Impacts of variability of habitat factors on species composition of ichthyoplankton and distribution of fish spawning ground in the Changjiang River estuary and its adjacent waters

Acta Ecologica Sinica 30 (2010) 155–165

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Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes

Impacts of variability of habitat factors on species composition of ichthyoplankton and distribution of fish spawning ground in the Changjiang River estuary and its adjacent waters Wan Ruijing a,*, Zhou Feng b, Shan Xiujuan a, Sun Shan a a

Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory for Sustainable Utilization of Marine Fisheries Resource, Ministry of Agriculture, Key Laboratory for Fishery Resources and Eco-environment, Shandong Province, Qingdao 266071, Shandong, China State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, Zhejiang, China

b

a r t i c l e

i n f o

Keywords: The Changjiang River estuary Ichthyoplankton Fish spawning ground Habitat factor Temperature Salinity

a b s t r a c t During June, August and October 2006, there were three multi-disciplinary surveys carried out in the Changjiang River estuary and its adjacent waters (122°000 –125°000 E, 27°500 –34°000 N) by R/V Beidou to study the species composition and abundance of ichthyoplankton (including fish eggs, larvae and juveniles), the spatial distribution of fish spawning ground and their relationship with habitat factors. There were 29, 29 and 25 grid stations sampled in the three cruises, respectively. The ichthyoplankton samples were collected by horizontally towing with a macro-plankton net (mouth diameter 80 cm, length 270 cm, mesh size 0.50 mm) at the sea surface, and the towing speed was 3.0 n mile/h at each sampling station. The towing lasted for 10 min. After hauling for each station, habitat factors including temperature and salinity were measured by Sea Bird-25 CTD. Samples were preserved in 5% formaldehyde solution immediately after sampling for analysis in laboratory. Since the trawl speed could not be accurately evaluated due to the effects of ocean currents and wind-induced wave, the amount of ichthyoplankton was evaluated by actual number of the sampling haul in each station. Ichthyoplankton collected were divided into three categories: dominant species, important species and main species by the index of relative importance (IRI). There are 71 species (including 1200 fish eggs and 2575 fish larvae and juveniles) collected during 3 cruises and 59 species have been correctly identified to species level, which belongs to 50 genera, 37 families and 9 orders; while 5 species can only be identified to genera level, 1 species only identified to family level and 6 species identified to order level. These 59 species identified to species level and 5 species identified to genera level are divided into three ecological patterns, i.e., brackish water species, neritic water species and coastal water species. Warm water species have 34 species in those 59 species identified to species level, accounting for 57.63%, warm temperature species have 25 species, accounting for 42.37%. According to the analysis of IRI, the dominant species are Engraulis japonicus (in June and August, that is important species in October), Scomber japonicus (in August), and Johnius grypotus (in October) during the survey; important species are Cynoglossus joyneri (in June and August), Trichiurus lepturus (in June, August and October), Gonorhynchus abbreviatus (in August), Stolephorus commersonii (in October), Saurida undosquamis (in October) and Saurida elongate (in October), and main species have 12 species in June, 9 species in August and 10 species in October, respectively. The amount of fish eggs and larvae of the dominant species, important species and main species (28 species) are 97.50% and 97.13% of the total amount of fish eggs and larvae, respectively, which are the important composition of fish eggs and larvae in the Changjiang River estuary and its adjacent waters. In June and August of 2006, if compared with that in corresponding months in 1986, there are great changes in the habitat factors especially for temperature and salinity in the investigating areas: high salinity water from off-shelf is much closer to the coastal areas which results in the dramatic increase of sea surface salinity during all three surveys. Sea surface temperature, on the other hand, decreases distinctively in June, but significantly increases in August. The run-off of the Changjiang River greatly reduced due to the long-term drought in summer 2006, which is responsible for the great changes of habitat factors in the Changjiang River estuary and its adjacent waters. The habitat of the Changjiang River estuary is greatly changed, which consequently has significant influences on the spawning, breeding and

* Corresponding author. E-mail address: [email protected] (W. Ruijing). 1872-2032/$ - see front matter Crown Copyright Ó 2010 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2010.04.006

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the spatial distribution of spawning ground of neritic water species, such as Sardinella zunasi, Thryssa kammalensis, Thryssa mystax, Setipinna taty and S. commersonii ect, and coastal water species, such as Ilisha elongate and Konosirus punctatus ect. Crown Copyright Ó 2010 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

1. Introduction

[14], Shan et al. [15], Jiang et al. [16], Wang et al. [17] and Liu et al. [18]. The present study was based on the survey data of June, August and October in 2006 in the Changjiang River estuary and its adjacent waters. By comparing with the results of Yang et al. [12] and Yang [13], analyzing the effects of environmental changes on the species composition and seasonal changes of ichthyoplankton, and spawning grounds, we provide the basic data and horizons for long-termed observation and systematical studies of the effects of the Three Gorges Dam on the structure and function of the Changjiang River estuary and its adjacent waters ecosystem.

The Changjiang River estuary is the largest estuary with exceptional favorable geographic location and natural conditions in China. The Changjiang River estuary and its adjacent waters is the place where salt water and fresh water mingle, and affected by the Changjiang River runoff, also limited by the occurrence and interaction among Subei Coastal Current, the Yellow Sea Cold Water Mass and Taiwan Warm Current, its environment is complicated and varied due to strong tides and river bed landform. The Yangtze River runoff carries out abundant of nutritional substance to the estuary and its adjacent waters, which maintains high productivity in the Changjiang River estuary ecosystem, supports favorable survival condition for marine biology, and forms the critical feeding, breeding and spawning grounds of fish. So the Changjiang River estuary and its adjacent waters is an ecosystem with complicated structure and unique function [1,2]. The species composition, distribution of individual quantity and their seasonal changes of ichthyoplankton, and their distribution of spawning grounds in estuaries, are limited by the species composition and distribution of quantity of reproductive stock, also closely connect with physical, chemical and biological factors of water area [3–8], the recruitment and sustainable utilization of fishery resource are determined by the survival, development, growth and quantity of ichthyoplankton [9], and their quantity distribution and dynamics play important roles in maintaining equilibrium of estuaries ecosystem. The monthly amount of the Changjiang River runoff and its seasonal distribution patterns were greatly modified by the construction of the Three Gorges Dam, and therefore the temperature, salinity, nutritional substance and abiotic factors were changed correspondingly [10], which caused inevitable changes of the distribution of spawning grounds, and the species composition as well as spatiotemporal distribution of ichthyoplankton [11], and further affected the recruitment of fishery resource and equilibrium of ecosystem [1,2]. The study of ichthyoplankton in the Changjiang River estuary and its adjacent waters was firstly carried out from August, 1985 to August, 1986 by Yang [12], thereafter, reanalyzed by Yang [13]; in addition, the relative studies were reported by Zhu et al.

