Environ Biol Fish (2011) 91:337–352 DOI 10.1007/s10641-011-9790-6
Importance of the upper estuary as a nursery ground for fishes in Ariake Bay, Japan Yuta Yagi & Izumi Kinoshita & Shinji Fujita & Daisuke Aoyama & Yoshio Kawamura
Received: 27 September 2010 / Accepted: 21 January 2011 / Published online: 9 April 2011 # Springer Science+Business Media B.V. 2011
Abstract To examine the importance of the upper estuarine areas of Ariake Bay as a nursery ground for fish, assemblages of larvae and juveniles were compared among various aquatic habitats. The upper estuaries of the bay (the Rokkaku and Hayatsue estuaries) are brackish, highly turbid waters with high tidal velocities, and differ substantially from the Isahaya area, which has Y. Yagi (*) : I. Kinoshita Usa Institute of Marine Biology, Kochi University, 194 Usa-cho, Tosa, Kochi 781–1164, Japan e-mail:
[email protected] S. Fujita Nishinihon Institute of Technology, Ltd., 9–30 Wakamatsu-cho, Kochi, Kochi 780–0812, Japan D. Aoyama SOUGOUMIZU Institute, Ltd., 1-4-6 Kan-nabe-cho, Sakai, Osaka 590–0984, Japan Y. Kawamura Saga Prefectural Ariake Fisheries Research and Development Center, 2753–2 Ashikari-cho, Ogi, Saga 849–0313, Japan Present Address: Y. Yagi Japan Sea National Fisheries Research Institute, Fisheries Research Agency, 5939–22 Suido-cho, Chuo-ku, Niigata, Niigata 951–8121, Japan
been separated from the bay by a man-made dike, to the middle estuary (the Kikuchi estuary). Abundances of larvae and juveniles were higher in the estuaries than in the open bay and Isahaya areas. Abundant species in the upper estuaries were similar to each other, but differed from those of the middle estuary. This was primarily due to larvae and juveniles of fishes that occurred almost entirely in the upper estuaries, such as Acanthogobius hasta, Boleophthalmus pectinirostris, Coilia nasus, Cynoglossus abbreviatus, Nibea albiflora, Odontamblyopus lacepedii, Trachidermus fasciatus and Tridentiger barbatus. These results suggest that the upper estuaries play an important role as nursery grounds for fishes. Keywords Fish community . Nursery habitat . Endemic species . Estuarine area . Ariake Bay
Introduction Estuaries and tidal zones are dynamic and heterogenous ecotones where extreme variability in hydrographic environment occurs with tremendous influences on residents and their trophic structures. Substantial efforts have been made on the habitat use and feeding ecology of many fishes (Blaber and Blaber 1980; Van der Veer and Bergman 1986; Sirois and Dodson 2000; Bennett et al. 2002; North and Houde 2003; Able 2005), and the role of these areas as nursery habitat for many commercially exploitable
338
fishes is well reported (Day et al. 1989; Hoss and Thayer 1993; Beck et al. 2001). Moreover, many studies have suggested that these nursery habitats contribute substantially to the recruitment success in fishes through providing higher juvenile growth and enhanced survival (Van der Veer et al. 2001; Yamashita et al. 2003; Ohta et al. 1997). Ariake Bay has the largest area of tidal flats with the highest tidal range in Japan (Inoue 1980). It harbors a diverse community of fishes, including several endemic and restricted species, such as Acanthogobius hasta, Boleophthalmus pectinirostris, Coilia nasus, Trachidermus fasciatus and Tridentiger barbatus, which are commonly distributed in the Yellow and East China Seas, where the tidal range is large and vast tidal flats develop as in Ariake Bay (Uchida and Tsukahara 1955; Kinoshita et al. 2000). Tanaka (1933) speculated that as the Japan Archipelago separated from the Asian continent, only Ariake Bay retained such an environment, consequently supporting these fishes as continental relicts. The early life histories of fishes within Ariake Bay have been studied, including the aggregation of juveniles in the upper estuary and littoral zone, which has been suggested as an important nursery habitat for fishes (Koshiishi et al. 2001; Hibino et al. 2002; Takita et al. 2003; Aoyama et al. 2007). However, the previous studies did not examine the community composition of larval and juvenile fishes with respect to habitat type or area, which is fundamental to establishing what areas of the bay are essential habitats as nursery grounds for commercially and ecologically-important fishes. Since 1997, a dike was built across Isahaya inlet blocking the Honmyo River to develop agricultural lands and prevent a storm surge, having the small culvert, which aquatic exchanges are little allowed, in the central part and reduced the vast estuarine area. In this study, to evaluate the importance of various estuarine and marine habitats as a nursery ground for fishes, we examined the various pelagic to demersal early life stages of the fish community, and from the perspective of comparing across diverse habitat types, including the Isahaya area of Ariake Bay.
