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Article

Research on the Acoustic Conditioning Taming on Fish and Application in Marine Ranching

by
Huarong Yuan
1,2,3,4,
Yanbo Zhou
1 and
Pimao Chen
1,2,3,4,*
1
South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, China
2
Key Laboratory of Marine Ranching, Ministry of Agriculture and Rural Affairs, Guangzhou 510300, China
3
National Digital Fisheries (Marine Ranching) Innovation Sub-Center, Guangzhou 510300, China
4
Scientific Observing and Experimental Station of South China Sea Fishery Resources and Environments, Ministry of Agriculture and Rural Affairs, Guangzhou 510300, China
*
Author to whom correspondence should be addressed.
Water 2023, 15(1), 71; https://doi.org/10.3390/w15010071
Submission received: 8 November 2022 / Revised: 19 December 2022 / Accepted: 22 December 2022 / Published: 25 December 2022
(This article belongs to the Special Issue Hydroacoustics in Marine, Transitional and Freshwaters)
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Abstract

:
Acoustic conditioning taming technology is one of the key tools for controlling and managing the behavior of target organisms in marine ranching. In this study, juvenile Pagrus major (Red Seabream) were subjected to acoustic conditioning taming with 400 Hz of square–wave continuous tones for 8 days in laboratory and 15 days in an open-sea area. At the same time, the elimination of conditioned reflexes to sounds and applications in marine ranching were tested. The Gaussian model was used to regression-fit the distribution of fish in the tank, and the fitting degree was 91.79%. Good conditioning was established after four days of acoustic conditioning taming, and the efficiency index was 44.49 in the laboratory. The average response time, aggregation time, and residence time of the test group were 0.95 s, 3.35 s, and 21.15 s, respectively. The aggregation rate of the test group showed an upward trend, and it remained at 100% from the 4th day to the 8th day. It took longer to establish the conditioned response to sound in the open-sea area, and good conditioning was established after the 18th acoustic conditioning taming. Juvenile Pagrus major with established acoustic conditioning were tagged before release. On the 18th day, 0.2% of released fish swam to a sound source when the sound was played, and from the 24th day, there was no fish presence in the area near the sound source. The conditioned response of fish to sound was gradually eliminated using the negative feedback mode of playing the sound without feeding bait. After 22 negative feedback tests, the sound was no longer attractive to the fish, meaning that the “sound–food” neural connection established by the acoustic conditioning taming had been eliminated. The results of this study show that acoustic conditioning taming technology was an effective method of fish behavior control, and it is feasible to apply this technology in the construction of marine ranching systems. A number of acoustic conditioning taming devices can be established in marine ranching to continuously tame the released fish and strengthen the impact of the sound. At the same time, the multi-point deployment of automatic taming devices can form an acoustic conditioning taming network to increase the action area and effects.

