Improvement on the Effectiveness of Marine Stock Enhancement in the Artificial Reef Area by a New Cage-Based Release Technique

ZHANG Junbo, HE Yufeng, GUO Zhixing, JI Shuheng, ZHANG Shuo,TANG Yanli, SHENG Huaxiang, WAN Rong,5), and KITAZAWA Daisuke

1) College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China

2) College of Economics and Management, Shanghai Ocean University, Shanghai 201306, China

3) Marine Hazard Mitigation Service, Ministry of Natural Resources, Beijing 100194, China

4) College of Fisheries, Ocean University of China, Qingdao 266003, China

5) National Engineering Research Center for Oceanic Fisheries, Shanghai Ocean University, Shanghai 201306, China

6) Institute of Industrial Science, the University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8574, Japan

Abstract The release technique, affecting the survival rate of fish species released for stock enhancement, plays a vital role in the effectiveness of the enhancement. In order to improve the probability of released fish settling down to bottom, a new cage-based release technique was designed and tested via a water tank with artificial reef models. Two coral reef fish species, Sebastes schlegelii and Paralichthys olivaceus were assessed using this technique. Fish behavior and distribution in water tank were recorded and compared with the traditional release release techniques. Results showed that in the case of cage-based release technique: 1) when the release process is just finished, the distribution index (DI) of juveniles S. schlegelii and P. olivaceus were 97.8% and 98.9% at reef area, 40% and 71.1% at release point, respectively, which was higher than those using two alternative techniques; 2) its impact duration was less than that in the other two conditions, where the DI within 4 hours was higher after releasing, especially for S. schiegelii. These findings indicated that the new cage-based technique could release the fish into the specified location, and has a potential to mitigate the stress reaction of fish caused by releasing process.

Key words release technique; cage-based device; distribution patterns; distribution index; stock enhancement

1 Introduction

The decline of offshore fishery resources, due to marine environmental pollution and overfishing, has become a global concern (Kitade, 2018; Rhodeset al., 2018). Stock enhancement, releasing the hatched juvenile fish into the resource-depleted waters, is regarded as a potential way to restore marine fishery resources and of practical significance for the sustainable development of fishery (Garlock and Lorenzen, 2017).

The effectiveness of stock enhancement is mainly affected by quality of juveniles, ecological capacity, release technique and post-release management (Blaxter, 2000;Aprahamianet al., 2003; Li and Qiu, 2008; Liang, 2013).An appropriate release technique can not only improve the survival rate of released juveniles, but also reduce the costs of stock enhancement (Lamadrid, 2004; Taylor, 2016).Traditional release techniques include the direct release and the boat-based chute release. However, the existing techniques only release fish at the surface of water, where most of juveniles cannot be released to the designated water layers during settling down process (Taylor, 2016).Meanwhile, these release techniques may generate external stimuli to fish (e.g., physical impact) during the releasing process. Fish may have a high stress reaction under this situation, thus flee quickly from the specified location after releasing, resulting in exposure of fish to the unexpected water condition and its predator.

However, few studies focus on release technique (Williams, 2015; Taylor, 2016; Demirci, 2019). Related studies revealed that sea cucumber (Apostichopus japonicus)larvae can be washed away from the original releasing location and preyed by sea stars (Asterina pectinifera),which is one of the main reasons for its low survival rate after releasing (Tanaka, 2000; Rougieret al., 2013).Lamadrid (2004) developed a chute device and applied to gilthead sea bream (Sparus aurata) in order to increase the survival rate of released fish. Although this device has avoided fish collision with water during releasing, high mortality during the process of settling down is still an unresolved issue (Taylor, 2016). In order to reduce the predation rate of the releasing process, Salayo (2020)released uncovered short PVC pipes with abalone (Haliotis asinina) juveniles to spaces between corals and rubbles. But the release time was limited, since it can only be applied when tides are not turbulent. It is indispensable to quickly settle the juveniles on the water bottom through existing release techniques.

