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Tide-induced changes in marine fish cage-shape cause changes in swimming behavior of cultured chub mackerel (Scomber japonicus)

Tide-induced changes in marine fish cage-shape cause changes in swimming behavior of cultured... We performed field measurements of the behavioral changes in cultured chub mackerel (Scomber japonicus) caused by tide-induced changes in the shapes of their small-sized tetragonal fish cages. The field measurements were conducted in two separate periods: neap tide, a period in which the shape of the fish cages was stable; and spring tide, a period in which the fish cages are significantly deformed, which was expected to have significant influences on fish behavior. In the spring tide, the cages were deformed greatly by the moving water, with different water velocities affecting the cages to different degrees; the volume loss was estimated at 4.9% and 7.3% for v = 0.114 m/ s and v = 0.221 m/s, respectively. The fish exhibited significantly different behaviors between the neap tide and spring tide. During the neap tide, the fish remained in the lower part of the cage, but during the spring tide they made frequent upward and downward movements, and their horizontal distribution changed significantly due to the changes in the shape of the cage. The cage deformation during the spring tide greatly influenced the swimming behavior of fish. Keywords: Acoustic positioning system, Aquaculture, Fish cage deformation, Fish behavior, Fish welfare Introduction 2004). In addition, an appropriate amount of sinking One continuous sea surface fish culture technique, mar- force (weight) is applied to maintain the shape and vol- ine cage culture, is conducted for many commercially ume of the cage, that is, to keep the structure and cap- valuable fish. In a marine cage aquaculture system, the acity of the cage as stable as possible. mechanical stability of the cage and the maintenance of Despite of these efforts, a marine cage system cannot a stable feeding environment are the most important avoid the influences of the tide and waves, and the entire factors, and thus, are the most basic conditions to be cage system continuously faces the tidal force, and so, considered at the time of the manufacture and installa- the shape of the cage net continuously changes. tion of the cage system. The marine cage facility should Such cage deformation greatly reduces farming cap- be installed in a hydraulically stable semi-enclosed acity (Lader et al. 2008; Gui et al. 2006); this decrease in coastal and inner bay area where the waves and currents cage space leads to decreased swimming space and in- are weak, in order to avoid damage and loss of facilities creased stress in the cultured fish, which leads to growth from strong currents or waves (Anras and Lagardère depression (Conte 2004). In addition, high-density farm- ing may lead to wounds in the fish due to collisions be- tween cultured fish or between fish and the cage net; * Correspondence: jihoon.lee@jnu.ac.kr 2 such injuries may considerably affect the health of the Department of Marine Porduction of Management, Chonnam National University, 50 Daehak-ro, Yeosu 59626, Korea cultured fish, leading to disease or even death. Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 2 of 12 Furthermore, cage deformation affects the natural circu- do, South Korea. The coastal area of Tongyoung has lation of seawater into and out of the cage, which means Korea’s most developed marine cage culture system, and that oxygen is not smoothly supplied to the cage; this, in a number of culture facilities are installed there. turn, greatly affects the growth and pathogenesis of the The shape of the cage system and the layout of the fish. equipment used in the experiment are shown in Fig. 1. Studies on marine cage systems have mainly been con- This facility contains a large cage system maintained for ducted to evaluate the stability of the cage by analyzing research and development of coastal marine resources; the changes in the shape of the cage net. Researchers cages of various sizes are attached to one another and have performed studies using scale-down models of fish are connected with a plastic structure. The cage system cages to investigate their stability and shape changes is installed in a manner such that one side of the tetrag- caused by the tide and waves; recently, it has become onal cage is parallel to 330° (left side in Fig. 1). possible to estimate these changes using computer simu- A radio-linked acoustic positioning system (VRAP, lations (Kim et al. 2001a; Kim et al. 2001b; Lee et al. Vemco Ltd., Canada) and recording current meter 2015; Lee et al. 2008; Bi et al. 2015; Zhao et al. 2015; Lee (RCM-9, Aanderaa, Norway) were used to observe the et al. 2017). In addition, there are numerous methods to swimming behavior of the cultured chub mackerel assess the behavior and change in volume of real cage (Scomber japonicus) in the cage. The VRAP is an under- nets using recent advances in underwater measurement water position measurement system that uses an LBL technology; examples of this technology include high- (long baseline) method, which consists of three sea sta- precision pressure sensors (Lader et al. 2008) and under- tions and one base station. Each sea station, in this water ultrasonic position measurement systems (Hwang study, was a buoy (RAP buoy) loaded with an omnidirec- and Shin 2003; Tae and Shin 2006; Miyamoto et al. tional hydrophone and installed on the sea surface; it re- 2006; Lee et al. 2017). ceived signals from transmitters. The base station How fish respond to the behavior of the cage net is controlled each sea station using a VHF modem; it re- also an important area of research. The effects of cage ceived data from the sea stations and processed the data. deformation on the fish are not well known, although To measure the current speed, direction, water there have been some studies on the behavioral charac- temperature, cloudiness, and conductivity, a recording teristics of salmon in cages (Juell and Westerberg 1993; current meter was installed 5 m below the water surface Cubitt et al. 2005; Johansson et al. 2014). It is necessary outside of the cage; it recorded every 5 min. to understand the effects that the changes in the shape The shape of the cage and the positions of the ultra- of cages have on fish behavior, and to, subsequently, sonic transmitters (P1–P8) attached to the cage, which minimize these effects. The influence of coastal environ- were the targets of the experiment, are shown in Fig. 2. mental pollution has increased in recent years as fish The cage for the experiment was a small fish culture cages have been installed further out to sea. In particu- cage, the type most commonly used along the Korean lar, it is necessary to pay attention to the change in the coast. Its shape was a cube, 6 m × 6 m × 6 m (L × W × swimming behavior of cultured fish according to the D), which is adequate for the chub mackerel housed in changes in the shape of the cage because the cage cul- it. The cage was made of polyethylene net with a mesh ture technique is used for tuna, a high value-added fish size of 30 mm and a mesh diameter of 2 mm, and each that swims at a relatively high speed. corner of the cage was tied with a rope having a sinker Recently, mackerel has gained popularity for consump- (W1–W4) weighing 15 kg and connected to the cage to tion as raw fish in Korea, and thus, has attracted atten- minimize tide- and wave-induced cage deformation. tion as a high value-added species of increasingly good Typically, in the VRAP system, as the number of quality. In neighboring Japan, mackerel is also receiving transmitters to be measured increases, greater inter- attention as an important aquaculture species. ference occurs between signals according to different In this study, we observed the changes in the shape of transmission periods of the transmitters. Therefore, marine cage nets due to the tide, using a 3D underwater the number of transmitters that can be used simul- position measurement system, and examined the taneously is theoretically limited to ten (Jørgensen changes in the swimming behavior of the mackerel to in- et al. 2007). A total of eight multi-purpose transmit- vestigate and analyze how fish cage deformation affects ters (V16-6H, Amirix Systems Inc., Canada) were the behavioral characteristics of cultured fish. used to record the movement of the cage. The trans- mitters were 95 mm × 16 mm (L × D) in size and Materials and methods weighed 34 g. The transmitters were attached to the Experimental area and system setup bottom of the cage (at a depth of 6 m), and the Field experiments were conducted at a marine cage facil- remaining four were attached to the center of each ity in the coastal area of Tongyoung in Gyeongsangnam- cage wall (at a depth of 3 m). Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 3 of 12 Fig. 1 Experimental setup of radio-linked acoustic positioning system and recording current meter at the marine cage system of the Marine Research Center, Tongyoung, South Korea In addition, an implantable transmitter (V9P-2H, three fish could swim. The transmitters used in the ex- Amirix Systems Inc.) was used to observe the swimming periments have the interval for saving data with 3 min behavior of chub mackerel within the cage. This tiny owing to signal interference from other transmitters. transmitter, just 47 mm × 9 mm and 4.7 g, has a pressure sensor that allowed measurement of the depth at which Experiment and data analysis the fish swim. The transmitter was surgically implanted First, the positional coordinates of the transmitters at- in the peritoneal cavity of a fish. First, a fish was anes- tached to the cage were used to estimate the movement thetized. Next, its abdominal cavity was opened. Then, of the cage sides and internal volume loss of the cage. an ultrasonic transmitter was inserted, and the fish was The shape of the cage was measured by the positions of sutured closed. After the operation, the experimental the transmitters at the stand of tide (current speed less fish was allowed to recover in a recovery tank and subse- than 0.01 m/s), which were estimated by approximating quently released in the experimental cage. Two add- the displacement of each part according to current itional mackerel, without transmitters, were also placed speed. At this point, the x and y coordinate values, in the experimental cage. Fish typically detect up to four which reflect the displacement of the sides of the cage, neighbors or objects and accordingly determine their were received from VRAP, and the water depth coordin- swimming direction based on their relative positions ate value, z, was obtained by estimating the interior (Aoki 1982; Huth and Wissel 1992; Shinchi et al. 2002), angle between the reference point of each side and its placing only a minimum number of fellow fish allowed present location based on the origin of the water the experimental fish to freely swim within the entire surface. space of the cage without experiencing crowding. As a The internal volume loss of the cage was estimated by result, the positional coordinates received from the ex- applying the prismoidal formula (Brinker and Minnick perimental fish reflected the cage space within which all 1995), a method to calculate volumes of polygonal Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 4 of 12 Fig. 2 Schematic diagram of the experimental cage, the position of ultrasonic transmitter attached to the cage (P1-P8), and 15-kg sinkers (W ~W ) 1 4 Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 5 of 12 columns. This formula is a simple method of calculating circadian activity rhythms of the fish based on the the total volume that uses the cross-sectional area of change in duration and intensity of light. both ends and the area of the central cross-section when the side is flat. It was convenient to estimate the volume Results change of the cage using the positions of the eight trans- Characteristics of the tide in the experimental sea area mitters attached to the cage. To calculate the volume of Changes in the current direction and speed of the tide the cage, the cage was divided into upper and lower vol- on November 7 (neap tide) and December 12 (spring umes at the 3-m point, and each volume was assumed to tide), 2017, are shown in Fig. 5. The main axis of the tide be a polygonal column. Assuming the cross-sectional was NNW–SSE. The tide with the fastest current speed areas of the polygonal columns to be A and A , the flowed in the directions of about 330° and 130° during U L center cross-section between A and A to be A , and the neap tide, as shown in Fig. 3a and about 340° and U L m the distance between both sides to be L, the each volume 140° during the spring tide, as shown in Fig. 3b. The was estimated by current direction was stable when flowing NNW but volatile when flowing SSE. As shown in Fig. 1, the main axis of the current was almost parallel to one plane of 1 the cage and perpendicular to the other plane because V ¼ LAðÞ þ 4A þ A ð1Þ U m L one side of the cage was installed in the direction of 330° (150°). where A is the top area of the upper polygonal col- The frequencies of extremely slow current speed (0.01 umn, A is the bottom area of the lower polygonal col- m/s), indicating the stand of tide, were 24.6% and 16.7% umn, and A is the middle area of the polygonal for the neap tide and spring tide, respectively. The max- column. imum instantaneous speed of the neap tide was 0.122 m/ In the case of actual fishing nets, the sides of a net s in the NNW direction (329.0°) and 0.122 m/s in the generally form a smooth surface when the net is moved, SSE direction (128.0°), whereas the maximum instantan- as by waves; however, the sides of the net were assumed eous current speed of the spring tide was 0.244 m/s in to be flat in the volume calculation. the NNW direction (344.6°) and 0.274 m/s in the SSE The swimming behavior of the fish in the cage was es- direction (148.0°). Thus, the maximum instantaneous timated by correlating the coordinates (x, y, z) of the fish current speed in the spring tide was about 2.2 times received from VRAP with fish cage deformation caused higher than that in the neap tide. The current speed by tide, and the horizontal and the vertical movements exhibiting the maximum frequency in the neap tide was of the fish. We also analyzed the change in the depth at 0.02 m/s (14.1%) and that in the spring tide was 0.03 m/s which the fish swam during the neap tide and the spring (11.1%), which were similar to each other; however, tide by day and night to investigate the patterns of 32.6% of current speed in the spring tide exceeded the Fig. 3 Changes in the current direction and current speed of the tide during the a neap tide (on November 7, 2016) and b spring tide (December 12, 2016) Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 6 of 12 maximum instantaneous speed in the neap tide. From direction that most affected cage deformation was stable. these results, it can be concluded that the environmental Figure 4 a depicts the cage shape at the stand of tide, conditions of the two experimental days were very dif- showing that there was hardly any influence by the tide, ferent because the current speed distributions between while Fig. 4b shows the shape of the cage at the max- the two experimental days showed significant imum current speed in the neap tide; the arrow below differences. the cage represents current direction. As the current speed increased, the net surface perpendicular to the Fish cage deformation and volume loss current direction encountered a large amount of fluid The three-dimensional cage deformation caused by the resistance and moved accordingly, which led to fish cage tide is illustrated in Fig. 4. The cage deformation was an- deformation; however, the shape of the net surface par- alyzed for the main axis (NNW) of the tide within a allel with the current direction did not change much. range of ± 15°, as shown Fig. 3, in which the current Each corner of the lower part of the cage showed less Fig. 4 Comparison of the fish cage deformation between neap tide and spring tide. a Stand of tide (neap tide). b Max. current speed to NNW (v = 0.111 m/s, D = 327.4°). c Stand of tide (spring tide). d Max. current speed to NNW (v = 0.221 m/s, D = 343.1°) Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 7 of 12 movement than did the net surface because of the sinker 2.2% at a current speed of 0.088 m/s, about 4.9% at (weight) at the lower part of the cage. The right corner, 0.111 m/s, and 5.8% at 0.155 m/s (the maximum current which received the current first, moved slightly more speed during the neap tide), whereas, it was 7.3% at the than did the left corner. Nevertheless, the shape of the maximum current speed of 0.221 m/s in the spring tide. cage did not exhibit considerable deformation, even with The cage was greatly deformed as the shape of the net the maximum current speed, in the neap tide. surface perpendicular to the current direction changed, Cage deformation in the spring tide is depicted in Fig. as shown in Fig. 4; however, it was inferred that there 4c and d, the former showing deformation during the was only a little internal volume loss owing to the stand of tide and the latter showing deformation at the sinkers