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Article

The Effects of Salinity on the Growth, Survival, and Feeding of Sanderia malayensis (Cnidaria: Scyphozoa) Ephyrae

by
Kyong-Ho Shin
1,2 and
Keun-Hyung Choi
1,*
1
Department of Earth, Environmental and Space Sciences, Chungnam National University, 99 Daehak-ro Yusung-gu, Daejeon 34134, Republic of Korea
2
Aqua Planet Corporation, Ltd., 300 Gwanggyohosugongwon-ro, Yeongtong-gu, Suwon-si 16514, Republic of Korea
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(4), 239; https://doi.org/10.3390/d17040239
Submission received: 8 March 2025 / Revised: 22 March 2025 / Accepted: 23 March 2025 / Published: 27 March 2025
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Abstract

:
Sanderia malayensis is a species from the phylum Cnidaria, class Scyphozoa, and order Semaeostomeae, found in tropical waters, including the Red Sea, Indian Ocean, and Malaysian waters. Its distribution extends to the waters of Australia and Japan. This study aimed to evaluate the effects of salinity on the growth and survival of Sanderia malayensis ephyrae and to determine its optimal salinity range. The experimental design included two temperature conditions (20 °C and 24 °C) and three salinity levels (21 PSU, 24 PSU, and 27 PSU). The results indicated that growth and feeding abilities were significantly higher in 24 PSU and 27 PSU environments compared to 21 PSU, with the best results observed at both temperatures. Survival rates were higher at 24 PSU (20 °C: 90%, 24 °C: 79%) and 27 PSU (20 °C: 87%, 24 °C: 86%) compared to 21 PSU (20 °C: 70%, 24 °C: 55%). Despite lower survival at 21 PSU, the species demonstrated wide environmental adaptability. These findings suggest that Sanderia malayensis ephyrae are highly adaptable to varying salinity conditions, indicating the potential for the species to expand its distribution into South Korean waters and other East Asian marine ecosystems, including China and Japan, which are impacted by climate change.

Graphical Abstract

1. Introduction

Jellyfish outbreaks have significant impacts on marine ecosystems and human activities [1,2,3,4]. In particular, they are known to have highly negative social and economic effects on human activities, especially in sectors such as fisheries and tourism [5,6]. These impacts include damage to aquaculture species, loss of fishing nets, a decrease in fishery resources due to food competition, disruptions to coastal power plant systems, and human sting incidents at beaches [7,8,9,10,11]. Jellyfish outbreaks occurring worldwide are primarily attributed to Scyphozoan species from the phylum Cnidaria [12,13], and species such as Aurelia coerulea and Nemopilema nomurai frequently experience annual outbreaks in East Asian waters, including those of Korea, Japan, and China [14,15,16,17]. The background of jellyfish outbreaks is multifaceted, driven by factors such as climate change, alterations in marine environments, human activities including marine resource development and global trade, and rising water temperatures [18].
The life cycle of most Scyphozoans is primarily carried out through sexual reproduction [19]. Eggs fertilized through mating develop into planula larvae, which then attach to the substrate and transform into polyps. These polyps undergo asexual reproduction to form numerous colonies. Subsequently, polyps release ephyrae through strobilation, and the ephyrae grow and develop into adult medusae. Research on Scyphozoans primarily focuses on various ecological studies of Aurelia spp. (Aureli coerulea, Aurelia solida, Aurelia labiata) [20,21,22,23,24,25]. Aurelia spp. have the widest distribution range globally and are not only easy to sample for experimental research but also exhibit exceptional survival in diverse environmental conditions. As a result, they have long been used as standardized model organisms for experimental studies on Scyphozoan ecology [24,26]. However, outside of Aurelia spp., ecological research on Scyphozoans is highly limited, and there is an increasing need for broader ecological studies on Scyphozoans [3,27]. This is particularly important as recent phenomena have shown a rise in the abundance of various Scyphozoan populations [28], and climate change-driven alterations in marine environments may lead to the expansion of their distribution ranges [29]. Such changes could potentially destabilize marine ecosystems, posing a risk of significant ecological impacts [4].
Sanderia malayensis is a species belonging to the phylum Cnidaria, class Scyphozoa, and order Semaeostomeae [30], and it is reported to inhabit tropical waters of the Indian Ocean and Pacific Ocean, including the Red Sea and Malaysian waters [31,32]. However, the distribution of this species has expanded to include northern Australian waters and East Asian waters, including those of Japan [33,34]. The first discovery of Sanderia malayensis in Japan was made in 1938 in the Amakusa region of Kyushu [35]. Later, in 2004, the discovery of natural polyps of Sanderia malayensis forming colonies and inhabiting deep-sea areas of the Kagoshima region was reported [36]. Ecological studies on Sanderia malayensis have primarily focused on various asexual reproductive strategies and habitat conditions during the polyp stage [30,31,37,38]. However, ecological research on the ephyra stage, the free-swimming phase produced through the strobilation process, remains highly limited [39]. Sanderia malayensis has continued to be observed in the East Asian waters of Japan since 2010, with reports indicating that its distribution range is gradually expanding in Japanese waters due to the influence of marine environmental changes [40,41,42]. This suggests that Sanderia malayensis could potentially become an invasive species with the possibility of expanding its distribution into South Korean waters, which are geographically the closest to Japan. Shin and Choi [39] conducted an experiment that simulated the summer temperature conditions of the southern coast of Korea and confirmed the stable growth and high survival rates of Sanderia malayensis ephyrae, suggesting that the environmental factors affecting the growth and survival of this species are more strongly influenced by temperature than by salinity. Additionally, they reported that no significant effects on growth and survival were observed when exposed to salinity levels close to those found in natural environments [39]. The impact of climate change on ocean temperatures, sea level rise, and precipitation is known to significantly influence salinity fluctuations, with increased precipitation playing a particularly important role in enhancing freshwater influx into marine environments, thereby promoting salinity reduction [43]. Additionally, this leads to changes in salinity levels in the marine environment, particularly strengthening salinity stratification [43]. The ephyra stage of Scyphozoans is significantly affected by salinity conditions, which are crucial for their growth and survival [44,45].
This study aimed to predict the potential changes in growth and survival of Sanderia malayensis ephyrae when exposed to coastal marine environments with frequent salinity fluctuations, by creating salinity conditions lower than the natural salinity environment used in the experiment by Shin and Choi [39], and to identify the optimal salinity range for this species. This study aims to understand the impact of salinity environmental factors on the growth and survival of this species, providing fundamental insights, and contributing to the use of this data as an ecological indicator to assess the potential for the expansion of its distribution into South Korean waters due to changes in marine environments caused by future climate change.