34

2. Materials and methods During June, August and October 2006, there were three multidisciplinary surveys carried out in the Changjiang River estuary and its adjacent waters (122°000 –125°000 E, 27°500 –34°000 N) by R/V Beidou to study the physics, chemistry, biological environment and resources, the species composition and abundance of ichthyoplankton, the spatial distribution of fish spawning ground and their relationships with habitat factors were important part of survey. Six sections with 29 stations, 7 sections with 29 stations and 7 sections with 25 stations were sampled in June, August and October, respectively (Fig. 1). Ichthyoplankton were sampled by macro-plankton nets (0.50 mm mesh size, net mouth diameter 80 cm, length of net 270 cm). The duration of trawls was 10 min, the hauling speed was 3.0 n mile/h in all surveys. After hauling for each station, environmental factors including temperature and salinity were measured by a CTD (Sea Bird-25) rosette sampler. Ichthyoplankton samples were fixed in 5% formaldehyde solution. Qualitative and quantitative analysis were carried out in lab, and the quantitative analysis was calculated by the individual number in each station for the effects of ocean currents, waves and hauling speed. The species composition of ichthyoplankton was evaluated by index of relative importance (IRI) [19], and according to the results of analysis, the ichthyoplankton were divided into dominant species, important species and main species. IRI was calculated as follows:

IRI ¼ ðN% þ W%ÞF%

34

34

50

33

6-3

6-1 6-2

32

50

6-4

6-8

31

6-18 6-19

6-20

6-21

29

6-23

6-22 6-26

6-27

29 8-25

6-28 6-29

100

8-26

28

50

27 120

122

123

124

125

126

27 120

8-17

121

122

10-9 10-10

10-11

8-28

100

124

10-20 10-22 10-19 10-21 10-23 10-24 10-25

28

8-29

125

126

50

27 120

10-14

10-18

10-15

29

August 123

10-16 10-17

30

8-23 8-24

8-27

10-12 10-13

31

8-21

50

June 121

8-15 8-16

8-19 8-20

6-25

28

32

8-18 8-22

6-24

50

10-8

8-14

30

6-17

8-13

10-2

10-5 10-6 10-3 10-4 10-7

33

8-10 8-11 8-12

8-9

31

6-12 6-16

30

32

6-13 6-14 6-15

6-11

6-10

6-9

10-1

8-5

8-3 8-4 8-1 8-2 8-6 8-7

33

6-5 6-6 6-7

ð1Þ

121

122

100

October 123

Fig. 1. Sampling stations of ichthyoplankton in the Changjiang River estuary and its adjacent waters in 2006.

124

125

126

W. Ruijing et al. / Acta Ecologica Sinica 30 (2010) 155–165

It took no account of the biomass for small individual size of ichthyoplankton [14,15,18], the formula of IRI could be simplified as follows:

IRI ¼ N%  F%

ð2Þ

During survey, eggs of one species were just found in some stations, and larvae and juveniles were just found in some stations, and in some stations, eggs, larvae and juveniles were found at one time, so the formula (2) could be changed as follows:

IRI ¼ ðN E % þ NL % þ NðEþLÞ %Þ  ðF E % þ F L % þ F ðEþLÞ %Þ IRIi ¼



ð3Þ

  s nEi nLi nei nli sLi sðeþlÞi  Ei  100 þ þ þ þ þ  100  NE NL Ne Nl S S S ð4Þ

  nEi nLi nei nli IRIi ¼ þ þ þ  F i  10; 000 NE NL Ne Nl

ð5Þ

In formula (5), NE and NL were the total amount of fish eggs (including all stations where eggs were just found) and fish larvae and juveniles (including all stations where fish larvae and juveniles were just found) in each survey; nEi and nLi were the total amount of one species eggs and (including all stations where this species eggs were just found) and fish larvae and juveniles (including all stations where this species larvae and juveniles were just found) in each survey; Ne and Nl were the total amount of fish eggs and fish larvae and juveniles (including all stations where fish eggs, larvae and juveniles were found at one time) in each survey; nei and nli were the total amount of one species eggs and fish larvae and juveniles (including all stations where this species eggs, larvae and juveniles were found at one time) in each survey; Fi was the frequency of one species in each survey (including all stations where this species were found). The IRI values of dominant species were beyond 1000; the IRI values of important species were from 100 to 1000; the IRI values of main species were from 10 to 100 [20,21]. The quantity distribution of ichthyoplankton and the distribution of temperature and salinity were performed with software Surfer 8.0. 3. Results 3.1. Species composition of ichthyoplankton and ecotypes There were 1200 fish eggs and 2575 fish larvae and juveniles collected in three surveys (June, August and October) altogether, which were sorted 71 species, including fish eggs 31 species, larvae and juveniles 53 species, and 13 species were found both in fish egg, larvae and juveniles; 59 species were correctly identified to species level, and which belonged to 50 genera, 37 families and 9 orders; 5 species only could be identified to genera level, 1 species only identified to family level and 6 species identified to order level. According to the characteristics of habit and distribution, 64 species (including 59 species identified to species level and 5 species identified to genera level) were divided into brackish water species, neritic water species and coastal water species (Table 1). Brackish water species: most of them were estuaries fishes, and early development were finished in the estuary and its adjacent waters, 6 species (mainly Mugilidae species and Gobiidae species) accounted for 9.38% of total species composition. Neritic water species: most of them were migrant species, feeding and spawning in coastal waters, and overwintering in the offshore waters; they accounted for 32.81% of the total species composition, including 21 species, such as Setipinna taty, Stolephorus commersonii, Sciaenidae species, Pampus argenteus, Psenopsis

157

anomala, Sebastiscus marmoratus, Minous pusillus, Minous monodactylus, Cynoglossus joyneri, Cynoglossus semilaevis, Kentrocapros aculeatus and so on. Coastal water species: composed by ocean water species and deep water species, feeding and spawning in the offshore waters with depth beyond 30 m. They accounted for 57.81% of the total species composition, including 37 species, such as Engraulis japonicus Synodontidae species, Ophichthus species, Sillaginidae species, Carangidae species, Trichiurus lepturus, Scomber japonicus, Bothidae species, Bethosema pterotum, Coryphaena hippurus, Auxis rochei and so on. According to the temperature tolerance of species, 59 species those were identified to species level were composed by 34 warm water species (57.63% of the total species composition) and 25 warm temperature species (42.37% of the total species composition). From above-mentioned, ichthyoplankton were mainly composed by coastal species and inshore species in the survey of the Changjiang River estuary and its adjacent waters, all species belonged to warm water species and warm temperature species, cold water species were not found in the survey. 3.2. Dominant species, important species, main species and their changes The IRI values of ichthyoplankton in each survey were calculated by the formula (5). The composition of dominant species (IRI > 1000), important species (100 < IRI < 1000) and main species (10 < IRI < 100) in three surveys are found in Table 2. The dominant species were Engraulis japonicus (June and August, but was important species in October), S. japonicus (August), Johnius grypotus (October); the important species were C. joyneri (June and August), T. lepturus (June, August and October), Gonorhynchus abbreviatus (August), S. commersonii (October), Saurida undosquamis (October), Saurida elongate (October); the main species included 12 species in June, 9 species in August, 9 species in October (Table 2). So the species composition of dominant species, important species and main species were changed with survey time in three surveys, which were caused by variation of spawning time and spawning season. The important components of fish egg, larvae and juveniles were composed by 28 species (including dominant species, important species and main species), the total individual number of 28 species was 97.50% of total species individual number for fish egg, and 97.13% for fish larvae and juveniles. 3.3. Quantity of fish eggs, larvae and juveniles and their distribution 3.3.1. Quantity of fish eggs and their distribution There were 738 fish eggs collected in June, accounted for 61.50% of total fish eggs, the frequency of fish egg was 65.52%. The average density of fish egg was 25.4 ind/station. Fish eggs mainly distributed station 6-5, 6-6, 6-27, 6-28 and 629, which formed the concentrated area of E. japonicus with average density 106.5 ind/station and concentrated area of K. aculeatus, Platycephalus indicus, T. lepturus, Trachinocephalus myops, Scomberomorus niphonius and the other 7 species with average density 96.0 ind/station; the distributed area of C. joyneri, T. lepturus and the other 6 species with average density 47.5 ind/station was formed in station 6-18 and 6-19; and station 6-22, 6-23 and 6-24 were the distributed area of C. hippurus, P. indicus and the other 8 species with average density 26.3 ind/station; station 6-12 and 6-13 were the distributed area of E. japonicus and the other 2 species; and fish eggs in the other 6 stations were just found 1–8 individuals (Fig. 2). Fish eggs included 23 species, most of them were E. japonicus, accounted for 33.47% of the total fish eggs in the survey, then were