1. Introduction

Changes in the environment and the environment surrounding human activities have led to the degradation of habitats and a reduction in fishery resources in the South China Sea [1,2,3,4]. In order to cope with the increasingly prominent problems related to resources and the environment, many coastal countries around the world have taken marine ranching as an important means of conserving resources, repairing damage to the environment, and realizing the transformation and upgrading of fisheries [5,6,7,8]. Based on the principles of marine ecosystems, marine ranching is a fishery model in which the areas needed by marine organisms to reproduce, grow, bait, and avoid enemies in specific sea areas are built or repaired through artificial reefs and stock enhancement, to increase and conserve fishery resources, improve marine ecological environments, and realize the sustainable utilization of fishery resources [9]. Since 2002, the Chinese government has allocated special funds for supporting the construction of marine ranching. By 2022, more than 300 marine ranches have been built, including 153 national-level marine ranching demonstration areas, with a sea area of 2506.95 km2. There was 19 national-level marine ranching demonstration areas in South China Sea, with a sea area of 1422.86 km2 [10]. Compared with 1964–1965, the resource density of main economic fisheries status in the northeastern of the South China Sea decreased seriously [11]. Acoustic conditioning taming technology is one approach used to effectively control fish stocks in marine ranching [12,13].
The acoustic conditioning taming of fish in marine ranching can not only prevent the fry from being lost from marine ranching, but also attract wild fish into the ecosystem, thus realizing the safe, high-quality production and efficient management of ecologically or economically important species [14]. Other studies have carried out research on acoustic conditioning taming technology for a variety of offshore economic fish [15,16,17,18]. In Japan, economic sea fish such as Pagrus major [19], Sparus macrocephalus [20], Sebastes schlegeli [21], and Paralichthys olivaceus [22] were used as acoustic conditioning taming objects, and methods of acoustic conditioning taming marine ranching have been established. Other developed fishery countries such as the United States, Norway, Britain, and Denmark have attached great importance to research into acoustic conditioning taming technology as well, and have conducted a large number of studies [23,24,25].
The principle of acoustic conditioning taming technology is based on the auditory characteristics of the fish. Using the method of played sound and feeding bait at the same time, through the repeated training of “played sound + feeding bait”, the experimental fish can establish a temporary neural connection between the sound signal and food. This can achieve the purpose of attracting dispersed individual fish into a group through sound signals, so as to effectively control fish behavior, and thus enable catching of the fish with fishing gear [26].
Sound is a mechanical disturbance that travels through a medium as a p-wave [27]. Sound energy is propagated outward in the form of sound pressure and particle motion. Fish auditory organs include the inner ear, swim bladder, lateral line, and air sacs, which help the fish to sense sound waves or overall vibrations in the water [28]. Sound signals are transmitted in an inertial-mediated pattern formed by the movement of acoustic particles, accompanied with the relative movement of dense otoliths and the sensory hair cell epithelium in the inner ear (Figure 1). The movement of sensory hair cells relative to otoliths (which are denser and lag behind as sound waves move) causes cilia to bend and ion channels to open, generating nerve impulses which are interpreted by the brain as sound [29,30], and thus complete the transmission of sound signals, which are eventually integrated into the central nervous system.
The inner ear of fish is composed of the associated sensory region, three semicircular canals, and three otoliths (Saccule, Utricle, and Lagena); each of the three pockets has one otolith (Figure 2). The otoliths have Maculae, which are covered with sensory hair cells. Auditory hair cells convert sound signals into electrical signals which are recognized by the nervous system, and otoliths identify the direction of sound vibrations.
The auditory characteristics vary between different fish species [31,32]. Most fish can hear sounds ranging from 50 to 1000 Hz, a few fish can hear sounds greater than 3 kHz, and only a few fish can hear sounds greater than 100 kHz [33]. The auditory sensitivity of fish is related to the presence, size, and shape of the swim bladder and the physiological structure of its connection with the inner ear. The ostariophysan, whose swim bladder is connected to the inner ear by Weber’s apparatus, has the most sensitive hearing, followed by the non-bone bladder. Fish without a swim bladder have poor hearing ability and a small range of audible frequencies [34]. Most fish are sensitive to low-frequency sounds, with 36–1250 Hz being the audible sound frequency range of Sparidae fish [35,36], and 200–600 Hz being their most sensitive sound range [37,38].
China started the construction of national marine ranching demonstration zones in 2015 [39]. Although the earliest research report on acoustic conditioning taming in China was published in 1989 [36], until now, acoustic conditioning taming technology has not been applied in the construction of national marine ranching demonstration areas in China. In this study, Pagrus major (Red Seabream) [40,41,42,43,44] fish were used as the experimental object, and 400 Hz square-wave continuous sound was used to study the acoustic conditioning training and applications of the acoustic conditioning of fish in laboratory conditions and open-sea areas. The Gaussian distribution model was chosen to analyzing the effects of target variables on fish behavior. The response time, aggregation time, residence time, and aggregation rate were measured. We compared the changes in these four indicators between the test group and the control group in an attempt to answer the following three questions: (1) What is the acoustic conditioning taming effect of 400 Hz square-wave continuous tones on Pagrus major? (2) How much negative feedback does it take to eliminate the fish’s conditioned responses to sound? (3) What are the effects of the acoustic acclimation test in the open-sea area? In answering these three questions, we evaluated the application effect of acoustic conditioning taming technology in marine ranching and provide technical accumulation conditions for fish behavior control in marine ranching.

2. Materials and Methods

2.1. Materials

The Pagrus major used in the experiment were bought from an aquafarm in Nanao Town, Shenzhen, Guangdong, China. The average fork length and weight of the fish were 5.5 cm and 3.9 g, respectively. After taking the fish back from the aquafarm, a potassium permanganate bath with a concentration of 0.01% was used for five minutes to disinfect the fish [45]; then, the fish were kept in a temporary tank which had the same conditions during the experiment for seven days in order to adapt to the new environment. After seven days of adaptation in the temporary tank, 200 fish were selected and divided into two groups, with 100 in the test group and 100 in the control group. The fish were moved into an experiment tank and a control tank; the acoustic conditioning taming experiment began after 48 h.