2. Materials and Methods

2.1. Acquisition of Sanderia malayensis Ephyrae

For the acquisition of Sanderia malayensis ephyrae in this experiment, Sanderia malayensis polyps were provided by researchers at the Shinagawa Aquarium, located in Minato, Tokyo, Japan (provided in May 2015), and the original source of the polyps could not be verified. Sanderia malayensis polyps were cultured and maintained in an incubator at the Aqua Planet Gwangyo Jellyfish Laboratory in Suwon, South Korea. The method for inducing strobilation to obtain ephyrae was based on the temperature stimulation method used by Fuchs et al. [46] and the temperature conditions under which ephyrae were released from Sanderia malayensis polyps as reported by Avian et al. [30].

2.2. Sanderia malayensis Ephyrae Growth, Survival, and Feeding Response to Salinity

The setup of the experimental treatments (Temperature and Salinity conditions) and the rearing information are shown in Figure 1. The tanks used in the experiment were Breeding Air Kreisel tanks designed and manufactured by Schuran Seawater Equipment BV (Netherlands). The temperature settings for the experimental treatments were designed based on the natural temperature range of 20–22 °C reported by Uchida and Sugiura [47,48] and the 24 °C temperature condition, which demonstrated the highest survival rate (98%) in the study by Shin and Choi [39]. Therefore, two temperature conditions, 20 °C and 24 °C, were chosen as the optimal temperature environments for evaluating the effects of salinity. This selection suggests that these temperatures represent the most preferred and stable temperature range when Sanderia malayensis occurs in the waters of Japan and South Korea [39,47,48].
The salinity settings for the experimental treatments were designed to assess the effects of low-salinity conditions, with three low-salinity treatments at 21 PSU, 24 PSU, and 27 PSU. These salinity values were set lower than the natural salinity range observed in the environment, based on the results from Shin and Choi [39], which found no significant differences in growth and survival at salinities ranging from 30 to 33 PSU. The three different salinity levels were applied equally under both temperature conditions of 20 °C and 24 °C.
All experimental treatments contained 50 ephyrae, which were cultured as described in Section 2.1, with each treatment set up in replicates. The seawater used in this experiment was prepared using Red Sea Salt (Public Aquarium Part A) artificial seawater product from the Red Sea. The experimental period lasted for a total of 20 days, following the duration of the experiment conducted by Shin and Choi [39]. During the experimental period, feeding was provided according to the method proposed by Purcell et al. [2] and the feeding method used in the study by Riisgård [49], where a sufficient amount of Artemia sp. was supplied once a day to ensure that all ephyrae in each treatment received enough food. This was to ensure that the feeding behavior of the cultured ephyrae was not restricted by providing a sufficient amount of Artemia sp. to each treatment. The water quality maintenance for ephyra health was managed through 100% water exchange every other day with pre-filtered clean artificial seawater following the feeding of Artemia sp. The growth, feeding, and survival records of the ephyrae were measured a total of 10 times at 2-day intervals throughout the 20-day experimental period. Growth and feeding were recorded by randomly extracting 10 ephyrae from each treatment, which were set up in replicates, and observing them under an optical microscope (Olympus model SZX2-ILLK, Tokyo, Japan). The growth size increase (mm) was measured according to the method devised by Straehler-Pohl and Jarms [50], using the total diameter of the ephyrae (central disk diameter + total marginal lappet length) as the measurement standard (Figure 2). On Days 1, 10, and 20 of the experiment, the largest individual in terms of diameter was visually selected from each treatment to observe the growth changes of the ephyrae, and images were captured using an optical microscope.
The growth rate of the ephyrae (% d−1) was calculated according to the method for measuring ephyra growth rate devised by Widmer [45], as follows. This method was developed through Båmstedt et al. [51].
% Growth day−1 = ln [(D2/D1)3]/(t2 – t1) × 100
Here, D1 represents the average diameter of the ephyrae on the first measurement day (Day 1), and D2 represents the average diameter two days later (Day 2). Since measurements were recorded at 2-day intervals for a total of 10 times during the 20-day experimental period, the average diameter at each measurement point was represented as D1 and D2 and calculated accordingly. The feeding records of the ephyrae were measured by randomly extracting ephyrae from each treatment 1 h after feeding Artemia sp. and visually confirming the gut content under an optical microscope. The number of Artemia sp. consumed, which was considered completed feeding, was counted and recorded. The survival records of the ephyrae were measured by counting all surviving ephyrae from each treatment and selecting individuals that showed good swimming and feeding behavior, which were then recorded.

