Differences in fish assemblage structure between vegetated and ...

Fish Sci (2014) 80:21–41 DOI 10.1007/s12562-013-0682-x

ORIGINAL ARTICLE

Biology

Differences in fish assemblage structure between vegetated and unvegetated microhabitats in relation to food abundance patterns in a mangrove creek Kusuto Nanjo • Hiroyoshi Kohno • Yohei Nakamura Masahiro Horinouchi • Mitsuhiko Sano

•

Received: 31 August 2013 / Accepted: 20 October 2013 / Published online: 11 December 2013 Ó The Japanese Society of Fisheries Science 2013

Abstract In order to clarify the mechanisms determining fish distribution patterns in a mangrove system on Iriomote Island, in southern Japan, fish assemblage structures were determined by visual observation, along with food abundance and environmental factors, in an area of mangrove roots on the banks, and a bare sand area at the center, within downstream, midstream and upstream portions of a branch creek from the Urauchi River. The fish assemblage structures differed significantly between the area types, with the mangrove-root area supporting a more diverse and abundant fish fauna. A canonical correspondence analysis revealed that the relationships between fish distribution and their food abundance differed among trophic groups. Benthic crustacean or plant feeders were positively associated with their prey i.e. crabs and macroalgae—in other words,

these trophic groups were abundant in downstream and/ or midstream mangrove-root areas in which their prey were also particularly abundant. However, zooplankton feeders did not show such relationships, their abundance being positively associated with fine sediment particles (characteristic of areas with weak water movement). These results suggested that food availability is a major factor determining the distribution patterns of benthic crustacean feeders and plant feeders, whereas for zooplankton feeders other factors, such as sheltering effects against water current and/or predators, may be more significant.

K. Nanjo (&) Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan e-mail: [email protected]

Introduction

H. Kohno Okinawa Regional Research Center, Tokai University, Uehara, Taketomi, Okinawa 907-1541, Japan Y. Nakamura Graduate School of Kuroshio Science, Kochi University, 200 Monobe, Nankoku, Kochi 783-8502, Japan M. Horinouchi Research Center for Coastal Lagoon Environments, Shimane University, 1060, Nishikawatsu-cho, Matsue, Shimane 690-8504, Japan M. Sano Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo 113-8657, Japan

Keywords Distribution Fish assemblage Food abundance Mangrove estuary Microhabitat Trophic group

Tropical and subtropical mangrove estuaries often support large numbers of fish species and individuals, including some that are commercially important, compared to nearby open bare sand/mud flats, which are usually characterized by fewer species and fewer individuals [1–5]. Habitat complexity structured by mangrove vegetation has been considered a major factor responsible for such a difference due to greater habitat complexity providing shelter from predation and/or strong water movement, increased microhabitat availability, and abundant food [2, 6]. For example, the structural complexity of mangrove prop roots and pneumatophores could reduce predation risks [7, 8], such being especially important for small-sized fishes, such as juveniles, because of their vulnerability to predation [9]; thus, the latter sometimes

123

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select mangrove areas in order to reduce predation risks [10]. In addition, the complex structure of mangrove roots enhances sedimentation rates, trapping suspended particles and leaf litter [11], and also harbor abundant epiphytic algae on their large surface area [12, 13], thereby enabling large numbers of small invertebrates (food resources for mangrove fishes), which feed upon such organic materials [14, 15], to reside within the mangrove system [7]. A greater abundance of food provides potential advantages, such as faster growth [16] to a size that is relatively free from predation [9, 17, 18]. Accordingly, small-sized fishes sometimes prefer mangrove areas to unvegetated, bare areas [7]. Several recent studies of fish assemblages in mangrove habitats, however, have suggested that fish species richness and/or abundance are not always greater in mangrove areas [19–21]. For example, in temperate Australia, Smith and Hindell [19] examined fish assemblage structures in the Barwon River Estuary, using fyke, gill and pop nets, and found that fishes were less abundant in the mangroveforested areas than in the unvegetated channels. In addition, Tse et al. [22] reported that fish species richness and gut fullness did not differ between a mangrove estuary and unvegetated mudflat within Tolo Harbour in southern China, suggesting that mangrove habitats may not necessarily be a better feeding area for fishes compared to mudflats. These findings are contrary to the general notion that mangrove-vegetated areas support a large number of fishes by harboring rich prey resources. Accordingly, the present study re-evaluated the relationships between fish distribution and prey abundance in a mangrove system. We conducted the study on a small spatial scale (i.e., vegetated/unvegetated microhabitats within a single mangrove creek), since the abiotic environmental factors (e.g., temperature) associated with such may not differ strongly between microhabitats, whereas they may affect fish distribution on a broader spatial scale due to significant differences among microhabitats, which may lead to the misinterpretation of results [23]. In order to re-evaluate the relationships between fish distribution and prey abundance in a mangrove system, we examined and compared fish assemblage structures and their prey abundance in mangrove-vegetated areas and adjacent open areas within a single mangrove creek.

Materials and methods Study site The study was conducted in a creek of the Urauchi River (24°240 N, 123°460 E), situated on the northern side of Iriomote Island, Ryukyu Islands, Japan (Fig. 1), in August

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Fish Sci (2014) 80:21–41

(summer) and November (autumn) of 2008, February (winter) and May (spring) of 2009, August (summer) and November (autumn) of 2009, and February (winter) and May (spring) of 2010. The former 4 months were regarded arbitrarily as the first year, and the latter 4 months as the second year. The study creek (1.1-km-long, 10–80 m in width until 900 m from the creek mouth), branching from the main river at a point about 2 km upstream from the river mouth, was fringed by dense, undisturbed mature mangrove forest, comprising mainly the red mangrove Rhizophora stylosa. Sampling stations were established at the lower- (0–250 m from the creek mouth), middle- (350–550 m from the creek mouth) and upper-portions (650–850 m from the creek mouth) of the study creek (hereafter referred to as ‘‘downstream’’, ‘‘midstream’’ and ‘‘upstream’’, respectively. See Fig. 1). Two microhabitat types within each station were targeted: (1) an offshore edge portion of the sand/mud area with mangrove roots on the creek bank (hereafter referred to as ‘‘mangrove-root area’’), and (2) an unvegetated sand area in the center of the creek (hereafter referred to as ‘‘bare sand area’’). The mean creek widths were 45.0 ± 12.3 m (standard deviation) downstream, 29.0 ± 6.1 m midstream and 23.4 ± 2.9 m upstream (n = 5). The mean root densities of R. stylosa in the mangrove-root area were 66.6 ± 14.8/ m2 downstream, 63.0 ± 12.6/m2 midstream and 59.0 ± 11.6/m2 upstream (n = 5). The tidal range within the creek was approximately 1.5 m, prop roots being inundated at high tide and partially exposed at low tide. Water temperature and salinity were measured at 10-min intervals by a small data logger (Compact-CT, JFE Advantech Co, Ltd.) anchored to a prop root, whereas water turbidity was measured using a portable water quality analyzer (Model U-20XD, Horiba Ltd.) at high tide, with ten replicates at each station in each season. The preliminary study conducted from 2007 through 2008 confirmed no difference in the three environmental factors between the microhabitats, although they varied among stations and/or seasons (three-way analysis of variance, water temperature: f = 0.014, p [ 0.05 for microhabitats; f = 1.563, p [ 0.05 for stations; f = 266.996, p \ 0.05 for seasons; salinity: f = 0.215, p [ 0.05 for microhabitats; f = 4.006, p \ 0.05 for stations, f = 2.814, p \ 0.05 for seasons; water turbidity: f = 0.038, p [ 0.05 for microhabitats; f = 27.015, p \ 0.05 for stations, f = 2.792, p \ 0.05 for seasons) (Nanjo K, unpubl. data). Sediment samples were taken from five points located randomly in each microhabitat at each station in each season. Dry sediment samples were sieved through mesh trays of decreasing size (2,000, 1,000, 500, 250, 180, 125, 63 lm) stacked vertically on a vibratory sieve shaker (Analysette 3 Pro, Fritsch Co.). The sediment retained in each sieve was weighed to the nearest 0.001 g and mean median grain sizes were calculated.

Fish Sci (2014) 80:21–41

23

each transect was positioned within 5–10 m from the outer border of the mangrove-root area. All fishes within the transect areas were counted by an observer (Nanjo K) using a snorkel, and their total lengths were estimated in size classes of 1 cm. Individual fishes were identified to species levels following Nakabo [24].

