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Effects of meteorological factors on the temporal distribution of red tides in Tolo Harbour, Hong Kong
Marine Pollution Bulletin 126 (2018) 419–427
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Effects of meteorological factors on the temporal distribution of red tides in Tolo Harbour, Hong Kong Jiansheng Huanga,b,c, Hao Liua,b,1, Kedong Yina,b,
T
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a
School of Marine Sciences, Sun Yat-sen University, Zhuhai, 519082, China Key Laboratory of Marine Resources and Coastal Engineering in Guangdong Province, Guangzhou, 510006, China c Dongguan Marine and Fishery Environmental Monitoring Station, Dongguan, 523002, China b
A R T I C L E I N F O
A B S T R A C T
Keywords: Red tides Harmful algal blooms Meteorology Hong Kong Diatoms Dinoflagellates
Red tides represent a major environmental issue in coastal waters globally. However, few studies have examined the relationship between red tides and meteorological factors. Thus, we used a 32-year time-series of frequent red tide events in Tolo Harbour and Channel, to study their relationship with meteorological factors. Most red tides are dominated by dinoflagellates in March, while most diatom red tides in May. Dinoflagellate and diatom red tides respond differently to different meteorological factors. Warming air temperatures in spring favor the generation of dinoflagellate red tides, while precipitation hinders them. The optimum temperature range is approximately 17–23 °C and 26–29 °C for dinoflagellate and diatom red tides, respectively. Moderate northeasterly winds promote the formation of dinoflagellate red tides. Dinoflagellate red tides are not hindered by cloudy weather and occur in sunlight of varying brightness, whereas diatoms red tides require a certain amount of bright sunlight.
1. Introduction The term “red tide” refers to the phenomenon of discoloration of seawater caused by the excessive accumulation of marine plankton biomass. Since 1950, red-tide outbreaks have become more frequent in the coastal waters in China (Yan et al., 2001; Zhou et al., 2008) and globally (Anderson, 2003, 2012). In 2003 alone, 119 red-tide events were reported in China (Tang et al., 2006). Red tides often lead to serious economic and ecological problems, causing concern for the safety of seafood caught in these areas because of the harmful toxins associated with algal blooms. Many studies have been conducted on the classification of red-tide-causing organisms (Liu et al., 2013) and the factors affecting red-tide outbreaks in the last three decades (Yin, 2003; Chika, 2016; Wang et al., 2016). Several mechanisms have been proposed to explain the formation of harmful algal blooms (HABs) (Yin et al., 2008; McLeod et al., 2012; Anderson et al., 2015). Among these mechanisms, eutrophication is generally regarded as the major cause of algal bloom formation, as nitrogen and phosphorus are the main limiting nutrients for phytoplankton biomass in marine waters. However, red tides with phytoplankton of high biomass also occur in low-nutrient waters. This phenomenon has been explained by a proposed and modeltested physical-biological coupling-induced aggregation mechanism in
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low-nutrient environments (Lai and Yin, 2014). Because of the complexity of marine ecosystems, it is often difficult to discern the relationships between marine environmental factors and red tides (Hu et al., 2016); consequently, it remains difficult to predict when and where a red tide will occur. As stated by Wells et al. (2015), data on the fundamental mechanisms driving red tides are lacking. Furthermore, the authors emphasized that climate change pressures will influence marine planktonic systems, leading to an increase in the occurrence of HABs. Therefore, there is a pressing need for the analysis of long timeseries datasets of red-tide events. The frequency of red tides in Hong Kong is one of the highest worldwide (Yin, 2003), resulting in the publication of many studies on red tides. Morton and Twentyman (1971) first reported the occurrence and toxicity of red tides caused by Noctiluca scintillans in Hong Kong. The annual red-tide events in Hong Kong waters became frequent during the 1980s (Li et al., 2004), with 27 harmful or potentially harmful dinoflagellate species being identified during 1997–1998 (Lu and Hodgkiss, 2004). Previous studies have found that the red tides in Hong Kong are generally correlated with wind speed and direction (Yin, 2003). However, few studies have examined how other meteorological factors influence the formation of red tides, particularly the red tides of dinoflagellates and diatoms. Thus, the aim of this study was to examine
Corresponding author at: School of Marine Sciences, Sun Yat-sen University, Zhuhai, 519082, China. E-mail address: [email protected] (K. Yin). Joint first author.
https://doi.org/10.1016/j.marpolbul.2017.11.035 Received 10 August 2017; Received in revised form 14 November 2017; Accepted 16 November 2017 0025-326X/ © 2017 Elsevier Ltd. All rights reserved.
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Fig. 1. Map of Tolo Harbour and Channel, Hong Kong and China coasts near Dalian, Zhejiang, Shenzhen and Hainan.
Similarly, on a red tide event day, we examined values of six meteorological factors and arranged them in eight corresponding bins. The total number of red-tides during 1983–2014 in a bin was counted, which was the frequency of red tides in the bin. The annual frequency or the monthly frequency of red tides was obtained by dividing the total by 32 years or 12 months. Therefore, for each bin (Table 1), there was a pair of the frequencies of red tides (days) and a regular meteorological factor (days), which were used to analyze their relationships. The software program Sigma Plot version 12.5 was used to perform the statistical analysis.
the relationship of total red-tide events, dinoflagellate red tides, and diatom red tides with various meteorological factors, such as air temperature, wind direction, wind speed, rainfall, cloud cover, and hours of bright sunlight. 2. Materials and methods In this study, a red tide is defined as a patch of discolored water caused by the high biomass of phytoplankton in a marine habitat. Red tides in Hong Kong waters have been monitored by the Agriculture, Fisheries, and Conservation Department (AFCD) of Hong Kong since 1983. This study used the AFCD red-tide time-series data collected in Tolo Harbour and Channel (Tolo) from 1983 to 2014 (Fig. 1). Data on red tides in other regions (including Hainan, Shenzhen, Zhejiang and Dalian) originate from the Red Tide Disasters Law in Typical Chinese Waters (Zhao, 2010) and the Bulletin of Marine Environmental Status of Hainan Province (DOFHP, 2001–2014). The meteorological factors used in this study include wind direction, wind speed, air temperature, rainfall, cloud cover, and hours of bright sunlight. The data during 1983–2014 originate from the Hong Kong Observatory (http://gb.weather.gov.hk/contentc.htm). Wind direction and wind speed are recorded at Wangler Island. All other meteorological factors are recorded by the Hong Kong Observatory site (Fig. 1). The data for air temperature at the other regions (including Hainan, Shenzhen, Zhejiang and Dalian; Fig. 1) from 1981 to 2010 originate from the National Meteorological Information Center (http:// data.cma.cn/); however, temperature data for 2011–2014 are not available. On a red-tide event day, the meteorological factors are referred to as the “red-tide-day meteorological factors”. The meteorological factors for all days, including red-tide days, are referred to as regular-day meteorological factors. The meteorological factor values during 1983–2014 were grouped into eight bins (Table 1). The number of days in a bin of a meteorological factor was counted, and represented the frequency of the meteorological factor in the bin. Thus, each meteorological factor generates eight frequencies from the eight bins. For each bin, we separated the total frequency into the monthly distribution, or divided the total frequency by 32 years to obtain the annual (mean) frequency or we divided the total by 12 months to obtain the monthly (mean) frequency.