2.3. Statistical Analysis

To evaluate the effects of salinity environmental factors on the growth and feeding of Sanderia malayensis ephyrae, we applied the aligned rank transform ANOVA (ART-ANOVA) method. The dependent variables were growth (mm) and feeding (number of individuals), while the independent variables were the three salinity levels (21 PSU, 24 PSU, 27 PSU) and the number of days measured during the experimental period (a total of 10 measurements: 2-day intervals over the 20-day experimental period). All analyses were performed independently under the experimental temperature conditions of 20 °C and 24 °C. To assess the effects of salinity over the course of the experimental period, the interaction effect of salinity × experimental days was included for each temperature condition.
As a result of preliminary testing for homogeneity of variance using Levene’s test, it was found that the assumption of homogeneity was not met for the growth changes measured at the three salinity levels at 20 °C and the feeding changes measured at the three salinity levels at 24 °C. Therefore, to avoid the potential occurrence of statistical errors when applying traditional ANOVA, we employed a non-parametric approach based on ART-ANOVA. ART-ANOVA is a validated non-parametric alternative known to effectively adjust for errors due to violations of homogeneity of variance and can also assess interaction effects between factors [52,53].
Since the assumption of homogeneity of variance was met for the feeding changes measured at the three salinity levels at 20 °C according to Levene’s test, ANOVA was applied. This was done to ensure high statistical power through the parametric method of ANOVA and to estimate clear statistical results and reliability (ART-ANOVA results for the three salinity levels of feeding changes measured at 20 °C, Supplementary Tables S1 and S2). The Holm adjustment was applied as a post hoc test (For the growth changes at three salinity levels at 20 °C and 24 °C, and for the feeding changes at three salinity levels at 24 °C). For the feeding changes measured at three salinity levels at 20 °C, Tukey’s honest significant difference (HSD) test was used to compare the differences between groups.
To evaluate the effect of salinity environmental factors on the survival rate of Sanderia malayensis ephyrae, we independently compared survival curves for each of the three salinity conditions at 20 °C and 24 °C using Kaplan–Meier survival analysis. The hazard ratio based on the survival analysis was assessed using the Cox proportional hazards model to evaluate the impact of salinity differences. All statistical analyses were performed using R version 4.4.2 (R Core Team, 2024). The ARTool package [52] was applied for growth and feeding changes analysis (ART-ANOVA), and the Survival package [54] was used for survival analysis.

3. Results

3.1. Effect of Salinity Environmental Factors on the Growth of Sanderia malayensis Ephyrae

During the 20-day experimental period, the growth changes of Sanderia malayensis ephyrae cultured under three different salinity conditions (21 PSU, 24 PSU, 27 PSU) at 20 °C and 24 °C were captured on Day 1, Day 10, and Day 20. The images of these growth changes for each treatment are shown in Figure 3 and Figure 4. At the end of the 20-day experimental period, the growth changes (size increase) of Sanderia malayensis ephyrae were measured as follows: at 20 °C, the size increased to 6.34 ± 0.14 mm (Mean ± SD) at 21 PSU, 8.47 ± 0.15 mm (Mean ± SD) at 24 PSU, and 8.51 ± 0.13 mm (Mean ± SD) at 27 PSU (Figure 5, Table 1). At 24 °C, the size increased to 6.35 ± 0.14 mm (Mean ± SD) at 21 PSU and 8.50 ± 0.13 mm (Mean ± SD) at both 24 PSU and 27 PSU (Figure 5, Table 1). The growth rate (% d−1) of Sanderia malayensis ephyrae during the 20-day experimental period was as follows: at 20 °C, the growth rate was 10.31% d−1 at 21 PSU, 14.88% d−1 at 24 PSU, and 14.86% d−1 at 27 PSU. At 24 °C, the growth rate was 10.24% d−1 at 21 PSU, 14.80% d−1 at 24 PSU, and 14.94% d−1 at 27 PSU (Table 2). The results of the ART-ANOVA for growth changes under three different salinity conditions at 20 °C and 24 °C showed statistically significant main effects for time (20 °C: F = 633.97, 24 °C: F = 633.98), salinity (20 °C: F = 6023.03, 24 °C: F = 6284.18), and the interaction effect between time and salinity (20 °C: F = 234.03, 24 °C: F = 207.09). These results are presented in Table 3 (p < 0.001). To further examine the interaction effect between time and the three different salinity environments, the Holm post hoc test results showed that the growth at 21 PSU was significantly lower than at 24 PSU and 27 PSU at both 20 °C and 24 °C (Table 1, p < 0.001). However, the difference between 24 PSU and 27 PSU was not statistically significant (Table 1, 20 °C: p = 0.461, 24 °C: p = 0.840).

