Ecophysiology of the kleptoplastidic dinoflagellate Shimiella gracilenta: II. Effects of temperature and global warming

Article information

Algae. 2022;37(1):49-62
Publication date (electronic) : 2022 March 15
doi : https://doi.org/10.4490/algae.2022.37.3.2
1School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul 08826, Korea
2Research Institute of Oceanography, Seoul National University, Seoul 08826, Korea
*Corresponding Author: E-mail: hjjeong@snu.ac.kr, Tel: +82-2-880-6746, Fax: +82-2-874-9695
Received 2022 January 10; Accepted 2022 March 2.

Abstract

Water temperature affects plankton survival and growth. The dinoflagellate Shimiella gracilenta survives using the plastids of ingested prey, indicating kleptoplastidy. However, studies on the effects of water temperature on kleptoplastidic dinoflagellates are lacking. We explored the growth and ingestion rates of S. gracilenta as a function of water temperature. Furthermore, using data on its spatiotemporal distribution in Korean coastal waters during 2015–2018, we predicted its distribution under elevated temperature conditions of +2, +4, and +6°C. Growth rates of S. gracilenta with and without Teleaulax amphioxeia prey as well as ingestion rates were significantly affected by water temperature. Growth rates of S. gracilenta with and without prey were positive or zero at 5–25°C but were negative at ≥ 30°C. The maximum growth rate of S. gracilenta with T. amphioxeia was 0.85 d−1, achieved at 25°C, and 0.21 d−1 at 20°C without prey. The ingestion rate of S. gracilenta on T. amphioxeia at 25°C (0.05 ng C predator−1 d−1) was greater than that at 20°C (0.04 ng C predator−1 d−1). Thus, feeding may shift the optimal temperature for the maximum growth rate of S. gracilenta from 20 to 25°C. In spring and winter, the distributions of S. gracilenta under elevated temperature conditions were predicted not to differ from those during 2015–2018. However, S. gracilenta was predicted not to survive at some additional stations under elevated temperature conditions of +2, +4, and +6°C in summer or under elevated temperature conditions of +6°C in autumn. Therefore, global warming may affect the distribution of S. gracilenta.

INTRODUCTION

Water temperature frequently affects the survival, growth, and distribution of marine organisms (Loeng 1989, Gillooly 2000, Hiscock et al. 2004, Ok et al. 2018, Lee et al. 2019, Frölicher et al. 2020, Lim and Jeong 2021). Thus, there have been many studies on the effects of temperature on the ecophysiology of marine organisms (Beitinger and Fitzpatrick 1979, Thompson et al. 1992, Oliver and Palumbi 2011, Thomas et al. 2012, Lim et al. 2020, Kang et al. 2021). In addition, there have been various studies on predicting the distributions of several target marine organisms during climate change periods (Perry et al. 2005, Witt et al. 2010, Freeman et al. 2013, Jueterbock et al. 2013, Langer et al. 2013, Poloczanska et al. 2016). However, there are still many species whose responses to changes in water temperature should be explored.

Dinoflagellates are a major group of eukaryotic microorganisms in marine ecosystems that are found from the equator to the poles (Taylor et al. 2008, Jeong et al. 2021). They play diverse ecological roles, including primary producers, prey, predators, symbionts, and parasites (Coats 1999, Jeong 1999, Stat et al. 2008, Jeong et al. 2010, Montero et al. 2017, Ok et al. 2017, You et al. 2020a). Moreover, dinoflagellates frequently dominate natural assemblages, causing red tides or harmful algal blooms (Smayda and Reynolds 2003, Kudela and Gobler 2012, Jeong et al. 2013, 2015, 2021, Eom et al. 2021, Ok et al. 2021c). Therefore, changes in the distribution of dinoflagellate species can alter the structure and function of marine ecosystems. Dinoflagellates experience natural fluctuations in water temperature due to seasonal changes, and their distributions are known to be affected by changes in water temperature (Anderson and Rengefors 2006, Torres et al. 2019, Lee et al. 2020). Dinoflagellates grow the fastest at optimal water temperatures but die below or above a certain water temperature (e.g., Lim et al. 2019, Ok et al. 2019, Kang et al. 2020). The optimal water temperature and lower or upper temperature limits for the survival of dinoflagellates are species-dependent (e.g., Nielsen 1996, Laabir et al. 2011, Jeong et al. 2018, You et al. 2020b). Global warming elevates water temperature and may seriously affect the survival or distribution of dinoflagellates (Tunin-Ley et al. 2009, Kibler et al. 2015, Intergovernmental Panel on Climate Change 2021). Therefore, determining the optimal water temperature and lower and upper temperature limits for the survival of each dinoflagellate species is a critical step in understanding their ecophysiology. Furthermore, predicting the distribution of dinoflagellate species in the global warming period is important for predicting changes in the structure and function of marine ecosystems.