East China Sea Japan 123˚ 46’ E

Food abundance

China Taiwan

Iriomote Island Ryukyu Islands 24˚ 24’ N

0

1 km

ORRC

Urauchi Bay

Urauchi River

N E

W Downstream

Midstream

S

Upstream

Fig. 1 Map of the Urauchi River mangrove estuary, Iriomote Island, Ryukyu Islands, Japan. Shaded areas indicate mangrove forests. Circles show each station (downstream, midstream and upstream). filled square, Okinawa Regional Research Center, Tokai University (ORRC)

Sampling design Fishes In order to clarify fish assemblage structures, visual censusing was conducted in both area types at high tide (ca. water depth 1.2 m) between 09:00 and 17:00 h at each station in each season in both years. For each census, sixbelt transects 1 m wide and 20 m long, parallel to the creek flow direction and separated from each other by at least 10 m, were established randomly in each microhabitat at depths of ca. 1.2 m (downstream), 1.4 m (midstream) and 0.8 m (upstream), using a scaled measure. For the mangrove-root area census, each transect was placed within the outer border of that area. For the bare sand area census,

Zooplankton, crabs, gammaridean amphipods, polychaetes, macroalgae and detritus were chosen as major food resources, since these food items were the most important (especially for the dominant species) for the mangrove fish assemblage at the present study site [25]. The six food types were collected at each station in each microhabitat in each season in both years. Zooplankton was collected at high tide, while the other food items were sampled at low tide between 09:00 and 17:00 h. Zooplankton, such as calanoid and cyclopoid copepods and their nauplii, was collected using a plankton net (20cm mouth diameter, 75-cm-long and 100-lm mesh size) equipped with a flow meter. The net was held in front of the collector (Nanjo K), who walked against the water flow for 20 m. Subsequently, the net contents were retrieved and the volume of water filtered was recorded. In the mangrove-root area, the collector maintained a position as close as possible to the prop roots. Five replicates were obtained for each microhabitat. Zooplankton densities were expressed as individual numbers per m3. In order to collect macroalgae, such as the red algae Bostrychia spp., attached to prop roots, mangrove root-bark samples were taken from roots some 30 cm above the substrate (ca. 20 cm2/root), with ten replicates collected from each mangrove-root area. The lack of above-ground structures in the bare sand areas precluded the collection of macroalgal samples. Epiphytic macroalgae on root-bark were removed (scraped off) using a small knife and weighed to the nearest 0.001 g (wet weight), with the algal biomass expressed as wet weight per surface area of each root-bark sample (g/cm2). Crabs on the sediment surface were collected from five quadrats (1 9 1 m) established randomly within each microhabitat. In the mangrove-root areas, crabs on the roots were also captured. Fiddler crabs (Uca spp.) were excluded from the crab samples because they are not taken by fishes in this mangrove estuary [see 25]. Gammaridean amphipods and polychaetes were sampled using a cylindrical core sampler (18 cm in diameter), collecting 500-cm3 of the sediment from five points located randomly in each microhabitat. Immediately after collection, the samples were preserved in 10 % buffered formalin, and the zooplankton, gammaridean amphipods, and polychaetes within each sample were later sorted and counted under a binocular microscope.

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The amount of detritus in the sediment was expressed by ignition loss. Five (ca. 10 g) sediment samples were collected to a depth of 1 cm from the surface using a small spoon, dried to a constant weight and then combusted at 560 °C for 8 h, and reweighed. The amount of detritus was expressed as the percentage of the dry weight reduced by combustion to the total dry sediment weight. Data analysis Species richness and abundance of fishes in each microhabitat were expressed as mean species and individual numbers per transect (20 m2), respectively. In addition, mangrove fishes were divided into seven trophic categories based on published dietary data [e.g., 25], including three well-represented groups—benthic crustacean feeders (preying mostly on crabs, shrimps and gammaridean amphipods), zooplankton feeders, and plant feeders (taking mainly macroalgae)—in addition to polychaete feeders, detritus feeders, fish feeders and insect feeders. The latter trophic categories were represented mostly by a few lowdensity species (see Appendix) and were not treated specifically in the analyses described below. Since the objective of the present study was to determine differences among microhabitats, stations and seasons, rather than differences between years, statistical analyses were made in each year. Three-way analyses of variance (ANOVAs) were employed to compare fish assemblage properties (i.e., mean species and individual numbers per transect of the overall fish assemblage and of each dominant trophic group) and abundances of food resources, i.e., zooplankton (ind/m3), crabs (ind/m2), gammaridean amphipods (ind/500 cm3), polychaetes (ind/ 500 cm3) and detritus (%), among microhabitats, stations and seasons. Since neither plant nor zooplankton feeders occurred in the bare sand area, mean species and individual numbers of such groups in the mangrove-root areas were compared among stations and seasons, using two-way ANOVA. For algal biomass (g/cm2), two-way ANOVA was employed for the same reason. When significant differences were recognized (p \ 0.05), post hoc Games– Howell tests were applied. Because the first-order interactions (microhabitat 9 station, microhabitat 9 season or station 9 season) were often significant (see Table 2), oneway ANOVAs and Games–Howell tests were conducted to compare the values between microhabitats at each station in each season, among stations in each microhabitat in each season, and among seasons in each microhabitat at each station. Some ANOVA results are not presented here due to space limitations. Prior to ANOVA, the detritus data (i.e., ignition loss) were transformed to arcsine, whereas other data were square-root (x ? 1) transformed, to improve homogeneity of variances. Such transformation, however,

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Fish Sci (2014) 80:21–41

did not produce homogeneous variances in some cases. In such cases, to compensate for the increased likelihood of Type 1 errors (the rejection of a true null hypothesis), the significance level was set at 0.01 [26]. In order to classify the assemblages into groups with similar species occurrence patterns, a cluster analysis was conducted. Initially, the degree of similarity of the assemblages between microhabitats at each station in each season in each year was calculated, using the Bray–Curtis similarity index, based on the individual numbers of each species. Subsequently, the resultant similarity matrix was subjected to an average linkage clustering method. Prior to the cluster analysis, data were square-root (x ? 1) transformed. Species contributing significant variation between the groups were identified using the SIMPER (similarity percentage) subroutine. In order to assess the relationships among fish distributions and biotic (food abundance) and abiotic (environmental) factors, a canonical correspondence analysis (CCA) [27] was conducted. For the CCA, data for ten dominant fish species from the study site were used to express species variables (see Table 1), in order to reduce the effect of rare species distorting the ordination of CCA [28]. The abundances of six food resources (zooplankton, crabs, gammaridean amphipods, polychaetes, detritus, and macroalgae) and environmental factors (water temperature, salinity, water turbidity, and median grain size of sediment) were used as explanatory variables.

Results Fish assemblage structure A total of 31,055 individuals, representing 29 families and 85 species, were observed during the study period (Table 1 and Appendix). In terms of individual numbers, the brackish cardinal fish Apogon amboinensis (8,539 individuals), hover goby Parioglossus raoi (8,499), P. palustris (3,375), freshwater demoiselle Neopomacentrus taeniurus (1,194), brackish damselfish Pomacentrus taeniometopon (1,137), mangrove snapper Lutjanus argentimaculatus (971), blacktail snapper L. fulvus (923), Ambasis miops (880), Parioglossus rainfordi (848) and Pomadasys argenteus (746) were dominant, accounting for 87.3 % of the total. In the present study, most fishes, including dominant species, were observed in the mangrove-root area at all stations in all seasons, although only a few low-density species, such as mojarra Gerres erythrourus, thornfish Terapon jarbua and sand goby Favonigobius reichei, occurred in the bare sand area (see Fig. 2; Table 1 and Appendix). One-way ANOVAs conducted following threeway ANOVAs (see explanation in Data analysis; Table 2)

B B

Apogon amboinensis (A. amb)

Lutjanus argentimaculatus (L. arg)

Lutjanus fulvus (L. ful)

Lutjanidae

Z

Parioglossus raoi (P. rao)

B B

Apogon amboinensis (A. amb)

Lutjanus argentimaculatus (L. arg)

Lutjanus fulvus (L. ful)