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W. Ruijing et al. / Acta Ecologica Sinica 30 (2010) 155–165

Table 1 Species composition, ecological patterns and appeared time of ichthyoplankton in the Changjiang River estuary and its adjacent waters in 2006. Taxon

Ecological pattern

Territorial system

Appeared month Eggs

Larvae

Gonorhynchiformes Gonorhynchidae Gonorhynchus abbreviatus Temminck et Schlegel, 1846

CW

WT

Clupeiformes Engraulidae Engraulis japonicus (Temminck et Schlegel, 1846) Setipinna taty (Valenciennes, 1848) Stolephorus commersonii (Lacépède, 1803)

CW NW NW

WT WW WW

6, 8, 10

6, 8, 10 8 10

Myctophiformes Synodontidae Trachinocephalus myops (Bloch et Schneider, 1801) Saurida (Temminck et Schlegel, 1846) Saurida undosquamis (Richardson, 1848) Saurida tumbil Bloch, 1775

CW CW CW CW

WW WT WW WW

6, 8 6, 10 6, 8, 10 8

6, 8 6, 8, 10 6

Myctophidae Bethosema pterotum (Alcock, 1891)

DW

WW

Anguilliformes Ophichthyidae Ophichthus sp.1 Ophichthus sp.2 Ophichthus sp.3 Ophichthus sp.4 Ophichthus sp.5 Anguilliformes gen. Anguilliformes gen. Anguilliformes gen. Anguilliformes gen. Anguilliformes gen. Anguilliformes gen.

CW CW CW CW CW

8

10

6, 8 6 8 8 8

sp.1 sp.2 sp.3 sp.4 sp.5 sp.6

6 6 6 10 10 10

Beloniformes Hemiramphidae Hyporhamphus sajori Temminck et Schlegel, 1846

NW

WT

8

Exocoetidae Cypselurus oxycephalus (Bleeker, 1852) Cypselurus angusticeps Nichols et Breder, 1935

CW CW

WW WW

6 6

Mugiliformes Mugilidae Liza haematocheila (Temminck et Schlegel, 1933) Mugil cephalus Linnaeus, 1758

BW BW

WT WW

6 6

Perciformes Apogonidae Apogon lineatus (Temminck et Schlegel, 1842)

CW

WW

10

Sillaginidae Sillago sihama Forskål, 1775 Sillago japonica Temminck et Schlegel, 1842

CW CW

WW WW

Carangidae Decapterus maruadsi (Temminck et Schlegel, 1844) Caranx equula Temminck et Schlegel, 1842

CW CW

WT WW

6, 8 8

Formionidae Formio niger (Bloch, 1792)

CW

WW

8

OW

WW

6

NW NW NW NW NW NW

WT WT WW WW WT WT

6 8, 10 6 8, 10 8

CW

WW

6

CW

WT

8

Coryphaenidae Coryphaena hippurus Linnaeus, 1758 Sciaenidae Collichthys lucidus (Richardson, 1844) Collichthys niveatus Jordan et Starks, 1906 Argyrosomus argentatus (Houttuyn, 1782) Johnius grypotus (Richardson, 1846) Pseudosciaena polyactis (Bleeker, 1877) Pseudosciaena crocea (Richardson, 1846) Leiognathidae Secutor ruconius (Hamilton, 1822) Pomadasyidae Hapalogenys nitens (Richardson, 1844) Mullidae

6 6

8 6, 8

10

6, 8 10 6 6

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W. Ruijing et al. / Acta Ecologica Sinica 30 (2010) 155–165 Table 1 (continued) Taxon

Ecological pattern

Territorial system

Appeared month

Upeneus bensasi (Temminck et Schlegel, 1842) Theraponidae Therapon theraps (Cuvier, 1829)

CW

WW

6, 8, 10

CW

WW

8

Labridae Pseudolabrus gracilis (Steindachner, 1887)

CW

WW

8, 10

Uranoscopidae Uranoscopus japonicus Houttuyn, 1782

CW

WT

Blenniidae Blennius yatabei Jordan et Snyder, 1900

NW

WT

Callionymidae Callionymus olidus Günther, 1873

CW

WT

6

Trichiuridae Trichiurus lepturus Linnaeus, 1758

CW

WT

6, 8, 10

Scombridae Scomber japonicus (Houttuyn, 1782) Scomberomorus niphonius (Cuvier, 1831)

CW CW

WW WT

6, 8, 10 6

Thunnidae Auxis rochei (Risso, 1802)

OW

WW

Stromateidae Pampus argenteus (Euphrasen, 1788)

NW

WW

Nomeidae Psenes cyanophrys Cuvier et Valenciennes, 1833 Cubiceps squamiceps (Lloyd, 1909)

NW NW

WW WW

6 6

Centrolophidae Psenopsis anomala (Temminck et Schlegel, 1844)

NW

WT

6

Gobiidae Amblychaeturichthys hexanema Bleeker, 1853 Glossogobius giuris (Hamilton, 1822) Synechogobius hasta (Temminck et Schlegel, 1850)

BW BW BW

WT WW WT

6 6 8

Taenioididae Odontamblyopus rubicundus (Hamilton, 1822)

BW

WT

6

Scropaeniformes Scorpaenidae Sebastiscus marmoratus (Cuvier et Valenciennes, 1829)

NW

WT

6

Synanceiidae Minous pusillus Temminck et Schlegel, 1842 Minous monodactylus (Bloch et Schneider, 1801)

NW NW

WW WW

6, 10 8

Triglidae Chelidonichthys kumu (Lesson et Garnot, 1830)

CW

WW

6

Platycephalidae Platycephalus indicus (Linnaeus, 1758)

CW

WW

6

Pleuronectiformes Bothidae Engyprosopon grandisquama (Temminck et Schlegel, 1846) Psettina iijimae (Jordan et Starks, 1902)

CW CW

WW WT

Eggs

Soleidae Soleidae gen. sp.

Larvae

6, 8 6, 10

8

6, 8 6

6

6 8 6

Cynoglossidae Cynoglossus joyneri Günther, 1878 Cynoglossus abbreviatus (Gray, 1832) Cynoglossus semilaevis Günther, 1873

NW CW NW

WT WT WT

6, 8 6 10

Tetraodontiformes Aracanidae Kentrocapros aculeatus (Houttuyn, 1782)

NW

WW

6

Tetraodontidae Lagocephalus inermis (Temminck et Schlegel, 1847)

NW

WW

8

8

Note: BW, brackish water; NW, neritic water; CW, coastal water; DW, deep water; OW, oceanic water; WW, warm water; WT, warm temperature.

K. aculeatus and C. joyneri, accounted for 23.44% and 10.03%, respectively; Argyrosomus argentatus and T. lepturus accounted for 6.64% and 5.15%, the proportions of the other 18 species were all less than 5%; the higher frequencies were found in Uranoscopus

japonicus (27.59%) and T. lepturus (20.69%), the frequencies of S. elongate and C. joyneri both were 13.79%, E. japonicus, P. indicus, S. niphonius and C. hippurus all were 10.34%, the frequencies of the other 15 species were less than 7%.

