Changes in the Macrobenthic Fauna of the Shigetomi-higata Tidal Flats in Kagoshima Bay: Comparison between 1994 and 2005

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1 64: 3244 (2009) Japanese Journal of Benthology Changes in the Macrobenthic Fauna of the Shigetomi-higata Tidal Flats in Kagoshima Bay: Comparison between 1994 and ), 1) 2) 2) 1) ) Tomoko YAMAMOTO 1),, Ai MASUYA 1),, Koji MATSUSHITA 2) and Masanori SATO 2) 1) Faculty of Fisheries, Kagoshima University Shimoarata, Kagoshima , Japan 2) Faculty of Science, Kagoshima University Korimoto, Kagoshima , Japan Abstract: Long-term macrobenthic faunal change was investigated in the Shigetomi-higata tidal flats of northern Kagoshima Bay by means of surveys conducted in spring and autumn of 1994 and Density and biomass of all species of macrobenthic animals and sediment characteristics were surveyed along four transect lines covering the entire intertidal area of the flats. In total, 37 and 38 species were collected from this area in 1994 and 2005 respectively. Density and biomass of the various benthic animals have changed di#erently among the transects, but gastropods remarkably increased in both density and biomass during this period along most of the transects. Especially, Batillaria multiformis dominated the flats in 2005 but were not found in In contrast, the density, biomass, and species number of bivalves decreased, and decrease of Ruditapes philippinarum in both density and size of individuals was remarkable. The dominant polychaete changed from Notomastus sp. with a larger body size to Armandia lanceolata with a smaller body size. In general, epibenthic and smaller species increased whereas endobenthic and larger species and larger individuals decreased during this period. We could not identify the environmental factors responsible for causing these faunal changes, but topographic changes in the tidal flats may have played a role in the biomass change of R. philippinarum. Key Words: Armandia, Batillaria, macrobenthos, faunal change, Notomastus, Ruditapes, tidal flats. 1993; 1994 (1994) ha ha ; km, 80 km, 1,130 Received 19 May 2008 Accepted 30 June 2009 Corresponding author km km ha 30 ha

2 ; 1981; 1984; 1985; 1988; 1993; 1994; ; ; 2005; (Fig. 1). 900 m 400 m 500 m 1997 Fig. 1. Maps showing the location of the study site (Shigetomi-higata tidal flats) in Kyushu, Japan (right), and the locations of four transect lines on the tidal flats (left). The limits of the area exposed at the lowest tide in October, 1994, are indicated by dashed lines (Fig. 1) cm15 cm, cm30 cm 40 cm40 cm cm25 cm m m m m 2 30 cm 1mm (nmds) (Bray-Curtis Index) 33

3 Bray-Curtis Index i x Ai x Bi (1) X A X B x Ai, x Bi A, B i X A, X B SPSS MDS cm cm 29 mm , mm 63 mm MRK-RETAC mm 1cm m mm 1cm (IS/Mill-E iuchi) 11 Wilcoxon Kendall (Table 1) (Musculista senhousia), (Nuttallia japonica), (Psammotaea minor), (Solen strictus), (Phacosoma japonicum) (Moerella rutila), (Clithon oualaniensis), (Batillaria multiformis), (B. multiformis) (B. cumingii) ( 2003) nmds , , 3 34

4 Fig. 2. Non-metric multidimensional scaling analysis of the benthic animal community in each quadrat. The distances between plots represents their similarity. Each symbol indicates quadrats along the same transect line in the same season and year. Closed symbols represent the data from spring of 1994, and open ones the spring of 2005; grey symbols show the data from autumn in both years. Positions (transect line number and distance from land) are shown beside the plots of quadrats isolated from others in the same transect line during the same season and year. MDS (Fig. 2) m 270 m m m m 90 m (Ruditapes philippinarum) (Fig. 3a, Table 2). 1m g (Fig. 3b) m g g/m g/m Fig. 3. Changes in macrobenthic community composition on the Shigetomi-higata tidal flats between 1994 and Averages of (a) density and (b) biomass (wet weight) for all four transect lines were calculated. 35