Lutjanidae

2–4

Z Z

Parioglossus rainfordi (P. rai)

Parioglossus raoi (P. rao)

6.3

19.2

21.2

4.5

20.5

4.3

23.8

5.3

4.8

25.2

16.0

6.3

14.3

4.2

33.3

23.0

4.3

1.8

0.7

13.2

13.7

3.0

9.8

9.0

186.0

2.8

19.2

7.3

5.5

9.5

10.3

4.3

6.0

7.8

135.3

S

30.7

1.0

4.7

1.2

1.7

2.5

24.5

44.8

6.5

1.0

0.5

1.0

14.2

8.3

M

S

2.7

1.3

13.5

24.8

6.0

21.3

4.8

51.3

13.2

2.7

17.5

6.5

15.0

13.8

3.0

45.7

0.2

M

S

M

M

S

Downstream

Midstream

Downstream

Upstream

Autumn

Summer

16.2

0.5

17.8

9.7

12.3

2.7

5.5

27.3

136.2

0.2

14.3

4.3

4.0

7.3

12.0

11.5

2.8

28.5

125.2

15.5

M

S

Midstream

14.8

5.5

46.7

0.3

2.0

13.5

16.3

6.3

44.2

0.2

0.8

5.2

5.0

M

S

Upstream

29.3

4.2

10.0

10.7

0.2

16.5

8.5

17.5

68.7

13.8

9.2

11.7

9.0

2.2

8.0

6.0

24.5

M

S

Downstream

Winter

6.7

81.8

10.0

44.8

5.8

10.3

8.7

3.5

14.8

107.2

6.7

81.8

3.5

17.7

6.7

3.0

9.8

3.5

11.7

120.5

M

S

Midstream

TC trophic category, TL total length (cm), M mangrove-root area, S bare sand area. Trophic category: B benthic crustacean feeders, Z zooplankton feeders, Pl plant feeders

1–5

1–4

Z

1–14

1–8

10–31

3–20

3–50

3–7

1–6

1–5

2–4

1–4

1–14

1–8

10–31

2–24

3–55

3–7

1–5

TL

Parioglossus palustris (P. pal)

Pl

Pomacentrus taeniometopon (P. tae)

Ptereleotridae

Pl

Neopomacentrus taeniurus (N. tae)

Pomacentridae

B

Pomadasys argenteus (P. arg)

Haemulidae

B

Ambassis miops (A. mio)

Apogonidae

Z

Z

Parioglossus rainfordi (P. rai)

Ambassidae

Second year

Z

Parioglossus palustris (P. pal)

Pl

Pomacentrus taeniometopon (P. tae)

Ptereleotridae

Pl

Neopomacentrus taeniurus (N. tae)

Pomacentridae

B

Pomadasys argenteus (P. arg)

Haemulidae

B

Ambassis miops (A. mio)

Z

TC

Apogonidae

Species (Abbreviation)

Ambassidae

First year

Family

Table 1 Mean individual number of dominant fish species per transect (20 m2, n = 6) at the study site in the first and second years

60.7

14.2

53.2

0.3

0.2

1.3

13.0

78.5

14.3

64.0

0.2

1.5

0.8

M

S

Upstream

51.0

7.0

5.5

13.8

33.3

15.0

12.5

9.3

21.7

45.8

12.0

10.8

10.0

10.3

12.2

11.3

4.8

40.0

16.7

M

S

Downstream

Spring

82.0

3.3

29.8

9.0

6.3

4.0

4.2

3.0

115.3

31.7

99.2

19.2

41.3

7.8

1.0

19.0

2.5

4.2

82.5

10.0

M

S

Midstream

0.3

0.8

101.2

1.7

62.7

0.5

0.2

0.3

1.7

6.2

121.8

1.7

64.3

M

S

Upstream

Fish Sci (2014) 80:21–41 25

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26

Fish Sci (2014) 80:21–41

revealed that the mean total species and individual numbers were significantly higher in the mangrove-root area than in the bare sand area at all stations in all seasons in both years (p \ 0.001). In the mangrove-root area, mean total midstream species and individual numbers were higher compared to downstream and/or upstream in each season in both years, although in some cases the differences were marginal (for species number in winter in the second year, p = 0.034; for individual number in winter in the first year, p = 0.021; for other cases, all p \ 0.01). In contrast, the mean total species and individual numbers in the bare sand areas seldom differed among stations and seasons. The trophic guild structure of the fish assemblage is summarized in Fig. 3. Because benthic crustacean feeders, plant feeders, and zooplankton feeders were dominant in the present study (see Fig. 3, Appendix), these three categories were applied to the analyses. One-way ANOVAs conducted First year

25

Mean species number/20 m 2

following three-way ANOVAs (see explanation in Data analysis; Table 2) indicated that the mean species and individual numbers of benthic crustacean feeders were higher in the mangrove-root area than in the bare sand area at each station in each season in both years, although in some cases the differences were marginal (for mean upstream individual number in winter and spring in the second year, p = 0.011; for other cases, all p \ 0.01). In the mangrove-root area, the mean individual number was greater downstream and/or midstream compared to upstream in each season in both years (for winter and spring in the second year, p \ 0.05; for other cases, all p \ 0.01). Since the plant feeders and zooplankton feeders never occurred in the bare sand area (see Fig. 3; Table 1 and Appendix), the mean species and individual numbers of these groups occurring in the mangrove-root area were compared among stations and seasons by two-way Second year

20

15

10

5

0

Mean individual number/20 m2

400

300

200

100 5

0 DS MS US

DS MS US

DS MS US

DS MS US

DS MS US

DS MS US

DS MS US

DS MSUS

Summer

Autumn

Winter

Spring

Summer

Autumn

Winter

Spring

Fig. 2 Mean fish species and individual numbers per transect (20 m2, n = 6) in the mangrove-root (filled square) and bare sand (open square) areas at each station in each season in the first and second years. Bars indicate standard deviation. DS downstream, MS midstream, US upstream

123

3.000

120

Residuals

3.000

6

Microhabitat 9 Station 9 Season

Individuals

Species

3 6 6 120

Station 9 Season


Residuals

2

Microhabitat 9 Station

Microhabitat 9 Season

3

6 120


Residuals 2

6

Station 9 Season

Season

3


Station

2


1

3

Season

Microhabitat

1 2

Microhabitat Station

18.00

3.000

1.600

1.000

7.200

203.5

6.100

212.6

1,774

0.110

0.030

0.120

0.480

0.830

0.100

105.8 1.710

2.000

3 6


Station 9 Season

88.00

18.00

3 2

Season


87.00

2

5,615

0.120

Station

120

Residuals

0.080

0.090

0.820

0.380 2.370

1

6


240.5 4.120

Microhabitat

3 6


3 2

Season Microhabitat 9 Station

Station 9 Season

1 2

Microhabitat

Station

Benthic crustacean feeders

Individuals

Species

Overall fish assemblage 2,004

0.539

0.318

2.389

67.94

2.047

70.98

592.1

0.303

1.085

4.497

7.752

0.895

983.4 15.92

0.979

0.781

6.367

31.59

6.489

31.50

2,024

0.692

0.709

6.873

3.148 19.74

34.33

3

3

0.778

0.926

120

6

6

3

2

\0.001** 0.072

3

2

\0.001** 0.111

1

120

6

6

\0.001**

0.934

0.375

3

2

\0.001** 0.005*

3

1 2

120

6

0.446

\0.001** \0.001**

0.443

6

\0.001** 0.587

3 2

\0.001**

2

\0.001** \0.001**

1

120

6

\0.001**

0.656

6

\0.001** 0.643

3 2

0.028 \0.001**

1 2

\0.001**

Games–Howell test

\0.001**

p

3.900

1.900

1.700

12.70

171.9

13.90

177.2

2,119

0.090

0.010

0.030

0.380

0.490

0.590

120.0 0.730

3.000

3.000

3.000

17.00

121.0

16.00

124.0

5,516

0.090

0.050

0.080

0.370

0.630 1.590

1.980

246.1

MS

df

f

df

MS

Second year

First year

0.480

0.446

3.264

44.17

3.578

45.53

544.6

0.114

0.387

4.343

5.572

6.701

1,364 8.341

1.005

1.122

6.073

43.47

5.596

44.45

1,982

0.536

0.927

4.251

7.219 18.20

22.64

2,816

f

0.822

0.846

0.024

\0.001**

0.016

\0.001**

\0.001**

0.995

0.886

0.006*

0.005*

\0.001**

\0.001** \0.001**

0.426

0.356

\0.001**

\0.001**

0.001*

\0.001**

\0.001**

0.780

0.478

\0.001**

\0.001** \0.001**

\0.001**

\0.001**

p

Games–Howell test

Table 2 Results of three-way ANOVA and two-way ANOVA testing differences in the mean numbers of fish species and individuals per transect (20 m2, n = 6) among microhabitats, stations and seasons in the first year and second year

