Nippon Suisan Gakkaishi 59(5), 745-751 (1993)

Red and White Muscle Activity of the Jack Mackerel Trachurus japonicus During Swimming

Gang Xu,*1,2 Takafumi Arimoto,*1 and Makoto Inoue*1 (Received June 26, 1992)

In order to examine the functions of the red and white muscle of jack mackerel Trachurus japonicus during swimming locomotion, the fish was dissected to observe muscle distribution along the body. The electrical activity of the lateral muscle was analyzed using an electrophysiological technique. The ratio of red muscle to total muscle in a transverse section of the fish body reached a maximum at a position between 55% and 65% of fork length from the snout. The red and white muscles accounted for 5.1% and 61% of the body weight respectively. The white muscle was 12 times as heavy as the red muscle. In the electromyographic observations, the red muscle was active in sustained swimming at low speeds, whereas there was no electrical activity from the white muscle at speeds below 108cm/s for fish of 17.8cm in fork length. The bursts of discharge ap pearing in the electromyograph were measured for three components: frequency, amplitude, and duration. The frequency increased in proportion to swimming speed in both muscles. The tendency for the amplitude to increase with swimming speed was much more re markable in the red muscle than in the white muscle. The duration in the red muscle decreased, whereas in the white muscle it rose with the swimming speed. The results indicate that for jack mackerel only the red muscle is used in sustained swimming, while the white muscle is used during burst swimming above a threshold speed of 6.4BL/s, together with red muscle.

In most fishes the mytomal Iocomotor mus than in the white muscle.3-6) There are only culature is made up of two main fibre types, a few research works with respect to the functions i.s. red and white muscle fibres.1) The red of the red and white muscles and how fish use them muscle is commonly found as a thin superficial relative to swimming speed.3,7-8) In this report, layer below the skin in some species such as the jack mackerel Trachurus japonicus, an im the sardine and the herring, whereas Scombridae portant commercial species in Japan, was utilized such as the skipjack Katsuwonus pelamis have as a experimental species. The relationship a large amount of deep red muscle.2) The ratio between muscle activity and swimming speed was of red muscle to white muscle has been con examined using electrophysiological techniques. sidered to be one of the factors related to the Muscle distribution along the fish body was ecological and locomotor properties of fish. also investigated in relation to swimming locomo There is general agreement that at low sustained tion. swimming speeds only the red muscle is employed and that the white muscle is active only during Materials and Methods burst of high speed, which cannot be sustained for longer periods.1) Histochemical studies in One group of jack mackerel Trachurusjaponicus dicate that the red and white muscles are different 17.4 to 22.0cm in fork length were caught in from each other with regard to innervation and Tomiura Bay., Chiba Prefecture by angling, biochemical characteristics. Observations with while another group 27.8 to 30.8cm in fork an electromicroscope show that more vasa and length were purchased from a fish farm. The mitochondria ara distributed in the red muscle fish used were held at the Banda Marine Labora-

*1 Faculty of Fisheries, Tokyo University of Fisheries, Konan, Minato, Tokyo 108, Japan (•™•@•„,—LŒ³‹M•¶,ˆä•ã•@ŽÀ:“Œ‹ž•…ŽY‘åŠw•…ŽYŠw•”).

*2 Present address: Fisheries and Marine Institute of Memorial University of Newfoundland, St.

John's, Newfoundland, Canada AIC 5R3 (Œ»•Z•Š:ƒJƒiƒ_ƒjƒ…•[ƒtƒ@ƒ“ƒhƒ‰ƒ“ƒh‹L”O‘åŠw). tory of Tokyo University of Fisheries in a 2•~1•~ of six specimens were calculated using Obatake &

1m tank with circulated water at about 18•Ž for Heya's method. That is, at first the muscle volume

a week before the experiments from April to July was calculated by integrating the areas, and then 1989. the specific gravity of 1.05 was multiplied by the

In order to investigate the distribution of red volume. One specimen of 21.8cm was immersed and white muscles, ten specimens of 18.5 to 30.8 in hot water at 60•Ž for 5 minutes and then

cm were used. Each was cut into eight round skinned so that the myotomes could be observed slices such that the transverse sectional area of from the lateral view. each round slice could be measured. The meas The bipolar electrode shown in Fig. I was made

uring procedure was as follows: the specimens of enamel-insulated stainless steel wires (MT

were killed by anaesthetizing with solution MS222 Giken) of 10mm in length and 0.2mm in diameter. and then frozen at -15•Ž for 3 hours. The The insulation was removed 1mm from its two specimens which were frozen into a moderate tips, which were separated by 1mm. The in

hardness and a straight body shape were cut at sulated copper wires of an XBT probe were used

seven points 25, 35, 45, 55, 65, 75, 85% of fork as leads to connect with the ends of the electrode,

l ength (L) starting from the snout. All the trans which was cemented with a syrup of perspex in verse sections were recorded using a still camer chloroform and had dimensions of 10mm in