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Table 2 Dominant species, important species and main species of ichthyoplankton in each survey. Species

June

Engraulis japonicus Cynoglossus joyneri Trichiurus lepturus Kentrocapros aculeatus Uranoscopus japonicus Argyrosomus argentatus Saurida undosquamis Trachinocephalus myops Coryphaena hippurus Saurida elongata Amblychaeturichthys hexanema Sillago japonica Platycephalus indicus Scomberomorus niphonius Sillago sihama Johnius grypotus Gonorhynchus abbreviatus Scomber japonicus Pseudosciaenas polyactis Collichthys niveatus Synechogobius hasta Stolephorus commersonii Anguilliformes gen. sp.4 Upeneus bensasi Minous pusillus Apogon lineatus Pseudolabrus gracilis Anguilliformes gen. sp.5

R

IRI

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

26,674 146 112 85 75 73 67 58 52 42 32 31 30 22 11

August

October

R

R

IRI

1 5 4

5829 263 683

9 8 10 12

46 48 40 23

7

62

IRI 2

819

6

179

34 50

33 32 31 30

4

325

29

9 5

25 267

28

Legend

100

(ind./hual) 0 1-10 11-50

50

27 120

121

122

123

124

125

126

Fig. 3. The fish egg abundance distribution in August 2006. 14 3 2 6 11 13

10 688 1627 89 35 16

1

4818

15

13

14

15

3 7 8 10 11 12 13

733 59 34 25 25 17 17

Note: R, ranking.

There were 213 fish eggs collected in August, accounted for 17.75% of total fish eggs, the frequency of fish egg was 51.72%. The average density of fish egg was 7.3 ind/station. Fish eggs mainly distributed station 8-9 and 8-10, which formed the distributed area of S. undosquamis, C. joyneri, T. lepturus and the other 4 species with average density 36.5 ind/station; in station 8-22, 8-23 and 8-24, there were S. japonicus, E. japonicus, T. lepturus and the other 4 species with 16.7 ind/station, and station 8-25, 8-26, 8-28 and 8-29 were the distributed area of T. lepturus, U. japonicus and the other 4 species with average density 13.4 ind/station; in station 8-21, T. lepturus egg was 11 individuals, Collichthys niveatus egg was 4 individuals, S. japonicus egg was 3 individuals; 1–2 fish egg was found in the other 4 stations (Fig. 3).

34

Fish eggs included 15 species, most of them were T. lepturus, accounted for 32.39% of the total fish egg in the survey, then were S. japonicus, S. undosquamis and C. joyneri, accounted for 11.74%, respectively; E. japonicus, Pseudosciaenas polyactis and U. japonicus accounted for 8.92%, 8.45% and 6.57%, respectively; and the proportions of the other 8 species were all less than 5%; the frequency of T. lepturus (20.69%) was higher than that of the other species, then were C. joyneri, E. japonicus, C. niveatus, P. polyactis and S. japonicus (the frequencies were 13.79%, respectively), the frequencies of Saurida tumbil and U. japonicus were 6.90%, respectively; the frequencies of the other 7 species were all less than 5%. There were 249 fish eggs collected in October, accounted for 20.75% of total fish eggs, the frequency of fish egg was 36.00%. The average density of fish egg was 10.0 ind/station. Fish eggs mainly distributed in station 10-15, 10-1 and 10-2, formed two distributed areas, one included S. undosquamis and the other 2 species with average density 114 ind/station, the other was mainly J. grypotus, S. elongate and T. lepturus with average density 57.5 ind/station; in addition, 12 fish eggs was found in station 10-22, including 11 T. lepturus eggs and 1 S. japonicus egg, there were just 1–3 fish eggs in the other 5 stations (Fig. 4). There were just 8 fish species eggs, most of them were J. grypotus and S. undosquamis, accounted for 39.76% and 39.36% of the total fish eggs in this survey; then were T. lepturus and S. elongate, accounted for 7.23% and 6.83%, respectively; the proportions of C. niveatus, S. japonicus, E. japonicus and C. semilaevis were less than 5%; the frequency of T. lepturus (24.00%) was higher than that of the other species, then were J. grypotus (12.00%), S. undosquamis (8.00%) and S. japonicus (8.00%), the frequencies of the other 4 species were 4.00%, respectively.

50

33 32 31

Legend (ind./hual)

30

0 1-10

29

11-50 51-100

100

28

101-200

50

> 200

27 120

121

122

123

124

125

126

Fig. 2. The fish egg abundance distribution in June 2006.

3.3.2. Quantity of fish larvae and juveniles and their distribution There were 1162 fish larvae and juveniles collected in June, accounted for 45.13% of total amount of fish larvae and juveniles in three surveys; the frequency of fish larvae and juveniles was 62.07%, and the average density of fish larvae and juveniles was 40.1 ind/station. Fish larvae and juveniles mainly distributed station 6-10, 6-11, 6-12, 6-13, 6-16 and 6-17, there was concentrated area of the dominant species E. japonicus and the other 13 species with average density 160.2 ind/station; station 6-21, 6-22, 6-23 and 6-24 were the distributed area of E. japonicus, T. myops and the other 8 species with average density 21.3 ind/station, station 6-27, 6-28 and 6-29 were the distributed area of E. japonicus and A. rochei and the other 10 species with average density 19.0 ind/station, the distributed area of E. japonicus, Amblychaeturichthys hexanema and the other

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2 species was station 6-3 and 6-4, and their average density was 19.0 ind/station; in addition, E. japonicus juveniles was 13, 5 and 3 individuals in station 6-25, 6-19 and 6-15, respectively (Fig. 5). There were 30 fish larvae and juveniles species, E. japonicus was the absolutely dominant species in the survey, accounted for 91.65% of the total amount of fish larvae and juveniles in the survey, the amount of the other 29 species was less than 5% of total amount of fish larvae and juveniles; the frequency of E. japonicus (51.72%) was higher than that of the other species, then were A. hexanema (17.24%) and Upeneus bensasi (10.34%), the proportions of the other 27 species were less than 7% that of total amount of fish larvae and juveniles. There were 1316 fish larvae and juveniles collected in August, accounted for 51.11% of total amount of fish larvae and juveniles in three surveys; the frequency of fish larvae and juveniles was 68.97%, and the average density of fish larvae and juveniles was 45.4 ind/station. There were four distributed areas of fish larvae and juveniles, the highest densities (159.0 ind/station) distributed area were found in station 8-25, 8-26, 8-27, 8-28 and 8-29, A. argentatus and S. elongate were the main species; then were the distributed area of station 8-12, 8-13, 8-17 and 8-21, there were 15 species in this distributed area with the average density was 58.0 ind/station, and G. abbreviatus and E. japonicus were the main species; the average density was 47.8 ind/station in station 8-14, 8-15, 8-18 and 8-19, E. japonicus and Synechogobius hasta were the main species in this distributed area; in station 8-1, 8-2, 8-3, 8-6, 8-7 and 8-