3. Results 3.1. Monthly distribution of red tides During 1983–2014, 436 red tides occurred in Tolo, and were caused by dinoflagellates, diatoms, and other taxa. Dinoflagellates are the dominant taxa causing red tides in Tolo (Fig. 2), accounting for 62.6% (273) of tides. Diatoms and other taxa account for 18.6% (81) and 18.8% (82) of red tides, respectively. From 1983 to 2014, the overall frequency of red tides was the highest in March (n = 60) and the lowest in August (n = 14). Dinoflagellate-dominated red tides peak in February–April and have the lowest frequency in August. Diatom red tides peak in May and remain relatively high through August, with the lowest frequency occurring in February. The frequency distribution of the other types of red tides roughly follows the same pattern as the overall pattern of all red tides (Fig. 2A–D). The most frequently occurring red tide dinoflagellate species are N. scintillans (73 times), P. minimum (44 times), P. triestinum (33 times), and G. polygramma (23 times) (Table 2). The most frequently occurring diatom species is S. costatum (23 times). 3.2. Red tides in relation to monthly changes in meteorological factors The monthly averages of red-tide-day meteorological factors were compared with those of regular-day meteorological factors (Fig. 3). Red-tide day values of air temperature are similar to those of regularday values. Red-tide day values of wind speed, wind direction, rainfall, and cloud cover are lower than those of regular-day values. Red-tideday air temperature (Fig. 3A) and wind direction (Fig. 3D) are similar to 420
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Table 1 Bin ranges of the data of six meteorological factors during 1983–2014 in Hong Kong. The values in parentheses represent the bin values for the given meteorological factor and were used to assess relationships between meteorological factors and red tides. Factors
Bins 1
2
3
4
5
6
7
8
Air temperature (°C) Wind direction (°)
< 11 (9.5) 337.5–22.4 (N)
11–13.9 (12.5) 22.5–67.4 (NE)
14–16.9 (15.5) 67.5–112.4 (E)
17–19.9 (18.5) 112.5–157.4 (SE)
20–22.9 (21.5) 157.5–202.4 (S)
23–25.9 (24.5) 202.5–247.4 (SW)
26–28.9 (27.5) 247.5–292.4 (W)
Wind speed (m s− 1) Rainfall (mm) Cloud cover (%) Bright sunlight (hours)
< 1.5 (0.5) 0 (0) < 30 (25) 0 (0)
1.5–3.4 (2.5) 0–9.9 (5) 30–39.9 (35) 0–1.9 (1)
3.5–5.4 (4.5) 10–19.9 (15) 40–49.9 (45) 2–3.9 (3)
5.5–7.4 (6.5) 20–29.9 (25) 50–59.9 (55) 4–5.9 (5)
7.5–9.4 (8.5) 30–39.9 (35) 60–69.9 (65) 6–7.9 (7)
9.5–11.4 (10.5) 40–49.9 (45) 70–79.9 (75) 8–9.9 (9)
11.5–13.4 (12.5) 50–59.9 (55) 80–89.9 (85) 10–11.9 (11)
29– (30.5) 292.5– 337.4 (NW) 13.45– 14.5 60– (65) 90– (95) 12– (13)
those on regular days. Red-tide-day wind speed is lowest in April (Fig. 3B). Red-tide-day rainfall is high in May–July and September, but is very low in August and the other months (Fig. 3C). Red-tide-day cloud cover values are lower than those of regular-day values in July and August (Fig. 3E). However, the number of bright sunlight hours is higher on red-tide days than on the regular days (Fig. 3F).
Table 2 List of most frequently occurring red tide species in Tolo Harbour and Channel, Hong Kong during 1983–2014.
3.3. Meteorological conditions for red tides Based on the bins defined in Table 1, the frequency distribution of red-tide days for the given meteorological factors (Fig. 4) indicates that certain weather conditions are favorable for red tides. The most suitable conditions for the occurrence of red tides include 6.5 m s− 1 easterly wind, 18.5 °C air temperature, low rainfall, 85% cloud cover, and 9 h of bright sunlight. In comparison, certain weather conditions, such as too high or too low air temperature, too fast or too slow wind, high rainfall, low cloud cover, and southerly and westerly winds, are not favorable for the occurrence of red tides. In particular, no red tides occur when the temperature drops below 9.5 °C, the rainfall exceeds 25 mm, and the wind is higher or lower than 12.5 m s− 1 and 0.5 m s− 1, respectively.
Ranking
Red tide species
Frequency
Group
1 2 3 4 5 6 7 8 9 10 11
Noctiluca scintillans Prorocentrum minimum Prorocentrum triestinum Gonyaulax polygramma Skeletonema costatum Scrippsiella trochoidea Heterosigma akashiwo Ceratium furca Prorocentrum sigmoides Heterocapsa circularisquama Leptocylindrus minimus
73 44 33 23 23 19 17 15 14 11 11
Dinoflagellates Dinoflagellates Dinoflagellates Dinoflagellates Diatoms Dinoflagellates Raphidophyta Dinoflagellates Dinoflagellates Dinoflagellates Diatoms
frequently than diatom red tides at wind speeds of 6.5–10.5 m s− 1 in a north or northeasterly direction, an air temperature of 15.5–21.5 °C, 15 mm rainfall, 85–95% cloud cover, and 0–1 h of bright sunlight. The most favorable conditions for dinoflagellate red tides are a wind speed of 6.5 m s− 1 in a northeasterly direction, an air temperature of 18 °C, 5 mm rainfall, 85–95% cloud cover, and 1 h of bright sunlight. The most favorable conditions for diatom red tides are a wind speed of 4.5 m s− 1 in an easterly direction, air temperature of 27.5 °C, 5 mm of rainfall, 65% cloud cover, and 9 h of bright sunlight (Fig. 5).
3.4. Effects of meteorological factors on the distribution of dinoflagellate and diatom red tides Dinoflagellate and diatom red tides respond differently to the same meteorological conditions. Dinoflagellate red tides occur more
Fig. 2. Monthly distribution of red tides in Tolo Harbour and Channel, Hong Kong, from 1983 to 2014. Distributions are shown for all red tides (A), those caused by dinoflagellates only (B), those caused by diatoms only (C), and those caused by other taxa only (D).
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Fig. 3. Comparison of the mean monthly values between redtide-day meteorological factors (closed circles) and regularday meteorological factors (open triangles) from 1983 to 2014 in Tolo Harbour and Channel.
regular meteorological factors, except for air temperature (Fig. 7). The frequency of diatom red-tides has a larger correlation coefficient r with rainfall and air temperature (Fig. 8). Based on correlation coefficient r, rainfall preceding red tides is considered the most influential factor for the occurrence of both dinoflagellate and diatom red tides (Figs. 6–8).
3.5. Relationship between red tides and meteorological factors Different red-tide taxa exhibit different responses to the meteorological factors evaluated in this study. All red tides are significantly correlated with rainfall, wind speed, wind direction, cloud cover, hours of bright sunlight, and air temperature (Fig. 6). The frequency of dinoflagellate red-tides is significantly correlated with the frequencies of
Fig. 4. Distribution of the frequency of red-tide days for the given bin values of meteorological factors (Table 1) during 1983–2014.
