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Fisheries Science ISSN 0919-9268Volume 80Number 6 Fish Sci (2014) 80:1241-1248DOI 10.1007/s12562-014-0811-1

Temperature effect on heart rate of jackmackerel Trachurus japonicus duringswimming exercise

Mochammad Riyanto & TakafumiArimoto

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ORIGINAL ARTICLE Biology

Temperature effect on heart rate of jack mackerel Trachurusjaponicus during swimming exercise

Mochammad Riyanto • Takafumi Arimoto

Received: 21 April 2014 / Accepted: 26 August 2014 / Published online: 18 September 2014

� Japanese Society of Fisheries Science 2014

Abstract The heart rate of jack mackerel [16.5–21.2 cm

fork length (FL), n = 24] was examined through forced

swimming exercise in a flume tank by 10-min step-ups of

speed levels in 1.5–6.0 FL/s range at different temperatures

of 10, 15, and 22 �C. Electrocardiograph (ECG) monitor-

ing was conducted by comparing the heartbeat pattern in

still water without flow as a control, and continuously

during exercise by speed levels until fatigue and during the

recovery phase. Average heart rates in the control at each

temperature were 36.5 beats/min at 10 �C, 56.1 beats/min

at 15 �C, and 75.2 beats/min at 22 �C. The heart rate of

jack mackerel significantly increased as the swimming

speed was increased in each temperature. At the lower

swimming speed of 1.5–2.4 FL/s, the heart rate was the

same level as the control value at each respective tem-

perature. The heart rate started to increase at swimming

speeds of 2.3–2.5 FL/s at all temperatures. The higher heart

rate in the range of 150–200 beats/min was achieved at a

swimming speed of 6.0 FL/s at 22 �C. The recovery time

after the maximum heart rate at high speed became longer

at high temperatures.

Keywords Jack mackerel � Heart rate � Temperature

effect � ECG � Swimming exercise � Recovery time

Introduction

Temperature can be considered the most important factor

affecting the swimming performance of fish [1]. The

effects of temperature change on swimming performance

have been examined through acclimated temperature

change [2, 3] or by acutely introduced change [4, 5]. Both

acute and acclimatory increases in temperature have been

shown to improve swimming performance by enhancing

metabolic rates [6], cardiac performance [7, 8], fish

movement [9], and muscle contractility [10, 11]. Low

temperature and forced swimming exercise significantly

affected the muscle contraction time, which indicated a

reduction of performance of the maximum swimming

speed [12]. Nofrizal et al. [13] reported that lower swim-

ming performance is observed in jack mackerel at a tem-

perature of 10 �C, with increasing trends of heart rate

performance at higher temperatures.

Heart rate is an important factor for the respiratory and

metabolic system of fish during swimming [14]. Previous

studies on the heart rate during swimming exercise have

demonstrated that heart rate activities increase in relation

to the swimming exercise level during step-up speed level

experiments [15–18]. However, the effect of the physio-

logical condition after exhaustion from swimming exercise

on the heart rate by post-exercise monitoring have not been

fully examined. Heart rate has been used as an indicator of

the level of fatigue in relation to swimming endurance and

during the post-exercise period [13]. The heart rate can be

used as a relative index to quantify the physiological

condition of the fish during swimming exercise and an

encounter with mobile fishing gear and the exhaustion level

after hard exercise from the capture process. In the present

study, the heart rate was measured in comparison with the

control phase, the forced swimming exercise by speed level

M. Riyanto � T. Arimoto (&)

Graduate School of Applied Marine Bio-sciences, Tokyo

University of Marine Science and Technology, Minato-ku,

Tokyo 108-8477, Japan

e-mail: tarimoto@kaiyodai.ac.jp

M. Riyanto

Faculty of Fisheries and Marine Sciences, Bogor Agricultural

University, Kampus IPB Dramaga, Bogor 16680, Indonesia

123

Fish Sci (2014) 80:1241–1248

DOI 10.1007/s12562-014-0811-1

Author's personal copy

step-up protocol, and the post-recovery response in dif-

ferent temperatures.