To develop a new technique that can precisely release juveniles with lower mortality in stock enhancement practice, a cage-based device is designed and applied to two high economic value fish speciesSebastes schlegeliiandParalichthys olivaceusin laboratory condition as a first step. Water tank experiment is one of the effective approaches to understand the behavior of the juveniles after releasing, considering the difficulty in observing the effects of releasing technologies in the real sea. The experiment was conducted to observe fish behavior and distribution in water tank with artificial reefs through cage-based, chute and direct release technologies. The purpose of this study is to release juveniles at the designated layer of water including the water bottom for enhancing their settlement, and to evaluate the impact duration on released juveniles by the different release techniques.

2 Materials and Methods

2.1 Experimental Water-Tank

Experiment was carried outviaa water tank (L × W ×H, 380 × 200 × 110 cm) at Marine Fish Behavior Laboratory of Ocean University of China. Water depth above the floor of the aquarium was 50 cm. A video camera(EZVIZ S1A, Hangzhou Hikvision Technology Co., Ltd.)was placed at the top of the tank to record fish behavior and their distribution. The bottom of water tank was divided into 18 × 32 grids by water proof tape. The internal area was enclosed by the artificial reef model and the adjacent grid area around models was used as the reef area (Fig.1). Blue color shows three locations of artificial reef model, and the radiation area of the artificial reef is defined as the reef area, where the red color is the release point, which is the vertical projection point at the bottom of the water tank and covers four grids.

Fig.1 Sketch of the water tank (a) and the bottom (b).

2.2 Experimental Devices

2.2.1 Cage-based device and chute device

The stainless-steel cage-based device was originally developed in this study which was a foldable structure with release and recycle ropes (Fig.2). The bottom of cage was equipped with a movable iron plate in order to release the juveniles. The top of cage has a removable net cover. Its periphery was also covered by the nylon mesh nets with twine diameter of 2 mm, to keep and protect fish during releasing. The cage is straightened and fixed before using.The experimental fish was moved into the cage from the top and then the device was covered. When the cage reached the designated layer of water, fish was released through the movable iron plate. The chute device is made of a white PVC pipe with a full length of 1 m and a diameter of 10 cm.

Fig.2 Sketch of the cage-based release device (a) and the chute device (b).

2.2.2 Artificial reef model

The structural design principle of artificial reef can be divided into three aspects: flow field effect, biological effect and hidden effect (Jianget al., 2019). The artificial reef model designed for reef fish is mostly cube structure with a side length from 15 to 30 cm (Liuet al., 2018). In this regard, a cubic artificial reef model (20 × 20 × 20 cm)made of PVC material was considered in this experiment(Fig.3). The diameter of the circular holes on the reef surface was 5 cm. These models were immersed in seawater for 3 d before using.

Fig.3 Sketch of the artificial reef model.

2.3 Experimental Fish

S. schlegeliiandP. olivaceusmainly inhabit in the reef area of offshore seabed and are widely distributed in the coastal areas of northern China, Japan and Korea (Wuet al., 2004; Fenget al., 2014). These two species play an important role in marine stock enhancement. In this study,200S. schlegelii(4.5 ± 0.5 cm, body length) and200P.olivaceus(4.8 ± 0.6 cm, full length) were purchased from Qingdao Ruiyuan Aquatic Seedling Aquaculture Co., Ltd.All the fish were reared in the storage pool for one week before the experiment.

2.4 Experiment Design

For each specie, experiments were carried out using the cage-based device, chute and direct release techniques,respectively. Each release technique experiment was repeated three times. 30 fish were randomly selected from 200 samples in the storage pool for each experiment. And they were randomly mixed in the storage pool after one experiment was finished, to ensure the randomness of the experimental samples and the experimental results are formed by different releasing techniques rather than the characteristics of fish itself. In order to avoid the effect of the previous experiment process on the fish, time interval of each experiment was set to one day. During each experiment, fish within the reef area was continuously recorded by a video camera for 7 h. The position and the number of fish in each grid were obtained from the video camera data to compare the release efficiency of three techniques. Hourly distributions of juveniles in the reef area were analyzed to further evaluate the impact duration of fish under different release techniques.