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Fig. 5. Percentage of dinoflagellate (closed circles) and diatom (open triangles) red tides over the total numbers of dinoflagellate and diatom red tides, respectively, during 1983–2014 vs the meteorological factors (mean bin values, Table 1).
4. Discussion
distribution of red tides in Tolo and along the coast of China. We observed some differences between dinoflagellates and diatoms in their responses to air temperature. The frequency of dinoflagellate red tides peaks in March and troughs in August (Fig. 2B), whereas the frequency of diatom red tides peaks in May, aligning with the timing of delayed
4.1. Effects of temperature Temperature plays an important role in regulating the monthly
Fig. 6. Correlation between the yearly frequencies of red tides and meteorological factors from 1983 to 2014. All significant correlations (p < 0.05) are indicated as solid lines.
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Fig. 7. Correlations between the yearly frequency of dinoflagellate red tides and annual frequency of corresponding meteorological factors (bin values) from 1983 to 2014. The correlations are significant (solid lines) for all meteorological factors (p < 0.05), except for air temperature (A) (dashed line, p > 0.05).
Fig. 8. Correlations between the yearly frequency of diatom red tides and annual frequency of corresponding meteorological factors (bin values) from 1983 to 2014. The correlations are significant (solid lines) (p < 0.05) for meteorological factors including air temperature, wind direction, wind speed and rainfall, and not significant for cloud cover and bright sunlight (dashed lines) (p > 0.05).
the water temperature is 17–21 °C (in winter and early spring), with abundance being negatively correlated with temperature in Hong Kong. In comparison, the suitable temperature range for S. costatum is 8–32 °C (Chin et al., 1965). Most red tide events of G. polygramma occur in February and March when the temperature is 15–20 °C (Yin, 2003). N.
spring blooms. Furthermore, the optimum temperatures for the occurrence of dinoflagellate and diatom red tides differ by approximately 10 °C. In Tolo, the correlation between the frequency of red tides and air temperature is significant for diatoms, but not for dinoflagellates. In fact, Zhang et al. (2017) shows that N. scintillans red tides occur when 424
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dinoflagellates and diatoms (Zhang and Dickman, 1999; Dickman and Zhang, 1999). In China, ballast waters contain many algal species and have become a major threat to coastal ecosystems in the seas of China (Wu et al., 2017). The alien red tide species, Gymnodinium catenatum, invaded the waters of Australia from Japan or Spain through ballast water, and began to appear in the southern part of Tasmania in 1972, leading to red tides in 1980, 1986, 1991, and 1993 (Mcminn et al., 1997; Allegraeff, 1998). When the temperature becomes suitable in a given region, these species flourish and bloom as red tides. In addition, the water column is stable at this temperature range in these regions. These disparities reflect the different adaptations of red tide species to temperature, as temperature is the key factor influencing changes to the community structure and the alternation of seasonally superior plankton species in nature (Bouman et al., 2005).
scintillans, G. polygramma, and S. costatum are the main red tide species showing how temperature differs between dinoflagellate and diatom red tides. The earlier dominance of dinoflagellate blooms over diatom blooms observed in the present study contrasts with the conventional paradigm, in which the opposite pattern occurs. Yin (2003) proposed that temperature in Hong Kong waters in spring is very close to that in the summer of temperate waters; thus, dinoflagellates might have found a niche to flourish in the spring temperatures of this non-limiting nutrient environment. Temperate phytoplankton species are carried into Hong Kong in ballast waters (Zhang and Dickman, 1999; Dickman and Zhang, 1999) and find their optimum summer temperature in spring in the subtropical waters. If nutrients are not limiting, they grow fast and form blooms. The temperature of the water warms from south to north during spring–summer, and appears to contribute to the spatial progression of red tides along the coast of China. In southern China, red tides occur most frequently in February in Hainan (18° N), where the temperature is higher than that in northern China (DOFHP, 2001–2014). In Shenzhen City (22° N), which is adjacent to Hong Kong (22° N), red tides occur most frequently from March to April. Moving north to Zhejiang (28° N), red tides occur most frequently from May to June. Even further northward in Dalian (39° N), a typical temperate region, the peak red tide months are July and August (Fig. 9), as reported by Zhao (2010). On average, the peak red-tide months appear to lag by 1–2 months for every 4–6° increase in latitude northward. This pattern corresponds to increasing air temperature from south to north. The average air temperature of Tolo in March is 19.0 °C. As shown in Fig. 9, the mean air temperature during the peak red-tide months in Hainan, Shenzhen, Zhejiang, and Dalian are 19.9, 22.8, 19.0, and 23.7 °C, respectively, with an air temperature difference of 4.7 °C. This effect of air temperature on the occurrence of red tides is consistent with observations from other studies. Uhlig and Sahling (1990) studied the temporal distribution pattern of the seasonal periodicity of Noctiluca scintillans and the German Bight red tide phenomena from 1968 to 1988. The authors found that the maximal abundance of these species occurred in June and July, when the monthly mean temperature was approximately 22 °C. Park et al. (2013) studied the monthly frequency of red tides dominated by each of the nine major mixotrophic dinoflagellate species in the coastal waters of Korea from 1981 to 2009. These authors show that the frequency of five red-tide species peaks in June and September, when the monthly mean air temperature was approximately 22 °C. Air temperatures in the range of 19–24 °C appear to be optimal for the development of temperate phytoplankton. Consequently, red tides occur in China, progressing northwards as the air warms. Because the ballast waters containing red-tide-causing species move around the world (Smayda, 2007), there is no lack of these species as phytoplankton seeds develop into local red tides. For example, ballast waters in ocean vessels to Hong Kong were found to contain many non-native
4.2. Effects of winds Wind conditions play an important role in the formation of red tides in Tolo (Fig. 6B, D). Easterly and northeasterly winds favor the formation of red tides (Fig. 4D). Yin (2003) show that prevailing northeasterly winds lead to downwelling and a longer residence time of water in the semi-enclosed bays, allowing local nutrient inputs to be utilized; thus, creating suitable conditions for red tides, which are similar to a batch culture confined in a bottle. The average residence time of water in Tolo is 28 days, which extends to 38 days in the dry season with winds from the east and northeast. Residence time is reduced to 14.4 days during the wet season, and is strongly affected by runoff, rainfall, and southwestern monsoon winds (Lee et al., 2006). A longer residence time allows a water body to behave as a batch culture and for the algae to respond to local nutrient inputs. For example, Lam Tsuen River flows into Tolo Harbour, carrying high concentrations of TP and TN (of up to 1.18 and 5.11 mg L− 1, respectively) in 1998 (Li et al., 2005), and TP and TN were 0.05 and 0.61 mg L− 1 at TM2 (EPD, 2016). Therefore, Tolo Harbour receives high nutrient input. Thus, favorable wind-induced conditions partly explain why more red tides occur in March and fewer in August. Dinoflagellates and diatoms differ in their responses to winds. Dinoflagellate red tides occur more frequently than diatom red tides when northeasterly wind speeds are high (Fig. 5B, D). Most N. scintillans red tides occur when the wind direction is northeasterly, while most S. costatum red tides occur when the wind direction is southeasterly in Hong Kong during 1983 to 1998 (Yin, 2003). N. scintillans and S. costatum played a major role in the wind direction difference between dinoflagellate and diatom red tides. Furthermore, Hinder et al. (2012) showed that dinoflagellate red tides are associated with calm conditions, whereas diatom red tides are associated with turbulent conditions. Diatoms are generally considered superior competitors to dinoflagellates because of their physiological advantages, including higher Fig. 9. Monthly distribution of red tides and air temperature in different coastal areas of China. Hainan (A), Shenzhen (B), Zhejiang (C), and Dalian (D) are in the direction of south to north during 1933–2014.