Fish Sci (2014) 80:21–41 27

123

123 p

Games–Howell test

3 6 60

Season

Station 9 Season

Residuals

60

Residuals 2

6

Station 9 Season

Station

2 3

60

Residuals

Station

6

Station 9 Season

Season

3

60

Residuals

Season

6

Station 9 Season 2

3

Season

Station

2

Station

2.760

0.710

16.98

59.63

0.077

0.039

1.175

3.724

7.960

5.380

207.1

88.10

0.064

0.314

0.120

0.777

0.258

6.157

21.62

0.514

15.33

48.58

0.677

26.03

11.07

4.902

1.874

12.15

Sum = Aut \ Win = Spr

\0.001**

0.954

0.001*

\0.001**

US \ DS = MS

Win = Spr \ Sum

\0.001** 0.795

US \ DS = MS

\0.001**

0.669

DS \ US

* p \ 0.01, ** p \ 0.001

60

6

3

2

60

6

3

2

60

6

3

2

60

6

\0.001**

3

0.144

2

\0.001**

\0.001**

2.360

1.260

6.350

113.5

0.070

0.076

0.449

3.628

7.890

14.20

253.5

173.6

0.067

0.110

0.532

0.882

MS

df

f

df

MS

Second year

First year

DS downstream, MS midstream, US upstream, Sum summer, Aut Autumn, Win winter, Spr spring

Individuals

Species

Plant feeders

Individuals

Species

Zooplankton feeders

Table 2 continued

0.534

2.689

48.11

1.085

6.385

51.54

1.800

32.14

22.01

1.638

7.907

13.11

f

\0.001**

0.780

0.054

\0.001**

0.382

\0.001**

\0.001**

0.114

\0.001**

US \ DS = MS

US \ DS = MS

Sum \ Win \ Spr, Aut \ Spr

DS \ MS = US

Sum \ Win \ Spr, Aut \ Spr

\0.001** 0.152

DS \ MS = US

Games–Howell test

\0.001**

p

28 Fish Sci (2014) 80:21–41

Fish Sci (2014) 80:21–41 Benthic crustacean feeders

Zooplankton feeders

First year

25

Plant feeders

Others

Second year

20

Mean species number/20 m2

Fig. 3 Mean fish species and individual numbers per transect (20 m2, n = 6) for each trophic group in the mangrove-root and bare sand areas at each station in each season in the first and second years. DS downstream, MS midstream, US upstream

29

15

10

5

0 350

Mean individual number/20 m2

300 250

200

150 100 50

0 DS MS US DS MS US Summer

Autumn

ANOVA. The mean species and individual numbers of plant feeders were greater downstream and midstream than upstream in both years (Table 2), and the mean species number also varied significantly among seasons in both years, being higher in summer than in winter and spring of both, although a post hoc test did not detect a significant difference (Table 2). The mean species number of zooplankton feeders tended to be higher midstream and/or upstream than downstream, and highest in spring and lowest in summer in both years, although the differences between pairs were not always statistically significant in the first year (Table 2). The mean individual number showed similar tendencies, being higher in midstream and/or upstream than downstream, and highest in winter and spring (lowest in summer and autumn) (Table 2). The cluster analyses revealed that fish assemblages in each microhabitat fell into six spatial groups (Groups 1-1–1-6) in the first year and five (Groups 2-1–2-5) in the

DS MS US DS MS US Winter

Spring

DS MS US DS MS US Summer

Autumn

DS MS US DS MS US Winter

Spring

second, at a similarity level of 45 (Fig. 4). In both years, fish assemblages in one microhabitat type sometimes grouped together, but never with assemblages in the alternative type. The mangrove-root area assemblages could be subdivided into downstream and midstream (Groups 1-1 and 2-1), and upstream (Groups 1-2 and 2-2) assemblages, whereas such among-station differences were not observed for the bare sand area assemblages. In Groups 1-1 and 2-1, benthic crustacean feeders, such as Apogon amboinensis, Lutjanus argentimaculatus and L. fulvus, plant feeders (Neopomacentrus taeniurus and Pomacentrus taeniometopon) and zooplankton feeders (Parioglossus raoi and P. rainfordi) were dominant species. SIMPER analysis showed that those species contributed greatly to similarities within the groups (Table 3). In Group 1-2 and 2-2, zooplanktivous fish P. raoi and P. palustris were abundant and primarily responsible for the similarity within the groups (Table 3). Within the bare sand area

123

30

Fish Sci (2014) 80:21–41

Spring Spring Winter May Autumn Winter Autumn Summer Winter Summer Autumn Spring Winter Autumn Summer Spring Winter Autumn Summer Summer Winter Autumn Spring Summer

MS DS MS US MS DS DS DS US US US US US US US MS MS MS DS MS DS DS DS MS

Microhabitat S S 1–6 S S S 1–5 S S 1–4 S S S 1–3 S M M 1–2 M M M M M M 1–1 M M M M S

Winter Autumn Winter Autumn Spring Spring Winter Summer Spring Summer Summer Autumn Autumn Summer Spring Winter Spring Winter Autumn Summer Spring Winter Summer Autumn

MS DS DS MS US MS US US DS MS DS US US US US US DS DS DS DS MS MS MS MS

S S S S S S S S S S S S M M M M M M M M M M M M

Season

(a) First year

Station

*

(b) Second year

0

20

40

60

80

2–5

2–4

2–3

2–2

Food abundance and environmental factors The spatial and seasonal abundance patterns of the studied food resources are summarized in Fig. 5. Food item abundance sometimes differed among microhabitats, stations and/or seasons. Statistical values for some comparisons are shown in Table 4 (some values omitted due to space limitations). Environmental factors, shown in Table 5, are not dealt with specifically in the text for the same reason, although some brief descriptions are provided below. Of the main food items, crabs, polychaetes and detritus were more abundant in the areas with mangrove roots than in the bare sand areas, whereas zooplankton tended to be more abundant in the bare sand areas, although the differences were only marginally significant (Fig. 5. See also Table 4). Gammaridean amphipod density did not differ between the microhabitats. Macroalgae were attached to the prop roots in the mangrove-root area at each station, but were lacking in the adjacent open microhabitats, which consisted of soft substrata lacking above-ground, hard structures. The abundance of macroalgae, crabs, gammaridean amphipods and detritus differed among stations, although not so for the remaining items (Table 4). Macroalgae were significantly more abundant downstream and midstream than upstream (Table 4), whereas crabs and detritus were mostly abundant midstream and upstream, respectively (Fig. 5), although post hoc tests did not always detect significant differences between station-pairs (Table 4). Zooplankton density showed seasonal differences in both years (Table 4), being highest in summer and lowest in winter (Fig. 5. See also Table 4). Polychaete density showed a similar seasonal fluctuation pattern in the first year, although not in the second (Table 4). No seasonal differences in abundance were apparent for the remaining items (Table 4).

2–1

100

Bray-Curtis similarity index Fig. 4 Dendrograms of the cluster analyses showing similarities of fish assemblages based on the density of each fish species in the mangrove-root and bare sand areas at each station in each season in the first and second years. DS downstream, MS midstream, US upstream, M mangrove-root area, S bare sand area. At a Bray-Curtis similarity index level of 45, the assemblages were divided into six groups in the first year (1-1–1-6) and five groups in the second year (2-1–2-5). Asterisk indicates an assemblage not belonging to any group

123

groups, Gerres erythrourus, Terapon jarbua, Bathygobius fuscus and Favonigobius reichei were the dominant species.

The relationships between fishes, food resources and abiotic factors The first two axes of the CCA ordination explained 87.1 % of the variances of species-explanatory variable bi-plots in the first year (axis 1, 67.0 %; axis 2, 20.1 %) and 83.9 % of the variance in the second year (axis 1, 62.0 %; axis 2, 21.9 %) (Fig. 6). In the first year, the vectors of detritus and water turbidity, which tended to be more abundant or higher upstream, were on the right (positive) side of axis 1, whereas the vectors of other factors, such as macroalgae, crabs and salinity, which tended to be more abundant or higher downstream and/or midstream, were on the left

Fish Sci (2014) 80:21–41

31

Table 3 Results of a SIMPER analysis showing contributing rates of fish species to similarity of each group in the first year and second year First year Group/species

Second year TC

Mean ind.

Contribution (%)

Apogon amboinensis

B

75.9

17.2

Apogon amboinensis

B

82.4

17.7

Parioglossus raoi

Z

43.4

12.0

Neopomacentrus taeniurus

Pl

16.6

9.7

Group 1-1

Group/species

TC

Mean ind.

Contribution (%)

Group 2-1

Pomacentrus taeniometopon

Pl

12.0

7.5

Parioglossus raoi

Z

34.2

9.4

Pomadasys argenteus

B

10.0

6.2

Pomacentrus taeniometopon

Pl

11.8

8.9

Parioglossus rainfordi

Z

8.5

5.9

Lutjanus fulvus

B

11.8

7.9

Neopomacentrus taeniurus Lutjanus fulvus

Pl B

8.5 7.8

5.7 5.4

Lutjanus argentimaculatus Pomadasys argenteus

B B

10.1 5.5

6.9 4.4

Parioglossus palustris

Z

12.9

3.3

Lutjanus argentimaculatus

B

8.8

5.3


Z

11.1

3.5

Parioglossus raoi

Z

51.9

20.4

Parioglossus raoi

Z

65.4

29.1


Z

41.8

18.2


Z

44.8

22.9

Apogon amboinensis

B

14.3

12.4

Group 1-2

Group 2-2

Acentrogobius moloanus

B

2.5

6.6


B

3.8

5.6


B

1.0

4.5


Z

5.6

5.3

Terapon jarbua

B

1.5

4.4


B

1.9

5.0


Z

5.6

4.0

Terapon jarbua

B

1.9

4.1

B

0.2

100

B

0.5

100

Favonigobius reichei

B

0.7

43.1

B

0.2

100

Yongeichthys criniger Gerres erythrourus

B B

0.3 0.3

39.8 17.1

B

0.2

100

B

0.2

100


B

0.5

57.6

Bathygobius fuscus

B

0.2

42.4

Group 1-3 Terapon jarbua

Group 2-3

Group 1-4

Terapon jarbua Group 2-4 Favonigobius reichei Group 2-5 Bathygobius fuscus

Group 1-5 Favonigobius reichei Group 1-6

TC trophic category, Mean ind. mean individual number per transect (20 m2, n = 6) in each group. Trophic category: B benthic crustacean feeders, Z zooplankton feeders, Pl plant feeders

(negative) side (Fig. 6a). Macroalgae (correlation coefficient, r = -0.81), detritus (r = 0.77), salinity (r = -0.64) and crabs (r = -0.60) were highly correlated with axis 1, and water turbidity (r = 0.50) and crabs (r = 0.48) were highly correlated with axis 2. Regarding the relationships of fish trophic groups and environmental and food resource vectors in the ordination, the dominant species of benthic crustacean feeders, such as A. amboinensis, P. argenteus, L. argentimaculatus and L. fulvus, and plant feeders (N. taeniurus and P. taeniometopon), located on the left side in the bi-plots, were positively associated with their main food items (i.e., crabs and macroalgae) and salinity, which tended to be higher midstream and downstream (Fig. 6a). In contrast, most zooplankton feeders (P. raoi, P. palustris and P. rainfordi) fell on the right side, being positively associated with detritus and water turbidity, but negatively with prey abundance.

Ambassis miops, occupying the center of axis 1 and upper part of the ordination, was positively associated with water turbidity (Fig. 6a). Similar results were obtained for the second year (Fig. 6b).

Discussion The present study revealed that fish assemblage structures differed very considerably between microhabitats, such differences being consistent across stations and seasons. The mangrove-root area consistently supported greater numbers of fish species and individuals compared to the unvegetated substrata, contrary to the findings of several previous studies [19–21], even though supported the general notion that mangrove-vegetated areas harbored large numbers of fish species and individuals [e.g., 1].

123

32

Fish Sci (2014) 80:21–41 First year Mean biomass (g/cm2 )

0.15

Second year

Macroalgae

0.10

0.05

Mean individual number/m 2

Mean individual number/m 3

0 30000

Zooplankton

20000

10000

0

Crabs 20

10

Mean individual number/500 cm 3

Mean individual number/500 cm3

0

Gammaridean amphipods 400

200

0

400

200

0 20

Ignition loss (%)

Polychaetes

Detritus

10

0

DS MS US DS MS US Summer

Autumn

DS MS US

DS MS US

DS MS US

DS MS US

DS MS US

DS MS US

Winter

Spring

Summer

Autumn

Winter

Spring

Fig. 5 Mean abundance of each food resource in the mangrove-root (filled square) and bare sand (open square) areas at each station in each season in the first and second years. Abundances of each food resource expressed as: mean biomass (g/cm2, n = 5) for macroalgae, mean individual numbers for zooplankton (/m3, n = 5), crabs (/m2,

123

n = 5), gammaridean amphipods (/500 cm3, n = 5), polychaetes (/500 cm3, n = 5) and ignition loss (%) of sediment (n = 5) for detritus. Bars indicate standard deviation. DS downstream, MS midstream, US upstream

3 6 108

Season

Station 9 Season

Residuals

3 2 3 6 6 96

Station

Season



Station 9 Season


Residuals

3 2 3 6 6 96

Season



Station 9 Season


Residuals

3 2 3 6 6 96

Station

Season



Station 9 Season


Residuals 1 2 3

Microhabitat

Station

Season

Polychaetes

1 2

Microhabitat

Gammaridean amphipods

1 2

Microhabitat

Station

Crabs

1 2

Microhabitat

Zooplankton

2

Station

Macroalgae

38.90

6.800

537.1

13.73

9.060

20.63

12.45

73.44

18.06

102.3

4.920

0.340

0.190

0.080

0.150

6.500

0.350

5.410

138.2

461.0

98.00

167.0

169.0

262.0

31,186

1,561

2,188

0.0002

0.0001

0.0007

0.0067

9.561

1.682

132.1

0.660

1.503

0.906

5.349

1.315

7.448

0.358

0.551

0.242

0.448

19.25

1.024

16.02

409.6

0.213

0.363

0.366

0.568

67.62

3.386

4.745

0.596

3.710

37.42

2 3

\0.001**

1

96

6

6

3

2

3

0.191

\0.001**

0.682

0.186

0.441

0.006*

0.274

1 2

0.551

96

6

6

3

\0.001**

0.768

0.961

0.720

3 2

0.385 \0.001**

1 2

\0.001**

96

6

6

3

\0.001**

0.972

0.901

0.778

2

3

0.569

\0.001**

1

108

6

3

2

2 Win \ Aut \ Spr \ Sum

US \ DS = MS

0.038

0.032

0.733

0.014

\0.001**

Games–Howell test

12.80

22.10

653.9

20.43

5.700

6.100

44.45

85.62

38.45

188.4

18.09

0.022

0.004

0.005

0.028

0.408

0.011

0.347

9.590

885.0

88.00

156.0

481.0

75.00

47,203

2,138

4,117

0.0004

0.0002

0.0001

0.0100

MS

df

p

Second year f

df

MS

First year

1.974

3.397

100.6

0.279

0.299

2.176

4.192

1.883

9.225

0.885

0.168

0.211

1.266

18.27

0.488

15.56

429.7

0.099

0.176

0.543

0.085

53.31

2.414

4.649

0.670

0.292

28.19

f

0.123

0.038

\0.001**

0.945

0.936

0.096

0.018

0.138

\0.001**

0.349

0.985

0.972

0.291

\0.001**

0.691

\0.001**

\0.001**

0.996

0.983

0.654

0.918

\0.001**

0.095

0.034

0.674

0.831

\0.001**

p

MS \ DS = US

Win \ Aut \ Spr = Sum

US \ DS = MS

Games–Howell test

Table 4 Results of three-way ANOVA and two-way ANOVA testing differences in the mean abundances of each food resource among microhabitats, stations and seasons in the first year and second year

Fish Sci (2014) 80:21–41 33

123

Fish Sci (2014) 80:21–41

Table 4 continued

Greater food availability may be a factor responsible for greater fish species richness and abundance in the mangrove-root area. Mangrove root structures trap suspended organic particles [11] and harbor abundant epiphytic algae [12, 13], such organic materials attracting many small invertebrates, which in turn serve as important food resources for fish [e.g., 7]. In fact, the present study demonstrated that crabs and polychaetes, along with macroalgae and detritus, were most abundant in the mangrove-root areas, fishes utilizing such food items also frequenting the mangrove-root areas but seldom or never the sand areas. This strongly supported the importance of food availability in their habitat choice. The abundance patterns of two dominant trophic groups (benthic crustacean feeders and plant feeders) from downstream to upstream matched those of their food items. Benthic crustacean feeders were most abundant in the midstream mangrove-root area where their prey crabs (mainly grapsids, sesarmids and ocypodids) were also most abundant. Plant feeders also frequented the mangrove-root areas, grazing actively upon macroalgae on the roots (Nanjo K, pers. obs.), but never occurred in the sand areas lacking such macroalgae. They were especially abundant downstream and midstream where macroalgae flourished densely. Additionally, in the CCA ordination, most component species of the dominant trophic groups (e.g., L. argentimaculatus and P. taeniometopon) showed a positive correlation with food abundance, further evidence for the importance of food availability in determining fish distributions in a mangrove system. Because a greater food supply provides a potential advantage for fishes, such as faster growth [16], many mangrove fishes prefer mangrove-root areas with abundant food [see also 13]. The latter conducted field experiments at the Caribbean Island Curac¸ao using artificial mangrove-root units and found that herbivorous fish species occurred in the experimental units with both mangrove roots and fouling algae but not in units without algae, thereby concluding that food was important for fish distribution. The importance of food availability for fish distribution has been pointed out elsewhere [29–32]. Contrary to the findings for the above two trophic groups, the distribution patterns of zooplankton feeders could not be explained by food availability. Although they were restricted entirely to the mangrove-root area, zooplankton tended to be more abundant in the bare sand area. Additionally, in the CCA ordination, most component species did not show a positive correlation with their prey. A similar phenomenon, the abundance patterns of planktivorous fishes not coinciding with those of pelagic copepods in Alligator Creek, northern Australia, previously reported by Robertson et al. [33], adds weight to the possibility that factors other than food availability may be

0.988 0.152 0.080

0.010 6

96

0.276

0.833

0.261

\0.001** 11.21 2 \0.001**

0.920

1.309 0.110 3 0.356

0.465

1.357 0.110

0.040 6

3

\0.001**

\0.001** 14.02

1,261 103.6 1

2

\0.001**

\0.001**

1.150

6.500 96

0.967

0.738

0.688

0.895 0.372 2.400 6

0.227 1.500 6

0.422

0.376 2.400

2.700 3

2

df df

123

* p \ 0.01, ** p \ 0.001

DS downstream, MS midstream, US upstream, Sum summer, Aut Autumn, Win winter, Spr spring

0.450 0.970 Residuals

0.070 6

96


0.080

25.33 2 Station 9 Season

1.910

1.092 3 Microhabitat 9 Season

0.080

0.358

0.159 1.588

1.089

6 Microhabitat 9 Station

0.080 3 Season

0.120

15.33

1,179 88.72 1

2

Microhabitat

Station

Detritus

4.100 96 Residuals

1.150

0.803 0.505 6 Microhabitat 9 Station 9 Season

2.100

0.302 1.221 6 Station 9 Season

5.000

0.006*

0.841 0.174

4.389 17.80 3 Microhabitat 9 Season

0.700 2 Microhabitat 9 Station

MS

f

p

Games–Howell test

Second year First year

MS

f

p

Games–Howell test

34

4.9 ± 4.6

2.0 ± 1.0

1.7 ± 1.1

Water turbidity (NTU)

3.8 ± 1.5

M mangrove-root area, S bare sand area

157.6 ± 10


Grain size (lm)

22.3 ± 2.2

24.8 ± 9.4

Water temperature (°C)

Salinity

Second year

150.6 ± 14

22.9 ± 1.9

25.3 ± 8.2

200.4 ± 23

218.8 ± 24

22.1 ± 2.2

162.6 ± 5

8.1 ± 2.8

21.9 ± 8.5

21.1 ± 2.5

158.2 ± 4

3.3 ± 1.2

26.2 ± 2.3

227.2 ± 21

236.8 ± 18

134.8 ± 20

12.6 ± 7.9

15.6 ± 10.2

20.5 ± 2.5

130.4 ± 20

5.7 ± 2.5

25.9 ± 2.7

21.4 ± 2.8

M

Upstream

183.6 ± 18

181.0 ± 10

S

178.8 ± 8

25.1 ± 1.5

150.2 ± 7

3.1 ± 1.7

22.1 ± 4.8

157.0 ± 8

6.7 ± 4.4

27.2 ± 4.6

26.3 ± 2.2

151.8 ± 13

5.1 ± 1.5

27.7 ± 7.3

25.6 ± 2.0

M

M

S

7.7 ± 3.5 122.6 ± 15

3.7 ± 1.8 142.8 ± 24

M

229.0 ± 30

30.3 ± 2.4 24.8 ± 2.8

184.0 ± 15

Downstream


Grain size (lm)

5.3 ± 1.0 154.4 ± 17

9.2 ± 7.1 109.6 ± 13

Midstream

Salinity

First year

30.0 ± 2.1 27.4 ± 3.2

215.2 ± 23

23.8 ± 9.4

23.6 ± 2.3

M

Downstream S

5.3 ± 2.7 146.0 ± 7.2

29.9 ± 1.6 29.4 ± 3.1

S

Spring

196.8 ± 8

189.8 ± 15

30.1 ± 1.7 30.9 ± 2.2

M

Winter

142.6 ± 18


Grain size (lm)

29.8 ± 1.7

27.5 ± 4.5


Salinity

Second year

134.4 ± 23


Grain size (lm)

29.6 ± 1.3

31.4 ± 2.6


Salinity

First year

S

M

M

S

Downstream

Midstream

Downstream

Upstream

Autumn

Summer

192.8 ± 9

193.0 ± 15

S

200.4 ± 23

182.0 ± 8

S

173.6 ± 8

8.6 ± 3.9

27.0 ± 4.5

26.7 ± 2.4

155.0 ± 17

5.8 ± 1.7

25.8 ± 7.1

26.2 ± 2.3

M

Midstream

162.6 ± 5

6.1 ± 3.6

20.7 ± 5.3

24.5 ± 1.7

150.2 ± 8

5.0 ± 1.2

21.9 ± 8.4

24.3 ± 3.1

M

Midstream

237.2 ± 16

225.2 ± 18

S

227.2 ± 21

225.2 ± 9

S

134.0 ± 5

12.3 ± 3.7

21.8 ± 7.5

26.3 ± 2.7

134.4 ± 12

6.0 ± 1.7

19.9 ± 7.5

25.9 ± 2.7

M

Upstream

134.8 ± 20

7.4 ± 3.3

18.4 ± 7.7

24.2 ± 1.7

121.4 ± 15.6

8.7 ± 1.5

16.0 ± 8.1

23.7 ± 3.3

M

Upstream

181.2 ± 12

188.8 ± 7

S

183.6 ± 18

185.6 ± 8

S

Table 5 Summary of the environmental factors (mean ± standard deviation) in each microhabitat in each station in each season in the first year and second year in a study creek in the Urauchi River mangrove estuary

Fish Sci (2014) 80:21–41 35

123

36

Fish Sci (2014) 80:21–41

-1.0

(a) First year

A. mio

0.5

Turb Crab

P. arg P. tae Gs N. tae L. ful

L. arg P. pal P. rao

Amphi

P. rai

-1.0

-0.5

0

De

Po

Sal A. amb

Algae

CCA 2

Temp Zp

-1.0

-0.5

0

1.0

0.5

CCA 1

(b) Second year 1.0

A. mio

0.5

Gs

Crab Sal

0

CCA 2

Algae

Zp

P. arg L. arg N. tae P. tae Temp L. ful A. amb

Turb

Amphi

P. rai

De P. pal

P. rao

1.0

-0.5

Po

-1.0

-0.5

0

0.5

1.0

CCA 1

Fig. 6 Canonical correspondence analysis (CCA) ordination diagrams based on the densities of ten dominant fish species in the mangrove-root and bare sand areas at each station in each season in the first and second years; first axis is horizontal, second axis is vertical. Environmental factors and food resources represented by vectors. Temp water temperature, Sal salinity, Turb water turbidity, Gs median grain size, Algae macroalgae, Zp zooplankton, Crab crabs, Amphi gammaridean amphipods, Po polychaetes, De detritus. Black symbols, benthic crustacean feeders; gray symbols, zooplankton feeders; white symbols, plant feeders. Species abbreviations given in Table 1

more significant in the habitat choice of small planktivorous fishes within a mangrove system. The sheltering effect of habitat structural complexity against strong water movement and/or predators is sometimes considered as an important factor influencing fish distribution [7, 8, 34, 35]. In the present study, plankton

123

feeders comprised mainly hover gobies, such as Parioglossus raoi and P. palustris, hovering in and around the root structure, into which they usually retreated (indicating a sheltering effect) when the water current became strong or predatory fishes approached (Nanjo K, pers. obs.). Because hover gobies are small (up to ca. 40 mm TL) and are likely to have relatively weak swimming ability, therefore being highly vulnerable to predation [9], such a sheltering effect of root structure is likely to be essential. The CCA results supported this conclusion. In the ordination, hover gobies showed a positive correlation with detritus and water turbidity, and negative with sediment particle size. A greater amount of detritus, higher water turbidity and smaller sediment particles are characteristic of areas with weak water movement [36]. In fact, hover gobies were most abundant in the upstream area of the present study site, where water movement was attenuated. The sheltering effect may therefore be the most important determinant of their distribution pattern, compensating for the disadvantage of a lower food supply. In summary, the present fish assemblages mainly comprised mangrove-root associated fishes, resulting in greater fish species richness and abundance in mangrove-root areas. Food availability may be responsible for the distribution patterns of some mangrove-associated fishes, such as benthic crustacean feeders and plant feeders, which were restricted mostly to the mangrove-root areas, but not so for other types of mangrove fishes, such as zooplankton feeders. For the latter, other possible factors, such as the sheltering effects of mangrove root structure against water current and/or predators, may be more significant. Accordingly, the fish response to factors provided by mangrove vegetation, such as food availability and sheltering effects, may be species-specific, not to mention region-specific, since fish assemblage structures (e.g., species compositions and trophic structures) may differ greatly among regions [23]. Therefore, a small-scale approach, as employed here, should contribute to a better understanding of the relationships between mangrove habitat and resident fishes, in addition to being useful for designing fishery management strategies or conservation policies suitable to a targeted region. Acknowledgments We are grateful to Ken Sakihara, Akira Mizutani and the Okinawa Regional Research Center, Tokai University, for assistance with the fieldwork. Constructive comments on the manuscript from Graham Hardy and two anonymous reviewers were much appreciated. This study was funded by a Grant-in-Aid for Scientific Research (B) from the Japan Society for the Promotion of Science (No. 21380121).

Appendix See Table 6.

F B B

Ambassis sp.

Epinephelus ongus

Caranx ignobilis

Caranx melampygus

Caranx papuensis

Caranx sexfasciatus

Ambassidae

Serranidae

Carangidae

Po Z

Chaetodon auriga

Heniochus acuminatus

Chaetodontidae

Gobiidae B B

Acentrogobius janthinopterus


B

B

Ophiocara porocephala

B

Eleotris melanosoma

Pl

Omox sp.

Butis amboinensis

Pl

Omox biporos

Eleotridae

Pl

Omobranchus ferox

Blenniidae

B

Terapon jarbua

Teraponidae

I

Toxotes jaculatrix

Toxotidae

B

B

Monodactylus argenteus

B

Parupeneus spilurus

B

Sparidae sp.

Parupeneus indicus

B

Acanthopagrus sivicolus

Po

Gerres oyena B

B

Gerres filamentosus

Acanthopagrus pacificus

B

B

Lutjanus russellii

Gerres erythrourus

B

Lutjanus fulviflamma

B

Z

F

Monodactylidae

Mullidae

Sparidae

Gerreidae

Lutjanidae

B

Pterois volitans

Scorpaenidae

F

Strongylura incisa

Belonidae

I

D

Liza melinopterus

Zenarchopterus dunckeri

D

F

Liza macrolepis

F

Evenchelys macrurus

TC

Echidna rhodochilus

Species

Hemiramphidae

Mugilidae

Muraenidae

First year

Family

3–9

6–11

20–22

5

10

3

3–5

2–5

9–23

10

4–5

12–20

1–10

10

8–14

20

11–33

15–30

5–18

8

4–20

6–18

8–20

13–15

8–18

9–15

8–16

12–16

5

15

30

4–10

8–21

8–20

150–200

30

TL

0.8

1.5

0.2

0.8

0.8

1.0

3.3

0.5

0.7

0.2

2.3

2.0

0.2

0.5

1.0

0.2

0.2

0.2

0.2

0.2

1.8

0.2

0.3

0.3

1.3

0.2

0.7

1.0

0.2

0.2

0.2

0.2

S

1.8

0.3

0.3

0.2

0.2

0.2

0.8

0.8

M

0.2

S

0.7

0.2

0.2

0.3

0.8

7.3

0.7

7.7

1.3

1.2

2.8

0.7

0.7

0.2

0.8

1.8

0.2

M

0.3

S

M

M

S

Downstream

Midstream

Downstream

Upstream

Autumn

Summer

0.3

0.2

0.7

0.7

9.0

0.3

1.2

0.3

1.3

2.2

0.2

0.2

0.3

0.8

6.8

0.3

M

S

Midstream

3.8

2.2

0.2

0.2

0.2

2.0

0.5

0.5

0.2

M

0.2

S

Upstream

1.0

0.7

0.2

0.5

1.5

0.2

2.0

0.2

2.2

5.3

3.3

1.3

0.3

0.2

M

0.3

S

Downstream

Winter

0.3

0.3

3.0

0.2

1.5

5.5

0.5

0.7

0.2

0.3

M

0.2

S

Midstream

1.7

0.7

0.5

2.0

0.2

0.2

0.3

0.2

M

0.2

S

Upstream

0.2

0.2

0.7

0.2

0.2

0.7

2.8

0.7

1.3

0.7

0.2

M

S

Downstream

Spring

0.2

0.5

0.3

5.3

0.2

0.2

0.3

0.2

0.5

0.3

0.2

M

S

Midstream

2.7

1.0

1.5

0.3

2.8

2.0

M

S

Upstream

Table 6 Mean individual number of fish species (except ten dominant species) per transect (20 m2, n = 6) in the mangrove-root area and bare sand area at each station in each season in the first and second years

Fish Sci (2014) 80:21–41 37

123

123 Pl B B B B B B D B B B

Oligolepis acutipennis

Oligolepis stomias

Oxyurichthys cornutus

Oxyurichthys ophthalmonema

Oxyurichthys visayanus

Pandaka lidwilli

Pandaka trimaculata

Pseudogobius javanicus

Redigobius balteatus

Vanderhorstia lanceolata

Yongeichthys criniger

B B

Arothron reticularis

Chelonodon patoca

Epinephelus ongus

Caranx melampygus

Serranidae

Carangidae

D

F

B

I

Liza melinopterus

Zenarchopterus dunckeri

Hemiramphidae

D

Liza macrolepis

Mugilidae

F

Evenchelys macrurus

Muraenidae

Second year

B

Arothron manilensis

Tetraodontidae

F

Sphyraena barracuda

Sphyraenidae

Pl

Pl

Siganus guttatus

Acanthurus xanthopterus

Pl

Siganus fuscescens

Z

B

Glossogobius circumspectus

Parioglossus interruptus

F

Glossogobius biocellatus

Z

B


Parioglossus dotui

B

Exyrias puntang

4–7

B B

B B

Bathygobius fuscus

Cryptocentrus singapurensis

Drombus sp.

3–6 5–8

Pl

Amblygobius phalaena

Eviota prasina

4–10

Pl

Amblygobius linki

9–15

12–16

4–10

8–21

8–20

150–230

12

10

6

18–30

4–10

5–20

5

2–3

1–5

2–11

8

5

2–5

1

1–2

8

5–9

4–10

10

2–10

4–8

1–10

2–7

4–13

6

1–6

4–6

B

Acentrogobius multifasciatus

TL

TC

Species

Acanthuridae

Siganidae

Ptereleotridae

Family

Table 6 continued

0.8

0.7

0.8

0.2

0.2

0.2

2.7

3.5

0.2

5.5

0.2

0.2

0.2

3.2

3.3

0.3

0.7

0.5

0.7

0.5

1.0

0.3

0.3

1.7

0.8

0.3

1.5

3.7

1.5

15.2

1.3

0.3

0.5

2.7

0.2

0.8

0.2

0.3

1.0

0.3

0.2

0.2

0.8

4.8

0.2

0.2

0.3

1.3

7.8

0.8

M

S

0.2

0.2

1.7

0.2

2.0

2.0

1.7

1.7

0.2

0.3

0.2

2.2

0.5

M

0.5

0.2

0.2

S

Downstream

Upstream

M

M

S

Midstream

Downstream S

Autumn

Summer

0.7

0.8

8.5

0.2

0.8

0.2

0.2

1.7

1.2

0.5

2.7

0.2

M

0.2

S

Midstream

0.2

0.2

2.2

0.5

0.3

0.2

4.3

0.5

0.2

0.5

S

Upstream M

0.2

0.2

0.3

0.5

0.2

0.5

0.2

1.2

0.2

M

0.2

0.5

0.3

S

Downstream

Winter

0.2

0.3

0.3

0.7

0.5

0.2

0.3

2.8

0.3

0.2

0.2

S

Midstream M

0.3

0.3

1.0

0.7

1.0

0.5

0.2

0.2

S

Upstream M

0.5

0.2

0.2

3.0

1.7

19.7

0.2

1.0

0.2

0.2

0.2

M

0.7

0.2

S

Downstream

Spring

0.3

0.2

0.3

0.2

0.3

0.7

0.3

23.3

0.7

0.2

0.3

2.2

2.0

0.3

3.8 0.7

0.2

0.2

S

Midstream M

0.2

0.2

0.7

0.5

1.7

1.7

0.7

0.5

0.2

0.2

S

Upstream M

38 Fish Sci (2014) 80:21–41

B

Acanthopagrus sivicolus

Po Z

Chaetodon auriga

Heniochus acuminatus

Chaetodontidae

B B

Eleotris melanosoma

Ophiocara porocephala

Gobiidae

B

Butis amboinensis

Eleotridae

B Pl B B B B F B B Pl B

Amblygobius phalaena

Bathygobius fuscus

Cryptocentrus singapurensis

Exyrias puntang


Glossogobius biocellatus

Glossogobius circumspectus

Myersina macrostoma

Oligolepis acutipennis

Oxyurichthys cornutus

B

Acentrogobius multifasciatus Pl

B


Amblygobius hectori

B

Acentrogobius janthinopterus

Amblygobius linki

B

Acentrogobius audax

Pl

Omox biporos

Blenniidae

B

Terapon jarbua

Teraponidae

I

Toxotes jaculatrix

Toxotidae

B B

Parupeneus spilurus

Monodactylus argenteus

B

Parupeneus indicus

Monodactylidae

Mullidae

Acanthopagrus pacificus

Sparidae

B B

Lethrinidae sp.

Lethrinidae

B

Po

Plectorhinchus albovittatus

B

B

Lutjanus sp.

Gerres oyena

B

Gerres erythrourus

B

B

Caranx sexfasciatus

Lutjanus russellii

B

Caranx papuensis

Lutjanus fulviflamma

TC

Species

Haemulidae

Gerreidae

Lutjanidae

Family

Table 6 continued

4–10

2–10

4

4–7

1–10

2–7

4–13

7

4

4–10

1–6

6

5

3–9

6–11

4

20–25

5

10

3–5

9–23

10

4–5

12–20

1–10

10

8–14

11–33

15–30

6

12

5–22

4–20

8

6–18

8–20

13–15

8–18

TL

2.2

0.3

0.8

0.7

0.5

0.5

0.7

0.5

1.2

0.2

0.2

0.8

0.8

0.5

3.3

0.5

0.5

2.2

3.7

0.7

0.2

3.2

0.7

0.2

0.2

0.8

0.3

0.2

1.8

0.2

0.7

0.7

0.2

1.8

4.7

0.7

1.8

1.5

0.8

4.3

0.3

0.2

1.7

0.2

1.2

0.2

0.2

0.7

M

0.2

0.2

S

1.2

0.2

1.3

0.8

0.2

1.8

7.3

0.3

3.5

0.2

1.8

0.2

0.2

M

0.2

S

Downstream

Upstream

M

M

S

Midstream

Downstream S

Autumn

Summer

0.2

0.2

0.5

0.3

0.2

0.3

1.8

9.0

1.7

0.3

2.0

2.0

3.5

M

0.2

S

Midstream

0.5

1.0

3.5

0.5

7.2

1.5

0.2

0.2

0.2

1.8

0.5

0.3

0.7

0.2

S

Upstream M

0.2

0.2

0.2

0.2

0.8

0.2

2.7

1.5

1.2

5.2

10.5

3.5

1.2

M

0.2

S

Downstream

Winter

0.3

0.2

1.8

0.2

0.3

0.7

0.3

3.0

0.2

1.5

2.3

1.3

0.3

0.2

0.2

0.2

S

Midstream M

0.2

0.7

0.7

0.2

1.0

0.3

0.2

2.7

1.7

0.3

0.5

0.2

S

Upstream M

0.2

0.5

0.2

0.2

0.2

0.5

0.2

2.8

0.2

0.2

0.2

1.0

0.3

1.2

1.8

M

0.3

0.2

S

Downstream

Spring

1.5

0.5

0.5

2.5

1.3

0.2

5.3

0.2

0.2

0.3

0.2

1.7

0.2

0.2

S

Midstream M

0.7

1.3

0.7

0.2

2.7

0.8

1.3

0.7

1.0

0.2

S

Upstream M

Fish Sci (2014) 80:21–41 39

123

123 D B B B

Pseudogobius javanicus

Redigobius balteatus

Yongeichthys criniger

Gobiidae sp.

B B

Arothron manilensis

Chelonodon patoca

Tetraodontidae 14

6

18–30

4–10

5–20

5

8

2–3

1–5

4

2–11

3

2–5

1–2

8

5–10

TL

0.2

1.8

0.8

0.2

0.2

5.3

0.2

0.2

2.0

0.3

1.0

2.2

3.3

0.7

3.2

7.8

2.2

M

S

0.2

0.2

1.2

3.5

0.2

1.5

M

S

Downstream

Upstream

M

M

S

Midstream

Downstream S

Autumn

Summer

0.2

0.7

0.2

0.2

0.2

M

S

Midstream

0.2

5.3

0.5

0.5

S

Upstream M

2.5

1.7

1.2

0.2

M

S

Downstream

Winter

0.5

6.7

0.3

0.2

S

Midstream M

2.8

0.2

0.3

0.5

1.0

S

Upstream M

0.3

1.7

3.8

0.5

0.2

M

S

Downstream

Spring

0.7

0.2

0.3

46.7

0.8

0.2

1.3

S

Midstream M

0.7

0.7

4.2

2.0

0.7

S

Upstream M

TC trophic category, TL total length (cm), M mangrove-root area, S bare sand area. Trophic category; B benthic crustacean feeders, Z zooplankton feeders, Pl plant feeders, Po polychaete feeders, F fish feeders, D detritus feeders, I insect feeders

F

Sphyraena barracuda

Sphyraenidae

Pl

Acanthurus xanthopterus

Pl

Siganus guttatus

Acanthuridae

Pl

Siganus fuscescens

D

Scatophagus argus

Siganidae

Z

B

Pandaka lidwilli

Z

B

Oxyurichthys visayanus

Parioglossus interruptus

B

Oxyurichthys ophthalmonema

Parioglossus dotui

TC

Species

Scatophagidae

Ptereleotridae

Family

Table 6 continued

40 Fish Sci (2014) 80:21–41

Fish Sci (2014) 80:21–41

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