Shimiella gracilenta (previously Gymnodinium gracilentum) is a kleptoplastidic dinoflagellate that survives for approximately one month using the plastids of ingested prey cells (Skovgaard 1998, Ok et al. 2021b). This species can feed on prey species belonging to diverse taxa and is preyed on by some heterotrophic protists (Jakobsen et al. 2000, Ok et al. 2021a, Park et al. 2021). Furthermore, S. gracilenta was found at all 28 stations in Korea from 2015 to 2018 (Ok et al. 2021a). Thus, S. gracilenta may play diverse roles in marine ecosystems. In the late 21st century, Suh et al. (2016) predicted an increase in the surface air temperature by up to 5–8°C on the Korean Peninsula. Moreover, up to 4–5°C increase in seawater temperature surrounding the Korean Peninsula has been predicted (Kim et al. 2016). Thus, the distribution of S. gracilenta in Korean coastal waters may change in the future. To predict the future distribution and survival of S. gracilenta during the current global warming period, the growth rates of S. gracilenta under different temperature conditions and its lower and upper temperature limits for survival should be determined.

In the present study, we determined the growth rates of S. gracilenta SGJH1904 with and without the presence of the prey Teleaulax amphioxeia TAGS0202 and the ingestion rates as a function of water temperature. Furthermore, using data on its spatiotemporal distribution in Korean coastal waters during 2015–2018, we predicted its spatiotemporal distribution under elevated water temperatures that deviated +2, +4, and +6°C from the average for the period. The results of the present study provide a basis for understanding the effects of water temperature on the ecophysiological characteristics and distributions of S. gracilenta.

MATERIALS AND METHODS

Temperature effects on the growth and ingestion rates of Shimiella gracilenta

The growth and ingestion rates of S. gracilenta SGJH-1904 with and without added T. amphioxeia TAGS0202 at a single high prey abundance were measured at 5, 10, 15, 20, 25, 30, and 35°C. Clonal cultures of S. gracilenta SGJH1904 and T. amphioxeia TAGS0202 were established and incubated at 20°C as described in our previous study (Ok et al. 2021a). A culture of S. gracilenta growing on T. amphioxeia prey was transferred into a 10-L polycarbonate (PC) bottle. Four days later, the abundance of prey cells in the bottle was <10 cells mL−1. The dense culture in the bottle (ca. 70,000 cells mL−1) was transferred to seven 250-mL flasks. A dense culture of T. amphioxeia TAGS0202 (ca. 100,000 cells mL−1) was also transferred to each of the seven 250-mL flasks.

The target temperatures were established in seven temperature-controlled chambers. Prior to the experiment, the cultures were gradually acclimated to the target temperature for nine days to minimize the thermal shock on S. gracilenta and T. amphioxeia, following Lim et al. (2019), Ok et al. (2019), You et al. (2020b), and Kang et al. (2020) (Supplementary Fig. S1). During the preincubation period, 5-mL aliquots were collected from each flask at 3-day intervals and fixed with 5% Lugol’s solution to measure the abundance of S. gracilenta and T. amphioxeia. Finally, each culture of S. gracilenta or T. amphioxeia was placed in each chamber where the target temperature was established and incubated under a 14: 10 h light: dark cycle and 100 μmol photons m−2 s−1 of a light-emitting diode (LED; FS-075MU, 6500 K; Suram Inc., Suwon, Korea). However, in the preliminary test, all S. gracilenta and T. amphioxeia cells died at 35°C. Therefore, each culture of S. gracilenta and T. amphioxeia was acclimated at 25°C for 8 days and then at 30°C for 1 day, and these were used for the experiment at 35°C (Supplementary Fig. S1).

The initial single high prey abundance at which the growth and ingestion rates of S. gracilenta SGJH1904 on T. amphioxeia TAGS0202 were saturated was chosen (Ok et al. 2021a). Triplicate 38-mL flasks with predator-prey mixtures, predator-only controls (i.e., S. gracilenta only), and prey-only controls (i.e., T. amphioxeia only) were set up for each target temperature. The cell-free filtrates of S. gracilenta and T. amphioxeia were added to prey-only controls and predator-only controls, respectively, as described in our previous study (Ok et al. 2021a). Five milliliters of f/2 medium was added to all the flasks and filled with freshly filtered seawater. To determine the actual predator and prey abundances (cells mL−1) at the beginning of the experiment (Table 1), 5-mL aliquots were taken from each flask and fixed with Lugol’s solution. After subsampling at the beginning of the experiment, the flasks were refilled to capacity with freshly filtered seawater. The flasks were incubated for two days at each target temperature under a 14: 10 h light: dark cycle and 100 μmol photons m−2 s−1 of a LED. After a 2-day incubation, 10-mL aliquots were taken from each flask and fixed as described above.

Actual initial abundance (cells mL−1) of the predator Shimiella gracilenta SGJH1904 and prey Teleaulax amphioxeia TAGS0202

The specific growth rate (μ, d−1) of S. gracilenta SGJH-1904 was calculated using the following equation:

μ=Ln(CtC0)t

, where C0 and Ct represents the abundance of S. gracilenta at the beginning of incubation and after the 2-day incubation, respectively. The ingestion and clearance rates were calculated using the equation of Frost (1972) and the modified equation of Heinbokel (1978). The carbon content of T. amphioxeia was determined by Jeong et al. (2005).

The ingestion rates of S. gracilenta on T. amphioxeia at 30 and 35°C were not provided because the growth rates of S. gracilenta on T. amphioxeia at these water temperatures were negative, which could overestimate its ingestion rates.