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frequency and hours of both bright sunlight and cloud cover for dinoflagellates (p < 0.05), but not for diatoms (p > 0.05), supporting these previous observations. In addition, heterotrophic dinoflagellates, such as N. scintillans, also feed on a variety of items, including phytoplankton, fish eggs, copepod eggs, and bacteria (Kirchner et al., 1996); consequently, their dependence on bright sunlight is reduced. These results demonstrate that dinoflagellate red tides are more strongly influenced by variation in the amount of bright sunlight and cloud cover than diatom red tides.
growth rates and a greater ability to compete for nitrogen at low concentrations (Hinder et al., 2012). However, dinoflagellates have the ability to swim. For example, the swimming speed of Akashiwo sanguinea is approximately 298 μm s− 1 (or approximately 1 m h− 1) (Park et al., 2002). Thus, dinoflagellates have an advantage over diatoms in a stratified water column. Because of their swimming ability, dinoflagellates are able to form high-biomass red tides via aggregation mechanisms (Lai and Yin, 2014). Dapeng Bay is one of the places where dinoflagellate red tides occur frequently in China (Zhou et al., 2008). These events create hotspots of dinoflagellates that move into Tolo Harbour with an easterly wind. Moreover, the accumulation of algal cells in the inner bay from the outer areas due to physical factors, such as wind and water currents, have been reported in Daya Bay, contributing to the occurrence of algal blooms (Wang et al., 2005). These accumulation events might be one of the mechanisms underlying the occurrence of more dinoflagellate red tides in March at Tolo.
5. Conclusions The current study utilized a 32-year red tide event time series (1983–2014) in Tolo Harbour and Channel to demonstrate how weather factors contribute towards driving the occurrence of red tides. The study shows that wind speed and direction influence the red tides of both dinoflagellates and diatoms, which is consistent with a previous study (Yin, 2003). Dinoflagellates dominate the monthly distribution of red tides, with mostred tides occurring in March. In comparison, diatom red tides primarily occur in May. The frequency of red tide outbreaks in the peak months was several times greater than that in non-peak months. Air temperature has a significant effect on red tide outbreaks in peak months, whereas rainfall affects red tide occurrence in non-peak months. Dinoflagellate and diatom red tides respond differently to meteorological factors. The optimum temperature difference related to dinoflagellate and diatom red tide outbreaks is about 10 °C, with the former growing at lower temperatures than the latter. Dinoflagellates are able to tolerate high cloud cover, whereas diatoms require less cloud cover and sufficient quantities of bright sunlight. Various mechanisms have been proposed for the formation of red tides. Wells et al. (2015) emphasized the importance of understanding the mechanisms that drive red tides to incorporate the effects of climate change driving. However, in many regions, sufficiently long time-series of data on red-tide events are lacking from which to assess their relationship with weather conditions. To our knowledge, this study is the first to demonstrate the effects of meteorological factors on red-tide events using a long (32-year) time-series. Our study provides a valuable insight into the mechanisms underlying red-tide formation, as well as a basis for linking red-tide events to weather conditions. Global climate change has already affected Hong Kong by causing an increase in air temperature, a rise in sea level, and a change in wind speed and direction (He et al., 2014; Environment Bureau, 2015, 2017). In conclusion, our findings suggest that we must consider the role of meteorological factors in the study and projection of the likely trends of redtide occurrences under different climate change scenarios.
4.3. Effects of rainfall, clouds, and sunlight In Tolo, red tides occur least frequently in summer, with diatom red tides peaking in May. This result is consistent with previous findings, such as the phytoplankton groups in Hong Kong (EPD, 2015), and the temporal distributions of dinoflagellates and diatoms (Yin, 2003). Red tides also occur least frequently in July in the adjacent waters of Shenzhen (Fig. 9B). Rainfall might be the key factor limiting the occurrence of red tides (Figs. 3C and 5C), because it affects the formation of red tides in different ways. Rainfall adds freshwater to the surface of coastal waters and strengthens water column stratification, while reducing salinity at the surface. In Tolo, rainwater runoff rich in nutrients flows from the catchment to the streams and rivers and, ultimately, Tolo Harbour. As a result, an estuarine-like circulation forms in the harbour, in which the surface water flows outward and the bottom layer flows inwards, creating a dilution effect (Yin et al., 2001). The freshwater runoff causes turbid surface plumes as well. These conditions (reduced salinity, high turbidity, and faster dilution) are favorable for diatoms, but not for dinoflagellates. As previously reported, some dinoflagellates are not able to adapt to high concentrations of suspended solids (Shirota, 1989). Moreover, Li et al. (2004) reported that the transparency of seawater and suspended solids affect red tides in Tolo, and the dilution effect might reduce the ability of vertically migrating dinoflagellates to acquire nutrients in the bottom layer (Yin, 2003). Therefore, frequent rainfall events might restrict outbreaks of red tides at our study site in July and August. In comparison, higher concentrations of silicate make diatoms grow better than dinoflagellates, due to the estuarine influence during summer (Yin, 2003). As a result, diatom red tides peak in summer. Furthermore, dinoflagellate and diatom red tides exhibit different responses to cloud cover and hours of bright sunlight, which are the reciprocal meteorological factors. Dinoflagellate red tides primarily occur under 85–95% cloud cover, whereas diatom red tides primarily occur under 55–65% cloud cover. Therefore, the former does not require as much bright sunlight as the latter. The days with the greatest number of bright sunlight hours do not favor the highest frequency of dinoflagellate and diatom red tides (Fig. 5F), possibly because phytoplankton are subject to photoinhibition. Dinoflagellate red tides primarily break out when there is only 1 h of bright sunlight in a day, whereas diatom red tides primarily break out when there are 9 h of bright sunlight in a day. Therefore, high cloud cover favors dinoflagellate red tides, whereas low cloud cover and more bright sunlight promote diatom red tides. Sun (2004) found that diatoms grow in sunlight (13–20 MJ m− 2 d− 1), but are suppressed by the bright sunlight of fall and winter. In comparison, the dinoflagellates Prorocentrum donghaiense and Alexandrium tamarense tend to grow in relatively weaker sunshine (8–11 MJ m− 2 d− 1) in the East China Sea. Diatoms have higher photosynthetic rates than dinoflagellates (Hinder et al., 2012). Our results show a significant correlation between red-tide
Acknowledgements This work was supported by grants from the National Science Foundation of China (No. 91328203 and 3141101302) and Guangdong Department of Science and Technology (DST; 2013B051000042). We acknowledge the Hong Kong Agriculture, Fisheries and Conservation Department for providing data on red-tide events. References Allegraeff, G.M., 1998. Transport of toxic dinoflagellates via ships' ballast water: bioeconomic risk assessment and efficiency of possible ballast water management strategies. Mar. Ecol. Prog. Ser. 168, 297–309. http://dx.doi.org/10.3354/meps168297. Anderson, D.M., 2003. The expanding global problem of harmful algal blooms. In: Ragaini, R. (Ed.), International Seminar on Nuclear War and Planetary Emergencies, 27th Session, Erice, Italy, 18–26 August 2002. World Scientific, Singapore, pp. 372–393. http://dx.doi.org/10.1142/9789812705150_0042. Anderson, D., 2012. HABs in a changing world: a perspective on harmful algal blooms, their impacts, and research and management in a dynamic era of climactic and environmental change. In: 15th ICHA Proceedings, (opening address). Anderson, C.R., Moore, S.K., Tomlinson, M.C., Silke, J., Cusack, C.K., 2015. Living with harmful algal blooms in a changing world: strategies for modeling and mitigating
