Next Article in Journal
Structural Influence of the Cargo Holds of a 3000 m3 Wellboat on a Double-Bottom Floor
Previous Article in Journal
Experimental and Numerical Investigation into the Effects of Air–Fluid Interaction on the Dynamic Responses of a Damaged Ship
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JMSE
Volume 12
Issue 6
10.3390/jmse12060993
jmse-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Shelter Capacity of Artificial Reefs for Sea Cucumber Apostichopus japonicas Is Influenced by Water Flow and Food Resources in Laboratory Experiments

by
Shengjun Yan
1,
Tao Sun
2,*,
Rui Yan
3,
Xiaoling Wang
2,
Guoxiang Liao
1 and
Wei Lei
1
1
State Environmental Protection Key Laboratory of Marine Ecosystem Restoration, National Marine Environmental Monitoring Center, Dalian 116023, China
2
State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing 100875, China
3
College of Marine Science and Environment, Dalian Ocean University, Dalian 116023, China
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2024, 12(6), 993; https://doi.org/10.3390/jmse12060993
Submission received: 28 April 2024 / Revised: 8 June 2024 / Accepted: 11 June 2024 / Published: 14 June 2024
(This article belongs to the Section Marine Aquaculture)
Browse Figures
Versions Notes

Abstract

:
Artificial reefs have been advocated and implemented as management tools for aquaculture, species conservation and habitat replacement. However, the shelter capacity of artificial reefs and its influencing factors are still not well understood. In this study, we identified factors that may limit the shelter capacity of artificial reefs for sea cucumber (Apostichopus japonicas) with a laboratory experiment. We investigated how water flow and food availability affect the shelter capacity and conducted shelter utilization experiments to determine whether sea cucumber sheltering behavior was density dependent. The results revealed that shelter capacity of artificial reefs in high velocity is significantly higher than that of artificial reefs in low velocity or no velocity. The artificial reefs that were provided food had significantly higher shelter capacity than those that did not have food. The densities did not affect the sheltering capacity of artificial reefs in the laboratory experiment. There was a logarithmic relationship between the shelter capacity and shelter availability assessed by the exposed surface area of the artificial reefs. In conclusion, abundant food resources and high water flow may have a positive effect on the shelter capacity of artificial reefs.

1. Introduction

Apostichopus japonicas is a sea cucumber that is a valuable resource in traditional fisheries in China [1,2]. It takes shelter by day [3] or seeks refuge to avoid predators, often relying on hard substrate surfaces such as rocky reefs or crevices as shelters [4]. Artificial reefs are usually believed to support more density levels of A. japonicas than natural reefs [5,6]. The use of artificial reefs to build shelters is currently an important technology for the culture and stock enhancement of sea cucumbers [7,8]. However, the shelter capacity of artificial reefs and its influencing factors are still not well understood.
Aggregation effects of artificial reefs are mainly influenced by shelter-seeking and foraging behavior for many species. The physical properties of reefs, such as the material, structural complexity, size and location, may affect the preference of an animal by changing environmental conditions surrounding the artificial reefs [2,4,9]. Furthermore, benthic algae growing attached to the artificial reefs and sediments captured through altered flow fields may influence the capacity of an artificial reef by changing food resources [10,11]. Movement pattern and feeding behavior in response to variable water currents have been observed in A. japonicas [12,13,14,15]. Nevertheless, how food resource constraints and water flow regulate habitat selection by A. japonicas and explain the role of refuges in limiting biological density still requires further investigation. Aggregation effects of artificial reefs may also be influenced by intraspecific competition when the shelter availability is limited [16,17,18]. Competition for limited resources and the resulting density-constraining processes are essential for population dynamics, especially in heterogeneous habitats [19,20]. Theoretically, increasing the amount of shelter will increase the number of animals that a reef can support. However, as shelter availability increases, the limiting factors affecting animal behavior will shift from shelter limitations to other factors (e.g., feeding efficiency limitations) [21].
A prerequisite for addressing the population constraints associated with refuges is a more detailed understanding of the quantitative relationship between the capacity and availability of the artificial reefs [16,22]. We hypothesized that a sustained increase in the number of artificial reefs may not result in a linear change in the number of A. japonicas inhabiting artificial reefs under effects of environmental factors and intraspecific interactions. This study aimed to quantify the artificial reefs holding capacity for A. japonicas and to determine the key factors affecting the shelter capacity based on laboratory experiments. Towards this goal, we discussed the following three questions: does the shelter have a fixed capacity? Is the shelter capacity regulated by food availability and water flow? Does a sustained increase in the number of artificial reefs result in a linear change in shelter capacity of artificial reefs?

2. Materials and Methods

2.1. Selection of Sea Cucumber and Maintenance

The laboratory experiments were conducted in an aquaculture workshop located in Liaoning, China. A total of 150 A. japonicas of similar size, color and intact appearance were selected and transferred to holding tanks for a period of 2 days before the experiments were conducted. A. japonicas wet weight was 80 ± 5 g (mean ± 1 standard deviation), and their average curl length was 8 ± 2 cm (mean ± 1 standard deviation). During the holding period, the seawater in the rectangular tank was renewed once a day at 8 am with filtered seawater, each time with a 50% sea water change. No food was provided during the holding period. The environmental conditions met the normal growth requirements of A. japonicas, including a dissolved oxygen content of greater than 6.0 mg/L, pH of 7.8–8.2, salinity of 29–31%, and temperature of 15 ± 2 °C.