(Canon, AE-1; Microlens, 50mm). The areas l ength and 1mm in diameter, weighing 0.5g. of red and white muscles in each transverse Under anaesthesia with MS222 solution (100

section were read by digitizing the photograph ppm), the implantation of electrods was carried using a digitizer (Graphtec, KD4300) and analyzed out. A pair of electrodes were implanted into

and calculated by a microcomputer (NEC, the lateral muscle of either the same or of different PC9801). Obatake and Heya9) estimated the weight types. To prevent the electrodes from vibrating

of both red and white muscles, based on the as a result of fish body movements, the leads were measurements of muscle area in the transverse sewn and fixed on the base of the second dorsal

section along the fish body. The specific gravities fin.

of the red and white muscles for the jack mackerel A small flume tank (Fig. 2) was designed to were obtained and found to be similar at 1.05. 9) allow fish to swim stably in its test section of The muscle weight and proportion for a total 70•~ 30•~20 can against the flow at differentFig. 1. Bipolar electrode used for the electromyographic measurements.

Fig. 2. Diagram of the electrophysiological apparatus and a small scale flume tank. Fig. 3. Lateral and transverse section views of a fish body, showing the distribution of red and white muscles. velocities up to 185cm/s. This flume tank Results provided a constant flow in the most portions of the test section, except areas within 2.5cm Muscle Distribution of each wall. After the implantation, the fish The muscle distribution could be observed were moved into the flume tank for recovery and clearly as shown in Fig. 3. In lateral views, the then acclimated at 20cm/s for 15 minutes. The superficial red muscle began at a position just electrophysiological apparatus consisted of a posterior to the operculum extending towards 2-channel high sensitivity amplifier (Nippon the tail along the lateral line and ended in the last Koden, AB-632J) with a filter and a 2-channel caudal spine. The myotomes were M-shaped digital storage oscilloscope (Iwatsu, DS-6612C), and locked into each other. The red muscle with a memory card (128KB) for recording and became thinner towards both dorsal and ventral analyzing data. In addition, two video cameras sides where it overlaid the white muscle much (Sony, CCD-V90) were used to simultaneously more thinly than in the vicinity of horizontal record the fish body movements and electro septum. The maximum width of the red muscle myographs from an oscilloscope. occurred at a position of 48%L from the snout. The amplifier was set at a sensitivity range of In the transverse section, most of the red muscle 0.1mv and the filter at a band width of 43 to was observed to be distributed in the superficial 1000Hz. Altogether ten specimens of 17.4 to layer. Some red muscle which was different from 20.7cm, weighing 70 to 122g, were examined. the deep red muscle found in the skipjack pene The flow velocity was set at several levels increas trated a deep layer near the vertebra. The areas ing from an initial level of 47cm/s to a maximum of red and white muscles in each transverse section of 154.3cm/s. Electromyographic recording was were obtained from specimens of 18.5 to 18.6 done at each flow velocity where steady swimming cm (Fig. 4). The maximum area of red muscle was maintained for more than 5 minutes. Here, was found between 55%L and 65%L, whereas the swimming speed of the fish was considered that of white muscle was between 35%L and to be equal to the flow velocity of the flume tank. 45%L. The area of white muscle decreased After each trial, the fish was dissected to determine quickly behind the 55%L position. However, the exact position of the electrode in the muscle. in the vertical direction along the fish body there Table 1. Weight of the red and white muscles and their ratios

is- Fig. 5. Electromyograms from red muscles on both sides of the fish body. The fish is 19cm long in fork length and is swimming at a speed of 93 cm/s.

Fig. 4. The transverse section area (At), red muscle area (Ar) and white muscle area (Aw) dependent on longitudinal position for fish of 18.5 to 18.6cm in fork length. were no great changes in the area of red muscle. The red muscle was distributed more evenly than the white muscle. On average, the red and white muscles accounted for 5.1% and 61% of the body weight, and the ratios of red and white muscle to total muscle were 7.7% and 92.3% respectively (Table 1). Therefore, it was found that the white muscle was 12 times greater in weight than the red muscle.