Materials and methods Surveys for dynamic sampling of fishes were categorized into pelagic and demersal sample periods, which
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were made almost bimonthly from March 2005 to February 2006 and from December 2003 to January 2005, respectively. Oblique tows of a larval net (1.3 m mouth-diameter) were performed in five parts of Ariake Bay representing different characteristic waters and their respective fish habitat. Meshapertures of the net were 1 mm in the upper estuaries (the Rokkaku, Hayatsue estuaries) and the middle estuary (the Kikuchi estuary) to avoid clogging of the net by suspended particulates, and 0.5 mm in the open bay and Isahaya areas (Fig. 1). Of the areas sampled, tidal collections were also carried out at Stns. 2 and 6 (the Rokkaku estuary), Stn. 34 (Hayatsue estuary), and Stns 39 and 40 (Kikuchi estuary) seasonally from May 2005 to February 2006, because it was reported that the larval ichthyofauna and physical environment in the estuarine area were largely changed by the tidal phases (Takita 1980). Depth of tows and volume of water filtered (m3) were measured and calculated using a Divers Watch (Log Memory 1473, Casio) and flow meter (2030R, General Oceanics) attached to the net, respectively. For demersal fishes, collections were made in the upper estuary (the Rokkaku estuary), and in the northern, western and Isahaya areas (Fig. 1) with a beam trawl (width 0.25×1.5 m, 2 mm mesh-aperture) modified after Kuipers (1975). Towing distance was calculated from measures of latitude to longitude recorded by GPS. All samples were fixed in 10% sea-water formalin, with fishes in the samples being sorted and transferred to 80% ethanol, and subsequently measured for size by developmental stages (Kendall et al. 1984). In this study, unlabeled lengths indicate body lengths (BL) (notochord length for preflexion and flexion larvae, and standard length for postflexion larvae). Family names and their order followed Nelson (2006), and genus and species names are in accordance with Nakabo (2000) and ordered alphabetically. Differences in the communities of fish larvae and juveniles among areas were analysed by the Cπ index (Kimoto 1976) based on the logarithm of fish density ðLnðx þ 1Þ; x ¼ n=1000m3 for pelagic larvae and juveniles; x ¼ n=100m2 for demersal fishesÞ. In the present study, endemic species are defined as the fishes that are restricted to Ariake Bay in Japanese waters, restricted species are common in Ariake Bay, but rare or uncommon in other Japanese waters, and an Ariake Bay stock is a distinct stock of species that
Environ Biol Fish (2011) 91:337–352
339
Fig. 1 Chart showing stations where fish larvae and juveniles were collected in Ariake Bay, Kyushu, southern Japan. Open and solid circles indicate the stations where collections were made by larva net oblique tows to examine horizontal distributions of pelagic larvae, and beam trawl tows to distinguish nursery grounds for demersal juveniles, from March
2005 to February 2006 and from December 2003 to January 2005, respectively. Investigated waters were categorized into five main habitat areas (the Rokkaku, Hayatsue and Kikuchi estuaries, the open bay and Isahaya areas) for pelagic larvae and juveniles and into four habitat areas (the Rokkaku estuary, northern, western and Isahaya areas) for demersal fishes
is common or more widely distributed in Japanese waters (Dotu 1957; Takita 1978, 1980; Menezes et al. 1990; Kinoshita et al. 1995; Yagi et al. 2009; Yamaguchi et al. 2009). At each sampling station, water temperature (°C) and salinity (psu) were measured at 0.5 m depthintervals using an STD (AST500-P, Alec Electronics), and turbidity (NTU) was measured at 1 m depthintervals using a Water Quality Checker (WQC-22A, TOA DDK). Current profile was measured with an ADCP (WHSZ12000-I-UG12, RD Instruments) at 0.5 m depth-intervals, from a depth of 1 m to the bottom.
seasons (Fig. 2). The waters from the open bay to Isahaya areas were vertically to horizontally very similar, except for slight stratification in August. Around the mouth of the Rokkaku River, distinctive turbidity fronts were observed, with extremely turbid water over 1,000 NTU inside the river mouth. During all seasons, it was notably less turbid in the open bay and Isahaya areas. In all seasons, strong tidal currents drastically changed the vertical structure of the water column in the upper estuaries (the Rokkaku and Hayatsue estuaries) (Fig. 3). Currents were markedly stronger in the upper estuaries than in the middle estuary (the Kikuchi estuary). In the upper estuaries, turbidities became higher when current speed was >0.5 kt during both tides, but were quite lower even during strong ebb tide in the middle estuary.
