The present study clearly shows that the growth rates of P. donghaiense, T. furca, and A. fraterculus added to the water from 20 m depth were similar to those from that of 40 m but significantly higher than those of 0 m, while the growth rates of M. polykrikoides added to the water from the depths of 0, 20, and 40 m were similar. The ability of P. donghaiense, T. furca, and A. fraterculus to reach deep cold eutrophic waters is, therefore, a critical factor affecting rapid growth and, in turn, the formation of red tide. Whether these four dinoflagellates can reach deep cold eutrophic waters is determined by a combination of vertical migration depth and the position of deep cold waters. The calculated migration depths of P. donghaiense, T. furca, A. fraterculus, and M. polykrikoides after 10 h of travel were reported to be 10, 15, 24, and 52 m, respectively (Jeong et al. 2017). This implies that P. donghaiense and T. furca may reach deep cold waters and grow rapidly when the top of the deep cold eutrophic waters (or thermocline) is located approximately < 10 and 15 m, and A. fraterculus and M. polykrikoides, when they are located approximately < 20 and 30 m.
Scenarios were further established for predicting the causative species of red tides in the South Sea of Korea using data on the growth rates of each species in seawater from different depths, the positions of deep cold waters (including intrusion and retreat), and vertical migration depth of each red-tide species (Fig. 8). The NO3 concentration in the surface water was 1.6 µM in the study area, but the addition of cultures elevated the NO3 concentration to approximately 4–5 µM. The growth rate of P. donghaiense at 1.6 µM NO3 was 0.05 d− 1, and those of A. fraterculus and M. polykrikoides, obtained by interpolation, were 0.10 and 0.19 d− 1, respectively (Gobler et al. 2012; Lee et al. 2019a). Furthermore, the growth rate of T. furca at the same NO3 concentration was 0.04 d− 1. As the highest growth rate of T. furca in the present study was almost zero when T. furca was incubated in seawater collected at 0 m, this was used as its growth rate in seawater with 1.6 µM NO3.
Considering the vertically migrating depths and the NO3 concentration at each depth, the growth rates of M. polykrikoides (0.25 d− 1) were revealed to be the highest, followed by A. fraterculus (0.21 d− 1), P. donghaiense (0.05 d− 1), and T. furca (0.04 d− 1) in our scenarios (Fig. 8c). However, as presented in Fig. 8b, if the deep cold waters intruded toward coastal zones and the nitracline ascended by 10 m, the growth rates of P. donghaiense and A. fraterculus increased to 0.16 and 0.42 d− 1, respectively, whereas there was no significant change in those of the other species. Furthermore, if the deep cold waters intruded and the nitracline ascended by 30 m or if upwelling occurred, the growth rates of P. donghaiense (0.30 d− 1) and T. furca (0.37 d− 1) were largely elevated, whereas those of A. fraterculus (0.45 d− 1) and M. polykrikoides (0.25 d− 1) did not change significantly (Fig. 8a). The intrusion of deep cold water of 10–30 m can thus be advantageous for P. donghaiense, T. furca, and A. fraterculus over M. polykrikoides. In contrast, as presented in Fig. 8d–e, the growth rate of A. fraterculus (0.10 d− 1) decreased when deep cold waters retreated and the nitracline descended by 10–30 m, however, the growth rate of other species did not change. The growth rate of M. polykrikoides was the highest under these conditions. Thus, the retreat of deep cold water and deepening nitracline may provide a competitive advantage to M. polykrikoides over other species.