attached to each corner of the cage to maintain maximum current speed. As seen in Fig. 4c, the shape of its shape. the cage at the stand of tide in the spring tide was simi- lar to that in the stand of tide in the neap tide (Fig. 4a), Changes in the swimming behavior of cultured fish but the cage was greatly deformed at the time of the The swimming behavior of chub mackerel was signifi- maximum current speed in the spring tide. Figure 4d cantly different between the neap tide and the spring shows that at the time of the maximum current speed, tide, as was the shape of the cage. The three- the center of the net perpendicular to the direction of dimensional underwater positions of the fish are shown the tide was greatly displaced. At this time, the net sur- in Fig. 6; Fig. 6a and b represents the distribution of the face parallel with the tide was slightly displaced as well. fish in the neap tide and in the spring tide, respectively. The lower right corner, moreover, had greater deform- The overall distribution pattern of the fish in Fig. 6a ation than the other corners, so, the shape of the cage during the neap tide shows that they moved closer to was entirely distorted from its original form of a tetrag- the water’s surface occasionally, but mostly stayed in the onal column (cube). The reason for this was that one lower part of the cage. The shape of the distribution side of the cage was in the direction of 330°, but the took the form of a discus, as the fish spent most of their current direction in the spring tide was about 344°, time in the lower part of the cage and swam in a circle. which means it flowed from the lower right to the upper This pattern verifies that the cultured chub mackerel in left at an angle of about 10°. As a result, it is inferred the cage shared characteristics of fish under regular con- that the fluid resistance at the lower right corner was ditions (Beveridge 2004). Thus, it is inferred that the cul- the largest. tured fish here exhibited relatively stable swimming The volume loss of the cage, as calculated by the pris- behavior in the cage during neap tide. moidal formula, at times of relatively stable current The shape of the distribution of the cultured fish in speed in the NNW direction, is shown in Fig. 5. Based the spring tide (Fig. 6b), however, showed a significantly on its shape at the stand of tide, the volume loss was different shape from that in the neap tide (Fig. 6a). The Fig. 5 Volume loss of cage caused by current speed (□ neap tide, ■ spring tide) Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 8 of 12 which led to an increased change in their swimming pattern. The results of the analysis of the three-dimensional distributions of the cultured fish by the current speed conducted to determine the effect of the cage deform- ation on their swimming behavior is represented in Fig. 7. Figure 7a shows the position distribution of the fish at the stand of tide in neap tide, in which it is assumed that the fish generally stayed below the depth of 4 m and swam across most of the horizontal area of the cage. The fish moved to the left because of cage deformation; however, they did not change their depth much and stayed in the lower part of the cage, at the time of the maximum current speed in the neap tide, as shown in Fig. 7b. Contrarily, the fish swam in the central part of the cage and frequently moved to the upper part of the cage, at the maximum current speed in the spring tide, as shown in in Fig. 7c. Such behavior occurred at current speeds of 0.14–0.16 m/s, in which the fish also moved to the right because of cage deformation, as shown in Fig. 7d. The swimming area of the fish moved further to the right at the maximum current speed in the spring tide as cage deformation increased, as shown in in Fig. 7e. At this time, they stayed mostly around the depth of 5 m. At these times, the fish appeared frequently in the cen- tral part of the left side, but did not appear in the bot- tom right side of the cage due to the severe cage deformation on the left net surface and the bottom right side of the cage, as shown in Fig. 4d. In conclusion, in the neap tide, the distribution of the cultured chub mackerel was mainly concentrated in deep water, near the lower part of the cage, and the cen- ter of the distribution shifted slightly to the right side Fig. 6 Comparison of the swimming space of the cultured chub owing to the slight cage deformation caused by the small mackerel between the neap tide and the spring tide. a Neap tide. b range of changes in the current speed. In the case of the Spring tide spring tide, however, the fish did not stay in the lower part of the cage even at the stand of tide; instead, they moved to other depths, where they had more space in position distribution pattern of the fish, which indicates which to swim freely, as the upper part of the cage was their swimming behavior, was not primarily near the significantly deformed. lower part of the cage in spring tide, unlike that in neap The changes in swimming depth over time in the neap tide, and took the form of a long discus in the direction tide and in the spring tide are depicted in Fig. 8.As of the x-axis. The reason for this is that the main axis of shown in Fig. 4, there was very little cage deformation the current was almost parallel with the x-axis, which during the neap tide; so, the changes in swimming depth limited and deformed the swimming area of the fish can be inferred to be fish reaction to light conditions owing to the displacement of the net surface perpen- within the cage. The mean swimming depth of the fish dicular to the current direction. It is inferred that the during the neap tide did not vary significantly between fish kept swimming aggressively to maintain their pos- day time (6.1 m), as shown in Fig. 8a, and night time ition against the fast current in the spring tide. These (5.9 m), as shown in Fig. 8b. The distribution of fish dur- factors prevented the fish from showing their stable ing the neap tide was identical between day and night, swimming behavior in the lower part of the cage as in and they were always concentrated in the lower part of the neap tide; instead, they frequently moved to areas the cage. During spring tide, the fish remained primarily near the surface of the sea, above the depth of 3 m, at a depth of 6.8 m during the day (Fig. 8c), deeper than Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 9 of 12 Fig. 7 Comparison of the swimming behavior of the cultured chub mackerel affected by cage deformation. a v < 0.1 m/s (stand of tide) in the neap tide. b v = 0.10–0.122 m/s in the neap tide. c v < 0.1 m/s (stand of tide) in the spring tide. d v = 0.14–0.16 m/s in the spring tide. e v = 0.2– 0.223 m/s in the spring tide that in neap tide. The fish showed relatively stable swim- considerably large cage deformation caused by the high ming depth, but occasionally moved upwards, to a depth current speed. In addition, the swimming distribution at of approximately 5 m. However, at night in spring tide, night time during the spring tide showed a significantly the fish tended to frequently move upwards toward the different shape (Fig. 8d). The mean swimming depth of surface of the sea (Fig. 8d). It can be inferred that the the fish at night during the spring tide was 3.7 m, and fish moved to a safer space because they could not stably they moved evenly between the depths of 1 m and 6 m. stay near the lower part of the cage owing to the In other words, their swimming was not concentrated at Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 10 of 12 Fig. 8 Comparison of swimming depth distribution during the neap and spring tide. a Neap tide/day. b Neap tide/night. c Spring tide/day. d Spring tide/night one specific depth. Thus, the fish did not show stable Our results indicate that cage deformation significantly swimming behavior at night in the spring tide, as op- affects the swimming behavior pattern of cultured chub posed to that in the neap tide. It is further inferred that mackerel. The fish generally swam in a circle in the neap they had to make frequent movements between the tide but moved to one side of the cage because of cage upper part and the lower part of the cage. Assuming that deformation in the spring tide. Moreover, the fish ap- the swimming depth at night in the neap tide is natural peared to make frequent movements to the upper and swimming behavior for fish in general, the behavior of lower parts of the cage in the spring tide; such changes the experimental fish was significantly affected by cage in the swimming depth were most pronounced at night deformation at night in the spring tide owing to the ex- in the spring