Annual variability of ichthyoplankton in the Yangtze River estuary of China from August 2002 to 2009

Oceanological and Hydrobiological Studies I n t e r n a t i o n a l J o u r n a l o f O c e a n o g r a p h y a n d H y d r o b i o l o g y

Volume 42, Issue 1

ISSN 1730-413X (59–69)

eISSN 1897-3191 2013

DOI: 10.2478/s13545-013-0060-4

Original research paperReceived: Accepted:

October 14, 2011September 08, 2012

Copyright© of Institute of Oceanography, University of Gdansk, Poland www.oandhs.org

Annual variability of ichthyoplankton in the Yangtze River estuary of China from August 2002 to 2009 Jiang Mei*, Shen Xin-Qiang, Li Lei, Quan Wei-Min East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key & Open Laboratory of Marine and Estuary, Ministry of Agriculture of China, Shanghai, 200090, China Key words: ichthyoplankton; abundance; composition; August; Yangtze River estuary

Abstract

The annual variability of ichthyoplankton in the Yangtze River estuary, located at the junction of the East China Sea and the Yellow Sea, on the continental shelf at the western rim of the Pacific Ocean, was studied using vertical tows at twenty stations from August 2002 to August 2009. Basic oceanographic parameters such as temperature and salinity were also measured to evaluate their relationship to the abundance of ichthyoplankton. The eggs or larvae of a total of 34 fish species were present in the samples. Only 8 species were found to occur during every year. Engraulis japonicus and Stolephorus commersoniieggs, as well as Coilia mystus and Stolephorus commersonii larvae, were highly abundant during this period. Additionally, water storage in the Three Gorges Reservoir, which began in June 2003, had significant effects on the abundance of estuarine species, as well as on the composition and diversity of ichthyoplankton; this became evident when these values were compared to the findings from 2002. The number of species (species richness) and abundance of each species varied among the stations relative to the salinity in the estuary during the study period.

* Corresponding author e-mail address: [email protected]

INTRODUCTION

Estuaries and coastal lagoons are known to be prime spawning and nursery areas for littoral and shelf fish populations because of their shallow areas and habitats offering suitable food, shelter, and ecophysiological conditions for eggs, embryos, larvae, and juvenile fish development (Blaber & Blaber 1980, Aimeer et al. 1999, William et al. 1990, Doreen 1992, Kimmerer 2002, Andrés et al. 2004). Larval fish assemblages are temporary components (meroplankton) of the zooplankton community, the structure of which is ultimately dependent upon reproductive cycles within populations of adult fish (Antonia et al. 2010, Hasan et al. 2003, Lanksbury et al. 2005). Ichthyoplankton studies are an important tool for providing information for ichthyology, environmental inventory, stock monitoring, and fisheries management (Rogério et al. 2010). Their quantity distribution and dynamics play important roles in maintaining the equilibrium of estuary ecosystems. There have been many studies of ichthyoplankton in the Yangtze River estuary of China (E Pacific), but most of these published studies encompassed only a few particularly commercially important species such as Engraulis japonicus, Scomber japonicus, Trichiurus lepturus, and Argyrosomus argentatus (Wan et al. 2010). Some studies have described the entire species assemblage (Liu et al. 2007), but sampling was restricted to one annual cycle. Other studies from the Yangtze River estuary and vicinity waters (Jiang et al. 2006) have sampled species over short periods of 3 or 4 years.

Studies in nearby estuaries indicate that spawning by numerous species of fish occurs in the Yangtze River estuary (Wan et al. 2010). The objective of the present study was to describe seasonal and inter-annual variation in species diversity, as well as species abundance for the whole surface

60 | Jiang Mei, Shen Xin-Qiang, Li Lei, Quan Wei-Min


ichthyoplankton assemblage on a short-term basis (<3 years) in the Yangtze River estuary of China. The sampling strategy was based upon eight annual collections to strengthen the temporal dimension of the long-term pattern. Data collection was restricted to vertical samples at each station. This study is part of a long-term monitoring project. It included the zooplankton, phytoplankton, and benthos communities of this region. These studies together aim to survey the environmental quality of fisheries in the East China Sea coastal area.