2.2. Equipment

2.2.1. Test Equipment in the Laboratory

The experiment tank was covered with a black cloth curtain, and the dimensions of the tank was 5.0 m × 4.0 m × 1.5 m. An underwater loudspeaker (STX S50) was placed at the center-point of the bottom of the tank, and it was padded away from the bottom of the tank with a square foam block which thickness was 7 cm. The audio signal was generated by a signal generator (DG1022) and transmitted to the underwater loudspeaker through a power amplifier (TA-8060). Circles with radii of 0.5 m, 1 m, 1.5 m, and 2 m were marked in the bottom of the experiment tank, to enable easy recognition of the position distribution of fish in the tank during the experiment.
In order to avoid the impact of human activities on the results, feedstuff was administered through a hard plastic tube with a length of 3.5 m and a diameter of 3.5 cm. The end of the tube was arranged directly above the underwater loudspeaker. For the feedstuff to easily flow through, the tube was placed at an angle of 60° from the vertical direction.
In order to avoid the influence of sound caused by the feedstuff falling into the water on the sound used in the experiment, the nozzle of the tube was placed slightly below the water’s surface; a video recorder (LC5201B5) with a monitoring system (ImagineWorldClient) was installed directly above the tank to record the behavior of the fish during the experiment (Figure 3).
In order to avoid the effects of acoustic conditioning taming due to the satiety of the fish, the weights of each instance of feeding were 0.6% of the total weight of the experimental subjects [46]. The inflator pump was shut off during the experiment, and the water depths in the experiment tanks were 0.7 m. The water temperature was 23.0–25.1 °C, the salinity was 22.9–23.5‰, and the pH was 7.7–7.8.

2.2.2. Test Equipment in the Open-Sea Area

The instruments and equipment used in the open-sea area were the same as those used in the laboratory experiments. A battery was used to supply power, and a camera and manual recording were used for observations of experimental data. The equipment was placed on the operation platform (Figure 4).

2.3. Methods

2.3.1. Laboratory Test Method

In the test group, the time of acoustic conditioning taming was set to 120 s each time, and the feedstuff was fed at the same time. Acoustic conditioning began at 8:00 every day, and was performed once every four hours, a total of four times each day; Fish conditioned to respond to sound through the process above were then exposed to sound without feedstuff once daily at 22:00 to evaluate the taming effect. The fish in control group were fed at the same time each day as the ‘test’ fish but no sound was played when feedstuff was dispensed. There was no sound and no feedstuff in the control group each day at 22:00.The experiment continued for eight days (Figure 5). The real-time monitoring system was used to record the behaviors of fish in the test group and control group within ten minutes before and after each acoustic conditioning taming test, including the response time, aggregation time, residence time, and aggregation number of fish.

2.3.2. Method for Eliminating Sound Conditioning

A test was carried out on the established conditioned fish with only one played sound, and the behaviors of the fish were observed with the monitoring system. The test was conducted three times a day, at 07:30, 12:00, and 17:00. The response time, aggregation time, residence time, and aggregation number of fish were recorded in each experiment. When there was no aggregation phenomenon and the behavior was the same as that of the control group at the moment sound was played, this suggested that the conditioned reflexes established by acoustic taming had been eliminated.

2.3.3. Open-Sea Area Test Method

The experimental device was placed on the open water operating platform. The experimental sample was divided into a test group and control group, and 100 fish were assigned to each group. In the test group, the length of acoustic conditioning taming was set at 150 s, in which sound was played for only 50 s and “sound played + feeding feedstuff” occurred for 100 s. The fish in control group were fed at the same time each day as the ‘test’ fish but no sound was played when feedstuff was dispensed. The experiment was conducted at 6:30 and 17:30 every day for 15 consecutive days. The response time, aggregation time, residence time, and aggregation number of fish were recorded in each experiment. In total, 500 Pagrus major which were established sound conditioning in tank of the laboratory were tagged and released into the sea. Every three days, sound was played with feedstuff for 300 s at the release point, and the response time, aggregation time, residence time, and aggregation number of fish were recorded. The experiment was conducted for 30 days. According to the results, the recapture rate after acoustic conditioning taming was estimated. The water depth of release area was 3.5 m, seawater surface temperature was 29.0 °C, and salinity was 31‰, the seabed surface sediments was silty sand.

2.4. Data Analysis

The response time, aggregation time, residence time, and aggregation rate of the juvenile Pagrus major were measured [47,48] (Table 1).
The Gaussian distribution model was used to analyze the positions of the fish in the tank when the sound was played. The efficiency index (I) was the ratio of the occurrence rate of fish in the aggregation area to its occurrence area [51]. The response time and aggregation time of fish in the control tank were calculated starting two minutes after the beginning of the test, and the residence time and aggregation rate of the fish in the aggregation area were the same as those in the test tank. We used the raw measured variables from the experiments when applying the Gaussian distribution model. We used the software Orign 8 for the data analysis.
The Gaussian distribution model formula is as follows:
y = y 0 + A w π / 2 e − 2 ( x − x 0 ) 2 w 2
where y is the frequency of occurrence of fish with the distance, y0 and A are correction coefficients, W is the standard deviation, X is the distance to the center of the pool, and X0 is the average value of random variables subject to the Gaussian distribution.
The formula of the efficiency index (I) is as follows:
I = P π r 2
where P is the average occurrence rate of fish in the aggregation area in the experiment tank, and r is the radius of the aggregation area.