tide. treme changes in the current speed and the cage sides The degree of cage deformation is affected by the dir- not being visible to the fish. ection of the current, waves, shape of the mesh and size In sum, the behavior of the cultured chub mackerel of the net, position and weight of the sinkers, and within the cage was limited by the shape of the cage. current speed. One study measured cage deformation They were not affected much by the minor cage deform- and calculated the volume loss due to the current using ation in the neap tide, in which the current speed was an underwater sensor; the volume loss of the cage was slow. However, the larger cage deformation in the spring 20% even at a low current speed of 0.2 m/s and up to tide appeared to affect their swimming behavior. This in- 40% at a current speed of 0.35 m/s (Lader et al. 2008). fluence was greater at night time, when their vision was Another study, on designing the shape of the sinkers at- limited. tached to the cage, showed that the volume loss of the cage was significant with current speeds greater than 0.2 Discussion m/s (Kim et al. 2001a). In our study, there was a volume Individual-based measurements enable us to understand loss of about 8% in the spring tide when the current the synchronous mechanisms by which fish cope with speed exceeded 0.2 m/s. The cage used in our study was environmental signals that cause changes in their behav- tetragonal (a cube), which was different from the shape ior in a production environment (Oppedal et al. 2011). of the cage used in the previous study (Lader et al. Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 11 of 12 2008). In addition, the sinkers attached to each corner system we used estimates the underwater position of an may have minimized cage deformation. At a low current object using the time delay of acoustic arrival, though speed, the fish generally showed very stable movement the accuracy varies based on the output level of the under the net in the cage. However, when the current transmitter or decreases and increases in signals (Baras speed increased, they tended to swim to the surface and Lagardere 1995). Previous studies show that the upon deformation of cage shape. This is believed to have VRAP system is accurate to about 1–2 m when a trans- increased the stress index of the fish, resulting in growth mitter station is installed using an anchor. Thus, such a and other adverse effects. The adverse effects of these system is unavoidably affected by the changes in baseline changes in behavior of the fish on the shape of the cage due to the movement of the station. In a previous study, have been discussed in other studies (Lader et al. 2008). we measured signals from a fixed transmitter attached to Moreover, although the volume loss was only 7.3%, the a cage in a quiet sea, in which the two-distance root impact on the fish caused by the volume loss is likely to mean square (2 drms) was 0.8 m (Tae and Shin 2006). be greater when considering the situation wherein large The standard deviations of the x-, y-, and z-axes were numbers of fish are farmed in the actual fish cage. 0.2, 0.4, and 1.0 m, respectively. The baseline in that ex- The cultured chub mackerel in the experimental cage periment was between 12 and 14 m, which was consider- generally swam in a circle during the day, while avoiding ably shorter than that in this study. the deep corners. Visual observation of highly populated Swimming area in a deformed cage is affected by vis- cages showed that they occasionally swim near the sur- ual stimulation (Ehrenberg and Steig 2003). Cage de- face; however, they usually swim near the lower part of formation affects the yield and health of the cultured the cage if there is enough space, as there was in this fish by reducing the space in which they can swim study. (Lader et al. 2008). In this study, we verified that cul- In our study, the fish mainly preferred the lower part tured chub mackerel frequently swam near the surface of the cage; however, they tended to swim at shallower of the water owing to cage deformation, and that they depths at night in the spring tide, when their vision was were hindered from stably resting and swimming be- limited. There were no significant changes in the water cause of limited space in the cage. In recent years, aqua- temperature, cloudiness, or conductivity by the measure- farms have begun moving to the open sea because of the ment, which could have influenced the swimming depth contamination of coastal water from cage-based fish cul- distribution of the fish, at the time of this field experi- ture (Kim et al. 2001b); therefore, cage deformation and ment. Thus, the vertical changes in the swimming depth changes in fish behavior due to the current speed are of the observed fish might have been caused by their cir- very important. With the new trend in the aquaculture cadian rhythm and deformation of the cage (Føre et al. industry, it is imperative to conduct in-depth studies on 2009; Johansson et al. 2014). the influences of current and waves on marine cages, Scale-down model experiments and simulations are and the fish reared in them. widely used to estimate fish cage deformation according to the design of the net. Survey experiments are impera- Conclusions tive to analyze the swimming behavior of the fish in The behavioral change in cultured fish according to these cages. Simultaneous observations of fish swimming changes in shapes of tetragonal small-sized fish cages behavior and measurements of cage deformation using a based on the tide was measured using the 3D under- current underwater telemetry system will require exten- water position measurement system and analyzed. The sive data collection over long durations. The transmit- swimming volume of the fish due to net deformation is ters used in the experiments have the interval for saving influenced by visual stimuli, and the net deformation af- data with 3 min owing to signal interference from other fects the yield and health of cultured fish by reducing transmitters. Even though the data collection interval the volume. Furthermore, fish are more likely to swim was not short, the fish continuously and repeatedly close to the water due to deformation of the net, and swam in an identical pattern in a small space, and the limited within the area where swimming is possible, thus shape of the cage did not rapidly change because of the confirming that the cultured fish are disturbed to stable current; so, the data was adequate to detect the pattern. rest and swimming. In recent years, since the waters oc- Since we were able to select several time periods with cupied by the cage aquaculture are becoming more pol- slight changes in the current, it was sufficient for us to luted and moving to the offshore, the shape changes of estimate the swimming area of the fish. the net and the behavior characteristics of the fish by In our results, the accuracy of the underwater telem- the flow rate will become more important. Regarding etry system was extremely important in verifying and the new trends of this aquaculture, it is necessary to in- evaluating the correlation between the changes in the vestigate in depth the relationship between the increas- current and cage deformation. The underwater telemetry ing influence of currents and waves on net and fish. Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 12 of 12 Acknowledgements Johansson D, Laursen F, Fernö A, Fosseidengen JE, Klebert P, Stein LH, Vagseth T, Not applicable Oppedal F. The interaction between water currents and salmon swimming behaviour in sea cages. Plos One. 2014;9:e97635. https://doi.org/10.1371/ journal.pone.0097635. Authors’ contributions Jørgensen T, Løkkeborg S, Fernö A, Hufthammer M. Walking speed and area BK Hwang carried out the field experiment and participated in drafted the utilization of red king crab (Paralithodes camtschaticus) introduced to the manuscript. J Lee analyzed the experimental data, participated in drafted, Baren Sea coastal ecosystem. Hydrobiologia. 2007;582:17–24. https://doi.org/ and finalized the manuscript. HO Shin carried out the field experiment. All 10.1007/978-1-4020-6237-7_3. authors read and approved the final manuscript. Juell JE, Westerberg H. An ultrasonic telemetric system for automatic positioning of individual fish used to track Atlantic salmon (Salmo salar L.) in a sea cage. Funding Aquacult Eng. 1993;12:1–18. https://doi.org/10.1016/0144-8609(93)90023-5. Not applicable Kim TH, Kim JO, Kim DA. 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Aquaculture. 2011;311:1–18. https://doi.org/ 10.1016/j.aquaculture.2010. 11.020. Received: 10 February 2020 Accepted: 30 March 2020 Shinchi T, Kitazoe T, Nishimura H, Tabuse M, Azuma N, Aoki I. Fractal evaluation of fish school movements in simulations and real observations. Artificial Life and Robotics. 2002;6:36–43. https://doi.org/10.1007/BF02481207. References Tae JW, Shin HO. Acoustic analysis of volume variation in a bag-net within a set- Anras MB, Lagardère JP. Measuring cultured fish swimming behavior: first results net. Fish Res. 2006;80:263–9. https://doi.org/10.1016/j.fishres.2006.03.030. on rainbow trout using acoustic telemetry in tanks. Aquaculture. 2004;240: Zhao YP, Wang XX, Decew J, Tsukrov I, Bai XD. Comparative study of two 175–86. https://doi.org/10.1016/j.aquaculture.2004.02.019. approaches to model the offshore fish cages. China Ocean Eng. 2015;29:– Aoki I. A simulation study on the schooling mechanism in fish. 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J Theor Biol. 1992;156:365–85. https://doi.org/10.1016/S0022-5193(05)80681-2. Hwang BK, Shin HO. Analysis on the movement of bag-net in set-net by acoustic telemetry techniques. Fish Sci. 2003;69:300–7. https://doi.org/10.1046/j.1444- 2906.2003.00621.x. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Fisheries and Aquatic Sciences Springer Journals