Prediction of the distribution of Shimiella gracilenta under elevated water temperature

To explore the effects of warming on the survival of S. gracilenta, data on its spatiotemporal distribution and water temperature from 28 stations in Korean coastal waters from 2015 to 2018 were obtained from our previous study (Ok et al. 2021a). The water temperatures at each station in each season from 2015 to 2018 were averaged (+0°C). Then, 2, 4, and 6°C were added to the average water temperature at each station in each season (hereafter, +2, +4, and +6°C, respectively). To predict the presence or absence of S. gracilenta under elevated temperature conditions, the range of water temperatures for the survival of S. gracilenta, 1.7–26.4°C, was chosen from the results of our field observations (Ok et al. 2021a). Eight stations (Ansan, AS; Dangjin, DAJ; Mageompo, MGP; Taean, TA; Seocheon, SCN; Kunsan, KS; Buan, BA; and Mokpo, MP) were included in the West Sea of Korea, nine stations (Jangheung, JAH; Goheung, GH; Yeosu, YS; Kwangyang, KY; Tongyoung, TY; Masan, MS; Jinhae, JH; Dadaepo, DDP; and Busan, BS) in the South Sea of Korea, six stations (Ulsan, US; Pohang, PH; Uljin, UJ; Donghae, DH; Jumunjin, JMJ; and Sokcho, SC) in the East Sea of Korea, and five stations (Aewol, AW; Seogwipo, SGP; Wimi, WM; Seongsan, SS; and Gimnyeong, GN) in Jeju Island (Ok et al. 2021a).

Statistical analysis

To examine the effects of water temperature on the growth and ingestion rates of S. gracilenta SGJH1904, a one-way analysis of variance (ANOVA) with a post-hoc Tukey’s honestly significant difference (HSD) test was used. Prior to analysis, the normality and homogeneity of the data were tested using the Shapiro-Wilk test and Levene’s median test, respectively. To determine the differential effects of water temperature on the growth rates of S. gracilenta with and without prey, a multivariate analysis of variance (one-way MANOVA; Pillai’s trace test) was performed. Moreover, an independent sample t-test was conducted to test significant differences in the growth rates of S. gracilenta with and without prey. Statistical significance was set at p < 0.05. These analyses were performed using SPSS ver. 26.0 (IBM-SPSS Inc., Armonk, NY, USA).

RESULTS

Temperature effects on the growth rates of Shimiella gracilenta without prey

With increasing water temperatures, the growth rate of S. gracilenta SGJH1904 without added prey increased at 5–20°C but decreased at 25–35°C (Fig. 1). The maximum growth rate of S. gracilenta was achieved at 20°C. Furthermore, the growth rates of S. gracilenta without added prey at 5–25°C were zero or positive but negative at 30–35°C. The growth rates of S. gracilenta without prey ranged from −4.67 to 0.21 d−1. The growth rates of S. gracilenta without prey were significantly affected by water temperature (one-way ANOVA, F6, 14 = 3,089.2, p < 0.001) and were divided into four subsets (Tukey’s HSD post-hoc test, p < 0.05) (Fig. 1).

Fig. 1

Specific growth rate of Shimiella gracilenta SGJH1904 with (red square) and without (blue circle) Teleaulax amphioxeia TAGS0202 as a function of water temperature. Significantly different subsets for the growth rate with (red letter with an apostrophe) and without prey (blue letter) were shown based on Tukey’s honestly significant difference post-hoc test after one-way ANOVA. Symbols represent treatment mean values ± standard error.

Temperature effects on the growth rates of Shimiella gracilenta with prey

With increasing water temperatures, the growth rate of S. gracilenta SGJH1904 with the added T. amphioxeia prey increased at 5–25°C but decreased at 30–35°C (Fig. 1). The maximum growth rate of S. gracilenta was achieved at 25°C. Furthermore, the growth rates of S. gracilenta with added T. amphioxeia prey were positive at 5–25°C but negative at 30–35°C. The growth rates of S. gracilenta with T. amphioxeia prey ranged from −4.66 to 0.85 d−1. The growth rates of S. gracilenta with T. amphioxeia prey were significantly affected by water temperature (one-way ANOVA, F6, 14 = 2,233.4, p < 0.001) and were divided into five subsets (Tukey’s HSD post-hoc test, p < 0.05) (Fig. 1).

Differential effects of water temperature between growth rates with and without prey

A MANOVA analysis revealed significant differences in the effects of water temperature on the growth rates of S. gracilenta SGJH1904 with and without prey (MANOVA, Pillai’s Trace = 1.93, F6, 14 = 60.6, p < 0.001) (Fig. 1). The growth rates of S. gracilenta with T. amphioxeia prey at 20°C and 25°C were significantly higher than those without added prey (one-tailed t-test, t4 = 13.3, p < 0.001 at 20°C; t4 = 27.9, p < 0.001 at 25°C).

Temperature effects on the ingestion rates of Shimiella gracilenta

With increasing water temperatures, the ingestion rate of S. gracilenta SGJH1904 on T. amphioxeia increased at 5–25°C (Fig. 2). The ingestion rate of S. gracilenta at 25°C, where its maximum growth rate with prey was observed, was 0.05 ng C predator−1 d−1 (2.9 cells predator−1 d−1). However, the ingestion rate of S. gracilenta at 20°C, where its maximum growth rate without prey was observed, was 0.04 ng C predator−1 d−1 (2.1 cells predator−1 d−1). The ingestion rates of S. gracilenta on T. amphioxeia were significantly affected by water temperature (one-way ANOVA, F4, 10 = 20.5, p < 0.001) and were divided into four subsets (Tukey’s HSD post-hoc test, p < 0.05) (Fig. 2).

