Abstract
Poor survival of seeds reduces the production efficiency of the sea cucumber Apostichopus japonicus in pond culture. We investigated the effects of sea mud on the movement-related behaviors of A. japonicus with different body sizes. Mud significantly decreased crawling behavior and wall-reaching behavior in small seeds (~ 1 g of body weight), but not in the large ones (~ 2.5 g of body weight). These behaviors were significantly greater in the large seeds of A. japonicus than those in the small individuals when they were both on the mud. This clearly suggests that mud has negative effects on the movement-related behaviors of small seeds, but not on large individuals. We further assessed the effects of inevitable transport stress on the movement-related behaviors of A. japonicus on mud. Significantly poorer performances in crawling behavior, wall-reaching behavior and struggling behavior were observed in stressed A. japonicus (both sizes) than those in unstressed groups. These new findings indicate that transport stress further increases the adverse effects on the movement-related behaviors of A. japonicus on mud. Moreover, we investigated whether adverse effects can be reduced when individuals are directly seeded onto artificial reefs. Crawling behavior, wall-reaching behavior and struggling behavior in stressed A. japonicus (both sizes) seeded onto artificial reefs were significantly greater than those on mud, whereas artificial reefs did not significantly improve the crawling and struggling behaviors of unstressed small seeds. These results collectively indicate that mud and transport stress show negative impacts on the movement-related behaviors of sea cucumbers. Artificial reefs greatly reduce these adverse effects and probably contribute to improving the production efficiency of sea cucumbers in pond culture.
Similar content being viewed by others
Introduction
Aquaculture plays an essential role in providing food and nutrition. Production from aquaculture and fisheries reached 214 million tonnes with a value of USD 424 billion1. In China, sea cucumbers Apostichopus japonicus are becoming more popular recent years because of their high medicinal and nutritional values2, compared to other cultured species. The increasing market demands greatly stimulate the aquaculture of A. japonicus, with an annual production of 222,707 metric tons in 2021 in China3. Pond culture plays a leading role in producing sea cucumbers4. The culture area of ponds, for example, is 425,522 hectares in 2021 in China3. Improving production efficiency is essential in aquaculture. Seed mortality, however, greatly reduces the production efficiency in the pond. Almost 100% of small seeds of sea cucumber (1 g of wet weight) died when they were directly seeded into the pond in Dalian5. This indicates body size is an important factor affecting the survival of seeds in pond culture6. Large seeds (> 2.5 g of wet weight) are commonly used in pond culture because of better survival. Small seeds (< 1 g of wet weight) are kept at the hatchery for ~ 3 months until reaching the appropriate size6. However, large seeds are costly to reach the same seeding net biomass compare with small seeds, which directly decreases the economic benefits. It is important to know the reasons for the mortality of seeds and accordingly establish an effective method to improve the production efficiency of sea cucumbers in pond culture.
The substrate in aquaculture pond is mainly silt which is difficult for sea cucumbers to crawl, because they cannot attach to the mud substrate7. Sea cucumbers were seldom found in muddy habitats in the field, despite the abundance of organic matter8,9. Therefore, it is reasonable to speculate that sea cucumbers probably get stuck in the mud and may consequently lead to death. Further, sea cucumbers are inevitably exposed to stress (e.g. handling and anoxia stresses) when they are transported from the seed hatchery to a pond. Environmental stress adversely affects the movement-related behaviors of sea cucumbers. For example, small A. japonicus exposed to high-intensity handling stresses showed decreased movement and foraging behaviors10. Thus, transport stress probably increases the adverse effects on the movement-related behaviors of sea cucumbers on mud. Juvenile sea cucumbers choose suitable habitats in the field for better fitness11,12. It has been well documented that artificial reefs (e.g. oyster shells and tiles) greatly improve the aggregation behavior of sea cucumbers13,14. Therefore, it is worth investigating whether directly seeding sea cucumbers onto artificial reefs reduces the adverse effects.