3.2. Effect of Salinity Environmental Factors on the Feeding of Sanderia malayensis Ephyrae

During the 20-day experimental period, the average feeding rate (Preys ind·h−1) of Sanderia malayensis ephyrae was as follows: at 20 °C, 2.10 ± 0.908 Preys ind·h−1 (Mean ± SD) at 21 PSU, 7.58 ± 1.138 Preys ind·h−1 (Mean ± SD) at 24 PSU, and 7.69 ± 1.165 Preys ind·h−1 (Mean ± SD) at 27 PSU (Figure 6, Table 4). At 24 °C, the average feeding rate was 2.16 ± 0.869 Preys ind·h−1 (Mean ± SD) at 21 PSU, 7.75 ± 1.118 Preys ind·h−1 (Mean ± SD) at 24 PSU, and 7.64 ± 1.136 Preys ind·h−1 (Mean ± SD) at 27 PSU (Figure 6, Table 4). Levene’s test was used for preliminary testing of homogeneity of variance, and based on the results, the analysis method was chosen. The average feeding rate at 20 °C was analyzed using ANOVA, while the average feeding rate at 24 °C was analyzed using ART-ANOVA (Section 2.3. Statistical Analysis). The results of the ANOVA for the average feeding rate (Preys ind·h−1) under three different salinity conditions (21 PSU, 24 PSU, 27 PSU) at 20 °C showed statistically significant main effects for time (F = 2029.04) and salinity (F = 3.16; Table 5, p < 0.001). However, the interaction effect between time and salinity (F = 1.47) was not statistically significant (Table 5, p = 0.085). To further examine the differences in the average feeding rate (Preys ind·h−1) between the three salinity conditions, Tukey post hoc analysis revealed significant differences between 21 PSU and 24 PSU, as well as between 21 PSU and 27 PSU (Table 4, p < 0.001). However, no significant difference was found between 24 PSU and 27 PSU, indicating that the average feeding rate was similar in the relatively higher salinity environments of 24 PSU and 27 PSU compared to 21 PSU (Table 4, p = 0.522).
The results of the ART-ANOVA for the average feeding rate (Preys ind·h−1) under three different salinity conditions at 24 °C showed statistically significant main effects for time (F = 633.18), salinity (F = 3.27), and the interaction effect between time and salinity (F = 2.75) (Table 6, p < 0.001). To further examine the interaction effects between time and the three salinity conditions, the Holm post hoc test revealed significant differences between 21 PSU and 24 PSU, as well as between 21 PSU and 27 PSU (Table 4, p < 0.05). However, no significant difference was found between 24 PSU and 27 PSU, indicating that the average feeding rate was similar in the relatively higher salinity environments of 24 PSU and 27 PSU compared to 21 PSU (Table 4, p = 0.100).

3.3. Effect of Salinity Environmental Factors on the Survival of Sanderia malayensis Ephyrae

The Kaplan–Meier survival analysis results for Sanderia malayensis ephyrae cultured under three different salinity conditions (21 PSU, 24 PSU, 27 PSU) at 20 °C and 24 °C during the 20-day experimental period are shown in Figure 7. The survival rates at 20 °C were 70% (95% CI: 62–80%) at 21 PSU, 90% (95% CI: 84–96%) at 24 PSU, and 87% (95% CI: 81–94%) at 27 PSU (Figure 7, Table 7). The results of the log-rank test showed a significant difference in the survival curves between the three different salinity conditions (χ2 = 17.746, df = 2, Figure 7, p < 0.001). The survival rates at 24 °C were 55% (95% CI: 46–66%) at 21 PSU, 79% (95% CI: 69–86%) at 24 PSU, and 86% (95% CI: 79–93%) at 27 PSU (Figure 7, Table 7). The log-rank test results also showed a significant difference in the survival curves between the three salinity conditions (χ2 = 28.008, df = 2, Figure 7, p < 0.001). In the Cox hazard ratio analysis to assess the effects of the three different salinity conditions (21 PSU, 24 PSU, 27 PSU), with 21 PSU set as the reference, the survival rates at both 20 °C and 24 °C were found to significantly increase at 24 PSU and 27 PSU (p < 0.001, Supplementary Figures S1 and S2). At 20 °C, the hazard ratios for 24 PSU and 27 PSU were 0.29 (95% CI: 0.14–0.59, p < 0.001) and 0.38 (95% CI: 0.20–0.72, p = 0.003), respectively. At 24 °C, the hazard ratios for 24 PSU and 27 PSU were 0.42 (95% CI: 0.25–0.69, p < 0.001) and 0.25 (95% CI: 0.14–0.46, p < 0.001), respectively. The p-value for the global log-rank test was calculated to be <0.001, indicating that there was a statistically significant difference in survival rates between the three different salinity conditions (p < 0.001).