3. Results

3.1. Results in the Tank

3.1.1. Aggregation Area

The fish in the control group were dispersed in the tank, and exhibited no clustering phenomenon. The probability of occurrence in all parts of the tank was basically the same. The Gaussian model was used to perform regression analysis of the scatter distribution diagram in the experiment at 22:00, and the regression curve showed a generally random distribution (Figure 6).
After juvenile Pagrus major had been subjected to acoustic conditioning taming by 400 Hz square-wave continuous tones for eight days, the fish gathered in groups and swam in the aggregation area only when sound was played at 22:00; the fish clustered close to the sound source (underwater loudspeaker). The radius of the aggregation area in the test tank was 79.79 cm. The results showed that the fish exhibited a trend effect positively related to the 400 Hz square-wave continuous tones (Figure 7). From the 1st to the 8th day of acoustic conditioning taming, the radius of the aggregation area showed a decreasing trend, indicating that, after acoustic conditioning taming, the fish had established conditioned reflexes to the sound and displayed a behavior of approaching sound sources even after sound was played without the release of feedstuff.

3.1.2. Behavior of Fish in the Test Tank

Before the test, the fish in the tank swam slowly and exhibited no clustering phenomenon. On the 1st day of acoustic conditioning taming, during the test at 22:00, the fish showed a behavioral response of panicking at the moment of the sound being played, with swimming speeds increasing sharply and fleeing away from the sound source. After 0.35–1.00 s, the fish gradually swam closer to the sound source, and swam in a whirling group which represented the seeking of feedstuff in the aggregation area. The duration of the panicking behavior was 0.75 s. On the 2nd day, the time of panicking and dissociation behaviors of the fish was less than 0.20 s. From the 3rd day to the 8th day, the fish demonstrated no panicking behavior and swimming away from the sound source at the moment of the sound being played; in contrast, the fish quickly gathered to the aggregation area and swam in a whirling group, in a state of seeking out the feedstuff. Within 120 s of the sound being played without the administration of feedstuff, the fish reacted strongly and their swimming speeds significantly increased. The fish gathered in the aggregation area within a very short space of time, swimming to the surface in regular circles under the tube (Figure 8). Occasionally, some of the fish jumped out of the water, expecting to catch the feedstuff. When that sound had finished playing, the gathered groups gradually dispersed and swam irregularly around the tank, but their swimming speeds were still higher than those before the sound was played. It took approximately five minutes for the fish behavior to return to that before the sound was played.

3.1.3. Response Time, Aggregation Time, Residence Time, and Aggregation Rate

After eight days of acoustic conditioning taming, the response times in the control group tended at approximately 2.66 ± 0.28 s. The response times of the test groups showed a trend of gradually decreasing, not changing significantly from the 5th day of acoustic conditioning taming and remaining at the minimum state. The average response time of the test group was 0.95 s (Figure 9).
In the control group, the aggregation time varied around 6.73 ± 0.80 s within 8 days of acoustic conditioning taming. The aggregation time of the test group showed a trend of shortening with the increase in experimental days, and the aggregation time from the 4th day did not change substantially. The average aggregation time of the test group was 3.35 s (Figure 9).
The residence time of the fish in the control group varied around 6.39 ± 1.70 s during the experiment. The residence times in the test group showed increasing trends with the increase in the experimental days and reached the peak on the 4th day; there was no major change thereafter. The average residence time of the test group was 21.15 s (Figure 9).
The aggregation rate of the fish in the control group showed no obvious changes during the experiment, and remained at around 22.95% ± 3.30%. The aggregation rate of the test group showed an upward trend, which remained at 100% from the 4th day to the 8th day (Figure 9).

3.1.4. Efficiency Index

The acoustic conditioning taming efficiency index on juvenile Pagrus major subjected to 400 Hz square-wave continuous tones was 44.49.

3.2. Elimination of Conditioned Reflex to Sound

By observing the changes in response time, aggregation time, and residence time of the fish, it could be seen that there were no significant changes in these variables from the 1st to the 6th test. After the 7th test, the response time and aggregation time of fish gradually increased, while the residence time gradually decreased (Figure 10). Thus, the established conditioned reflexes of fish gradually weakened after the 7th test. By the 22nd test, the response time, aggregation time, and residence time of the fish reached average levels before acoustic conditioning taming: 2.5 s, 6.5 s, and 8.2 s, respectively. This means that, after 22 tests of only playing the sound without delivering feedstuff, the sound had no attracting effect on the fish, and the conditioned reflex to the 400 Hz square-wave tone could be eliminated after 22 negative feedback events.

3.3. Results in the Open-Sea Area

3.3.1. Behavior of Fish

Before playing the sound, the fish in the test group and the control group exhibited similar behavior, both swimming in the water without direction, order, and without swarming; the swimming speeds varied between fast and slow; and most of the fish activities occurred at the bottom of the net cage, with almost no fish coming to the surface of the water. From the 1st to the 7th acoustic conditioning taming events, the fish in the test group exhibited no obvious response to playing the sound, which was similar to that in the control group. From the 8th to the 15th test, it took a long time for the test group to gather under the feeding tube which was situated above the underwater loudspeaker (Figure 11). The number of fish aggregating was about 30, accounting for 10.00% of the total. From the 16th to the 20th tests, the time for the test group to gather under the feeding tube was relatively shorter, and the number of aggregated fish was about 100, accounting for 33.33% of the total. From the 21st to the 30th tests, the gathering time of fish in the test group decreased, and there was no obvious change during this period. The number of aggregated fish was about 150, accounting for 50.00% of the total number. Based on the results, the 1st to the 7th acoustic conditioning taming tests in open water were classified as the adaptation period; the 8th to 15th tests were classified as the conditional response period; the 16th to 20th tests were classified as the conditional formation period; and the 21st to 30th tests were classified as the conditional establishment period.