The purpose of the present study is to investigate the behavioral responses of A. japonicus to mud under various conditions, which may provide valuable information for pond culture. We ask (1) whether mud adversely affects the movement-related behaviors of A. japonicus in different body sizes; (2) whether transport stress increases the adverse effects on the movement-related behaviors on mud; (3) whether adverse effects can be reduced by seeding individuals onto the artificial reefs.
Results
Experiment I
Crawling behavior
There was no significant difference between groups M2 (21.07 ± 1.28) and W2 (20.87 ± 1.33) in the number of crawling cycles (t = 0.108, P = 0.914) (Fig. 1B). The number of crawling cycles in group M1 (17.03 ± 1.48) was significantly lower than that in group W1 (22.03 ± 1.26) (t = 2.575, P = 0.013) (Fig. 1A) and group M2 (21.07 ± 1.28) (t = 2.060, P = 0.044) (Fig. 1C).
The numbers of crawling cycles in groups M1 and W1 (A), groups M2 and W2 (B), and groups M1 and M2 (C). Crawling distance for groups M1 and W1 (D), groups M2 and W2 (E), and groups M1 and M2 (F). The proportion of individuals reaching the wall for groups M1 and W1 (G), groups M2 and W2 (H), and groups M1 and M2 (I). Group W1: small seeds without mud. Group W2: large seeds without mud. Group M1: small seeds with mud. Group M2: large seeds with mud. The asterisks * and ** mean P < 0.05 and P < 0.01, respectively.
Crawling distance was not significantly different between group W1 (1124.13 ± 102.80 mm) and group M1 (874.51 ± 88.31 mm) (t = 1.842, P = 0.074) (Fig. 1D). Crawling distance in group W2 (923.36 ± 82.81 mm) was significantly shorter than that in group M2 (1498.31 ± 142.57 mm) (t = 3.487, P = 0.002) (Fig. 1E). Group M2 (1498.31 ± 142.57 mm) showed significantly longer crawling distance, compared to group M1 (874.51 ± 88.31 mm) (t = 3.719, P = 0.001) (Fig. 1F).
Wall-reaching behavior
No significant difference was found in the proportion of individuals reaching the wall between groups M2 (83.33 ± 3.33%) and W2 (96.67 ± 3.33%) (Mann–Whitney U = 30, P = 0.065) (Fig. 1H). Group M1 (3.33 ± 3.33%) showed a significantly lower proportion of individuals reaching the wall, compared to group W1 (100 ± 0.00%) (Mann–Whitney U = 36, P = 0.002) (Fig. 1G). The proportion of individuals reaching the wall was significantly greater in group M2 (83.33 ± 3.33%) than that in group M1 (3.33 ± 3.33%) (Mann–Whitney U = 36, P = 0.002) (Fig. 1I).
Experiment II
Crawling behavior
The number of crawling cycles in group S1 (5.57 ± 0.90) was significantly lower than that in group M1 (17.03 ± 1.48) (t = 6.610, P < 0.001) (Fig. 2A). Consistently, significantly lower number of crawling cycles occurred in group S2 (9.90 ± 1.34) than that in group M2 (21.07 ± 1.28) (t = 6.015, P < 0.001) (Fig. 2F).
The number of crawling cycles (A), crawling distance (B), proportion of individuals reaching the wall (C), proportion of individuals that failed to struggle (D), and the duration of individuals that failed to struggle (E) for groups S1 and M1. The number of the crawling cycles (F), crawling distance (G), proportion of individuals reaching the wall (H), proportion of individuals that failed to struggle (I), and the duration of individuals that failed to struggle (J) for groups S2 and M2. Group S1: stressed small seeds with mud. Group S2: stressed large seeds with mud. Group M1: small seeds with mud. Group M2: large seeds with mud. The asterisks *, ** and ***mean P < 0.05, P < 0.01 and P < 0.001, respectively.
Significantly shorter crawling distance was found in group S1 (324.79 ± 60.34 mm) than that in group M1 (874.51 ± 88.31 mm) (Mann–Whitney U = 34, P < 0.001) (Fig. 2B). Consistently, group S2 (1037.99 ± 157.75 mm) showed significantly shorter crawling distance than group M2 (1498.31 ± 142.57 mm) (Mann–Whitney U = 92, P = 0.027) (Fig. 2G).