Fish-bait and oxygen pump were not used during the experiment to reduce external influence on the distribution of fishes. The parameters of water quality were set as follows: water temperature (22 ± 0.3)℃, salinity 34 ± 1 psu,pH 7.1 ± 0.1, and dissolved oxygen ca. 6 mg L-1. In addition,the indoor light intensity was 135 ± 5 lx. Sea water in the tank was circulated for 24 h, and a half tank of seawater was changed every 4 d.

2.5 Statistical Analysis

Distribution index (DI) is used to analyze the dynamic change in the quantities ofS. schlegeliiandP. olivaceusat the reef area and the release point for different release techniques.DIrepresents the instantaneous ratio of fish counts stayed in the grid to the total number released. The equation is as follows:

whereNiis the number of observed fish inith grid,Nis the total number of released fishes, andnis the number of grids.

TheDIof the juvenile fish in the reef area was calculated every hour, and the differences among the three release techniques were compared by Repeated Measures One-way ANOVA (SPSS Version 21.0).

3 Results

3.1 Distribution Patterns

Fig.4 The initial distribution index of S. schlegelii at reef area and release point after releasing. Error bars indicate the standard deviation, and different lowercase letters mean the significant difference (P ＜ 0.05).

Fig.5 The initial distribution pattern of S. schlegelii (a Direct, b Chute, c Cage-based device) after releasing.

TheDIs of fish in the reef area and release point just after releasing finished (at the initial time) were shown in Fig.4. TheDIofS. schlegeliireleased by the cage-based device reaches 97.8%. It was significantly higher than that released by chute device (P ＜0.05), while no significant difference in the DI could be found between the cage-based and the direct release techniques. However,40% of individuals gathered around the release point when using the cage-based device, which was significantly higher than those of the other two techniques (P ＜0.05). The initial distribution patterns of fish were represented in Fig.5.S. schlegeliimainly gathered in the center of the tank (cage-based release technique), while they distributed widely in the reef area after applying the direct and the chute release techniques.

Fig.6 The initial distribution index of P. olivaceus at reef area and release point after releasing. Error bars indicate the standard deviation, and different lowercase letters mean the significant difference (P ＜ 0.05).

ForP. olivaceus, theDIof juveniles released by the cage-based device was 98.9%, which was significantly higher than that of direct release technique (P ＜0.05), but no significant difference in theDIcould be found compared with that in chute release technique (Fig.6). 71.1%ofP. olivaceusreleased by the cage-based device gathered at the release point, significantly higher than that by other techniques (P ＜0.05).P. olivaceusshowed a central dense distribution pattern (Fig.7) when using the cagebased device technique. The juveniles released by chute and direct techniques were found mainly distributed at the left and outer parts of the reef area, showing a central and central-left distribution pattern, respectively.

Fig.7 The initial distribution pattern of P. olivaceus (a, Direct; b,Chute; c, Cage-based device) after releasing.

3.2 Impact Duration of Release Technique on Fish

An hourly observation on the behavior of juveniles was conducted after releasing. As shown in Fig.8, juveniles ofS. schlegeliireleased by the cage-based device stayed at the reef area for a long time. After 1 hour from the release,theDIofS. schlegeliiwas 51.1% for the cage-based device, 40% for chute, and 42.2% for the direct release technique. During the first 4 h, theDIusing the cagebased device was 10% higher than those applying the other two techniques. Then the difference shrank gradually, and theDItended to be stable and remained between 45% and 60% from the 5th hour. The juveniles at the reef area showed no obvious swimming behavior, with the majority resting near the edge of the reef or entering into the reef; while those outside of the reef area were found mainly distributed around the edge of the bottom, swimming along the inside walls or crossing the reef area to the edge of the tank. In the case ofP. olivaceus, from the 2nd hour after releasing, theDIdecreased to 13.3%(cage-based device), 11.1% (chute), and 5.7% (direct), respectively. Then their differences decreased gradually and theDIs changed between 0% and 8%. TheDIfor the cage-based device was higher than the others within 4 h after releasing. After that, theDIfor the three techniques was around 0%.

Fig.8 The dynamic changes in distribution index of S. schiegelii (a) and P. olivaceus (b) at reef area. Error bars indicate the standard deviation.