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Effects of meteorological factors on the temporal distribution of red tides in Tolo Harbour, Hong Kong Jiansheng Huanga,b,c, Hao Liua,b,1, Kedong Yina,b,
T
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a
School of Marine Sciences, Sun Yat-sen University, Zhuhai, 519082, China Key Laboratory of Marine Resources and Coastal Engineering in Guangdong Province, Guangzhou, 510006, China c Dongguan Marine and Fishery Environmental Monitoring Station, Dongguan, 523002, China b
A R T I C L E I N F O
A B S T R A C T
Keywords: Red tides Harmful algal blooms Meteorology Hong Kong Diatoms Dinoflagellates
Red tides represent a major environmental issue in coastal waters globally. However, few studies have examined the relationship between red tides and meteorological factors. Thus, we used a 32-year time-series of frequent red tide events in Tolo Harbour and Channel, to study their relationship with meteorological factors. Most red tides are dominated by dinoflagellates in March, while most diatom red tides in May. Dinoflagellate and diatom red tides respond differently to different meteorological factors. Warming air temperatures in spring favor the generation of dinoflagellate red tides, while precipitation hinders them. The optimum temperature range is approximately 17–23 °C and 26–29 °C for dinoflagellate and diatom red tides, respectively. Moderate northeasterly winds promote the formation of dinoflagellate red tides. Dinoflagellate red tides are not hindered by cloudy weather and occur in sunlight of varying brightness, whereas diatoms red tides require a certain amount of bright sunlight.
1. Introduction The term “red tide” refers to the phenomenon of discoloration of seawater caused by the excessive accumulation of marine plankton biomass. Since 1950, red-tide outbreaks have become more frequent in the coastal waters in China (Yan et al., 2001; Zhou et al., 2008) and globally (Anderson, 2003, 2012). In 2003 alone, 119 red-tide events were reported in China (Tang et al., 2006). Red tides often lead to serious economic and ecological problems, causing concern for the safety of seafood caught in these areas because of the harmful toxins associated with algal blooms. Many studies have been conducted on the classification of red-tide-causing organisms (Liu et al., 2013) and the factors affecting red-tide outbreaks in the last three decades (Yin, 2003; Chika, 2016; Wang et al., 2016). Several mechanisms have been proposed to explain the formation of harmful algal blooms (HABs) (Yin et al., 2008; McLeod et al., 2012; Anderson et al., 2015). Among these mechanisms, eutrophication is generally regarded as the major cause of algal bloom formation, as nitrogen and phosphorus are the main limiting nutrients for phytoplankton biomass in marine waters. However, red tides with phytoplankton of high biomass also occur in low-nutrient waters. This phenomenon has been explained by a proposed and modeltested physical-biological coupling-induced aggregation mechanism in
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low-nutrient environments (Lai and Yin, 2014). Because of the complexity of marine ecosystems, it is often difficult to discern the relationships between marine environmental factors and red tides (Hu et al., 2016); consequently, it remains difficult to predict when and where a red tide will occur. As stated by Wells et al. (2015), data on the fundamental mechanisms driving red tides are lacking. Furthermore, the authors emphasized that climate change pressures will influence marine planktonic systems, leading to an increase in the occurrence of HABs. Therefore, there is a pressing need for the analysis of long timeseries datasets of red-tide events. The frequency of red tides in Hong Kong is one of the highest worldwide (Yin, 2003), resulting in the publication of many studies on red tides. Morton and Twentyman (1971) first reported the occurrence and toxicity of red tides caused by Noctiluca scintillans in Hong Kong. The annual red-tide events in Hong Kong waters became frequent during the 1980s (Li et al., 2004), with 27 harmful or potentially harmful dinoflagellate species being identified during 1997–1998 (Lu and Hodgkiss, 2004). Previous studies have found that the red tides in Hong Kong are generally correlated with wind speed and direction (Yin, 2003). However, few studies have examined how other meteorological factors influence the formation of red tides, particularly the red tides of dinoflagellates and diatoms. Thus, the aim of this study was to examine
Corresponding author at: School of Marine Sciences, Sun Yat-sen University, Zhuhai, 519082, China. E-mail address: [email protected] (K. Yin). Joint first author.
https://doi.org/10.1016/j.marpolbul.2017.11.035 Received 10 August 2017; Received in revised form 14 November 2017; Accepted 16 November 2017 0025-326X/ © 2017 Elsevier Ltd. All rights reserved.
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Fig. 1. Map of Tolo Harbour and Channel, Hong Kong and China coasts near Dalian, Zhejiang, Shenzhen and Hainan.
Similarly, on a red tide event day, we examined values of six meteorological factors and arranged them in eight corresponding bins. The total number of red-tides during 1983–2014 in a bin was counted, which was the frequency of red tides in the bin. The annual frequency or the monthly frequency of red tides was obtained by dividing the total by 32 years or 12 months. Therefore, for each bin (Table 1), there was a pair of the frequencies of red tides (days) and a regular meteorological factor (days), which were used to analyze their relationships. The software program Sigma Plot version 12.5 was used to perform the statistical analysis.
the relationship of total red-tide events, dinoflagellate red tides, and diatom red tides with various meteorological factors, such as air temperature, wind direction, wind speed, rainfall, cloud cover, and hours of bright sunlight. 2. Materials and methods In this study, a red tide is defined as a patch of discolored water caused by the high biomass of phytoplankton in a marine habitat. Red tides in Hong Kong waters have been monitored by the Agriculture, Fisheries, and Conservation Department (AFCD) of Hong Kong since 1983. This study used the AFCD red-tide time-series data collected in Tolo Harbour and Channel (Tolo) from 1983 to 2014 (Fig. 1). Data on red tides in other regions (including Hainan, Shenzhen, Zhejiang and Dalian) originate from the Red Tide Disasters Law in Typical Chinese Waters (Zhao, 2010) and the Bulletin of Marine Environmental Status of Hainan Province (DOFHP, 2001–2014). The meteorological factors used in this study include wind direction, wind speed, air temperature, rainfall, cloud cover, and hours of bright sunlight. The data during 1983–2014 originate from the Hong Kong Observatory (http://gb.weather.gov.hk/contentc.htm). Wind direction and wind speed are recorded at Wangler Island. All other meteorological factors are recorded by the Hong Kong Observatory site (Fig. 1). The data for air temperature at the other regions (including Hainan, Shenzhen, Zhejiang and Dalian; Fig. 1) from 1981 to 2010 originate from the National Meteorological Information Center (http:// data.cma.cn/); however, temperature data for 2011–2014 are not available. On a red-tide event day, the meteorological factors are referred to as the “red-tide-day meteorological factors”. The meteorological factors for all days, including red-tide days, are referred to as regular-day meteorological factors. The meteorological factor values during 1983–2014 were grouped into eight bins (Table 1). The number of days in a bin of a meteorological factor was counted, and represented the frequency of the meteorological factor in the bin. Thus, each meteorological factor generates eight frequencies from the eight bins. For each bin, we separated the total frequency into the monthly distribution, or divided the total frequency by 32 years to obtain the annual (mean) frequency or we divided the total by 12 months to obtain the monthly (mean) frequency.