3.3.2. Response Time, Aggregation Time, Residence Time, and Aggregation Rate

The response time and aggregation time of the fish in the test group decreased with the increase in number of experiments, and reached the lowest at the 18th and 17th experiments, respectively, and then maintained the same state (Figure 11). The response time in the 1st test was 3.41 s, and that in the 30th test was 0.40 s, with an average of 1.31 s. The response times of fish in the control group showed little change, in the range of 3.0–3.6 s, with an average reaction time of 3.24 s. The aggregation times in the 1st and 30th tests of the test group were 41.50 s and 10.17 s, respectively, with an average aggregation time of 19.69 s. The aggregation time of fish in the control group exhibited little change, with an average reaction time of 38.54 s. The aggregation rate of fish in the test group increased with the increase in the number of tests, with the best effect at the 21st test, and then fluctuated at that level (Figure 12). The aggregation rates of the group in the 1st and 30th tests were 46.20% and 93.60%, respectively, with an average aggregation rate of 77.63%. The average aggregation rate of fish in the control group was 49.38%.

3.3.3. Applications in Marine Ranching

After releasing the conditioned fish, over time, the time taken to swim to the sound source showed an increasing trend, and the occurrence rate showed a gradually decreasing trend (Figure 13). On the 15th day after release, eight fish clustered to the sound source, accounting for 1.6% of the total. On the 18th and 21st days, only one fish swam to the sound source after the sound was played, accounting for 0.2% of the total. In terms of the time required to swim to the sound source, on the 1st day of release it took 0.5 s; on the 21st day, the time taken was 87 s. After the 24th day, there were no fish gathering in the area near the sound source.

4. Discussion

4.1. Acoustic Conditioning Taming Effect on Fish in Laboratory

According to the results, juvenile Pagrus major were sensitive to the 400 Hz square-wave continuous tone and demonstrated obvious positive feedback. After four days of acoustic taming of the 400 Hz square-wave continuous tone, the fish can establish a conditioned response to the sound.
In this study, we analyzed the effect of acoustic conditioning taming using the spatial distribution of fish in the tank when sound played without the administration of feedstuff, which reduced the influence of feedstuff factor and only reflected the influence of sound on the behavior. According to the central limit theorem, when we add a large number of independent random variables, regardless of their original distribution, their normalized sum tends to Gaussian distribution. The implications of the theorem include that a large number of scientific and statistical methods developed specifically for the Gaussian model can also be applied to a wide range of problems that may involve any other type of distribution. The Gaussian model was used to regression-fit the distribution of fish in the tank, and the fitting degree was 91.79%, which reflected the real positions of fish when the sound played.
In the control group, there was no aggregation phenomenon and the probability of fish appearing in anywhere of the tank was similar, showing a random distribution overall. The response time and aggregation time of fish were lower than those in the control group from the 2nd day, whereas the residence time was higher than that in the control group from the 2nd day and the aggregation rate was higher than that in the control group from the 1st day of acoustic conditioning taming. On the 1st test day, the fish showed signs of panic when the sound played and briefly strayed away from the sound source; this phenomenon was possibly due to an instinctive response of fish to external stimuli [52]. After the panic action, the fish gradually swam towards the source of the sound due to conditioned responses. After the 2nd day of sound training, the panic phenomenon had dissipated, indicating that the fish were developing a positive conditioned response to sound.
Over time, the response time and aggregation time of the fish showed trends of shortening, and the residence time and aggregation rate showed trends of increasing. The response time, aggregation time, residence time, and aggregation rate exhibited no significant changes since the 4th day of acoustic conditioning taming, and remained at an optimal level throughout the test period. This means that good conditioning was established after four days of acoustic conditioning taming.
In this study, the sound was played through an underwater speaker at the bottom of the test tank. After the sound wave had been emitted from the speaker, it was reflected in the wall and corner of the tank and induced the superposition phenomenon; thus, the sound pressure increased at the four corners of the tank and near of tank wall. The sound source and sound pressure did not exhibit completely spherical distributions because of the attenuation of vibrations in water. This situation may have caused some negative effects in the experiment. Sound-absorbing boards installed on the edge of the tank would have prevented such a phenomenon. The relationship between the distribution of sound pressure at each point in the test tank and the behavior of fish in the acoustic conditioning taming test remains to be further studied.
Jiang Zhaoyang [38] used a 300 Hz rectangular-wave continuous tone to perform acoustic taming on Pagrus major: the time taken to establish a conditioned reflex was five-seven days; the reaction time after the conditioned reflex had been established was 3.8 s; and the aggregation time was 10.8 s. In this study, the time to establish the conditioned response was four days, and the average response time and aggregation time during the whole test process were 0.9 s and 3.4 s, respectively. The differences between the two experiments may have been caused by the differences in the selected frequency, the fork length, body weight, and quantity of the tested fish, or the test methods. Cheng Minghua [36] proposed that changes in water temperature during acoustic conditioning taming can influence the test, and juvenile fish are more likely to establish conditioned reflexes than adult fish.