Materials and methods

The temperature effect on the heart rate of jack mackerel

during swimming exercise was examined at the Fish

Behavior Laboratory at Tokyo University of Marine Sci-

ence and Technology in April 2013 [fork length

(FL) = 17.9 ± 0.9 cm, n = 8 at 15 �C], August 2013

(FL = 19.1 ± 0.6 cm, n = 8 at 22 �C), and January 2014

(FL = 17.9 ± 1.5 cm, n = 8 at 10 �C).

Experimental fish

Jack mackerel were obtained from a local fish farmer in

Numazu Bay, Shizuoka Prefecture, Japan, every 3 months

between March and November 2013, for 50 individuals

respectively, in order to avoid the effect of holding period

to the physiological conditions of the fish. The fish were

kept in a rectangular holding tank of 200 cm long, 90 cm

wide, and 100 cm deep, with the aeration and bio-filtering

circulation system at a temperature of 17 ± 0.6 �C and

salinity 32.5–33.5 psu. Each sample fish was acclimated

for a minimum of 10 days, prior to the swimming trial

experiment at designated temperatures of 10, 15, and

22 �C. The fish were fed commercial fish meal pellets

(Nippon Formula Feed Manufacturing Co., Ltd.) every day

during both the acclimation and experimental periods.

Heart rate monitoring in swimming exercise

and post-exercise

The heart rate of jack mackerel during swimming exercise

was monitored using an electrocardiography (ECG) tech-

nique with a similar protocol as a previous paper [12] in the

flume tank (West Japan Fluid Engineering Laboratory, PT-

70) with a swimming channel of 70 cm long, 30 cm

wide, 30 cm deep. A pair of electrodes for ECG mea-

surements was implanted in the pericardial cavity by pin-

inserting from the ventral side, under anesthesia with

80 ppm (0.008 %) solution of 4-Allyl-2-methoxy phenol

(Tanabe Seiyaku Co., Ltd., FA100) for 10–15 min. The

electrodes were made of enamel-insulated stainless wire

(MT Giken) of 15 mm in length and 0.25 mm in diameter.

A 1-mm length of wire insulation was exposed to serve as

an electrode for the bipolar leads. The electrodes were

connected with insulated copper wire cable (Tsurumi Seiki,

T-GA XBT cable) to deliver the heartbeat signal. The other

end of the wire cable was connected to a digital oscillo-

scope (Iwatsu, DS-5102) via a bio-amplifier (Nihon Koh-

den, Bio-electric Amplifier AB-632 J). To prevent

electrode vibration due to body movement, the pin posi-

tions of the electrodes were covered by super glue (Aron

Alpha, Toa-gosei), then the wire cable was sutured to the

base of second dorsal fin using the procedure described in

previous papers on ECG measurement protocol [19–21]. A

schematic diagram of the ECG recording in the flume tank

is shown in Fig. 1.

After the implantation of the electrodes and the recovery

phase for 180 min from anesthesia, the heart rate was

monitored for a subsequent 30 min adaptation to the still-

water and slow-flow (14.2 cm/s) conditions, then each fish

was forced to swim at given speeds ranging from 14.2 to

142.5 cm/s. The flow speed was elevated in increments of

14.2 cm/s in every 10 min until the fish reached fatigue

[12, 22], when the fish could not counteract the increase in

the flow speed and came into contact with the downstream

screen mesh and stopped swimming [12].

The increment ratio of heart rate during exercise was

analyzed by the relative heart rate for each individual. The

relative heart rate is the average of heart rate during

exercise divided with the average heart rate in control.

When the relative heart rate is close to 1, there was no large

difference in heart rate between the swimming exercise and

control phases [21].

The display screen of the oscilloscope was set to show a

period of 12 s in one screen-scanning, hence to integrate 5

screens enabled for estimation of the heart rate per 1 min.

Heart rate per minute was recorded for the entire experi-

ment period for the control in still water and during the

forced swimming exercise. In final moment of swimming

trial at high flow speed, fish could not continue the steady

tail beating so as to perform the kick-and-glide maneuver

[11, 12] until stopping to swim against flow. The data

collection during the post-exercise recovery phase was

conducted after the fish stopped swimming and was con-

tinuously monitored until the heart rate was stabilized to

the maximum level of the control, which was defined as the

full recovery time of heart rate. The recovery data were

analyzed by the moving average with 10-min intervals [13,

21] as shown in Fig. 2. The recovery time data according to

the maximum swimming speed for each individual were

compared among the different temperatures of 10, 15, and

22 �C. The effect of temperature on heart rate during the

control and swimming exercise were tested by analysis of

variance (ANOVA) for each individual at different tem-

perature. The statistical significance level was set at

P \ 0.01.