Muscle Activities Based on the results of dissection and video recordings of fish swimming locomotion, it was found not only that there was more red muscle but also that the fish body vibration was greatest around the 60%L position. All the electro myographs were derived from a pair of electrodes imbedded in the lateral muscle at the 60%L position during steady swimming. The electrical activity of lateral muscle on both sides of the fish body was simultaneously observed Fig. 6. Electromyograms from both red and and recorded as electromyograms while the white muscles at different swimming speeds fish were swimming. Alternating bursts of d for fish of 17.8cm in fork length . Fig. 7. A sequence of video recordings showing the electromyographs and swimming locomotions for fish of 17.8cm in fork length which was swimming at speed of 123.7cm/s. W: white muscle on the left side of the fish body. R: red muscle on the right side of the fish body. charge in the red muscle from one side to the other speed. There were differences in the threshold appeared with regularity (Fig. 5). The frequency speed among individuals with different body of discharge bursts in the red muscle increased sizes and electrode position inside the muscle. in proportion to the swimming speed, and coincid For individuals whose white muscle activity was ed with that of the tail beats, as was observed detected by the electrodes, the initial electro and analyzed from the video recordings. The myograms of white muscle appeared between red muscle was active over the whole range of 93cm/s and 124cm/s, or 5.5 to 7.2 body lengths swimming speed tested. However, no electrical per second (BL/s) of swimming speed with a mean activity was detected in the white muscle when value of 6.25•}0.62BL/s. In the case of fish the fish was swimming at lower speeds (Fig. 6). of 17.8cm in fork length, the threshold speed was The video recordings showed clearly that the ap considered to be between 93cm/s (5.8BL/s) and pearance of each discharge burst in either the red 108cm/s (6.7BL/s) (Fig. 6). or the white muscle was exactly in accordance In order to examine three major components with the bending of the fish body (Fig. 7). The of the discharge burst, i.e. frequency, amplitude, white muscle became active when the swimming and duration (Fig. 8), each of the discharge bursts speed increased over a certain level of threshold was enlarged on the oscilloscope and each com- s it increased in the white musde, The ffeque ncy, amplitude, and duration of the discharge burst s in rel ation to swimming speed are shwon in Fig. 9 for fishof 17.8cm in fork length.