The China Yangtze Three Gorges Project (TGP), as one of the biggest hydropower-complex projects in the world, ranks as the key project for improving and developing the Yangtze River. The dam is located in the area of Xilingxia Gorge, one of the three gorges of the river, which will control a drainage area of 1 million km2, with an average annual runoff of 451 billion m3. The open valley at the dam site, with hard and integral granite as the bedrock, has provided favourable topographical and geological conditions for dam construction. On 8 Nov 1997, the river close-off succeeded, completing phase I of construction. On 6 Nov 2002, the close-off of the diversion channel succeeded. On 1 June 2003, the reservoir began its storage, and the water reached a level of 135 m on 10 June. The changes in the water level of the Three Gorges Reservoir will affect the distributional range of the brackish water in the Yangtze River estuary (Liu et al. 1992).

The aim of this paper is to study the abundance and composition of the egg and larval fish community in the Yangtze River estuary and its relationship with surface temperature, salinity, runoff and sediment runoff, and how it changed when the Three Gorges Dam began storing water. To achieve this objective, we employed a zooplankton net that sampled bottom to surface water layers and measured chemical and physical parameters that characterised the water. MATERIALS AND METHODS Study area

The Yangtze River, with a length of about 6,300 km, is the largest river flowing into the northern part of the Pacific Ocean. The Yangtze River estuary of China is located at the junction of the East China Sea (ECS) and the Yellow Sea (YS), on the continental shelf at the western rim of the Pacific Ocean (Fig. 1). The estuary and adjacent coastal waters are mainly

affected by freshwater runoff from the Yangtze River. The Yangtze River estuary and its adjacent waters are also affected by the East China Sea Coastal Current (ECSCC), Yellow Sea Coast Current (YSCC), and the Taiwan Warm Current (TWC), and by the interactions between these currents. The Taiwan Warm Current originates from the Taiwan Strait and a branch of the Kuroshio Current that extends into the area from northeast Taiwan (Su et al. 1998, Ming et al. 2008). During the summer season, however, southwest winds prevail, and the intensified runoff of the Yangtze River normally turns eastward or northeastward toward Cheju Island, Korea. During this period, the ECSCC also moves northeastward along the coast, driven by the southwest monsoon. This force causes the area affected by freshwater to extend northward, occupying a large area of the ECS and YS. The affected area even reached Cheju Island during a huge flood from the Yangtze River (Wang et al. 2002).

The environment of the estuary is complicated and varied due to strong tides and the river bed landform. Like most of the estuaries in the world, the Yangtze River estuary is a very productive and resource-rich aquatic ecosystem (Ning et al. 2004). High primary production supports high fishery production in adjacent coastal waters. It is also an important spawning area for many fishes and supports a diverse array of larval fish species throughout the early spring to late autumn months. The nearby Zhoushan and Lusi fisheries are both important fishery grounds in China. The construction of the Three Gorges Dam has raised increasing concerns about the long-term changes to the Yangtze River and their impacts on the aquatic ecosystem in the estuary and adjacent coastal waters. Sample collection

The ichthyoplankton were surveyed in a single area (30°15.85′N – 31°14.96′N and 121°30.42′E – 122°14.40′E) in the Yangtze River estuary from 2002 to 2009 (Fig. 2). Three important sections were studied: the Changjiang fish spawning ground, the Hangzhou Bay fish spawning ground, and the Zhoushan fish spawning ground. Samples from 20 stations were analyzed, of which six were in the Changjiang fish spawning ground, five in the Hangzhou Bay fish spawning ground, and nine in the Zhoushan fish spawning ground. Sampling was carried out each voyage during daylight at high tide, at 20 stations distributed throughout the Changjiang

Annual variability of ichthyoplankton in the Yangtze River estuary of China from August 2002 to 2009| 61

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River estuary and its adjacent waters, from 12 to 18 August during the 8-year sampling period. The sampling occurred during cruises conducted by the East China Sea Fisheries Research Institute Chinese Academy of Fishery Sciences Fisheries aboard the research vessel DONGHAI YU ZHEN. The survey was conducted for 8 years, yielding a total of 160 samplings.