3. Results 3.1. Monthly distribution of red tides During 1983–2014, 436 red tides occurred in Tolo, and were caused by dinoflagellates, diatoms, and other taxa. Dinoflagellates are the dominant taxa causing red tides in Tolo (Fig. 2), accounting for 62.6% (273) of tides. Diatoms and other taxa account for 18.6% (81) and 18.8% (82) of red tides, respectively. From 1983 to 2014, the overall frequency of red tides was the highest in March (n = 60) and the lowest in August (n = 14). Dinoflagellate-dominated red tides peak in February–April and have the lowest frequency in August. Diatom red tides peak in May and remain relatively high through August, with the lowest frequency occurring in February. The frequency distribution of the other types of red tides roughly follows the same pattern as the overall pattern of all red tides (Fig. 2A–D). The most frequently occurring red tide dinoflagellate species are N. scintillans (73 times), P. minimum (44 times), P. triestinum (33 times), and G. polygramma (23 times) (Table 2). The most frequently occurring diatom species is S. costatum (23 times). 3.2. Red tides in relation to monthly changes in meteorological factors The monthly averages of red-tide-day meteorological factors were compared with those of regular-day meteorological factors (Fig. 3). Red-tide day values of air temperature are similar to those of regularday values. Red-tide day values of wind speed, wind direction, rainfall, and cloud cover are lower than those of regular-day values. Red-tideday air temperature (Fig. 3A) and wind direction (Fig. 3D) are similar to 420
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Table 1 Bin ranges of the data of six meteorological factors during 1983–2014 in Hong Kong. The values in parentheses represent the bin values for the given meteorological factor and were used to assess relationships between meteorological factors and red tides. Factors
Bins 1
2
3
4
5
6
7
8
Air temperature (°C) Wind direction (°)
< 11 (9.5) 337.5–22.4 (N)
11–13.9 (12.5) 22.5–67.4 (NE)
14–16.9 (15.5) 67.5–112.4 (E)
17–19.9 (18.5) 112.5–157.4 (SE)
20–22.9 (21.5) 157.5–202.4 (S)
23–25.9 (24.5) 202.5–247.4 (SW)
26–28.9 (27.5) 247.5–292.4 (W)
Wind speed (m s− 1) Rainfall (mm) Cloud cover (%) Bright sunlight (hours)
< 1.5 (0.5) 0 (0) < 30 (25) 0 (0)
1.5–3.4 (2.5) 0–9.9 (5) 30–39.9 (35) 0–1.9 (1)
3.5–5.4 (4.5) 10–19.9 (15) 40–49.9 (45) 2–3.9 (3)
5.5–7.4 (6.5) 20–29.9 (25) 50–59.9 (55) 4–5.9 (5)
7.5–9.4 (8.5) 30–39.9 (35) 60–69.9 (65) 6–7.9 (7)
9.5–11.4 (10.5) 40–49.9 (45) 70–79.9 (75) 8–9.9 (9)
11.5–13.4 (12.5) 50–59.9 (55) 80–89.9 (85) 10–11.9 (11)
29– (30.5) 292.5– 337.4 (NW) 13.45– 14.5 60– (65) 90– (95) 12– (13)
those on regular days. Red-tide-day wind speed is lowest in April (Fig. 3B). Red-tide-day rainfall is high in May–July and September, but is very low in August and the other months (Fig. 3C). Red-tide-day cloud cover values are lower than those of regular-day values in July and August (Fig. 3E). However, the number of bright sunlight hours is higher on red-tide days than on the regular days (Fig. 3F).
Table 2 List of most frequently occurring red tide species in Tolo Harbour and Channel, Hong Kong during 1983–2014.
3.3. Meteorological conditions for red tides Based on the bins defined in Table 1, the frequency distribution of red-tide days for the given meteorological factors (Fig. 4) indicates that certain weather conditions are favorable for red tides. The most suitable conditions for the occurrence of red tides include 6.5 m s− 1 easterly wind, 18.5 °C air temperature, low rainfall, 85% cloud cover, and 9 h of bright sunlight. In comparison, certain weather conditions, such as too high or too low air temperature, too fast or too slow wind, high rainfall, low cloud cover, and southerly and westerly winds, are not favorable for the occurrence of red tides. In particular, no red tides occur when the temperature drops below 9.5 °C, the rainfall exceeds 25 mm, and the wind is higher or lower than 12.5 m s− 1 and 0.5 m s− 1, respectively.
Ranking
Red tide species
Frequency
Group
1 2 3 4 5 6 7 8 9 10 11
Noctiluca scintillans Prorocentrum minimum Prorocentrum triestinum Gonyaulax polygramma Skeletonema costatum Scrippsiella trochoidea Heterosigma akashiwo Ceratium furca Prorocentrum sigmoides Heterocapsa circularisquama Leptocylindrus minimus
73 44 33 23 23 19 17 15 14 11 11
Dinoflagellates Dinoflagellates Dinoflagellates Dinoflagellates Diatoms Dinoflagellates Raphidophyta Dinoflagellates Dinoflagellates Dinoflagellates Diatoms
frequently than diatom red tides at wind speeds of 6.5–10.5 m s− 1 in a north or northeasterly direction, an air temperature of 15.5–21.5 °C, 15 mm rainfall, 85–95% cloud cover, and 0–1 h of bright sunlight. The most favorable conditions for dinoflagellate red tides are a wind speed of 6.5 m s− 1 in a northeasterly direction, an air temperature of 18 °C, 5 mm rainfall, 85–95% cloud cover, and 1 h of bright sunlight. The most favorable conditions for diatom red tides are a wind speed of 4.5 m s− 1 in an easterly direction, air temperature of 27.5 °C, 5 mm of rainfall, 65% cloud cover, and 9 h of bright sunlight (Fig. 5).
3.4. Effects of meteorological factors on the distribution of dinoflagellate and diatom red tides Dinoflagellate and diatom red tides respond differently to the same meteorological conditions. Dinoflagellate red tides occur more
Fig. 2. Monthly distribution of red tides in Tolo Harbour and Channel, Hong Kong, from 1983 to 2014. Distributions are shown for all red tides (A), those caused by dinoflagellates only (B), those caused by diatoms only (C), and those caused by other taxa only (D).
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Fig. 3. Comparison of the mean monthly values between redtide-day meteorological factors (closed circles) and regularday meteorological factors (open triangles) from 1983 to 2014 in Tolo Harbour and Channel.
regular meteorological factors, except for air temperature (Fig. 7). The frequency of diatom red-tides has a larger correlation coefficient r with rainfall and air temperature (Fig. 8). Based on correlation coefficient r, rainfall preceding red tides is considered the most influential factor for the occurrence of both dinoflagellate and diatom red tides (Figs. 6–8).
