Coastal waters, which lie at the transition zones between oceans and continents, are the most relevant to human society. They also support rich fishing grounds and provide economic benefits due to their relatively higher productivity (Herrera-Silveira and Morales-Ojeda, 2009; Lange et al., 2010). Coastal areas support relatively greater plankton production and degradation and also play a key role in biogeochemical processes. However, their biodiversity and ecological function are threatened by global changes and anthropogenic pressures which cause the degradation of biotopes and biocenosis (Kemp and Boynton, 2012; Zhang, et al., 2021). Increased anthropogenic activities have accelerated the process of eutrophication, leading to dystrophic crises and/or irreversible deterioration—for example, a decrease in the mean size of dominant copepods from the late 1940s to 2012 was detected in the Central Basin of Long Island Sound, Japan (Rice et al., 2015).

Daya Bay is a semi-enclosed, shallow embayment with depths ranging from 5 to 20 m and an area of 650 km², which is located in the northern part of the South China Sea (Song et al., 2004). It contains complex habitats, tremendous biological resources, abundant biodiversity, and plentiful marine products, which make it one of the most important treasure houses for sub-tropical aquatic resources. In recent years, rapid social and economic developments have resulted in environmental degradation in Daya Bay. Studies have shown that degradation and habitat modification have significantly increased (Wu et al., 2009; Liu et al., 2018), while eutrophication has reduced the zooplankton species richness by about 50% (Li et al., 2014). Dominant species in the spring have changed because of the rapid increase in water temperature and abundant food supply in Daya Bay (Xiang et al., 2021; Zhao et al., 2022), and Li et al. (2021) reported that the zooplankton community was undergoing great changes, showing tendencies of miniaturization and gelatinization over the past 30 years. Several large-scale zooplankton blooms have occurred in Daya Bay, which were related to changes in water temperature, salinity, and food supply variation (Zeng et al., 2019; An et al., 2021; Zeng et al., 2021; Liu et al., 2022).

Zooplankton are sensitive to chemical, physical, and biological factors in marine systems (Sun et al., 2010; Shi et al., 2015). The composition and abundance of zooplankton are highly dependent on environmental conditions and respond quickly to environmental variations. Consequently, zooplankton are considered as bio-indicators of environmental quality and water mass (Dam, 2013; Carter et al., 2017; Wang et al., 2020; Wang et al., 2022). Zooplankton are not only a key link in energy transfer from primary production to higher trophic levels but also a key factor in controlling the harmful effects of eutrophication and proliferation of microalgae (Rissik et al., 2009)—for example, dinoflagellates and prasinophytes are the most preferred phytoplankton groups by the mesozooplankton in Daya Bay (Li et al., 2018).

Daya Bay Nuclear Power Station and Ling-Ao Nuclear Power Station were built in 1994 and 2002, respectively. They are located in the inner regions of west Daya Bay. The thermal discharge is affected by tidal currents, which depend on the topography of Daya Bay (Yuan et al., 2021). The residual current is relatively small within the bay in summer but is stronger with the stronger current fields in winter, and the self-purification capacity of this area is weak (Wu et al., 2007). In addition, other studies have demonstrated that the thermal discharge has a significant impact on the Daya Bay ecosystem, including levels of nutrients, and zooplankton and phytoplankton (Jiang and Wang, 2020). Therefore, it is vital to monitor the zooplankton composition and variation in Daya Bay.

The aims of this research were to (1) investigate whether there is significant variation in the zooplankton composition in the research area, (2) identify the indicator composition under different environmental conditions, (3) measure the correlation of indicator species with the environmental parameters in the research area, and (4) discuss whether the indicator species caused a potential threat to the safety of the nuclear power plant cooling systems in the research area.

Daya Bay, which is located in a subtropical zone, is a semi-closed bay. Due to the influence of the monsoon, there is plenty of rainfall from May to October and less from November to April (Wu and Wang, 2007). In the dry season (winter), the northeast monsoon prevails, with low temperatures and precipitation. In contrast, in the wet season (summer), the southwest monsoon predominates, with relatively high levels of precipitation and temperature. Spring and autumn are the monsoon transition seasons in the research area (Xu, 1989; Wu et al., 2009; Wu et al., 2010, Wu et al., 2011, Wu et al., 2012; Wu et al., 2016). The highest surface water temperature was observed during summer in this study. Owing to the precipitation and runoff, the surface water was diluted, resulting in relatively low salinity, pH, DO, and Chl-a concentration in summer. The correlation analysis showed that there was a significantly positive correlation between salinity, DO, and pH. Nevertheless, a significantly negative correlation was observed between DO and Chl-a in summer (Supplementary), which was consistent with the results reported for the northern region of the South China Sea during autumn (Long et al., 2006). Shen et al. (2017) reported that a significantly negative correlation was also observed between salinity and Chl-a in Daya Bay. In contrast, we found a notably positive correlation between Chl-a and salinity in autumn and a negative correlation in spring. However, no obvious correlation was detected between Chl-a and salinity in summer or winter in this study. During the dry and monsoon transition seasons, the values of surface water salinity, pH, and DO remained fairly constant without the effects of rainfall dilution in the research area.