All of the samples were obtained from vertical tows at depths ranging from 30.5 m (max. depth) to 0 m (surface) using a macro-plankton net at every station; the net (0.20 – 0.20 m2 mouth) was fitted with 505 µm mesh. There was only one sample haul at each station. The volume of water filtered during

each tow was estimated with a flow meter attached across the centre of the net mouth. The samples were preserved in 4% formaldehyde in sea water buffered with sodium borate and transported monthly to the laboratory for analysis. All eggs, embryos, and larvae were sorted and counted; fish eggs and larvae were separated from debris under a stereoscopic microscope (10×) using an Olympus counting chamber. Following ichthyoplankton separation and quantification, the larvae were identified to the lowest taxonomic level. Since some specimens could not be identified at the genus or species level, the abundance data were interpreted at the family level in the quantitative analyses.

A multi-parameter water quality sonde (YSI- 6600) was used at every station to obtain the salinity, temperature, and turbidity of the water column. The probes were calibrated both before and after the cruises. Seawater was sampled at the surface layer and at half of the water depth beneath the euphotic layer (hereafter referred to as the bottom layer). Data analysis

The total egg and larval counts were standardised by volume (abundance, numbers per 100 m3) and were separately analysed for each voyage. The mean yearly abundance was calculated as the arithmetic mean of individual tows coming from all stations sampled in each year. One-way analysis of variance (ANOVA) calculations were performed to determine the statistical significance of the annual changes in several variables: egg density, density of larvae, temperature, and salinity. Monthly values of the response variables were previously temperature and salinity. To evaluate the intensity of the associations between the density of eggs and larvae and temperature and salinity, a pairwise correlation analysis (Pearson’s r) was conducted (Alan et al. 1997). The mean of all surface readings and the mean of all bottom layer readings were calculated for both salinity and temperature. Then surface and bottom layer means were averaged. Two diversity indexes were calculated for the family taxa: the Shannon-Wiener diversity function (H’) was computed for each month according to Zar (1996), with units in ‘bits’ using the log base 2, and an index of ‘richness’ calculated as the absolute number of families per month (Lourdes et al. 2000). Data on the runoff and sediment runoff was obtained from the River Sediment Bulletin of China (www.irtces.org).

Fig. 1. Circulation pattern in the East China Sea and Yellow Sea in summer circulation features. YSCC: Yellow Sea Coastal Current; CRP: Changjiang River Plume; ECSCC: East China Sea Coastal Current; TWC: Taiwan Warm Current; TC: Tsushima Current; YSWC: Yellow Sea Warm Current; KCC: Korean Coastal Current.

Fig. 2. Study area in the Yangtze River estuary of China.



RESULTS Temperature and salinity

At each station, temperature and salinity were measured. The data revealed differences among the stations from August 2002 to 2009 in the Yangtze River estuary of China (Fig. 3). The eight-year mean temperatures ranged from 26.30°C at station 14 to 29.01°C at station 9; thus, the temperature only varied by 2.71°C among the stations. Specifically, the mean temperature of stations 13 and 14, which were farthest from the Yangtze River inlet, reached a low of 26°C. In 2006, the average temperature for all stations reached a low of 26.40°C. The lowest temperature was observed at station 13 (only 22.3°C).

The maximum (31.98°C) was recorded at station 9 in 2007.

Salinity varied very little among the stations (Fig. 3). Stations 1 and 2, which were nearest to the Yangtze River inlet, had the lowest salinities: their mean salinity was less than 5. The mean salinity of stations 5, 6, and 14, which were nearest to the inlets of the external currents, had the highest salinities, with a mean greater than 20. In each year, the average salinity ranged from 10.00 to 17.82. The peak appeared in 2006, and the low appeared in 2009. Runoff and sediment runoff

The data describing the runoff and sediment runoff collected in the Yangtze River estuary was

Fig. 3. Temporal variability distribution of temperature (°C) and salinity from 2002-2009.


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from a bulletin concerning Chinese river sediment that was authorised by the Ministry of Water Resources of China. Runoff peaked twice: in 2002 (53,700 ×108 m3), when the water level in the Three Gorges Reservoir had not yet reached 150 meters, and in 2007 (48,137 ×108 m3). The least amount of runoff was found in 2006 (27,430 ×108 m3) during the rare occurrence of a seriously low flow in the Yangtze River (Fig. 4). The sediment runoff decreased yearly. The maximum amount of sediment runoff occurred in 2002 (5,400 ×104 t), and the minimum amount of sediment runoff was observed in 2009 (900 ×104 t).