Fig. 2

Ingestion rate of Shimiella gracilenta SGJH1904 on Teleaulax amphioxeia TAGS0202 as a function of water temperature. Significantly different subsets for the ingestion rate were shown based on Tukey’s honestly significant difference post-hoc test after one-way ANOVA. Symbols represent treatment mean values ± standard error.

Prediction of the distribution of Shimiella gracilenta

In spring, the average water temperature during 2015–2018 at the 28 stations in Korea was 9.6–15.8°C, and S. gracilenta did not exist at 10 stations: one station in the West Sea, four stations in the South Sea, two stations in the East Sea, and three stations in Jeju Island (Fig. 3A). Under the +2, +4, and +6°C conditions in spring, the distribution of S. gracilenta was predicted not to differ from that during 2015–2018 spring seasons (Fig. 3B–D).

Fig. 3

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in spring under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during the spring seasons of 2015–2018 (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

In summer, the average water temperature during 2015–2018 at the 28 stations in Korea was 19.1–25.7°C, and S. gracilenta did not exist at 10 stations: two stations in the West Sea, four stations in the South Sea, two stations in the East Sea, and two stations in Jeju Island (Fig. 4A). However, under the +2°C condition, S. gracilenta was predicted not to survive at 14 stations: five stations in the West Sea, five stations in the South Sea, two stations in the East Sea, and two stations in Jeju Island (Fig. 4B). Under the +4°C condition, S. gracilenta was predicted not to survive at 20 stations: eight stations in the West Sea, seven stations in the South Sea, two stations in the East Sea, and three stations in Jeju Island (Fig. 4C). Under the +6°C condition, S. gracilenta was predicted not to survive at 24 stations: eight stations in the West Sea, nine stations in the South Sea, two stations in the East Sea, and five stations in Jeju Island (Fig. 4D).

Fig. 4

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in summer under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during 2015–2018 summer seasons (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

In autumn, the average water temperature during 2015–2018 at the 28 stations in Korea was 18.3–22.6°C, and S. gracilenta did not exist at 12 stations: three stations in the West Sea, five stations in the South Sea, two stations in the East Sea, and two stations in Jeju Island (Fig. 5A). Under the +2 and +4°C conditions in autumn, the distribution of S. gracilenta was predicted not to differ from that during 2015–2018 (Fig. 5B & C). However, under the +6°C condition, S. gracilenta was predicted not to survive at 19 stations: three stations in the West Sea, nine stations in the South Sea, two stations in the East Sea, and five stations in Jeju Island (Fig. 5D).

Fig. 5

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in autumn under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during 2015–2018 autumn seasons (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

In winter, the average water temperature during 2015–2018 at the 28 stations in Korea was 4.2–16.2°C, and S. gracilenta did not exist at 15 stations: two stations in the West Sea, five stations in the South Sea, five stations in the East Sea, and three stations in Jeju Island (Fig. 6A). Under the +2, +4, and +6°C conditions in winter, the distribution of S. gracilenta was predicted not to differ from that during 2015–2018 winter seasons (Fig. 6B–D).

Fig. 6

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in winter under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during 2015–2018 winter seasons (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

DISCUSSION

Using the culture of Shimiella gracilenta SGJH1904, the present study revealed that the growth rates were zero or positive at 5–25°C but negative at 30–35°C, regardless of the presence of added prey. Our previous study investigating the distribution of S. gracilenta at 28 stations in Korean coastal waters during the 2015 to 2018 period showed that the lowest water temperature at which S. gracilenta cells were detected was 1.7°C (Ok et al. 2021a). Thus, S. gracilenta may survive at water temperatures considerably lower than 5°C, which is the lowest water temperature tested in the present study. The highest water temperature at which S. gracilenta cells were found in Korean coastal waters during 2015–2018 was 26.4°C (Ok et al. 2021a). Therefore, the results from the field data were generally consistent with the experimental results of the present study.

At 20 and 25°C, the growth rates of S. gracilenta SGJH1904 with prey were 0.73 and 0.85 d−1, respectively, whereas those without prey were 0.21 and 0.05 d−1. Furthermore, the ingestion rates of S. gracilenta on prey at 20 and 25°C were 0.04 and 0.05 ng C predator−1 d−1, respectively. Thus, feeding elevated the growth rates of S. gracilenta to a greater extent at 25°C than at 20°C, and additionally, changed the optimal temperature for supporting the maximum growth rate.

The growth rates of T. amphioxeia, the prey species that supports the highest growth rate of S. gracilenta, were negative at ≥ 30°C (Kang et al. 2020). Therefore, water temperatures of ≥ 30°C may negatively affect the survival of S. gracilenta directly (i.e., physical damage) and indirectly (prey limitation).

The results of the present study showed that the distribution of S. gracilenta may be affected by global warming in summer and autumn months in Korean waters. According to our prediction, in summer, S. gracilenta is expected not to survive at some additional stations in the West and South Sea of Korea when the water temperatures are elevated by 2, 4, and 6°C above those temperatures recorded in 2015–2018, whereas S. gracilenta is expected to survive at most stations in the East Sea of Korea. In summer, warm currents such as the West Korea Coastal Current, the Tsushima Warm Current, and the Jeju Warm Current flow in the West Sea and South Sea of Korea and Jeju Island, while a southward cold current (the North Korea Cold Current) and a northward warm current (the Tsushima Warm Current) flows into the East Sea of Korea (Fig. 7) (Park et al. 2015, 2017). Therefore, the southward cold current can lower the water temperature in the East Sea of Korea in the summer and enable the survival of S. gracilenta here when it cannot survive in the West and South Seas of Korea and Jeju Island during this season.

