Ecological Environment Changes in Daya Bay, China, from 1982 to 2004

Marine Pollution Bulletin 56 (2008) 1871–1879

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Marine Pollution Bulletin

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Ecological environment changes in Daya Bay, China, from 1982 to 2004

You-Shao Wang a,*, Zhi-Ping Lou a, Cui-Ci Sun a, Song Sun b a Key Laboratory of Tropical Marine Environmental Dynamics, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China b Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China article info abstract

Keywords: Data collected from 12 marine monitoring stations in Daya Bay from 1982 to 2004 reveal a substantial Daya Bay (DYB) change in the ecological environment of this region. The average N/P ratio increased from 1.377 in Ecological environment 1985 to 49.09 in 2004. Algal species changed from 159 species of 46 genera in 1982 to 126 species of Marine biological resources 44 genera in 2004. Major zooplankton species went from 46 species in 1983 to 36 species in 2004. The Mangrove plants annual mean biomass of benthic animals was recorded at 123.10 g m2 in 1982 and 126.68 g m2 in Coral reef 2004. Mean biomass and species of benthic animals near nuclear power plants ranged from Coastal protection 317.9 g m2 in 1991 to 45.24 g m2 in 2004 and from 250 species in 1991 to 177 species in 2004. A total of 12–19 species of hermatypic corals and 13 species of mangrove plants were observed in Daya Bay from 1984 to 2002. Ó 2008 Elsevier Ltd. All rights reserved.

1. Introduction of thermal plumes from nuclear power plants that discharge cool- ing water into the coastal zone. Variations in phytoplankton bio- Bays and estuaries are known to be biologically productive and mass and primary production in the western part of Daya Bay strongly inﬂuenced by human activities (Burger, 2003; Sohma during spring and summer have been reported (Song et al., et al., 2001; Tagliani et al., 2003; Zhao et al., 2005). Coastal bays 2004). Wang et al. (2006) used multivariate statistical analysis to are regions of strong land–ocean interaction. Their ecological func- reveal the relationship between water quality and phytoplankton tions are more complicated and vulnerable to human activity inﬂu- characteristics in Daya Bay, China, from 1999 to 2002. Wu and ences and land-source pollution than in the open ocean (Bodergat Wang (2007) used chemometrics to evaluate anthropogenic effects et al., 2003; Hansom, 2001; Huang et al., 2003; Yung et al., 2001). in Daya Bay and found that increases in human activity alter the With population increases and rapid economic development, lit- balance of nutrients in Chinese coastal waters. They also found that toral areas are facing many ecological problems. Eutrophication human activities were the main factor having an impact on the and environmental pollution obviously occur in many coastal sea ecological environment in Daya Bay (Wang et al., 2006; Wu and areas, especially in estuaries and coastal bays (Cloern, 1996; Turner Wang, 2007). and Rabalais, 1994; Yin et al., 2001). These have directly resulted in In this paper, monitoring and research data obtained from 1982 the ecological imbalance, biodiversity decrease, and rapid reduc- to 2004 are summarized and analyzed to understand the long-term tion of biological resources in estuaries and coastal bays. Coastal ecological environmental variations in Daya Bay. ecosystems, as well as the study of marine biological resources and the ecological environment, have attracted worldwide attention (Buzzelli, 1998; Fisher, 1991; Huang et al., 1989, 2003; Sohma 2. Research area, materials and methods et al., 2001; Souter and Linden, 2000; Zhang and Zhou, 1987; Zhang, 2001; Yung et al., 2001). Many international programs Daya Bay is a semi-enclosed bay. It is one of the largest and and projects have been launched to address problems confronting most important gulfs along the southern coast of China. Daya coastal ecosystems and biological resources in the world Bay is located at 113°2904200-114°4904200E and 23°3101200- (Yanez-Arancibia et al., 1999; Huang et al., 2003). 24°5000000N(Fig. 1). It covers an area of 600 km2, with a width of Tang et al. (2003) applied AVHRR data to the study of thermal about 15 km and a north–south length of about 30 km. About plumes from a power plant at Daya Bay. Satellite remote sensing 60% of the area in the Bay is less than 10 m deep (Xu, 1989; Wang can provide information on the distribution and seasonal variation et al., 2006). Dapeng Cove (location of station 3 in this work), in the southwest portion of Daya Bay, is about 4.5 km (N–S) by 5 km (E–W). Located in a subtropical region, the annual mean air tem- * Corresponding author. Tel./fax: +86 20 89023102. E-mail address: [email protected] (Y.-S. Wang). perature in Daya Bay is 22 °C. The coldest months are January