Results Physical environment
Fish community Based on water temperature and salinity, the Rokkaku estuary was vertically well-mixed and received tidal exchange of water to the upper reaches during all
Overall species richness and higher densities of pelagic larvae and juveniles were recorded from the
340
Environ Biol Fish (2011) 91:337–352
Fig. 2 Seasonal change in the vertical profiles of physical parameters along an axis from Stn. 14 to Stn. 1 (see Fig. 1)
estuaries than in the open bay to Isahaya areas (Table 1). Dominant taxa in the upper estuaries, which were similar to each other, were Acanthogobius hasta, Tridentiger barbatus, Odontamblyopus lacepedii, Trachidermus fasciatus, Cynoglossus abbreviatus and Boleophthalmus pectinirostris (Table 2). In the middle estuary, Gymnogobius macrognathos was the most abundant, followed by Salangichthys microdon and Engraulis japonicus. On the other hand, the Isahaya area community was dominated almost entirely by the gobiid Amblychaeturichthys hexanema. In the open bay area, A. hasta and E. japonicus were the most abundant pelagic larvae. In the four areas, both species richness and overall density of settled juveniles were highest in the Rokkaku estuary (Table 3). In this estuary, Odontamblyopus lacepedii was the most abundant, followed by Tridentiger barbatus and Cynoglossus lighti. Acentrogobius sp. B and C. lighti were also abundant in
the other three areas, followed by T. barbatus in the northern area, T. nudicervicus in the western area, and Amblychaeturichthys hexanema in the Isahaya area. Of the species observed, the abundant species common between the various areas were Acentrogobius sp. B, T. barbatus and C. lighti; of the three, individuals <20 mm of T. barbatus and C. lighti were mainly found from the Rokkaku estuary, and Acentrogobius sp. B, in the Isahaya area (Fig. 4). During all seasons, pelagic larval and juvenile communities in the upper estuaries (the Rokkaku and Hayatsue estuaries) were very similar, but differed markedly from those of the middle estuary to Isahaya area (Fig. 5). The demersal fish community of the Fig. 3 Comparison of vertical profiles of water temperature, salinity, turbidity and current speed with tidal cycle among the three estuaries. Solid arrows indicate the hour at high tide. Flood and ebb velocities are denoted as + and −, respectively
Environ Biol Fish (2011) 91:337–352
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342
Fig. 3 (continued)
Environ Biol Fish (2011) 91:337–352
E
Elops hawaiensis
Anguilla japonica
Elopiformes
Anguillidae
Engraulidae
Neosalanx reganius**1
C–D E
E C–E
Plectorhinchus cinctus
Acanthopagrus latus
Nibea albiflora†3
Ammodytes personatus
Omobranchus elegans
Callionymidae spp.
Acanthogobius hasta**1
Sparidae
Sciaenidae
Ammodytidae
Blenniidae
Callionymidae
Gobiidae A–E
C
4.4–18.4
4.3
4.0–120.4
11.3–14.1
8.2–32.5
A–E
D
C–E
E
D–E
D–E
16.4
5.2–19.4
3.3–103.2
12.9
5.8–41.7
12.1–34.2
C
E
D–E
Haemulidae
D–E
Leiognathus nuchalis
Leiognathidae
15.1–32.2
C
D–E
Lateolabrax japonicus†2
6.0–26.3
Moronidae
A–E
A–E
Trachidermus fasciatus**1
Cottidae 5.3–28.0
E
Platycephalus sp.
Platycephalidae
9.6–11.6
E
D–E
Sebastes inermis 20.5
6.2–6.3 38.1–76.2
Scorpaenidae
C–E
E
E
C
C–E
E
C–E
C–D
B–C
D
10.8–11.8
3.1–4.7
5.6
62.5
6.3–45.4
10.2
10.5
19.8–102.8
6.8
9.2–73.8
5.7
6.7–13.6
8.8–11.7
5.7–8.7
10.7–12.2
B–D
B
C–D
E
B
C
D
B–C
D
Stage
6.2–9.2
2.1–2.4
4.3–5.6
11.8–13.2
5.1–6.0
7.2
11.8–21.1
5.7–8.2
18.5–22.3
Range of BL (mm)
D–E
C
B–C
B–D
Stage
67
B–E
C–D
C–D
C
C
E
81.9–84.5
7.1–11.4
22.4–24.2
4.2–7.4
30.1
45.4–48.1
6.6–8.4
4.1–20.1
6.1–9.8
14.5–28.4
9.6–16.3
31.0–171.2
48.6–56.8
Range of BL (mm)
73
227
≥15
1.7–5.1
4.3–6.0
5.0–6.9
4.3–4.5
6.8–7.8
11.1–11.7
24.6
17.3–31.8
3.5–3.8
4.0–6.9
6.4–11.4
Range of BL (mm)
Isahaya area
E
E
C–D
E
C–D
E
E
C
C–E
C
D–E
C–D
E
E
Stage
323
254
≥13
Open bay area
Trachyrhamphus longirostris
Hippocampus mohnikei
Syngnathidae
7.5–19.2
20.8–24.6
3.6–7.3
5.1–13.5
6.3–14.7
7.1
18.3–46.5
10.5–19.7
16.8–218.4
54.2–56.9
32.6
Stage
356
3309
≥33
Kikuchi estu.
