¹School of Science and Technology, The Open University of Hong Kong

Hong Kong, CHINA

kcho@ouhk.edu.hk

　

²Department of Ecology & Biodiversity, The University of Hong Kong

Hong Kong, CHINA

　

　

Since the 1980s, waters in Hong Kong and Southern China have suffered from occasional attacks of harmful algal blooms (HABs). An episode in 1998 resulted in a total loss of 350 million Hong Kong dollars in the aquacultural industry. While most HABs were triggered by special oceanographic and climatic conditions, microalgal biomass was closely related to nutrient supplies. Past research showed that dinoflagellate-caused HABs were associated with changes in N:P (atomic) ratio when the minimum concentration of 0.1 mg-N/L of TIN and 0.02 mg-P/L of DIP was reached. Recent findings indicate that interspecific competition between diatoms and dinoflagellates should not be overlooked. Silicate (Si), the limiting factor for diatom growth, has played a significant role in determining the dominant species and the magnitude of red tides. The Redfield Ratio should be critically reviewed in terms of its application to HABs dominated by dinoflagellates and the Si:N ratio should be considered in parallel with N:P ratios. Data from Tolo Harbour of Hong Kong show that dinoflagellate blooms are favored by N:P (atomic) ratio of 10-22 and Si:N (atomic) ratio <1; diatom blooms are favored by larger N:P and Si:N ratios; whereas micro-flagellate blooms often occur after collapse of diatom and dinoflagellate blooms. Therefore, besides discharges of domestic sewage and agricultural wastes, which contain a huge quantity of TIN and DIP, variation of Si input due to urbanization, soil erosion and river diversion should be considered.

　

　

Harmful algal blooms (HABs), which used to be known as red tide, are a global concern. Like other temperate and subtropical waters. Hong Kong and indeed the whole southern portion of China have been frequently affected by HABs since the 1980s. A total of 644 HAB incidents were recorded in Hong Kong waters particularly Tolo Harbour from 1980 to 2001 (Hong Kong Red Tide Information Network. 2002). In addition, 69 HABs/red tides occurred in other South China waters (Hodgkiss et al., 2001).

　

Harmful algal blooms often result in extensive fishkills in aquacultural zones. For example, a prolonged HAB in April - May 1998 caused around a 350 million Hong Kong dollars (〜42 million US dollars) loss in the local aquacultural industry (Lu and Hodgkiss, 1999). While a great deal of resources have been deployed in forecasting as well as mitigating HABs, the major formation mechanism and limiting factors have yet to be clarified by scientists. This paper presents analysis of the observed characteristics of HABs in Hong Kong waters and this information is anticipated to be useful in understanding the principal ecological processes of HABs in the coastal marine environment.

　

　

　

Of the various affected waters in Hong Kong, Tolo Harbour, a semi-enclosed embayment with a narrow outlet channel in the northeast of Hong Kong (Fig.1), have been extensively studied in terms of the causes and impacts of HABs (Holmes and Lam, 1985; Hodgkiss and Chan, 1987; Lam and Ho, 1989a and 1989b; Wong, 1989; Lam and Yip, 1990; Hodgkiss and Ho, 1992; Ho and Hodgkiss, 1993a and 1993b; Hodgkiss and Ho, 1997). In addition to tidal force and oceanic intrusion of water which carried vegetative cells into Tolo Harbour, salinity shock and the uniform meteorological conditions (cool temperature, overcast skies and low rainfall) in March to early May every year were believed to allow favorable growth of causative dinoflagellates during HABs (Lam and Yip, 1990; Yung et al., 1997). While nutrients (N, P) and micro-nutrients (ferric ions, Vitamins) are considered the major triggering and supporting factors of HAB (HO and Hodgkiss, 1991), interestingly, Holmes and Lam (1985) and Holmes (1988) showed the positive correlation between nitrogen loading increase in the watershed of Tolo Harbour and the increase in red tide incidents there. Extensive urban development, untreated domestic sewage and discharge of livestock wastes were considered the major contributors to increase nitrogenous compounds and phosphates in inner Tolo Harbour during the 1980s to early 1990s. Going one step further, Ho and Hodgkiss (1993b) and Hodgkiss and Ho (1997) reported that when the minimum concentration of 0.1 mg-N/L of TIN and 0.02 mg-P/L of DIP was reached, red tide occurrence in Tolo Harbour was highly possible. Furthermore, Hodgkiss and Ho (1997) revealed that the decline in annual mean N:P (atomic) ratio 1982 - 1989 in the surface water of Inner Tolo Harbour was often associated with increase in red tide incidents in the same year (Fig.2A). Their conclusions were generally agreed with the findings of Hodgkiss and Chan (1987), Chan and Hodgkiss (1987) and Huang et al. (1994) that a decline in N:P ratio in surface water usually resulted in dinoflagellates (the main red tide causative organisms) taking over dominance from the diatoms. Thus, the decline of annual mean N:P (atomic) ratios from around 20:1 in 1981 to 11:1 in 1990 reflected the change in phytoplankton community in Inner Tolo Harbour during the 1980s , when incidents of red tide peaked.