8, A. argentatus and C. joyneri were the main species, and the average density was just 16.2 ind/station (Fig. 6). There were 23 fish larvae and juveniles species, the dominant species was G. abbreviatus accounted for 66.34% of the total amount of fish larvae and juveniles in this survey; then was E. japonicus (16.19%), Saurida elongata (6.00%), the other 20 species were less than 5%. E. japonicus occupied the highest frequency (34.48%), then were S. hasta, U. bensasi and T. myops, were 13.79%, respectively; Sillago sihama, A. argentatus, G. abbreviatus, S. elongate and M. monodactylus were 10.34%, respectively; the proportion of the other 14 species were no more than 7%. There were 97 fish larvae and juveniles collected in October, accounted for 3.77% of total amount of fish larvae and juveniles in three surveys; the frequency of fish larvae and juveniles was 76.00%, and the average density of fish larvae and juveniles was 3.9 ind/station. There were two distributed areas of fish larvae and juveniles, the distributed area of E. japonicus, S. commersonii and the other 9 species mainly included station 10-12, 10-15, 10-16, 10-17, 1019, 10-20 and 10-21, and average density was 9.0 ind/station in this area; the average density of distributed area of station 10-1, 10-3, 10-4, 10-5, 10-6 and 10-7 was 4.2 ind/station, mainly included S. commersonii and the other 4 species; the amount of fish larvae and juveniles was 1–3 individuals in the other 6 stations (Fig. 7). A total of 14 fish larvae and juveniles species were collected in this survey, the amount of E. japonicus and S. commersonii was

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more than that of the other species, accounted for 29.90% and 27.84%, respectively; then were Anguilliformes gen. sp.4, S. elongate and J. grypotus, accounted for 7.22%, 6.19% and 5.15%, respectively; the other 9 species accounted less than 5%. The frequency of E. japonicus and S. commersonii were highest, were 24.00%, respectively, then were S. elongate (16.00%) and J. grypotus (12.00%), the frequency of the other 10 species accounted less than 8%.

August 2006 was lower than that in June, which was contrary to the normal conditions. Second, the extension of the CDW was mainly in the southeast direction instead of the northeast direction as normal years. Furthermore, the off-shore area was dominated by a large tongue-like saline inflow, which was closer to the mouth of the Changjiang River than the June survey. The surface salinity off the estuary was even higher in October than in the preceding two surveys for the duration of drought in the drainage basin of the Changjiang River (Fig. 9 left). The surface salinity in most of the stations exceeded 30 PSU except for the station in the west end of the cross-section 30°N.

3.4. Physical environment of the spawning ground 3.4.1. Sea surface temperature On June 2006 (Fig. 8 left), the sea surface temperature was relatively high in the south part of the investigating area than in the south part. The isotherm was along the meridian direction and shows a tongue-like pattern. It was lower than 16 °C in the northeastern part of these areas where is deeper than 50 m; while increasing to 19–20 °C outside the mouth of the Changjiang River and reaching 20–23 °C off the northern coast of the Zhejiang province. There was a strong horizontal temperature gradient between the isotherms 17–19 °C. From June to August, the temperature increased fast during the period, while its gradient decreased (Fig. 8 middle). The most of the investigating off-shore areas were higher than 29 °C with maximum value exceeding 30 °C in east tip of the cross-section along 32°N, in contrast the near-shore was less than 28 °C due to the frequent upwelling events in all summer seasons. In October, the isotherm pattern was similar to that in June, both of which show a distinct tongue-like water mass coming from the south, but different from that in August (Fig. 8 right).

4. Discussion 4.1. Causes of variability of the physical environment The big change in the physical environment of the spawning ground in the Changjiang River estuary and adjacent areas was at first a direct response to the climate change in the drainage basin of the river. In detail, the middle-upper reaches of the river met a severe drought situation during the normal rainy season in 2006. The average precipitation decreased by 30–50% in the river valley from June to August. The situations in the Chongqing and Sichuan depression were even worse during these periods when the precipitations are down by 50–80%. For example, the mean precipitation was only 89.6 mm in the whole basin and the river level in the Nanjing hydrological station descended to the minimum value 3.90 m in the history [23]. The minor reason was the water storage in the Three Gorges Reservoir from September 20 to October 29, which accounted for about 13% reduction of the freshwater discharge [23]. Due to the above two factors, the mean flux through the Datong station was down by 6%, 24%, 38%, 54% and 58%, respectively from June to October with comparison to the multi-year average records. The tremendous reduction in the fresh water discharge of the Changjiang River resulted in the significant retreat of the river plume and consequently the saline water incursion. A brief comparison was conducted in the region from 30°300 to 32°000 N along 122°300 E in June and August: the sea surface salinity was 25 and 29–31 PSU in 2006, while the minimum (maximum) value was 10(29) and 15(26) in 1986; on the other hands, the SST was 19–20 and 28 °C at that region in 2006 in contrast to 23–26 and 25–28 in 1986 [24]. In general, the water was remarkable saline in summer of 2006; for temperature, it was relatively low in June while much higher in August in 2006 comparing with the year of 1986. The year-to-year variability was related mainly to the great reduction of the freshwater runoff which corresponded to

3.4.2. Sea surface salinity It is well known that the fresh water of the Changjiang River forms a plume named as Changjiang Diluted Water (CDW), after flowing into the East China Sea and mixing with ambient water. According to the measurements in June, the plume was still small and constrained to the near-shore areas (Fig. 9 left). The minimum surface salinity sampled in this time was only 24 PSU and there was a strong salinity front surrounding the river mouth in curve shape in the west side of 123°E. There was also a tongue-like saline water incursion from the southeast of the investigating area where was influenced by the Kuroshio and its branches. Comparing with the historical surveys, the most significant variations was the surface salinity value and distribution in August (Fig. 9 middle). First, the measured minimum salinity was large than 25 which could be explained by the tremendous reduction of the Changjiang River discharge [22]. According to the observations at Datong hydrological station, the freshwater discharge on

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the long endured abnormal drought and high temperature weather in the drainage basin.

4.2. Species composition and changes of ecotypes About the classification of ecotype of ichthyoplankton in estuaries, according to the adaptability of species to temperature and salinity and characteristics of species distribution, freshwater type, brackish water type (including estuaries fishes), coastal type and neritic type (including ocean water species and deep water species) in the Changjiang River estuary and its adjacent waters were determined by Yang et al. [12] and Yang [13] for annual survey from August 1985 to August 1986, Zhu et al. [14] for the spring survey in 1999 and Shan et al. [15] for the autumn survey in 2002 and 2003; Liu et al. [18] reported estuaries type, coastal type and neritic type of ichthyoplankton determined by two-way indicator species analysis in the Changjiang River estuary and its adjacent waters in spring survey in 1999 and 2001; and fish larvae and juveniles in the estuaries of the southwestern part of Australia and southeastern part of Africa were divided into opportunists, stagglers, estuarine, diadromous and freshwater by Potter et al. [25] according to the habitat of fish larvae and juveniles; in the studies of ichthyoplankton in Chikugo estuary, Islam et al. [26] reported oligohaline (salinity 0.5–5), mesohaline (salinity 5–18), polyhaline (salinity 18–30) and euryhaline by the adaptability of species. In the present study, in order to compare with the results of Yang et al. [12] and Yang [13], so fish larvae and juveniles in the Changjiang River estuary and its adjacent waters in 2006 were divided into brackish water species (including estuaries species), coastal water species and neritic water species (including ocean water species and deep water species). The amount of freshwater species reduced in the survey when compared with the results by Yang et al. [12] and Yang [13]. This was caused by the decrease of freshwater from the Changjiang River, and the reduction of freshwater distribution for high salinity water from offshore. In addition, this also was closely connected with no stations in coastal waters. In brackish water species, Megalops cyprinoides, Trachidermus fasciatus, Coilia mystus, Coilia ectenes, Salangidae and Takifugu spp. were not collected in this survey. In neritic water species, Sardinella zunasi, Sardinops melanostictus, Thryssa kammalensis, Thryssa mystax and Hexagrammos otakii were not collected, S. taty was collected 1 individual in station 820 (total length 15.8 mm), and 29 S. commersonii (total length 32.0–42.0 mm) were collected in coastal shallow waters in October.