Tide-induced changes in marine fish cage-shape cause changes in swimming behavior of cultured chub mackerel (Scomber japonicus)

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Abstract

We performed field measurements of the behavioral changes in cultured chub mackerel (Scomber japonicus) caused by tide-induced changes in the shapes of their small-sized tetragonal fish cages. The field measurements were conducted in two separate periods: neap tide, a period in which the shape of the fish cages was stable; and spring tide, a period in which the fish cages are significantly deformed, which was expected to have significant influences on fish behavior. In the spring tide, the cages were deformed greatly by the moving water, with different water velocities affecting the cages to different degrees; the volume loss was estimated at 4.9% and 7.3% for v = 0.114 m/ s and v = 0.221 m/s, respectively. The fish exhibited significantly different behaviors between the neap tide and spring tide. During the neap tide, the fish remained in the lower part of the cage, but during the spring tide they made frequent upward and downward movements, and their horizontal distribution changed significantly due to the changes in the shape of the cage. The cage deformation during the spring tide greatly influenced the swimming behavior of fish. Keywords: Acoustic positioning system, Aquaculture, Fish cage deformation, Fish behavior, Fish welfare Introduction 2004). In addition, an appropriate amount of sinking One continuous sea surface fish culture technique, mar- force (weight) is applied to maintain the shape and vol- ine cage culture, is conducted for many commercially ume of the cage, that is, to keep the structure and cap- valuable fish. In a marine cage aquaculture system, the acity of the cage as stable as possible. mechanical stability of the cage and the maintenance of Despite of these efforts, a marine cage system cannot a stable feeding environment are the most important avoid the influences of the tide and waves, and the entire factors, and thus, are the most basic conditions to be cage system continuously faces the tidal force, and so, considered at the time of the manufacture and installa- the shape of the cage net continuously changes. tion of the cage system. The marine cage facility should Such cage deformation greatly reduces farming cap- be installed in a hydraulically stable semi-enclosed acity (Lader et al. 2008; Gui et al. 2006); this decrease in coastal and inner bay area where the waves and currents cage space leads to decreased swimming space and in- are weak, in order to avoid damage and loss of facilities creased stress in the cultured fish, which leads to growth from strong currents or waves (Anras and Lagardère depression (Conte 2004). In addition, high-density farm- ing may lead to wounds in the fish due to collisions be- tween cultured fish or between fish and the cage net; * Correspondence: jihoon.lee@jnu.ac.kr 2 such injuries may considerably affect the health of the Department of Marine Porduction of Management, Chonnam National University, 50 Daehak-ro, Yeosu 59626, Korea cultured fish, leading to disease or even death. Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 2 of 12 Furthermore, cage deformation affects the natural circu- do, South Korea. The coastal area of Tongyoung has lation of seawater into and out of the cage, which means Korea’s most developed marine cage culture system, and that oxygen is not smoothly supplied to the cage; this, in a number of culture facilities are installed there. turn, greatly affects the growth and pathogenesis of the The shape of the cage system and the layout of the fish. equipment used in the experiment are shown in Fig. 1. Studies on marine cage systems have mainly been con- This facility contains a large cage system maintained for ducted to evaluate the stability of the cage by analyzing research and development of coastal marine resources; the changes in the shape of the cage net. Researchers cages of various sizes are attached to one another and have performed studies using scale-down models of fish are connected with a plastic structure. The cage system cages to investigate their stability and shape changes is installed in a manner such that one side of the tetrag- caused by the tide and waves; recently, it has become onal cage is parallel to 330° (left side in Fig. 1). possible to estimate these changes using computer simu- A radio-linked acoustic positioning system (VRAP, lations (Kim et al. 2001a; Kim et al. 2001b; Lee et al. Vemco Ltd., Canada) and recording current meter 2015; Lee et al. 2008; Bi et al. 2015; Zhao et al. 2015; Lee (RCM-9, Aanderaa, Norway) were used to observe the et al. 2017). In addition, there are numerous methods to swimming behavior of the cultured chub mackerel assess the behavior and change in volume of real cage (Scomber japonicus) in the cage. The VRAP is an under- nets using recent advances in underwater measurement water position measurement system that uses an LBL technology; examples of this technology include high- (long baseline) method, which consists of three sea sta- precision pressure sensors (Lader et al. 2008) and under- tions and one base station. Each sea station, in this water ultrasonic position measurement systems (Hwang study, was a buoy (RAP buoy) loaded with an omnidirec- and Shin 2003; Tae and Shin 2006; Miyamoto et al. tional hydrophone and installed on the sea surface; it re- 2006; Lee et al. 2017). ceived signals from transmitters. The base station How fish respond to the behavior of the cage net is controlled each sea station using a VHF modem; it re- also an important area of research. The effects of cage ceived data from the sea stations and processed the data. deformation on the fish are not well known, although To measure the current speed, direction, water there have been some studies on the behavioral charac- temperature, cloudiness, and conductivity, a recording teristics of salmon in cages (Juell and Westerberg 1993; current meter was installed 5 m below the water surface Cubitt et al. 2005; Johansson et al. 2014). It is necessary outside of the cage; it recorded every 5 min. to understand the effects that the changes in the shape The shape of the cage and the positions of the ultra- of cages have on fish behavior, and to, subsequently, sonic transmitters (P1–P8) attached to the cage, which minimize these effects. The influence of coastal environ- were the targets of the experiment, are shown in Fig. 2. mental pollution has increased in recent years as fish The cage for the experiment was a small fish culture cages have been installed further out to sea. In particu- cage, the type most commonly used along the Korean lar, it is necessary to pay attention to the change in the coast. Its shape was a cube, 6 m × 6 m × 6 m (L × W × swimming behavior of cultured fish according to the D), which is adequate for the chub mackerel housed in changes in the shape of the cage because the cage cul- it. The cage was made of polyethylene net with a mesh ture technique is used for tuna, a high value-added fish size of 30 mm and a mesh diameter of 2 mm, and each that swims at a relatively high speed. corner of the cage was tied with a rope having a sinker Recently, mackerel has gained popularity for consump- (W1–W4) weighing 15 kg and connected to the cage to tion as raw fish in Korea, and thus, has attracted atten- minimize tide- and wave-induced cage deformation. tion as a high value-added species of increasingly good Typically, in the VRAP system, as the number of quality. In neighboring Japan, mackerel is also receiving transmitters to be measured increases, greater inter- attention as an important aquaculture species. ference occurs between signals according to different In this study, we observed the changes in the shape of transmission periods of the transmitters. Therefore, marine cage nets due to the tide, using a 3D underwater the number of transmitters that can be used simul- position measurement system, and examined the taneously is theoretically limited to ten (Jørgensen changes in the swimming behavior of the mackerel to in- et al. 2007). A total of eight multi-purpose transmit- vestigate and analyze how fish cage deformation affects ters (V16-6H, Amirix Systems Inc., Canada) were the behavioral characteristics of cultured fish. used to record the movement of the cage. The trans- mitters were 95 mm × 16 mm (L × D) in size and Materials and methods weighed 34 g. The transmitters were attached to the Experimental area and system setup bottom of the cage (at a depth of 6 m), and the Field experiments were conducted at a marine cage facil- remaining four were attached to the center of each ity in the coastal area of Tongyoung in Gyeongsangnam- cage wall (at a depth of 3 m). Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 3 of 12 Fig. 1 Experimental setup of radio-linked acoustic positioning system and recording current meter at the marine cage system of the Marine Research Center, Tongyoung, South Korea In addition, an implantable transmitter (V9P-2H, three fish could swim. The transmitters used in the ex- Amirix Systems Inc.) was used to observe the swimming periments have the interval for saving data with 3 min behavior of chub mackerel within the cage. This tiny owing to signal interference from other transmitters. transmitter, just 47 mm × 9 mm and 4.7 g, has a pressure sensor that allowed measurement of the depth at which Experiment and data analysis the fish swim. The transmitter was surgically implanted First, the positional coordinates of the transmitters at- in the peritoneal cavity of a fish. First, a fish was anes- tached to the cage were used to estimate the movement thetized. Next, its abdominal cavity was opened. Then, of the cage sides and internal volume loss of the cage. an ultrasonic transmitter was inserted, and the fish was The shape of the cage was measured by the positions of sutured closed. After the operation, the experimental the transmitters at the stand of tide (current speed less fish was allowed to recover in a recovery tank and subse- than 0.01 m/s), which were estimated by approximating quently released in the experimental cage. Two add- the displacement of each part according to current itional mackerel, without transmitters, were also placed speed. At this point, the x and y coordinate values, in the experimental cage. Fish typically detect up to four which reflect the displacement of the sides of the cage, neighbors or objects and accordingly determine their were received from VRAP, and the water depth coordin- swimming direction based on their relative positions ate value, z, was obtained by estimating the interior (Aoki 1982; Huth and Wissel 1992; Shinchi et al. 2002), angle between the reference point of each side and its placing only a minimum number of fellow fish allowed present location based on the origin of the water the experimental fish to freely swim within the entire surface. space of the cage without experiencing crowding. As a The internal volume loss of the cage was estimated by result, the positional coordinates received from the ex- applying the prismoidal formula (Brinker and Minnick perimental fish reflected the cage space within which all 1995), a method to calculate volumes of polygonal Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 4 of 12 Fig. 2 Schematic diagram of the experimental cage, the position of ultrasonic transmitter attached to the cage (P1-P8), and 15-kg sinkers (W ~W ) 1 4 Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 5 of 12 columns. This formula is a simple method of calculating circadian activity rhythms of the fish based on the the total volume that uses the cross-sectional area of change in duration and intensity of light. both ends and the area of the central cross-section when the side is flat. It was convenient to estimate the volume Results change of the cage using the positions of the eight trans- Characteristics of the tide in the experimental sea area mitters attached to the cage. To calculate the volume of Changes in the current direction and speed of the tide the cage, the cage was divided into upper and lower vol- on November 7 (neap tide) and December 12 (spring umes at the 3-m point, and each volume was assumed to tide), 2017, are shown in Fig. 5. The main axis of the tide be a polygonal column. Assuming the cross-sectional was NNW–SSE. The tide with the fastest current speed areas of the polygonal columns to be A and A , the flowed in the directions of about 330° and 130° during U L center cross-section between A and A to be A , and the neap tide, as shown in Fig. 3a and about 340° and U L m the distance between both sides to be L, the each volume 140° during the spring tide, as shown in Fig. 3b. The was estimated by current direction was stable when flowing NNW but volatile when flowing SSE. As shown in Fig. 1, the main axis of the current was almost parallel to one plane of 1 the cage and perpendicular to the other plane because V ¼ LAðÞ þ 4A þ A ð1Þ U m L one side of the cage was installed in the direction of 330° (150°). where A is the top area of the upper polygonal col- The frequencies of extremely slow current speed (0.01 umn, A is the bottom area of the lower polygonal col- m/s), indicating the stand of tide, were 24.6% and 16.7% umn, and A is the middle area of the polygonal for the neap tide and spring tide, respectively. The max- column. imum instantaneous speed of the neap tide was 0.122 m/ In the case of actual fishing nets, the sides of a net s in the NNW direction (329.0°) and 0.122 m/s in the generally form a smooth surface when the net is moved, SSE direction (128.0°), whereas the maximum instantan- as by waves; however, the sides of the net were assumed eous current speed of the spring tide was 0.244 m/s in to be flat in the volume calculation. the NNW direction (344.6°) and 0.274 m/s in the SSE The swimming behavior of the fish in the cage was es- direction (148.0°). Thus, the maximum instantaneous timated by correlating the coordinates (x, y, z) of the fish current speed in the spring tide was about 2.2 times received from VRAP with fish cage deformation caused higher than that in the neap tide. The current speed by tide, and the horizontal and the vertical movements exhibiting the maximum frequency in the neap tide was of the fish. We also analyzed the change in the depth at 0.02 m/s (14.1%) and that in the spring tide was 0.03 m/s which the fish swam during the neap tide and the spring (11.1%), which were similar to each other; however, tide by day and night to investigate the patterns of 32.6% of current speed in the spring tide exceeded the Fig. 3 Changes in the current direction and current speed of the tide during the a neap tide (on November 7, 2016) and b spring tide (December 12, 2016) Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 6 of 12 maximum instantaneous speed in the neap tide. From direction that most affected cage deformation was stable. these results, it can be concluded that the environmental Figure 4 a depicts the cage shape at the stand of tide, conditions of the two experimental days were very dif- showing that there was hardly any influence by the tide, ferent because the current speed distributions between while Fig. 4b shows the shape of the cage at the max- the two experimental days showed significant imum current speed in the neap tide; the arrow below differences. the cage represents current direction. As the current speed increased, the net surface perpendicular to the Fish cage deformation and volume loss current direction encountered a large amount of fluid The three-dimensional cage deformation caused by the resistance and moved accordingly, which led to fish cage tide is illustrated in Fig. 4. The cage deformation was an- deformation; however, the shape of the net surface par- alyzed for the main axis (NNW) of the tide within a allel with the current direction did not change much. range of ± 15°, as shown Fig. 3, in which the current Each corner of the lower part of the cage showed less Fig. 4 Comparison of the fish cage deformation between neap tide and spring tide. a Stand of tide (neap tide). b Max. current