4.2. Acoustic Conditioning Taming Effect on Fish in the Open-Sea Area

According to the test results, the response time and aggregation time of acoustic conditioning taming of fish decreased over time, and the residence time gradually increased.
Compared with the experiment in the laboratory, the response time and aggregation time of fish were increased in the acoustic conditioning taming experiment in the open-sea area, but the residence time was not increased, and it took longer to establish a conditioned response to sound; good conditioning was established after the 18th acoustic conditioning taming test. It is argued that all vertebrate auditory systems are required to perform certain basic tasks, including acoustic feature discrimination, sound source localization, frequency analysis, and auditory scene analysis, among others [53]. A second critical caveat is that, when studies are performed in tanks and other enclosures, the sound fields may be very different from those that fish experience in the wild, especially in terms of the magnitude of particle motion relative to sound pressure [54].
In the open sea, fish are easily disturbed by other external factors, such as the sounds generated by human activities, water surface flow, waves, etc., which can weaken the effect of acoustic conditioning taming. In this study, the fish could easily have been attracted by other factors, such as feeding on water zooplankton, small fish, etc., thereby reducing the attractive effect of feedstuff being delivered in tandem with the sound being played. Therefore, fish need a long adaptation period and conditional response period in open-sea water acoustics acoustic conditioning taming.
Juvenile Pagrus major with established acoustic conditioning were tagged before release to distinguish between experimental and wild fish. The sound-conditioned fish were released into the open-sea area, and on the 1st day after release, 100% of the fish swam to the sound source when the sound played. On the 18th day, this ratio dropped to 0.2%, and the time taken for the fish to swim to the sound source gradually became longer. It was difficult to control the distance from the release point of fish in open-sea waters; some fish had swum far away from the release point.
When the sound was played at the release point, fish farther away from the release point did not swim back to the sound source even though the conditioned reflexes to sound may have still been present, because sound waves cannot effectively travel far. Compared with the simple environment of the laboratory tank, the environment of the open-sea area was complex and changeable. Fish released into the open sea were easily affected by currents, the seabed terrain, plankton, water noise, predators, and other factors, which made the behavior of fish subject to comprehensive influences from many aspects. At the time of playing the sound, the fish might have been avoiding predators, already be fully fed, or resting on the reef, and were thus unable or unwilling to swim back to the sound source. Underwater sound signals are gradually weakened in the process of transmission, and the effective transmission distance is limited. Fish swimming outside this range would not have perceived the sound signals.

4.3. Elimination of Conditioned Reflexes to Sound

Zhang Guosheng [37,42] pointed out that non-bone bladder species such as Pagrus major are sensitive to sound, and the most sensitive frequency range is 200–600 Hz. The results of this experiment also showed that the fish were sensitive to the 400 Hz square-wave continuous sound, a positive acoustic property, and could retain a certain memory ability for the sound stimulus, which was consistent with the results of Fay RR’s studies [38,55].
Regarding the neural mechanism of forming a conditioned reflex, Pavlov proposed the idea of “temporary contact connected”; eventually, it was understood that the connection site should occur between the conditioned stimulus center and the unconditioned stimulus center of the cerebral cortex [56]. Mei Zhentong demonstrated that temporary connections of the conditioned reflexes are established between the sensory and motor centers of the cerebral cortex [57]. The original conditioned reflex was balanced by reverse reinforcement for elimination.
The aim of this study was to assess fish after they had established sound acoustic conditioning memory. In this study, the conditioned response of Pagrus major to sound was gradually eliminated using the negative feedback mode of only playing the sound without feeding bait. As the experiment continued, the response time and aggregation time exhibited an increasing trend, whereas the residence time showed a continuously decreasing trend. The continuous negative feedback of only playing sound without feeding made the sound gradually lose its attraction to the fish; the fish gradually moved away from the sound source, and eventually no longer gathered towards the source when playing the sound. After 22 negative feedback tests, the sound was no longer attractive to the fish, meaning that the “sound–food” neural connection established by the acoustic conditioning taming had been eliminated. Therefore, attention should be paid to the possibility of eliminating the sound conditioning of fish established by acoustic taming when applying acoustic conditioning taming technology in marine ranching.
Due to the vast areas involved in marine ranching, it takes a certain amount of time for fish to reach the source of a sound after hearing it. If the sound stops before the fish reaches the sound source and the fish receives no reward (feedstuff), this is “negative feedback”. According to the results of this study, after 22 “negative feedback” events, the acoustic conditioning taming technology will no longer be effective in marine ranching. Therefore, this study suggests that the “negative feedback” effect should be fully considered in the construction of marine ranching systems, and as many devices which can provide “sound–food” should be installed as possible; in addition, the time of each acoustic conditioning taming event should be set according to the range of marine ranching, so as to maintain the “sound–food” neural relationship of fish in marine ranching. In this way, the survival rate of fish in marine ranching systems can be improved, and selective fishing can subsequently be performed.