Results

Figure 2 shows an example record of ECG pattern for the

control and swimming exercise, and recovery phases of a

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17.9 cm FL jack mackerel at 15 �C. The heart rate during

the control phase in this record was observed as 55 beats/

min, and gradually increased with increasing swimming

speed. The heartbeat patterns are also shown in Fig. 3 for

identifying the heart rate (beats/min) according to the

swimming speed level in FL/s. At the lower swimming

speeds of 1.6 and 2.4 FL/s, the heart rate was a similar

level to the control as 55 and 60 beats/min, respectively.

The heart rates started to increase at the swimming speed of

3.2 FL/s as 70 beats/min. The high heart rate was observed

at a swimming speed of 4.7 FL/s as 145 beats/min as

shown in Fig. 3. At the faster speed of 5.4 FL/s fish could

swim for only 4 min duration, and stopped swimming due

to exhaustion. Then, the full recovery time was analyzed

with 10 min moving average so as to estimate for requiring

approximately 300 min (Fig. 2).

Figure 4 shows the monitoring results of the heart rate

patterns for all individuals tested during the control and

swimming exercise at 10, 15, and 22 �C. Here, the swim-

ming speed (FL/s) is shown with the average fork length

for tested individuals at each temperature. The heart rates

in the control were 25–50 beats/min (36.5 ± 7.7, n = 8) at

Fig. 1 Schematic diagram of

the ECG recording during

swimming exercise in the flume

tank

Fig. 2 An example record of

heart rate during control and

swimming exercise at speed

levels of 1.6–5.4 FL/s and the

recovery analysis for the post-

exercise of a 17.9-cm FL jack

mackerel at 15 �C. Horizontal

dashed line is the maximum

heart rate of the control, solid

black line is heart rate in

exercise and grey line is the

heart rate in recovery phase with

strip black line as the moving

average in every 10-min

interval. a–f is the step-up speed

level shown in Fig. 3

Fish Sci (2014) 80:1241–1248 1243

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10 �C, which were significantly less frequent than

51–74.5 beats/min (56.1 ± 9.3, n = 8) at 15 �C, and

57–104 beats/min (75.2 ± 9.3 n = 8) at 22 �C (One way

ANOVA, P \ 0.01). In the lower temperature of 10 �C, a

high peak of the heart rate was observed in the range of

4.9–5.3 FL/s (Fig. 4a). A similar trend was observed at

15 �C, however, the high peak of heart rate was observed at

the higher swimming speed as 4.8–5.7 FL/s (Fig. 4b). High

heart rates were observed at 22 �C, while a high peak of the

heart rate was observed at swimming speeds of 5.2–6.0 FL/

s (Fig. 4c).

The effect of temperature and swimming exercise on

heart rate according to speed level is shown in Fig. 5. The

results for all fish used in this study showed a significant

increase in heart rate with the swimming speed, with higher

trends in higher temperature (regression analysis,

P \ 0.01). Heart rate varied considerably among tested

fish, while there were significant differences in heart rate

with increase of swimming speed (one way ANOVA,

P \ 0.01). For all temperatures, the heart rate during

swimming exercise was higher than the control phase,

while at the lower swimming speed of 1.5–1.7 FL/s the

heart rate was a similar level to the control at each tem-

perature. The heart rate started to increase at swimming

speeds of 2.3–2.5 FL/s at all temperature. The higher heart

rate in the range of 150–200 beats/min was achieved at a

swimming speed of 6.0 FL/s at 22 �C. The results in this

paper were compared with previous studies listed in

Table 1, for detail examination in the discussion.

The result of relative heart rate analysis is shown in

Fig. 6, for showing the gradual increase by step-up of

swimming speed levels for each individual for each tem-

perature. The heart rate at the high speed was observed in

the range of 1.6–2.8 times the heart rate in the control at 15

and 22 �C. However, for some individuals at 10 �C the

heart rate exceeded 3.0 times, due to the very low heart rate

at 25–50 beats/min in the control phase (Fig. 6a). A high

relative heart rate was observed at 10 �C, when the fish

were carried backward and touched the mesh screen, but

they could thrust themselves with kick-and-glide maneuver

with the high heart rate until swimming stopped at

4.8–5.0 FL/s. At a higher temperature of 22 �C, some

individuals showed a very low relative heart rate, due to the

heart rate in the control was already high as 100 beats/min

as shown in Fig. 6c.