Taxonomic composition of the ichthyoplankton

A total of 1126 fish eggs and 530 fish larvae were sorted yearly during the month of August from 2002 to 2009. Twenty-three families, 2 genera, and 34 species of eggs and fish larvae were identified (Table 1). Eleven species were represented as eggs, while larvae from 30 species were identified. Twenty of the species identified were characterised as offshore spawners. The greatest number of families was collected in 2002. The lowest number of families of eggs and larvae were observed in 2003, when only two and three were represented, respectively. Only 8

Table 1 List of species, period of occurrence, and estimated maximum abundance (number per 100 m3) of eggs or larvae found in the Yangzte River estuary during 2002 – 2009.

Taxa Common name Occurence Maximum abundance Eggs Larvae Eggs Larvae

Clupeidae Ilisha elongata whiter herring - 2004 - 39.44 Konosirus punetatis dotted gizzard shad - 2006,2009 - 28.82

EngraulidaeStolephorus commersonii longjawed anchoy 2002-2006, 2008-2009 2002-2009 570.64 131.41 Engraulis japonicus halfmouthed sardine 2002,2007-2009 2004-2005, 2007-2009 218.92 29.57 Coilia mystus Osbeck's grenadier anchovy 2002 2002-2009 37.07 222.03

Synodidae Saurida filamentosa whipfin lizardfish 2004,2005,2007 2002,2004,2005 230.86 74.36 Trachinocephalus myops bluntnose lizardfish - 2007 - 1.90

Sphyraenidae Sphyraena pinguis fatty barracuda - 2005,2006 - 10.86

Myctophidae Bethosema pterotum skinnycheek lanternfish - 2005 - 4.11

CyprinidaePseudolaubuca sinensis silver bream - 2002-2004 - 17.75

Mugilidae Liza haematocheila redeye mullet - 2008,2009 - 29.83

Priacanthidae Priacanthus macracanthus bullseye perch 2006 2002 5.12 8.93

Sillaginidae Sillago sihama common asohos 2007,2009 2004,2005,2008 19.52 10.86

Sciaenidae Johnius sp. corvina - 2004,2005 - 8.91 Collichthys lucidus spinyhead croaker - 2002-2003, 2006-2007,2009 - 9.46 Argyrosomus argentatus roncadore 2002,2005 2003-2007,2009 3.57 26.52 Larimichthys crocea greater yellow croaker - 2006-2009 - 9.46 Johnius grypotus corvina - 2008 - 3.25

Champsodontidae Champsodon capensis gaper - 2002 - 111.51

Callionymidae Callionymus olidus smelly 2007,2009 2005 21.58 9.33

Gobiidae Acanthogobius flavimanus genuin goby - 2006,2009 - 6.39 Amblychaeturichthys hexanema pinkgray goby - 2002-2009 - 28.00

Taenioididae Odontamblyopus rubicundus green eelgoby - 2002 - 15.31

Taenioididae Ctenotrypauchen chinensis Chinese goby - 2002-2003, 2006-2008 - 21.91 Trypauchen vagina burrowing goby - 2004 - 3.57

Trichiuridae Trichiurus lepturus Atlantic cutlassfish 2002,2005 2002,2008 3.92 3.57

ScombridaeScomber japonicus blue mackerel - 2002 - 10.71

Thunnidae Auxis thazard bullet mackerel 2008 - 7.21 -

Scorpaenidae Marmoratus sp. rock cods 2002 - 3.57 -

SynanceidaeInimicus japonicus japanese goblinfish - 2002 - 7.14

Triglidae Chalidonichthys kumu bluefin gurnard - 2002 - 3.57 Bothidae bartard hlibuts 2003,2004 - 38.09 -Pseudorhombus cinnamoneus cinnamon flounder - 2002-2005 - 7.07

Pleuronectidae Cleisthenes herzensteini pointhead plaice - 2004 - 5.85

Cynoglossidae Cynoglossus joyneri Joyners tongue-sole - 2004-2007,.2009 - 16.23

Unidentified 2002,2004,2006 - 11.38 -



species (Stolephorus commersonii, Engraulis japonicus, Coilia mystus, Saurida filamentosa, Priacanthus macracanthus, Sillago sihama, Argyrosomus argentatus, and Trichiurus lepturus) were sampled as both eggs and larvae. The other species were found either as eggs or larvae. Most species did not occur in each year. In the present study, Stolephorus commersonii and Coilia mystus were found in their larval form in every year. The species that was most abundant as eggs was the longjawed anchovy (Stolephorus commersonii), which occurred at a level of 570.64 eggs per 100 m3. However, the most abundant larvae were those of the Osbeck's grenadier anchovy (Coilia mystus), which were found at a level of 131.41 larvae per 100 m3.