Fig. 7

Schematic maps of the surface currents in summer (A) and winter (B) in Korean waters, redrawn from Park et al. (2015, 2017).

During 1968–2004 in Korea, the water temperature at the surface increased by 0.975°C and at a depth of 10 m the temperature was elevated by 0.918°C (Jung 2008). This study demonstrated that warming affects the water temperature to a depth of 10 m. The average swimming speed of S. gracilenta has been reported to be 160 μm s−1 (Park et al. 2021). Theoretically, this dinoflagellate can migrate from the surface to a depth of 6 m for 10 h (Jeong et al. 2015). Therefore, the survival of S. gracilenta may be affected by warming sea water during the global warming period, despite its capability to descend to 6-m depths.

Shimiella gracilenta SGJH1904 was isolated from temperate coastal regions, while a sister species, the Ross Sea dinoflagellate W5-1 and RS-24, was isolated from Antarctica (Gast et al. 2006, Ok et al. 2021a, 2021b). The effects of water temperature on the survival of the Ross Sea dinoflagellate has not yet been reported. Thus, determining the effects of water temperature on the survival of the Ross Sea dinoflagellate and comparing this data with that of S. gracilenta SGJH1904 may provide insight into the adaptations and evolution of these two closely related species that live in contrasting habitats.

Numerous studies have been conducted on the effects of temperature and global warming on plankton communities, but fewer studies have examined the effects of temperature and global warming on populations of certain dinoflagellate species (Huertas et al. 2011, Yvon-Durocher et al. 2015, Jonkers et al. 2019, Lee et al. 2019, Benedetti et al. 2021). The abundance of dinoflagellate species can affect prey and predator populations (Smalley and Coats 2002, Kim et al. 2013, Yoo et al. 2013, Lee et al. 2017, Lim et al. 2017, Jang and Jeong 2020). Therefore, it is necessary that key species be assessed to increase the accuracy of models predicting the effects of temperature changes and global warming on the structure and function of marine ecosystems.

ACKNOWLEDGEMENTS

This research was supported by the National Research Foundation funded by the Ministry of Science and ICT (NRF-2020M3F6A1110582;NRF-2021M3I6A1091272; NRF-2021R1A2C1093379) award to HJJ.

Notes

The authors declare that they have no potential conflicts of interest.

SUPPLEMENTARY MATERIALS

Supplementary Fig. S1

Outline of the preincubation and experimental incubation periods of Shimiella gracilenta SGJH1904 (A) and Teleaulax amphioxeia TAGS0202 (B) (https://www.e-algae.org).