3.5. Relationship between red tides and meteorological factors Different red-tide taxa exhibit different responses to the meteorological factors evaluated in this study. All red tides are significantly correlated with rainfall, wind speed, wind direction, cloud cover, hours of bright sunlight, and air temperature (Fig. 6). The frequency of dinoflagellate red-tides is significantly correlated with the frequencies of
Fig. 4. Distribution of the frequency of red-tide days for the given bin values of meteorological factors (Table 1) during 1983–2014.
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Fig. 5. Percentage of dinoflagellate (closed circles) and diatom (open triangles) red tides over the total numbers of dinoflagellate and diatom red tides, respectively, during 1983–2014 vs the meteorological factors (mean bin values, Table 1).
4. Discussion
distribution of red tides in Tolo and along the coast of China. We observed some differences between dinoflagellates and diatoms in their responses to air temperature. The frequency of dinoflagellate red tides peaks in March and troughs in August (Fig. 2B), whereas the frequency of diatom red tides peaks in May, aligning with the timing of delayed
4.1. Effects of temperature Temperature plays an important role in regulating the monthly
Fig. 6. Correlation between the yearly frequencies of red tides and meteorological factors from 1983 to 2014. All significant correlations (p < 0.05) are indicated as solid lines.
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Fig. 7. Correlations between the yearly frequency of dinoflagellate red tides and annual frequency of corresponding meteorological factors (bin values) from 1983 to 2014. The correlations are significant (solid lines) for all meteorological factors (p < 0.05), except for air temperature (A) (dashed line, p > 0.05).
Fig. 8. Correlations between the yearly frequency of diatom red tides and annual frequency of corresponding meteorological factors (bin values) from 1983 to 2014. The correlations are significant (solid lines) (p < 0.05) for meteorological factors including air temperature, wind direction, wind speed and rainfall, and not significant for cloud cover and bright sunlight (dashed lines) (p > 0.05).
the water temperature is 17–21 °C (in winter and early spring), with abundance being negatively correlated with temperature in Hong Kong. In comparison, the suitable temperature range for S. costatum is 8–32 °C (Chin et al., 1965). Most red tide events of G. polygramma occur in February and March when the temperature is 15–20 °C (Yin, 2003). N.
spring blooms. Furthermore, the optimum temperatures for the occurrence of dinoflagellate and diatom red tides differ by approximately 10 °C. In Tolo, the correlation between the frequency of red tides and air temperature is significant for diatoms, but not for dinoflagellates. In fact, Zhang et al. (2017) shows that N. scintillans red tides occur when 424
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dinoflagellates and diatoms (Zhang and Dickman, 1999; Dickman and Zhang, 1999). In China, ballast waters contain many algal species and have become a major threat to coastal ecosystems in the seas of China (Wu et al., 2017). The alien red tide species, Gymnodinium catenatum, invaded the waters of Australia from Japan or Spain through ballast water, and began to appear in the southern part of Tasmania in 1972, leading to red tides in 1980, 1986, 1991, and 1993 (Mcminn et al., 1997; Allegraeff, 1998). When the temperature becomes suitable in a given region, these species flourish and bloom as red tides. In addition, the water column is stable at this temperature range in these regions. These disparities reflect the different adaptations of red tide species to temperature, as temperature is the key factor influencing changes to the community structure and the alternation of seasonally superior plankton species in nature (Bouman et al., 2005).
scintillans, G. polygramma, and S. costatum are the main red tide species showing how temperature differs between dinoflagellate and diatom red tides. The earlier dominance of dinoflagellate blooms over diatom blooms observed in the present study contrasts with the conventional paradigm, in which the opposite pattern occurs. Yin (2003) proposed that temperature in Hong Kong waters in spring is very close to that in the summer of temperate waters; thus, dinoflagellates might have found a niche to flourish in the spring temperatures of this non-limiting nutrient environment. Temperate phytoplankton species are carried into Hong Kong in ballast waters (Zhang and Dickman, 1999; Dickman and Zhang, 1999) and find their optimum summer temperature in spring in the subtropical waters. If nutrients are not limiting, they grow fast and form blooms. The temperature of the water warms from south to north during spring–summer, and appears to contribute to the spatial progression of red tides along the coast of China. In southern China, red tides occur most frequently in February in Hainan (18° N), where the temperature is higher than that in northern China (DOFHP, 2001–2014). In Shenzhen City (22° N), which is adjacent to Hong Kong (22° N), red tides occur most frequently from March to April. Moving north to Zhejiang (28° N), red tides occur most frequently from May to June. Even further northward in Dalian (39° N), a typical temperate region, the peak red tide months are July and August (Fig. 9), as reported by Zhao (2010). On average, the peak red-tide months appear to lag by 1–2 months for every 4–6° increase in latitude northward. This pattern corresponds to increasing air temperature from south to north. The average air temperature of Tolo in March is 19.0 °C. As shown in Fig. 9, the mean air temperature during the peak red-tide months in Hainan, Shenzhen, Zhejiang, and Dalian are 19.9, 22.8, 19.0, and 23.7 °C, respectively, with an air temperature difference of 4.7 °C. This effect of air temperature on the occurrence of red tides is consistent with observations from other studies. Uhlig and Sahling (1990) studied the temporal distribution pattern of the seasonal periodicity of Noctiluca scintillans and the German Bight red tide phenomena from 1968 to 1988. The authors found that the maximal abundance of these species occurred in June and July, when the monthly mean temperature was approximately 22 °C. Park et al. (2013) studied the monthly frequency of red tides dominated by each of the nine major mixotrophic dinoflagellate species in the coastal waters of Korea from 1981 to 2009. These authors show that the frequency of five red-tide species peaks in June and September, when the monthly mean air temperature was approximately 22 °C. Air temperatures in the range of 19–24 °C appear to be optimal for the development of temperate phytoplankton. Consequently, red tides occur in China, progressing northwards as the air warms. Because the ballast waters containing red-tide-causing species move around the world (Smayda, 2007), there is no lack of these species as phytoplankton seeds develop into local red tides. For example, ballast waters in ocean vessels to Hong Kong were found to contain many non-native
4.2. Effects of winds Wind conditions play an important role in the formation of red tides in Tolo (Fig. 6B, D). Easterly and northeasterly winds favor the formation of red tides (Fig. 4D). Yin (2003) show that prevailing northeasterly winds lead to downwelling and a longer residence time of water in the semi-enclosed bays, allowing local nutrient inputs to be utilized; thus, creating suitable conditions for red tides, which are similar to a batch culture confined in a bottle. The average residence time of water in Tolo is 28 days, which extends to 38 days in the dry season with winds from the east and northeast. Residence time is reduced to 14.4 days during the wet season, and is strongly affected by runoff, rainfall, and southwestern monsoon winds (Lee et al., 2006). A longer residence time allows a water body to behave as a batch culture and for the algae to respond to local nutrient inputs. For example, Lam Tsuen River flows into Tolo Harbour, carrying high concentrations of TP and TN (of up to 1.18 and 5.11 mg L− 1, respectively) in 1998 (Li et al., 2005), and TP and TN were 0.05 and 0.61 mg L− 1 at TM2 (EPD, 2016). Therefore, Tolo Harbour receives high nutrient input. Thus, favorable wind-induced conditions partly explain why more red tides occur in March and fewer in August. Dinoflagellates and diatoms differ in their responses to winds. Dinoflagellate red tides occur more frequently than diatom red tides when northeasterly wind speeds are high (Fig. 5B, D). Most N. scintillans red tides occur when the wind direction is northeasterly, while most S. costatum red tides occur when the wind direction is southeasterly in Hong Kong during 1983 to 1998 (Yin, 2003). N. scintillans and S. costatum played a major role in the wind direction difference between dinoflagellate and diatom red tides. Furthermore, Hinder et al. (2012) showed that dinoflagellate red tides are associated with calm conditions, whereas diatom red tides are associated with turbulent conditions. Diatoms are generally considered superior competitors to dinoflagellates because of their physiological advantages, including higher Fig. 9. Monthly distribution of red tides and air temperature in different coastal areas of China. Hainan (A), Shenzhen (B), Zhejiang (C), and Dalian (D) are in the direction of south to north during 1933–2014.