Only 12 species of fish eggs and larvae, which represented greater than 10% of the total abundance, were included in any one year (Table 2). The number of dominant species varied yearly from 5 to 8 species; the maximum was observed in 2002. The egg samples were numerically dominated by anchovies (Engraulidae, 78.5%). After anchovy eggs, the next most abundant eggs were those of Saurida filamentosa (13.6%). Most eggs were not identified to the family level (1.0%). Ten species represented 79.2% of the total larvae captured. Coilia mystus accounted for 24.34% of the larvae taken. Other species with relatively abundant larvae were Stolephorus commersonii, Champsodon capensis, and Engraulis japonicus. The abundance percent composition of each species of eggs or larvae varied significantly from year to year. Diversity of eggs and larvae

From 2002 to 2009, diversity (H’) and species richness were stable (Fig. 5) with respect to the number of accumulated samples. The total diversity of eggs and larvae (H’) was 0.23 and 0.62,

respectively. For the species represented as eggs, the lowest diversity was recorded in 2006 (0.07) and the highest in 2002 (0.53). The larvae mean diversity was lowest in 2007 and highest in 2002. The low diversity value in 2006 was due to a great abundance of longjawed anchovy (Stolephorus commersonii) eggs. The abundance of Osbeck's grenadier anchovy (Coilia mystus) larvae contributed to the low diversity value in 2007.

Richness varied yearly from 2 to 13 families of eggs and 4 to 10 families of larvae. For the species represented as eggs, the lowest value richness was recorded in 2008 and the highest in 2002 (Fig. 5). The larvae richness expressed as the number of families ranged from a low of 4 families in 2007 to a high of 11 families in 2002.

Fig. 4. Annual variability of runoff and sediment runoff collected in the Yangtze River estuary during August from 2002 to 2009.

Table 2 List of dominant species, their contribution (%) of the total number of eggs or larvae caught over each cruise.

2002 2003 2004 2005 2006 2007 2008 2009 Mean of 8 year-total

Temperture(°C) 28.58 26.97 28.09 26.47 26.14 29.12 28.82 28.86 27.88 Salinity(PSU) 11.07 13.70 14.92 16.86 17.82 16.85 15.22 10.00 14.43 currents

Species eggs Engraulis japonicus 76.0 - - - - 59.0 62.0 7.0 20.6 Coilia mystus 13.0 - - - - - - - 2.0 Stolephorus commersonii 1.0 77.0 22.0 94.0 96.0 - 32.0 87.0 55.9 Saurida filamentosa 3.0 - 64.0 1.0 - 26.0 - - 13.6 Sillago sihama - - - - - 13.00 - - 1.6

Species larvae Ilisha elongata - - 18.0 - - - - - 2.7 Konosirus punetatis - - - - 15.0 - - 1.0 2.1 Engraulis japonicus - - 13.0 12.0 - 18.0 20.0 5.0 6.7 Coilia mystus 1.0 21.0 9.0 19.0 3.0 13.0 34.0 64.0 24.3 Stolephorus commersonii 1.0 51.0 3.0 13.0 67.0 - 6.0 11.0 18.8 Saurida elongata 2.0 - 34.0 3.0 - - - - 5.8 Argyrosomus argentatus - 6.0 3.0 15.0 3.0 5.0 - 2.0 3.7Champsodon capensis 46.0 - - - - - - - 7.6 Amblychaeturichthys hexanema 12.0 4.0 1.0 3.0 1.0 5.0 7.0 2.0 4.1 Ctenotrypauchen chinensis 5.0 6.0 - - 2.0 19.0 16.0 - 3.5

The dominant species are listed where species contribution of eggs or larvae is >10% in any one year during 2002-2009. - no eggs and larvae caught, species in bold >10% (calculated for total abundance of the 8-year study).