Recovery time against peak heart rate at the maximum

speed during swimming exercise at different temperatures

of 10, 15, and 22 �C is shown in Fig. 7. Recovery time

tended to increase against the peak of heart rate at the high

speed. Recovery time for post-exercise at 22 �C was

256–480 min at the peak heart rate of 152–187 beats/min,

Fig. 3 Examples of heartbeat record patterns on the oscilloscope

display screen for 12 s, according to speed levels, for the case in

Fig. 2

Fig. 4 Changes in heart rate at different temperatures of 10, 15, and

22 �C in the control and during swimming exercise at speed levels

from 1.5–6.0 FL/s for every 10 min with the average fork length at

each temperature. Each connected line represents each individual

tested

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which show the different trends with lower temperature to

be much longer than 164–240 and 180–300 min at 10 and

15 �C, respectively.

Discussion

The heart rate pattern during swimming exercise in this

study supports previous findings by Priede [15] and

Nofrizal et al. [13]. Based on the result of ECG monitoring

of 17.9-cm jack mackerel at 15 �C in Fig. 2, we can

understand that the heart rate gradually increased with the

increase of swimming speed. However, the heart rate was

not increased at low speed. This indicates that the energy

cost of swimming was effectively metabolized to sustain

the same level of swimming speed level for an extended

period [13]. Fish consume extra energy in response to the

increased swimming speed, and is required to increase the

metabolic and respiratory process [23] in order to reform

the lost energy. Moreover, Korsmeyer et al. [24] stated that

the cardiorespiratory system has adjusted the elevation

demand of oxygen as velocity increases during step up

swimming by speed level.

The heart rate of jack mackerel in the present study did

not increase at low swimming speed for all temperatures,

where no big changes in heart rate were observed, as in

Fig. 6. The heart rate is related to cardiac work to supply

oxygen to the body, as increasing trend with faster swim-

ming [23]. Generally, the change of heart rate during

swimming exercise at the three different temperatures

showed variation among individuals as reported by Nofri-

zal et al. [13]; An and Arimoto [20]; and Ito et al. [21]. The

individual variability of the heart rate can be attributed to

factors due to either prior physical conditions or handling

stress through the experimental protocol. Some individuals

Fig. 5 Average heart rate (beats/min) change according to the

swimming speed U (FL/s) with the average fork length for tested

individuals at each water temperature of 10 �C (open triangles),

15 �C (filled-grey squares), and 22 �C (filled-black circles)

Table 1 Comparison of heart

rate measurements of fish

during swimming with the

present study on the jack

mackerel

a Data logging system in a tankb Fixed speed for examining the

endurance time

Species FL

(cm)

Temp

(�C)

Swimming speed

(FL/s)

Heart rate

(beats/min)

References

Carp Cyprinus carpio 12.3 23.3 1.0–5.0 50–114 Ito et al. [21]

Red sea bream Pagrus

major

54.6 27 1.0–4.6 60–115 Kojima et al. [26]a

Rainbow trout

Oncorhynchus mykiss

23–28.2 6.5 0.6–1.9 35–89.4 Pride [15]

Rainbow trout

Oncorhynchus mykiss

29.1 15 0.8–1.9 31.8–77.5 Altimiras and

Larsen [18]

Atlantic salmon Salmo

salar

50.7 15 1.0–2.0 60.3–81.3 Lucas [17]

Yellowtail Seriola

quinqueradiata

29.7–33 24 1.0–2.6 80–100 Hanyu et al. [16]

Skipjack Katsuwonus

pelamis

44.7 25 1.6 76.8 Bushnel and Brill

[27]

Kawakawa Eutynnus

affinis

46 25 1.3 128 Jones et al. [28]

Yellowfin tuna Thunnus

albacares

46.1 25 1.2 67.9 Bushnel and Brill

[27]

38.3 24 1.0–2.9 67.9–101.9 Korsmeyer et al.

[24]

Jack mackerel Trachurus

japonicus

18.5 10 1.1–8.6 20–60 Nofrizal et al.