4.4. Application Prospects of Acoustic Conditioning Taming Technology

Offshore fishery resources have seriously declined due to overfishing and man-made water pollution [58,59,60]. Marine ranching systems and their enhancement are an effective way to increase fishery resources, and they have gradually entered a new stage of development [61,62]. Although Hu et al. carried out the acoustic conditioning experiments on black seabreams in Xiangshan Bay Sea Ranch [63], but they only conducted the experiment on the application of the acoustic conditioning system they designed. At present, the application of acoustic conditioning technology has not been realized in the construction of marine ranching national demonstration areas in China. Acoustic conditioning taming technology has broad application prospects, because it is one of the most widely available fish behavior control technologies [28]. After the fish that have been acoustically tamed and established conditioned reflexes to sound are released into the sea, the survival rate of the released fish could be improved via artificial feeding with sound aggregation before they have learned to search for food by themselves. However, due to the complex noise environment in seawater and the Doppler effect of sound waves [64], the propagation distances of acoustic conditioning taming sound waves are limited. Moreover, there are many factors that can affect the behavior of fish in an actual marine environment. When acoustic signals are weakened, the impact of acoustic waves becomes smaller than that of other factors, and it can no longer play a role in attracting fish into groups. Therefore, the question of how to improve the attractive effects through the use of acoustic conditioning taming technology in marine ranching requires further study. We believe that a number of acoustic conditioning taming devices that can make sound regularly, feed quantitatively, and have image recording and transmission functions should be set up in marine ranching to continuously tame released fish and strengthen the impact of the sound. At the same time, the multi-point deployment of automatic taming devices can form an acoustic conditioning taming network to increase the action area and effects. This model has wide application prospects in acoustic conditioning taming marine ranching systems and the enhancement of fish stocks.

5. Conclusions

In the context of the nationwide promotion and construction of marine ranching systems, it is of great significance to study acoustic conditioning taming technology, which is one of the key technologies for controlling and managing the behavior of target organisms. In this study, we tamed juvenile Pagrus major using 400 Hz square-wave continuous tones for eight days in the laboratory and 15 days in an open-sea area. At the same time, the elimination of conditioned reflexes to sound and applications in marine ranching were tested. The Gaussian model was used to regression-fit the distribution of fish in the tank; the fitting degree was 91.79%. In both the laboratory and open-sea area tests, over time, the response time and aggregation time of the fish showed shortening trends, and the residence time and aggregation rate showed increasing trends. Good conditioning was established after four days of acoustic conditioning taming in the laboratory; it took longer to establish a conditioned response to sound in the open-sea area, and good conditioning was established after the 18th acoustic conditioning taming event. Juvenile Pagrus major with established acoustic conditioning were tagged before release to distinguish between experimental and wild fish. The sound-conditioned fish were released into the open-sea area, on the 18th day, 0.2% of the released fish swam to the sound source when the sound was played. After the 24th day, no fish gathered in the area near the sound source. This study assessed for how long fish responded after establishing sound acoustic conditioning memory. In this study, the conditioned response of Pagrus major to sound was gradually eliminated using the negative feedback mode of playing the sound without feeding bait. After 22 negative feedback tests, the sound was no longer attractive to the fish, meaning that the “sound–food” neural connection established by the acoustic conditioning taming had been eliminated.
The results of this study show that acoustic conditioning taming technology is an effective method of controlling fish behavior, and it is feasible to apply this technology in the construction of marine ranching systems. We believe that a number of acoustic conditioning taming devices, which can make sound regularly, feed quantitatively, and exhibit image recording and transmission functions, should be set up in marine ranching to continuously tame the released fish and strengthen the impacts of the sound. At the same time, the multi-point deployment of automatic taming devices can form an acoustic conditioning taming network to increase the action area and its effects. We hope that this study will provide a theoretical and data basis for the construction of acoustic conditioning taming marine ranching systems.

Author Contributions

H.Y. and P.C. designed this study. H.Y. and Y.Z. conducted the acoustic conditioning taming experimental. H.Y. processed and analyzed data and wrote the original manuscript. P.C. and Y.Z. helped with data analysis and reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research is funded by (1) Central Public-interest Scientific Institution Basal Research Fund, CAFS, China (2020TD06, 2021SD02); (2) R&D Projects in Key Areas of Guangdong Province, China (2020B1111030002).