algae-2022-37-1-49-suppl.pdf

References

Anderson DM, Rengefors K. 2006;Community assembly and seasonal succession of marine dinoflagellates in a temperate estuary: the importance of life cycle events. Limnol Oceanogr 51:860–873.
Beitinger TL, Fitzpatrick LC. 1979;Physiological and ecological correlates of preferred temperature in fish. Am Zool 19:319–329.
Benedetti F, Vogt M, Elizondo UH, Righetti D, Zimmermann NE, Gruber N. 2021;Major restructuring of marine plankton assemblages under global warming. Nat Commun 12:5226.
Coats DW. 1999;Parasitic life styles of marine dinoflagellates. J Eukaryot Microbiol 46:402–409.
Eom SH, Jeong HJ, Ok JH, Park SA, Kang HC, You JH, Lee SY, Yoo YD, Lim AS, Lee MJ. 2021;Interactions between common heterotrophic protists and the dinoflagellate Tripos furca: implication on the long duration of its red tides in the South Sea of Korea in 2020. Algae 36:25–36.
Freeman LA, Kleypas JA, Miller AJ. 2013;Coral reef habitat response to climate change scenarios. PLoS ONE 8:e82404.
Frölicher TL, Ramseyer L, Raible CC, Rodgers KB, Dunne J. 2020;Potential predictability of marine ecosystem drivers. Biogeosciences 17:2061–2083.
Frost BW. 1972;Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus . Limnol Oceanogr 17:805–815.
Gast RJ, Moran DM, Beaudoin DJ, Blythe JN, Dennett MR, Caron DA. 2006;Abundance of a novel dinoflagellate phylotype in the Ross Sea, Antarctica. J Phycol 42:233–242.
Gillooly JF. 2000;Effect of body size and temperature on generation time in zooplankton. J Plankton Res 22:241–251.
Heinbokel JF. 1978;Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar Biol 47:177–189.
Hiscock K, Southward A, Tittley I, Hawkins S. 2004;Effects of changing temperature on benthic marine life in Britain and Ireland. Aquat Conserv Mar Freshw Ecosyst 14:333–362.
Huertas IE, Rouco M, López-Rodas V, Costas E. 2011;Warming will affect phytoplankton differently: evidence through a mechanistic approach. Proc R Soc B Biol Sci 278:3534–3543.
Intergovernmental Panel on Climate Change 2021 Summary for policymakers. In : Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B, eds. Climate Change 2021: The Physical Science Basis Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press. Cambridge: p. 42.
Jakobsen HH, Hansen PJ, Larsen J. 2000;Growth and grazing responses of two chloroplast-retaining dinoflagellates: effect of irradiance and prey species. Mar Ecol Prog Ser 201:121–128.
Jang SH, Jeong HJ. 2020;Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations. Algae 35:45–59.
Jeong HJ. 1999;The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J Eukaryot Microbiol 46:390–396.
Jeong HJ, Kang HC, Lim AS, Jang SH, Lee K, Lee SY, Ok JH, You JH, Kim JH, Lee KH, Park SA, Eom SH, Yoo YD, Kim KY. 2021;Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci Adv 7:eabe4214..
Jeong HJ, Lee KH, Yoo YD, Kang NS, Song JY, Kim TH, Seong KA, Kim JS, Potvin E. 2018;Effects of light intensity, temperature, and salinity on the growth and ingestion rates of the red-tide mixotrophic dinoflagellate Paragymnodinium shiwhaense . Harmful Algae 80:46–54.
Jeong HJ, Lim AS, Franks PJS, Lee KH, Kim JH, Kang NS, Lee MJ, Jang SH, Lee SY, Yoon EY, Park JY, Yoo YD, Seong KA, Kwon JE, Jang TY. 2015;A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97–115.
Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH. 2010;Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45:65–91.
Jeong HJ, Yoo YD, Lee KH, Kim TH, Seong KA, Kang NS, Lee SY, Kim JS, Kim S, Yih WH. 2013;Red tides in Masan Bay, Korea in 2004–2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30(Suppl 1):S75–S88.
Jeong HJ, Yoo YD, Seong KA, Kim JH, Park JY, Kim S, Lee SH, Ha JH, Yih WH. 2005;Feeding by the mixotrophic red-tide dinoflagellate Gonyaulax polygramma: mechanisms, prey species, effects of prey concentration, and grazing impact. Aquat Microb Ecol 38:249–257.
Jonkers L, Hillebrand H, Kucera M. 2019;Global change drives modern plankton communities away from the pre-industrial state. Nature 570:372–375.
Jueterbock A, Tyberghein L, Verbruggen H, Coyer JA, Olsen JL, Hoarau G. 2013;Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecol Evol 3:1356–1373.
Jung S. 2008;Spatial variability in long-term changes of climate and oceanographic conditions in Korea. J Environ Biol 29:519–529.
Kang HC, Jeong HJ, Lim AS, Ok JH, You JH, Park SA, Lee SY, Eom SH. 2020;Effects of temperature on the growth and ingestion rates of the newly described mixotrophic dinoflagellate Yihiella yeosuensis and its two optimal prey species. Algae 35:263–275.
Kang HC, Jeong HJ, Park SA, Ok JH, You JH, Eom SH, Park EC, Jang SH, Lee SY. 2021;Comparative transcriptome analysis of the phototrophic dinoflagellate Biecheleriopsis adriatica grown under optimal temperature and cold and heat stress. Front Mar Sci 8:761095.
Kibler SR, Tester PA, Kunkel KE, Moore SK, Litaker RW. 2015;Effects of ocean warming on growth and distribution of dinoflagellates associated with ciguatera fish poisoning in the Caribbean. Ecol Model 316:194–210.
Kim B-T, Lee J-S, Seo Y-S. 2016;An analysis on the climate change exposure of fisheries and fish species in the southern sea under the RCP scenarios: focused on sea temperature variation. J Fish Bus Adm 47:31–44.
Kim JS, Jeong HJ, Yoo YD, Kang NS, Kim SK, Song JY, Lee MJ, Kim ST, Kang JH, Seong KA, Yih WH. 2013;Red tides in Masan Bay, Korea, in 2004–2005: III. Daily variations in the abundance of mesozooplankton and their grazing impacts on red-tide organisms. Harmful Algae 30(Suppl 1):S102–S113.
Kudela RM, Gobler CJ. 2012;Harmful dinoflagellate blooms caused by Cochlodinium sp.: global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14:71–86.
Laabir M, Jauzein C, Genovesi B, Masseret E, Grzebyk D, Cecchi P, Vaquer A, Perrin Y, Collos Y. 2011;Influence of temperature, salinity and irradiance on the growth and cell yield of the harmful red tide dinoflagellate Alexandrium catenella colonizing Mediterranean waters. J Plankton Res 33:1550–1563.
Langer MR, Weinmann AE, Lötters S, Bernhard JM, Rödder D. 2013;Climate-driven range extension of Amphistegina (Protista, Foraminiferida): models of current and predicted future ranges. PLoS ONE 8:e54443.
Lee KH, Jeong HJ, Lee K, Franks PJS, Seong KA, Lee SY, Lee MJ, Jang SH, Potvin E, Lim AS, Yoon EY, Yoo YD, Kang NS, Kim KY. 2019;Effects of warming and eutrophication on coastal phytoplankton production. Harmful Algae 81:106–118.
Lee MJ, Jeong HJ, Kim JS, Jang KK, Kang NS, Jang SH, Lee HB, Lee SB, Kim HS, Choi CH. 2017;Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: III. Metazooplankton and their grazing impacts on red-tide organisms and heterotrophic protists. Algae 32:285–308.
Lee SY, Jeong HJ, Ok JH, Kang HC, You JH. 2020;Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters. Algae 35:225–236.
Lim AS, Jeong HJ. 2021;Benthic dinoflagellates in Korean waters. Algae 36:91–109.
Lim AS, Jeong HJ, Ok JH, You JH, Kang HC, Kim SJ. 2019;Effects of light intensity and temperature on growth and ingestion rates of the mixotrophic dinoflagellate Alexandrium pohangense . Mar Biol 166:98.
Lim AS, Jeong HJ, Seong KA, Lee MJ, Kang NS, Jang SH, Lee KH, Park JY, Jang TY, Yoo YD. 2017;Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: II. Heterotrophic protists and their grazing impacts on red-tide organisms. Algae 32:199–222.
Lim MH, Lee CH, Min J, Lee HG, Kim KY. 2020;Effect of elevated pCO2 on thermal performance of Chattonella marina and Chattonella ovata (Raphidophyceae). Algae 35:375–388.
Loeng H. 1989;The influence of temperature on some fish population parameters in the Barents Sea. J Northw Atl Fish Sci 9:103–113.
Montero P, Pérez-Santos I, Daneri G, Gutiérrez MH, Igor G, Seguel R, Purdie D, Crawford DW. 2017;A winter dinoflagellate bloom drives high rates of primary production in a Patagonian fjord ecosystem. Estuar Coast Shelf Sci 199:105–116.
Nielsen MV. 1996;Growth and chemical composition of the toxic dinoflagellate Gymnodinium galatheanum in relation to irradiance, temperature and salinity. Mar Ecol Prog Ser 136:205–211.
Ok JH, Jeong HJ, Kang HC, Park SA, Eom SH, You JH, Lee SY. 2021a;Ecophysiology of the kleptoplastidic dinoflagellate Shimiella gracilenta: I. spatiotemporal distribution in Korean coastal waters and growth and ingestion rates. Algae 36:263–283.
Ok JH, Jeong HJ, Lee SY, Park SA, Noh JH. 2021b; Shimiella gen. nov. and Shimiella gracilenta sp. nov. (Dinophyceae, Kareniaceae), a kleptoplastidic dinoflagellate from Korean waters and its survival under starvation. J Phycol 57:70–91.
Ok JH, Jeong HJ, Lim AS, Lee KH. 2017;Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists. Harmful Algae 68:178–191.
Ok JH, Jeong HJ, Lim AS, Lee SY, Kim SJ. 2018;Feeding by the heterotrophic nanoflagellate Katablepharis remigera on algal prey and its nationwide distribution in Korea. Harmful Algae 74:30–45.
Ok JH, Jeong HJ, Lim AS, You JH, Kang HC, Kim SJ, Lee SY. 2019;Effects of light and temperature on the growth of Takayama helix (Dinophyceae): mixotrophy as a survival strategy against photoinhibition. J Phycol 55:1181–1195.
Ok JH, Jeong HJ, You JH, Kang HC, Park SA, Lim AS, Lee SY, Eom SH. 2021c;Phytoplankton bloom dynamics in incubated natural seawater: predicting bloom magnitude and timing. Front Mar Sci 8:681252.
Oliver TA, Palumbi SR. 2011;Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440.
Park K-A, Lee E-Y, Chang E, Hong S. 2015;Spatial and temporal variability of sea surface temperature and warming trends in the Yellow Sea. J Mar Sys 143:24–38.
Park K-A, Park J-E, Choi B-J, Lee SH, Shin HR, Lee SR, Byun D-S, Kang B, Lee E. 2017;Schematic maps of ocean currents in the Yellow Sea and the East China Sea for science textbooks based on scientific knowledge from oceanic measurements. The Sea 22:151–171.
Park SA, Jeong HJ, Ok JH, Kang HC, You JH, Eom SH, Park EC. 2021;Interactions between the kleptoplastidic dinoflagellate Shimiella gracilenta and several common heterotrophic protists. Front Mar Sci 8:738547.
Perry AL, Low PJ, Ellis JR, Reynolds JD. 2005;Climate change and distribution shifts in marine fishes. Science 308:1912–1915.
Poloczanska ES, Burrows MT, Brown CJ, García Molinos J, Halpern BS, Hoegh-Guldberg O, Kappel CV, Moore PJ, Richardson AJ, Schoeman DS, Sydeman WJ. 2016;Responses of marine organisms to climate change across oceans. Front Mar Sci 3:62.
Skovgaard A. 1998;Role of chloroplast retention in a marine dinoflagellate. Aquat Microb Ecol 15:293–301.
Smalley GW, Coats DW. 2002;Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. J Eukaryot Microbiol 49:63–73.
Smayda TJ, Reynolds CS. 2003;Strategies of marine dinoflagellate survival and some rules of assembly. J Sea Res 49:95–106.
Stat M, Morris E, Gates RD. 2008;Functional diversity in coral–dinoflagellate symbiosis. Proc Natl Acad Sci U S A 105:9256–9261.
Suh M-S, Oh S-G, Lee Y-S, Ahn J-B, Cha D-H, Lee D-K, Hong S-Y, Min S-K, Park S-C, Kang H-S. 2016;Projections of high resolution climate changes for South Korea using multiple-regional climate models based on four RCP scenarios. Part 1: surface air temperature. Asia-Pac. J Atmos Sci 52:151–169.
Taylor FJR, Hoppenrath M, Saldarriaga JF. 2008;Dinoflagellate diversity and distribution. Biodivers Conserv 17:407–418.
Thomas MK, Kremer CT, Klausmeier CA, Litchman E. 2012;A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085–1088.
Thompson PA, Guo M-X, Harrison PJ. 1992;Effects of variation in temperature. I. On the biochemical composition of eight species of marine phytoplankton. J Phycol 28:481–488.
Torres G, Carnicer O, Canepa A, De La Fuente P, Recalde S, Narea R, Pinto E, Borbor-Córdova MJ. 2019;Spatio-temporal pattern of dinoflagellates along the tropical eastern Pacific coast (Ecuador). Front Mar Sci 6:145.
Tunin-Ley A, Ibañez F, Labat J-P, Zingone A, Lemée R. 2009;Phytoplankton biodiversity and NW Mediterranean Sea warming: changes in the dinoflagellate genus Ceratium in the 20th century. Mar Ecol Prog Ser 375:85–99.
Witt MJ, Hawkes LA, Godfrey MH, Godley BJ, Broderick AC. 2010;Predicting the impacts of climate change on a globally distributed species: the case of the loggerhead turtle. J Exp Biol 213:901–911.
Yoo YD, Jeong HJ, Kim JS, Kim TH, Kim JH, Seong KA, Lee SH, Kang NS, Park JW, Park J, Yoon EY, Yih WH. 2013;Red tides in Masan Bay, Korea in 2004–2005: II. Daily variations in the abundance of heterotrophic protists and their grazing impact on red-tide organisms. Harmful Algae 30(Suppl 1):S89–S101.
You JH, Jeong HJ, Kang HC, Ok JH, Park SA, Lim AS. 2020a;Feeding by common heterotrophic protist predators on seven Prorocentrum species. Algae 35:61–78.
You JH, Jeong HJ, Lim AS, Ok JH, Kang HC. 2020b;Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae . Mar Biol 167:64.
Yvon-Durocher G, Allen AP, Cellamare M, Dossena M, Gaston KJ, Leitao M, Montoya JM, Reuman DC, Woodward G, Trimmer M. 2015;Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biol 13:e1002324.

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Fig. 1

Specific growth rate of Shimiella gracilenta SGJH1904 with (red square) and without (blue circle) Teleaulax amphioxeia TAGS0202 as a function of water temperature. Significantly different subsets for the growth rate with (red letter with an apostrophe) and without prey (blue letter) were shown based on Tukey’s honestly significant difference post-hoc test after one-way ANOVA. Symbols represent treatment mean values ± standard error.

Fig. 2

Ingestion rate of Shimiella gracilenta SGJH1904 on Teleaulax amphioxeia TAGS0202 as a function of water temperature. Significantly different subsets for the ingestion rate were shown based on Tukey’s honestly significant difference post-hoc test after one-way ANOVA. Symbols represent treatment mean values ± standard error.

Fig. 3

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in spring under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during the spring seasons of 2015–2018 (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

Fig. 4

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in summer under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during 2015–2018 summer seasons (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

Fig. 5

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in autumn under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during 2015–2018 autumn seasons (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

Fig. 6

Map showing the results of a prediction of the nationwide distribution of Shimiella gracilenta in Korean coastal waters in winter under elevated water temperature conditions. The results were determined using the data on the distribution of S. gracilenta during 2015–2018 (Ok et al. 2021a). (A) Presence (red circles) or absence (white circles) of S. gracilenta at the average water temperature during 2015–2018 winter seasons (+0°C). (B–D) Prediction of presence or absence of S. gracilenta at the average water temperature plus 2°C (+2°C) (B), 4°C (+4°C) (C), and 6°C (+6°C) (D). Numbers in the box indicate the number of stations where S. gracilenta was (or was predicted to be) present or absent. The West Sea of Korea: Ansan (AS), Dangjin (DAJ), Mageompo (MGP), Taean (TA), Seocheon (SCN), Kunsan (KS), Buan (BA), and Mokpo (MP). The South Sea of Korea: Jangheung (JAH), Goheung (GH), Yeosu (YS), Kwangyang (KY), Tongyoung (TY), Masan (MS), Jinhae (JH), Dadaepo (DDP), and Busan (BS). The East Sea of Korea: Ulsan (US), Pohang (PH), Uljin (UJ), Donghae (DH), Jumunjin (JMJ), and Sokcho (SC). Jeju Island: Aewol (AW), Seogwipo (SGP), Wimi (WM), Seongsan (SS), and Gimnyeong (GN).

Fig. 7

Schematic maps of the surface currents in summer (A) and winter (B) in Korean waters, redrawn from Park et al. (2015, 2017).

Table 1

Actual initial abundance (cells mL−1) of the predator Shimiella gracilenta SGJH1904 and prey Teleaulax amphioxeia TAGS0202

Temperature (°C) Species Actual initial abundance
5, 10, 15, 20, 25, 30, 35 Teleaulax amphioxeia/Shimiella gracilenta in predator-prey mixture 17,684/1,535, 22,281/1,550, 20,800/1,621, 18,055/1,714, 19,626/1,438, 19,018/1,293, 19,163/1,108
5, 10, 15, 20, 25, 30, 35 Teleaulax amphioxeia in prey-only control 16,761, 19,514, 18,903, 18,584, 18,729, 19,065, 17,153
5, 10, 15, 20, 25, 30, 35 Shimiella gracilenta in predator-only control 1,586, 1,633, 1,619, 1,385, 1,298, 1,375, 1,133