2.2. Construction of the Sheltering Behavior Observation System for Sea Cucumber

A sheltering behavior observation system for A. japonicas was constructed in a laboratory to record their location around the shelter (Figure 1). The observation system unit included an infrared video camera (Hikvision, EZVIZ-C6CN 3MP, Hangzhou, China), a rectangular glass fiber-reinforced plastic tank (2.00 m × 1.20 m × 0.70 m) and a shelter made up of artificial reefs. A wooden frame held the infrared video camera 1.0 m above the water’s surface of each tank to record the A. japonicas’s location. The sea cucumbers have an ability to grip the smooth plastic surface of the tanks, just as they have an ability to grip the muddy benthic surface in the wild. Therefore, we placed concrete artificial reefs in the glass fiber-reinforced plastic tanks to simulate the difference in materials created by placing artificial reefs on the muddy benthic surface in the wild. The artificial reefs were constructed from prefabricated, hollow concrete modules, with each module measuring 0.18 m × 0.18 m × 0.18 m. The artificial reefs, with an exposed surface area of 0.2560 m2, were placed in the middle of the tank. The cavity of the artificial reef allowed the A. japonicas sufficient mobility to seek a suitable refuge site. The tanks were equipped with aeration devices. A 40-mesh screen was installed at the inlet of the tank to filter out fine impurities. Each tank was illuminated using a low-intensity infrared light bulb (5 W, 220 V). The infrared light lamp was switched on when the ambient light became too low (usually 6:00 p.m. to 7:00 a.m. the following day) for regular filming. Preliminary observations showed that the spatial distribution of adult A. japonicas is not affected by the presence of the infrared light bulb used in this study [23].

2.3. Experimental Design

2.3.1. Experiment 1: Effect of Water Flow on Shelter Capacity

The shelter utilization response of A. japonicas to different water flows was tested in laboratory experiments. Four adult A. japonicas were introduced into each of the nine 0.80 m × 0.45 m × 0.45 m tanks containing artificial reefs. The artificial reefs, consisting of two hollow concrete modules stacked vertically, were placed in the middle of the bottom of each tank. At the start of experiment, three tanks were provided with the aquarium super wave maker WP-400M (power, 15 W; maximum flow, 10,000 L/h, SOBO, Guangzhou, China) per tank (low velocity), and three tankss were provided with the aquarium super wave maker WP-800M (power, 25 W; maximum flow, 20,000 L/h, SOBO, Guangzhou, China) per tank (high velocity). Another three tanks had no aquarium super wave maker (no velocity). In the experiment, all the hollows of the artificial reefs pointed in the direction of the outlet of the wave maker, but they were not in a straight line, and the aquarium super wave maker was placed in one corner of the tank. To begin the trial, four A. japonicas were placed on the upper surface of the artificial reefs in each tank, and their location was observed remotely by video for 24 h (8:00 a.m. to 8:00 a.m. the following day). Nine treatment tanks were cleaned at the end of each experiment. Three replicates with a different group of A. japonicas were conducted sequentially for each velocity.

2.3.2. Experiment 2: Effect of Food Availability on Shelter Capacity

Laboratory experiments were performed to compare the shelter capacity with the presence or absence of food. The treatments with and without food were randomly assigned to the three tanks (0.80 m × 0.45 m × 0.45 m), respectively. Within each tank, two artificial reef modules stacked vertically were placed in the middle of the bottom of each tank. In the food treatment, a mixture of commercially available dried sea mud power and algae (Laminaria japonica: 40%, Cyanobacteria: 10%, Phaeophyceae: 10%, Sargassum: 10%) in a 3:1 mass ratio was evenly coated on the outer and inner surfaces of the wetted artificial reefs. The mixture of sea mud and algae (MSMA) was used as the food for A. japonicas in this experiment to better simulate the conditions of a natural artificial reef. This was followed by a slow refill of filtered seawater to avoid turbid water, which facilitates video filming. To begin the trial, four A. japonicas were placed on the upper surface of the artificial reef in each tank, and their location was observed remotely by video for 24 h. Six treatment tanks were cleaned at the end of each experiment, and three replicates with a different group of A. japonicas were conducted sequentially for each treatment. We did not conduct further two-factor experiment design analyses in this study due to the turbid water produced by having treatments with food and water flow together, which made it impossible to obtain clear images of the distribution of sea cucumbers.

2.3.3. Experiment 3: Density-Dependent Sheltering Behavior

We enhanced density with the addition of food to investigate whether A. japonicas density affected the shelters capacity in laboratory experiments. To accommodate the artificial reefs and avoid too-small distance between the artificial reefs and the tank sidewall, larger-sized tanks were chosen for the experiment. Three adult A. japonicas densities, 4, 6 and 8 individuals per tank, were randomly introduced into two tanks (2.00 m × 1.20 m × 0.70 m) containing artificial reefs, respectively. The artificial reefs, consisting of two hollow concrete modules on the bottom and one stacked vertically on top, were placed at the middle of the bottom of each tank. The outer and inner surfaces of the artificial reef and the bottom of the tank were evenly coated with MSMA. Each experimental tank was divided into three sections: the tank wall non-shelter zone (WNSZ), which consisted of a sidewall zone around the tank; the shelter zone (SZ), which consisted of a zone at the bottom of the tank where the artificial reefs are located; and the bottom non-shelter zone (BNSZ), which consisted of a nonartificial reef zone on the tank bottom. The location of A. japonicas within the WNSZ and BNSZ was recorded remotely by video in real-time for 24 h. To avoid the effects of any chemical cues from the last experiments, three treatment tanks were cleaned at the end of each experiment. Three replicates with a different group of A. japonicas were conducted sequentially for each density using three tanks.