4. Discussion

This study aimed to evaluate the effects of salinity on the growth and survival of Sanderia malayensis ephyrae and to determine their optimal salinity range. Sanderia malayensis ephyrae showed stable growth changes in environments with salinities of 24 PSU and 27 PSU (Figure 5, Table 1), which was also confirmed by the survival rate results (Figure 7, Table 7). The environment with 21 PSU showed significantly lower growth changes (Figure 5, Table 1, p < 0.001) and survival rates (Figure 7, Table 7, p < 0.001) compared to 24 PSU and 27 PSU. However, a certain level of environmental adaptability was observed. These findings demonstrate that this species has the ability to adapt very well to a wide range of salinity conditions.
Previous studies on Sanderia malayensis ephyrae have primarily focused on morphological characteristics [37,50,55], as well as ecological studies during the polyp stage [30,31,38,48]. However, biological and ecological research on the free-swimming phase, which follows the polyp stage, remains largely unexplored [39]. This may be due to the technical challenges involved in studying the free-swimming stage, including the need for advanced techniques and the establishment of life-support systems [56]. Sanderia malayensis is known to be a representative species of Scyphozoans commonly exhibited in aquariums worldwide [30], and aquariums possess the necessary technologies and manuals for year-round display of various Scyphozoans [57].
This aspect may present one of the significant challenges faced by researchers in studying the free-swimming phase of Scyphozoan species, including Sanderia malayensis. The effects of salinity environmental factors on the survival and growth of Scyphozoan ephyrae during the free-swimming stage have been reported in various studies [24,44,45,58,59,60]. Båmstedt et al. [44] found no significant impact on growth rate and growth efficiency between 17.5 PSU and 35 PSU in their experiment on Aurelia aurita, but they reported very high feeding rates when exposed to 35 PSU, suggesting that the stable feeding rate of Aurelia aurita is attributed to higher salinity environments. Purcell et al. [58] suggested that Chrysaora quinquecirrha prefers survival in environments with salinities below 20 PSU, and Windmer [45] confirmed a high growth rate of Cyanaea capillata in the low-salinity environment of 21 PSU, while Chyrasora hyoscella showed maximum growth rate at 34 PSU.
Additionally, in studies on Aurelia coerulea, Fu et al. [59] reported that Aurelia coerulea increased its growth rate when exposed to lower salinity, and research by Schäfer et al. [24] and Yu et al. [60] also suggested that salinity levels of 20 PSU and 25 PSU resulted in higher growth rates of Aurelia coerulea compared to environments with salinities above 30 PSU, indicating that lower salinity environments had a significant effect on growth. In this study, Sanderia malayensis ephyrae showed a tendency for both growth (Figure 5, Table 1) and survival (Figure 7, Table 7) to increase with higher salinity, while feeding rates were found to be lower in the 21 PSU environment compared to 24 PSU and 27 PSU (Figure 6, Table 4, p < 0.001). These results suggest that this species has the ability to adapt to a wide range of salinity conditions, but it prefers higher salinity environments for stable growth and survival.
In the study by Shin and Choi [39], which simulated the summer temperature conditions of the southern coast of Korea, no significant differences were observed in the growth and survival of Sanderia malayensis ephyrae under salinity conditions of 30–33 PSU at 24 °C, with a very high survival rate of 98%. In this study, the survival rates at 24 PSU and 27 PSU were 90% and 87% (Figure 7, Table 7) at 20 °C, and 79% and 86% (Figure 7, Table 7) at 24 °C. However, the survival rate at 21 PSU was significantly lower than at 24 PSU and 27 PSU (20 °C: 70%, 24 °C: 55%, p < 0.001).
Therefore, based on the results of both the Shin and Choi [39] study and this study, the ideal salinity range for the growth and survival of Sanderia malayensis ephyrae is estimated to be between 24 PSU and 33 PSU. In the study by Shin and Choi [39], the salinity range of 30 PSU to 33 PSU may represent the stable optimal salinity range for this species.
Chrysaora species such as Cynanea capillata and Cynanea lamarckii have a medusivorous ecology, feeding on gelatinous plankton [45], and Avian et al. [30] reported in a laboratory study that Sanderia malayensis ephyrae were observed to unilaterally prey on Aurelia solida ephyrae. In natural environments, the abundance of zooplankton is a contributing factor to Scyphozoan outbreaks [1], and feeding on prey with appropriate nutrients has a significant impact on the growth and survival of Scyphozoans [61]. The most commonly used zooplankton in global Scyphozoan research are Artemia sp. and Brachiounus spp. [8,62]. In this study, Artemia sp. was provided as the prey for Sanderia malayensis ephyrae, with no additional nutritional supplementation.
Considering that Sanderia malayensis has a medusivorous ecology feeding on gelatinous plankton [30], it is possible that rapid growth could be induced when Sanderia malayensis ephyrae prey on Aurelia spp. (Aurelia solida, Aurelia labiata, Aurelia coerulea). Additionally, if Sanderia malayensis expands its distribution into South Korean waters in the future, it may compete for food in the marine ecosystem with Aurelia coerulea, which is known for its outbreaks during the summer and may prey on Aurelia coerulea [4]. This possibility is supported by the findings of this study, which demonstrate that Sanderia malayensis is highly adaptable to a wide range of salinity conditions, similar to the results found in studies on Aurelia spp. [24,44,59,60,63].
Shin and Choi [39] suggested that the optimal temperature range for the growth and survival of Sanderia malayensis is between 20 °C and 24 °C, while Avian et al. [30] reported that the polyps of this species have the ability to reproduce even at 20 °C. Furthermore, this species has a wide distribution range, not only in the Indian Ocean, Pacific Ocean, and Suez Canal but also in East Asian waters, including Japan [32]. Notably, the species has been reported to appear from spring to summer May to August in the waters of Japan, which are geographically close to the waters of Republic of Korea [40,41,42].
This study confirmed that Sanderia malayensis ephyrae exhibit stable growth and survival across a range of salinity environments, demonstrating a high level of adaptability. These findings suggest that Sanderia malayensis could potentially become an invasive species capable of expanding its distribution into South Korean waters, which are affected by climate change.
Considering the broad salinity tolerance of Sanderia malayensis ephyrae, it is important to evaluate the broader ecological implications of its potential distribution. This is supported by the outbreak of Nemopilema nomurai, which expanded from China to Korea and Japan [64,65].
Such an expansion could lead to significant ecological changes, particularly in terms of competition for food resources with native marine organisms, such as Aurelia coerulea [4], and it could result in important changes to regional marine ecosystems [1,2,3]. Moreover, the effects of climate change should be recognized in terms of the interconnectedness of marine ecosystems across borders [43]. In particular, jellyfish movement may be influenced by ocean currents [66], potentially leading to regional jellyfish blooms that could have widespread effects on fisheries, tourism, and marine biodiversity [8,9].
As seen in the outbreak of Nemopilema nomurai in East Asian waters [64,65], future research on Sanderia malayensis should broadly examine the impacts on neighboring regions, including China and Japan. Therefore, future studies should not only focus on localized research but also consider the potential impacts on these regions.
By integrating data on jellyfish occurrences from these regions, we can gain a more comprehensive understanding of the impacts on food webs and ecosystem services. Considering the global economic and ecological consequences of jellyfish blooms [5,6], further research into the potential invasion of Sanderia malayensis and its role in the broader context of climate change and marine ecosystem health is crucial, particularly regarding the potential impacts on ecosystems when this species expands its distribution.