In coastal water species, Ilisha elongate, Konosirus punctatus, Sphyraena pinguis, Lateolabrax japonicus, Priacanthus macracanthus, Paralichthys olivaceus, Pleuronichthys cornutus, Zebrias zebra, Paraplagusia japonica, Cynoglossus interruptus, Cynoglossus sinics, Cynoglossus melampetalut, Cynoglossus gracilis were not collected in the survey. The brackish species T. fasciatus was warm water species, and spawning in the cave with stone and shelf and egg mass was stick to the wall of cave, the spawning season was from middle February to middle March [27]. So the surface horizontal trawl did not collect its egg and fish larvae and juveniles for missing its spawning season; M. cyprinoides was warm water species in upper and middle coastal waters, widely distributed in tropic and sub-tropic water areas in Indian Ocean and Pacific Ocean [28], so was in the East China Sea and the South Sea [29,30], and it spawn in the shallow water of coast, its egg was demersal egg, so the surface horizontal trawl did not collect its egg, and leptocephalus larval was mainly found in the offshore waters of estuaries [31,32], when their metamorphosis finished, then fish larvae and juveniles entered into freshwater of estuaries [33,34], so its leptocephalus larvae and juveniles were not collected in the survey for not covering the coastal waters and freshwater area in the Changjang River. In estuaries fishes, Salangidae fishes spawning time was from earlier March to earlier May, and the hatching time was relative long, such as the hatching time of Hemisalanx prognathus was 285 h (about 12 days) at temperature 11.5–16.0 °C [35]; the spawning season of C. mystus and C. ectenes was from later April to later August [36], though this survey time was consist with the spawning season of Salangidae fishes, C. mystus and C. ectenes, but the salinity for Salangidae fishes, C. mystus and C. ectenes were 0.12–12.0 and 0.1– 15.0, respectively [12], so their spawning ground might distribute in coastal waters in estuaries, it was just a little possibility to collect their fish egg, larvae and juveniles for not covering the coastal waters. The spawning time of H. otakii was from October to November, and its egg was demersal egg, the hatching time was 528–567 h (22–24 days) at 11.8–13.6 °C [37]; the spawning time of P. cornutus was from middle November to later December, and its egg was pelagic egg [38], so it was impossible to collect the fish egg, larvae and juveniles of the two fishes, even their fishery resource was in better condition. The spawning time of S. melanostictus was from later April to later June [36]; the spawning time of L. japonicus was from earlier August to earlier November, and spawning season was from earlier October to later October [39]; the spawning time of P. olivaceus and Z. zebra was from middle May to earlier July and from middle May to middle July, respectively [36]; the spawning time of S. pinguis

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was from April to June, and its spawning time was from July to August in the Yellow Sea [40]; the spawning time of P. macracanthus was from July to September in the East China Sea [41]; Takifugu fishes egg were demersal egg, Takifugu obscurus, Takifugu pardalis, Takifugu rubripes spawning time were from May to June, May to July and April to June, respectively [42]; P. japonica spawning time was from June to August [43]; but no more information about C. interruptus, C. sinics, C. melampetalut, C. gracilis were found. The spawning season of the above-mentioned species was consist with this survey time, but no fish egg, larvae and juveniles were collected, which might be closely related to the biomass of these species. In the fishery resource bottom trawl of this survey, the catch of these species occupied small proportion, even some species were not collected in the survey, such as S. melanostictus, Lateolabrax japonica, P. macracanthus, P. olivaceus, C. interruptus, C. melampetalut and so on [44]. The coastal species S. zunasi, T. kammalensis, T. mystax, S. taty and S. commersonii and inshore species I. elongate, K. punctatus were not collected or just a few individuals were found in the survey, these fish species spawn in the earlier and middle April, and spawning time reached to later June (S. taty and K. punctatus), later July (K. punctatus and S. zunasi), later August (T. kammalensis and T. mystax) and later October (S. commersonii) [13,45–48]. This survey was in the spawning time of these species, excluding I. elongate, S. zunasi, S. taty, K. punctatus, T. kammalensis, T. mystax, S. commersonii were still collected a few individuals in the catch of fishery resource bottom trawl [44], but fish egg, larvae and juveniles of these fishes were hardly not found in the survey, and the composition of coastal species and inshore species also were changed. 4.3. Variations of spawning ground in the Changjiang River estuary waters The Changjiang River estuary (the western part of 31°000 N, 122°300 E) and its adjacent shallow waters was controlled by the main waters of the Changjiang River freshwater and the northern runoff of the Qiantangjiang River in 1986, and characterized by low salinity (not beyond 26), high turbidity and low surface water temperature (22–29 °C) [12,13,24]. It was helpful to reproduction for many fishes, such as neritic water species S. zunasi, T. kammalensis, T. mystax, S. taty, S. commersonii, and coastal water species I. elongate, K. punctatus and so on [12,13]. The surface water salinity in the Changjiang River estuary and its adjacent waters (the western part of 122°300 E) in June 2006 was higher than that in June 1986, but the surface water temperature decreased 4–6 °C; The surface water salinity in August and October in 2006 was higher than that in the corresponding months in 1986, which was caused by the decrease of the freshwater of the Changjiang River and high salinity water from offshore to coastal waters. So the environmental factors (e.g. salinity and temperature) was changed in this sea areas, which caused the spawning grounds of above-mentioned fish species were greatly changed, particularly S. commersonii, it was necessary that temperature was beyond 21.0 °C in spawning ground [24], so no S. commersonii eggs were collected in the survey. 4.4. Application of IRI to determine the dominant species of ichthyoplankton IRI was firstly introduced by Pinkas et al. [19], combined with individuals, composition of biomass and the frequency, which were widely used to determine community structure of fish, dominant species gradient of feeding ecology [20,21,49–51]; the individual size of ichthyoplankton was very small, so we could think about the amount of individuals and the frequency [14,15,18] to determine the dominant species of ichthyoplankton. The develop-

mental stages of ichthyoplankton were different transient stages in the characteristics of biology and ecology in fish life history, particularly the amount of fish egg, including the effects of the fertilized rate, the survival rate of embryo development, hatched rate and the catch rate by enemy animal [52–58], so the amount of fish larvae and juveniles was far less than the amount of fish egg. For example, 12 days after hatching Engraulis encrasicholus ponticus (total length 12 mm) in Black Sea coastal waters was just 0.15% of the original amount of fish egg [59], namely just 15 fish larvae and juveniles survived from 10,000 fish eggs; the mortality of Scomber scombrus was 99.2% from the hatched larvae to the total length 8 mm fish larvae [60]; the survival individuals of 43 days after hatching Sardinops caerulea (average standard length 21.25 mm) was 88 and 113 from 100,000 fish eggs in 1950 and 1951 [61]. In the sequence of development, the development of fish larvae and juveniles delayed the development of fish egg, so the distribution patterns of fish larvae and juveniles was not equal to that of fish egg in the survey area. So the distribution patterns of one fish larvae and juveniles was not equal to the distribution patterns of one fish egg according to their characteristics of biology and ecology. In the survey of spawning ground, one species, fish egg just was caught in some stations, or fish larvae and juveniles was just collected in some stations, or fish egg, larvae and juveniles were found in one station. In the present study, the IRI, combined with the characteristics of biology and ecology, determined the dominant species, the amount and frequency of different stations (station that was just found fish egg, station that was just found fish larvae and juveniles, station that fish egg, larvae and juveniles were simultaneously found) calculated according to formula (5), which better showed the regulations of biology and ecology in fish egg, larvae and juveniles, and better elucidated the significance of IRI, this was the significant difference between the present study and the previous report [14,15,18].