speed to NNW (v = 0.111 m/s, D = 327.4°). c Stand of tide (spring tide). d Max. current speed to NNW (v = 0.221 m/s, D = 343.1°) Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 7 of 12 movement than did the net surface because of the sinker 2.2% at a current speed of 0.088 m/s, about 4.9% at (weight) at the lower part of the cage. The right corner, 0.111 m/s, and 5.8% at 0.155 m/s (the maximum current which received the current first, moved slightly more speed during the neap tide), whereas, it was 7.3% at the than did the left corner. Nevertheless, the shape of the maximum current speed of 0.221 m/s in the spring tide. cage did not exhibit considerable deformation, even with The cage was greatly deformed as the shape of the net the maximum current speed, in the neap tide. surface perpendicular to the current direction changed, Cage deformation in the spring tide is depicted in Fig. as shown in Fig. 4; however, it was inferred that there 4c and d, the former showing deformation during the was only a little internal volume loss owing to the stand of tide and the latter showing deformation at the sinkers attached to each corner of the cage to maintain maximum current speed. As seen in Fig. 4c, the shape of its shape. the cage at the stand of tide in the spring tide was simi- lar to that in the stand of tide in the neap tide (Fig. 4a), Changes in the swimming behavior of cultured fish but the cage was greatly deformed at the time of the The swimming behavior of chub mackerel was signifi- maximum current speed in the spring tide. Figure 4d cantly different between the neap tide and the spring shows that at the time of the maximum current speed, tide, as was the shape of the cage. The three- the center of the net perpendicular to the direction of dimensional underwater positions of the fish are shown the tide was greatly displaced. At this time, the net sur- in Fig. 6; Fig. 6a and b represents the distribution of the face parallel with the tide was slightly displaced as well. fish in the neap tide and in the spring tide, respectively. The lower right corner, moreover, had greater deform- The overall distribution pattern of the fish in Fig. 6a ation than the other corners, so, the shape of the cage during the neap tide shows that they moved closer to was entirely distorted from its original form of a tetrag- the water’s surface occasionally, but mostly stayed in the onal column (cube). The reason for this was that one lower part of the cage. The shape of the distribution side of the cage was in the direction of 330°, but the took the form of a discus, as the fish spent most of their current direction in the spring tide was about 344°, time in the lower part of the cage and swam in a circle. which means it flowed from the lower right to the upper This pattern verifies that the cultured chub mackerel in left at an angle of about 10°. As a result, it is inferred the cage shared characteristics of fish under regular con- that the fluid resistance at the lower right corner was ditions (Beveridge 2004). Thus, it is inferred that the cul- the largest. tured fish here exhibited relatively stable swimming The volume loss of the cage, as calculated by the pris- behavior in the cage during neap tide. moidal formula, at times of relatively stable current The shape of the distribution of the cultured fish in speed in the NNW direction, is shown in Fig. 5. Based the spring tide (Fig. 6b), however, showed a significantly on its shape at the stand of tide, the volume loss was different shape from that in the neap tide (Fig. 6a). The Fig. 5 Volume loss of cage caused by current speed (□ neap tide, ■ spring tide) Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 8 of 12 which led to an increased change in their swimming pattern. The results of the analysis of the three-dimensional distributions of the cultured fish by the current speed conducted to determine the effect of the cage deform- ation on their swimming behavior is represented in Fig. 7. Figure 7a shows the position distribution of the fish at the stand of tide in neap tide, in which it is assumed that the fish generally stayed below the depth of 4 m and swam across most of the horizontal area of the cage. The fish moved to the left because of cage deformation; however, they did not change their depth much and stayed in the lower part of the cage, at the time of the maximum current speed in the neap tide, as shown in Fig. 7b. Contrarily, the fish swam in the central part of the cage and frequently moved to the upper part of the cage, at the maximum current speed in the spring tide, as shown in in Fig. 7c. Such behavior occurred at current speeds of 0.14–0.16 m/s, in which the fish also moved to the right because of cage deformation, as shown in Fig. 7d. The swimming area of the fish moved further to the right at the maximum current speed in the spring tide as cage deformation increased, as shown in in Fig. 7e. At this time, they stayed mostly around the depth of 5 m. At these times, the fish appeared frequently in the cen- tral part of the left side, but did not appear in the bot- tom right side of the cage due to the severe cage deformation on the left net surface and the bottom right side of the cage, as shown in Fig. 4d. In conclusion, in the neap tide, the distribution of the cultured chub mackerel was mainly concentrated in deep water, near the lower part of the cage, and the cen- ter of the distribution shifted slightly to the right side Fig. 6 Comparison of the swimming space of the cultured chub owing to the slight cage deformation caused by the small mackerel between the neap tide and the spring tide. a Neap tide. b range of changes in the current speed. In the case of the Spring tide spring tide, however, the fish did not stay in the lower part of the cage even at the stand of tide; instead, they moved to other depths, where they had more space in position distribution pattern of the fish, which indicates which to swim freely, as the upper part of the cage was their swimming behavior, was not primarily near the significantly deformed. lower part of the cage in spring tide, unlike that in neap The changes in swimming depth over time in the neap tide, and took the form of a long discus in the direction tide and in the spring tide are depicted in Fig. 8.As of the x-axis. The reason for this is that the main axis of shown in Fig. 4, there was very little cage deformation the current was almost parallel with the x-axis, which during the neap tide; so, the changes in swimming depth limited and deformed the swimming area of the fish can be inferred to be fish reaction to light conditions owing to the displacement of the net surface perpen- within the cage. The mean swimming depth of the fish dicular to the current direction. It is inferred that the during the neap tide did not vary significantly between fish kept swimming aggressively to maintain their pos- day time (6.1 m), as shown in Fig. 8a, and night time ition against the fast current in the spring tide. These (5.9 m), as shown in Fig. 8b. The distribution of fish dur- factors prevented the fish from showing their stable ing the neap tide was identical between day and night, swimming behavior in the lower part of the cage as in and they were always concentrated in the lower part of the neap tide; instead, they frequently moved to areas the cage. During spring tide, the fish remained primarily near the surface of the sea, above the depth of 3 m, at a depth of 6.8 m during the day (Fig. 8c), deeper than Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 9 of 12 Fig. 7 Comparison of the swimming behavior of the cultured chub mackerel affected by cage deformation. a v < 0.1 m/s (stand of tide) in the neap tide. b v = 0.10–0.122 m/s in the neap tide. c v < 0.1 m/s (stand of tide) in the spring tide. d v = 0.14–0.16 m/s in the spring tide. e v = 0.2– 0.223 m/s in the spring tide that in neap tide. The fish showed relatively stable swim- considerably large cage deformation caused by the high ming depth, but occasionally moved upwards, to a depth current speed. In addition, the swimming distribution at of approximately 5 m. However, at night in spring tide, night time during the spring tide showed a significantly the fish tended to frequently move upwards toward the different shape (Fig. 8d). The mean swimming depth of surface of the sea (Fig. 8d). It can be inferred that the the fish at night during the spring tide was 3.7 m, and fish moved to a safer space because they could not stably they moved evenly between the depths of 1 m and 6 m. stay near the lower part of the cage owing to the In other words, their swimming was not concentrated at Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 