2.3.4. Experiment 4: Relationship between Shelter Availability and Shelter Capacity

The number of artificial reefs is mostly used in current studies to characterize the availability of shelters [24,25,26]. However, in practice, the stacking of multiple artificial reefs can result in a loss of the effective available surface area within the shelter, thus affecting the accuracy of this indicator in describing the shelter availability. The exposed surface area of artificial reef is directly related to space and refuge availability.
We conducted another experiment to analyze the quantitative relationship between the shelter capacity and the shelter availability with unlimited food resources over varying the exposed surface area of artificial reefs. The exposed surface area of artificial reefs in each tank was 2236, 4148, 5736, 9560 and 13,384 cm2, while the corresponding number of A. japonicas was 4, 6, 8, 10 and 12, respectively. Five groups of artificial reefs and their matching numbers of A. japonicas were randomly introduced into two tanks (2.00 m × 1.20 m × 0.70 m) containing artificial reefs, respectively, and their location was observed remotely by video for 24 h. The outer and inner surfaces of the artificial reefs and the bottom of the tank were evenly coated with MSMA. Three replicate trials, each with a different group of A. japonicas, were performed.

2.4. Data Collection and Data Analysis

In order to evaluate the capacity of the shelters to hold A. japonicas under different treatments during the study period, image snapshots from video recordings were taken at 1-min intervals. From image snapshots, the number of A. japonicas in the artificial reefs was determined at 1-h intervals. Sea cucumbers move very slowly or are sedentary [12,14], with the medium-size A. japonicas (60.08 ± 6.05) moving at a speed of 0.022 m/h [4]. It is, therefore, assumed that when an A. japonicas appears at a certain location at hour t, it will stay at that location until hour t + 1. If any part of the A. japonicas body had physical contact with the artificial reef, it was considered to be in the shelter.
The shelter capacity was used as the response variable in all analyses. Considering the use course of artificial reefs by A. japonicas, the shelter capacity was defined as the average fluctuation value of A. japonicas in artificial reefs after the spatial distribution of free-ranging A. japonicas reached a relatively stable fluctuating state. We call the state, which varies up and down around a certain value, a relatively stable fluctuating state. In this study, it was assumed that A. japonicas would reach a steady fluctuating state at 12 h after release (Figure 2), and the mean number of A. japonicas in the shelter at each hourly interval after steady fluctuating state was counted as the shelter capacity. The number of occupants was used to quantify the shelter capacity (K) of the artificial reefs. The shelter capacity (K) was calculated as the following:
K = ∑ i = 1 n ∑ j = 1 m ( d − f i j ) / ( n × m ) ,
where d is the total number of A. japonicas in each experimental tank, fij is the number of A. japonicas outside the shelter in the tank at time point i in the jth replicate experiment, n is the number of experimental records after reaching a relatively stable fluctuating state in a trial and m is the number of replicate experiments.
It is necessary to define the exposed surface area of artificial reefs to be able to estimate shelter availability. For example, the internal and external surface area of a hollow cube-type artificial reef module, as shown in Figure 1B, can be defined as 0.1008 m2 and 0.1552 m2 due to its known dimensions. In this case, the usable exposed surface area of the module is defined as the sum of internal and external surface area, regardless of the area in contact with the ground. Considering an artificial reef set comprising multiple modules [27], the usable exposed surface area is excluding the surface area in contact with the ground and overlap among the artificial reef modules. Therefore, Equation (2) was established to express the relationship between the usable exposed surface area (Aues) of an artificial reef set and the usable exposed surface area of an artificial reef module (Auem).
A u e s = n × A u e m − n × A g − 2 × A o ,
where Ag is the area contact with the ground, Ao is the overlap area among the artificial reef modules and n is the number of modules used to establish the artificial reef set.
The Shapiro–Wilk test [28] was used to test the normality of the data, and Levene’s test [29] was used to test the homoscedasticity of variance. When the data did not fit normality and equal variance, the Kruskal–Wallis test [30] and the Nemenyi post hoc test [31] were used to compare the shelter capacity and the number of individuals in each of the three zones of the tank. The Kruskal–Wallis test and the Nemenyi post hoc test were used to compare the shelter capacity under different water flow conditions. The Mann–Whitney test [32] was used to compare the significance of the difference in the shelter capacity in the tank with or without food. Regression models were conducted to determine the relationship between the exposed surface area of the artificial reefs and their shelter capacity. All statistical analyses were performed with R software (R Development Core Team, v.4.3.0., 2023).