4 Discussion

In this study, the initial distribution of juvenile fish after releasing was significantly affected by the release technique. Compared with the chute and the direct release techniques, theDIofS. schlegeliiandP. olivaceususing the newly developed cage-based device was the highest,and most individuals stayed at the release point, which is the specified location as expected. A similar result can be observed in real sea conditions, where a remote-open cage device was applied to red snapper (Lutjanus campechanus)and gray triggerfish (Balistes capriscus) in the northern Gulf of Mexico (Williamset al., 2015). However, fish were distributed widely in the reef area when applying the direct and chute release techniques. A possible explanation is that both techniques released fish at water surface,and fish swam randomly away from the release point.Taylor (2016) found that if a chute with its length equal or greater than the water depth is used to release sea cucumber juveniles in high-energy marine environments of northern Australia, an intensive distribution of sea cucumber around the release area can be observed.

In general, the value ofDIkeeps relatively stable for one certain fish in an artificial reef, depending on the size and shape of the reef. TheDIofS. schlegeliiremained at about 50% after 1 h of release,while that ofP. olivaceuspresented a decreasing trend during the observation period,and almost all of the juveniles left the reef area after 4 h.This was different from the findings of previous study which showed a 23% attractive rate at the reef area (Wuet al., 2004). That may be attributed to the difference of reef and tank design between the experiments. This also demonstrated that the design of artificial reefs affects fish behavior around the reef (Simonet al., 2011; Zhou, 2011;McLeanet al., 2015; Laymanet al., 2016). Compared with the direct and the chute release techniques, mostS.schlegeliireleased by the cage-based device stayed around the reef area for a long time, and we can clearly find itsDIwas the highest within 4 h after releasing, which demonstrated that the impact duration of cage-based device is less than the other two techniques. This is because that the cage-based device could mitigate fish’s stress reaction generated by external stimuli in the releasing process. Both chute and direct release techniques cause a relatively heavy physical impact on fish during releasing, probably bringing more stimuli to the released fish for about 4 h.Previous studies showed that long-term stress reaction resulted in a high mortality, a weakened immune system and a lower fertility of released fish (Liu, 2007).

At the present stage, it is reported that two effective device release techniques,i.e., the remote-open cage device and the long chute, were applied to the stock enhancement in real sea (Williamset al., 2015; Taylor, 2016).The remote-open cage was limited to artificial habitats without barriers around the reef, because the door was at one side of the device, cameras are therefore required to determine whether the cage door opens or not after it reached to the targeted area. Although a long chute (from water surface to bottom) can avoid this weakness, a high cost of labors hinders its wide application. The cage-based device newly developed in this study can be opened from the bottom side, which might be suitable for areas with complex seabed types, and is low-costly, easily operated and reusable.

However, the cage-based device was only tested in water tank without water current. Juvenile fish may be washed away in real sea conditions due to water current during the process of settling down, resulting in a lowDIin the reef area, especially for bottom and near-bottom fish species. The influence of water flow needs to be considered in future studies to understand if the juveniles could return to the favorable habitat after releasing (Gitschlag and Renaud, 1994; Hannahet al., 2012; Hairet al., 2016).Moreover, the mortality or injury of fish juveniles in stock enhancement process caused by predators has been reported as an essential issue to be solved (Allenet al., 2017).Whether the newly developed cage-based device can protect the released juveniles should be further evaluated by water tank experiment with predators, and its practical effectiveness are necessary to be tested in real sea.

5 Conclusions

The newly developed cage-based device in this study has been tested successful in laboratory condition. The main conclusions are summarized in the following aspects:1) releasing juveniles at the designated layer of water including the water bottom for enhancing their settlement;2) potentially mitigating fish’s stress reaction generated by external stimuli from the releasing process; 3) using available and inexpensive materials, which is reusable and easily-operated. The cage-based device would provide an effective release technique for improving the release effect of reef fish after it is further studied in the real sea conditions.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Nos. 41501560, 41606110),the Young Orient Scholars Programme of Shanghai (No.QD2017038), and the Shanghai Special Research Fund for Training College’s Young Teachers (No. ZZSHOU 18025). The authors would like to thank the assistance of the staffs in marine ranching laboratory in Ocean University of China.