**1. Introduction**

The sea cucumber (*Apostichopus japonicus*) is popular internationally because of its high nutritional and medicinal value [1]. High market demand stimulated the development of sea cucumber aquaculture [2,3]. The annual production of sea cucumber aquaculture was 222,707 tons in 2022 in China, which was 13.3% higher than that in 2021 [4]. Seed production is a common process in aquaculture, in which small sea cucumbers (~1 g of wet body weight) are intensively cultured in land-based factories until they reach the size available for the following pond culture and stock enhancement [5]. During this process, sea cucumbers are commonly challenged by high temperatures in summer [5]. Sea cucumbers are most suitable for survival in the temperature range between 10 and 21 ◦C, and the physiology and growth of sea cucumbers are greatly affected when water temperature is higher than 23 ◦C [6,7]. High temperature (>25 ◦C) damages the immune system and gut microbiota [6,7] and, consequently, causes mass mortality and morbidity of sea cucumbers in summer. It is very expensive to decrease the water temperature in

**Citation:** Wang, H.; Wu, G.; Hu, F.; Tian, R.; Ding, J.; Chang, Y.; Su, Y.; Zhao, C. Artificial Reefs Reduce Morbidity and Mortality of Small Cultured Sea Cucumbers *Apostichopus japonicus* at High Temperature. *J. Mar. Sci. Eng.* **2023**, *11*, 948. https://doi.org/10.3390/ jmse11050948

Academic Editor: Jean-Claude Dauvin

Received: 8 March 2023 Revised: 23 April 2023 Accepted: 26 April 2023 Published: 28 April 2023

**Copyright:** © 2023 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/).

seed production in summer. Therefore, it is essential to establish a cost-effective method to reduce the mortality and morbidity of sea cucumbers at high temperatures.

Changing seawater and removing feces are necessary in seed production. Thus, sea cucumbers are inevitably exposed to the air during this process. Air exposure leads to tissue damage and complicated oxidative stress [8,9], which increases the risk of death and disease in sea cucumbers [10]. Sea cucumbers are more severely affected when high temperature and air exposure happen together [11], which is probably responsible for the high mortality and morbidity of sea cucumbers in seed production in summer. In addition, skin ulcer syndrome (SUS) is one of the most common and severe diseases that occur to sea cucumbers in aquaculture, resulting in high mortality due to the high infectivity [12]. High temperature decreases the immunity of sea cucumbers and increases the transmission of pathogenic bacteria [13]. Therefore, sea cucumbers are more susceptible to disease in summer. Diseased sea cucumbers probably spread the disease to other individuals and increase the frequency of disease outbreaks [14,15], resulting in mass mortality and morbidity in aquaculture [16]. Therefore, it is of primary importance to reduce the mortality and morbidity of sea cucumbers after air exposure and disease outbreaks.

Although there is no obvious symptom (e.g., skin ulceration) in the early stages of the disease, sea cucumbers show decreased feeding, movement, and adhesion [16,17]. Thus, fitness-related behaviors are helpful for determining whether sea cucumbers are affected. Decreasing disease transmission is key to reducing mortality and morbidity during the disease outbreak. Our previous study suggests that separation effectively decreases the disease transmission of the sea urchin *Strongylocentrotus intermedius* [18]. However, it is costly and difficult to separate diseased/affected from unaffected individuals in aquaculture. We attempted to reduce mortality and morbidity by reducing the frequency that unaffected individuals have contact with diseased/affected ones [19]. Sea cucumbers are naturally attracted to artificial reefs [20], and they hide into crevices formed by rocks or reefs at high temperatures [21]. Diseased and affected individuals probably struggle to move to crevices because of their poor movement ability [16]. Tian et al. [11] found that artificial reefs improve fitness-related behaviors of stressed sea cucumbers at high temperatures. It is necessary to explore the key role of artificial reefs, which is beneficial to reduce the mortality and morbidity of sea cucumbers at high temperatures. Thus, we hypothesized that artificial reefs reduce mortality and morbidity by reducing physical contact between diseased/affected and unaffected sea cucumbers in seed production at high temperatures.

The main aim of the present study is to investigate whether artificial reefs improve sea cucumber survival in summer, as detailed below: (1) whether artificial reefs reduce the morbidity and mortality of sea cucumbers exposed to the air at high temperatures; (2) whether artificial reefs reduce the morbidity and mortality of sea cucumbers under a disease outbreak at high temperatures; and (3) whether artificial reefs improve the fitnessrelated behaviors of sea cucumbers exposed to both air exposure and disease outbreak at high temperatures.