Wall-reaching behavior
No significant difference was found in the proportion of individuals reaching the wall between groups S1 (6.67 ± 4.22%) and M1 (3.33 ± 3.33%) (Mann–Whitney U = 15, P = 0.699) (Fig. 2C). Group S2 (26.67 ± 12.29%) showed a significantly lower proportion of individuals reaching the wall, compared to group M2 (83.33 ± 3.33%). (Mann–Whitney U = 33.50, P = 0.009) (Fig. 2H).
Struggling behavior
Group S1 (86.67 ± 6.67%) showed a significantly greater proportion of individuals that failed to struggle than group M1 (30.00 ± 14.38%) (t = 3.576, P = 0.009) (Fig. 2D). Consistently, a significantly greater proportion of individuals that failed to struggle occurred in group S2 (46.67 ± 18.38%) than that in group M2 (3.33 ± 3.33%) (Mann–Whitney U = 7.50, P = 0.043) (Fig. 2I). The duration of individuals that failed to struggle was significantly longer in group S1 (1115.67 ± 104.19 s) than that in group M1 (396.40 ± 113.88 s) (t = 4.660, P < 0.001) (Fig. 2E). Consistently, significantly longer duration of individuals that failed to struggle was found in group S2 (508.47 ± 110.67 s) than that in group M2 (16.50 ± 16.50 s) (Mann–Whitney U = 248, P < 0.001) (Fig. 2J).
Experiment III
Crawling behavior
There was no significant difference in the number of crawling cycles between groups M1 (17.03 ± 1.48) and UR1 (20.20 ± 1.33) (t = 1.593, P = 0.117) (Fig. 3A). The number of crawling cycles was significantly higher in group SR1 (9.17 ± 0.74 times) than that in group S1 (5.57 ± 0.90) (t = 3.087, P = 0.003) (Fig. 3B). The number of crawling cycles in group SR2 (25.87 ± 2.10) was significantly higher than that in group S2 (9.90 ± 1.34 times) (t = 6.397, P < 0.001) (Fig. 3C).
The number of crawling cycles for groups UR1 and M1 (A), groups SR1 and S1 (B), and groups SR2 and S2 (C). Crawling distance for groups UR1 and M1 (D), groups SR1 and S1 (E), and groups SR2 and S2 (F). The proportion of individuals reaching the wall for groups UR1 and M1 (G), groups SR1 and S1 (H), and groups SR2 and S2 (I). The proportion of individuals that failed to struggle for groups UR1 and M1 (J), groups SR1 and S1 (K), and groups SR2 and S2 (L). The duration of individuals that failed to struggle for groups UR1 and M1 (M), groups SR1 and S1 (N), and groups SR2 and S2 (O). Group S1: stressed small seeds with mud. Group S2: stressed large seeds with mud. Group M1: small seeds with mud. Group SR1: stressed small seeds with mud and artificial reefs. Group SR2: stressed large seeds with mud and artificial reefs. Group UR1: unstressed small seeds with mud and artificial reefs. The asterisks *, ** and ***mean P < 0.05, P < 0.01, P < 0.001, respectively.
No significant difference was found in crawling distance between groups M1 (874.00 ± 88.31 mm) and UR1 (1033.13 ± 84.53 mm) (t = 0.831, P = 0.412) (Fig. 3D). The crawling distance in group SR1 (639.02 ± 59.08 mm) was significantly longer than that in group S1 (324.79 ± 60.33 mm) (t = 3.721, P = 0.001) (Fig. 3E). Consistently, significantly longer crawling distance occurred in group SR2 (1617.09 ± 170.35 mm) than that in group S2 (1037.99 ± 157.75 mm) (Mann–Whitney U = 65, P = 0.002) (Fig. 3F).