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frequency and hours of both bright sunlight and cloud cover for dinoflagellates (p < 0.05), but not for diatoms (p > 0.05), supporting these previous observations. In addition, heterotrophic dinoflagellates, such as N. scintillans, also feed on a variety of items, including phytoplankton, fish eggs, copepod eggs, and bacteria (Kirchner et al., 1996); consequently, their dependence on bright sunlight is reduced. These results demonstrate that dinoflagellate red tides are more strongly influenced by variation in the amount of bright sunlight and cloud cover than diatom red tides.
growth rates and a greater ability to compete for nitrogen at low concentrations (Hinder et al., 2012). However, dinoflagellates have the ability to swim. For example, the swimming speed of Akashiwo sanguinea is approximately 298 μm s− 1 (or approximately 1 m h− 1) (Park et al., 2002). Thus, dinoflagellates have an advantage over diatoms in a stratified water column. Because of their swimming ability, dinoflagellates are able to form high-biomass red tides via aggregation mechanisms (Lai and Yin, 2014). Dapeng Bay is one of the places where dinoflagellate red tides occur frequently in China (Zhou et al., 2008). These events create hotspots of dinoflagellates that move into Tolo Harbour with an easterly wind. Moreover, the accumulation of algal cells in the inner bay from the outer areas due to physical factors, such as wind and water currents, have been reported in Daya Bay, contributing to the occurrence of algal blooms (Wang et al., 2005). These accumulation events might be one of the mechanisms underlying the occurrence of more dinoflagellate red tides in March at Tolo.
5. Conclusions The current study utilized a 32-year red tide event time series (1983–2014) in Tolo Harbour and Channel to demonstrate how weather factors contribute towards driving the occurrence of red tides. The study shows that wind speed and direction influence the red tides of both dinoflagellates and diatoms, which is consistent with a previous study (Yin, 2003). Dinoflagellates dominate the monthly distribution of red tides, with mostred tides occurring in March. In comparison, diatom red tides primarily occur in May. The frequency of red tide outbreaks in the peak months was several times greater than that in non-peak months. Air temperature has a significant effect on red tide outbreaks in peak months, whereas rainfall affects red tide occurrence in non-peak months. Dinoflagellate and diatom red tides respond differently to meteorological factors. The optimum temperature difference related to dinoflagellate and diatom red tide outbreaks is about 10 °C, with the former growing at lower temperatures than the latter. Dinoflagellates are able to tolerate high cloud cover, whereas diatoms require less cloud cover and sufficient quantities of bright sunlight. Various mechanisms have been proposed for the formation of red tides. Wells et al. (2015) emphasized the importance of understanding the mechanisms that drive red tides to incorporate the effects of climate change driving. However, in many regions, sufficiently long time-series of data on red-tide events are lacking from which to assess their relationship with weather conditions. To our knowledge, this study is the first to demonstrate the effects of meteorological factors on red-tide events using a long (32-year) time-series. Our study provides a valuable insight into the mechanisms underlying red-tide formation, as well as a basis for linking red-tide events to weather conditions. Global climate change has already affected Hong Kong by causing an increase in air temperature, a rise in sea level, and a change in wind speed and direction (He et al., 2014; Environment Bureau, 2015, 2017). In conclusion, our findings suggest that we must consider the role of meteorological factors in the study and projection of the likely trends of redtide occurrences under different climate change scenarios.
4.3. Effects of rainfall, clouds, and sunlight In Tolo, red tides occur least frequently in summer, with diatom red tides peaking in May. This result is consistent with previous findings, such as the phytoplankton groups in Hong Kong (EPD, 2015), and the temporal distributions of dinoflagellates and diatoms (Yin, 2003). Red tides also occur least frequently in July in the adjacent waters of Shenzhen (Fig. 9B). Rainfall might be the key factor limiting the occurrence of red tides (Figs. 3C and 5C), because it affects the formation of red tides in different ways. Rainfall adds freshwater to the surface of coastal waters and strengthens water column stratification, while reducing salinity at the surface. In Tolo, rainwater runoff rich in nutrients flows from the catchment to the streams and rivers and, ultimately, Tolo Harbour. As a result, an estuarine-like circulation forms in the harbour, in which the surface water flows outward and the bottom layer flows inwards, creating a dilution effect (Yin et al., 2001). The freshwater runoff causes turbid surface plumes as well. These conditions (reduced salinity, high turbidity, and faster dilution) are favorable for diatoms, but not for dinoflagellates. As previously reported, some dinoflagellates are not able to adapt to high concentrations of suspended solids (Shirota, 1989). Moreover, Li et al. (2004) reported that the transparency of seawater and suspended solids affect red tides in Tolo, and the dilution effect might reduce the ability of vertically migrating dinoflagellates to acquire nutrients in the bottom layer (Yin, 2003). Therefore, frequent rainfall events might restrict outbreaks of red tides at our study site in July and August. In comparison, higher concentrations of silicate make diatoms grow better than dinoflagellates, due to the estuarine influence during summer (Yin, 2003). As a result, diatom red tides peak in summer. Furthermore, dinoflagellate and diatom red tides exhibit different responses to cloud cover and hours of bright sunlight, which are the reciprocal meteorological factors. Dinoflagellate red tides primarily occur under 85–95% cloud cover, whereas diatom red tides primarily occur under 55–65% cloud cover. Therefore, the former does not require as much bright sunlight as the latter. The days with the greatest number of bright sunlight hours do not favor the highest frequency of dinoflagellate and diatom red tides (Fig. 5F), possibly because phytoplankton are subject to photoinhibition. Dinoflagellate red tides primarily break out when there is only 1 h of bright sunlight in a day, whereas diatom red tides primarily break out when there are 9 h of bright sunlight in a day. Therefore, high cloud cover favors dinoflagellate red tides, whereas low cloud cover and more bright sunlight promote diatom red tides. Sun (2004) found that diatoms grow in sunlight (13–20 MJ m− 2 d− 1), but are suppressed by the bright sunlight of fall and winter. In comparison, the dinoflagellates Prorocentrum donghaiense and Alexandrium tamarense tend to grow in relatively weaker sunshine (8–11 MJ m− 2 d− 1) in the East China Sea. Diatoms have higher photosynthetic rates than dinoflagellates (Hinder et al., 2012). Our results show a significant correlation between red-tide
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