Syngnathus schlegeli
Gambusia affinis
Poeciliidae
C–E
E
Mugil cephalus cephalus
Hypoatherina valenciennei
Chelon sp.
Mugilidae
Atherinidae
C–D
Synodontidae sp.
Synodontidae
Salangichthys microdon
Silurus asotus
Sardinella zunasi†1
Salangidae
C–D
Konosirus punctatus†1
Siluridae
C
Ilisha elongata†1
C–E
D–E
Engraulis japonicus
Cyprinidae spp.
C–E C–D
Coilia nasus**1
Cyprinidae
Clupeidae
Stage
Species name
Family name E
516
Mean density (n 103 m−3) Range of BL (mm)
15049
Total number of individual
Range of BL (mm)
≥44
≥41
Species number 8252
Hayatsue estu.
Rokkaku estu.
Study site
Table 1 List of fishes collected with a larval net in five studied areas of the Ariake Bay from March 2005 to February 2006
3–5, 8
11
8
4
2–5, 8, 11
11
8
8, 11
2–5
2–5
3, 5
2–4
11
11
8, 11
8
8
2–4
5
8
2, 5, 8
2
8
4, 5, 8
8
5
8
2–4, 8, 11
2–4, 8, 11
2
11
Month
Environ Biol Fish (2011) 91:337–352 343
Stage A–E
Species name
A. flavimanus
Family name
B–E E E
Cynoglossus abbreviatus*2
C. lighti**2
Takifugu xanthopterus*3
Cynoglossidae 41.1
43.8–123.4
10.2–18.5
13.1–14.1 E
B–E
59.5–95.4
10.3–14.1
5.9–9.3
6.7–9.9
18.7–27.8
28.9–52.5
6.7–16.7
19.7–23.5
10.4–11.5
D–E
D–E
E
E
9.0–13.5
7.1–10.1
19.7–22.1
26.2–34.8
10.0–11.1
8.6–15.5
8.7–17.8
6.2–22.9
27.2
12.7–15.6
5.3–9.7
12.8–18.6
Range of BL (mm)
B
B–C
C–D
Stage
73
254
≥13
8.3–9.9
3.4–6.2
7.4–9.6
Range of BL (mm)
Open bay area
B–C
B–D
Stage
67
227
≥15
3.5–5.8
5.1–10.5
Range of BL (mm)
Isahaya area
8
4, 11
3–5
2
2, 5, 8, 11
5
2
2, 8, 11
8
5, 8
5, 11
8
2, 5, 8, 11
5
5
5
2
8
2, 11
5
8
8
2, 8
8
8
3, 4
Month
** = endemic species by Uchida and Tsukahara (1955)**1, 2 , Takita (1978)**1 , and Yagi et al. (2009)**2 , * = restricted species by Dotu (1957)*1 and Takita (1980*2 , 2000*3 ), † = Ariake Bay stock by Takita (2000)†1 , Kinoshita et al. (1995)†2 and Menezes et al. (1990)†3 , Yamaguchi et al. (2009)†3
Stage: A Yolk–sac, B Preflexion, C Flexion, D Postflexion, E Juvenile and adult
Tetraodontidae
E
Kareius bicoloratus
Pleuronectidae
B–E
D–E
Gobiidae spp.
5.4–11.2
D–E B–E
T. spp.
7.1–10.4
E
T. nudicervicus
E
D–E
E
6.7–23.5
D–E
Tridentiger barbatus*1
T. bifasciatus
22.1–30.2
E
Taenioides cirratus
6.8
E
E
Pseudogobius masago
11.1–11.8
E
Periophthalmus modestus
4.8–144.1
D–E
D–E
Odontamblyopus lacepedii**1 6.1–133.4
D–E
D–E
Luciogobius spp.