5. Conclusions

This study confirmed that Sanderia malayensis ephyrae exhibit stable growth (Figure 5, Table 1) and high survival rates (Figure 7, Table 7) across a wide range of salinity environments, demonstrating a high level of adaptability to varying salinity conditions. Sanderia malayensis is distributed in the waters of Japan, which is geographically close to South Korea. Considering this, the findings suggest that this species could potentially expand its distribution into South Korea and other East Asian waters affected by climate change. Therefore, future research should focus on evaluating the potential ecological impacts of its distribution expansion in East Asian waters, including China and Japan, particularly in terms of competition with other marine organisms and the resulting changes to regional marine ecosystems within the context of climate change.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d17040239/s1, Tables S1 and S2: ART-ANOVA results for feeding rate changes at three salinity levels (21 PSU, 24 PSU, 27 PSU) measured at 20 °C. Figure S1 and S2: Cox hazard ratio analysis results for survival rates at salinities of 21 PSU, 24 PSU, and 27 PSU under two different temperatures (20 °C and 24 °C) for evaluation.

Author Contributions

Conceptualization, K.-H.S. and K.-H.C.; Methodology, K.-H.S. and K.-H.C.; Formal analysis and investigation, K.-H.S.; Supervision, K.-H.C.; Writing—original draft preparation, K.-H.S.; Writing—review and editing, K.-H.S. and K.-H.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by Chungnam National University (Project No. 2023–0652–01).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data generated or analyzed during this study are available upon reasonable request. The data are either included in the main body of the article or provided as supplementary materials.

Acknowledgments

We would like to express our sincere gratitude to Aqua Planet Aquarium for providing and supporting the Sanderia malayensis ephyrae for this study. We also extend our heartfelt thanks to Keun-Hyung Choi from the Department of Earth, Environmental and Space Sciences at Chungnam National University for his extensive guidance and invaluable advice throughout the course of this research.

Conflicts of Interest

Author Kyong-Ho Shin was employed by Aqua Planet Corporation, Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