yuans in 1993 to 29.64 billion yuans in 2001. Total industrial output value of main towns along the Daya Bay coast increased 7.8 times between 1993 and 2001 (Table 2). The Daya Bay Nuclear Power Plant (DNPP) was the first nuclear power plant and the largest foreign investment joint project in China since 1982. It marks the first step taken by China toward the development of large- capacity commercial nuclear power units (Zang, 1993). Since 1993, sea water from the Daya Bay Nuclear Power Plant has been discharged at about 95 m3 s1 and a temperature of 65 °C. This warm water is placed in the south area of Daya Bay. Another nuclear power plant, called Lingao Nuclear Power Plant (LNPP), near the Daya Bay Nuclear Power Plant has also run since 2002. These changes can also have an impact on the ecological environment of Daya Bay (Bodergat et al., 2003; Wang et al., 2006; Wu and Wang, 2007; Zheng et al., 2001). A variety of ecological and environmental factors in Daya Bay have been monitored since 1982. A total of 12 stations were monitored during four voyages each year. All stations were located between 113°2904200-114°4904200E and 23°3101200-24°5000000N. The main marine monitoring investigation included assessment of the ecological environment, the ecological function of marine biological resources and the community organization in Daya Bay. Water temperature and salinity were measured in the field using CTD probes. Seawater samples were taken for the analysis of nutrients, dissolved oxygen, pH, chemical oxygen demand, and chlorophyll a. These were collected using 5-L GO FLO bottles at both Fig. 1. Map of Daya Bay and locations of the 12 monitoring stations Wang et al. surface and bottom layers. Other samples were collected according (2006). to the methods and sampling tools described in ‘‘The specialties for oceanography survey” (GB12763-91, China). All sample analyses and February, having a monthly mean air temperature of 15 °C, and were carried out at the National Field Station of Marine Ecosystem the hottest months are July and August, having a monthly mean air Research and Observation in Daya Bay, Shenzhen, China and at the temperature of 28 °C. The minimum sea surface temperature oc- South China Sea Institute of Oceanology, Chinese Academy of Sci- curs in winter (15 °C), while the maximum occurs in summer ences. Analytical methods for the various physical–chemical and and fall (30 °C) (Xu, 1989; Wang et al., 2006). No major rivers dis- biological parameters were applied according to Huang et al. charge into Daya Bay and most of its water originates from the (2003) and Wang et al. (2006). South China Sea. There are three small rivers (Nanchong River, All samples were collected during one day at the beginning of Longqi River and Pengcheng River) that discharge into Dapeng the first month for each season (spring-summer-fall-winter). Sam- Cove. The Pearl River is to the west of Daya Bay and has diverse ples (except phytoplankton, zooplankton, benthos and fish) in- subtropical habitats, including coral reefs, mangroves, rocky and cluded those taken at the Daya Bay surface and bottom. Data for sandy shores, mudflats, etc. The coral reefs and mangroves have this paper are given as mean values between the surface and special resource values and ecological benefits. These are very bottom. important to sustainable social and economic development in these subtropical coastal areas. Coral reefs and mangrove areas have important relationships to the regulation and optimization 3. Results of subtropical marine environments and have become the subject of much international attention in recent years (Mumby et al., Seasonal variations in temperature and salinity at Daya Bay 2004; Pearson, 2005). from 1982 to 2004 are shown in Figs. 2 and 3. The annual mean Relatively few residents and industries were located along the temperature was 24.04 °C, based on data measured from 1982 to coast of Daya Bay prior to the 1980s. At present, there are about 2004. The highest surface and bottom water temperatures oc- 239,400 inhabitants living along the coast of Daya Bay (Table 1). curred in August and the lowest values were in January (Wang The population has nearly doubled from 1986 to 2002. Many facto- et al., 2006). The temperature of western Daya Bay, near the nucle- ries were built in this time. The total industrial output value of ar power plants, was higher by about 1 °C than in other areas of main towns along the Daya Bay coast increased from 3.804 billion Daya Bay. This is mainly due to warm waste water that is dis-

Table 1 Population changes for main towns along the Daya Bay coast (unit, ten thousands)

Year Xiachong Aotou Xunliao Nianshan Pinghai Gangkou Yanzhou Dapeng Total 1986 1.22 1.66 0.58 4.93 2.74 1.93 1.27 0.57 14.90 1989 1.24 1.94 0.62 5.18 2.90 2.00 1.40 0.66 15.94 1993 1.95 2.20 0.75 5.76 3.02 2.10 1.37 – 17.15 1995 1.95 1.35 0.78 6.01 3.09 2.13 1.40 2.58 19.29 1998 2.11 2.79 0.85 6.27 3.26 2.13 1.42 3.95 22.78 2002 2.19 2.99 0.88 6.35 3.44 2.11 1.48 4.50 23.94 Main annual increase 4.68% 4.71% 3.04% 1.69% 1.50% 0.549% 0.973% 40.6% 3.57% Y.-S. Wang et al. / Marine Pollution Bulletin 56 (2008) 1871–1879 1873

Table 2 Total industrial output values for main towns along the Daya Bay coast in different years (unit, ten thousands yuans)