3. Results

3.1. Distribution Dynamics of A. japonicas

During the first few hours of the experiment (0–12 h), the number of A. japonicas in the artificial reefs was in a state of rapid change. Subsequently, the number of A. japonicas in the shelter fluctuated up and down to a relatively stable fluctuating state until the end of the experiment. During the experiment, two or more A. japonicas were not seen leaving the artificial reefs at the same time. No group movements of A. japonicas were observed.
The A. japonicas showed a similar pattern of movement in artificial reefs under different treatment conditions (Figure 2). The steepness of these lines reflects the rate of change in the number of A. japonicas in the artificial reefs, with steeper lines indicating more A. japonicas leaving during that time period. During the first 12 h, the number of A. japonicas in the shelter varied rapidly under the static water and no food condition, while the number of A. japonicas in the shelter changed more slowly with the addition of food or a low-flow condition (flow velocity generated by the aquarium super wave maker WP-400M in the tank). After reaching steady fluctuating state, the group with food or low-flow velocity had a greater number of A. japonicas in their shelters than the group with no food in still water. Overall, food and water flow only altered the number of A. japonicas in the artificial reefs and did not change the pattern of A. japonicas movement to a steady fluctuating state in the artificial reefs.

3.2. Shelter Capacity under Different Water Flow Conditions

There was a significant effect of water flow on the shelter capacity (Figure 3). The shelter capacity was significantly greater with a high water flow condition (flow velocity generated by the aquarium super wave maker WP-800M in the tank) than with low or no water flow condition (df = 2, F = 13.71, p < 0.0001). At a high flow rate, the shelter capacity (3.76 ± 0.25) was significantly greater than that at a low flow rate (2.21 ± 1.27). At a low flow rate (flow velocity generated by the aquarium super wave maker WP-400M in the tank), the artificial reefs supported greater numbers of A. japonicas than in the absence of flow (1.37 ± 1.10).

3.3. Shelter Capacity under Food Availability

There was a significant effect of food availability on the shelter capacity (Figure 4). The shelter capacity was significantly greater with food availability than with no food (df = 1, F = 9.10, p < 0.01). The number of A. japonicas supported by artificial reefs (2.72 ± 0.78) with food was twice that supported by artificial reefs without food (1.37 ± 1.10).

3.4. Density-Dependent Sheltering Behavior

There was no significant difference in the number of A. japonicas in the artificial reefs among the three treatment densities (p = 0.38), with a mean of 5.52 ± 0.93 (Figure 5A). Shelter behavior did not change as density increased. The average density of A. japonicas inhabiting the artificial reefs is 10 individuals/m2 of exposed surface area. The number of A. japonicas in the artificial reefs was significantly greater than the number of A. japonicas inhabiting the BNSZ and WNSZ (p < 0.001). During the experiment, the A. japonicas outside the reef area spent less time at the bottom of the tank (where food was available) and instead inhabited the sidewall areas of the tank. At low densities of A. japonicas, they only chose artificial reefs as a shelter, and at high densities, some of them chose other locations to inhabit (Figure 5B). The average density of A. japonicas per unit of exposed surface area on the artificial reefs from all the treatment was 14.52 times greater than that at other places of the tank.

3.5. Relationship between Shelter Capacity and Shelter Availability

The shelter capacity (y) was positively correlated with the exposed surface area (x) of the artificial reefs (Figure 6). Further examination of the relationship provided a significant fit of the logarithmic functional relationship (y = 3.85log(x) − 27.59, p < 0.01). Although the number of A. japonicas inhabiting the shelter increased as the exposed surface area of the artificial reefs increased, there was a decreasing trend in the number of A. japonicas per unit surface area of the artificial reefs. In the group of the artificial reefs with the exposed surface area of 5736 cm2, the average density of A. japonicas in the artificial reefs was 10 individuals/m2, while in the group of the artificial reefs with the exposed surface area of 13,384 cm2, the average density of A. japonicas in the artificial reefs was reduced to 7 individuals/m2.