Zooplankton species composition and abundance are known to change seasonally in the marine environment (Sammacro and Crenshaw, 1984). Zooplankton diversity and abundance are also greatly affected by environmental parameters (Wang et al., 2018; Aguilera, 2020; Wang et al., 2020; Wang et al., 2022). In this study, there was a significantly negative correlation between the total zooplankton abundance and Chl-a concentration. This finding was in accordance with the result of Jiang and Wang (2020). They found that the seasonal change of zooplankton had its own characteristic pattern, which did not coincide with the phytoplankton but lagged behind by nearly 1 month (Jiang and Wang, 2020). Similarly, in our research, there was a significant seasonal variation in zooplankton composition, and the highest species number was observed in winter. Interestingly, many warm temperature species appeared in winter. This warm temperature species intrusion could be carried by the China Coastal Current—for instance, Salpa fusiformis has been defined as a warm temperature indicator species in California and displays a massive occurrence in the Southern Yellow Sea during summer (Silver, 1975; Liu et al., 2012). Calanus sinicus is the indicator species of the China Coastal Current in the Taiwan Strait and was collected only during winter in the research area (Hwang and Wong, 2005; Wang et al., 2020). In addition, the zooplankton abundance was highest in spring. Dolioletta gegenbauri is a warm-water species which was the most dominant species in spring. It commonly appears in productive subtropical neritic regions worldwide. The abundance of D. gegenbauri is usually at bloom concentrations, which could consume a large fraction of daily primary production (Paffenhöfer and Köster, 2011; Walters et al., 2019).

Temora turbinata is regarded as the predominant species in mesozooplankton communities in various environments around the world. It is able to adapt to various habitats, such as eutrophic lagoons, polluted and eutrophicated waters, outfall areas, and nuclear power plant discharge areas (Hsu et al., 2008; Tseng et al., 2011; Wang et al., 2021). In particular, T. turbinate and Karenia brevis can co-occur in the Gulf of Mexico. Karenia brevis is a toxic dinoflagellate, which often causes blooms (Lester et al., 2008). Copepodites and adults of T. turbinata are often found in upwelled water masses which are usually preferred by D. gegenbauri (Paffenhöfer and Köster, 2011). Li et al. (2018) reported that T. turbinanta ranges in abundance from 1 individual/m³ to 1,185 individuals/m³ in Daya Bay, and the highest abundance was recorded during a winter survey in 2017. Consistent with previous results, T. turbinata was the only dominant species present throughout the year. Temora turbinanta was recorded during our 1-year survey, and the average abundance ranged from 3.60 individuals/m³ (autumn) to 90.84 individuals/m³ (winter) in this study. T. turbinanta abundance changed significantly with season, but it was the dominant species throughout the year. Thus, we suggest that T. turbinanta could be considered as a potential indicator species to monitor its aquatic habitat. Notably, T. turbinanta abundance was obviously lower in the research area than in the northeast coastal area of Taiwan (Tseng et al., 2011; Wang et al., 2021). The seasonal variation characteristics of T. turbinanta abundance were also different. Undoubtedly, these differences could be due to differences in sampling method, local conditions, or the thermal discharge from the nuclear power plant in Daya Bay. Additionally, the other indicator species, P. avirostris, is not only a quality live food supply for marine pelagic fish but also an important component of the zooplankton community of many tropical, subtropical, and temperate waters and occurs seasonally with especially high abundance in summertime (Calbet et al., 2001; Fernández de Puelles et al., 2003; Marazzo and Valentin, 2003; Rose et al., 2004). The body length of female P. avirostris ranges from 0.70 to 1.09 mm (Zhou et al., 2022). Thus, P. avirostris blooms could block the cooling system of a nuclear power plant by attracting huge numbers of larva and adult pelagic fish (such as herring, mackerel, sardine, horse mackerel, etc.). Centropages tenuiremis is an important common copepod in the neritic mesozooplankton assemblage. It is an obviously omnivorous feeding species and can expand its food spectrum under stressful conditions (Xu et al., 2020). Dolioletta gegenbauri and D. denticulatum have been reported to form dense blooms in shallow waters of the continental shelf (Paffenhöfer et al., 1995; Nakamura, 1998; Tew and Lo, 2005). Our results are consistent with previous reports (Lian et al., 2011; Li et al., 2011; Li et al., 2021). These species mentioned above have also become the dominant species in Daya Bay. Additionally, our research revealed that P. avirostris blooms and C. tenuiremis blooms might also threaten the cooling system by acting as the food supply for pelagic fish in spring. It is noteworthy that most of the above-mentioned indicator species in spring belong to kollaplankton. Thus, we suggest that kollaplankton could cause potential disaster to the nuclear power plant cooling system due to their relatively large body size and potential to form huge blooms in spring. Moreover, C. tenuiremis blooms in spring and P. avirostris blooms in summer could also threaten the cooling system security by attracting larva or adult pelagic fish assemblages into Daya Bay. Therefore, these species should be considered as key species in future ecological studies.

In summary, the zooplankton communities showed a significant seasonal variation in terms of species composition, abundance, and dominant species in Daya Bay. Seasonal variations in the dominant species were observably related to environmental variations, such as thermal discharge, pH, salinity, and Chl-a. Thus, zooplankton could be considered as a favorable indicator of the marine environment. In addition, some kollaplankton, cladocera, and copepod species might directly or indirectly affect nuclear power plant cooling systems.

The original contributions presented in the study are included in the article/ Supplementary Material . Further inquiries can be directed to the corresponding authors.

F-XW: conceptualization, data curation, writing—original draft, and writing—review and editing. H-HH: Writing—review and editing and funding acquisition. Y-GW: Writing—review and editing, validation, and visualization. Y-GG: investigation and supervision. Q-XL, S-FZ, Y-YR, H-XL, and MD: investigation and formal analysis. All authors contributed to the article and approved the submitted version.