Distribution and diets of larval and juvenile fishes: Influence of salinity gradient and turbidity maximum in a temperate estuary in upper Ariake Bay, Japan

Estuarine, Coastal and Shelf Science 68 (2006) 62e74www.elsevier.com/locate/ecss

Distribution and diets of larval and juvenile fishes: Influence of salinitygradient and turbidity maximum in a temperate estuary in upper

Ariake Bay, Japan

Md. Shahidul Islam a,*, Manabu Hibino b, Masaru Tanaka a

a Laboratory of Estuarine Ecology, Field Science Education and Research Center, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japanb Aichi Fisheries Promotion Fund, Department of Sea-Farming, 1-3 Ichizanmatu Nakayama, Atsumi-cho, Astumi-gun, Aichi 441-3615, Japan

Received 26 October 2005; accepted 13 January 2006

Available online 10 March 2006

Abstract

We investigated the fish assemblage and distribution, diversity, and diets in relation to copepod prey communities along the Chikugo estu-arine gradient in the Ariake Bay, Japan. Larval and juvenile fish samples, ambient copepod samples were collected and major hydrographicparameters were recorded at seven selected sampling stations (salinity range: 0.4e28.8 psu) during four sampling cruises in spring 2001. Azone of estuarine turbidity maximum (ETM) was identified in the upper part of the estuary which was characterized by low salinity. Two dif-ferent fish and copepod communities based on the spatial distribution patterns were identified: the oligohaline community in the upper estuary,which was associated with the ETM; and the euryhaline community in the lower estuary, downstream of the ETM. The oligohaline fish com-munity was composed of Acanthogobius flavimanus, Acanthogobius hasta, Coilia nasus, Neosalanx reganius, and Trachidermus fasciatus whilethe euryhaline community was composed of Engraulis japonicus and Sebastes inermis. Lateolabrax japonicus was distributed over wide spatialareas. Sinocalanus sinensis was the single dominant member of the oligohaline copepod community while the euryhaline community was dom-inated by Oithona davisae, Acartia omorii and Paracalanus parvus. Strong dietary relationships were identified between fishes and copepods inthe same community. ETM appears to have significant influence on the distribution and abundance of the oligohaline copepod S. sinensis and thisprey copepod appears to have strong influence on the fishes in the oligohaline regions. Most of the fishes were distributed in the low saline upperestuary where they foraged on the single dominant copepod S. sinensis which contributes the majority of the copepod standing biomass of theestuary and thus appear to support nursery for fishes. It was concluded that the ETM-based copepod S. sinensis plays a key role in survival anddistribution of larval and juvenile fishes in Chikugo estuary.� 2006 Elsevier Ltd. All rights reserved.

Keywords: distribution and diet; fish larvae and juveniles; estuarine turbidity maximum; Sinocalanus sinensis; Chikugo estuary

1. Introduction

The estuarine turbidity maximum (ETM) is a ubiquitousfeature in dynamic estuarine ecosystems with substantial im-pacts on abundance and distribution of fishes. Previous studieshave shown that ETM is advantageous for feeding of larvaland juvenile fishes because ETM regions are characterized

* Corresponding author.

E-mail address: [email protected] (Md.S. Islam).

0272-7714/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2006.01.010

by higher prey concentrations. Thus larval and juvenile fishpredators encounter more prey under conditions of elevatedturbidity due to turbulence-induced encounter rates (Roths-child and Osborn, 1988). Moreover, ETM also offers increasedsurvival rates because predators of larval fishes are generallyless frequented in these regions (Parrish, 1989). Consequently,high abundance of larval and juvenile fishes occurs in areas ofturbidity maxima (North and Houde, 2003). At the same time,significantly higher net primary production results in higherzooplankton production in the ETM zones than the upstreamand downstream areas (Laprise and Dodson, 1994; Irigoien

mailto:[email protected]

http://www.elsevier.com/locate/ecss

63Md.S. Islam et al. / Estuarine, Coastal and Shelf Science 68 (2006) 62e74

and Castel, 1997; Roman et al., 2001; Winkler et al., 2003).The role of ETM in estuarine productivity and its relationwith estuarine dependent fishes have been reported in the ma-jor estuarine system such as in the St. Lawrence estuary (La-prise and Dodson, 1989; Dodson et al., 1989; Dauvin andDodson, 1990; Sirois and Dodson, 2000a,b; North and Houde,2003), the San Francisco Bay estuary (Jassby et al., 1995;Bennett et al., 2002), the upper Chesapeake Bay (North andHoude, 2003; Shoji et al., 2005) and in the Dollard-Ems estu-ary in the Netherlands (Jager, 1998). ETM usually correspondsto areas just near the saltfront where freshwater mixes withseawater and, therefore, ETM zones have its characteristiczooplankton communities which are different from that foundin upper freshwater and lower euryhaline marine areas (La-prise and Dodson, 1994; Roman et al., 2001; Winkler et al.,2003). Therefore, it could be expected that the larval and juve-nile fish communities and their dietary relations in the ETMdiffer from the downstream marine assemblage. There havebeen many reports on the processes associated with fish andzooplankton community assemblages in the ETM, suggestingthat elevated abundance of larval and juvenile fishes is relatedto potential prey concentrations; however, spatial comparisonsin fish and copepod community assemblages and dietary rela-tions between ETM and downstream areas have not been suf-ficiently documented.

As in many major estuarine systems of the world (e.g., theChesapeake Bay, the St. Lawrence estuary, the San FranciscoBay, the Gironde estuary), the Chikugo estuary is character-ized by a zone of turbidity maximum in its upper part, the eco-logical characteristics of which differ tremendously from thatin the downstream areas. Previous studies on the fish speciesfrom in Ariake Bay are mono-specific and are largely re-stricted to the distribution patterns and morphological investi-gations. Variations in the community assemblage, diversityand diets of fishes in relation to prey distribution along thespatial gradient have been relatively poorly known. The aimof this study was to characterize the spatial distribution and di-ets of dominant larval and juvenile fishes in relation to preycopepod distribution and dominant hydrographic featuresalong the Chikugo estuary.

2. Materials and methods

2.1. Study area

The Ariake Bay (Fig. 1) is a semi-enclosed and a relativelywell-mixed bay with the highest tidal differences (w6.0 m) inJapan. The Chikugo River is the largest river flowing into theAriake Bay at its western part with the mean width of approx-imately 200 m and mean depth of approximately 6.0 m duringhigh tide. Tidal influences usually reach to around 16 km fromthe river mouth during high tide. Seven sampling stations wereestablished along the axis of the Chikugo estuary (Fig. 1);among them, four stations were within the river (R4, R3,R2, and R1), the other three were outside the river mouthalong the estuary (E1, E2, and E3). River stations variedfrom station R1 at the river mouth to the most upriver site,

R4, which was 16 km upstream from the mouth and experi-enced little seawater influence even at spring high tide. Start-ing from the river mouth, the estuarine stations were situatedon the tidal flat and E3 was the farthest station with the highestsalinity.