4. Discussion

In this study, we found significantly greater numbers of A. japonicas inhabiting artificial reefs with food availability or with water flow condition than with only artificial reefs present. This finding suggests that food availability and water flow are important environmental factors influencing shelter capacity. The two are aligned in terms of the direction of movement of A. japonicas using the shelter, and both promote shelter use by A. japonicas. These patterns are consistent with our proposed hypothesis that enrichment of food and increased water flow around artificial reefs will increase the use of artificial reefs by A. japonicas. These phenomena might be the result of individual trade-offs between its foraging rate and safety under specific environmental conditions [33]. Species exhibit a tendency to seek shelters of higher suitability when the negative environmental condition is greater than the food resource limit and a tendency to seek other shelters of lower suitability when the cost of food resources is greater than the negative environmental condition.
There is a non-density-dependent effect on the shelter use by A. japonicas. In our experiments, we found that the number of A. japonicas inhabiting the shelter was a relatively stable fluctuating state when the initial density of A. japonicas increased, while the number of A. japonicas present in other locations of the tank increased. This finding suggests that there is a fixed capacity for A. japonicas in a given area of the shelter. A similar phenomenon was found in the experiments on the mean aggregation rate of A. japonicas in their habitat, i.e., the mean aggregation rate did not change significantly as the density of A. japonicas increased [34]. The high number of A. japonicas had a strong competitive effect, causing the number of A. japonicas in the shelter to fluctuate around a value. As the experiment progressed, the number of individuals inhabiting the shelter gradually stabilized, indicating that the A. japonicas needed some time to become familiar with their new habitat and the other individuals within it.
A larger proportion of A. japonicas inhabited the interior of artificial reefs, indicating that shelter is an important habitat resource for A. japonicas. A. japonicas exhibited shelter-sharing behavior regardless of whether they were present at a low or high density, with more than two A. japonicas inhabiting the shelter in each experiment. A. japonicas in artificial reefs with added food were less likely to leave their shelters. This behavior pattern can be explained by the theory of transience [35]. As they find suitable feeding and sheltering sites, individual A. japonicas optimize energy intake by reducing the distance travelled and staying in specific areas for a longer period of time to feed. In our experiments, we found more individual mobile activity in other parts of the tank. The literature suggests that individuals with less access to shelter are more active over a wider span of time each day compared to individuals with abundant shelter [21]. The search for better shelter conditions drives A. japonicas to move long distances, and a lot of movement can deplete their own energy stores, which is detrimental to the accumulation of biomass.
Our experiments found an increasing trend in the number of A. japonicas in the shelters as the shelter availability increased. Using the average number of individuals in the artificial reefs, we found that the shelter capacity increased logarithmically with the exposed surface area of the artificial reefs. This finding suggests that the number of A. japonicas inhabiting a shelter is related to shelter availability, with the absolute number of shelter surface area regulating the shelter capacity. An increased shelter surface area has the potential to accommodate more A. japonicas through the increased provision of spatial refuges and the increased availability of food resources to avoid adverse environmental conditions [16,22,36]. It can be expected that the availability of shelter in natural marine areas with tidal cycle environments will determine the population of A. japonicas in the area, since individual A. japonicas will be at risk of predation in the absence of shelter [37]. Especially in sea ranching in shallow areas during low tides, the construction of shelters will be crucial for high-density A. japonicas farming.
The shelter capacity increased as a logarithmic function of the exposed surface area but at a slower rate than predicated based on a linear increase under the combined effect of food resources and intraspecific competition. This means that as the shelter availability increases, the amount of shelter space occupied by each A. japonicas is progressively greater. This may lead to a situation where some of the artificial reefs are uninhabited by A. japonicas when the availability of shelter increases. This phenomenon may be due to a shift in the limiting factor. As artificial reefs grow in size, the factors limiting the choice of shelter shift from risk avoidance to greater feeding efficiency. In our experiments, we found that the A. japonicas were not evenly distributed within the artificial reefs and that localized aggregations also occurred. This result of increased shelter availability leading to the absence of A. japonicas on some artificial reefs has been observed in the field with other benthic organisms. For example, in the study of intraspecific competition for shelter use by lobsters, Steneck et al. [16] found that more shelters were uninhabited by lobsters when the shelters were densely distributed. Actual dive surveys in artificial reef areas also have revealed this phenomenon; i.e., not every artificial reef was inhabited by A. japonicas, and the larger the number of artificial reefs, the more pronounced this phenomenon became. This also supports, to some extent, that the size of individual shelters does not need to be as large as it could be and that there is a size of shelter that has a high number of A. japonicas per unit shelter area and a high utilization of the whole shelter [8].
The current study focused on quantifying the relationship between the shelter availability and the number of A. japonicas in artificial reefs. Nevertheless, in the future, it is necessary to further explore the mechanisms behind the decline in the number of A. japonicas each shelter holds when the shelter availability increases. In this study, we explored the influencing factors affecting shelter capacity through laboratory experiments, but the specific numerical values obtained are not yet sufficient to guide specific production practices and need to be further verified in field experiments. In addition, the shelter capacity of artificial reefs for sea cucumbers will change with the size of the individual, and the effect of the morphological size of sea cucumbers on the shelter capacity of artificial reefs needs to be considered in future studies.

5. Conclusions

Our study highlights that food availability and water flow are important factors affecting shelter capacity. The capacity of artificial reefs to hold A. japonicas under defined environmental conditions is closely related to shelter availability and not to A. japonicas density. Although non-density-dependent effects on the shelter use were found at the laboratory scale, there is still a logarithmic relationship between shelter availability and shelter capacity, and there may be a shelter-constrained peak in shelter capacity. Therefore, attention should be given in the enhancement release to the possible capacity peaks under the combined effect of environment and biological interspecific relationships to improve the efficiency of artificial reef utilization.

Author Contributions

Conceptualization, S.Y., R.Y. and T.S.; methodology, S.Y., R.Y. and X.W.; software, S.Y. and R.Y.; validation, S.Y., R.Y. and T.S.; formal analysis, G.L. and W.L.; investigation, S.Y. and X.W.; data curation, S.Y. and R.Y.; writing—original draft preparation, S.Y.; writing—review and editing, T.S., G.L. and W.L.; visualization, S.Y., R.Y. and W.L.; supervision, T.S. and G.L.; project administration, T.S.; funding acquisition, T.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the State Environmental Protection Key Laboratory of Marine Ecosystem Restoration Fund (2023-05) and the National Key R&D Program of China (grant no. 2018YFC1406400).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Acknowledgments

