Priede and Holliday, 1980; Duthie, 1982; Hashimoto et al., 1996), which suggests that slow swimming may be a way to minimize the cost of locomotion over long distances (Block et al., 1992).
The probable reason why Japanese flounder adopt tailbeat-and-glide behaviour during vertical movement is as a way to reduce the cost of locomotion (Weihs, 1973). As shown in Figure 3b, our results indicate clearly that flounders glide downwards without using tailbeats for propulsion during the descent phase; their tailbeats are limited to the ascent phase. The frequency distribution of body angles of flounder clearly showed a bimodal distribution, having two peaks, both negative and positive. The positive part of the distribution would be the swimming angle and the negative part the gliding angle. Tanaka et al. (2001) demonstrated that chum salmon during their homing migration in coastal waters descended at faster rates and steeper angles than they ascended, and tailbeat frequency and thrust were higher during the ascent phase than during the descent, because salmon could not regulate the volume of air in their swimbladder. Our results during the ascent and descent phase are similar to those of their study. Our data thus suggest that negative buoyancy, i.e. having no swimbladder, could allow flounder to descend with lower energy cost of locomotion than for the ascent phase. Another reason for adopting the tailbeat-and-glide behaviour when making vertical movement may be associated with metabolic recovery in Japanese flounder. As mentioned above, our data suggest that the white muscle of flounder operates anaerobically at their swimming speed during the ascent phase (Duthie, 1982). Flounder always therefore need to recover the oxygen debt, alternating with resting periods on the seabed. Milligan et al. (2000) reported that sustained swimming at low speed following a bout of exhaustive exercise enhanced metabolic recovery in rainbow trout and, as a result, muscle glycogen was completely resynthesized and lactate cleared within 2 h of exercise in swimming fish compared with more than 6 h required in the case of fish held in still water. This suggests that migration adopting intermittent gliding behaviour instead of sustained swimming at low speed should recover the oxygen debt more quickly than continuous swimming, after returning from midwater to the seabed.
Although tailbeat-and-glide behaviour of marine fish with negative buoyancy has been hypothesized to result in a saving of energy required for locomotion between two points, there have been no studies directly testing this hypothesis in the wild. In future research, we will compare the migrating energy costs (using tailbeat numbers) during continuous swim and tailbeat-and-glide behaviour directly. This method could be used to monitor the behaviour and activities not just of flatfish, but also of marine and freshwater fish (Tanaka et al., 2001; Kawabe et al., 2003a). The overall design of this logger offers high flexibility in the study of different marine animals (Sato et al., 2003) and enables the behaviour of the animal to be analyzed precisely in its natural environment.
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Acknowledgements |
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We thank all the fishers who kindly recovered the loggers, T. Mishima of the Shiriuchi Town Office, K. Akiyama and C. Ishiyama of Shiriuchi Fisherman's Association, T. Kawano, N. Yoshiura, N. Nakano, S. Torisawa, Y. Ioki, and T. Suga for their field assistance, K. Nashimoto, A. Kato, and H. Muramoto for their efficient cooperation, and two anonymous referees for constructive criticism of our manuscript. This study was supported by Grants-in-Aid from the Japan Society for the Promotion of Science (nos. 12660157 and 15255003).
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References |
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