Year Xiachong Aotou Xunliao Nianshan Pinghai Gangkou Yanzhou Dapeng Total 1993 1140 2942 192 9351 3226 5027 286 15,875 38,039 1995 2523 5040 388 21,483 8937 10,396 969 – 49,736 1998 6428 17,035 701 40,600 25,813 30,257 1880 47,500 170,214 2001 4744 17,568 860 71,191 50,532 56,371 3224 91,900 296,390 Mean annual increase 35.13% 55.24% 38.66% 73.48% 162.9% 113.5% 114.1% 53.21% 75.46%

40 35

35 30

30 25

25 20

20 15 Temperature,ºC Salinity 15 10 10 5 5 0 1996 1998 1999 2000 2001 2002 2003 2004 Mean 0 1982 1987 1991 1998 1999 2000 2001 2002 2003 2004 Mean Year Year Spring Summer Autumn Winter Mean Spring Summer Autumn Winter Mean Fig. 4. Temperature of western Daya Bay with different seasons from 1996 to 2004 (Unit, °C). Fig. 2. Salinity of Daya Bay with different seasons from 1982 to 2004 (Unit, ‰).

10 35 9 30 8 7 25

-1 6 20 5

15 DO, mgl 4

Temperature, ºC Temperature, 3 10 2 5 1 0 0 1982 1985 1991 1998 99919992000 2001 2002 2003 2004 Mean 1982 1987 1991 1996 1998 1999 2000 2001 2002 2003 2004 Mean Year Year Spring Summer Autumn Winter Mean Spring Summer Autumn Wnter Mean Fig. 5. Dissolved oxygen of Daya Bay from 1982 to 2004 (Unit, mg l1). Fig. 3. Temperature of Daya Bay with different seasons from 1982 to 2004 (Unit, °C).

within the National First Class Water Quality Standards for China charged in southern Daya Bay by nuclear power plants (Fig. 4) (Wang et al., 2003)(Table 3). The nutrient P decreased from (Wang et al., 2006). 1.12 lmol l1 to 0.110 lmol l1 in the period from 1985 to 2004 The spatial distribution of dissolved oxygen (DO) in Daya Bay in Daya Bay, probably as a result of fan-used detergency powder was as uniform as the temperature. Seasonal variations were evi- (contains P) in recent years. The average ratio of TIN/P increased dent from 1982 to 2004 (Fig. 5). Annual mean pH variations were from 1.377 in 1985 to 49.09 in 2004 and the highest value was from 8.15 to 8.25 during 1982 to 2004, with little observable 61.90 in 2003. The average ratio of Si/P increased from 35.27 in change in Daya Bay (Fig. 6). Chemical oxygen demand (COD) values 1985 to 285.82 in 2004. were 0.63 to 1.18 mg l1 in Daya Bay from 1989 to 2004 (Fig. 7). About 300 species of phytoplankton have been identiﬁed in Inorganic N and P levels were low, from 1.53 lmol l1 to Daya Bay since 1982. They belong to Cyanophyta, Bacillariophyta, 5.40 lmol l1 and from 0.0945 lmol l1 to 1.12 lmol l1. Mean Pyrophyta, Chrysophyta and Xanthophyta, among others. Most of values were 3.68 lmol l1 and 0.266 lmol l1 from 1985 to 2004, them are diatoms (about 70%) and chaetocero (about 20%). Of the 1874 Y.-S. Wang et al. / Marine Pollution Bulletin 56 (2008) 1871–1879

8.5 ima, Leptocylindrus danicua, Skeletonema costatum and Thalassio- nema nitzschioide. The chaetocero has Ceratium sp. as the 8.4 dominant species. Phytoplankton species have been gradually decreasing since the 1990s when compared to the 1980s (Table 8.3 4). In particular, there were only 80 species in 1998. The phyto- 8.2 plankton cell density has also been gradually decreasing since 1998, when compared with 1985. Annual mean values of phyto- 8.1 plankton in Daya Bay were between 8.88 105 and pH 6.63 107 cells m3 from 1985 to 2004. Phytoplankton abundance 8 peaked in spring, reaching 1.03 108 cells m3 in 1985 (Table 5), and was lowest in spring, at 7.30 104 cells m3 (1/1411), in 1999. 7.9 Two hundred sixty five species of zooplankton from Daya Bay 7.8 have been studied since 1982. They can be divided into four ecological forms: estuary, inner bay, warm coastal and warm open 7.7 sea types (Lian et al., 1990). The latter two types account for most 1982 1986 1991 1998 1999 2000 2001 2002 2003 2004 Mean species. Variations in dominant species exhibited a seasonal suc- Year cession. The abundance of zooplankton varied seasonally, with Spring Summer Autumn Winter Mean the maximum number of individuals occurring in autumn. Main zooplankton species in Daya Bay showed a decreasing trend from Fig. 6. pH of Daya Bay with different seasons from 1982 to 2004. 46 of 60 familiar species in 1983 to 36 of 60 familiar species in 2004 (Fig. 8). However, the annual mean individual number of zooplankton has been gradually increasing from 55.42 ind m3 to 1.4 384.05 ind m3, since 1998, and the value in 2004 already exceeds 1.2 the 352.70 ind m3 level for 1985 (Table 5). A total of 328 species of fish were captured from 1985 to 2004 1 and 304 species of fishes were identified. These included many edi-

-1 ble species of high economic value, such as Sardinella jussieu Clu- 0.8 panodon punctatus, Nematalosa nasus, Thrissa setirostris, Thrissa 0.6 dussumieri, Thrissa kammalensis, Thrissa hamiltonii, Thrissa vitiros-

COD, mgl tris, Harpodon nehereus, Plotosus anguillaris, Lactarius lactarius, Car- 0.4 anx (atule) kalla, Pseudosciaena arocea, Leioganthus rivulatus, Pagrosomus major, Rhabdosargus sarba, Siganus oramin, Trichiurus 0.2 haumela, Stromateoides argenteus, Stromateoides nozawae, Stroma- 0 teoides sinensis and Lagocephalus lunaris spsdiceus. The dominant 1989 1992 1998 1999 2001 2002 2003 2004 Mean species were perciformes, including the warm water and warm Year and temperate water species. These accounted for about 90% and 10% in Daya Bay, respectively. Main fish were about 20–28 species Fig. 7. Chemical oxygen demand of Daya Bay from 1989 to 2004 (Unit, mg l1). of the 47 main fish species captured in Daya Bay from 1985 to 2004 (Fig. 9). Though the main fish species experienced a small change Table 3 in Daya Bay from 1985 to 2004, the amount of edible fish as a nat- Concentrations of different forms of N, SiO3–Si and PO4–P in Daya Bay from 1985 to ural resource has decreased greatly from 1985 to 2000. The mean 1 2004 (Unit, lmol l ) individual weight of fish changed from 14.60 g tail1 in 1985 to þ 2 3 1 Year NH4 NO2 NO3 TIN SiO3 PO4 TIN/P Si/P 10.80 g tail in 2004 (Table 6). 1985 0.698 0.230 0.602 1.53 39.50 1.12 1.377 35.27 Daya Bay has a high diversity of natural habitats, with more 1989 0.607 1.10 1.52 3.23 10.85 0.377 8.560 28.78 than 700 species of benthos found by mud sampling and trawling 1991 1.10 0.230 0.798 2.13 20.66 0.358 5.950 57.71 since 1982 (Xu, 1989). Benthic plants were less than 10%, including 1997 1.38 0.150 2.55 4.08 14.57 0.122 33.44 119.43 about 60 species of diatoms, which represented the main benthic 1998 1.86 0.0554 0.433 2.35 5.125 0.0405 57.99 126.54 plants. Benthic animals were more than 90%. Besides a very few 1999 1.99 0.389 2.46 4.84 9.810 0.118 40.02 76.46 2000 1.59 0.508 1.92 4.01 27.54 0.252 15.91 109.29 species, benthic animals in Daya Bay were almost all warm water 2001 2.28 0.134 1.93 4.33 23.21 0.229 18.91 101.35 species, with relatively few individuals. The annual mean bio- 2002 1.32 0.446 0.680 2.40 27.01 0.0945 25.40 285.82 masses of benthic animals ranged from 55.70 g m2 to 2003 2.54 0.260 3.39 6.19 23.06 0.100 61.90 230.60 148.91 g m2 between 1982 and 2004 (Table 7). The lowest mean 2004 3.06 0.085 2.25 5.40 12.82 0.110 49.09 116.54 biomass of benthic animals in Daya Bay was found to occur during Mean 1.68 0.326 1.68 3.68 19.47 0.266 28.96 117.07 between 1990 and 1997, which was the period of largest foreign *Quality standards of seawater from GB3097-1997; TIN, China first class investment along the Daya Bay coast (Zang, 1993; Wang et al., 1 6 1 6 (lmol l ) 14.28, second class (lmol l ) 21.43; PO4–P, China first class 2006; Tang et al., 2003). Annual mean biomasses of benthic ani- 1 6 1 6 (lmol l ) 0.4839, second class (lmol l ) 0.9677. mals have increased between 1990 and 2004. In recent years they have also reached 1980 levels. The highest biomass (1326 g m2) was collected in the north region of Daya Bay in the spring of 183 species of diatoms, chaetoceros has many more species than 1982. Polychaeta (about 150 species account for about 21%) and other genera (45 spp.), followed by Rhizosolenia (23 spp.) and Cos- mollusks (about 148 species accounted for about 21%) were the cinodiscus (22 spp.) (Yang, 1990). The main dominant species of dominant groups, followed by crustacea (about 130 species ac- Daya Bay are Chaetoceros, Nitzschia, Rhizosolenia, Leptocylindrus counted for about 18%) and echinoderms (about 52 species ac- and Skeletonema, such as Chaetoceros affinis, Chaetoceros compres- counted for about 7%). The rest (about 13%, such as Spongia, sus, Chaetoceros lorenzianus, Chaetoceros Curvisetus, Chaetoceros Coelenterata, Bryozoa and Nemertinea, etc.) exhibited the lowest Pseudocurvisetus, Rhizosolenia alata f.grecillisma, Nitzschia delicatiss- biomass. Seventy three species of ground fish (accounting for about Y.-S. Wang et al. / Marine Pollution Bulletin 56 (2008) 1871–1879 1875