Wall-reaching behavior
The proportion of individuals reaching the wall in group M1 (3.33 ± 3.33%) was significantly lower than that in group UR1 (73.33 ± 9.8%) (Mann–Whitney U = 21, P = 0.002) (Fig. 3G). Group S1 (6.67 ± 4.22%) showed a significantly lower proportion of individuals reaching the wall than that in group SR1 (60.00 ± 11.55%) (Mann–Whitney U = 1.00, P = 0.004) (Fig. 3H). Consistently, a significantly greater proportion of individuals reaching the wall in group SR2 (83.33 ± 9.55%) was found than that in group S2 (26.67 ± 12.29%) (t = 3.641, P = 0.005) (Fig. 3I).
Struggling behavior
No significant difference was detected in the proportion of individuals that failed to struggle between groups M1 (30.00 ± 14.38%) and UR1 (13.33 ± 8.43%) (Mann–Whitney U = 23, P = 0.485) (Fig. 3J). Group SR1 (10.00 ± 6.83%) showed a significantly lower proportion of individuals that failed to struggle compared to group S1 (86.67 ± 6.67%) (Mann–Whitney U = 36, P = 0.002) (Fig. 3K). Consistently, a significantly lower proportion of individuals that failed to struggle occurred in group SR2 (0 ± 0%) than that in group S2 (46.67 ± 18.38%) (t = 2.539, P = 0.029) (Fig. 3L). The duration of individuals that failed to struggle in group M1 (327.90 ± 98.77 s) was not significantly different from that in group UR1 (89.70 ± 49.77 s) (Mann–Whitney U = 536, P = 0.078) (Fig. 3M). Group SR1 (109.27 ± 61.12 s) showed a significantly shorter duration of individuals that failed to struggle, compared to group S1 (1115.67 ± 104.19 s) (Mann–Whitney U = 807, P < 0.001) (Fig. 3N). Consistently, a significantly shorter duration of individuals that failed to struggle occurred in group SR2 (0.00 ± 0.00 s) than that in group S2 (508.47 ± 110.67 s) (t = 2.031, P < 0.001) (Fig. 3O).
Discussion
Mud negatively affects the movement-related behaviors of small A. japonicus
Improving the survival of seeds is crucial for the pond culture of sea cucumbers. In common practice, large individuals (~ 2.5 g) are seeded into the pond for better survival15, despite it greatly reducing the harvested net biomass and the economic benefits. There were no significant differences in the number of crawling cycles and the proportion of individuals reaching the wall of large seeds, whether they were exposed to mud or not. It has been well documented that movement capability is strongly related to the survival of sea cucumbers and sea urchins7,16,17. Crawling behavior is essential for sea cucumbers to move to a suitable place for feeding and habitat18,19,20. The walls of the experimental tanks simulated nearby artificial reefs in pond culture in the present study. These results suggest that mud does not negatively affect the experimental behaviors of larger seeds of sea cucumbers. Seeding small individuals (~ 1 g) is promising to increase economic efficiency, but it remains largely unknown why mass mortality exists when they are seeded in the ponds. This study found that the wall-reaching behavior and crawling behavior of smaller A. japonicus exposed to mud were significantly poorer than those not being exposed. Adhesion to the substrate is necessary for sea cucumbers to carry out the movement-related behaviors13. The mud may not have sufficient surface area for sea cucumbers to adhere7, which consequently reduces the crawling behavior. These results suggest that mud greatly hampers the effective movements of small A. japonicus and consequently prevents them from moving to artificial reefs, even if they are placed nearby. We further found that the crawling distance, the number of crawling cycles and the proportion of individuals reaching the wall of small seeds were significantly smaller than those of large ones, when they were both exposed to mud. This confirms that body size is an important factor affecting the movement-related behaviors of sea cucumbers on mud. A possible explanation is that small A. japonicus has not fully developed its motor capabilities19, which leads to poor performances in crawling and wall-reaching behaviors on mud. These findings explain the rationality of seeding large A. japonicus into the pond.