Data Availability Statement

The raw data supporting this article are available on request from the authors. The data are not publicly available due to privacy policy.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Otolith structure of a fish. Image Credits: Lasse Amundsen.
Figure 1. Otolith structure of a fish. Image Credits: Lasse Amundsen.
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Figure 2. Structure of the inner ear of a fish. Image Credits: Youyulehao.
Figure 2. Structure of the inner ear of a fish. Image Credits: Youyulehao.
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Figure 3. Sketch of the experimental acoustic conditioning taming tank.
Figure 3. Sketch of the experimental acoustic conditioning taming tank.
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Figure 4. Images of the acoustic conditioning taming experimental setup in the open water.
Figure 4. Images of the acoustic conditioning taming experimental setup in the open water.
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Figure 5. Schematic diagram of the acoustic conditioning taming method in laboratory.
Figure 5. Schematic diagram of the acoustic conditioning taming method in laboratory.
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Figure 6. Spatial distribution frequency of juvenile Pagrus major in the control tank (a) and test tank (b) after eight days of training with 400 Hz square-wave continuous tones.
Figure 6. Spatial distribution frequency of juvenile Pagrus major in the control tank (a) and test tank (b) after eight days of training with 400 Hz square-wave continuous tones.
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Figure 7. Changes in the radius of the aggregation area of the juvenile Pagrus major trained with 400 Hz square-wave continuous tones from the 1st day to the 8th day.
Figure 7. Changes in the radius of the aggregation area of the juvenile Pagrus major trained with 400 Hz square-wave continuous tones from the 1st day to the 8th day.
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Figure 8. The behavioral responses of juvenile Pagrus major before the sound was played (a), when sound was playing (b), and after the sound had finished playing (c).
Figure 8. The behavioral responses of juvenile Pagrus major before the sound was played (a), when sound was playing (b), and after the sound had finished playing (c).
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Figure 9. Changes in the response time (a), aggregation time (b), residence time (c), and aggregation rate (d) of juvenile Pagrus major trained with 400 Hz square-wave continuous tones from the 1st day to the 8th day.
Figure 9. Changes in the response time (a), aggregation time (b), residence time (c), and aggregation rate (d) of juvenile Pagrus major trained with 400 Hz square-wave continuous tones from the 1st day to the 8th day.
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Figure 10. Changes in the response time, aggregation time, and residence time of juvenile Pagrus major after the elimination of the conditioned reflex test.
Figure 10. Changes in the response time, aggregation time, and residence time of juvenile Pagrus major after the elimination of the conditioned reflex test.
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Figure 11. The behavioral responses of juvenile Pagrus major when the sound was played.
Figure 11. The behavioral responses of juvenile Pagrus major when the sound was played.
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Figure 12. Changes in the response time (a), aggregation time (b), and aggregation rate (c) of juvenile Pagrus major with the elimination of conditioned reflex test.
Figure 12. Changes in the response time (a), aggregation time (b), and aggregation rate (c) of juvenile Pagrus major with the elimination of conditioned reflex test.
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Figure 13. Changes in the time required to swim to the sound source and occurrence rate of juvenile Pagrus major.
Figure 13. Changes in the time required to swim to the sound source and occurrence rate of juvenile Pagrus major.
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Table
Table 1. Description of the measured parameters.
Table 1. Description of the measured parameters.
NumberParameterDescriptionRelated Reference
1Aggregation areaThe concentration areas of the distributions of the fish when sound was played. This parameter was calculated using the Gaussian distribution model.LIANG, J. 2014. [49]
2Response timeThe time from when the sound was played to the time when the fish entered the aggregation area.ZHANG, G.S. 2010. [37]
3Aggregation timeThe time from when the sound was played to the time when there were no fish entering the aggregation area.JIANG, Z.Y. 2008. [38]
4Residence timeThe time from when no fish were in the aggregation area to when 70% of fish had drifted away from the aggregation area.YUAN, H.R. 2011. [46]
5Aggregation rateThe proportion of fish gathered in the aggregation area compared with the total number during the aggregation time.TIAN, F. 2012. [50]
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Yuan, H.; Zhou, Y.; Chen, P. Research on the Acoustic Conditioning Taming on Fish and Application in Marine Ranching. Water 2023, 15, 71. https://doi.org/10.3390/w15010071

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Yuan H, Zhou Y, Chen P. Research on the Acoustic Conditioning Taming on Fish and Application in Marine Ranching. Water. 2023; 15(1):71. https://doi.org/10.3390/w15010071

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Yuan, Huarong, Yanbo Zhou, and Pimao Chen. 2023. "Research on the Acoustic Conditioning Taming on Fish and Application in Marine Ranching" Water 15, no. 1: 71. https://doi.org/10.3390/w15010071

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