We thank Zhiyang Yu and Lei Li for their assistance in this experiment.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Ru, X.; Zhang, L.; Li, X.; Liu, S.; Yang, H. Development strategies for the sea cucumber industry in China. J. Oceanol. Limnol. 2019, 37, 300–312. [Google Scholar] [CrossRef]
  2. Dong, G.; Dong, S.; Wang, F.; Tian, X. Effects of materials, incubation time and colors of artificial shelters on behavior of juvenile sea cucumber Apostichopus japonicus. Aquac. Eng. 2010, 43, 1–5. [Google Scholar] [CrossRef]
  3. Sun, J.; Zhang, L.; Pan, Y.; Lin, C.; Wang, F.; Kan, R.; Yang, H. Feeding behavior and digestive physiology in sea cucumber Apostichopus japonicus. Physiol. Behav. 2015, 139, 336–343. [Google Scholar] [CrossRef] [PubMed]
  4. Kwon, I.; Lee, K.; Kim, T. Shelter material and shape preferences of the sea cucumber, Apostichopus japonicus. Aquaculture 2019, 508, 206–213. [Google Scholar] [CrossRef]
  5. Zhang, L.; Zhang, T.; Xu, Q.; Qiu, T.; Yang, H.; Liu, S. An artificial oyster-shell reef for the culture and stock enhancement of sea cucumber, Apostichopus japonicus, in shallow seawater. Aquac. Res. 2014, 46, 2260–2269. [Google Scholar] [CrossRef]
  6. Chen, J. Overview of sea cucumber farming and sea ranching practices in China. SPC Beche-De-Mer Inf. Bull. 2003, 18, 18–23. [Google Scholar]
  7. Zhang, L.; Yang, H.; Xu, Q.; Xing, K.; Zhao, P.; Lin, C. A new system for the culture and stock enhancement of sea cucumber, Apostichopus japonicus (Selenka), in cofferdams. Aquac. Res. 2011, 42, 1431–1439. [Google Scholar] [CrossRef]
  8. Hu, F.; Ding, P.; Yu, Y.; Wen, B.; Cui, Z.; Yang, M.; Chi, X.; Sun, J.; Luo, J.; Sun, Z.; et al. Effects of artificial reefs on selectivity and behaviors of the sea cucumber Apostichopus japonicas: New insights into the pond culture. Aquac. Rep. 2021, 21, 100842. [Google Scholar] [CrossRef]
  9. Lin, C.G.; Ru, S.G.; Yang, H.S.; Zhang, L.B.; Liu, S.L.; Xu, Q. Selectivity of sea cucumber (Apostichopus japonicus, Selenka) for key indicators in artificial reef structure design. Mar. Sci. 2012, 36, 13–21. [Google Scholar]
  10. MacTavish, T.; Stenton-Dozey, J.; Vopel, K.; Savage, C. Deposit-Feeding Sea Cucumbers Enhance Mineralization and Nutrient Cycling in Organically-Enriched Coastal Sediments. PLoS ONE 2012, 7, e50031. [Google Scholar] [CrossRef]
  11. Xia, B.; Ren, Y.; Wang, J.; Sun, Y.; Zhang, Z. Effects of feeding frequency and density on growth, energy budget and physiological performance of sea cucumber Apostichopus japonicus (Selenka). Aquaculture 2017, 466, 26–32. [Google Scholar] [CrossRef]
  12. Pan, Y.; Zhang, L.; Lin, C.; Sun, J.; Kan, R.; Yang, H. Influence of flow velocity on motor behavior of sea cucumber Apostichopus japonicus. Physiol. Behav. 2015, 144, 52–59. [Google Scholar] [CrossRef] [PubMed]
  13. Lin, C.; Liu, X.; Sun, L.; Liu, S.; Sun, J.; Zhang, L.; Yang, H. Effects of different flow velocities on behavior and TRPA1 expression in the sea cucumber Apostichopus japonicas. J. Oceanol. Limnol. 2020, 38, 1328–1340. [Google Scholar] [CrossRef]
  14. Chen, M.; Sun, S.; Xu, Q.; Gao, F.; Wang, H.; Wang, A. Influence of Water Temperature and Flow Velocity on Locomotion Behavior in Tropical Commercially Important Sea Cucumber Stichopus monotuberculatus. Front. Mar. Sci. 2022, 9, 931430. [Google Scholar] [CrossRef]
  15. 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. Aquac. Int. 2014, 22, 423–433. [Google Scholar] [CrossRef]
  16. Steneck, R.S. Possible Demographic Consequences of Intraspecific Shelter Competition among American Lobsters. J. Crustac. Biol. 2006, 26, 628–638. [Google Scholar] [CrossRef]
  17. Finstad, A.G.; Einum, S.; Forseth, T.; Ugedal, O. Shelter availability affects behaviour, size-dependent and mean growth of juvenile Atlantic salmon. Freshw. Biol. 2007, 52, 1710–1718. [Google Scholar] [CrossRef]
  18. Zhang, H.; Zhu, B.; Lu, Y.; Yu, L.; Wang, F.; Liu, D. An evaluation of the preferences of the juvenile swimming crab, Portunus trituberculatus, for different structural properties of shelters. Aquaculture 2022, 557, 738316. [Google Scholar] [CrossRef]
  19. Finstad, A.G.; Einum, S.; Ugedal, O.; Forseth, T. Spatial distribution of limited resources and local density regulation in juvenile Atlantic salmon. J. Anim. Ecol. 2009, 78, 226–235. [Google Scholar] [CrossRef]
  20. Zhang, Y.; Sun, T.; Ding, G.; Yu, D.; Yang, W.; Sun, Q.; Wang, X.; Lin, H. Moderate relative size of covered and non-covered structures of artificial reef enhances the sheltering effect on reef fish. Front. Mar. Sci. 2023, 10, 1130626. [Google Scholar] [CrossRef]
  21. Larranaga, N.; Steingrímsson, S. Shelter availability alters diel activity and space use in a stream fish. Behav. Ecol. 2015, 26, 578–586. [Google Scholar] [CrossRef]