Transport stress increases the adverse effects on the movement-related behaviors of A. japonicus on mud
Sea cucumber seeds are commonly transported from nurseries to ponds for further culture4,13, which indicates transport stress is inevitable for sea cucumbers in pond culture. The present study found that the proportion of individuals reaching the wall was significantly lower in stressed large seeds than that in the unstressed group. The significantly smaller number of crawling cycles and crawling distance consistently occurred in stressed large seeds than those in the unstressed group. These results clearly suggest that transport stress greatly reduces the ability to move in large seeds, while mud alone does not show negative effects on the behaviors of large individuals. The proportion and duration of individuals that failed to struggle consistently increased in the large seeds after they were stressed. This suggests that transport stress probably decreases the movement-related behaviors of sea cucumbers. Stressed small A. japonicus showed significantly poorer performances in the number of crawling cycles and crawling distance than those in unstressed A. japonicus. The proportion and duration of individuals that failed to struggle were significantly higher in stressed sea cucumbers than those in the unstressed group. This is consistent with the finding of Yang et al.10 who found that the handling stress significantly inhibited the movement and foraging behavior of small A. japonicus (~ 0.8 g). A possible explanation is that small sea cucumbers are particularly sensitive to the adverse environments21,22. These results collectively suggest that inevitable transport stress further increases the adverse effects on the movement-related behaviors of A. japonicus in different sizes (at least ~ 1 g and ~ 2.5 g) on mud. It is important to find a method to minimize transport stress on seeds for pond culture of sea cucumbers.
Artificial reefs reduce the adverse effects of mud on the movement-related behaviors of A. japonicus
Developing an effective approach to reducing the adverse effects is essential to improve the production efficiency of sea cucumbers in pond culture. We found that all experimental behaviors of stressed A. japonicus seeded onto artificial reefs were significantly greater than those placed on mud. These findings suggest that artificial reefs greatly improve the movement-related behaviors of sea cucumbers and probably contribute to their survival in pond culture. Artificial reefs are commonly used to provide habitats4,13 and promote food utilization23,24 for sea cucumbers in pond culture. Seeding stressed sea cucumbers onto artificial reefs is a cost-effective method to increase the production efficiency of pond culture. Interestingly, the struggling behavior and crawling behavior of unstressed small A. japonicus did not significantly improve when they were seeded onto artificial reefs. This indicates that unstressed small A. japonicus are likely to crawl out of the artificial reefs and get stuck in the mud.
Conclusion
There were no significant differences in the number of crawling cycles and wall-reaching behavior of large seeds exposed to mud, compared to those not exposed. Transport stress further negatively affected these movement-related behaviors of A. japonicus on mud. Seeding directly onto artificial reefs is thus an effective approach to improving the movement-related behaviors of sea cucumbers in pond culture.
Mud negatively affected the number of crawling cycles and wall-reaching behavior of small A. japonicus. Stressed small A. japonicus showed significantly poorer performances in the movement-related behaviors, compared to those unstressed on mud. Artificial reefs are beneficial to all the experimental behaviors in stressed small A. japonicus, but not in the unstressed group. We suggest that stressed sea cucumbers should be directly seeded onto artificial reefs in pond culture. Notably, the present study is a short-term experiment based on a laboratory, more evidence from long-term experiments should be collected in the field.
Materials and methods
Sea cucumbers
One thousand sea cucumbers of two different sizes (~ 1 g and ~ 2.5 g of wet body weight, respectively) were separately selected from a local seed hatchery and transported to Dalian Ocean University on 12 December 2021. Large (~ 2.5 g) and small (~ 1 g) seeds of sea cucumbers were maintained in fiberglass tanks (length × width × height: 1150 × 750 × 600 mm) with aeration, fed with a commercial diet (Anyuan Industrial Co., Ltd., China) ad libitum, and were under the natural photoperiod (9 L: 15 D) for two weeks until the experiment began. Water temperature was 11.08 ± 0.66 °C, salinity 32.31 ± 0.81‰ and pH 8.03 ± 0.05 according to weekly measurements (YSI Incorporated, OH, USA).