2.2. Sample collection and analysis

Hydrographic parameters such as temperature ( �C), salinity(psu), turbidity (NTU) and dissolved oxygen (DO, mg l�1)were recorded on the board during each cruise using an envi-ronmental monitoring system (YSI 650 MDS, YSI Incorpo-rated, USA). Hydrographic parameters were recorded ata minimum of three depths at all stations and the mean valuesare reported. Larval and juvenile fishes were collected by foursampling cruises on 11 March, 23 March, 10 April and 22April 2001. Samples were collected by surface tows of a larvanet (1.3 m mouth diameter, 5 m long, 1 mm mesh at the body,and 0.33 mm mesh at the cod end) equipped with a flow meter.At each station, the net was towed at a depth of about 0.5 mfrom the surface for 10 min against tidal flow; during eachcruise, two fishing casts were made at each station startingat 09:00 hours and finishing before 12:00 hours. Fish sampleswere immediately fixed with 10% formalin solution on thesampling site and transported to the laboratory. Fish larvaeand juveniles were sorted at the laboratory and were identifiedaccording to the lowest possible taxonomic level (Okiyama,1988) and the developmental stages were characterized(Moser, 1984). For each species, all fish were counted andstandard lengths (SL) were measured to the nearest 0.1 mm.From samples containing large numbers, at least 500 fisheswere randomly sub-sampled for measurements. Result offish density was expressed as the number per unit of water vol-ume. Fish diversity was estimated using three complementaryindices. ShannoneWiener Index of diversity (H ) was com-puted as: H ¼ �

PSi¼1 pi ln pi, where H is the Shannon Index

of diversity and pi is the proportion of the total number of in-dividuals occurring in species i. Species richness (S ) was cal-culated as the number of taxa collected during each cruise.Equitability or evenness (E ) was computed as E¼H/ln[S].The evenness index ranges from near 0, indicating that thecommunity is heavily dominated by one species, to 1, indicat-ing that all species have nearly identical abundance.

Numerical abundance and distribution of ambient copepodwas analyzed by collecting samples simultaneously duringeach cruise by oblique towing a plankton net (45 cm mouth di-ameter; 0.1 mm mesh) equipped with a flow meter. Copepodswere identified to the lowest possible taxonomic level and werecounted. Copepod density was expressed as number m�3 ofwater filtered. Copepod dry biomass at each sampling stationwas determined by drying samples at 45 �C for 24 h in a ther-mostat oven and the dry weight was expressed as mg m�3.

Among the fishes collected, eight dominant species,namely, Acanthogobius hasta, Lateolabrax japonicus, Trachi-dermus fasciatus, Engraulis japonicus, Acanthogobius flavima-nus, Coilia nasus, Sebastes inermis, and Neosalanx reganiuswere selected for gut content analysis. Guts of the fishes

64 Md.S. Islam et al. / Estuarine, Coastal and Shelf Science 68 (2006) 62e74

Japan Sea

Pacific Ocean

AriakeBay

Japan

Ariake Bay

33º N

32º30′ N

130º20′ E

R4

R3

R2

R1

E1

E2

E3

ChikugoRiver

N

2 km

Fig. 1. Map of the Ariake Bay and the Chikugo River estuary showing the sampling stations.

were dissected with fine needles under a stereomicroscope.Twenty fishes (depending on availability) of each species ateach station were randomly selected for gut study. The gutswere opened and food organisms were separated from the oe-sophagus to the rectum and were examined under microscope.Prey organisms were counted and identified to the lowest pos-sible taxonomic level according to Chihara and Murano(1997). Feeding intensity was calculated as the total numberof prey items per gut analyzed. Feeding incidence was calcu-lated as the percentage of the number of fishes with foods inrelation to the total number analyzed (number of fishes withprey/total number of fish analyzed� 100); for calculation offeeding incidence, only fishes with identifiable gut contentswere considered.

2.3. Data analysis

Between-station variations in temperature, salinity, turbid-ity, DO, fish density, diversity indices, copepod density and

copepod dry biomass were analyzed by one way analysisof variance (ANOVA). Pearson’s correlation coefficient wascalculated to characterize the relationships between differentparameters. The relationships between fish size and corre-sponding number of prey items occurring in the guts wereassessed by simple linear regression analysis. All analyseswere done using SPSS version 12.0.

3. Results

3.1. Fish assemblage, distribution and diversity

A total of 26,242 larvae and juveniles constituting 27 spe-cies under 15 families were collected (Table 1). However, onlyfive species contributed as much as 99% of the total catch(Table 2). Acanthogobius hasta was the most abundant fishwhich alone contributed as much as 73.0% of the total fishabundance which was followed by Lateolabrax japonicus con-tributing 15.6% and Trachidermus fasciatus contributing


Table 1

Numerical composition of catches of larval and juvenile fishes at each sampling cruise

Family Species 11 March 23 March 10 April 22 April Total %

Ammodytidae Ammodytes personatus e 4 e e 4 0.015

Anguillidae Anguilla japonica 7 5 1 e 13 0.050

Clupeidae Ilisha elongata e e 1 e 1 0.004

Konosirus punctatus e 1 e e 1 0.004

Cottidae Trachidermus fasciatus 300 1375 325 67 2067 7.877

Cyprinidae Unidentified cyprinidae e 1 e e 1 0.004

Pseudorasbora parva 5 e e e 5 0.019

Engraulididae Coilia nasus 9 22 13 e 44 0.168

Engraulis japonicus e 13 199 187 399 1.520

Gobiidae Acanthogobius flavimanus e 34 162 47 243 0.926

A. hasta 6 14,381 3593 1174 19,154 72.990

Eutaeniichthys gilli e e 1 e 1 0.004

Unidentified gobiidae e e e 62 62 0.236

Gymnogobius cylindricus 2 4 e e 6 0.023

G. macrognathus 14 e 10 28 52 0.198

Taenioides rubicundus 1 e 4 1 6 0.023

Tridentiger bifasciatus e 1 e 6 7 0.027

Parachaeturychthys polynema 1 e e e 1 0.004

Leiognathidae Leiognathus nuchalis e 1 e e 1 0.004

Mugillidae Mugil cephalus 3 1 e e 4 0.015

Percichthidae Lateolabrax japonicus 1068 2591 341 86 4086 15.570

Plecoglossidae Plecoglossus altivelis 1 5 4 e 10 0.038

Salangidae Neosalanx reganius 9 14 11 2 36 0.137

Salanx ariakensis e 1 e 3 4 0.015

Scorpaenidae Sebastes inermis 16 16 e e 32 0.122

Sparidae Acanthopagrus schlegeli e e 1 e 1 0.004

Tetraodontidae Takifugu xanthopterus e 1 e e 1 0.004

Total 1442 18,471 4666 1663 26,242 100.0

7.9%. Almost all the dominant fish species showed maximumabundance during late March with gradual decrease until lateApril and the same trend of numerical abundance was ob-served also for the total catch in each cruise. The highest den-sity of fish was recorded at R2 but the spatial variations in fishdensity were not significant and thus showed no correlationwith the hydrographical parameters. Although most of thedominant catch was composed of larvae and juveniles, allspecimens of Coilia nasus and Neosalanx reganius wereyoung-of-the-year (YOY) to adults (Table 2). Since only fewspecies dominated the total fish catch, diversity was generallylow along the estuary; this is evident from the calculated diver-sity indices (Fig. 2). None of the diversity indices showedsignificant between-station variations although the ShannoneWeiner Index and species richness were generally higher in

the oligohaline (R4eR2) than the euryhaline stations (R1eE3) (Fig. 2).