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Abundance and annual variability of the ichthyoplankton A relatively large peak in the abundance of fish eggs occurred in 2006 (Fig. 6). During that time, the egg mean egg density (over all stations) was 1167.9 eggs per 100 m3. The abundance of eggs during this year was 1.26-10.42 times higher than that of the other years. The peaks were primarily due to intense spawning by the longjawed anchovy (Table 2). Their eggs were found when the water temperature exceeded 29°C. In 2003, the abundance of eggs was lowest (only 57.28 per 100 m3). The maximum larval abundance (mean over the 14

stations) occurred in 2009 (Fig. 4). At that time, the total number of larvae averaged 116, and abundance averaged 348.74 per 100 m3. The peaks were dominated by the Japanese grenadier anchovy (Table 2). The lowest abundance of larvae was recorded as 57.84 per 100 m3 in 2007. Relationship between physical factors and ichthyoplankton abundance

The regression analysis suggested that different aspects of the abundance of ichthyoplankton were affected differently by the environmental factors of temperature and salinity. When tested individually, the abundance of only 4 of the 34 species was significantly correlated with environmental variables in any given year (Table 3). Interestingly, egg abundance was significantly correlated with salinity, but not temperature. The egg abundance of Engraulis japonicus was only negatively correlated with salinity in one year, unlike the other two species (Stolephorus commersonii and Saurida elongata). In contrast, larvae abundance was closely correlated with salinity and temperature. Coilia mystus larvae, the most common type of larvae collected, were the only ones

Fig. 5. Shannon–Wiener diversity (H’) and richness of families of eggs and larvae collected in the Yangtze River estuary from 2002 to 2009.

Fig. 6. Annual variability of total ichthyoplankton collected in the Yangtze River estuary during 2002-2009.

Table 3

Pearson correlation coefficients for taxa and environmental variables.

2002 2003 2004 2005 2006 2007 2008 2009

T S T S T S T S T S T S T S T S Eggs

Stolephorus commersonii - - -0.327 0.583a -0.350 0.649b -0.289 0.334 -0.450a 0.336 - - -0.598a 0.701b -0.637a 0.612a Engraulis japonicus -0.381 -0.440a - - - - - - - - -0.675a 0.785b -0.782b 0.732b -0.259 0.690a Saurida elongata 0.347 0.578a - - 0.319 0.601a 0.284 0.521a - - -0.222 0.485a - - - -

Larvae Stolephorus commersonii 0.454 a -0.507a 0.313 -0. 413a 0.376 -0.269 0.432a -0.507a 0.543a -0.186 - - 0.657a -0.498a 0.490a -0.428a Coilia mystus -0.543 a 0.722b -0.679a 0.739b -0.337 0.523a -0.724b 0.734a -0.541a 0.552a -0.650a 0.636a -0.698a 0.803b 0.625a 0.733b Saurida elongata 0.311 0.522b - - 0.433a 0. 422 0.343 0.628a - - - - - - - - T – temperature S – salinity; a – p<0.05, b – p<0.01



negatively correlated with temperature and positively correlated with salinity. In contrast to the 2 other species (Engraulis japonicus and Saurida elongata), Stolephorus commersonii larval abundance was negatively correlated with salinity. DISCUSSION

The ichthyoplankton of the Yangtze River estuary was dominated by Engraulidae, Champsodontidae, and Sciaenidae. Engraulidae and Sciaenidae were the only two families that appeared in all years, and each was represented by a wide range of ontogenetic intervals, from eggs to early embryos and juveniles. This high abundance of Engraulidae larvae in August has been reported in other studies (Ruple 1984, Houde & Lovdal 1984, Ditty 1988). Engraulidae Coilia mystus is a traditional brackish estuary species, and it has the ability to inhabit coastal waters and estuaries (Whitehead et al. 1988). Sciaenidae fish are found worldwide in both fresh and saltwater. They are small to medium-sized bottom dwelling fishes that live primarily in estuaries and bays, as well as along muddy river banks (Nelson 1994). They were relatively more abundant than the other species.