Experiment I
This study aimed to investigate whether mud negatively affects the movement-related behaviors of sea cucumbers in different body sizes. Mud was collected from the intertidal zone at Heishijiao (121°56′E, 38°87′N), where the mud is similar to that in pond culture. Sea mud was subsequently added to an experimental plastic tank (length × width × height: 250 × 180 × 60 mm) in a thickness of ~ 3 cm. To set groups, five sea cucumbers were placed on the bottom in the center of the experimental plastic tanks with or without mud as follows (Fig. 4A): small seeds without mud (group W1), large seeds without mud (group W2), small seeds with mud (group M1), and large seeds with mud (group M2). Each group contains six replicates (N = 6). Crawling behavior and wall-reaching behavior were subsequently evaluated according to the methods of assessment described below.
Experiment designs for experiments I (A), II (B), and III (C). Crawling behavior (D) and struggling behavior (E) of Apostichopus japonicus.
Experiment II
This experiment was designed to investigate whether transport stress further increases adverse effects on the movement-related behaviors of A. japonicus on mud. To simulate transport stress, sea cucumbers of different body sizes were randomly selected and put into plastic bags filled with seawater in an aerated tank (length × width × height: 750 × 450 × 350 mm) for 3 h. Then, each of the five stressed sea cucumbers was subsequently placed onto the bottom and in the center of experimental plastic tanks (length × width × height: 250 × 180 × 60 mm) to set groups as follows (Fig. 4B): stressed small seeds with mud (group S1), and stressed large seeds with mud (group S2). Each group contains six replicates (N = 6). Crawling behavior, wall-reaching behavior and struggling behavior were evaluated according to the methods of assessment described below.
Experiment III
This experiment investigated whether adverse effects can be reduced when sea cucumbers are seeded onto artificial reefs. Each of the five sea cucumbers was placed in the center of experimental plastic tanks (length × width × height: 250 × 180 × 60 mm) with mud and three connected plastic tubes (diameter × length: 20 × 50 mm, according to Tian et al.25 with some revisions) as follows (Fig. 4C): stressed small seeds (group SR1), stressed large seeds (group SR2) and unstressed small seeds (group UR1). Each group contains six replicates (N = 6). Crawling behavior, wall-reaching behavior and struggling behavior then were evaluated according to the methods of assessment described below.
Crawling behavior
Sea cucumber crawls like earthworms to find a suitable place for feeding and habitat7. Crawling behavior was evaluated to assess the movement of sea cucumbers on the mud, according to Lin26 with some revisions. Crawling behavior was divided into five stages as follows (Fig. 4D): (1) a sea cucumber is in the inactive state; (2) the individual begins contraction; (3) the individual contracts the anus back and gradually moves by contraction of the middle of the body to the mouth; (4) the individual gradually stops contraction and (5) returns to the inactive state. Crawling behavior was recorded for 30 min using a digital camera (Legria HF20, Canon, Japan). One crawling cycle covers the above five stages. The crawling distance was measured using the software Image J (version 1.51n).
Wall-reaching behavior
Sea cucumbers tend to move until they contact the wall of the aquarium and remain there7. This behavior simulated the situation in that sea cucumbers get rid of the mud and successfully move to nearby artificial reefs in the pond. A digital camera (Legria HF20, Canon, Japan) was used to record the behaviors for 30 min and then the collected data was used to calculate the proportion of sea cucumbers reaching the wall.
Struggling behavior
Struggling behavior was evaluated based on Clements et al.27 with some revisions. Sea cucumbers lose their ability to move normally on the mud7, and they try to correct their body posture. If fail to struggle, they may get stuck in the mud and consequently die. The struggling behavior of sea cucumbers on mud was recorded for 30 min using a digital camera (Legria HF20, Canon, Japan) (Fig. 4E). We calculated the proportion and duration of individuals that failed to struggle based on the collected data by using the camera.
Statistical analysis
Kolmogorov–Smirnov test and Levene test were used to analyze the distribution and homogeneity of variance, respectively. The independent-sample t test was used to compare the differences in the number of crawling cycles and the crawling distance in experiment I; the number of crawling cycles, the proportion and duration of individuals that failed to struggle (both between groups M1 and S1) in experiment II; the number of crawling cycles and the crawling distance (except between groups SR2 and S2), the proportion of individuals reaching the wall (between groups SR2 and S2), the proportion and duration of individuals that failed to struggle (both between groups SR2 and S2) in experiment III. Mann–Whitney U test was carried out to analyze the rest of the data, because of non-normal distribution and/or heterogeneity of variance. All data analyses were performed using SPSS 19.0 statistical software. A probability level of P < 0.05 was considered as being significant.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.