The vertical PO4 concentration profile in the study area (on July 31, 2020) had a pattern similar to that of the NO3 concentration (Fig. 8). Similarly, considering the vertically migrating depths and the PO4 concentration at each depth, the growth rates of A. fraterculus (0.42 d− 1) were revealed to be the highest, followed by those of M. polykrikodes (0.25 d− 1), P. donghaiense (0.16 d− 1), and T. furca (0.04 d− 1) (Fig. 8h). However, when the deep cold waters intruded toward coastal zones and the phosphocline ascended by 10 m (Fig. 8g), the growth rates of P. donghaiense and T. furca increased to 0.30 and 0.37 d− 1, respectively, whereas there was no significant change in the growth rates of the other species. Moreover, if the deep cold waters intruded and the phosphocline ascended by 30 m or upwelling occurred (Fig. 8f), no significant change occurred in the growth rates of the four species. The intrusion of deep cold water (by 10–30 m) may favor P. donghaiense, T. furca, and A. fraterculus over M. polykrikoides. In contrast, when deep cold waters retreated and the phosphocline descended by 10–30 m, the growth rate of A. fraterculus (0.21 d− 1) decreased, but that of the other species did not change. Under these conditions, the growth rate of M. polykrikoides was the highest, followed by that of A. fraterculus, and thus, the growth of M. polykrikoides and A. fraterculus could be favored (Fig. 8i–j). Either NO3 or PO4 concentration at the same depth could have lowered the growth rate of each red-tide species because of the lack of one nutrient. Therefore, in the scenario based on the combination of NO3 and PO4 concentrations, the lower of the two growth rates of each red-tide species at the same depth was chosen (Fig. 9). Considering the vertically migrating depths and the NO3 and PO4 concentrations at each depth, the growth rates of M. polykrikoides (0.25 d− 1) were revealed to be the highest, followed by those of A. fraterculus (0.21 d− 1), P. donghaiense (0.05 d− 1), and T. furca (0.04 d− 1) (Fig. 9c). However, when the deep cold waters intruded toward coastal zones and the nitracline and phosphocline ascended by 10 m, the growth rates of P. donghaiense and A. fraterculus increased to 0.16 and 0.42 d− 1, respectively, whereas there was no change in those of the other species (Fig. 9b). Moreover, when the deep cold waters intruded and the nitracline and phosphocline ascended by 30 m or if upwelling occurred, the growth rates of P. donghaiense (0.30 d− 1) and T. furca (0.35 d− 1) increased considerably, whereas those of A. fraterculus (0.45 d− 1) and M. polykrikoides (0.21 d− 1) did not change substantially (Fig. 9a). The intrusion of deep cold water (by 10–30 m) was thus advantageous for P. donghaiense, T. furca, and A. fraterculus compared with M. polykrikoides. In contrast, the growth rate of A. fraterculus (0.10 d− 1) decreased when deep cold waters retreated and the nitracline and phosphocline descended by 10–30 m, however, the growth rates of the other species did not change (Fig. 9d–e). The growth rate of M. polykrikoides was the highest under these conditions. Therefore, the retreat of deep cold water and deepening nitracline and phosphocline may provide a competitive advantage to M. polykrikoides over other species, similar to the results in the scenario based on NO3 concentration.
Some red-tide dinoflagellate species prefer NH4, and some harmful algal blooms caused by dinoflagellates are associated with an increased NH4 proportion (Berg et al. 2003; Kudela et al. 2008). However, the vertical profile of the NH4 concentrations in the study area on July 31, 2020, showed that the NH4 concentrations at different depths did not widely vary and were considerably lower than the NO3 concentrations at deep depths. Thus, the present study did not consider scenarios based on the NH4 concentration. Instead, the results of the scenarios based on the combination of total dissolved inorganic nitrogen (DIN) and PO4 were similar to those based on the combination of NO3 and PO4 concentrations (Figs. S2–S3).
The predicted scenarios for the red-tide causative species of the present study were tested by comparing the results with that of the causative species in the serial red-tide events in 2014 (Jeong et al. 2017). The previous field observations conducted in the South Sea of Korea in 2014 showed that deep cold waters intruded (July 22, August 06, and September 15) and retreated (August 21 and September 01) (Fig. 10a–b). The gradients of water temperature in the South Sea of Korea had patterns similar to those of the NO3 concentrations (Fig. 10b); the NO3 concentrations at shallow depths increased as the deep cold waters intruded but decreased as the deep cold waters retreated. This indicated that the deep cold waters contained high concentrations of NO3.