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Figure 1. Schematic figure representing the experimental design: The experimental design to assess the effects of low salinity on the survival and growth of Sanderia malayensis ephyrae was as follows. The experiment was conducted under two temperature conditions, 20 °C and 24 °C, with three different salinity levels. Each experimental group was replicated twice, with 50 ephyrae cultured in each Breeding Air Kreisel tank. As a result, 100 ephyrae were cultured per salinity level under each temperature condition, totaling 600 ephyrae across both temperature conditions.
Figure 1. Schematic figure representing the experimental design: The experimental design to assess the effects of low salinity on the survival and growth of Sanderia malayensis ephyrae was as follows. The experiment was conducted under two temperature conditions, 20 °C and 24 °C, with three different salinity levels. Each experimental group was replicated twice, with 50 ephyrae cultured in each Breeding Air Kreisel tank. As a result, 100 ephyrae were cultured per salinity level under each temperature condition, totaling 600 ephyrae across both temperature conditions.
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Figure 2. In this experiment, the measurement points and range criteria for assessing the growth changes of Sanderia malayensis ephyrae were adapted from Straehler-Pohl and Jarms [50]. The red lines represent the measurement ranges for each section, and the blue lines indicate the diameter names corresponding to each measurement range. Measurements were taken based on the central disc diameter (mm) and total marginal lappet length (mm) of the ephyrae (the image was captured using an Olympus model SZX2-ILLK microscope, Tokyo, Japan).
Figure 2. In this experiment, the measurement points and range criteria for assessing the growth changes of Sanderia malayensis ephyrae were adapted from Straehler-Pohl and Jarms [50]. The red lines represent the measurement ranges for each section, and the blue lines indicate the diameter names corresponding to each measurement range. Measurements were taken based on the central disc diameter (mm) and total marginal lappet length (mm) of the ephyrae (the image was captured using an Olympus model SZX2-ILLK microscope, Tokyo, Japan).
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Figure 3. The growth changes of Sanderia malayensis ephyrae were recorded three times during the 20-day experimental period (on Days 1, 10, and 20). The experiment was conducted at a temperature of 20 °C with three different salinity conditions: 21 PSU, 24 PSU, and 27 PSU.
Figure 3. The growth changes of Sanderia malayensis ephyrae were recorded three times during the 20-day experimental period (on Days 1, 10, and 20). The experiment was conducted at a temperature of 20 °C with three different salinity conditions: 21 PSU, 24 PSU, and 27 PSU.
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Figure 4. The growth changes of Sanderia malayensis ephyrae were recorded three times during the 20-day experimental period (On days 1, 10, and 20). The experiment was conducted at a temperature of 24 °C with three different salinity conditions: 21 PSU, 24 PSU, and 27 PSU.
Figure 4. The growth changes of Sanderia malayensis ephyrae were recorded three times during the 20-day experimental period (On days 1, 10, and 20). The experiment was conducted at a temperature of 24 °C with three different salinity conditions: 21 PSU, 24 PSU, and 27 PSU.
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Figure 5. The growth changes (size increase: mm) of Sanderia malayensis ephyrae over 20 days: At temperatures of 20 °C and 24 °C, the growth in the 21PSU salinity environment was significantly lower than in the 24 PSU and 27 PSU environments ((A,B): p < 0.001). However, no significant differences were observed between the 24 PSU and 27 PSU salinity environments—(A): p = 0.461, (B): p = 0.840.
Figure 5. The growth changes (size increase: mm) of Sanderia malayensis ephyrae over 20 days: At temperatures of 20 °C and 24 °C, the growth in the 21PSU salinity environment was significantly lower than in the 24 PSU and 27 PSU environments ((A,B): p < 0.001). However, no significant differences were observed between the 24 PSU and 27 PSU salinity environments—(A): p = 0.461, (B): p = 0.840.
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Figure 6. The feeding rate changes (preys ind−1 h−1) of Sanderia malayensis ephyrae over 20 days: At temperatures of 20 °C (Tukey post hoc test) and 24 °C (Holm post hoc test), the feeding rate in the 21 PSU salinity environment was significantly lower compared to the 24 PSU and 27 PSU environments ((A,B): p < 0.001). However, no significant differences were observed between the 24 PSU and 27 PSU salinity environments (A): p = 0.522, (B): p = 0.100).
Figure 6. The feeding rate changes (preys ind−1 h−1) of Sanderia malayensis ephyrae over 20 days: At temperatures of 20 °C (Tukey post hoc test) and 24 °C (Holm post hoc test), the feeding rate in the 21 PSU salinity environment was significantly lower compared to the 24 PSU and 27 PSU environments ((A,B): p < 0.001). However, no significant differences were observed between the 24 PSU and 27 PSU salinity environments (A): p = 0.522, (B): p = 0.100).
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Figure 7. Kaplan–Meier survival analysis of Sanderia malayensis ephyrae over 20 days: Significant differences in survival curves were observed between the salinity conditions (21 PSU, 24 PSU, 27 PSU) at 20 °C and 24 °C (20 °C: χ2 = 17.746, DF = 2; 24 °C: χ2 = 28.008, DF = 2, p < 0.001). The effects of the three different salinity conditions were further evaluated using the Cox hazard ratio analysis, as shown in Figures S1 and S2.
Figure 7. Kaplan–Meier survival analysis of Sanderia malayensis ephyrae over 20 days: Significant differences in survival curves were observed between the salinity conditions (21 PSU, 24 PSU, 27 PSU) at 20 °C and 24 °C (20 °C: χ2 = 17.746, DF = 2; 24 °C: χ2 = 28.008, DF = 2, p < 0.001). The effects of the three different salinity conditions were further evaluated using the Cox hazard ratio analysis, as shown in Figures S1 and S2.
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Table 1. The growth changes (size increase) of Sanderia malayensis ephyrae were measured under two temperature conditions (20 °C, 24 °C) across three salinity levels (21 PSU, 24 PSU, 27 PSU). Statistical significance was determined using the Holm post hoc test. Growth at 21 PSU was significantly lower than at 24 PSU and 27 PSU (a, p < 0.001), while no significant difference in growth was observed between 24 PSU and 27 PSU (b, p > 0.05).
Table 1. The growth changes (size increase) of Sanderia malayensis ephyrae were measured under two temperature conditions (20 °C, 24 °C) across three salinity levels (21 PSU, 24 PSU, 27 PSU). Statistical significance was determined using the Holm post hoc test. Growth at 21 PSU was significantly lower than at 24 PSU and 27 PSU (a, p < 0.001), while no significant difference in growth was observed between 24 PSU and 27 PSU (b, p > 0.05).
Temperature (°C)Salinity