References
FAO. The State of World Fisheries and Aquaculture 2022. Towards Blue Transformation (Roma, 2022).
Zhang, L. B. et al. A new system for the culture and stock enhancement of sea cucumber, Apostichopus japonicus (Selenka), in cofferdams. Aquac. Res. 42, 1431–1439. https://doi.org/10.1111/j.1365-2109.2010.02735.x (2011).
Liu, X. Z. China Fishery Statistical Yearbook 2020 (China Agriculture Press, 2022).
Ru, X. S. et al. Development strategies for the sea cucumber industry in China. J. Oceanol. Limnol. 37(1), 300–312. https://doi.org/10.1007/s00343-019-7344-5 (2019).
Zhou, J.B., Gao, G.B., Wang, X.H. Observation, analysis and discussion on the ecological nursery, rearing and morbidity of sea net tanks for sea cucumber. 5, 53–55 (2006)
Chang, Y., Ding, J., Song, J. & Yang, W. Biology and Aquaculture of Sea Cucumbers and Sea Urchins (Ocean Press, 2004).
Qiu, T., Zhang, L., Zhang, T. & Yang, H. Effects of mud substrate and water current on the behavioral characteristics and growth of the sea cucumber Apostichopus japonicus in the Yuehu lagoon of northern China. Aquacult. Int. 22(2), 423–433. https://doi.org/10.1007/s10499-013-9650-9 (2014).
Sloan, N. & Von Bodungen, B. Distribution and feeding of the sea cucumber Isostichopus badionotus in relation to shelter and sediment criteria of the Bermuda platform. Mar. Ecol. Prog. Ser. 2, 257–264 (1980).
Dissanayake, D. C. T. & Stefansson, G. Habitat preference of sea cucumbers: Holothuria atra and Holothuria edulis in the coastal waters of Sri Lanka. J. Mar. Biol. Assoc. UK 92, 581–590 (2012).
Yang, M. et al. Effects of handling stresses on fitness related behaviors of small sea cucumbers Apostichopus japonicus: New insights into seed production. Aquaculture 546, 737321. https://doi.org/10.1016/j.aquaculture.2021.737321 (2021).
Woodby, D., Smiley, S. & Larson, R. Depth and habitat distribution of Parastichopus californicus near Sitka, Alaska. Alsk. Fish. Res. Bull. 7, 22–32 (2000).
Wang, X.G. The effects of environmental factors on behavior and growth of sea cucumber Apostichopus japonicas. Doctoral Thesis., Shandong Univ. (2013).
Chen, J. Overview of sea cucumber farming and sea ranching practices in China. SPC Beche-de-mer Info. Bull. 18, 18–23 (2003).
Zhang, L. B. et al. An artificial oyster shell reef for the culture and stock enhancement of sea cucumber, Apostichopus japonicus, in shallow seawater. Aquac. Res. 46, 2260–2269. https://doi.org/10.1111/are.12383 (2014).
Battaglene, S. C., Seymour, J. E. & Ramofafia, C. Survival and growth of cultured juvenile sea cucumbers, Holothuria scabra. Aquaculture 178, 293–322. https://doi.org/10.1016/S0044-8486(99)00130-1 (1999).
Brothers, C. J. & McClintock, J. B. The effects of climate-induced elevated seawater temperature on the covering behavior, righting response, and Aristotle’s lantern reflex of the sea urchin Lytechinus variegatus. J. Exp. Mar. Biol. Ecol. 467, 33–38. https://doi.org/10.1016/j.jembe.2015.02.019 (2015).
Ding, J. et al. Effects of water temperature on survival, behaviors and growth of the sea urchin Mesocentrotus nudus: New insights into the stock enhancement. Aquaculture 519, 734873. https://doi.org/10.1016/j.aquaculture.2019.734873 (2020).