  22. Lachance, A.-A.; Dutil, J.-D.; Larocque, R.; Daigle, G. Shelter use and behaviour of juvenile Spotted Wolffish (Anarhichas minor) in an experimental context. Environ. Biol. Fishes 2010, 88, 207–215. [Google Scholar] [CrossRef]
  23. Zhang, S.; Chen, Y.; Sun, M. Behavior characteristics of Apostichopus japonicus and attractive effects of artificial reef models under different light intensities. J. Fish Sci. China 2006, 13, 20–27. [Google Scholar]
  24. Bohnsack, J.A.; Harper, D.E.; McClellan, D.B.; Hulsbeck, M. Effects of Reef Size on Colonization and Assemblage Structure of Fishes at Artificial Reefs Off Southeastern Florida, USA. Bull. Mar. Sci. 1994, 55, 796–823. [Google Scholar]
  25. Behringer, D.C.; Butler, M.J. Density-dependent population dynamics in juvenile Panulirus argus (Latreille): The impact of artificial density enhancement. J. Exp. Mar. Biol. Ecol. 2006, 334, 84–95. [Google Scholar] [CrossRef]
  26. Wocher, H.; Harsányi, A.; Schwarz, F.J. Husbandry conditions in burbot (Lota lota L.): Impact of shelter availability and stocking density on growth and behaviour. Aquaculture 2011, 315, 340–347. [Google Scholar] [CrossRef]
  27. Yoon, H.-S.; Kim, D.; Na, W.-B. Estimation of effective usable and burial volumes of artificial reefs and the prediction of cost-effective management. Ocean Coast. Manag. 2016, 120, 135–147. [Google Scholar] [CrossRef]
  28. Shapiro, S.S.; Wilk, M.B. An analysis of variance test for normality (complete samples). Biometrika 1965, 52, 591. [Google Scholar] [CrossRef]
  29. Yitnosumarto, S.; O’Neill, M.E. On Levene’s Tests of Variance Homogeneity. Aust. J. Stat. 1986, 28, 230–241. [Google Scholar] [CrossRef]
  30. Ostertagová, E.; Ostertag, O.; Kováč, J. Methodology and Application of the Kruskal-Wallis Test. Appl. Mech. Mater. 2014, 611, 115–120. [Google Scholar] [CrossRef]
  31. Demšar, J. Statistical comparisons of classifiers over multiple data sets. J. Mach. Learn. Res. 2006, 7, 1–30. [Google Scholar]
  32. Mann, H.B.; Whitney, D.R. On a Test of Whether one of Two Random Variables is Stochastically Larger than the Other. Ann. Math. Stat. 1947, 18, 50–60. [Google Scholar] [CrossRef]
  33. Sadeh, A.; Mangel, M.; Blaustein, L. Context-dependent reproductive habitat selection: The interactive roles of structural complexity and cannibalistic conspecifics. Ecol. Lett. 2009, 12, 1158–1164. [Google Scholar] [CrossRef] [PubMed]
  34. Xin, X.; Zhang, L.; Yu, Z.; Yang, H. Effects of habitat distribution and intraspecific competition on aggregation features of sea cucumber Apostichopus japonicus. Mar. Sci. 2018, 42, 138–144. [Google Scholar]
  35. Hirsch, P.; Burkhardt-Holm, P.; Töpfer, I.; Fischer, P. Movement patterns and shelter choice of spiny-cheek crayfish (Orconectes limosus) in a large lake’s littoral zone. Aquat. Invasions 2016, 11, 55–65. [Google Scholar] [CrossRef]
  36. Folpp, H.R.; Schilling, H.T.; Clark, G.F.; Lowry, M.B.; Maslen, B.; Gregson, M.; Suthers, I.M. Artificial reefs increase fish abundance in habitat-limited estuaries. J. Appl. Ecol. 2020, 57, 1752–1761. [Google Scholar] [CrossRef]
  37. Xu, Q.; Zhang, L.; Zhang, T.; Zhang, X.; Yang, H. Functional groupings and food web of an artificial reef used for sea cucumber aquaculture in northern China. J. Sea Res. 2017, 119, 1–7. [Google Scholar] [CrossRef]
Jmse 12 00993 g001
Figure 1. A diagram of the observation system for the shelter use of A. japonicas. (A) The spatial distribution of the A. japonicas observation system, (B) a schematic of the outline of the shelter, (C) the diagram of the different zones designated in the tank. WNSZ: the sidewall zone around the tank, SZ: the zone at the bottom of the tank where the artificial reefs are located, and BNSZ: the nonartificial reef zone on the tank bottom.
Figure 1. A diagram of the observation system for the shelter use of A. japonicas. (A) The spatial distribution of the A. japonicas observation system, (B) a schematic of the outline of the shelter, (C) the diagram of the different zones designated in the tank. WNSZ: the sidewall zone around the tank, SZ: the zone at the bottom of the tank where the artificial reefs are located, and BNSZ: the nonartificial reef zone on the tank bottom.
Jmse 12 00993 g001
Jmse 12 00993 g002
Figure 2. Shelter use dynamics over 24 h in experiments testing four A. japonicas in a rectangular tank (n = 9 replicates). Vertical bars represent the means of nine replicates of each treatment ± 1 standard error. Low-flow velocity is the intensity of the flow velocity generated by the aquarium super wave maker WP-400M in the tank. Individual sea cucumbers appeared to leave the shelter for only a small amount of time under high-flow treatment, and this situation of no dynamic change in shelter utilization was not included in this figure.