8.7–12.3
D–E
G. spp.
8.9–15.9
D–E
D–E
26.6–27.9
20.1–24.5
G. macrognathos
E
E
6.2–15.1
14.5–16.8
C–E 9.2–10.7
24.3–40.5
D–E
E
B–D
Gymnogobius breunigii D–E
E
Ctenotrypauchen microcephalus
7.1–19.7
15.7–58.3
6.1–9.1
E
E
D–E
B–D
4.0–16.2 24.3
Glossogobius olivaceus
E
Boleophthalmus pectinirostris**1
8.6
E
B–E
Stage
323
E
C
Amblychaeturichthys hexanema Apocryptodon punctatus
7.7–17.6
3.3–16.9
Stage
356
3309
≥33
Kikuchi estu.
Favonigobius gymnauchen
D–E
A. sp. B
Acentrogobius sp. A
516
Mean density (n 103 m−3) Range of BL (mm)
15049
Total number of individual
Range of BL (mm)
≥44
≥41
Species number 8252
Hayatsue estu.
Rokkaku estu.
Study site
Table 1 (continued)
344 Environ Biol Fish (2011) 91:337–352
Environ Biol Fish (2011) 91:337–352
345
Table 2 Comparison of dominant fishes collected with a larva net among five studied areas of the Ariake Bay from March 2005 to February 2006 (Otherwise same as in Table 1) Waters
Rokkaku estu.
Hayatsue estu.
Kikuchi estu.
Open bay area
Isahaya area
Species name
Rank
Rank
Rank
Rank
Rank
Acanthogobius hasta**
1
71.6
2
28.5
Tridentiger barbatus*
2
16.8
1
44.6
Odontamblyopus lacepedii**
3
3.6
3
5.7
Trachidermus fasciatus**
4
1.9
4
4.2
Cynoglossus abbreviatus*
5
1.3
11
0.7
Gobiidae spp.
6
0.9
10
1.0
Coilia nasus**
7
0.7
6
2.9
Boleophthalmus pectinirostris**
8
0.7
5
2.9
Acanthogobius flavimanus
9
0.5
16
0.3
Nibea albiflora†
10
0.4
8
2.2
Sardinella zunasi†
11
0.4
7
Konosirus punctatus†
32
+
9
Gymnogobius macrognathos
12
0.1
15
0.4
%
%
%
15
0.2
6
1.2
2.4
12
0.3
1.6
5
3.3
Salangichthys microdon
1
62.0
2
14.4
%
%
1
48.7
8
0.7
8
0.7
5
0.7
5
1.2
2
1.5
Engraulis japonicus
15
0.1
12
0.5
3
11.5
2
42.5
3
1.0
Amblychaeturichthys hexanema
32
+
22
0.1
4
3.9
3
1.5
1
92.9
7
0.9
Gymnogobius breunigii Leiognathus nuchalis
8
0.4
Favonigobius gymnauchen
9
0.4
Gymnogobius spp.
10
0.3
Callionymidae spp.
14
0.2
4
1.5
16
0.1
6
1.1
9
0.4
6
0.6
Hippocampus mohnikei
17
0.1
25
+
Acanthopagrus latus
20
Lateolabrax japonicus†
13
14
0.4
28
+
+
34
+
7
1.0
0.1
13
0.4
10
0.4
21
0.1
12
0.3
Sebastes inermis Trachyrhamphus longirostris Omobranchus elegans
32
+
Chelon sp.
20
+
23
0.1
20
+
20
+
11
0.3
4
0.9
6
0.6
8
0.5
9
0.4
+ indicates less than 0.05% % calculated from amount of monthly mean density (n 103 m−3 )
Rokkaku estuary differed from that of the other three areas in all seasons, to the communities of the western and Isahaya areas were relatively similar to each other (Fig. 5).
Discussion The settling juveniles of endemic species in the upper estuaries locally aggregated even from the time of their early pelagic stage in the present
study (Tables 1, 2, 3 and 4). It has been reported that larvae and juveniles of common species accumulated in littoral zones of tidal flats, but few of the endemic species were found in this area (Hibino et al. 2002). These facts suggest that the endemic species are more dependent on the upper estuary as a nursery ground. It is understandable that larval and juvenile fishes originally born around the upper estuaries (e.g., Acanthogobius hasta, Boleophthalmus pectinirostris, Coilia nasus, Neosalanx reganius, Odontamblyopus lacepedii, Salanx ariakensis and Trachidermus fasciatus) still occur
Muranesox cinereus
Coilia nasus**
Muraenesocidae
Engraulidae
Lateolabrax japonicus†
Leiognathus nuchalis
Moronidae
Leiognathidae
E
Chelidonichthys spinosus
Platycephalus sp.
Triglidae
Platycephalidae
D, E
E
Sebastes inermis
D E
21.2–23.4
17.2
11.6
52.9
Scorpaenidae
E
Hypoatherina valenciennei
Hippocampus mohnikei
E
E
E
E
Atherinidae
25.5
15.9
56.7
44.5
20.9–35.4
12.5–37.8
60.5–136.3
Stage
7.7
Syngnathidae
E E
Chelon haematocheilus
Mugil cephalus cephalus
Mugilidae
E
Synodontidae sp.
E
Neosalanx reganius**
Salanx ariakensis**1
D, E
Konosirus punctatus†
Synodontidae
Salangidae
D, E
Ilisha elongata†
Engraulis japonicus
Dasyatis akajei
Dasyatidae
Clupeidae
Stage
Species name
Family name
E
15.6
Mean density (n 102 m−2)
25.9
12.3–26.4
125.1
37.3
35.2
98.5–129.3
Range of BL(mm)
1431
Total number of individual
Range of BL(mm)
≥28
≥32
Species number 746
Northern area
Rokkaku estu.
Study site
E
E
Stage
3.5
138
≥16
15.8–16.2
336.3
Range of BL(mm)
Western area
E
E
E
E
E
Stage
5.6
387
≥22
15.8–31.4
251.6
31.5–33.7
60.4–71.4
312.6
Range of BL(mm)
Isahaya area
10
3
10
4
3
7
7
4
4
7
4
1
7
7, 10
7
1, 3, 4, 10, 12
4
3
Month
Table 3 List of fishes collected with a beam trawl by four studied areas of the Ariake Bay from December 2003 to January 2005 (Otherwise same as in Table 1)
346 Environ Biol Fish (2011) 91:337–352
T. xanthopterus*
E
C. lighti**
Takifugu rubripes†
E
Cynoglossus abbreviatus*
Cynoglossidae
Tetraodontidae
E
Pleuronichthys sp.
D, E
Gobiidae spp.
Paralichthys olivaceus
D
Pleuronectidae
E
T. nudicervicus
T. spp.
Paralichthyidae
D, E D, E
Tridentiger barbatus*
T. bifasciatus
E
Silhouettea dotui
Parachaeturichthys polynema
D, E
Odontamblyopus lacepedii**
36.6–41.7
14.1–240.1
22.4
8.7–14.1
12.7
16.4–27.3
14.4–60.8
9.5–85.9
23.4
11.3–234.9
12.8–120.5
55.9–60.5
D, E
E
Amblychaeturichthys hexanema Apocryptodon puntatus
20.6–40.1
11.7–13.4
E
A.sp. B
9.7–300.8 14.0–34.8
D, E
D, E
25.7
13.2–59.6
8.5–144.2
38.8
Range of BL(mm)
Boleophthalmus pectinirostris** Ctenotrypauchen microcephalus Favonigobius gymnauchen
D, E
Acanthogobius hasta**
Acentrogobius sp. A
Gobiidae
E
E
Pennahia argentata†3
Ammodytes personatus
D, E
Repomucenus valenciennei
E
Nibea mitsukuri
N. albiflora†
Scienidae
Ammodytidae
Stage
Species name
Family name
Callionymidae
15.6
Mean density (n 10 m )
E
E
E
D, E
D, E
D, E
D, E
E
D, E
E
E
E
E
E
E
E
E
E
E
E
Stage
7.7
72.9
18.2–249.8
160.8
11.0–20.8
10.8–14.1
15.8–27.5
12.3–19.3
21.8–83.5
10.8–19.7
40.7–78.2
18.9–112.3
27.7–61.0
51.5–114.6
18.0–50.3
17.2–22.2
41.2–257.4
19.2–27.5
23.6–40.3
16.8–36.9
50.6–93.6
Range of BL(mm)
E
E
E
E
D, E
D, E
E
30.5–249.1
140.7
14.3–29.4
218.2
10.2–10.8
17.3–40.4
48.1–49.1
21.1–61.5
14.2–39.6
E
E
25.6–27.4
26.7–87.1
21.1–48.8
23.6–24.8
22.7–92.8
Range of BL(mm)
E
E
E
E
E
Stage
3.5
E
D, E
E
E
E
E
E
E
E
E
D, E
D, E
E
E
E
E
Stage
5.6
18.9–245.3
9.2–11.0
14.6
29.9–30.8
45.6–47.2
20.3–22.6
20.0
13.9–40.9
21.9–39.5
35.3–78.7
12.8–210.1
16.3–53.2
96.1–104.6
14.4–122.8
12.8–104.4
29.8–35.1
Range of BL(mm)
7
7
1, 3, 4, 7, 10, 12
3, 4
3
10
4, 7
1, 7
1, 3, 4, 7, 12
1, 3, 4, 7, 10
1, 3, 4, 7, 10, 12
1, 4
10
1, 3, 4, 7, 10, 12
1, 3, 10, 12
1, 3, 4, 7, 10
7
1, 3, 4
1, 3, 4, 7, 10, 12
1, 3, 4, 7, 10, 12
1, 3, 4, 7, 10, 12
1, 3, 4, 7, 10, 12
1, 3, 4, 7, 10, 12
3
7, 10
1, 3, 4, 7, 10, 12
7
Month
Environ Biol Fish (2011) 91:337–352 347
348
Environ Biol Fish (2011) 91:337–352
Fig. 4 Comparison of size frequency distributions for the three abundant species collected with a beam trawl among the four areas
Fig. 5 Dendrogram of the similarity among the areas based on cluster analysis of fish communities of pelagic and demersal periods
Environ Biol Fish (2011) 91:337–352
349
Table 4 Comparison of dominant fishes collected with a beam trawl among four studies areas of Ariake Bay from December 2003 to January 2005 (Otherwise same as in Table 1) Study site
Rokkaku estu.
Northern area
Western area
Isahaya area
Species name
Rank
Rank
Rank
Rank
%
Odontamblyopus lacepedii**
1
38.1
8
2.7
Tridentiger barbatus*
2
27.3
2
14.8
16
0.7
Cynoglossus lighti**
3
11.2
1
41.5
1
39.0
1
40.8
Nibea albiflora†
4
5.4
13
1.3
13
0.2
Acanthogobius hasta**
5
3.6
11
1.5
11
0.3
Pennahia argentata†
6
2.7
6
4.5
8
1.5
Acentrogobius sp. B
7
2.6
3
7.0
3
13.7
2
30.9
4
11.9
4
8.0
8
1.2
17
0.2
%
%
Acentrogobius sp. A
8
2.2
4
5.8
Coilia nasus**
9
1.7
9
2.1
Boleophthalmus pectinirostris**
10
1.4
Repomucenus valenciennei
21
0.1
Ammodytes personatus
5
5.5
7
3.6
%
Tridentiger bifasciatus
15
0.2
10
2.0
6
1.5
10
0.5
Tridentiger nudicervicus
16
0.2
22
0.4
2
22.4
7
1.6
5
1.6
9
0.9
19
0.5
7
1.4
9
1.2 0.2
Favonigobius gymnauchen Sebastes inermis Paralichthys olivaceus Gobiidae spp.
14
0.3
Amblychaeturichthys hexanema Ctenotrypauchen microcephalus
11
1.2
Parachaeturichthys polynema
17
0.6
10
0.9
16
12
1.3
13
0.7
3
8.2
15
0.8
11
0.7
5
4.0
24
0.2
6
2.2
% calculated from amount of monthly mean density (n 102 m−2 )
there as adults (Takita 1980; 2000). On the other hand, although the sciaenids (Nibea albiflora and Pennahia argentata) and the cynoglossids (Cynoglossus abbreviatus and C. lighti) spawn offshore (Takita 1974, 1980; Hayashi et al. 2000), their pelagic larvae also aggregated in the upper estuaries (Tables 1 and 3). In this aggregation mechanism, Hibino et al. (2007) reported the transportation of pelagic larvae of Lateolabrax japonicus from offshore waters to the upper estuaries by a counterclockwise circular current in the bay (Inoue 1980), but there was no reference to whether this mechanism led to localized settlement within the estuaries itself. In case of Paralichthys olivaceus in Wakasa Bay, the Japan Sea, it is suggested that an eddy permits the drifting larvae with consequent high recruitment of settlers in the bay (Kinoshita et al. 2000). Accordingly, it is likely that the circular current encounters strong tidal currents in front of the river mouth, forming variable eddies that tend to
entrain drifting larvae from offshore waters, thus resulting in high concentrations of larvae in the upper estuaries of Ariake Bay. It has been previously reported that larvae and juveniles of the endemic (Matsui et al. 1987; Takita and Chikamoto 1994; Aoyama et al. 2007), restricted species (Dotu 1957; Yagi et al. 2009) and Ariake Bay stock (Takita 1974; Islam et al. 2006; Fujita et al. 2007) were found mainly in the tidal reaches of the rivers. In the case of Lateolabrax japonicus and Cynoglossus abbreviatus, the larvae were distributed in the surface and middle layers at flood tide, and aggregated near the bottom at ebb tide, thus the larvae seem to remain in the estuary by vertical migration (Matsumiya et al. 1982; Yagi et al. 2009). However, the retention of larvae cannot be attributed to vertical migration, because there is little differentiation in the current speed between surface and bottom layers during both flood and ebb tides (Fig. 3). Rather, this
350
Environ Biol Fish (2011) 91:337–352
phenomenon likely occurs by not vertical but by the horizontal movement of larvae, which may move to the shallow banks with relatively lower currents to avoid dispersing offshore at the ebb tide. The upper estuaries are brackish, highly turbid waters, with high tidal velocities, which are very different from those of the middle estuary. Furthermore, the dominant species in the upper estuaries were similar to each other, but differed from those in the middle estuary, i.e., the endemic and unique species (restricted species and Ariake Bay stock) of Ariake Bay, such as Coilia nasus, Trachidermus fasciatus, Nibea albiflora, Acanthogobius hasta, Boleophthalmus pectinirostris, Odontamblyopus lacepedii, Tridentiger barbatus and Cynoglossus abbreviatus occurred almost entirely in the upper estuaries (Tables 2 and 4). On the other hand, Engraulis
japonicus, Salangichthys microdon and Gymnogobius macrognathos, being common in the inlets and estuaries of Japan (Kanou et al. 1999; Yamaguchi 2006), were abundant in the middle estuary (Tables 1 and 2). These results suggest that there is a substantial difference in the larval and juvenile fish community among the estuaries in Ariake Bay, with highly turbid waters being likely important as essential nursery grounds for the unique species of the bay. Prior to the construction of a dike across the Isahaya inlet in 1997, the Honmyo estuary had an environment similar to that of the upper estuaries. Kinoshita (2007) showed that about 30 year ago the Honmyo estuary was an important nursery ground for fishes, especially for the endemic and restricted species (Table 5). Accordingly, the Honmyo estuary should have comprised a significant portion of the
Table 5 Dominant fish larvae and juveniles collected with a larval net in the Honmyo estuary of the Isahaya area in spring and summer of 1979 and 1980 (modified after Kinoshita (2007), otherwise same as in Table 1) Species number
22
Total number of individual
4058
Species name
Rank
%
Stage
Range of BL (mm)
Nibea albiflora†
1
34.1
B–E
2.4–28.7
Tridentiger spp.
2
30.9
E
11.2–14.1
Acanthogobius hasta**
3
13.8
E
10.1–44.0
Tridentiger barbatus*
4
11.0
D, E
9.9–13.7
Odontamblyopus lacepedii**
5
3.1
B–E
3.9–10.9
Pseudogobius masago
6
2.7
E
5.8–7.7
Sardinella zunasi
†
7
2.0
B–E
Apocryptodon punctatus
8
1.0
E
11.6–15.5
6.6–16.8
Gymnogobius macrognathos
9
0.8
E
12.4–21.5
Chelon haematocheilus†
10
0.1
E
21.5–26.6
Gobiidae spp.
10
0.1
B
2.5–3.3 23.1–28.7
Konosirus punctatus
†
12
0.1
E
Cyprinidae spp.
12
0.1
B, C
Takifugu xanthopterus*
14
0.1
E
Trachidermus fasciatus**
15
+
E
23.7
Acanthogobius flavimanus
15
+
E
5.9
Mugil cephalus cephalus
15
+
E
36.2
Omobranchus elegans
15
+
E
11.5
Periophthalmus modestus
15
+
E
10.8
Lateolabrax japonicus†
15
+
E
35.2
Hippichthys penicillus
15
+
E
49.3
Tridentiger trigonocephalus
15
+
E
9.8
5.1–8.3 7.7–9.0
Environ Biol Fish (2011) 91:337–352
available nursery habitat in Ariake Bay. In the present study, the pelagic larval community of the Isahaya area was quite poor (Table 1), and the demersal juvenile community was very similar to that of western area, along which there is little river inflow (Fig. 5). Hence, the separation between the Honmyo River and Isahaya inlet by the dike could have substantially reduced the area of essential nursery habitat and thus production of fishes in Ariake Bay. Acknowledgments We express our gratitude to J.M. Leis and T.W. Miller for his critical reading the manuscript. We are grateful to T. Noguchi and K. Kuno, Saga Prefectural Government, for their assistance with this study and two anonymous reviewers for helpful comments. Sincerely, thank for assistance of our laboratory staffs for their support during field researches. This work was partially supported by the Ministry of Education, Science and Culture, Japan (no. 20580203).
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