Spatial patterns of fish distribution were highly influencedby salinity. Fish can be divided into two major categoriesbased on their spatial distribution and abundance as: (1) thosedistributed and abundant mainly in the low-to-medium salinezone of the upper estuary (the oligohaline or ‘true-estuarine’assemblage) such as Acanthogobius hasta, Acanthogobius fla-vimanus, Coilia nasus, Trachidermus fasciatus, and Neosalanxreganius; and (2) those distributed and abundant mainly in thezone of higher salinity in the lower estuary (the euryhaline as-semblage) such as Engraulis japonicus and Sebastes inermis(Fig. 3). An intermediate pattern of distribution was repre-sented by Lateolabrax japonicus. This fish was distributedand abundant almost equally over the whole spatial scale

Table 2

Size range, mean (�SD) size, total number and the developmental stages of eight most dominant fish species collected during four sampling cruises

Species Size range Mean (�SD) size N (%) Stage

A. hasta 3.9e15.5 9.0� 3.89 19,154 (73.0) Yolk sack e Juvenile

L. japonicus 13.5e35.0 23.6� 6.65 4088 (15.6) Juvenile

T. fasciatus 6.9e24.8 14.1� 5.27 2067 (7.9) Preflexion e Juvenile

E. japonicus 12.3e30.4 21.0� 5.63 399 (1.5) Flexion e Juvenile

A. flavimanus 11.7e16.6 13.5� 1.87 243 (0.93) Juvenile

C. nasus 70.5e139.0 102.3� 13.72 44 (0.17) Young-of-the-year

S. inermis 10.8e25.6 16.6� 3.57 32 (0.12) Postflexion e Juvenile

N. reganius 39.7e60.7 49.2� 5.73 36 (0.14) Young-of-the-year


0

1

2

3

4

5

6

7

0

0.2

0.4

0.6

0.8

1

0

2

4

6

8

10

12

0

0.2

0.4

0.6

0.8

R4 R3 R2 R1 E1 E2 E3

Sampling stations

HS

Jln

[D

en

sity (100m

-3)]

Fig. 2. Spatial variations in fish density {ln (density 100 m�3)}, ShannoneWiener Index (H ) of diversity, species richness (S ) and evenness (J ) for the

fish community assemblage along the Chikugo estuary; values are mean� SD

derived from four sampling cruises.

studied with two peaks, one in the uppermost station (lowestsalinity) and the other in the lowermost station (highest salin-ity) (Fig. 3).

3.2. Diets

Feeding habits were strongly related to distribution patternsof the fishes and the copepods. A total of 17 prey types wererecorded including those unidentified. Among the prey types,nine species of copepods were recorded that contributed ashigh as 88.8% of the total prey by quantity. Diets of fishesin the oligohaline assemblage were highly dominated by Sino-calanus sinensis (Fig. 4) which is the most dominant oligoha-line copepod. Sinocalanus sinensis contributed 35.1, 65.9,87.7, 99.3%, and as much as 100% of the diet of Acanthogo-bius flavimanus, Trachidermus fasciatus, Neosalanx reganius,Coilia nasus, and Acanthogobius hasta, respectively. In con-trast, fishes in the euryhaline assemblage showed multi-speciesdietary habits and preyed on euryhaline copepods (Fig. 4).Among the prey types of the euryhaline fishes, Acartia omoriiand Oithona davisae were predominant, in association withParacalanus parvus, Pseudodiaptomus marinus, Tortanus der-jugini, O. davisae, and unidentified copepod nauplii. Acartiaomorii contributed 58.0% of the diet of Engraulis japonicusand O. davisae contributed 64.2% of the diet of Sebastes iner-mis. On average, S. sinensis contributed about half (42.9%) ofthe total diets by quantity, followed by A. omorii (13.2%),O. davisae (8.3%), and T. derjugini (7.0%). Since Lateolabraxjaponicus was distributed in all sampling stations, this fishpreyed on both oligohaline and euryhaline copepods (Fig. 4).The fish fed almost exclusively on S. sinensis in the oligoha-line stations (R4eR2) while in the euryhaline stations, thefish fed on a number of copepods mainly dominated byA. omorii, P. parvus, and T. derjugini. Sinocalanus sinensiscontributed 37.3% of the total diets of L. japonicus, followedby A. omorii which contributed 31.9%.

Feeding intensity and feeding incidence for each species ateach station are shown in Table 3. Mean feeding intensity foreach of the species studied was 18.5 (Lateolabrax japonicus),2.2 (Acanthogobius hasta), 22.1 (Trachidermus fasciatus),98.4 (Coilia nasus), 13.1 (Neosalanx reganius), 3.7 (Acantho-gobius flavimanus), 2.6 (Engraulis japonicus), and 2.0 (Se-bastes inermis) and mean feeding incidence for each specieswas 88.3% (L. japonicus), 72.7% (A. hasta), 78.2% (T. fascia-tus), 100% (C. nasus), 100% (N. reganius), 77.1% (A. flavima-nus), 69.7% (E. japonicus), and 60.9% (S. inermis). Highervalues of both feeding intensity and feeding incidence were re-corded in the oligohaline stations of the upper estuary than theeuryhaline stations of the lower estuary (Fig. 5). Linear regres-sion analysis showed no significant relationship between fishsize and feeding intensity in any fish species.

3.3. Ambient copepod assemblage

A total of 11 species of copepods were recorded includingthose unidentified. They were Sinocalanus sinensis, Paracala-nus parvus, Acartia omorii, Pseudodiaptomus marinus,


A. hasta

0

30

60

90

120

A. flavimanus

0

1

2

3

T. fasciatus

0

3

6

9

12

15

E. japonicus

0

1

2

3

N. reganius

0

0.05

0.1

0.15

0.2

0.25

S. inermis

0

0.1

0.2

0.3

C. nasus

0

0.1

0.2

0.3

0.4

R4 R3 R2 R1 E1 E2 E3

L. japonicus

0

2

4

6

8

10

R4 R3 R2 R1 E1 E2 E3

Sampling stations Sampling stations

Fish

d

en

sity (n

um

ber m

-3)

Fig. 3. Spatial variations in the density (number m�3) of the dominant fish species along the Chikugo estuary; Black and white bars represent, respectively, the

oligohaline and euryhaline communities; the shaded bars represent the intermediate type.