The depth of the top of deep cold waters is primarily affected by the thermocline, which is usually affected by solar insolation (Fig. 11). It was found to be shallower from July to early August (i.e., 5–15 m) but deeper in September (20–32 m). Due to the solar insolation, the intrusion and retreat of deep cold waters pushed up or pulled down the position of the deep cold waters. P. donghaiense caused red tides on July 1 when the depth of the top of thermocline (or deep cold waters) was 8 m, T. furca from July 11 to August 21 at 5–17 m, A. fraterculus on August 21 at 17 m, and M. polykrikoides from August 21 to September 28 at 17–32 m (Figs. 11, 12). These red-tide outbreaks by each species in 2014 corresponded to our scenarios showing the combination of the relative growth rates of the four dinoflagellate species at each depth, vertical migration depth, and the position of deep cold waters.
The ichthyotoxic M. polykrikoides have formed red tides in the waters of many countries, causing large-scale mortality of fish (Granéli and Turner 2006, Anton et al. 2008, Richlen et al. 2010, Park et al. 2013, Anderson et al. 2021, Sakamoto et al. 2021). Red tides caused by M. polykrikoides cause great losses to the aquaculture industry in Korea every year (Park et al. 2013). Thus, understanding and predicting red tide outbreaks caused by M. polykrikoides is a critical concern to scientists, government officials, aquafarmers, and the public. The results of the present study revealed that the growth rate of M. polykrikoides (0.21–0.25 d− 1) was lower than those of P. donghaiense, T. furca, and A. fraterculus (0.30–0.45 d− 1) when the NO3 concentration was 10–20 µM, but higher when the NO3 concentration was < 5 µM.
P. donghaiense, T. furca, and M. polykrikoides are mixotrophic, whereas A. fraterculus is not (Bockstahler and Coats 1993; Jeong et al. 2004, 2005; Lee et al. 2016). Thus, the effect of mixotrophic ability on the growth rates of P. donghaiense, T. furca, and M. polykrikoides in the study area should be considered. In the study area on July 31, 2020, the total phytoplankton carbon biomass at the depths of 0, 20, and 40 m was 1.3, 7.4, and 2.7 ng C mL− 1, respectively (Table 2). When all phytoplankton was assumed to be cryptophyte prey, the mixotrophic growth rates of P. donghaiense and M. polykrikoides at depths of 0, 20, and 40 m were calculated to be 0.37–0.39 d− 1 and 0.16–0.20 d− 1, respectively, by interpolation using the Michaelis-Menten curves provided in the literature (Jeong et al. 2004, 2005). The calculated mixotrophic growth rates of P. donghaiense and M. polykrikoides on July 31, 2020, were higher by 1–5 and 5–21%, respectively, than the autotrophic growth rates of these two species (0.37 and 0.15 d− 1, respectively) (Table 2). The mixotrophy of P. donghaiense and M. polykrikoides may not have significantly affected their growth rates due to low prey abundance in the study area on July 31, 2020. Unfortunately, the mixotrophic growth rate of T. furca could not be calculated because there is no available data on the mixotrophic growth rate of T. furca as a function of the prey concentration.
Table 2
Calculated mixotrophic growth rates (MixoGR) of Prorocentrum donghaiense and Margalefidinium polykrikoides on total phytoplankton (ng C mL− 1) at Station 111 located off Yeosu in the South Sea of Korea on July 31, 2020. The growth rate in parenthesis is the autotrophic growth rates of P. donghaiense and M. polykrikoides (i.e., without prey) calculated from the equations in Jeong et al. (2005) and Jeong et al. (2004), respectively.
|
|
Prorocentrum donghaiense
|
Margalefidinium polykrikoides
|
Depth
(m)
|
Total phytoplankton
(ng C mL− 1)
|
MixoGR on phytoplankton (d− 1)
|
Elevated GR due to mixotrophy (%)
|
MixoGR on phytoplankton (d− 1)
|
Elevated GR due to mixotrophy (%)
|
0
|
1.3
|
0.37 (0.37)
|
1
|
0.16 (0.15)
|
5
|
20
|
7.4
|
0.39 (0.37)
|
5
|
0.20 (0.15)
|
21
|
40
|
2.7
|
0.38 (0.37)
|
2
|
0.17 (0.15)
|
10
|
The MixoGR was calculated using the equations of the growth rates as a function of cryptophyte prey concentration with the assumption that all phytoplankton at the sampling station were cryptophytes (Jeong et al. 2004, 2005). |
The vertical profile of water temperature in the study area showed that the water temperatures ranged from 16.4°C at 50 m to 24.1°C in the surface water. Therefore, P. donghaiense, T. furca, A. fraterculus, and M. polykrikoides could have experienced different water temperatures during vertical migration. The growth rates of P. donghaiense, T. furca, and M. polykrikoides at 40 m at 16.7°C can be calculated as 0.32, 0.21, and 0.18 d− 1, respectively, which differed from those obtained in our study by 2%, 41%, and 14%, respectively (Nordi 1957; Kim et al. 2004; Xu et al. 2010). Therefore, the growth rates of P. donghaiense and M. polykrikoides found in previous studies were not notably different at 40 m from those obtained in the present study. The growth rate of T. furca may be lowered if this species reaches a 40 m depth; however, T. furca may not reach a 40 m depth in the calculation of its vertical migration depth, as described above.
The NO3 concentrations in the surface waters at nearshore stations located 30 km away from the mouth of the Seomjin River during the dry season are usually 1–3 µM, but those after heavy rains reach 40 µM (Ok et al. 2021). The depths at the stations are 6–7 m (Kim et al. 2006). Therefore, the water volume is relatively small and does not contain a large amount of nutrients. The period during which high nutrients due to freshwater input are provided is episodic and relatively short. Under these circumstances, nutrients are usually limited, and red-tide species compete severely for nutrient uptake and growth (Table 3). Fast-growing diatoms form red tides but decline quickly. The NO3 concentrations in the surface waters at offshore stations located 70 km away from the mouth of the Seomjin River during the dry season are usually 1–5 µM, whereas those in deep cold waters are 10–20 µM (Jeong et al. 2017). The depth at the stations is approximately 50 m. The water volume is thus relatively large and contains a large amount of nutrients. Under these circumstances, nutrients may not be limited, and red-tide species may not compete for nutrients (Table 3). However, the vertical migration ability of dinoflagellates during the period (or cycle) of intrusion and retreat of deep cold water is the most important factor affecting red-tide formation and probably an adaptive strategy.
Table 3
Comparisons of two major nutrient sources at seas: deep cold water versus freshwater.
|
Deep cold water
|
Freshwater
|
Chemical characteristics
|
High saline,
nutrient-rich
|
Usually low saline,
nutrient-rich
|
Water volume and nutrient limitation
|
Vast and almost unlimited
|
Relatively small and limited
|
Important factor affecting dominance
|
Vertical migration depth
|
Half-saturation constant for growth or nutrient uptake
|
Competition
|
Less direct competition than in freshwater
|
Direct competition
|
Advantageous organisms
|
Vertically migrating flagellates or dinoflagellates
|
Fast-growing diatoms
|
In conclusion, the present study showed that red-tide causative species can be predicted using data on their growth rates at different depths, their vertical migration depths, and the position of deep cold waters. This study provides actual data on the growth rates of the major red-tide species at different depths in the South Sea of Korea and insights into the adaptive strategies of the species concerning the position of deep cold waters. Considering the intrusion and retreat of deep cold waters in several countries affected by dinoflagellate red tides (Cullen et al. 1982; Probyn et al. 2010; Jeong et al. 2017; McGowan et al. 2017; Condie et al. 2019), the results of the present study can be used to predict the outbreak of dinoflagellate red tides offshore in the waters of these countries. Deep cold waters are known to intrude and retreat at 15-day intervals and are affected by tidal periods (Kaneda et al. 2002). Thermoclines are generally affected by the surface water temperature, which, in turn, is affected by solar insolation (Kraus and Turner 1967; Denman 1973). The intrusion and retreat of deep cold waters and the shallowing and deepening of thermoclines (and nitraclines and phosphoclines) can therefore be predicted. In turn, the causative species of dinoflagellate red tides can also be predicted.