Navarro, P. G., Garcia-Sanz, S., Barrio, J. M. & Tuya, F. Feeding and movement patterns of the sea cucumber Holothuria sanctori. Mar. Biol. 160(11), 2957–2966. https://doi.org/10.1007/s00227-013-2286-5 (2013).
Pan, Y. et al. Influence of flow velocity on motor behavior of sea cucumber Apostichopus japonicus. Physiol. Behav. 144, 52–59. https://doi.org/10.1016/j.physbeh.2015.02.046 (2015).
Dam-Bates, P. V., Curtis, D. L., Cowen, L., Cross, S. F. & Pearce, C. F. Assessing movement of the California sea cucumber Parastichopus californicus in response to organically enriched areas typical of aquaculture sites. Aquacult. Environ. Interact. 8, 67–76. https://doi.org/10.3354/aei00156 (2016).
Xi, X., Zhang, L., Liu, S., Tao, Z. & Yang, H. Aerated sea mud is beneficial for post-nursery culture of early juvenile sea cucumber Apostichopus japonicus (Selenka). Aquac. Int. 24(1), 211–224. https://doi.org/10.1007/s10499-015-9920-9 (2016).
Ning, Y. et al. An evaluation on the selenium yeast supplementation in the practical diets of early juvenile sea cucumber (Apostichopus japonicus): Growth performance, digestive enzyme activities, immune and antioxidant capacity, and body composition. Aquac. Nutr. 27(6), 2142–2153. https://doi.org/10.1111/anu.13350 (2021).
Hu, F. et al. Effects of artificial reefs on selectivity and behaviors of the sea cucumber Apostichopus japonicas: New insights into the pond culture. Aquac. Rep. 21, 100842. https://doi.org/10.1016/j.aqrep.2021.100842 (2021).
Xu, Q. et al. Functional groupings and food web of an artificial reef used for sea cucumber aquaculture in northern China. J. Sea Res. 119, 1–7. https://doi.org/10.1016/j.seares.2016.10.005 (2017).
Tian, R. et al. An effective approach to improving fitness-related behavior and digestive ability of small sea cucumbers Apostichopus japonicus at high temperature: New insights into seed production. Aqauculture 562, 738755. https://doi.org/10.1016/j.aquaculture.2022.738755 (2023).
Lin, C.G. Effects of four physical environment factors on the movement and feeding behavior of sea cucumber Apostichopus japonicas (Selenka). Doctoral Thesis. Institute of Oceanology, Chinese Academy of Sciences (2014).
Clements, J. et al. Roll, right, repeat: short-term repeatability in the self-righting behaviour of a cold-water sea cucumber. J. Mar. Biol. Assoc. UK 100, 115–120. https://doi.org/10.1017/S0025315419001218 (2020).
Acknowledgements
This article was funded by a high-level talent support grant for innovation in Dalian (2020RD03), Liaoning Province “Xingliao Talents Plan” project (XLYC2002107), the Central Guidance on Local Science and Technology Development Fund of Liaoning Province (2023), China Scholarship Council (202208210081) and Fund of Key Laboratory of South China Sea Fishery Resources Exploitation and Utilization, Ministry of Agriculture and Rural Affairs. P. R. China (FREU2020-02). We appreciate Prof. John Lawrence and Wei Tang for editorial suggestions. We thank Jiangnan Sun, Mingfang Yang, Xiaomei Chi, and Tongdan Zhang for their assistance.
Author information
Authors and Affiliations
Contributions
C.Z., F.H. and Y.C. designed the experiments. F.H., H.W., R.T. and G.W. carried out the experiments. F.H., H.W. and G.W. did the data analysis. F.H., H.W., L.W. and C.Z. wrote and reviewed the manuscript. F.H., L.W., Y.C. and C.Z. provided funding support. All authors gave final approval for publication.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
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/.
About this article
Cite this article
Hu, F., Wang, H., Tian, R. et al. Artificial reefs reduce the adverse effects of mud and transport stress on behaviors of the sea cucumber Apostichopus japonicus. Sci Rep 13, 9576 (2023). https://doi.org/10.1038/s41598-023-36791-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-023-36791-0
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.