5 Table 1. List of benthic species sampled along each transect line during Phylum Class Japanese Name Species Name Cnidaria Anthozoa 1 Actiniaria gen. sp. Platyhelminthes Turbellaria 1 Platyhelminthes gen. sp. Nemertea 1 Nemertinea gen. sp. Mollusca Gastropoda Clithon oualaniensis Batillaria multiformis Reticunassa festiba Bivalvia Musculista senhousia Mactra veneriformis Moerella rutila Macoma tokyoensis Nuttallia japonica Psammotaea minor Solen strictus Phacosoma japonicum Ruditapes philippinarum Laternula marilina Annelida Polychaeta Glycera nicobarica Hemipodia yenourensis 1 Goniada sp. Sigambra hanaokai 1 Syllidae gen. sp. 1 Hediste sp. Ceratonereis erythraeensis 1 Leonnnates sp. 1 Nephtyidae gen. sp. 1 Chrysopetalidae gen. sp. Marphysa sanguinea 1 Marphysa sp. 1 Lumbrineridae gen. sp. Pseudopolydora cf. kempi 1 Scolelepis sp. 1 Prionospio sp. Mesochaetopterus japonicus Cirriformia tentaculata Armandia lanceolata 1 Notomastus sp. 1 Capitellidae gen. sp. 1 Polychaeta gen. sp. Arthropoda Crustacea sp. 1 Amphipoda gen. sp. 1 sp. 2 Amphipoda gen. sp. 2 Neomysis japonica 1 Cumacea gen. sp. 1 Caprellidae gen. sp. Hippolytidae gen. sp. Crangon a$nis complex Callianassa japonica Upogebia yokoyai Philyra pisum Scopimera globosa Hemigrapsus penicillatus 1 Grapsidae gen. sp. Polyonyx sinensis 1 Paguridae gen. sp. Diogenes nitidimanus Echinodermata Holothuroidea Patinapta ooplax No. of species Total area of quadrats (m 2 ) ) Identified by Ken-ichi Hayashi. ) Identified by Katsuji Sakai. N) Only nest tubes were sampled. 36

6 surveys in the Shigetomi-higata tidal flats of Kagoshima Bay in 1994 and spring 2005 spring 1994 autumn 2005 autumn line 1 line 2 line 3 line 4 line 1 line 2 line 3 line 4 line 1 line 2 line 3 line 4 line 1 line 4 N (lines 1, 4: 15) (lines 1, 4: 0.36)

7 Table 2. Mean density (no. of individuals per 1 m 2 ) of macrobenthic species along each transect line in the Shigetomi-higata tidal flats no data indicates that the sample was too small or in poor condition. line 1 spring Phylum Class Japanese Name Species Name Cnidaria Anthozoa 1 Actiniaria gen. sp. 4.0 (0.15) Platyhelminthes Turbellaria 1 Platyhelminthes gen. sp. Nemertea 1 Nemertinea gen. sp. 4.0 no data Mollusca Gastropoda Clithon oualaniensis Batillaria multiformis 96.0 (0.85) Reticunassa festiba 6.0 Bivalvia Musculista senhousia Mactra veneriformis Moerella rutila 22.0 (0.17) Macoma tokyoensis Nuttallia japonica Psammotaea minor 5.7 Solen strictus Phacosoma japonicum Ruditapes philippinarum (0.49) (0.42) Laternula marilina 3.7 Annelida Polychaeta Glycera nicobarica 11.7 Hemipodia yenourensis Goniada sp. 2.0 Sigambra hanaokai 1 Syllidae gen. sp Hediste sp. Ceratonereis erythraeensis Leonnnates sp. 1 Nephtyidae gen. sp. 1 Chrysopetalidae gen. sp. Marphysa sanguinea 1 Marphysa sp Lumbrineridae gen. sp Pseudopolydora cf. kempi Scolelepis sp. 1 Prionospio sp. Mesochaetopterus japonicus 2.0 Cirriformia tentaculata Armandia lanceolata (0.01) (0.01) 1 Notomastus sp (0.35) no data 1 Capitellidae gen. sp Polychaeta gen. sp. Arthropoda Crustacea 1 (sp. 1) Amphipoda gen. sp (0.002) 1 (sp. 2) Amphipoda gen. sp. 2 Neomysis japonica 1 Cumacea gen. sp Caprellidae gen. sp. 1 Hippolytidae gen. sp. Crangon a$nis complex Callianassa japonica (0.06) (0.96) Upogebia yokoyai Philyra pisum Scopimera globosa Hemigrapsus penicillatus Grapsidae gen. sp. Polyonyx sinensis 1 Paguridae gen. sp. 2.0 Diogenes nitidimanus 38