Discussion

The electromyographic results obtained from the jack mackerel are in agreement with those of the pacific herring Clupea harengus pallasi1) and yellowtail Seriola quinqueradiata8)in terms of Fig. 8. Enlarged bursts of discharge from red red and white muscles functions during swimming. and white muscles, defining the amplitude and duration. Generally speaking for the jack mackerel, the red muscle plays an important role in sustained swim ming. The white muscle is used only when the fish is struggling or swimming rapidly at high speeds. The lateral musculature of the jack mackerel seems to consist of two types of muscle fibres, i. e. red and white muscle fibres. There is no evidence in our anatomical observations to show that an intermediate type of muscle between the red and white muscles, (i. e. pink muscle) exists. However, pink muscle has been found in rainbow trout Salmo gairdneri and carp Cyprinus carpio, and its electrical activity begins at higher sustained speeds. 1, 7) The muscular structure of the jack mackerel is likely to be very similar to that of the pacific herring without the pink muscle. Muscle distribution was investigated in detail for different transverse sections along the fish body. The ratio of red muscle to total muscle was estimated to be 7.7%, close to the value of 8.6% measured by Obatake and Heya. 9) In a transverse section at 65%L which corresponds to a position of one-third of the fish length from the tail, there is a maximal red muscle with a ratio of 12.8% to total muscle in the jack mackerel. For Scomber scombrus, Clupea harengus, and Trachurus trachurus, Greer-Walker and Pull10) Fig. 9. Variations of the frequency, amplitude, determined the ratios of red muscle to tota and duration of discharge bursts with swim l muscle at the position of one-third of fish length ming speed. and obtained values of 18.8%, 15.2%, and 18.3% respectively. Since the jack mackerel used was ponent was measured. Generally, the frequency about 18cm in fork length, much smaller than increased linearly with swimming speed and was those (about 30cm long) used by Greer-Walker & higher in the red muscle than in the white muscle Pull, a comparison between the two species is within the range of swimming speed tested. not simple. The growth stage and/or preparation The amplitude in the red muscle increased with of materials should be considered as a key factor the swimming speed, while there was little change which causes discrepancies . in the white muscle in swimming above the thresh Webb11) described fish swimming locomotion old speed. As the swimming speed increased, in three levels of swimming activities: sustained , the duration in the red muscle decreased, wherea prolonged, and burst. According to the results of an endurance test for the jack mackerel, 12) power output from the whole white muscle is the fish were able to swim for more than 200 in excess of that from the whole red muscle. minutes at sustained speeds below 6.2BL/s of These facts are in agreement with the findings maximum sustained speed. When cruising at for the yellowtail, 13) and indicate that the white prolonged speeds of over 6.2BL/s, the fish would muscle supplies most of the energy required gradually become exhausted and would finally during rapid swimming at high speeds. fail to swim continuously, while at burst speeds above 11BL/s the fish could swim for only a few Acknowledgements seconds. The jack mackerel threshold speed of 5.8-6.7BL/s (intermediate value: 6.4BL/s) We are grateful to Dr. Pingguo He for his for fish of 17.8cm in fork length was very close technical advice on the fabrication of electrodes to the maximum sustained speed of 6.2BL/s and to Mr. Barry McCallum and Dr. Joseph A. measured in the endurance test for the same species Brown for their kind inspection of the manuscript. of similar size. 12) It was proved electrophysiolo Thanks are also due to Drs. Makoto Suzuki, gically that the white muscle was used in rapid Haruyuki Kanehiro, Toshiyuki Hirano, professors swimming at high speeds, while the red muscle of Tokyo University of Fisheries, as well as to was used for sustained swimming. In the pacific Taiyo Fishery Co. Ltd. for the scholarship sup herring, the threshold speed is found to be 5BL/s, 1) port to the first author during the course of close to that of the jack mackerel. But the the study. rainbow trout and the yellowtail have threshold speeds of 2BL/s1) and 1.8BL/S8) respectively, References which are lower than those of the jack mackerel and the pacific herring. We believe that the di 1) Q. Bone, J. Kiceniuk,and D. R. Jone: On the role of the dif ferent fibre types in fish myotomesat intermediate swimming screpancies in threshold speed among species speeds. Fish. Bull., 76, 691-699 (1978). is due to the differences in species, growth stage, 2) M. D. Rayner and M. J. Keenan: Role of red and whit and experimental apparatus. e muscles in the swimming of the skipjack tuna. Nature, 214, 392-393(1967). Tsukamoto13) suggested for yellowtail that the 3) Q. Bone: One the function of the two types of myotomal work for a burst was obtained from the product muscle fibrein elasmobranch fish. J. Mar. Biol. Assoc. UK, of the maximum amplitude (A) and the square 46, 321-349 (1966). 4) R. C. L. Hudson: Polyneuronal innervation of the fast of the duration (D2) of the burst of discharge, muscles of the marine teleost Cottus scorpius L.. J. Exp. and the relative power (P) derived from n bursts Biol., 50, 47-67 (1969). for a period of T seconds was given by; 5) S. Patterson, I. A. Johnston, and G. Goldskink: A histo chemical study of the lateral muscles of five teleost species. J. Fish Biol., 7, 159-166(1975). P•åƒÎƒ°i=1Ai•EDi2/T (1) 6) K. Shindo, T. Tsuchiya, and J. Matsumoto: Histological study on white and dark muscles of various fishes. Nippon Suisan Gakkaishi,52, 1377-1399(1986). Assuming that our electromyographic data suit 7) R. C. L. Hudson: On the function of the white muscles in the above formula (1), we calculated the power teleosts at intermediate swimming speeds. J. Exp. Biol., output of the jack mackerel during swimming 58, 509-522 (1973). 8) K. Tsukamoto: The role of the red and white muscles based on amplitude, duration, and frequency during swimming of the yellowtail. Nippon Suisan Gak (=1/T) observed in this study. The power kaishi, 50, 2025-2030(1984a). output per unit of red muscle is estimated to be 9) A. Obatake and H. Heya: A rapid method to measure dark muscle content in fish. Nippon Suisan Gakkaishi,51, 1001- greater than that per unit of white muscle within 1004 (1985)(in Japanese). the experimental speeds. For example, the P 10) M. Greer-Walker and G. A. Pull: A survey of red and white muscle in marine fish. J. Fish Biol., 7, 295-300(1975). of the red muscle was 6.9ƒÊv•Es, while that of the 11) P. W. Webb: Hydrodynamics and energetics of fish pro white muscle was 0.7ƒÊv•Es at 108cm/s. As the pulsion. Bull. Fish. Res. Bd. Can., 190, 1-158 (1979). swimming speed increased to 154cm/s, the P 12) G. Xu: Study on the swimming behaviour of fish and its application to the trawl gear. Doctoral thesis, Tokyo Uni of the white muscle jumped to 4.0ƒÊv•Es, but that versityof Fisheries,Tokyo, 1989,pp. 1-231(in Japanese). of the red muscle was almost unchanged (6.8 13) K. Tsukamoto: Contribution of the red and white muscles ƒÊv•E s). Since the white muscle weighs 12 times to the power output required for swimmingby the yellowtail. NipponSuisan Gakkaishi,50, 2031-2042(1984b). as much as the red muscle, consequently the total

Nippon Suisan Gakkaishi: Formerly Bull. Japan. Soc. Sci. Fish.