Tortanus derjugini, Oithona davisae, Calanus sinicus, Corrya-ceous affinis, Harpacticoida sp., Cyclopoida sp. and unidenti-fied copepod nauplii. Two contrasting copepod communitieswere identified based on the spatial distribution (Fig. 6). Anoligohaline community was recorded in the low salinityregions of the upper estuary (‘true-estuarine’ community;

salinity 0.37e3.1 psu), which was overwhelmingly dominatedby S. sinensis. In contrast, a euryhaline, multi-species copepodassemblage was observed in the high saline lower estuary(salinity 19.7e28.8 psu) which was dominated by O. davisae,A. omorii, P. parvus, and C. sinicus (Fig. 6). Copepod densityshowed significant spatial variations (P< 0.05) with the


Sinocalanus sinensis Cyclopoida Mysidacea

Paracalanus parvus Acartia omorii Oithona davisae

Nauplii Polychaeta Calanus sinicus

Tortanus derjugini Pseudodiaptomus marinus Others

0

25

50

75

100

0

25

50

75

100

0

25

50

75

100

0

25

50

75

100

0

25

50

75

100

0

25

50

75

100

0

25

50

75

100

R4 R3 R2 R1 E1 E2 E3

0

25

50

75

100

R4 R3 R2 R1 E1 E2 E3

Sampling stations

Prey co

mp

ositio

n in

g

uts (%

)

A

B

C

D

E

F

G

H

Sampling stations

Fig. 4. Numerical composition of prey items in the guts of the dominant fish species; AeE, represent the oligohaline fishes (A. hasta, T. fasciatus, C. nasus,

N. reganius, and A. flavimanus, respectively) feeding predominantly on the oligohaline copepods and FeG, represent the euryhaline fishes (E. japonicus and

S. inermis) feeding on euryhaline copepods; H, represents the intermediate type feeding on both prey communities over the whole spatial gradient.

lowest density (6532.7� 494.2 m�3) at R4 and the highest(25 266.3� 7813.5 m�3) at E3 (Fig. 7). A completely differentscenario was observed in the copepod dry biomass whichshowed significant (P< 0.001) spatial variations with thehighest value (78.7� 40.8 mg m�3) at R3 and the lowest value(5.1� 0.23 mg m�3) at E3 (Fig. 7).

3.4. Role of hydrographic environment

Spatial variations in the major hydrographic parametersare presented in Fig. 8. Variations in temperature were not sig-nificant while salinity and turbidity showed significant(P< 0.001) spatial variations. The lowest mean salinity


Table 3

Feeding incidence, numerical composition of food items and size range of different fish species examined

Station (salinity) R4 (0.37) R3 (3.01) R2 (19.67) R1 (25.29) E1 (27.40) E2 (27.80) E3 (28.81)

A. flavimanus No. of fish examined 6 6 4 6 e e e

Size range (SL, mm) 15.47e17.0 15.4e16.7 15.2e16.2 14.1e16.4 e e e

Feeding incidence (%) 83.3 100 25 100 e e eTotal No. of foods 29 28 1 30 e e e

Feeding intensity 4.8 4.7 0.3 5.0

A. hasta No. of fish examined 11 11 6 3 e e eSize range (SL, mm) 12.1e15.6 11.7e14.1 13.0e14.1 13.1e13.1 e e e

Feeding incidence (%) 81.8 63.6 0 0 e e e

Total No. of foods 29 19 0 0 e e e

Feeding intensity 2.6 1.7 0 0

C. nasus No. of fish examined e 16 3 e e e e

Size range (SL, mm) e 104.4e121.0 102.0e114.5 e e e e

Feeding incidence (%) e 100 100 e e e eTotal No. of foods e 1974 220 e e e e

Feeding intensity 123.4 73.3

N. reganius No. of fish examined 5 13 3 e e e eSize range (SL, mm) 40.5e52.5 46.6e56.6 45.2e48.4 e e e e

Feeding incidence (%) 100 100 100 e e e e

Total No. of foods 57 286 18 e e e e

Feeding intensity 11.4 22.0 6.0

T. fasciatus No. of fish examined 18 20 20 3 e e e

Size range (SL, mm) 19.2e22.6 14.6e25.0 13.0e24.2 11.2e13.6 e e e

Feeding incidence (%) 94.4 100 85 33.3 e e eTotal No. of foods 812 667 161 6 e e e

Feeding intensity 45.1 33.4 8.1 2.0

E. japonicus No. of fish examined e e 15 8 11 15 14

Size range (SL, mm) e e 20.3e29.5 16.8e27.8 22.3e29.9 21.8e29.6 25.5e32.0

Feeding incidence (%) e e 40 75 81.82 80 71.43

Total No. of foods e e 21 15 43 53 33

Feeding intensity 1.4 1.9 3.9 3.5 2.4

S. inermis No. of fish examined e e 1 4 3 5 11

Size range (SL, mm) e e 16.8 11.8e17.2 16.8e19.5 18.1e19.4 13.5e20.7

Feeding incidence (%) e e 0 75 66.66 20 81.81

Total No. of foods e e 0 8 2 3 54

Feeding intensity 0 2.0 0.7 0.6 4.9

L. japonicus No. of fish examined 58 64 61 55 48 46 62

Size range (SL, mm) 17.6e28.3 18.4e33.7 18.6e29.6 16.2e32.4 17.2e35.3 17.7e29.2 17.2e28.6

Feeding incidence (%) 93.1 89.1 83.6 72.7 87.5 93.48 98.39

Total No. of foods 887 1889 682 1020 636 719 1631

Feeding intensity 15.3 29.5 11.2 18.5 13.3 15.6 26.3

(0.37� 0.18) was recorded at R4 and the highest (28.8� 0.67)at E3. In contrast, the lowest turbidity (28.8� 13.7) was re-corded at E3 and the highest (258.4� 209.7) at R4. Thus,the ETM occurs at R4 which is the saltfront, the area of1.0 psu isohaline. Strongly significant correlations were ob-served between temperature, turbidity and salinity. Tempera-ture and turbidity had negative correlation (P< 0.01) withsalinity (Table 4) while temperature and turbidity were posi-tively (P< 0.01) correlated (Table 4). These correlations indi-cate that the estuary is characterized by gradients in theseparameters. Fish density as well as none of the diversity indi-ces showed significant correlation with temperature, salinityand turbidity or with prey density and biomass. As expected,dominant oligohaline fishes (Acanthogobius hasta, Acanthogo-bius flavimanus, Trachidermus fasciatus, Coilia nasus, andNeosalanx reganius) showed negative correlation with salinity

and positive correlation with temperature and turbidity (Table 4).In contrast, dominant euryhaline fishes (Engraulis japonicusand Sebastes inermis) showed positive correlations withsalinity and negative correlations with temperature and turbid-ity. Similarly, oligohaline copepod (Sinocalanus sinensis)showed negative correlation with salinity and positive correla-tion with temperature and turbidity in contrast to the euryhalinecopepods (Oithona davisae, Acartia omorii, Paracalanus par-vus) that showed positive correlations with salinity and negativecorrelations with temperature and turbidity. Oligohaline fishesshowed negative correlation with copepod density but positivecorrelation with biomass; in contrast, euryhaline fishes showedpositive correlation with copepod density but negative correla-tion with biomass. Density of oligohaline fishes correlated pos-itively with the density of oligohaline copepod (S. sinensis) andnegatively with the density of euryhaline copepods (O. davisae,


0

13

26

39

52

65

0

20

40

60

80

100

R4 R3 R2 R1 E1 E2 E3

Feed

in

g in

ten

sity

Feed

in

g in

cid

en

ce

Sampling stations

ANOVA

P < 0.05

ANOVA

P < 0.05

Fig. 5. Spatial variations in feeding intensity (number of prey fish�1) and feed-

ing incidence (% of fish with prey items in the gut) of the dominant fish spe-

cies along the Chikugo estuary.

A. omorii, P. parvus). Similarly, density of euryhaline fishescorrelated positively with the density of euryhaline copepods(O. davisae, A. omorii, P. parvus) and negatively with the den-sity of oligohaline copepod (S. sinensis) (Table 4). Both feedingintensity and feeding incidence correlated positively with tem-perature, turbidity, copepod biomass and S. sinensis density andnegatively with salinity and the density of euryhaline copepods.These trends indicate a clear partitioning between two contrast-ing fish communities associated with two contrasting copepodcommunities along the estuary.

4. Discussion

The Chikugo River estuary is a dynamic ecosystem whichsupports relatively high abundances of nearshore fishes. Diver-sity is generally low because the assemblage structure is dom-inated by relatively few species and such patterns are typicalof temperate estuaries and embayments and are consistentwith previous reports on temperate estuaries and coastal areas(Jackson and Jones, 1999; Velez et al., 2005). The number ofspecies and diversity was generally high in the upper estuary

0

20

40

60

80

100

R4 R3 R2 R1 E1 E2 E3

Sampling stations

Co

pep

od

co

mp

ositio

n (%

)

T. derjugini

S. sinensis

P. parvus

P. marinus

O.davisae

Nauplii

Cyclopoida sp.

C.sinicus

A.omorii

Fig. 6. Numerical composition (%) of ambient copepods.

Table 4

Relationships (Pearson’s correlations coefficient) between the density of fishes and copepod and the abiotic environmental factors (**P< 0.01 and *P< 0.05)

Salinity Temperature Turbidity Copepod density Copepod biomass S. sinensis O. davisae A. omorii P. parvus

Temperature �0.976**

Turbidity �0.922** 0.833**

H �0.522 0.599 0.344

S �0.402 0.404 0.423

J 0.029 0.049 �0.350

Fish density �0.029 0.000 0.080

Copepod density 0.461 �0.377 �0.667

Copepod biomass �0.920** 0.918** 0.751* �0.104

L. japonicus �0.326 0.209 0.352 0.149 0.476 0.283 �0.218 �0.550 �0.076

A. flavimanus �0.812* 0.694* 0.926** �0.442 0.711* 0.801* �0.780* �0.709* �0.719*

A. hasta �0.020 �0.012 0.078 �0.537 �0.139 �0.171 0.331 �0.093 0.448

T. fasciatus �0.204 0.191 0.153 �0.446 0.125 0.038 0.122 �0.299 0.224

N. reganius �0.904** 0.964** 0.684* �0.237 0.903** 0.925** �0.905** �0.865** �0.829*

C. nasus �0.754* 0.692* 0.890** �0.404 0.740* 0.746* �0.730* �0.694* �0.680*

E. japonicus 0.806* �0.777* �0.766* 0.823** �0.711* �0.761* 0.704* 0.690* 0.759*

S. inermis 0.695* �0.698* �0.766* 0.869** �0.701* �0.698* 0.762* 0.449 0.539

Feeding intensity �0.764* 0.847** 0.779* �0.106 0.833* 0.765* �0.719* �0.817* �0.621

Feeding incidence �0.741* 0.741* 0.729* 0.171 0.871** 0.803* �0.805* �0.812* �0.794*

S. sinensis �0.980** 0.974** 0.871** �0.326 0.944**

O. davisae 0.933** �0.940** �0.816* 0.230 �0.920**

A. omorii 0.930** �0.922** �0.783* 0.223 �0.957**

P. parvus 0.839** �0.830* �0.736* 0.215 �0.810*


which is consistent with other temperate estuaries (Loneraganet al., 1986; Loneragan and Potter, 1990). Two distinct fishcommunities showed differential distribution patterns basedon the environmental gradient along the estuary. Differentialdistribution patterns and dietary habits of fishes, which wereassociated with the distribution and abundance of copepodprey, were identified along the Chikugo estuary. The estuarywas characterized by gradients in turbidity and salinity. TheETM occurred near the saltfront, 16 km upstream from theriver mouth, which corresponded to the uppermost station inthis study. The ETM was characterized by slightly higher tem-perature but lowest salinity, lowest copepod density but high-est copepod biomass. There were two contrasting fish as wellas copepod communities along the estuary. The oligohalinecommunity of fishes and copepods were associated with theETM zone while the euryhaline communities were associatedwith the downstream coastal marine environment. The ETMappears as an important nursery area for the oligohaline fishcommunity (Acanthogobius hasta, Acanthogobius flavimanus,Coilia nasus, Neosalanx reganius, Trachidermus fasciatus)where larvae are retained in a region of elevated prey concen-trations. ETM influences the distribution of passively trans-ported fish early-life stages as well as Sinocalanus sinensisin the upper estuary. This oligohaline copepod, the majorprey item for the oligohaline fishes appears to strongly influ-ence the distribution of oligohaline fishes.

0

7

14

21

28

35

0

20

40

60

80

100

120

R4 R3 R2 R1 E1 E2 E3

Sampling stations

Bio

mass (m

g m

-3)

Den

sity (x10

3 m

-3)

ANOVA

P < 0.01

ANOVA

P < 0.05

Fig. 7. Copepod density (number� 103 m�3) and dry biomass (mg m�3) in the

environment along the Chikugo estuary showing contrasting spatial patterns;

values are mean (�SD) derived from four sampling cruises.

The roles of ETM in influencing distribution and feeding ofestuarine dependent fish species have been clarified by manyworkers in major estuarine systems. Roman et al. (2001) andNorth and Houde (2003) reported that the ETM region inthe upper Chesapeake Bay is an important nursery area forstriped bass and white perch, where larvae are retained in a re-gion of elevated concentrations of Eurytemora affinis and Bos-mina longirostris, the major prey items of striped bass andwhite perch larvae. Similar to this study, peak abundance ofcertain zooplankton species was reported to be associatedwith the ETM zones in other estuaries. For example, peakabundances of E. affinis were reported within the ETM regionin the Columbia River estuary (Simenstad et al., 1994), theSan Francisco Bay estuary (Kimmerer et al., 1998) and inthe Gironde estuary in France (Castel and Veiga, 1990; Davidet al., 2005). High concentrations of zooplankton occur in the

0

4

8

12

16

20

0

100

200

300

400

500

600

0

5

10

15

20

25

30

R4 R3 R2 R1 E1 E2 E3

Salin

ity (P

SU

)

Tu

rb

id

ity (N

TU

)

Sampling stations

Tem

peratu

re (ºC

)

ANOVA

P < 0.001

ANOVA

P < 0.001

Fig. 8. Spatial variations in temperature, turbidity and salinity showing longi-

tudinal gradient along the Chikugo estuary; values are mean (�SD) derived

from four sampling cruises.


ETM zones because zooplankton are retained within the ETMthrough passive accumulation in this convergence zone (Ro-man et al., 2001) and such high prey concentrations may resultin enhanced encounter rate between fish larvae and prey, pro-moting larval feeding success (Shoji et al., 2005). Encounterrates may be critical factor for larval feeding success becausethe early larval stages of most fishes are characterized by poorswimming ability and visual acuity (Margulies, 1990). First-feeding fish larvae are generally susceptible to starvation,grow faster in high versus low prey concentrations and may re-quire high prey concentrations to offset the energetic cost ofosmoregulation in low salinity waters near the saltfront.Therefore, the early-life histories of the oligohaline fish com-munity may be adapted to exploit the consistently high con-centrations of zooplankton that occur within the ETMregion. The importance of prey concentrations in the feedingsuccess of larval and juvenile fishes has been discussed ina number of previous studies. Shoji et al. (2005), for example,reported that prey concentration was the most important small-scale factor affecting feeding success of white perch in theChesapeake Bay turbidity maximum and Sirois and Dodson(2000b) found that growth of larval rainbow smelt Osmerusmordax was enhanced at high turbidities and high preyconcentrations.

There has been no comprehensive information on multi-species distribution patterns of fishes along the Chikugo estu-ary except for a few monospecies studies. Some of the fishessuch as Acanthogobius hasta, Trachidermus fasciatus, Coilianasus and Neosalanx reganius are reported to occur only inthe Ariake Bay and mainly in the Chikugo estuary. Most offishes of the Ariake Bay use the tidal flat of the euryhalinelower estuary for spawning; the larvae move upstream afterhatching and they reside the brackishwater areas of the riverwhich is used as the feeding ground (Matsui et al., 1986,1987; Takita and Chikamoto, 1994; Takeshita et al., 1995,1997; Takita, 1996; Kuno and Takita, 1997; Onikura et al.,1999). Some fishes (e.g., C. nasus and N. reganius) spawnin freshwater areas of the river and these species also moveto the brackishwater areas for feeding. Therefore, the brack-ishwater area of the Chikugo River is an important foragingground for many fishes in the Ariake Bay. Although no infor-mation is available on the distribution of Engraulis japonicusand Sebastes inermis from the Ariake Bay, these species arecommonly reported from euryhaline coastal pelagic fish com-munities along the coast of Japan and elsewhere (Harada,1962; Safran and Omori, 1990; Houde and Zastrow, 1993; Hir-akawa et al., 1997; Nagasawa et al., 2000; Yukio, 2000). Thesespecies are reported as obligatory resident in the offshore highsalinity regions and prefer regions of coastal upwelling whichis consistent with our results. The upstream movement of thesespecies may be restricted by their poor ability to low salinitytolerance.

Lateolabrax japonicus was the only species distributed overthe whole spatial gradient studied. Spawning of L. japonicusoccurs in seawater and the fish immigrate to freshwater atthe larvaejuvenile transformation phase or at the early juve-nile stage. Ohta et al. (1997) employed otolith microchemistry

to investigate estuarine dependency of the fish from the samestudy site and observed that a substantial fraction of newlytransformed juveniles invaded freshwater and occurred abovethe saltfront while the other fraction of juveniles remainedin coastal or polyhaline estuarine habitats, demonstrating a fac-ultative amphidromous distribution. In the present study, basswere collected at all the sampling stations over a wide salinityrange indicating a similar facultative amphidromy. Dietaryhabits of L. japonicus were closely related to the distributionof the fish, i.e., the fish preyed on euryhaline copepod in theeuryhaline zone and oligohaline copepods in the oligohalinezones. The dominant copepods in the euryhaline regions (Oi-thona davisae and other Cyclopoid copepods and nauplii) aresmaller in size which, in addition to the low amounts of cope-pod biomass in these regions, indicate that prey organismsmay be distributed more patchily in these regions than thatin the upper estuary, resulting in lower feeding success.Such smaller copepods may be suitable for the first-feedinglarvae but are less likely to satisfy the food requirement ofthe growing larvae and juveniles which necessitates a portionof the larvae and juveniles to ascend upstream nursery to for-age on Sinocalanus sinensis which is bigger in size and abun-dant in these regions. Therefore, it is reasonable to speculatethat the density-dependent foraging may be a significantsource of early mortality in sea bass in the lower estuaryand this may lead to further speculation that the fish performsascending migration as an adaptation to reduce this early mor-tality. The portions of the population that still remain in thelower estuary are either too weak to perform ascending move-ment or find a suitable density-independent foraging conditionas the majority have already moved upstream. Ludwig andRowe (1990) suggested that since food requirements and pre-dation risk change during ontogeny, shifts in habitat should oc-cur to meet the changing demands of the fish. The highestabundance of L. japonicus at the uppermost (R4) and the low-ermost (E3) stations probably indicate that the fish exploits theoligohaline and euryhaline copepod communities, respec-tively, as the highest densities of copepods of the oligohalineand euryhaline communities correspond to these two stations,respectively. In addition to the ETM-based hydrographic con-ditions that retain planktonic eggs and larvae within the ETMregions, elevated temperature and lower salinity, together withenhanced densities of food, may allow developing larvae togrow rapidly, thus helping them to avoid predators and resistbeing dispersed by currents (Olney and Boehlert, 1988; Doyleet al., 1993; Velez et al., 2005). Since achieving faster growthis the basic survival strategy in the early-life stages of fishes, itis reasonable to assume that the larval and juvenile fishes uti-lize the upper estuary because these regions offer bettergrowth through efficient foraging.

We have observed a longitudinal succession of two differ-ent copepod assemblages in the Chikugo estuary. One is theoligohaline assemblage associated with the ETM in the upperestuary and the other is a euryhaline assemblage seaward ofthe ETM in the lower estuary. Sinocalanus sinensis is the dom-inant species in the low saline areas of the estuary and was as-sociated with the turbidity maximum. In contrast to the low


saline upstream community, a multi-species colony wasformed in the high salinity areas of the lower estuary wherea number of species dominated. Oithona davisae, Paracalanusparvus, Acartia omorii were the three most dominant speciesin this community. The copepod colony in this area was char-acterized by commonly occurring coastal copepods; similarand related species have been reported in many coastal estuar-ies in the world (Plourde et al., 2002; Satapoomin et al., 2004;David et al., 2005). An exactly similar pattern of longitudinalzooplankton assemblage was reported along the St. LawrenceETM (Bousfield et al., 1975; Laprise and Dodson, 1994; Win-kler et al., 2003). These authors have reported a longitudinalsuccession of two well-defined assemblages of zooplanktonalong the estuary. A true estuarine assemblage composed ofEurytemora affinis, Neomysis americana and Mysis stenolepisoccurring in salinities of 0.5 to 5 which correspond to the ETMand this assemblage was reported as the most abundant of theestuary. At higher salinities, the estuarine community was re-placed by a euryhaline marine assemblage composed of Cala-nus spp. and other commonly occurring coastal marinezooplanktons (Bousfield et al., 1975; Laprise and Dodson,1994). The highest total copepod density occurred at E3, themost downstream station; in contrast, the highest standing bio-mass occurred at R4, the most upstream station, indicating thatS. sinensis accounts for most of the secondary production bycopepods in the estuary. As a single species, S. sinensis, whichis associated with the ETM zone of the estuary, contributedmore than 80% of the overall copepod biomass in the estuary.This implies that the ETM zone accounts for majority of thecopepod biomass production and is consistent with otherwell mixed estuarine systems that are characterized by anETM zone (Laprise and Dodson, 1994; Winkler et al.,2003). High concentrations of zooplankton prey may be an im-portant and ubiquitous characteristic of ETM nursery areasand this appears the most important reason why so many estu-arine dependent species gather in this transition zone. Con-cerns may be raised on limitations of our data that wesampled fish larvae and juveniles only at the surface and sub-surface areas which may not completely represent the entirelarval fish community if not all species are evenly distributedin the water column which is generally the case in river estu-ary. In estuarine ecosystems, larval and juvenile fishes gener-ally exhibit their highest abundance near the surface andsubsurface waters, particularly during high tides. Therefore,our data represent the majority of the fish species distributedin the Chikugo River estuary. Moreover, we have eliminatedany temporal or tidal influence by sampling all the stationsnearly the same time of the day and, therefore, at the sametidal condition. Nevertheless, we still believe that depth inte-grated samples throughout the water column would be a betterchoice for describing larval fish assemblage and distributionpatterns.

