Marine Biology (2006) 149: 1185-1197 DOI 10.1007/s00227-006-0298-0

RESEARCH ARTICLE

Paolo Magni • Serena Como • Shigeru Montani Hiroaki Tsutsumi Interlinked temporal changes in environmental conditions, chemical characteristics of sediments and macrofaunal assemblages in an estuarine intertidal sandflat (Seto Inland Sea,Japan)

Received: 11 November 2005 / Accepted: 20 January 2006 / Published online: 21 March 2006 © Springer-Verlag 2006

Abstract Five field surveys were conducted in an estu­ sation of macrofauna, initiated by few opportunistic arine intertidal sandflat of the Seto Inland Sea (Japan) polychaetes (e.g., Cirriformia tentaculata and Polydora between April 1994 and April 1995. Chlorophyll a, sp.), apparently promoting a fast sediment recovery in pheopigments, total organic carbon and acid-volatile winter, and followed by new bivalve recruits in the next sulphides (AVS) of surface and subsurface sediments, spring. This study provides the first evidence of significant and macrofaunal assemblages were investigated in par­ and interlinked within-year changes in chemical char­ allel at 15 stations. Monthly hydrological data of low- acteristics of sediments and macrofaunal assemblages tide creek water adjacent to the flat were used as a com­ in an estuarine intertidal flat at a small spatial scale (i.e., plementary environmental characterisation of the tens of meters). This demonstrates the high temporal study area. Strong temporal changes were found among variability of species-environment relations in these sampling dates, most remarkably in autumn with a systems and a close relationship in seasonally driven major increase of algal detritus and AVS, a sharp trophodynamic processes among primary producers reduction in macrofaunal abundances and species rich­ and benthic consumers. We conclude that a thorough ness, and a massive mortality of the clam Ruditapes parallel evaluation of the temporal changes in chemical philippinarum. This dystrophic event was preceded by a characteristics of sediments should be taken into photoautotrophic and hypertrophic spring-summer account in assessing the year-round distribution and characterized by abundant fresh (i.e., living) algal mate­ changes of intertidal macrofauna, particularly in eutro- rial, including microphytobenthos and macroalgae phic, estuarine intertidal flats. ( Ulva sp.). In summer, abundant macrofaunal assem­ blages reached the highest biomass values (455 g wet weight m ~2 or 60.6 g ash free dry weight m -2), with a major contribution of filter-feeding bivalves Musculista Introduction senhousia and R. philippinarum. These are among the highest values reported in the literature for sedimentary Numerous studies on sandy beaches have recognized shores. From autumn, there was a progressive recoloni- physical forces (e.g., tidal level and beach morphody- namic states), environmental harshness (e.g., sediment instability) and sediment bulk properties (e.g., grain size) as major factors affecting macrofaunal distribution Conniiunicated by R. Cattaneo-Vietti, Genova (Dexter 1984; Allen and M oore 1987; Jaramillo et al. 1993; Brazeiro and Defeo 1996; James and Fairweather P. M agni (ED) • S. C om o IMC - International Marine Centre, Località Sa Mardini, 1996; McLachlan 1996; Defeo and McLachlan 2005). In Torregrande, 09072 Oristano, Italy tidally dominated estuarine flats, benthic animals are E-mail : [email protected] also exposed to a highly dynamic environment, as related to tidal state and amplitude, current velocity and sedi­ S. M ontani Graduate School of Environmental Science, ment morphodynamics (Grant 1981; Renshun 1992; Hokkaido University, Kita 13 Nislii 8 , Dyer et al. 2000; Magni and M ontani 2005). Accord­ Kita-ku, Sapporo, 060-0813 Hokkaido , Japan ingly, intertidal macrofauna possess a variety of capacity adaptations (sensu Gillmor 1982) to cope with the effect H. Tsutsumi Faculty of Environmental & Symbiotic Sciences, of physical variables, including changes in mechanical Prefectural University of Kumamoto, activity (Tamaki 1987; Richardson et al. 1993) and feed­ 3-1-100 Tsukide, 863-8502 Kumamoto , Japan ing behaviour (Miller et al. 1992; Hawkins et al. 1996; 1186

Karrh and Miller 1996). Along with species-specific extended studies on sediment characteristics and micro- adaptational strategies, estuarine macrofauna tend to phytobenthic assemblages (Magni and Montani 1997; associate in patchy assemblages (Reise 1979; Thrush Magni et al. 2000a; M ontani et al. 2003), water chemistry 1991; Morrisey et al. 1992; Crooks 1998) and may (M ontani et al. 1998; Magni and M ontani 2000), and remain relatively stable in terms of their spatial distribu­ benthic macrofauna (Magni and M ontani 1998; Magni tion (McArdle and Blackwell 1989; Krager and Woodin et al. 2000b). Complete emersion of the study area occurs 1993), even where the sediment and organisms are twice a month, during a spring low tide, at about +50 cm mobile (Hewitt et al. 1997). Ysebaert and Herman (2002) the local (Takamatsu port) mean sea level (Magni and assessed the influence of environmental variables (e.g., M ontani 1998). D uration of sediment emersion varies mud content, chlorophyll a (chi a), bed-level height, between few hours per cycle in December-January to salinity, tidal current velocity) on the interannual vari­ less than 1-2 h/cycle in September-October (Magni and ability of estuarine intertidal macrofauna at various spa­ M ontani 1998). At low tide, a creek of the river Shin con­ tial scales, varying from kilometres to metres. They nects the upper estuary to the rear to the adjacent sub- showed that on larger ( 104—103 m) spatial scales “assem­ tidal zone (Fig. 1). blages and individual-species abundances correlate sig­ nificantly with the environmental variables that are Field sampling influenced by geomorphological changes” (Ysebaert and Herman 2002). Samplings were conducted at low tide at 15 stations In addition to physical variables, especially in estua­ randomly chosen within a surface area of about rine tidal flats, re-suspension and deposition of organic 50x100 m and were repeated on five different dates matter from the overlying water, in situ processes of between spring 1994 and spring 1995: 25 April (spring micro- and macroalgal production and decompositon 94, Sp94), 22 July (summer, Su), 25 October (autumn, A) tend to be high and strongly fluctuating throughout the and 20 January (winter, W) 1994, and 15 April 1995 year (Heip et al. 1995; Magni and M ontani 2000; (spring 95, Sp95). At each sampling station, emerged M ontani et al. 2003). These processes suggest that the sediment samples were collected for geochemical analy­ chemical characteristics of sediments may also have sis at seven to eight locations using an acrylic core tube major implications on the composition and temporal (3 cm i.d.) gently pushed by hand into the sediment. The changes of macrofaunal assemblages. On the other hand, surface (0-0.5 cm) and subsurface (0.5-2 cm) layers few field studies are available in this regard (Castel et al. were carefully sliced off the sediment. Sediment samples 1989), especially on a year-round basis in estuarine from the same layer were pooled together and brought intertidal sandflats. to the laboratory within 2 h for further treatment and This work is a follow-up of a multi-year study on the chemical analysis. Duplicate sediment samples for mac­ cycling of biophilic elements (C, N, P, Si) conducted in a rofauna were collected at each station using a 100-cm2 tidal estuary of the Seto Inland Sea, Japan (e.g., Magni stainless steel core (10 cm in depth) and sieved on a 1998; M ontani et al. 1998; Magni and M ontani 2000). In mesh size of 1 mm. The residue of each replicate was the present work, we investigated the year-round distri­ separately fixed in a 10% buffered formaldehyde solu­ bution of hydrological features of low-tide creek water, tion, stained with rose Bengal. chemical characteristics of sediments and macrofaunal Low-tide ebbing water near the emerged flat was assemblages in the lower part of the sandflat. We aimed monitored at two creek stations monthly between 1994 to evaluate the temporal changes in both environmental and 1996, as extensively reported in Magni and Montani variables, including sediment chi a, pheopigments, total (2000). We present here the mean values of major hydro- organic carbon (TOC) and acid-volatile sulphide (AVS), logical variables most relevant to this study [i.e., temper­ and macrofauna, and to assess their relationships. This ature, salinity, dissolved oxygen (DO), NH^N, chi a, work is intended to assess temporal patterns, links and pheopigments, particulate organic carbon (POC) and trophodynamic processes among primary producers and total suspended matter (TSM)] and redirect for details benthic consumers of an estuarine intertidal sandflat on water sample treatment and analysis to our compan­ occurring on a year-round basis at a small spatial scale ion paper (Magni and M ontani 2000). (i.e., tens of meters ). Sediment sample treatment and analysis

In the laboratory, chi a and phyto-pigment degradation Materials and methods products (pheopigments) were extracted from duplicate subsamples of wet sediment (about 1 g) using 90% ace­ Study area tone. After 24 h of darkness at 4°C, the samples were sonicated for 5 min, centrifuged at 3,000 rpm (1000 g) We conducted the investigations on a sandflat of the for 10 min, and extracts were spectrophotometrically Seto Inland Sea, southwestern Japan (Fig. 1). The flat is analysed (Jasco, Flvidec—320). Chi a and pheopigment located in a mixed-semidiurnal type estuary (mean tidal values were obtained before and after acidification with range of about 2 m) where we have previously conducted 1 N HC1, respectively, according to Lorenzen’s (1967) 1187

Seto Inland, 2000). From the same pool of fresh sediments, the AVS Sea concentrations, as a measure of reducing conditions of sediments, were determined simultaneously in duplicate

YashimaJ subsamples (about 1 g) using a H2S-absorbent column km (GASTEC, Kanagawa, Japan). Phyto-pigment and AVS values were expressed as pg g_1 and mg g_1 of DW sediment, respectively. The water content was obtained after drying sediment subsamples at 105°C for 20 h. The TOC concentration of DW sediments (only in the surface layer) was determined from freeze-dried subsamples, after acidification with 2 N HC1 and neu­ tralization with NaOH, using a CHN analyser (Yanako). Macrofauna was sorted, identified to the species level, Yashima when possible, counted under a stereo-microscope (Olympus, Wild M3Z) and preserved in 75% ethanol and 10 m 2.5% ethylene-glycol. All individuals of a species in a given core were grouped for biomass measurements. The Seto Inland Sea wet weights (WW) of polychaetes and minor and/or fs™! : uncommon taxa were obtained from each sample after carefully blotting off any excess fluid. The two dominant bivalves Musculista senhousia and Ruditapes philippina­ rum were weighed with shells. Their soft tissue WW bio­ mass was then calculated using a linear equation obtained from the shell-length/weight relationship of 291 and 155 individuals, respectively, collected in different periods from the same study area. These animals were depurated in the laboratory and their length, total weights (TW), WW and DW were measured, as detailed in Magni et al. (2000b). Relevant equations were WW = 0.320xTW —0.002 (r2 = 0.885, P < 0.001) for M. senhousia and WW = 0.167xTW+0.025 (r2 = 0.886, P < 0.001 ) for R. phil­ — Low tide creek ippinarum. Takamatsu city Statistical analysis

Temporal changes in the chemical characteristics of sedi­ ments (i.e., chi a, pheopigments, pheopigments to chia ratio, TOC and AVS) were analysed using one-factor model ANOVA (Underwood, 1997). Factor “dates” (D; Tsumeta River Shin River 5 levels) was fixed and there were 15 replicates for each

2 0 0 4 0 0 m date. Differences among dates in macrofaunal assem­ blages in terms of abundances and biomass were tested using one-factor permutational multivariate analysis of Fig. 1 Location of the study area on an estuarine sandflat of the Seto Inland Sea, southwestern Japan. On the flat, the approximate variance, PERMANOVA (Anderson 2001; McArdle and area of sediment sampling comprising 15 stations (rectangular box) Anderson 2001), based on Bray-Curtis (dis)similarity and the tidal creek, formed at low tide, for hydrological measure­ measures. SIMPER was used to identify taxa which con­ ments are indicated tribute most to the differences among dates (Clarke 1993). Changes in total abundance (V), total number of species (S), Shannon-Weiner diversity (PI'), and total biomass, and abundance and biomass of the taxa identi­ method, as described by Parsons et al. (1984), where the fied by SIMPER, were analysed by one-factor model volume of water is substituted by the dry weight (DW) ANOVA. Factor “dates” (D; 5 levels) was fixed and of the sediment expressed in grams. Acetone-extract- there were 15 replicates for each date. When significant able chi a estimates, obtained after correction for deg­ differences in the factors of interest were found, a posteri­ radation products (i.e., pheopigments), were considered ori comparisons were done using SNK test (Underwood as a reliable indicator of (living) microphytobenthic 1997), as indicated in Results section. Homogeneity of biomass in surface sediments according to concurrent variances was checked using Cochran’s C-test (Winer spectrophotometric and HPLC comparative measure­ et al. 1991), and when necessary, data were log(v+l) ments which gave similar chi a estimates (Magni et al. transformed to remove the heterogeneous variances. 1188

(A) in both layers (4.7±0.6 and 7.0±1.0, surface and sub­ Results surface, respectively). This ratio tended to be higher at the subsurface than at the surface in each sampling date. Hydrological features of low-tide water Major changes among dates were also observed in the

Figure 2 shows the temporal distribution of hydrological variables in low-tide creek water. Temperature varied G 36 between 5.6 (February) and 32.2°C (July), and salinity var­ &... ied between 22.7 (June) and 30.4 psu (April 1995). There was an opposite trend of DO (range 3.2-12.6 mg I-1) and 18 18 NHjN (range 11.7-89.4 pM) concentrations, with a major increase of NH^N in October, in coincidence with the low­ V. est DO values. Subsequently, DO increased throughout C 0 winter and spring, while NH^N peaked in winter and sharply decreased in the next spring. With regard to the 18 100 temporal distribution of particulate compounds, two major peaks occurred in August and October (Fig. 2). They most noticeably differed from each other in that chi o Q 9 a concentration was highest in August, while pheopig­ CD— ments, POC and TSM were highest in October. Consistent with this trend, chi a was poorly correlated with pheopig­ ments and POC, and not significantly correlated with 0 TSM, while pheopigments, POC and TSM were strongly correlated with each others (Table 1). In addition, salinity 120 was not significantly correlated with chi a, while it was correlated positively with DO and negatively with NH^N, S pheopigments, POC and TSM (Table 1 ).

Sediment characteristics 0 Lfc During sampling activities, the temperature of emerged sediments closely paralleled that of low-tide ebbing water, 20 560 widely ranging between 4.5 (February) and 30.8°C (July) (Magni et al. 2000). There were also strong changes in the chemical characteristics of sediments among dates (Fig. 3, U O 10 280 gj Table 2). Chi a ranged from 2.9±0.4 (subsurface, A) to &H 8.7±0.5 |ig g_1 (surface, Sp95) and was significantly lower in the autumn date (A) than in all other sampling dates in both surface and subsurface layers. Pheopigments showed 0 ..e-* a different trend from that of chi a. At the surface pheopig­ AMJ J A SONDJ FMA 95 ments were higher in the summer date (Su, 22.5±1.7 94 pig g-1) than in all other sampling dates (minimum of Fig. 2 Temporal variations (mean ± SE) of hydrological variables 8.2±0.7 pig g_1 in W), while at the subsurface they tended in low-tide water of a creek located near the emerged tidal flat (see to increase progressively from the spring (Sp94) to the Fig. 1 ). F rom top to bottom: temperature and salinity, dissolved oxy­ autumn (A) dates. Consistent with these temporal gen (DO) and ammonium (NHjN), chlorophyll a (Chi a) and pheo- pigm ents (pheop), and particulate organic carbon (POC) and total changes, the pheopigments to chia ratio showed an oppo­ suspended matter (TSM). Interrupted lines: data not available be­ site trend to that of chi a, being highest in the autumn date tween 2 m onths

Table 1 Correlation coefficient R among hydrological variables

Tem p Sal DO Chi a Pheop POC

DO 0.68** (n = 19) N H jN -0 .6 2 * * (n = 23) -0.52**(77 = 27) -0.56** (77 = 21) Pheop -0.62** (71 = 26) 0.42* (77 = 35) D CD CD , ir , ir

0 9 9 *** II Il POC -0.61** (n = 27) 0.40* (77 = 35) TSM -0.52**(77 = 27) 0.95*** 0.96*** (77 = 36)

Only statistically significant correlations are indicated: *P<0.05, **p<0.01, ***P<0.001; in bold: negative correlations DO dissolved oxygen, Chi a chlorophyll a, Pheop pheopigments,POC particulate organic carbon, TSM total suspended matter, n num ber o f samples 1189

AVS concentrations which sharply increased in the abundance and only for 12% of the total number of taxa. autumn date (A) in both surface and subsurface layers Crustaceans and gastropods comprised 6 and 1% of the (0.31±0.11 and 0.49±0.09 mg g_1, respectively), when they total abundance, and 27 and 6% of the total number of were significantly higher than in all other sampling dates. taxa, respectively. By contrast, bivalves dominated the TOC in surface sediments varied between 6.2±1.0 ( W) and biomass, M. senhousia and R. philippinarum comprising 11.7±2.8 mg g_1 (A) and tended to be higher in the sum­ 73% of the total biomass. Polychaetes, crustaceans and mer (Su) and autumn (A) dates than in the spring (both gastropods accounted for 25, 0.6 and 0.4% of the total Sp94 and Sp95) and winter (W) dates (Fig. 3), althougli the biomass, respectively. SNK test failed to discriminate alternative hypothesis Macrofaunal assemblages were different in the five (Table 2). sampling dates in terms of abundances and biomass (Table 3). The autumn date (A) showed the greatest val­ Macrofaunal assemblages ues of dissimilarities within dates, both in terms of abun­ dances and biomass, and among dates in terms of A total of 11,146 specimens belonging to 33 taxa were abundances (Table 3). collected. Polychaetes were dominant, comprising 57% The results from analyses of variance for the total of the total abundance and 55% of the total number of abundance (N), total number of species (S), Shannon- taxa. Seven out of the 18 polychaetes taxa found were Wiener diversity (Hr) and total biomass, are reported in most abundant (i.e., 75% of the total abundances of Table 4. S, N and H’ showed a decrease in the autumn polychaetes and 43% of total abundances). Bivalves, date (A) in respect to all other dates, although it was not overwhelmingly represented by M. senhousia and R. phil­ possible to identify this pattern with the SNK test at ippinarum (i.e., 99%), contributed for 36% of the total P = 0.05 (Table 4; Fig. 4). Twelve and five taxa, respectively, contributed most for the differences among dates in terms of abundances and biomass (SIMPER analysis, cut-off 70%; see Table 5 Surface (0-0.5 cm) Subsurface (0.5-2 cm) for the reference list ). The analyses of variance and the post hoc comparisons indicated that the abundances of Cirriphormia tentaculata decreased in the summer date (Table 5; Fig. 5), and those of R. philippinarum, Gam­ maridae sp. and Polydora sp. decreased in the autumn ! II III ■I date (Table 5), although it was not possible to identify this pattern with the SNK test for Polydora sp. (Table 5). As an example, R. philippinarum is illustrated in Fig. 5. Gammaridae sp. was also less abundant in the spring ■ I I - -■■■ 1994 date (Sp94). On the contrary, the abundances of

Table 2 Analyses of variance for chlorophyll a (Chi a) concentra­ tions in the surface layer (0-0.5 cm) of sediments for differences among dates, and SNK test. Summary of analyses of variance and SNK test for the other sediment variables in both surface and sub­ - 0.6 -, surface layers so Source d f MS F P S N K test

Chi a D ate 4 2.04 18.87 0 . 0 0 0 0 A < Sp94 = Su = W = Sp95 Sp94 Su A W Sp95 Residual 70 0 . 1 1 T otal 74 er 16 MS p S N K test 60 R ajo bO Other sediment variables ê s Surface (0-0.5 cm): U Pheop 498.33 19.47 0 . 0 0 0 0 Su > Sp94 = A = W = Sp95 R o Pheop/C hl a 2.35 30.43 0 . 0 0 0 0 A > Su > Sp94 = W = Sp9s AVS 0.09 34.95 0 . 0 0 0 0 A > Sp94 = Su = W = Sp9( Sp94 Su A W Sp95 TOC 0.85 4.05 0.0052 NAH Subsurface (0.5-2 cm) Fig. 3 M ean concentrations (;j = 15 ± SE) o f sedim ent variables in Chi a 0.48 4.81 0.0018 A < S p94 = Su = W = Sp9, the surface (0-0.5 cm, left side) and subsurface (0.5-2 cm, right side) Pheop 307.51 3.22 0.0175 NAH layers in each sampling date. From top to bottom: chlorophyll a (Chi Pheop/C hl a 47.94 12.60 0 . 0 0 0 0 A > Su = Sp94 = W = Sp9s a), pheopigments(pheop), pheopigm ents to chlorophylla (PheoplChl AVS 0.15 10.30 0 . 0 0 0 0 A > S p94 = Su = W = Sp9, a) ratio, acid-volatile sulphide (AVS) and total organic carbon (TO C). Sp94 spring 1994, Su sum m er, A autum n, W w inter, Sp95 Pheop pheopigm ents,A V S acid-volatile sulphides, TOC total organ­ spring 1995 ic carbon. NAH no alternative hypothesis 1190

Table 3 PERM AN OVA on Bray-Curtis dissimilarities for differences oí macrofaunal assemblages among dates in ternis of abundances and biomasses

Source df M S F P Within dates Among dates

A bundances Date 4 5,386.57 4.50 0.001 Sp94 41.35 Sp9 4 vs. Su 43.74 R esidual 70 1,197.59 Su 38.70 Sp9 4 vs. A 58.22 T otal 74 A 60.85 Sp9 4 vs. W 49.53 W 44.11 Sp9 4 vs. Sp95 45.27 Sp95 37.60 Su vs. A 60.19 Su vs. W 48.40 Su vs. Sp9s 44.05 A vs. W 56.43 A vs. Sp95 58.17 W vs. Sp95 45.77 d f M S F P Within dates Among dates Biomasses Date 4 4,497.10 2.92 0.001 Sp94 35.11 Sp9 4 vs. Su 48.04 Residual 70 1,542.04 Su 39.84 Sp9 4 vs. A 59.61 T otal 74 A 64.25 Sp9 4 vs. W 49.77 W 55.71 Sp9 4 vs. Sp95 45.96 Sp95 49.70 Su vs. A 57.42 Su vs. W 52.41 Su vs. Sp9s 50.98 A vs. W 52.41 A vs. Sp95 50.98 W vs. Sp95 61.28

Mean Bray-Curtis dissimilarity (%) within and among dates are also reported. Data were square-root transformed (Clarke 1993; Clarke and W arw ick 2001 ) Spg4 spring 1994, Su sum m er, A autum n, W w inter, Sp95 spring 1995

Tig. 4 M ean (7j = 15±SH) ab u n ­ 140 dances (ind. 1 0 0 cm -2, N), num ­ ber of species (S), Shannon- Wiener diversity (H') and total 70 biom ass (g W W 100 cm -2 ) in each sampling date. Sp94 spring 1994, Su sum m er, A autum n, W ■■■■I i l l i i i winter, Spg5 spring 1995

1

liuiSp94 Su A W Sp95 dilliiSp94 Su A W Sp95

Spionidae sp., Dimorphostylis sp. and Capitella sp. here based on individual-species, owing to similar pat­ increased in Su, Sp94 and Sp95, respectively (Table 5). terns of assemblage changes in relation to environmental Unlike the abundances of M. senhousia which did not changes. One of the main reasons was the relatively good show significant differences among sampling dates, the correspondence between the dominant species and each biomass of this bivalve was greater in the summer (Su) trophic group (i.e., filter-feeding bivalves M. senhousia and autumn (A) dates, although the SNK test failed to and R. philippinarum, deposit-feeding polychaetes Cirri­ discriminate alternative hypothesis (Table 5, Fig. 5). formia tentaculata, Capitella sp. and Polydora sp., and Greater biomass was also described for R. philippinarum grazing crustacean Gammaridae sp.). in the summer date (Su) (Table 5, Fig. 5). For Polydora sp. the biomass was greater in the spring 1995 date (Sp95) Relationships of macrofauna with sediment (Table 5, Fig. 5). On the contrary, the biomass of C. ten­ characteristics taculata was lower in the summer (Su) and autumn (A) dates (Table 5, Fig. 5). We found several significant correlations between As a side note, results of analysis based on trophic chemical variables of sediments and macrofauna. Most groups (not shown) were consistent with those presented noticeably, chi a, pheopigments and TOC in surface 1191

Table 4 Analyses of variance for the total abundance (N) for differences among dates, and SNK test. Summary of analyses of variance and SNK test for the total number of species (S), Shannon-W iener diversity (H'), and total biomass

Source d f MS F P S N K test

Total abundance ( N) D ate 4 28.50 3.01 0.0238 NAH Residual 70 9.47 Total 74

MS R ajo P S N K test

Total no. of species 5 75.25 7.72 0 . 0 0 0 0 NAH H' 0.76 5.72 0.0005 NAH Total biomass 0.67 1.42 0.2358 NS

NAH no alternative hypothesis, NS no significant effects

Fig. 5 M ean (7j = 15±SH) ab u n ­ Abundances (ind. 100 cm'2) Biomass (gWW 100 cm'2) dances (left side) an d biom ass 16 (right side) o f Cirriformia tentac­ ulata, Ruditapes philippinarum, Musculista senhousia an d P oly­ dora sp. Sp94 spring 1994, Su sum m er, A autum n, W w inter, Sp95 spring 1995 l-iii I..Il S 40

Bí o lii-i 20 ■s 10 Lii.i -il». 50 - 8 25 —.I Sp„4 Su A W Sp9, Sp94 Su A W Sp9,

and/or subsurface sediments were all positively corre­ 8 and 13 vs. 10, respectively). By contrast, among chem­ lated with the total abundance (TV), total number of ical variables of sediments, subsurface AVS alone gave species (S ), Shannon-W iener diversity ( II' ) and the all negative correlations with macrofaunal univariate total biomass (Table 6). The abundances and/or bio­ measures, including N, S, H ' , the abundances of R. phil­ mass of several dominant taxa were also positively cor­ ippinarum, Polydora sp. and Dimorphostylis sp., and the related with chemical variables of sediments, most biomass of C. tentacidata and Polydora sp. (Table 6). strongly M. senhousia with pheopigments and TOC. Finally, temperature of emerged sediments was corre­ Among individual variables, subsurface chi a had the lated positively with S, H ', total biomass, the abun­ highest number of highly significant (P< 0.001) correla­ dances and biomass of R. philippinarum, and the tions with macrofauna. As to both chi a and pheopig­ abundances of M. senhousia, and correlated negatively ments, the subsurface showed a relatively larger with the abundance and biomass of C. tentaculata number of positive correlations than the surface (14 vs. (Table 6). 1192

Table 5 Analyses oí variance for the abundance of Cirriphormia tentaculata for differences among dates, and SNK test and summary of analyses of variance and SNK test for the taxa contributing most for the differences among dates in terms of abundances and biomass (SIMPER, cut-off 70%)

Source d f MS F P SN K test

C. tentaculata D ate 4 4.14 5.58 0.0006 S u < S p94 = A = W = Sp9 R esidual 70 0.74 T otal 74

MS -^ 4 ,7 0 P SN K test A bundances R. philippinarum 9.80 13.41 0 . 0 0 0 0 A < W = Sp94 = Su = Sp9 Gammaridae sp. 6 . 2 0 19.36 0 . 0 0 0 0 Sp94 = A < W = Su = Sp9 Polydora sp. 9.57 8.25 0 . 0 0 0 0 NAH Spionidae sp. 17.74 6.17 0.0003 S u > S p94 = A = W = Sp9 Dimorphostylis sp. 17.39 10.38 0 . 0 0 0 0 Sp9 4 > S u > A = W = Sp9 Capitella sp. 69.84 12.98 0 . 0 0 0 0 Su = Sp94 = A = W < Sp9 M. senhousia 1.51 0.96 0.4348 NS C. erithraeensis 1.32 0.97 0.4294 NS A. oxycephala 0.54 1.05 0.3893 NS C. muromiensis 0.43 2.35 0.0627 NS Nephtys sp. 0.25 1.71 0.1583 NS

Biomass M. senhousia 1.50 3.99 0.0056 NAH R. philippinarum 1.15 7.88 0 . 0 0 0 0 S u > S p94 = A = W = Sp9 C. tentaculata 0.18 7.31 0 . 0 0 0 1 Su = A < S p94 = W = Sp9 C. erithraeensis 0 . 1 1 1.76 0.1464 NS Polydora sp. 0.07 5.68 0.0005 Su = Sp94 = A = W < Sp9

NAH no alternative hypothesis, NS no significant effects

Table 6 Correlation coefficient R between sediment variables and dominant macrofaunal taxa

Tem p Chi a surf Chi a subsurf Pheop surf Pheop subsurf T O C surf AVS surf AVS subsurf

N 0.31** Q 49*** 0.25* 0.32** 0.31** —0.41*** S 0.23* 0.45*** 0.41*** 0.35** 0.23* 0.32** —0.40*** H' 0.23* 0.36** 0.25* 0.28* 0.27* -0.32** T ot-bio 0.25* 0.31** 0.51*** 0.43*** 0.52***

A bundances M. senhousia 0.29* 0 4g*** 0.34** 0 4 7 *** R. philippinarum 0.31** 0.36** —0.41*** Capitella sp. 0.35** 0.31** C. tentaculata -0.50*** 0.28* Nephtys sp. 0.23* C. erithraeensis 0.28* 0.38** 0.35** -0 .2 4 * A. oxycephala 0.27* 0.26* 0.31** -0 .2 3 * Polydora sp. 0.28* 0 45 *** 0.25* -0.32** Spionidae sp. 0.43*** 0.31** Gammaridae sp. 0.23* 0.26* 0.38** 0.26* 0.24* 0.26* -0 .2 4 * Dimorphostylis sp. 0.25* -0 .2 6 * C. muromiensis 0.31**

Biomass M. senhousia 0.52*** 0.45*** 0.55*** 0.25* R. philippinarum Q 4g*** 0.27* 0.34** C. tentaculata -0 .2 8 * 0.31** -0.32** C. erithraeensis 0.41*** Q 4g*** 0.31** Polydora sp. 0.24* 0 4i*** 0.25* -0 .2 9 *

Only statistically significant correlations are indicated: *P< 0.05, **P<0.01, ***P< 0.001; in bold: negative correlations; n = 15) N total abundance, S total number of species, H' Shannon-Wiener index, Tot-bio total biomass, Temp surface sediment temperature, CU a chlorophyll a, Pheop pheopigments,TOC total organic carbon, A VS acid-volatile sulphide, su rf surface, i.e. 0-0.5 cm, subsurf subsurface, i.e. 0.5-2 cm 1193

Bourget 1999) and provide an indirect, novel evidence of Discussion the high potential for secondary production in a typical small-sized, estuarine intertidal flat of Japan. The need to continually check the nature of the species- It has been shown that microphytobenthos and algal- environment relations in a changing estuary and the lack enriched suspended matter are primary food sources to of evidence of macrofaunal responses to within-year intertidal benthic animals (Middelburg et al. 2000; Takai changes in environmental variables within the intertidal et al. 2002, 2004), the latter especially important to filter zone has been emphasized recently (Ysebaert and Her­ feeders such as R. philippinarum (Kasai et al. 2004; m an 2002). This study provides the first evidence of sig­ Kanaya et al. 2005). Recent field experiments in Ulva- nificant and interlinked within-year changes in chemical dominated areas further suggest that benthic grazers characteristics of sediments, including phyto-pigments, such as amphipods can consume significant amounts of TOC and AVS, and macrofaunal assemblages in an estu­ macroalgae provided that there are no hypoxic condi­ arine intertidal flat at a small spatial scale (i.e., tens of tions and depending on the seasonal cycles of Ulva itself meters). This demonstrates the high flexibility and strong (Balducci et al. 2001; Sfriso et al. 2001). The importance temporal variability of these systems, and a close rela­ of detritus and associated bacteria in coastal food webs tionship in seasonally-driven trophodynamic processes is also well established (e.g., M ann 1986; Lopez and among primary producers and benthic consumers. Levington 1987; D ’Avanzo et al. 1991). In the case of From spring to summer 1994, strong solar radiation macroalgae, Everett (1994) conducted removal experi­ and high temperatures (Magni and Montani 2000) ments on Ulva expansa to measure the effects of algal favoured the development of conspicuous algal assem­ cover on the structure of an intertidal benthic assem­ blages (Magni and M ontani 1998; M ontani et al. 2003 ). blage. He concluded that increased abundance of small High chi a concentrations in both ebbing water (e.g., deposit-feeding macrofauna after a season of algal cover August, Fig. 2) and surface sediments (e.g., spring and was likely a result of an increase of food resource due to summer dates, Fig. 3), along with low pheopigments to in situ burial and decomposition of U. expansa (Everett chi a ratios, were evidences of a large fraction of fresh 1994). Uchida and Numaguchi (1996) investigated (i.e., living) algal material. High amounts of macroalgae microbial decomposition of U. pertusa from Japanese Ulva sp. were also periodically found in our study area, coastal waters. They suggested that the formation of pro­ especially between July and mid-September (P. Magni, toplasmatic detritus from the macroalgae may represent direct observations). Algal development seemed to be a readily available food source to macrofauna. Whitlatch consistent with high DO and low nutrient (e.g. ammo­ (1981) further indicated that food abundance and vari­ nium) concentrations in tidal stream in spring-summer, ety, related to a seasonal change in abundance of during daytime (Fig. 2, see also Magni and Montani organic-mineral aggregates (“detritus”), may regulate 2000). We found, however, that Ulva may be responsible the organization of deposit-feeding assemblages. for strong diurnal variations in water column DO, vary­ In our study area, high primary production estimates of ing from over-saturation (up to > 200%) during irradi­ microphytobenthos (on average 1.2 gC m~2 d-1, Montani ated and wann hours, to hypoxia (i.e., < 20%) at dawn et al. 2003) support the inference that, especially in (Magni and Montani 2005). During the growing period, spring-summer, large amounts of fresh algal material are macroalgal mats did not apparently negatively affect readily available to benthic consumers. Parallel to intense macrofaunal assemblages. By contrast, macrofaunal algal production in spring-summer, high amounts of total biomass nearly tripled between the spring and the detrital algal material may become progressively summer dates (1.67±0.16 and 4.55±0.82 g available on the flat from various sources, including WW 100 cm~2, respectively), with a major contribution decaying microalgae, either in situ produced or trans­ of bivalves M. senhousia and R. philippinarum which ported from the upper estuary (Magni and Montani 1997, increased their biomass nearly 11 (from 0.18±0.09 to 2000; Magni et al. 2002), and Ulva fragments that par­ 1.96±0.54 g WW 100 cm~2) and 4 times (from 0.55±0.11 tially accumulate onto the sediment. Grazing pressure by to 2.11±0.35g WWlOOcnG2), respectively. We infer abundant animals may also contribute to reduce the liv­ that in spring-summer high rates of benthic nutrient ing phyto-Carbon fraction by converting chloro-pig- regeneration related to the activity of abundant macrofa­ ments to phytosynthetic degradation products (Nicotri una (Magni et al. 2000; Bartoli et al. 2001) may have 1977; Bianchi et al. 1988; Abele-Oescher and Theede acted as a positive feedback to Ulva requirements of 1991; Smith et al. 1996). In this study, we consistently nutrients (Bartoli et al. 2003, 2005). Based on wet weight found multiple positive correlations between macrofauna (WW) to DW and ash free dry weight (AFDW) conver­ and both chi a and pheopigments (the latter most corre­ sion factors (Ricciardi and Bourget 1998; Magni et al. lated with organic-carbon, in sediments as well as in ebb­ 2000), we calculated the mean annual macrofaunal bio­ ing water). This indicates that in our study area both mass in our study area as to be 42.5 g AFDW m ~2 (or living and detrital algal materials are important food 311 g W W m -2), up to a maximum of 60.6 g A FDW m ~2 sources able to sustain abundant macrofauna. Among (or 455 g WW m-2) in the summer date. These values are dominant bivalves, it is interesting to note that while among the highest animal standing stocks reported in R. philippinarum was strongly correlated with chi a the literature for sedimentary shores (Ricciardi and and little with pheopigments, M. senhousia was highly 1194 correlated with pheopigments (and TOC), in both surface spring to summer, abruptly crashed in autumn when sed­ and subsurface sediments, but it was not with chi a iments, found darkish and bad smelling, were largely (Table 6). These results suggest possible feeding and/or covered by open shell of (dead) bivalves, mostly R. phil­ behavioural differences between R. philippinarum and ippinarum. By contrast, the thin-shelled mytilid M. sen­ M. senhousia, the former importantly relying on fresh housia, which did not show any negative correlation with algal material from the water column (Kasai et al. 2004; AVS, displayed similar life-span characteristics as Kanaya et al. 2005), either re-suspended or transported, described in other bays and estuaries in Japan and the latter more closely linked to the presence of sedimen­ around the world (Tanaka and Kikuchi 1978; Crooks tary algal detritus. Several polychaetes were also posi­ 1996 and therein references), quickly growing in spring- tively correlated with chi a and pheopigments, especially in summer and gradually decreasing from autumn through­ the subsurface layer. This seemed to be consistent with the out winter. M. senhousia thus appeared to be more resis­ progressive increase and burial onto the sediments of tant than R. philippinarum to the unfavourable phyto-pigments in summer and autumn, and an increase of environmental conditions occurred in late summer. The deposit-feeders and scavengers in autumn (see also below). drop in abundances of R. philippinarum in the autumn According to recurrent seasonal patterns, large date may actually have been exacerbated by the presence amounts of Ulva sp., particularly abundant in early Sep­ of M. senhousia which increased in biomass during sum­ tember (Magni, direct observation), rapidly decayed mer and autumn. Similarly to other mussel species between late September and early October. Consistently, (Commito et al. 2005 and reference therein), M. senhou­ temporal changes in the relative amount of fresh and sia is known to form compact and complex mats, and to detrital algal material were most evident in the autumn alter the surrounding habitat by binding the sediment sampling date with a general decrease of chi a and a with its byssal threads (Crooks 1998). Crooks (2001) marked increase of pheopigments (and organic-carbon) showed for instance that the survivorship of clams was both in the sediments and ebbing water (Figs. 2, 3). Ulva reduced in the presence of mussel and its mats. By con­ decay occurred in coincidence with unfavourable meteo­ trast, Mistri (2004) did not find differences in the rological conditions, including a drastic reduction of mortality of R. philippinarum at different densities of solar radiation and temperature drop, and a seasonally M. senhousia. In our study, the presence of M. senhousia higher mean low-tide water level which left our sampling mats may have enhanced the effects of unfavourable stations submerged for several days, thus impeding air environmental conditions in autumn by acting as a trap exposure of sediments (Magni and Montani 1998 ). These of accumulating bio-deposits and algal detritus in events may have triggered the formation and persistence decomposition. A reduction of oxygen penetrability in of low-DO water masses within the intertidal zone and surface sediments seems to be consistent with the (only) the subsequent enhancement of hydrogen sulphide pro­ positive correlation found between the biomass of duction related to the presence of decaying algal mate­ M. senhousia and surface AVS. In contrast to R. philipp­ rial, with a possible synergistic, toxic effect of macroalgal inarum, the polychaete Cirriphormia tentaculata strongly exudates (Norkko and Bonsdorff 1996a, b). In the recovered in abundances in the autumn date following autumn date, macrofaunal assemblages showed the most the reduction described in the summer date (Fig. 5, remarkable changes, with a sharp reduction in abun­ Table 5). We infer that in autumn, reduced conditions of dances and species richness, and the largest within date sediments and high amounts of algal-derived detrital dissimilarity. The latter was even larger than the among organic-C may have favoured species showing opportu­ date dissimilarity. We infer that this could be related to nistic life traits, such as C. tentaculata, Polydora sp. and decaying Ulva that causes a more patchy environment. Capitella sp. (Cognetti 1982; Tsutsumi 1987; Tagliapietra Although the effect of sulphide on various benthic et al. 1998). The presence of mats ofM. senhousia was animals has been extensively investigated in laboratory thus likely to drive the recruitment after the dystrophic experiments (Fansó 1991; Fueller 1994; Oeschger and event. Specifically, M. senhousia may have facilitated Vismann 1994; Saiz-Salinas and Francés-Zubillaga 1997) opportunistic species and inhibited others by entrapping there are relatively few field data available on the rela­ detritus for a longer period of time than in the case of tionships between AVS and macrofaunal assemblages in bare sediments, as described for other mussel species coastal marine environments (Tsutsumi and Kikuchi (Commito et al. 2005 and reference therein). 1983; Yokoyama 1998, 2002; Magni et al. 2005 ), and Macrofaunal recolonisation occurred throughout the even fewer in tidal flats (Meksumpun and Merksumpun winter with a progressive increase of small-sized, deposit- 1999). This study clearly shows how a significant increase feeding and scavenger polychaetes. As an example, while of AVS in both surface and subsurface sediments in the abundance of the deposit-feeder C. tentaculata m ark­ autumn corresponded to the most remarkable changes edly increased in the autumn date, its biomass remained as among macrofaunal assemblages. This was emphasized low as that in the summer date, indicating the progressive by the negative correlation between AVS and several recruitment of this polychaete. In the subsequent spring, individual taxa among bivalves (e.g., R philippinarum), the biomass of C. tentaculata and most significantly that polychaetes (e.g., Polydora sp.) and crustaceans (e.g., of Polydora sp. was highest (Fig. 5, Table 5 ). These tempo­ Gammaridae sp.). Most evidently, the hard-shelled clam ral changes suggest a trophic shift from filter-feeding biv­ R. philippinarum, which had strongly increased from alves in spring-summer, characterized by large amounts of 1195 fresh, suspended algal material, to deposit-feeders in Acknowledgements We wish to thank K. Ichimi and the students of autumn, characterized by a larger availability of sedimen­ the Laboratory of Environmental Oceanography, Kagawa Univer­ sity, particularly T. Sezaki and M. Harada, for their cooperation tary, detrital phyto-carbon. Following the late-summer during the field work and assistance in the laboratory. This study dystrophic crisis, sediment recolonisation was parallel to was partly supported by a research fund ( 15201001 ) from the Minis­ the sharp and fast decrease of AVS in both surface and try of Education, Culture, Sports, Science and Technology of Japan subsurface sediments, suggesting a beneficial effect of bur­ (Grant-in-Aid of Scientific Research). It is contribution number rowing macrofauna, in the reoxidation and detoxification MPS-06013 of the EU Network of Excellence MarBEF. of the sediments through sediment reworking (Bartoli et al. 2000). Subsequent to the recolonisation of opportu­ nistic polychaetes, M. senhousia and most remarkably References R. philippinarum showed a major increase in abundances in spring 1995, indicating the settlement of new popula­ Abele-Oescher D, Theede H (1991) Digestion of algal pigments by tions of bivalves and the re-establishment of environmen­ the common periwinkle Littorina littorea L. (Gastropoda) J Exp tal conditions and macrofaunal assemblages similar to M ar Biol Ecol 147:177-184 those found in the previous year, in spring 1994. Allen PL, Moore JJ (1987) Invertebrate macrolaima as potential indicators of sandy beach instability. Estuar Coast Shelf Sei 24:109-125 Aim IY, Choi JW (1998) Macrobenthic communities impacted by anthropogenic activities in an intertidal sand flat on the west Conclusions coast (Yellow sea) of Korea. M ar Poll Bull 36:808-817 Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust J Ecol 26:32-46 In the light of our results, the following within-year tem­ Arias AM, Drake P (1994) Structure and production of the benthic poral patterns and links among primary producers and macroinvertebrate community in a shallow lagoon in the Bay of benthic consumers, and trophodynamic processes are pro­ Cádiz. M ar Ecol Prog Ser 115:151-167 posed; Balducci C, Sfriso A, Pavoni B (2001) Macrofauna impact on Ulva rigida C. Ag. Production and relationship with environmental • Spring-summer; high primary production of micro­ variables in the lagoon of Venice. M ar Environ Res 52:27-49 phytobenthos and Ulva, and progressive increase of Bartoli M, Nizzoli D, Welsh DT, Viaroli P (2000) Short-term influ­ ence of recolonisation by the polychaete worm Nereis succinea algal detritus; presence of abundant and diverse mac­ on oxygen and nitrogen fluxes and denitrification: a microcosm rofaunal assemblages dominated by deposit-feeding simulation. Hydrobiologja 431:165-174 polychaetes (abundances) and filter-feeding bivalves Bartoli M, Nizzoli D, Viaroli P, Turolla E, Castaldelli G, Fano EA, (biomass); fast growth of bivalves M. senhousia and Rossi R (2001) Impact of Tapes philippinarum on nutrient R. philippinarum contributing to animal biomass val­ dynamics and benthic respiration in the Sacca di Goro. Hydro- biologia 455:203-212 ues among the highest reported in the literature for Bartoli M, Naldi M, Nizzoli D, Roubaix V, Viaroli P (2003) Influ­ sedimentary shores. ence of clam fanning on macroalgal growth: a microcosm exper­ • Fate summer, early autumn; rapid decomposition of iment. Cheni Ecol 19:147-160 excessive amounts of algal-derived organic material Bartoli M, Nizzoli D, Naldi M, Vezzulli L, Porrello S, Lenzi M, Viar­ oli P (2005) Inorganic nitrogen control in wastewater treatment and subsequent production of toxic hydrogen sulphide ponds from a fish fanii (Orbetello, Italy): denitrification versus in sediments; drastic shift from a photoautotrophic Ulva uptake. M ar Poll Bull 50( 11 ): 1386-1397 and hypertrophic phase sensu ( Viaroli and Christian Bianchi TS ( 1988 ) Feeding ecology of subsurface deposit-feeder Lei­ 2003) to dystrophic conditions; major reduction of toscoloplos fragilis Verrili. I. Mechanisms affecting particle availability on intertidal sandflat. J Exp M ar Biol Ecol 115:79-97 macrofaunal abundances and species richness to envi­ Bianchi TS, Dawson R, Sawangwong P (1988) The effects ofmacro- ronmental changes, with a negative impact on less tol­ benthic deeposit-feeding on the degradation of chloropigments erant species, such as R. philippinarum. in sandy sediments. J Exp M ar Biol Ecol 122:243-255 • Fate autumn, winter; shift in food resources (i.e., from Bourget E, Messier D (1983) Macrobenthic density, biomass, and fresh micro- and macroalgae to detrital material) and fauna of intertidal and subtidal sand in a Magdalen Islands la­ goon, Gulf of St. Lawrence. Can J Zool 61:2509—2518 major changes in macrofaunal assemblages (i.e., from Brazeiro A, Defeo O (1996) Macrofauna zonation in microtidal relatively large bivalves to small-sized polychaetes), sandy beaches: it is possible identify pattem in such variable with a progressive recolonisation of few opportunistic environments? Estuar Coast Shelf Sei 42:523-526 species (C. tentaculata, Polydora sp. and Capitella sp.); Brown AC, McLachlan A (1990) Ecology of sandy shores. Elsevier, A m sterdam fast sediment recovery enhanced by macrofauna Castel J, Labourg PJ, Escaravage V, Auby I, Garcia ME (1989) through borrowing and bioturbation. Influence of seagrass beds and oyster parks on the abundance and biomass patterns of meio- and macrobenthos in tidal flats. We conclude that a thorough, parallel evaluation of the Estuar Coast Shelf Sei 28:71-85 temporal changes of chemical characteristics of sedi­ Clarke KR ( 1993 ) Non-parametric multivariate analyses of changes ments, including chi a, pheopigments, TOC and AVS, in community structure. Aust J Ecol 18:117-143 should be taken into account in assessing the year-round Clarke KR, Waiwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation,2 nd edn. distribution, changes and species-environment relations PRIMER-E Ltd, Plymouth of intertidal macrofauna, particularly in eutrophic, estu­ Cognetti G (1982) Adaptive strategies of brackish water fauna in arine intertidal flats. pure and polluted water. M ar Pollut Bull 13:247-250 1196