[13]b18.5 15 1.1–8.6 70–125

18.5 22 1.1–8.6 115–208

Jack mackerel Trachurus

japonicus

17.9 10 1.6–5.9 29–124 Present study

17.9 15 1.6–5.9 45–165

19.1 22 1.6–5.9 60–212

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at 10 �C showed high heart rate values as 3–4 times of

heart rate in the control at the high swimming speeds of

4.8–5.0 FL/s, due to low heart rate in the control at low

temperature, similarly with the low muscle performance of

swimming [12], with the differences in metabolic rate at

given speed [25].

Previous studies measuring the heart rate of fish during

swimming are summarized in Table 1, for different tem-

peratures of 6.5–10 �C for cold-water species such as

rainbow trout [15, 18] and Atlantic salmon [17], up to

higher temperature conditions of 23.3–27 �C for species

such as carp [21], red sea bream [26], yellowtail [16],

skipjack [27], kawakawa [28] and yellowfin [24, 27], with

the variation in sizes of tested fish for each species. The

exercise levels were set either by the given flow speed in

the flume tank at a fixed speed or increment speeds with

step-up protocol, with only one case using the data logger

system for free swimming in a large tank. The different

experimental protocols can result in the differences of heart

rate change, while higher heart rate around 70–130 beats/

min was monitored for pelagic species in the higher tem-

peratures tested, even with the low speed levels of the

sustained swimming. The present study on jack mackerel

covered the wider speed range up to the prolonged level,

for monitoring the heart rate in a wider temperature range

of 10–22 �C.

Modern trawls vary in gear scales to allow different

types of fishing boats to tow them at a maximum speed

between 3 and 4 knots when using full power [29]. Those

speeds correspond to swimming speeds of 8.6–11.4 FL/s

for fish with an average FL of 18 cm used in this study.

Thus, fish swim at prolonged or burst swimming speed, to

avoid and escape during the capture process. The heart rate

at these speeds could be maximally beating, and the fish

may be under stress and tachycardia even if they could

escape from the gear. Chopin and Arimoto [30] stated that

the fish swimming in the trawl codend during the capture

process will be subjected to severe exercise. This may

evoke mortalities, which have been attributed to stress

associated with various capture stressors even if the fish

were able to escape successfully from capture. This study

demonstrated that the magnitude of the stress given to the

fish during exercise at more than 3 FL/s swimming speed

at different temperatures of 10, 15, and 22 �C was scaled

by heart rate activity. Endurance in fish swimming to

prolonged speed is limited by the heart function for blood

circulation pumping [31], a situation that most likely

happens during the capture process by mobile fishing gear.

Recovery time analysis for the post-exercise phase

shown in Fig. 7 revealed that the recovery time after high

heart rates at high speed at the high temperature of 22 �C is

longer than at the low temperature of 10 �C. At 22 �C fish

required from 250 to 480 min for post-exercise recovery

from swimming speeds of 1.6–5.9 FL/s for around 60 min

at the series of step-up speed levels. The recovery time for

jack mackerel in this result was much longer than carp at

20–60 min after swimming exercise of 1–5 BL/s at

23.4 �C [21]. The results of the present study are in

agreement with the previous results for the same species by

Nofrizal et al. [13], the longer endurance times at higher

temperatures completely exhausted the fish and require

longer recovery time. Swimming exercise in fish generally

Fig. 6 Relative heart rate during exercise for all tested fish according to the swimming speeds at different temperature of 10, 15, and 22 �C

Fig. 7 Recovery time for jack mackerel against peak heart rate at

maximum speed during swimming exercise

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involves the use of glycogen and adenosine triphosphate

(ATP) which are stored within the ordinary muscle [32].

During the recovery period, most of the lactic acid remains

in the fish muscle [33, 34] and is converted back to gly-

cogen without leaving the muscle cells [35]. Previous

studies have reported that recovery of the muscle lactate in

rainbow trout takes about 6–8 h [36], and the time required

for muscle glycogen re-synthesis also varies from 4–6 to as

much as 12 h [37]. The recovery of the heart rate of jack

mackerel in this paper was 4.2–8.0 h, which suggests that

the heart rate can be a key fatigue indicator related to

swimming activities, and thus requires further examination

of the muscle activity performance according to the

swimming speed and exercise levels.

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