Figure 2. Shelter use dynamics over 24 h in experiments testing four A. japonicas in a rectangular tank (n = 9 replicates). Vertical bars represent the means of nine replicates of each treatment ± 1 standard error. Low-flow velocity is the intensity of the flow velocity generated by the aquarium super wave maker WP-400M in the tank. Individual sea cucumbers appeared to leave the shelter for only a small amount of time under high-flow treatment, and this situation of no dynamic change in shelter utilization was not included in this figure.
Jmse 12 00993 g002
Jmse 12 00993 g003
Figure 3. Shelter capacity (±1 standard deviation) of artificial reefs for adult A. japonicas in laboratory experiments in which the flow velocity was experimentally manipulated. Values with different letters indicate significant differences (p ≤ 0.05). “Low” is the intensity of the flow velocity generated by the aquarium super wave maker WP-400M in the tank. “High” is the intensity of the flow velocity generated by the aquarium super wave maker WP-800M in the tank.
Figure 3. Shelter capacity (±1 standard deviation) of artificial reefs for adult A. japonicas in laboratory experiments in which the flow velocity was experimentally manipulated. Values with different letters indicate significant differences (p ≤ 0.05). “Low” is the intensity of the flow velocity generated by the aquarium super wave maker WP-400M in the tank. “High” is the intensity of the flow velocity generated by the aquarium super wave maker WP-800M in the tank.
Jmse 12 00993 g003
Jmse 12 00993 g004
Figure 4. Shelter capacity (±1 standard deviation) of artificial reefs for adult A. japonicas with or without food. Values with different letters indicate significant differences (p ≤ 0.05).
Figure 4. Shelter capacity (±1 standard deviation) of artificial reefs for adult A. japonicas with or without food. Values with different letters indicate significant differences (p ≤ 0.05).
Jmse 12 00993 g004
Jmse 12 00993 g005
Figure 5. The effect of A. japonicas density on the spatial distribution of A. japonicas at steady fluctuating state in tanks under conditions of still water and available food. (A) The number (±1 standard deviation) of A. japonicas at steady fluctuating state in the artificial reefs. The letter “a” indicates that there was no significant difference in the shelter capacity at different A. japonicas densities (p > 0.05). (B) The distribution of A. japonicas in the experimental tank. WNSZ: the sidewall zone around the tank, SZ: the zone at the bottom of the tank where the artificial reefs are located, and BNSZ: the nonartificial reef zone on the tank bottom.
Figure 5. The effect of A. japonicas density on the spatial distribution of A. japonicas at steady fluctuating state in tanks under conditions of still water and available food. (A) The number (±1 standard deviation) of A. japonicas at steady fluctuating state in the artificial reefs. The letter “a” indicates that there was no significant difference in the shelter capacity at different A. japonicas densities (p > 0.05). (B) The distribution of A. japonicas in the experimental tank. WNSZ: the sidewall zone around the tank, SZ: the zone at the bottom of the tank where the artificial reefs are located, and BNSZ: the nonartificial reef zone on the tank bottom.
Jmse 12 00993 g005
Jmse 12 00993 g006
Figure 6. The relationship between the capacity and availability of artificial reefs. (A) The deployment of shelters in the observation tank. (B) Regression relationship of the shelter capacity and the exposed surface area of the artificial reefs. Error bars indicate ± 1 standard error.
Figure 6. The relationship between the capacity and availability of artificial reefs. (A) The deployment of shelters in the observation tank. (B) Regression relationship of the shelter capacity and the exposed surface area of the artificial reefs. Error bars indicate ± 1 standard error.
Jmse 12 00993 g006
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yan, S.; Sun, T.; Yan, R.; Wang, X.; Liao, G.; Lei, W. Shelter Capacity of Artificial Reefs for Sea Cucumber Apostichopus japonicas Is Influenced by Water Flow and Food Resources in Laboratory Experiments. J. Mar. Sci. Eng. 2024, 12, 993. https://doi.org/10.3390/jmse12060993

AMA Style

Yan S, Sun T, Yan R, Wang X, Liao G, Lei W. Shelter Capacity of Artificial Reefs for Sea Cucumber Apostichopus japonicas Is Influenced by Water Flow and Food Resources in Laboratory Experiments. Journal of Marine Science and Engineering. 2024; 12(6):993. https://doi.org/10.3390/jmse12060993

Chicago/Turabian Style

Yan, Shengjun, Tao Sun, Rui Yan, Xiaoling Wang, Guoxiang Liao, and Wei Lei. 2024. "Shelter Capacity of Artificial Reefs for Sea Cucumber Apostichopus japonicas Is Influenced by Water Flow and Food Resources in Laboratory Experiments" Journal of Marine Science and Engineering 12, no. 6: 993. https://doi.org/10.3390/jmse12060993

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop