**1. Introduction**

Integrated Multi-Trophic Aquaculture (IMTA) system attracts wide attentions in recent years [1], because it brings higher profits and more diversification of commercial production with less environmental pollution [2–4]. The land-based IMTA of sea urchins (as primary product species) and sea cucumbers (as subsidiary product species) has been successfully developed due to their high commercial value and feeding habits [5–7]. For example, sea cucumbers *Holothuria tubulosa* ingested 54% of organic matters from the feces of sea urchins *Paracentrotus lividus* [8], which greatly reduces the total waste and increases additional value (i.e., sea cucumbers). However, the aquaculture production of sea cucumber is higher than that of sea urchins in China. The annual production, for example, is 196,564 metric tons in sea cucumbers and 7952 metric tons in sea urchins in China in 2020 [9]. This suggests that the above approach probably is not applicable to producing echinoderms in China. It is, therefore, essential to develop a new approach to IMTA with sea cucumbers, as the primary species, and sea urchins as the subsidiary species with a high stocking biomass in China.

The sea cucumber *Apostichopus japonicus* and the sea urchin *Strongylocentrotus intermedius* are two commercially important species and are widely cultured in China [10,11]. Seed productions of *A*. *japonicus* and *S*. *intermedius* are both feasible in May and June [12,13].

**Citation:** Hu, F.; Wang, H.; Tian, R.; Gao, J.; Wu, G.; Yin, D.; Zhao, C. A New Approach to Integrated Multi-Trophic Aquaculture System of the Sea Cucumber *Apostichopus japonicus* and the Sea Urchin *Strongylocentrotus intermedius*. *J. Mar. Sci. Eng.* **2022**, *10*, 1875. https://doi.org/10.3390/ jmse10121875

Academic Editor: Ka Hou Chu

Received: 14 October 2022 Accepted: 20 November 2022 Published: 3 December 2022

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

The body weight of *A*. *japonicus* reaches 1–2.5 g in November while the test diameter of *S*. *intermedius* reaches 6–15 mm at that time [12]. In the production of juvenile *A*. *japonicus*, polyethylene nets were commonly used as the substrate on the top of nursery tanks to increase culture biomass and avoid intraspecific competition [11]. In this context, many sea cucumber diets (mainly commercial powdered diets) fail to adhere to the nets and settle at the bottom of tanks, making it difficult to use the water space and deposited diets below the nursery tanks for *A*. *japonicus* situated on the nets. Sea urchins are omnivorous animals and their unique feeding organ, Aristotle's lantern, is adapted for omnivorous diets such as macroalgae, hard calcified surfaces, and soft sediments [14–16]. Many edible macroalgae for sea urchins, such as *Saccharina japonica* (the most commonly food used for sea urchin aquaculture), *Sargassum thunbergii*, *S*. *polycystum*, are made into powdered diets and used for sea cucumber aquaculture [17–19]. Thus, it is reasonable to assume that the powdered diets wasted in nursery tanks can be effectively used by *S*. *intermedius*. However, the sufficient food source for *S*. *intermedius* is not enough to support an effective IMTA with *A*. *japonicus*. Physical interactions between sea urchins and sea cucumbers display negative effects on the fitness of both species. For example, Sun et al. [20] found that sea cucumbers showed significantly higher escaping speed when behavioral interactions existed between sea cucumbers and sea urchins. Mass mortality occurred in *A*. *japonicus* with the increased stocking density of *S*. *intermedius* when they were not cultured separately [21], which may be due to the injuries caused to the sea cucumbers by sea urchin spines. This suggests that a specialized culture facility is further required to separate *S*. *intermedius* from *A*. *japonicus* in the IMTA system. Our previous studies found that segregation in multi-layer culture significantly improved survival [22], food utilization and body growth [23] of *S*. *intermedius*, compared with those without the multi-layer culture. We assumed that a plastic box divided into three layers (each layer has many compartments) full of holes would represent a promising candidate for the *S*. *intermedius* aquaculture, because it not only allows the powdered diets to enter the facility through the holes for *S*. *intermedius* consumption, but also provides an additional substrate for *A*. *japonicus* in the IMTA system.

Here, the main purposes of the present study are to investigate: (1) whether juvenile *S*. *intermedius* show better survival, feeding behaviors and growth in the IMTA system; (2) whether the survival, fitness-related behaviors and growth of juvenile *A*. *japonicus* are better in the IMTA system; (3) what is the application potential of the new IMTA system with *A*. *japonicus* as the primary species and *S*. *intermedius* as the subsidiary species.