Table 4 Species and genera of phytoplankton in Daya Bay from 1982 to 2004

Phylum 1982 1983 1985 1987 1990 1994 1998 2002 2003 2004 Bacillariophyta 37/134 38/120 38/127 41/137 37/140 25/78 24/72 25/96 31/92 34/100 Pyrophyta 9/25 9/32 8/30 8/27 17/61 10/30 5/8 9/27 12/30 8/23 Cyanophyta 0 1/3 1/3 2/4 2/5 1/2 0 2/4 2/3 2/3 Total (genera /species) 46/159 48/155 49/160 51/168 56/206 36/110 29/80 36/127 46/125 44/126

Table 5 Seasonal production measurements in Daya Bay from 1985 to 2004

Seasons Production 1985 1998 1999 2000 2001 2002 2003 2004 Spring Chl a (mg m3) 2.06 1.46 2.00 0.979 1.49 0.830 5.88 1.94 Phytoplankton (cells m3) 1.03 108 2.16 107 7.30 104 5.27 106 6.59 105 1.71 106 1.53 105 3.43 106 Zooplankton (ind m3) 109.20 28.90 – 90.00 34.97 135.29 137.58 204.67 Summer Chl a (mg m3) 2.36 1.44 3.44 4.07 1.32 6.09 1.91 3.93 Phytoplankton (cells m3) 9.61 107 7.59 105 6.28 105 5.25 107 9.31 105 1.87 106 2.45 106 1.66 107 Zooplankton (ind m3) 578.90 82.70 – – 404.08 248.62 191.97 131.33 Autumn Chl a (mg m3) 1.19 3.50 4.69 3.46 2.25 2.82 1.44 1.67 Phytoplankton (cells m3) 1.53 107 6.00 106 1.02 106 3.86 105 5.63 105 3.70 105 1.99 105 3.49 105 Zooplankton (ind m3) 523.90 43.65 – – 131.11 258.80 58.41 581.15 Winter Chl a (mg m3) 1.70 1.77 5.01 1.85 2.81 2.98 3.32 2.06 Phytoplankton (cells m3) 3.77 107 6.73 106 1.83 106 8.49 104 2.74 106 6.21 105 2.24 106 3.63 106 Zooplankton (ind m3) 189.30 66.41 94.72 – 204.16 455.54 309.32 619.05 Mean Chl a (mg m3) 1.83 2.04 3.78 2.63 1.97 3.18 3.14 2.40 Phytoplankton (cells m3) 6.30 107 8.77 106 8.88 105 1.46 107 1.22 106 1.14 106 1.60 106 6.00 106 Zooplankton (ind m3) 352.70 55.42 94.72 90.00 193.58 283.56 174.32 384.05

10%) were captured in Daya Bay between 1982 and 2004. Seasonal variations in biomass showed similar trends, with a maximum dur- 60 ing winter and spring and a minimum during autumn and summer, from 2001 to 2002 (Table 8). The maximum biomass in the year oc- 50 curred mainly at the northeast and middle parts of Daya Bay, which were living areas of mollusks (Xu, 1989). The mean biomass 40 of benthic animals in western Daya Bay (near nuclear power plants) has decreased from 317.7 g m2 in 1991 to 45.24 g m2 in 30 2004 (Table 9) and the number of benthic animal species has also Species decreased since 1993 (Fig. 10). 20 On coral reefs, hermatypic corals are concentrated in the vicin- ity of Dalajia, Xiaolajia and westward in the mouth of Daya Bay, lo- 10 cated at the northern edge of the global coral reef zone. Based on data collected in 1983 and 1984, there were formerly at least 19 0 1983 1987 1990 1994 1998 2002 2003 2004 coral species in Daya Bay (not including the Haotou harbour), Year accounting for 76.4% of the hermatypic coral from Dalajia and Xiaolajia to the mouth of the bay (Zhang and Zhou, 1987), with Fig. 8. Main species of familiar zooplankton in Daya Bay changed from 1983 to Acropora pruinosa (Brook) as the dominant species. Only approxi- 2004. mately 12–16 species were found between 1991 and 2002, accounting for 32% (Wen et al., 1996) and 36% of total cover rate for the hermatypic coral (Table 10). There has been a shift in the dominant species since the 1990s. For example, the dominant spe- 30 cies were Favites abdita (Ellis & Solander) in 1991 and Platygyra daedalea (Ellis & Solander) in 2002, which was 7.4% of the herma- 25 typic coral for its total cover rate. 20 Mangrove plants grow along the coast of Daya Bay, such as in Aotou, Nianshan, Dongshan, Sanmen Island and Dalajia Island. 15 Species 10 Table 6 Mean individual weight of ﬁsh (g tail1) changed from 1985 to 2004