Acknowledgements This study was supported by the National Key Basic Research Program from the Ministry of Science and Technology of China (2006CB400600), the National Natural Science Foundation of China (Grant Nos. 30490233 and 40706018), the Natural Science Foundation of Zhejiang Province (Grant No. Y507229), and Yellow and Bohai Seas scientific observation and experiment station for fishery resources and environment, Ministry of Agriculture. We greatly appreciated the captain, the chief engineer, crew aboard the R/V Beidou and colleagues for their support in collecting samples.

References [1] R.Y. Liu, B.Z. Luo, Y.H. Cui, et al., Effects of the Three Gorge Project on estuarine biology and fishery resources, in: The leading group of ecological and environmental project of Three Gorges Dam, Chinese Academy of Sciences (Ed.), Proceedings on the Impacts of the Three Gorge Project on the Ecology and Environment and Possible Countermeasures, Science Press, Beijing, 1987, pp. 430–446. [2] B.Z. Luo, H.T. Shen, Three Gorge Project and estuarine ecology and environment, Science Press, Beijing, 1994. pp. 1–343. [3] M.J. Kingsford, I.M. Suthers, The influence of tidal phase on patterns of ichthyoplankton abundance in the vicinity of an estuarine front, Botany Bay, Australia, Estuarine, Coastal and Shelf Science 43 (1) (1996) 33–54. [4] C.F. Rakocinski, J. Lyczkowski-Shultz, S.L. Richardson, Ichthyoplankton assemblage structure in Mississippi Sound as revealed by canonical correspondence analysis, Estuarine, Coastal and Shelf Science 43 (2) (1966) 237–257. [5] A. Grioche, P. Koubbi, A preliminary study of the influence of a coastal frontal structure on ichthyoplankton assemblages in the English Channel, ICES Journal of Marine Science 54 (1) (1997) 93–104. [6] S.J.M. Blaber, M.J. Farmer, D.A. Milton, et al., The ichthyoplankton of selected estuaries in Sarawak and Sabah: composition, distribution and habitat affinities, Estuarine, Coastal and Shelf Science 45 (2) (1977) 197–208.

W. Ruijing et al. / Acta Ecologica Sinica 30 (2010) 155–165 [7] J.C. Joyeux, Spatial and temporal entry patterns of fish larvae into North Carolina Estuaries: comparisons among one pelagic and two demersal species, Estuarine, Coastal and Shelf Science 47 (6) (1998) 731–752. [8] S. Ramos, R.K. Cowen, P. Réd, et al., Temporal and spatial distributions of larval fish assemblages in the Lima estuary (Portugal), Estuarine, Coastal and Shelf Science 66 (1–2) (2006) 303–314. [9] R.J. Wan, S. Sun, The category composition and abundance of ichthyoplankton in the ecosystem of the Yellow Sea and the East China Sea, Acta Zoologica Sinica 52 (1) (2006) 28–44. [10] F.G. Zhang, G.F. Yang, Z.L. Shen, Effect of the Three Gorge Project on hydrographical, hydrochemical and sedimentary environments of the Changjing River estuary, in: The leading group of ecological and environmental project of Three Gorges Dam, Chinese Academy of Sciences (Ed.), Proceedings on the Impacts of the Three Gorge Project on the Ecology and Environment and Possible Countermeasures, Science Press, Beijing, 1987, pp. 369–402. [11] P. Morais, M.A. Chícharo, L. Chícharo, Changes in a temperate estuary during the filling of the biggest European dam, Science of the Total Environment 407 (7) (2009) 2245–2259. [12] D.L. Yang, G.Z. Wu, J.R. Sun, The investigation of pelagic eggs, larvae and juveniles of fishes at the mouth of the Changjiang River and adjacent areas, Oceanologia et Limnologia Sinica 21 (4) (1990) 346–353. [13] D.L. Yang, Fish eggs and larvae, in: B.Z. Luo, H.T. Shen, et al. (Eds.), Three Gorges Project and Estuarine and Environment, Science Press, Beijing, 1994, pp. 224–238. [14] X.H. Zhu, D. Liu, X.S. Sha, Relationship between community structure of ichthyoplankton and environmental factors in the estuary of Changjiang River in spring, Studia Marina Sinica 44 (2002) 169–179. [15] X.J. Shan, W.W. Xian, Y.F. Wu, Dynamic changes in the ichthyoplankton community structure after the sluice of the Three-Gorges Dam, Periodical of Ocean University of China 35 (6) (2005) 936–940. [16] M. Jiang, X.Q. Shen, Y.L. Wang, et al., Species of fish eggs and larvae and distribution in Changjiang estuary and vicinity waters, Acta Oceanologica Sinica 28 (2) (2006) 171–174. [17] J.H. Wang, Y.W. Sun, C.C. Liu, et al., The ichthyoplankton resource investigation in Changjiang Estuary, Journal of Marine Sciences 25 (4) (2007) 40–50. [18] S.D. Liu, W.W. Xian, D. Liu, Characteristics of ichthyoplankton assemblages in Yangtze estuary and adjacent waters in spring, Chinese Journal of Applied Ecology 19 (10) (2008) 2284–2292. [19] L. Pinkas, M.S. Oliphant, I.L.K. Iverson, Food habits of albacore, bluefin tuna, and bonito in California waters, California Department of Fish and Game Fish Bulletin 152 (1971) 1–105. [20] J.S. Cheng, The structure and diversity of fish community in the offshore of the Bohai Sea, Acta Oceanologica Sinica 25 (Supp. 1) (2003) 165–170. [21] J.S. Cheng, L.F. Yu, The change of structure and diversity of demersal fish communities in the Yellow Sea and East China Sea in winter, Journal of Fisheries of China 28 (1) (2004) 29–34. [22] F. Zhou, J.L. Xuan, X.B. Ni, et al., A preliminary study on variations of the Changjiang Diluted Water between August 1999 and 2006, Acta Oceanologica Sinica 31 (4) (2009) 1–12. [23] Y.F. Guo, Q.Y. Bao, Y. Du, Water level analysis of the Nanjing Changjiang River section during the droughty season from August to September in 2006. Jiangsu Water Resources (10) (2007) 21–23. [24] G.Z. Wu, The ecological characteristics of distribution of eggs, larvae and juveniles of the Engraulis japonicus (Temminck and Schlegel) and Anchovielle commersonii (Lecépède) in the Changjiang River estuary, Oceanologia et Limnologia Sinica 20 (3) (1989) 217–229. [25] I.C. Potter, L.E. Beckley, A.K. Whitfield, et al., Comparisons between the role played by estuaries in the life cycles of fishes in temperate Western Australia and Southern Africa, Environmental Biology of Fishes 28 (1–4) (1990) 143– 178. [26] M.S. Islam, M. Tanaka, Spatial variability in nursery functions along a temperate estuarine gradient: role of detrital versus algal trophic pathways, Canadian Journal of Fisheries and Aquatic Sciences 63 (8) (2006) 1848– 1864. [27] Z.J. Zang, Trachidermus fasciatus Heckel, in: C.Y. Zhao, R.Z. Zhang, et al. (Eds.), Fish Eggs and Larvae in the Offshore Waters of China, Shanghai Science and Technology Press, Shanghai, 1985, pp. 179–180. [28] J.S. Nelson, Fish of World, second ed., John Wiley, New York, 1984. p. 523. [29] Q.W. Meng, J.X. Su, X.Z. Miao, Systematics of Fishes, China Agriculture Press, Beijing, 1995. pp. 126–127. [30] S.Y. Zhang, Fauna Sinica, Osteichthyes, Acipenseriformes, Elopiformes, Clupeiformes, Gonorhychiformes, Science Press, Beijing, 2001. pp. 47–49. [31] N. Mochioka, Elopidae, in: M. Okiyama (Ed.), An Atlas of the Early Stage Fishes in Japan, Tokai University Press, Tokyo, 1988, p. 17. [32] W.N. Tzeng, C.E. Wu, Y.T. Wang, Ago of Pacific Tarpon, Megalops cyprinoides, at estuarine arrival and growth during metamorphosis, Zoological Studies 37 (3) (1998) 177–183. [33] W.N. Tzeng, S.Y. Yu, Occurrence of the leptocephalus larvae of Elops hawaiensis and Megalops cyprinoides in the Gong-shy-tyan River estuary of north Taiwan with reference to some ecological and taxonomic aspects, in: Proceeding of the