8 of Kagoshima Bay ( indicates absence). Wet weight (g) per individual is shown in parentheses for the dominant species of each class; line 2 spring line 3 spring line 4 spring line 1 autumn line 4 autumn no data 4.9 (0.01) no data no data (0.42) (0.76) (0.35) (0.15) (0.06) (0.05) (0.06) (0.03) (3.23) (5.06) (0.53) (0.39) (0.24) (0.29) (2.69) (0.40) (1.42) (0.32) (0.004) (0.01) (0.001) (0.12) (0.23) (0.03) (0.02) (0.003) (0.001) (0.006) 43.4 (0.001) (1.68) (0.02) (0.09) (0.24)

9 1 0.4 g 2.7 g 0.06 g 0.17 g (Table 2) g 0.4 g (Table 2) : 100 /m /m 2 3: 130 /m /m 2 (Fig. 3a). 2 1m g (Fig. 3b, Table 2), 3 50 g/m 2 20 g/m (Fig. 3b) g 0.4 g (Table 2). 2, 3 Notomastus sp. (Armandia lanceolata) g g (Table 2). 4 (Fig. 3a) /m 2 70 /m /m 2 80 /m g/m 2 10 g/m 2 40 g/m 2 10 g/m 2 (Fig. 3b). (Table 2) Hediste diadroma H. atoka 2005 Notomastus sp. (Fig. 4) m 493 /m 2 ; 1466 /m 2 (Fig. 4a, b), m (Fig. 4a, b), 656 /m 2 ; 912 /m 2 60 m 30 m 2, : 30 m 75 m 3: 10 m 210 m (Fig. 4c, d) (Fig. 4c), 3 (Fig. 4d) m m 180 m 4 30 m, 60 m, 150 m, 210 m (Fig. 4e) m 2005 (Fig. 4f). 3. Fig. 5 Table Fig. 5ad m 300 m m 3 50 cm Fig. 5ad : : 211 3: 14 4: : 171 2: : 310 4: 461 Wilcoxon n20, p m : Wilcoxon n10, p Wilcoxon n10, p Wilcoxon n7, p0.05 (SD) 2.21 ( 40

10 Fig. 4. Changes in vertical distribution of macrobenthic animals on the Shigetomi-higata tidal flats between 1994 and The number of individuals per 1 m 2 was calculated for each quadrat. Figures of zero ( 0 ) in (e) indicate quadrats from which no macrobenthic animals were recovered. Symbol explanations in (f) pertain to all graphs. 0.61) (SD) 0.43 (0.43) Fig. 5ad m Kendall n33, p0.05 (Table 3), : : 31 3: : : : : 932 4: m 3 90 m 4 30 m m m MDS (Fig. 2)

11 Fig. 5. Environmental characteristics of each transect line (a-d: lines 14, respectively). Upper graphs show the profiles of the tidal flats along the transects. Middle graphs indicate the mud contents at each sampling point along the transects. Lower graphs show the proportion of ignition loss at each sampling point along the transects. MHWS: mean high water level in spring tides; MTL: mean tidal level; MLWS: mean low water level in spring tides. Symbol explanations in (d) pertain to all graphs. Sato (1994) (Table 2) Notomastus sp Notomastus sp. (1996)

12 Table 3. Salinity of the interstitial water in each quadrat along the four transect lines in the Shigetomi-higata tidal flats of Kagoshima Bay. Water samples were not taken in some quadrats, indicated by. Transect Distance from land September 1994 () April 2005 () Line 1 30 m m m m m m m 30.0 MeanSD Line 2 30 m m m m 18.2 MeanSD Line 3 30 m m m m m m m 18.8 MeanSD Line 4 30 m m m m m m m m m 32.0 MeanSD m m ; Notomastus sp cm

13 NPO pp pp pp : : : WWF Japan Science Report, 2: Calanus, 13: : pp pp pp : : : pp pp Heteromastus, Mediomastus, Notomastus Journal of National Fisheries University, 54: pp : : pp : 115. Sato, S Analysis of the relationship between growth and sexual maturation in Phacosoma japonicum (Bivalvia: Veneridae). Marine Biology, 118: pp p : : : WWF Japan Science Report, 3: : Nature Study, 34: Nature of Kagoshima, 35:

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