5 Year April May October December Mean 1985 9.70 6.30 27.80 14.60 0 1987 2.85 4.16 1.92 2.98 1985 1987 1991 1996 2000 2004 1996 1.08 2.51 7.39 3.66 Year 2000 2.28 2.28 2004 10.80 10.80 Fig. 9. Main species of ﬁsh in Daya Bay from 1985 to 2004. 1876 Y.-S. Wang et al. / Marine Pollution Bulletin 56 (2008) 1871–1879

Table 7 Mean biomasses of benthic animals in Daya Bay from 1982 to 2004 (Unit, g m2)

Year 1982 1987 1990 1996 1997 1998 2001 2002 2004 Biomass 1.9–1326 1.5–1210 5.5–99 0.1–1197 0.4–823 2–1122 0–1236.6 0–1152 2.6–506.9 Mean 123.1 123.6 55.70 74.20 78.60 152.80 148.91 117.71 126.68

Table 8 1000 Seasonal variation in biomasses of benthic animals in Daya Bay changed from 2001 to 2002. (Unit, g m2)

Year Spring Summer Autumn Winter 2001 256.18 88.05 47.10 248.77 2002 96.11 14.11 64.98 279.53 100

There were 13 species in this area, belonging to 13 different fami-

lies (Chen et al., 1999; Zhong et al., 1999). Some herbaceous and Species number 10 ornamental vines were present in the mangrove plants of Daya Bay, such as Cyperusmalaccensis, Derristktrifoliata, Canavliamariti- ma, Ipomoeapescaprae, Plucheaindica, Sporobolusirginicus and Scavo- lahinanensis. Dominant species were Kandelia candel, Bruguiera 1 gymnorrhiza, Aegiceras corniiculatum and Avicennia marina. Also, 1987 1989 1991 1993 1997 2000 2004 Ceriops tagal, Lumnitzera eacemosa, Rhizophora stylosa are gradually Year being deracinated (Chen et al., 1999). They now cover only 4% in Polychaeta Mollusca Crustacea Echinodermala some areas (such as in Baisha Bay of the northwest part of Daya Groundfish Bay) as compared to 60–90% in the 1950s, which mainly consisted Others Total number of small shrubs and bushes. Fig. 10. Number of benthic animal species of western Daya Bay from 1987 to 2004.

4. Discussion

Table 10 The spatial distribution of water temperatures showed high val- Investigation results of hermatypic coral from 1984 to 2002 ues in the western region, near nuclear power stations, and low values in the mouth of Daya Bay for all analyzed years. Stratifica- Year 1984 1991 2002 tion due to temperature and salinity differences between surface Total species/total cover rate (%) 19/76 12/32 16/36 and bottom waters inside the bay began to develop in June, became strongest from July to September, and disappeared in November. Temperature and salinity were uniformly distributed with depth from November to May in the following year (Xu, 1989; Wang power plant was 1 °C warmer than the surrounding seawater, then et al., 2004). the affected area of Daya Bay was about 5.51 km2 (Han, 1991; Cold-water upwelling influenced the distribution of nutrients Wang et al., 2006). and temperature, as well as their fluctuations in Daya Bay. Vertical Distributions of dissolved oxygen in spring and winter were and seasonal variations, as well as the distribution of water tem- higher than in summer and autumn. The highest dissolved oxygen peratures, suggest that the bay is affected by the East Guangdong content occurred in winter and the lowest in summer. There was a upwelling and a thermocline occurring during June–August (Han, decrease from 7.29 mg l1 to 7.03 mg l1 of dissolved oxygen from 1991; Wang et al., 2006). During this time, the thermocline tem- 1991 to 2002. This is probably due to progressive increases in the perature gradient averaged 0.5–1 °Cm1. Depths of the thermo- sea surface temperature of Daya Bay (Fig. 3). Although results indi- cline were about 6–10 m with a thickness of approximately cate there was a small decreasing trend in dissolved oxygen (DO), 2–4 m in Daya Bay (Wang et al., 2006). The thermocline disap- the seawater of Daya Bay was also within the First Class of National peared from November to the following May, owing to seawater Seawater Quality Standards for China (6.00 mg l1, GB3097-1997) mixing. (Wang et al., 2003). Annual mean temperatures increased from 1982 to 2004, prob- The mean chemical oxygen demand values were lower than for ably owing to global change. Climate change scenarios for the year other sea areas in China, such as the COD between 2.90 mg dm3 2100 indicate a significant increase in air temperature (by 2.3– and 7.50 mg dm3 in the Pearl River Estuary (Lin and Li, 2003) 4.5 °C), which is a major factor that influences the Gulf environ- and from 3.32 mg l1 to 4.01 mg l1 in Rongcheng Bay, which is ment (Kont et al., 2003). Nuclear power plants have a direct impact in a temperate zone (Mu et al., 1999). The chemical oxygen de- on the ecological environment of Daya Bay (Zheng et al., 2001). mand values also indicate that organic pollution in Daya Bay was Assuming that the waste water temperature from the nuclear much lower than for other sea areas in China. The results of chem-