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42]

[43] [44]

[45]

[46]

[47]

[48]

[49]

[50] [51] [52] [53] [54]

[55] [56]

[57]

[58]

[59]

[60]

[61]

165

Symposium on Marine Biological Science, Biology Research Center, Nation Science Council Monograph Series, vol. 14, 1986, pp. 165–176. D. Coates, Observations on the biology of Tarpon, Megalops cyprinoides (Broussonet) (Pisces: Megalopidae), in the Sepik River, Northern Papua New Guinea, Australian Journal of Marine and Freshwater Research 38 (4) (1987) 529–535. Z.J. Zang, Hemisalanx prognathus Regan, in: C.Y. Zhao, R.Z. Zhang, et al. (Eds.), Fish Eggs and Larvae in the Offshore Waters of China, Shanghai Science and Technology Press, Shanghai, 1985, pp. 31–32. Z.J. Zang, Coilia mystus (Linnaeus), in: C.Y. Zhao, R.Z. Zhang, et al. (Eds.), Fish Eggs and Larvae in the Offshore Waters of China, Shanghai Science and Technology Press, Shanghai, 1985, pp. 28–30. R.J. Wan, Y.W. Jiang, The species and biological characteristics of the eggs and larvae of osteichthyes in the Bohai and Yellow Sea, Journal of Shanghai Fisheries University 9 (4) (2000) 290–297. T. Takita, S. Fujita, Egg development and prolarval stages of the turbot, Pleuronichthys cornutus (Temminck et Schlegel), Bulletin of the Japanese Society of Scientific Fisheries 30 (8) (1964) 613–618. R.J. Wan, R.S. Chen, Reproductive behavior and early development of Lateolabrax japonicus (Cuvier and Valenciennes) in the Bohai Sea, Marine Fisheries Research 9 (1988) 203–211. R.Z. Zhang, Sphyraena pinguis Günther, in: C.Y. Zhao, R.Z. Zhang, et al. (Eds.), Fish Eggs and Larvae in the Offshore Waters of China, Shanghai Science and Technology Press, Shanghai, 1985, pp. 47–48. R.Z. Zhang, Priacanthus macracanthus Cuvier and Valenciennes, in: C.Y. Zhao, R.Z. Zhang, et al. (Eds.), Fish Eggs and Larvae in the Offshore Waters of China, Shanghai Science and Technology Press, Shanghai, 1985, pp. 60–63. Y.W. Jiang, Tetraodontidae, in: C.Y. Zhao, R.Z. Zhang, et al. (Eds.), Fish Eggs and Larvae in the Offshore Waters of China, Shanghai Science and Technology Press, Shanghai, 1985, pp. 188–194. T. Minami, The early life history of a tongue fish Paraplagusia japonica, Bulletin of the Japanese of Scientific Fisheries 48 (8) (1982) 1041–1046. X.S. Jin, X.J. Shan, X.W. Gou, et al., Community structure of fishery biology in the Yangtze River estuary and its adjacent waters, Acta Ecologica Sinica 29 (9) (2009) 4761–4772. H.W. Chang, X.S. Sha, Z.R. Chen, et al., Observations on the egg and larval development of a Clupeid Harengula zunasi Bleeker, in: China Ichthyological Society (Ed.), Transactions of the Chinese Ichthyological Society, vol. 1, Science Press, Beijing, 1981, pp. 57–64. Z.R. Chen, H.W. Chang, A description of the morphological characters of the eggs, larvae and young of Clupanodon punctatus (T. & S.), Oceanologia et Limnologia Sinica 7 (3) (1965) 205–214. X.S. Sha, H.C. Ruan, The habits and morphological development of early stages of Ilisha elongate (Bennett), in: China Ichthyological Society (Ed.), Transactions of the Chinese Ichthyological Society, vol. 2, Science Press, Beijing, 1981, pp. 81–88. H.W. Zhang, Z.R. Chen, H.C. Ruan, On the development of the eggs and larvae of Thrissa kammalensis and Thrissa mystax, Acta Zoologica Sinica 28 (2) (1982) 183–189. J.Y. Deng, T.X. Meng, S.M. Ren, et al., Species composition, abundance and distribution of fishes in the Bohai Sea, Marine Fisheries Research 9 (1988) 11– 89. J.Y. Deng, T.X. Meng, S.M. Ren, Food web of fishes in the Bohai Sea, Marine Fisheries Research 9 (1988) 151–171. X.H. Zhu, J.M. Yang, Q.S. Tang, Study on characteristics of fish community structure in Bohai Sea, Oceanologia et Limnlogia Sinica 27 (1) (1996) 6–13. M.C. Yin, Fish Ecology, China Agriculture Press, Beijing, 1995. pp. 132–151. M.D. McGurk, Natural mortality of marine pelagic fish eggs and larvae: role of spatial patchiness, Marine Ecology Progress Series 34 (1986) 227–242. A. Marconata, D.Y. Shapiro, Sperm allocation, sperm production, and fertilization rates in the bucktooth parrotfish, Animal Behavior 52 (1996) 971–980. J.R. Hunter, C.A. Kimbrell, Egg cannibalism in the northern anchovy, Ehgraulis mordax, Fishery Bulletin 78 (1980) 811–816. R. Toesen, Predation on the eggs of Norwegian spring spaened herring at a spawning ground outside the west coast of Norway in 1981, ICES Council Meeting 55 (1985) 1–16. P.E. Smith, H. Santander, J. Alheit, Comparison of mortality rates of Pacific Sardine, Sardinops sagax, and Peruvian anchovy, Engraulis ringens, eggs off Peru, Fishery Bulletin 87 (1989) 497–508. P. Pepin, Effect of temperature and size on development, mortality, and survival rates of the pelagic early history stages of marine fish, Canadian Journal of Fisheries and Aquatic Sciences 48 (1991) 503–518. C.Y. Zhao (translated), F.S. Lin, J.X. Ye (proofread), Impairment index of embryonic and larval stages of Black anchovy, Translation Series on Fisheries Research (3) (1963) 1–9. O.E. Sette, Biology of the Atlantic mackerel (Scomber scombrus) of North America, Part I: Early life history, including growth, drift and mortality of the egg and larval population, Fishery Bulletin 50 (38) (1943) 149–237. E.H. Ahlstrom, Distribution and abundance of egg and larval populations of the Pacific sardine, Fishery Bulletin 56 (93) (1954) 83–140.