5. Conclusion

The Chikugo estuary is characterized by salinity and turbid-ity gradients with a zone of ETM in the upper part of the

estuary which is characterized by low salinity and high tem-perature. Surface net sampling showed that there are two dif-ferent fish and copepod communities based on the spatialdistribution patterns along the estuary: the oligohaline com-munity which was associated with the turbidity maximumand the euryhaline community seaward of the turbidity maxi-mum in the lower estuary. The oligohaline fish communitywas composed of Acanthogobius flavimanus, Acanthogobiushasta, Coilia nasus, Neosalanx reganius, and Trachidermusfasciatus while the euryhaline community was composed ofEngraulis japonicus and Sebastes inermis. Lateolabrax japoni-cus was distributed over wide spatial areas. Sinocalanus sinen-sis was the single dominant member of the oligohalinecopepod community while the euryhaline community wasdominated by Oithona davisae, Acartia omorii and Paracala-nus parvus. It appears that intimate dietary relationships occurbetween fish and copepod species in the same community. TheETM appears to influence the distribution and abundance ofthe oligohaline copepod S. sinensis and the dynamics of thisprey species may have strong influence on the dynamics of lar-val and juvenile fishes. Most of the fishes were distributed inthe upper estuary where they fed on S. sinensis which contrib-uted the majority of the copepod standing biomass of the estu-ary. It was concluded that habitat partitioning occurs betweentwo differential fish and copepod communities and the ETM-based copepod S. sinensis appears to play a key role as the pri-mary prey to support important nursery for most of the fishspecies in Chikugo estuary. Future studies on the fish commu-nities in the Chikugo estuary should be done on a broader per-spective taking into account wider spatial and temporal scalesincluding the biotic and abiotic environment to have a morecomprehensive understanding on the factors affecting the hab-itat use patterns by fishes.

Acknowledgement

This research was supported by the research grant providedby the Japanese Government Ministry of Education, Culture,Sports, Science and Technology (Monbukagakusho, MEXT)and the first author acknowledges the financial support pro-vided by the ‘Monbukagakusho’ (through ‘MonbukagakushoScholarship’) during his stay in Japan.

References

Bennett, W.A., Kimmerer, W.J., Burau, J.R., 2002. Plasticity in vertical migra-

tion by native and exotic estuarine fishes in a dynamic low salinity zone.

Limnology and Oceanography 47, 1496e1507.

Bousfield, E.L., Filteau, G., O’Neill, M., Gentes, P., 1975. Population dynam-

ics of zooplankton in the middle St. Lawrence estuary. Estuarine Research

1, 325e351.

Castel, J., Veiga, J., 1990. Distribution and retention of the copepod Euryte-

mora affinis hirundoides in a turbid estuary. Marine Biology 107, 119e

128.

Chihara, M., Murano, M., 1997. An Illustrated Guide to Marine Plankton in

Japan. Tokai University Press, Japan, 1574 pp.

Dauvin, J.C., Dodson, J.J., 1990. Relationship between feeding incidence and

vertical and longitudinal distribution of rainbow smelt larvae (Osmerus


mordax) in a turbid well-mixed estuary. Marine Ecology Progress Series

60, 1e12.

David, V., Sautour, B., Chardy, P., Leconte, M., 2005. Long-term changes of

the zooplankton variability in a turbid environment: the Gironde estuary

(France). Estuarine, Coastal and Shelf Science 64, 171e184.

Dodson, J.J., Dauvin, J.C., Ingram, R.G., d’Anglejan, B., 1989. Abundance of

larval rainbow smelt (Osmerus mordax) in relation to the maximum turbid-

ity zone and associated macroplankton fauna of the middle St. Lawrence

estuary. Estuaries 12, 66e81.

Doyle, M.J., Morse, W.W., Kendall Jr., A.W., 1993. A comparison of larval

fish assemblages in the temperate zone of the northeast Pacific and north-

west Atlantic Oceans. Bulletin of Marine Science 53, 588e644.

Harada, E., 1962. A contribution to the biology of the black rockfish, Sebastes

inermis Cuvier et Valenciennes. Publ. Seto. Marine Biology 10, 307e361.

Hirakawa, K., Goto, T., Hirai, M., 1997. Diet composition and prey size of lar-

val anchovy, Engraulis japonicus, in Toyama Bay, southern Japan Sea.

Bulletin of the Japan Sea National Fisheries Research Institute 0, 67e78.

Houde, E.D., Zastrow, C.E., 1993. Ecosystem and taxon-specific dynamic and

energetics properties of fish larvae assemblages. Bulletin of Marine Sci-

ence 53, 290e335.

Irigoien, X., Castel, J., 1997. Light limitation and distribution of chlorophyll

pigments in a highly turbid estuary: the Gironde (SW France). Estuarine,

Coastal and Shelf Science 44, 507e517.

Jackson, G., Jones, G.K., 1999. Spatial and temporal variation in nearshore

fish and macroinvertebrate assemblages from a temperate Australian estu-

ary over a decade. Marine Ecology Progress Series 182, 252e268.

Jager, Z., 1998. Accumulation of flounder larvae (Platichthys flesus L.) in the

Dollard (Ems estuary, Wadden Sea). Journal of Sea Research 40, 43e57.

Jassby, A.D., Kimmerer, W.J., Monismith, S.G., Armor, C., Cloern, J.E.,

Powell, T.M., Schubel, J.R., Vendlinski, T.J., 1995. Isohaline position as a hab-

itat indicator for estuarine populations. Ecological Applications 5, 272e289.

Kimmerer, W.J., Burau, J.R., Bennet, W.A., 1998. Tidally oriented vertical mi-

gration and position maintenance of zooplankton in a temperate estuary.

Limnology and Oceanography 43, 1697e1709.

Kuno, Y., Takita, T., 1997. The growth, maturation and feeding habits of the

gobiid fish Acanthogobius hasta distribution in Ariake Sound, Kyushu, Ja-

pan. Fisheries Science 63, 242e248.

Laprise, R., Dodson, J.J., 1989. Ontogeny and importance of tidal vertical mi-

grations in the retention of larval smelt Osmerus mordax in a well-mixed

estuary. Marine Ecology Progress Series 55, 101e111.