10 of 12 Fig. 8 Comparison of swimming depth distribution during the neap and spring tide. a Neap tide/day. b Neap tide/night. c Spring tide/day. d Spring tide/night one specific depth. Thus, the fish did not show stable Our results indicate that cage deformation significantly swimming behavior at night in the spring tide, as op- affects the swimming behavior pattern of cultured chub posed to that in the neap tide. It is further inferred that mackerel. The fish generally swam in a circle in the neap they had to make frequent movements between the tide but moved to one side of the cage because of cage upper part and the lower part of the cage. Assuming that deformation in the spring tide. Moreover, the fish ap- the swimming depth at night in the neap tide is natural peared to make frequent movements to the upper and swimming behavior for fish in general, the behavior of lower parts of the cage in the spring tide; such changes the experimental fish was significantly affected by cage in the swimming depth were most pronounced at night deformation at night in the spring tide owing to the ex- in the spring tide. treme changes in the current speed and the cage sides The degree of cage deformation is affected by the dir- not being visible to the fish. ection of the current, waves, shape of the mesh and size In sum, the behavior of the cultured chub mackerel of the net, position and weight of the sinkers, and within the cage was limited by the shape of the cage. current speed. One study measured cage deformation They were not affected much by the minor cage deform- and calculated the volume loss due to the current using ation in the neap tide, in which the current speed was an underwater sensor; the volume loss of the cage was slow. However, the larger cage deformation in the spring 20% even at a low current speed of 0.2 m/s and up to tide appeared to affect their swimming behavior. This in- 40% at a current speed of 0.35 m/s (Lader et al. 2008). fluence was greater at night time, when their vision was Another study, on designing the shape of the sinkers at- limited. tached to the cage, showed that the volume loss of the cage was significant with current speeds greater than 0.2 Discussion m/s (Kim et al. 2001a). In our study, there was a volume Individual-based measurements enable us to understand loss of about 8% in the spring tide when the current the synchronous mechanisms by which fish cope with speed exceeded 0.2 m/s. The cage used in our study was environmental signals that cause changes in their behav- tetragonal (a cube), which was different from the shape ior in a production environment (Oppedal et al. 2011). of the cage used in the previous study (Lader et al. Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 11 of 12 2008). In addition, the sinkers attached to each corner system we used estimates the underwater position of an may have minimized cage deformation. At a low current object using the time delay of acoustic arrival, though speed, the fish generally showed very stable movement the accuracy varies based on the output level of the under the net in the cage. However, when the current transmitter or decreases and increases in signals (Baras speed increased, they tended to swim to the surface and Lagardere 1995). Previous studies show that the upon deformation of cage shape. This is believed to have VRAP system is accurate to about 1–2 m when a trans- increased the stress index of the fish, resulting in growth mitter station is installed using an anchor. Thus, such a and other adverse effects. The adverse effects of these system is unavoidably affected by the changes in baseline changes in behavior of the fish on the shape of the cage due to the movement of the station. In a previous study, have been discussed in other studies (Lader et al. 2008). we measured signals from a fixed transmitter attached to Moreover, although the volume loss was only 7.3%, the a cage in a quiet sea, in which the two-distance root impact on the fish caused by the volume loss is likely to mean square (2 drms) was 0.8 m (Tae and Shin 2006). be greater when considering the situation wherein large The standard deviations of the x-, y-, and z-axes were numbers of fish are farmed in the actual fish cage. 0.2, 0.4, and 1.0 m, respectively. The baseline in that ex- The cultured chub mackerel in the experimental cage periment was between 12 and 14 m, which was consider- generally swam in a circle during the day, while avoiding ably shorter than that in this study. the deep corners. Visual observation of highly populated Swimming area in a deformed cage is affected by vis- cages showed that they occasionally swim near the sur- ual stimulation (Ehrenberg and Steig 2003). Cage de- face; however, they usually swim near the lower part of formation affects the yield and health of the cultured the cage if there is enough space, as there was in this fish by reducing the space in which they can swim study. (Lader et al. 2008). In this study, we verified that cul- In our study, the fish mainly preferred the lower part tured chub mackerel frequently swam near the surface of the cage; however, they tended to swim at shallower of the water owing to cage deformation, and that they depths at night in the spring tide, when their vision was were hindered from stably resting and swimming be- limited. There were no significant changes in the water cause of limited space in the cage. In recent years, aqua- temperature, cloudiness, or conductivity by the measure- farms have begun moving to the open sea because of the ment, which could have influenced the swimming depth contamination of coastal water from cage-based fish cul- distribution of the fish, at the time of this field experi- ture (Kim et al. 2001b); therefore, cage deformation and ment. Thus, the vertical changes in the swimming depth changes in fish behavior due to the current speed are of the observed fish might have been caused by their cir- very important. With the new trend in the aquaculture cadian rhythm and deformation of the cage (Føre et al. industry, it is imperative to conduct in-depth studies on 2009; Johansson et al. 2014). the influences of current and waves on marine cages, Scale-down model experiments and simulations are and the fish reared in them. widely used to estimate fish cage deformation according to the design of the net. Survey experiments are impera- Conclusions tive to analyze the swimming behavior of the fish in The behavioral change in cultured fish according to these cages. Simultaneous observations of fish swimming changes in shapes of tetragonal small-sized fish cages behavior and measurements of cage deformation using a based on the tide was measured using the 3D under- current underwater telemetry system will require exten- water position measurement system and analyzed. The sive data collection over long durations. The transmit- swimming volume of the fish due to net deformation is ters used in the experiments have the interval for saving influenced by visual stimuli, and the net deformation af- data with 3 min owing to signal interference from other fects the yield and health of cultured fish by reducing transmitters. Even though the data collection interval the volume. Furthermore, fish are more likely to swim was not short, the fish continuously and repeatedly close to the water due to deformation of the net, and swam in an identical pattern in a small space, and the limited within the area where swimming is possible, thus shape of the cage did not rapidly change because of the confirming that the cultured fish are disturbed to stable current; so, the data was adequate to detect the pattern. rest and swimming. In recent years, since the waters oc- Since we were able to select several time periods with cupied by the cage aquaculture are becoming more pol- slight changes in the current, it was sufficient for us to luted and moving to the offshore, the shape changes of estimate the swimming area of the fish. the net and the behavior characteristics of the fish by In our results, the accuracy of the underwater telem- the flow rate will become more important. Regarding etry system was extremely important in verifying and the new trends of this aquaculture, it is necessary to in- evaluating the correlation between the changes in the vestigate in depth the relationship between the increas- current and cage deformation. The underwater telemetry ing influence of currents and waves on net and fish. Hwang et al. Fisheries and Aquatic Sciences (2020) 23:14 Page 12 of 12 Acknowledgements Johansson D, Laursen F, Fernö A, Fosseidengen JE, Klebert P, Stein LH, Vagseth T, Not applicable Oppedal F. 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