Table 9 Mean biomasses of benthic animals of western Daya Bay from 1991 to 2004 (Unit, g m2)

Year 1991 1993 1994 1996 1996 1997 1998 2001 2002 2004 Biomass 0.4–1651 0.4–254.1 0.1–120.8 0.1–117.5 0.1–158.0 0.4–113.0 4.4–1222 0–197.7 0–115.6 20.6–76.6 Mean 317.9 82.00 26.60 25.60 28.60 25.80 21.4.3 34.15 28.84 45.24 Y.-S. Wang et al. / Marine Pollution Bulletin 56 (2008) 1871–1879 1877 ical oxygen demand in Daya Bay show that the sea water was also eral weeks, about 90-95% of coral will die (Zhang, 2001). The her- within the First Class of National Seawater Quality Standards for matypic coral of Daya Bay had a small recovery from 1991 to 2002. China (62.00 mg l1, GB3097-1997) (Wang et al., 2003). The increased temperature of Daya Bay, being associated with glo- These results of inorganic N and P levels are similar to Mirss Bay bal changes and warm water from nuclear power plants, may also in Hong Kong (Yin, 2003). NH4–N (about 49%) and NO3–N (about be other reasons for the observed decrease in cover rate for herma- 43%) were the dominant total inorganic nitrogen (TIN) forms, which typic coral in Daya Bay (Zheng et al., 2001). accounted for about 90% of the TIN and 8% of NO2–N in recent years. A number of mangrove plants were felled to create farmland in 2 The NO3–N content was lower than NH4–N, revealing a thermody- the 1970s. At present, mangrove plants cover about 850 hm along namic imbalance between NH4–N, NO2–N and NO3–N. Biological the Daya Bay coast. In recent years, mangrove plants were again activity might also be a main factor influencing the balance (Huang seriously destroyed and this phenomenon was accompanied with et al., 2003), but there were different degrees of NH4–N transforma- aquatic culture, travel and economic development (Xue, 2002; tion for different bay regions. The concentration of both N and Si Hens et al., 2000; Zorini et al., 2004). were higher than inorganic P. Spatially, the nutrient N increased Obviously the coral reefs, including hermatypic corals and man- from 1985 to 2004 in Daya Bay, probably as a result of waste water grove plants, in Daya Bay have been seriously degraded and de- from people living along the coast, land-sources (such as Nanchong stroyed since the 1970s and 1980s. We need to make a much River, Longqi River and Pengcheng River discharges into Dapeng greater effort to protect these diverse resources to maintain their Cove and nuclear power plant waste water discharges into the ecological function. south area of Daya Bay), seawater breed aquatics, and the effect of water from the Preal River on Daya Bay (Han, 1991). Limiting nutrients in Daya Bay have changed from N to P between 1985 5. Conclusions and 2004 (Justice et al., 1995). These were different from those at Jiaozhou Bay, which shifted from N and/or P to Si from the 1960s Daya Bay has a rich biodiversity, including a multi-type ecosys- to the 1990s in the temperate zone (Shen, 2001), and Sanya Bay, tem that has coral reefs, mangroves and rock reefs. It is a good which shifted from N in summer and autumn to P in winter in Sanya place for the reproduction and culturing of fish, shrimp, crabs Bay from 1998 to 2000 in the tropic zone (Huang et al., 2003). and shellfish. Owing to constant interaction between land and Although the mean annual abundances of phytoplankton ocean areas, its ecology is more complicated and vulnerable than showed a slightly decreasing trend from 1999 to 2004, species that of the open sea. It is especially vulnerable to the effects of fre- and values of phytoplankton in Daya Bay were increasing. This quent human activity and land-based pollution. Despite the pro- may be due to high ratios of TIN to P and Si to P occurring in recent gressive increase in human activities, including more domestic years (Sommer et al., 2002). Annual mean values of chlorophyll a sewage and industrial waste water discharge as well as nutrient were 1.83–3.78 mg m3 in different seasons from 1985 to 2004, enrichment and toxins derived from the cage culture of fish and with the higher values always being found in autumn and summer. seashells, the concentrations of N, P, DO and COD must not be al- The nutrient structure has become more balanced for phytoplank- lowed to exceed water quality standards at the risk of serious eco- ton growth (Shen, 2001; Olivieri and Chavez, 2000). system degradation. Concentrations are still within the First Class The annual mean individual number of zooplankton has been of National Seawater Quality Standards for China. Temperatures gradually increasing since 1998. One reason might be the strictly of seawater in Daya Bay were increasing from 1982 to 2004, prob- enforced regulations relating to the marine environment and fish- ably due to global changes. The average ratio of N/P increased from eries from June to August in each year since 1995. Another reason 1.377 in 1985 to 49.09 in 2004 and the limiting factor of nutrients might be high levels of plant nutrients and high ratios of Si to N changed from N to P. Changes in the composition of the biological and P. Most phytoplankton has fallen into the food spectrum of community have been small, with biodiversity