Laprise, R., Dodson, J.J., 1994. Environmental variability as a factor control-

ling spatial patterns in distribution and species diversity of zooplankton in

the St. Lawrence estuary. Marine Ecology Progress Series 107, 67e81.

Loneragan, N.R., Potter, I.C., Lenanaton, R.C.J., Caputi, N., 1986. Spatial and

seasonal differences in the fish fauna in the shallows of a large Australian

estuary. Marine Biology 92, 575e586.

Loneragan, N.R., Potter, I.C., 1990. Factors influencing community structure

and distribution of different life-cycle categories of fishes in shallow wa-

ters of a large Australian estuary. Marine Biology 106, 25e37.

Ludwig, D., Rowe, L., 1990. Life-history strategies for energy gain and pred-

ator avoidance under time constraints. American Naturalist 135, 686e707.

Margulies, D., 1990. Vulnerability of larval white perch, Morone americana,

to fish predation. Environmental Biology of Fishes 27, 187e200.

Matsui, S., Tomishige, S.I., Tsukahara, H., 1986. Ecological studies of the

engraulid fish, Coilia nasus, I. Preliminary report on the ecology of the

ascending population. Science Bulletin of the Faculty of Agriculture,

Kyushu University 40, 221e228.

Matsui, S., Nakagawa, K., Tomishige, S.I., 1987. Ecological studies of the en-

graulid fish, Coilia nasus, III. Appearance and feeding habits of the juve-

nile in the Chikugo River (Japan). Science Bulletin of the Faculty of

Agriculture, Kyushu University 41, 55e62.

Moser, H.G. (Ed.), 1984. Ontogeny and Systematics of Fishes e International

Symposium held in August 15e18, 1983, La Jolla, California. American

Society of Ichthyologists and Herpetologists, 760 pp.

Nagasawa, T., Tamashita, Y., Yamada, H., 2000. Early life history of mebaru,

Sebastes inermis (Scorpaenidae) in Sendai Bay, Japan. Ichthyological Re-

search 47, 231e241.

North, E.W., Houde, E.D., 2003. Linking ETM physics, zooplankton prey, and

fish early-life histories to white perch (Morone americana) and striped bass

(M. saxatilis) recruitment success. Marine Ecology Progress Series 260,

219e236.

Ohta, T., Arai, N., Tanaka, M., 1997. Otolith Sr concentration analyzed by

PIXE in Ariake estuarine-dependent sea bass juveniles. International Jour-

nal of PIXE 7, 147e151.

Okiyama, M., 1988. An Atlas of the Early Stage Fishes in Japan. Tokai

University Press, Japan, Tokyo, xiiiþ1154 pp.

Onikura, N., Takeshita, N., Matsui, S., Kimura, S., 1999. Distribution area and

optimum salinity of larvae and juveniles of Trachidermus fasciatus, Cotti-

dae. Nippon Suisan Gakkaishi 65, 42e47.

Olney, J.E., Boehlert, G.W., 1988. Nearshore ichthyoplankton associated with

seagrass beds in the lower Chesapeake Bay. Marine Ecology Progress Se-

ries 45, 33e43.

Parrish, J.D., 1989. Fish communities of interacting shallowwater habitats in

tropical oceanic regions. Marine Ecology Progress Series 58, 143e160.

Plourde, S., Dodson, J.J., Runge, J.A., Therriault, J.C., 2002. Spatial and tem-

poral variations in copepod community structure in the lower St. Lawrence

Estuary, Canada. Marine Ecology Progress Series 230, 211e224.

Roman, M.R., Holliday, D.V., Sanford, L.P., 2001. Temporal and spatial pat-

terns of zooplankton in the Chesapeake Bay turbidity maximum. Marine

Ecology Progress Series 213, 215e227.

Rothschild, B.J., Osborn, T.R., 1988. Small scale turbulence and plankton con-

tact rates. Journal of Plankton Research 10, 465e474.

Safran, P., Omori, M., 1990. Some ecological observations on fishes associated

with drifting seaweed off Tohoku coast, Japan. Marine Biology 105, 395e402.

Satapoomin, S., Nielsen, T.G., Hansen, P.J., 2004. Andaman Sea copepods:

spatio-temporal variations in biomass and production, and role in the

pelagic food web. Marine Ecology Progress Series 274, 99e122.

Shoji, J., North, E.W., Houde, E.D., 2005. The feeding ecology of Morone

americana larvae in the Chesapeake Bay estuarine turbidity maximum:

the influence of physical conditions and prey concentrations. Journal of

Fish Biology 66, 1328e1341.

Simenstad, C.A., Morgan, C.A., Cordell, J.R., Baross, J.A., 1994. Flux, passive

retention, and active residence of zooplankton in Columbia River estuarine

turbidity maxima. In: Dyer, K.R., Orth, R.J. (Eds.), Changes in Fluxes in

Estuaries: Implications from Science to Management. Olsen and Olsen,

Fredensborg, pp. 473e482.

Sirois, P., Dodson, J.J., 2000a. Critical periods and growth-dependent survival

of larvae of an estuarine fish, the rainbow smelt Osmerus mordax. Marine

Ecology Progress Series 203, 233e245.

Sirois, P., Dodson, J.J., 2000b. Influence of turbidity, food density and para-

sites on the ingestion and growth of larval rainbow smelt Osmerus mordaxin an estuarine turbidity maximum. Marine Ecology Progress Series 193,

167e179.

Takeshita, N., Matsui, S., Onikura, N., Kimura, S., 1995. The effects of salinity

on the viability of eggs of the roughskin sculpin, Trachidermus fasciatus.

Fisheries Science 65, 888e889.

Takeshita, N., Onikura, N., Matsui, S., Kimura, S., 1997. Embryonic, larval

and juvenile development of the roughskin sculpin, Trachidermus fasciatus

(Scorpaeniformes, Cottidae). Ichthyological Research 44, 257e266.

Takita, T., Chikamoto, H., 1994. Distribution and life history of Trachidermus

fasciatus in rivers around Ariake Sound, Japan. Japanese Journal of Ichthy-

ology 41, 123e129.

Takita, T., 1996. Threatened fishes of the world, Neosalanx reganius Wakiya and

Takahashi, 1937 (Salangidae). Environmental Biology of Fishes 47, 100.

Velez, J.A., Watson, W., Arntz, W., Wolff, M., Schnack-Schiel, S.B., 2005.

Larval fish assemblages in Independencia Bay, Pisco, Peru: temporal and

spatial relationships. Marine Biology 147, 77e91.

Winkler, G., Dodson, J.J., Bertrand, N., Thivierge, D., Vincent, W.F., 2003.

Trophic coupling across the St. Lawrence River estuarine transition

zone. Marine Ecology Progress Series 251, 59e73.

Yukio, M., 2000. Maturation of the Japanese Anchovy, Engraulis japonicus,

off southeastern Hokkaido and adjacent waters. Bulletin of the Japanese

Society of Fisheries Oceanography 64, 10e17.

Documents

Distribution and diets of larval and juvenile fishes: Influence of salinity gradient and turbidity maximum in a temperate estuary in upper Ariake Bay, Japan