(PSU)		Size Increase (mm, n = 10)95% Confidence Interval
MeanSDLower Limit
(CI)		Upper Limit
(CI)
20216.34 a0.146.16.7
248.47 b0.158.28.7
278.51 b0.138.38.7
24216.35 a0.146.16.6
248.50 b0.138.38.7
278.50 b0.138.38.7
Table 2. The growth rates (% d−1) of Sanderia malayensis ephyrae at three salinity levels (21 PSU, 24 PSU, 27 PSU) under two temperature conditions (20 °C, 24 °C) were measured following the method outlined by Bamstedt et al. [51]. The sample size for each treatment group was n = 10.
Table 2. The growth rates (% d−1) of Sanderia malayensis ephyrae at three salinity levels (21 PSU, 24 PSU, 27 PSU) under two temperature conditions (20 °C, 24 °C) were measured following the method outlined by Bamstedt et al. [51]. The sample size for each treatment group was n = 10.
Temperature (°C)Salinity
(PSU)		 95% Confidence Interval
Growth Rate
(% d−1, n = 10)		Lower Limit
(CI)		Upper Limit
(CI)
202110.3110.1910.71
2414.8814.8314.86
2714.8614.8315.05
242110.2410.1910.47
2414.814.3815.05
2714.9414.3815.05
Table 3. The statistical significance of growth changes (size increase) in Sanderia malayensis ephyrae under two temperature conditions (20 °C, 24 °C) and three salinity levels (21 PSU, 24 PSU, 27 PSU) was assessed using ART-ANOVA. A significant interaction effect between time and salinity was observed (p < 0.001), and the results of the Holm post hoc analysis are provided in the main text.
Table 3. The statistical significance of growth changes (size increase) in Sanderia malayensis ephyrae under two temperature conditions (20 °C, 24 °C) and three salinity levels (21 PSU, 24 PSU, 27 PSU) was assessed using ART-ANOVA. A significant interaction effect between time and salinity was observed (p < 0.001), and the results of the Holm post hoc analysis are provided in the main text.
Temperature (°C) Source Size Increase (mm, n = 10)
Degrees of
Freedom		Sum of
Squares		F-Valuep-Value
20Time215,988,153.54 633.97<0.001
Salinity1023,703,043.106023.03<0.001
Salinity × Days2020,791,713.35234.03<0.001
24Time215,974,650.91633.98<0.001
Salinity1023,715,381.336284.18<0.001
Salinity × Days2020,437,093.72207.09<0.001
Table 4. The feeding rate (Preys ind−1 h−1) results of Sanderia malayensis ephyrae under two temperature conditions (20 °C, 24 °C) and three salinity levels (21 PSU, 24 PSU, 27 PSU) are presented. Statistical significance was determined using the Tukey post hoc test at 20 °C and the Holm post hoc test at 24 °C. Growth at 21 PSU was significantly lower compared to 24 PSU and 27 PSU (a, p < 0.001), while no significant difference in growth was observed between 24 PSU and 27 PSU (b, p > 0.05).
Table 4. The feeding rate (Preys ind−1 h−1) results of Sanderia malayensis ephyrae under two temperature conditions (20 °C, 24 °C) and three salinity levels (21 PSU, 24 PSU, 27 PSU) are presented. Statistical significance was determined using the Tukey post hoc test at 20 °C and the Holm post hoc test at 24 °C. Growth at 21 PSU was significantly lower compared to 24 PSU and 27 PSU (a, p < 0.001), while no significant difference in growth was observed between 24 PSU and 27 PSU (b, p > 0.05).
Temperature (°C)Salinity
(PSU)		Feeding Rate
(Artemia ind−1 h−1, n = 10)		95% Confidence Interval
MeanSDLower Limit
(CI)		Upper Limit
(CI)
20212.10 a0.9080.004.00
247.58 b1.1385.0010.00
277.69 b1.1654.0010.00
24212.16 a0.8690.005.00
247.75 b1.1185.0010.00
277.64 b1.1365.0011.00
Table 5. The statistical significance of feeding rates of Sanderia malayensis ephyrae at three salinity levels (21 PSU, 24 PSU, 27 PSU) under a temperature condition of 20 °C was assessed using ANOVA. No significant interaction effect between time and salinity was observed (p = 0.085), and the results of the Tukey post hoc analysis are provided in the main text.
Table 5. The statistical significance of feeding rates of Sanderia malayensis ephyrae at three salinity levels (21 PSU, 24 PSU, 27 PSU) under a temperature condition of 20 °C was assessed using ANOVA. No significant interaction effect between time and salinity was observed (p = 0.085), and the results of the Tukey post hoc analysis are provided in the main text.
Source Feeding Rate (Artemia ind−1 h−1, n = 10)
Sum of
Squares		Degrees of
Freedom		Mean of
Squares		F-Valuep-Value
Time4489222452029.04<0.001
Salinity351033.16<0.001
Salinity × Days332021.470.085
Table 6. The statistical significance of feeding rates of Sanderia malayensis ephyrae at three salinity levels (21 PSU, 24 PSU, 27 PSU) under a temperature condition of 24 °C was assessed using ART-ANOVA. A significant interaction effect between time and salinity was observed (p = 0.001), and the results of the Holm post hoc analysis are provided in the main text.
Table 6. The statistical significance of feeding rates of Sanderia malayensis ephyrae at three salinity levels (21 PSU, 24 PSU, 27 PSU) under a temperature condition of 24 °C was assessed using ART-ANOVA. A significant interaction effect between time and salinity was observed (p = 0.001), and the results of the Holm post hoc analysis are provided in the main text.
Source Feeding Rate (Artemia ind−1 h−1, n = 10)
Degrees of
Freedom		Sum of
Squares		F-Valuep-Value
Time215,983,505.68633.18<0.001
Salinity101,186,144.583.27<0.001
Salinity × Days201,927,731.322.75<0.001
Table 7. The Kaplan–Meier survival analysis results of Sanderia malayensis ephyrae under two temperature conditions (20 °C, 24 °C) and three salinity levels (21 PSU, 24 PSU, 27 PSU) are presented. The log-rank test revealed a significant difference in survival curves among the three salinity levels (a, b, c: There were significant differences among salinity levels, p < 0.001).
Table 7. The Kaplan–Meier survival analysis results of Sanderia malayensis ephyrae under two temperature conditions (20 °C, 24 °C) and three salinity levels (21 PSU, 24 PSU, 27 PSU) are presented. The log-rank test revealed a significant difference in survival curves among the three salinity levels (a, b, c: There were significant differences among salinity levels, p < 0.001).
Temperature (°C)Salinity
(PSU)		Survival Rate
(%)		Observed
Event		95% Confidence Interval
Lower Limit
(CI)		Upper Limit
(CI)
2021 a70300.620.80
24 b90100.840.96
27 c87130.810.94
2421 a55450.460.66
24 b79210.690.86
27 c86140.790.93
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MDPI and ACS Style

Shin, K.-H.; Choi, K.-H. The Effects of Salinity on the Growth, Survival, and Feeding of Sanderia malayensis (Cnidaria: Scyphozoa) Ephyrae. Diversity 2025, 17, 239. https://doi.org/10.3390/d17040239

AMA Style

Shin K-H, Choi K-H. The Effects of Salinity on the Growth, Survival, and Feeding of Sanderia malayensis (Cnidaria: Scyphozoa) Ephyrae. Diversity. 2025; 17(4):239. https://doi.org/10.3390/d17040239

Chicago/Turabian Style

Shin, Kyong-Ho, and Keun-Hyung Choi. 2025. "The Effects of Salinity on the Growth, Survival, and Feeding of Sanderia malayensis (Cnidaria: Scyphozoa) Ephyrae" Diversity 17, no. 4: 239. https://doi.org/10.3390/d17040239

APA Style

Shin, K.-H., & Choi, K.-H. (2025). The Effects of Salinity on the Growth, Survival, and Feeding of Sanderia malayensis (Cnidaria: Scyphozoa) Ephyrae. Diversity, 17(4), 239. https://doi.org/10.3390/d17040239

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