becoming simpli- herbivorous, crustacean zooplankton in recent years (Sommer fied and the biological natural resources declining. For example, et al., 2002; Sommer and Lengfellner, 2008). phytoplankton species decreased from 206 species of 56 genera Although a policy to ban fishing in the China Sea was put into in 1990 to 126 species of 44 genera in 2004. The main species of practice from July to August since 1995, the amount of the fish nat- zooplankton in Daya Bay have decreased from 46 species in 1983 ural resource has recovered slowly because of excessive catching to 36 species in 2004. The mean individual weight of fish has chan- and pollution. This is especially true for the time period between ged from 14.8 g tail1 in 1985 to 10.80 g tail1 in 2004. The waste 1987 and 2000. The investigation data show that Daya Bay has a warm water from nuclear power plants was the main factor influ- sandy bottom with coral reefs and an environment suitable for encing the ecology and environment in western areas of Daya Bay. growth. Fish resources are abundant as compared to those in other This is particularly true for the benthos, which were a directly im- China bays that have less suitable environments. For example, pacted marine organism. Many changes have taken place in Daya there were only 91 species in Jiaozhou Bay in the temperate zone Bay from 1982 to 2004, such as stony coral bleaching and changes of China (Zhou, 1984). in dominant species of the coral community, as well as seriously These results for the mean biomasses and species of benthic degraded and destroyed mangrove plants. These results indicate animals indicate that warm water from the Daya Bay Nuclear that the ecosystem of Daya Bay is undergoing a rapid deterioration Power Plant (since 1993) and Lingao Nuclear Power Plant (since in some areas and in some aspects. At the same time, some aspects 2002) have great effects on this area’s ecology and environment. of its ecological environment were recovering due to strategic pro- This is particularly true for the benthos, which were directly im- tection and management steps for the protection and management pacted marine organisms (Zheng et al., 2001). of coastal marine ecosystems in China. For example, the annual Hermatypic corals were demolished from 1984 to 2002, some of mean biomasses of benthic animals increased from 72.40 g m2 which were destroyed by humans (Wen et al., 1996; Souter and in 1996 to 1126.68 g m2 in 2004 and the nutrient P decreased Linden, 2000; Bellwood et al., 2004) using methods such as bomb from 1985 to 2004. Daya Bay is a multi-type ecosystem mainly dri- fishing, underwater coral reef sightseeing and exploitation of coral ven by human activities (Wang et al., 2006; Wu and Wang, 2007). reef for financial gain. One kind of sensitivity that marine biology Regional coordination in the protection and management of such demonstrates is toward water temperature and coral bleaching is vulnerable coastal marine ecosystems should be strengthened. related to increases in water temperature (Souter and Linden, The following strategic protection and management steps are rec- 2000). If the seawater temperature increases by 0.5–1.5 °C in sev- ommended: (i) Enhance information dissemination and education 1878 Y.-S. Wang et al. / Marine Pollution Bulletin 56 (2008) 1871–1879 to improve environmental protection awareness for people in the C.C.C., Llewellyn, G., 2004. Mangroves enhance the biomass of coral reef fish region; (ii) Strengthen the long-term monitoring of the marine communities in the Caribbean. Nature 427, 533–536. Olivieri, R.A., Chavez, F.P., 2000. A model of plankton dynamics for the coastal environment and coastal ecosystems in Daya Bay, enhance the re- upwelling system of Monterey Bay, California. Deep-Sea Research II 47, 1077– search of regional environmental capacity, and use that capacity to 1106. establish large-scale control of pollutant discharges; (iii) Promote Pearson, H., 2005. Scientists seek action to fix Asia’s ravaged ecosystems. Nature 433, 94. the protection of coral reefs, mangroves, the coastal ecosystem Shen, Z.-L., 2001. Historical changes in nutrient structure and its influences on and regional biodiversity by carrying out scientific plans for re- phytoplankton composition in Jiaozhou Bay. Estuarine, Coastal and Shelf source-use based on marine system functions; (iv) Strictly enforce Science 52, 211–224. Sohma, A., Sekiguchi, Y., Yamada, H., Sato, T., Nakata, K., 2001. A new coastal Marine regulations relating to the marine environment and fisheries from ecosystem model study coupled with hydrodynamics and tidal flat ecosystem June to August in each year; (v) Carry out more research concern- effect. Marine Pollution Bulletin 43 (7–12), 187–208. ing warm waste water from nuclear power plants and its effect on Sommer, U., Stibor, H., Katechakis, A., Sommer, F., Hansen, T., 2002. Pelagic food web configurations at different levels of nutrient richness and their implications for the ecosystem of Daya Bay. the ratio fish production: primary production. Hydrobiologia 484 (1–3), 11–20. 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