　

　

　

During the 1990s, the levels of TIN and DIP in the surface water of Inner Tolo Harbour were significantly reduced due to enforcement actions under the Water Pollution Control Ordinance of Hong Kong (Environmental Protection Department 1991-2001). While the frequency of red tide have also been reduced since 1991. Figure 2B shows that the association between decreases in N:P (atomic) ratio and increases in red tide incidents as shown in Figure 2A is nearly no changed. This confirms that red tide formation, which is mainly due to rapid dinoflagellates growth in the surface water of Inner Tolo Harbour, demands minimum (critical) concentrations of TIN and DIP and specific N:P (atomic) ratios. This conclusion is supported by bottle algal bioassay experiments (Hodgkiss and Ho, 1997) which showed that out of the 15 red-tide causative organisms studied in Tolo Harbour, eleven dinoflagellates were favored by N:P (atomic) ratios of 4-16 and only four were favored by N:P (atomic) ratios from 12-30 in the initial culture medium (Table 1). For Skeletonema costatum, a red-tide causative diatom, was favored by an N:P (atomic) ratio >24. The optimal N:P ratios in coastal diatoms and dinoflagellates are found to be different from the Redfield Ratio of 16:1 which has been applied to phytoplankton of open water (Redfield et al., 1963). The discrepancy is probably due to the adapting ability of phytoplankton to strong land-based discharge and salinity stress in estuarine and coastal environment.

　

　

While the relationship between N:P (atomic) ratios and HAB occurrences has been widely discussed, the related inter-specific competition within the phytoplankton community has not yet been comprehensively elaborated (HO and Hodgkiss, 1991). In fact, from the above conclusions regarding the relationship between N:P ratios and red tide occurrences at Tolo Harbour, it can be seen that diatoms and dinoflagellates are assumed to have a similar ecological niche in coastal marine waters and their strive for a nutrient supply similar too. Hence, it is not unexpected that strong biological competition occurs between diatoms, dinoflagellates and other small flagellates (including zooplankton) in the community. This hypothesis is supported by Figure 3, which records the population dynamics of diatoms, dinoflagellates and small flagellates during a red tide in Inner Tolo Harbour in March 2000. During most times of the year, diatoms are the dominant group within phytoplankton in Inner Tolo Harbour (Chan and Hodgkiss, 1987; Lam and Ho, 1989b). Nevertheless, as seen in Figure 3, when the seed population of Noctiluca scintillans began to bloom, the cell concentration of diatoms (dominated by Skeletonema costatum ) was significantly reduced, with dominance taken over by dinoflagellates. While the population of N. scintillans changed occasionally due to diurnal migration between surface and middle layers (Blasco, 1979; Ho, 1994), after one to two days the red tide caused by N. scintillans dissipated, and then, diatoms (mainly Skeletonema costatum ) resumed their dominance of the phytoplankton community. When both dinoflagellate and diatoms blooms were over small flagellates assumed dominance for a short period of time. A few days after this red tide event, diatoms resumed their normal dominance in Inner Tolo Harbour.

　

On the basis of observations and studies, HABs cannot be viewed solely as a chemical response by specific species of phytoplankton to supply of nutrients. Although nutrients are able to trigger and support HABs, the fundamental changes in phytoplankton dynamics are closely related to biological processes and ecological competition. Therefore, it is likely that HABs are actually a succession process in the coastal marine environment, where the dominance by diatoms, dinoflagellates and small flagellates (including zooplankton) is gradually taken over by each in turn.

　

　

It has been reported that dinoflagellates have a relatively slow growth rate, rarely exceeded one doubling per day (Karentz, 1983). Since diatoms are able to have 2-6 doublings per day, this can result in prolonged dominance of diatoms in marine and estuarine environments (Werner, 1977; Stoermer and Smol, 1999). As observed in Tolo Harbour, only when the available nutrients or environmental conditions changed, dinoflagellates take over the dominance (Lam and Ho 1989b). Thus, when the surface nutrient supply dwindled, diatoms receded in importance and dinoflagellates took up dominance because of their migrating ability between surface and middle layers and their different requirement for nutrients and N:P ratios (HO and Hodgkiss, 1991; Ho, 1994). Further studies on phytoplankton dynamics in relation to competition at genus and species levels should be considered in future HAB research.