The dominant ichthyoplankton found was different from that reported in annual ichthyoplankton surveys, except for Coilia mystus and Amblychaeturichthys hexanema (Table 2). The composition of species abundance reported in this study was similar to that reported by Wan (2010); the dominant species of eggs and larvae were Engraulis japonicus, Stolephorus commersonii, and Saurida elongate. The species noted by Wan that were not collected in this study were Upeneus bensasi, Therapon theraps, and Lagocephalus inermis. However, these species were rare and had low mean densities. The composition of dominant species and the main species changed throughout the 8 years of this study as a result of variation in environment factors, such as surface temperature and salinity. We found a strong association between the abundance of 4 dominant species and temperature (Table 3), but salinity had a higher correlation with abundance. Estuaries are defined as places where freshwater from rivers mixes with saltwater from the sea. Likewise, Alan et al. (1995) found a similarly strong correlation between freshwater inflows and the salinity gradients in San Francisco Bay. However, the salinity gradients in many estuarine ecosystems can be seriously affected by upstream utilisation of freshwater flows including

dams, inter-basin transfers, and surface water withdrawals. Longitudinal distributions of surface salinity depend strongly on freshwater runoff (Uncles et al. 2000). The runoff of the Yangtze River estuary varied in relation to water storage in the Three Gorges Reservoir and rainfall. In this study, we can see how variable the dominant species and richness of ichthyoplankton were then; these values changed significantly with changes in runoff and salinity in 2003 and 2006 in the Yangtze River estuary. Studies in other shallow water estuaries have shown that the species richness and the larval abundance of each species varied among stations relative to the salinity gradient in the estuary (Yves, 1990); this was also true of our study.

The annual variation in temperature (7.38%) was much less than that of salinity (43.9%) in this study (Table 2). Temperature was directly related to water and air exchange at the surface (Tang et al. 2005), and the temperature values were influenced by the atmospheric temperature and ocean currents. The results of the analysis of the temperature and salinity data showed that the second highest temperature and lowest salinity occurred in 2009. The abundance of eggs and larvae peaked in this survey. Additionally, the eggs of Stolephorus commersonii, which were captured in station 14, represented 85% of the total eggs and caused egg abundance to peak in this year. Due to the over-representation of this species, Stolephorus commersonii egg abundance appeared to be low, even though this was not the case. This was similar to what was observed by other studies (Yves 1990). Coilia mystus larvae were prevalent in the study area, and accounted for 64% of total larvae abundance, the highest abundance over the 8-year study period. Temperature and salinity had significant effects on the abundance of these two species in this year (Table 3).

The diversity values for ichothyoplankton found in this study were possibly less than 1 (Fig 4). The distribution of biological communities mirrored the distribution of salinity in the estuary; each species lived in its optimum salinity range. Environmental conditions varied frequently, however, which caused only a few communities to be inhabited in the estuaries, giving rise to the low observed diversity. The highest diversity of eggs and larvae and the greatest richness occurred in 2002. There was a sharp decline in the richness of eggs and larvae in 2003 (Fig. 5). The diversity of ichthyoplankton decreased to 30.77% – 72.7% of the 2002 levels. Over the 8 years of our study, ichthyoplankton species that


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occurred in 2002 were not present in the 7 later years (2003-2009) (Table 1). Champsodon capensis, Odontamblyopus rubicundus, Scomber japonicus, Inimicus japonicus, Chalidonichthys kumu, and Marmoratus sp. were found in 2002, but these species were absent from 2003 to 2009. Moreover, 19 new species appeared from 2003 to 2009, but not in 2002, such as Ilisha elongate, Konosirus punetatis, Trachinocephalus myops, Sphyraena pinguis, and Bethosema pterotum, but their abundances were low (Table 2). Pombo (2002) found that the hydroelectric project, fishing, pollution and other human factors caused the fluctuation of environmental conditions in the river estuary area. In this report, some species disappeared, and some new species occurred. One explanation of this change in species composition was the level of water storage in the Three Gorges Reservoir beginning in June 2003, which accounted for an approximately 13% reduction in the freshwater discharge.

As predicted by Liu et al. (1992), changes in the water level of the Three Gorges Reservoir affected the distributional range of the brackish water in the Yangtze River estuary. As the brackish water range decreased from the original 4,500 km2 to 1,800 km2, the estuarine salinity rose by 1-4, and the 30 isohaline shrank back to the mouth. The mean salinity gradient rose simultaneously, and nutrient salts and organic compounds in the water decreased accordingly; the high concentration area also shrank back towards the estuary. Flow regime is recognised as a key factor in determining the biological and physical processes and characteristics in a river. However, water projects can substantially change the natural flow regimes of water bodies. Compared with 2002, the amount of runoff and sediment runoff collected in the Yangtze River estuary decreased 25.55% and 66.67% in 2003, respectively (Fig. 4). Water and sediment from the upstream Yangtze River was intercepted and stored in the Three Gorges Reservoir. The sharp decrease in sediment runoff in this study was similar to that observed by James et al. (2005). As a result, the flow velocity became slow and the water became limpid according to the increased runoff; there were evident influences on the ecosystems of the downstream river and estuary. The variation in flow can change habitat conditions to different spatial and temporal extents; Drinkwater et al. (1994) noted that river-runoff changes caused variation in terrain, temperature, salinity, turbidity, and dissolved oxygen. This affected the distribution and abundance of estuarine species, as well as the composition and diversity of biological communities (Converse et al.

1998). However, these new species belonged to

incidental and rare species. Only a few of these species became dominant species with high abundances. In our study, 23% of the egg samples belonged to Priacanthus macracanthus, which was a dominant species in 2003, while Ilisha elongata represented 18% of the total larvae in 2004 (Table 2). The adaptability of these species was poorer than that of the dominant species and common species. The species number and the diversity would increase under stable environmental conditions. If environmental conditions became unfavourable, their number and diversity would drop rapidly. Human activities such as dam construction and basin water transfer, which change the natural runoff and continuity of rivers, can give rise to certain ecological problems (Richard et al. 2001). As a result of the decrease in runoff and sediment runoff caused by the storage of water in the Three Gorges Reservoir, pollutants expanded to the edge, hydrological conditions alternated, and fish spawning, feeding, and migration environments were changed. As a result, the abundance and diversity of eggs decreased significantly from 2002 to 2003. The egg abundance was the lowest during this year of the sampling period. The results indicated that the water storage in the Three Gorges Reservoir had an impact on estuarine fish spawning. Similarly, Autumn et al. (2008) reported that when the Aswan Dam was completed on the Nile in Egypt nutrient transport from the waters adjacent to the estuary decreased as much as 90%, and fisheries resources caused a serious failure in coastal waters. The Three Gorges reservoir is a seasonally adjusted reservoir, which adjusted the natural runoff into the sea to some extent. Based on the estuary flow change, we can see that some factors, particularly the hydrological regime, chemical composition, and amount of sediment, were directly affected when the runoff changed. In addition, the biological community can change in terms of its structure, quantity, spatial and temporal distribution, and the relationships between species, as well as the whole ecosystem, by the enlarging, reducing, and superposition effect in the ecosystem. It is an extremely complicated process with many interacting factors involved; however, it will take a long time for the affected ecosystem to display obvious changes.

The year 2006 was extraordinarily dry (Wang, 2011). Weak flow conditions prevailed, and runoff and sediment runoff were at their lowest points



during the period of this study (Fig. 6). The species diversity and abundance of ichthyoplankton were significantly different from those of the neighbouring years, 2005 and 2007. Changes in the estuary ecosystem affected the biological clustering characteristics (Kimmerer 2002). There were 5 stations where no eggs or larvae were collected during this year. The rising tide is the signal and trigger point for fish spawning and migration (Jackie et al. 1998). The runoff decrease affected the timing of the tides, leading to changes in fish reproduction and the recruitment of the fish population.

In conclusion, ichthyoplankton abundance and species contributions in the Yangtze River estuary were fundamentally linked to variations in temperature, salinity, and runoff from August 2002 to August 2009. We suggest that these intrinsic associations may be modified by water level variation in the Three Gorges Reservoir. These observations may be particularly relevant, given the interest in the potential effects of runoff variation on ecological systems. The result could be a reference between spawn to eggs and recruitment to larvae nursery habitat. ACKNOWLEDGMENTS

We wish to thank Lian-Fang Chen for her assistance in the laboratory. Sampling would not have been possible without Wang Yun-Long, Luo Ming-Bo, Shen Ang-Lv, Ping Xian-Yin, Zhu Jiang-Xin, Chao Min, Han Jin-Di, and Chen Yuan-Quan at the East China Sea Fisheries Research Institute Chinese Academy of Fishery Sciences. We would also like to thank Yuan Qi for her valuable help with the data analysis. We thank Professor Chen Ya-Qu, Shi Li-Yan, and Xia Pei-Yan for supporting the first author in the preparation of this article. This research was partially supported by the China Ministry of Science and Technology under Contract (G2010CB429005). REFERENCES Aimee, A. K., Grace K.M., Jeanne, S.T. & Onge, B. (1999).

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Annual variability of ichthyoplankton in the Yangtze River estuary of China from August 2002 to 2009