Commito JA, Celano EA, Célico EU, Como S, Johnson CP (2005) Krager CD, Woodin SA (1993) Spatial persistence and sediment dis­ Mussels matter: postlarval dispersal dynamics altered by a spa­ turbance of an arenicolid polychaete. Limnol Oceanogr 38:509- tially complex ecosystem engineer. J Exp M ar Biol Ecol 316:133— 520 147 Lansó RJ (1991) Tolerance of low dissolved oxygen and hydrogen Crooks JA (1996) The population ecology of an exotic mussel, Mus­ sulfide by the polychaete Streblospio benedecti (Webster). J Exp culista senhousia, in a southern California bay. Estuaries 19:42- M ar Biol Ecol:153:165-178 50 Lopez GR, Levington JS (1987) Ecology of deposit-feeding animals Crooks JA (1998) Habitat alteration and community-level effects of in marine sediments. Quart Rev Biol 62:235-260 an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser Lorenzen CJ (1967) Determination of chlorophyll and pheo-pig- 162:137-152 ments: spectrophotometric equations. Limnol Oceanogr 12:343— Crooks JA (2001) Assessing invader roles within changing ecosys­ 346 tems: historical and experimental perspectives on an exotic mus­ Magni P (1998) A multidisciplinary study on the dynamics of bio- sel in an urbanized lagoon. Biol Invasions 3:23-36 philic elements (C, N, P, Si) in a tidal estuary of the Seto Inland D ’Avanzo C, Alber M, Valiela I (1991) Nitrogen assimilation from Sea, Japan: physico-chemical variability and macrozoobenthic amorphus detritus by two coastal consumers. Estuar Coast Shelf communities. PhD Thesis, The United Graduate School of Sei 33:203-209 Ehime University, Ehime Defeo O, McLachlan A (2005) Patterns, processes and regulatory Magni P, Montani S (1997) Development of benthic microalgal mechanisms in sandy beach macrofauna: a multi-scale analysis. assemblages on an intertidal flat in the Seto Inland Sea, Japan: M ar Ecol Prog Ser 295: 1-20 effects of environmental variability. La Mer 35:137-148 Dexter DM (1984) Temporal and spatial variability in the commu­ Magni P, Montani S (1998) Responses of intertidal and subtidal nity structure of the fauna of four sandy beaches in South-east­ communities of the macrobenthos to organic load and oxygen ern New South Wales. Aust J M ar Freshw Res 35:663-672 depletion in the Seto Inland, Japan. J Rech Océanogr 23:47-56 Dyer KR, Christie MC, Feates N, Fennessy MJ, Pejrup M, van der Magni P, Montani S (2000) Physical and chemical variability in the Lee W (2000) An investigation into processes influencing the lower intertidal zone of an estuary in the Seto Inland Sea, Japan: morphodynamics of an intertidal mudflat, the Dollard estuary, seasonal patterns of dissolved and particulate compounds. Hyd- the Netherlands: I. Hydrodynamics and suspended sediments. robiologia 432:9-23 Estuar Coast Shelf Sei 50:607-625 Magni P, Montani S (2005) Physical and chemical variability of tidal Everett RA (1994) Macroalgae in marine soft-sediment communi­ streams. In: Lehr JH, Keeley J, Lehr J, Kingery TB III (eds) W a­ ties: effects on benthic faunal assemblages. J Exp M ar Biol Ecol ter encyclopedia, vol 4. Wiley, Hoboken, pp 6-11 175:253-274 Magni P, Abe N, Montani S (2000a) Quantification of microphyto­ Fueller CM (1994) Effects of porewater hydrogen sulfide on the feed­ benthos biomass in intertidal sediments: layer-dependent varia­ ing activity of the subsurface deposit-feeding polychaete, Clyme­ tion of chlorophyll a content determined by spectrophotometric nella torquata, Leidy. J M ar Res 52:1101-1127 and HPLC methods. La Mer 38:57-63 Gillmor RB (1982) Assessment of intertidal growth and capacity Magni P, Montani S, Takada C, Tsutsumi H (2000b) Temporal scal­ adaptations in suspension-feeding bivalves. M ar Biol 68:277-286 ing and relevance of bivalve nutrient excretion on a tidal flat of Grant J (1981) Sediment transport and disturbance on an intertidal the Seto Inland Sea, Japan. M ar Ecol Prog Ser 198:139-155 sandflat: infaunal distribution and recolonization. Mar Ecol Magni P, Montani S, Tada K (2002) Semidiurnal dynamics of salin­ Prog Ser 6:249-255 ity, nutrients and suspended particulate matter in an estuary in Haynes D, Quinn GP (1995) Temporal and spatial variability in the Seto Inland Sea, Japan, during a spring tide cycle. J Oceanogr community structure of a sandy intertidal beach, Cape Paterson, 58:389-402 Victoria, Australia. M ar Freshw Res 46:931-942 Magni P, Micheletti S, Casu D, Floris A, Giordani G, Petrov A, De Hawkins AJS, Smith RFM , Bayne BL, Héral M (1996) Novel obser­ Falco G, Castelli A (2005) Relationships between chemical char­ vations underlying the fast growth of suspension-feeding shell­ acteristics of sediments and macrofaunal communities in the Ca­ fish in turbid environments: Mytilus edulis. M ar Ecol Prog Ser bras lagoon (Western Mediterranean, Italy). Hydrobiologia 131:179-190 550:105-119 Heip CHR, Goosen NH, Herman PMJ, Kromkamp J, Middelburg Mann KH (1986) The role of detritus at the land-sea boundary. In: JJ, Soetart K (1995) Production and consumption of biological Lasserre P, Martin JM (eds) Biogeochemical processes at the particles in temperate tidal estuaries. Oceanogr Mar Biol Ann land-sea boundary. Elsevier, Amsterdam, pp 123-139 Rev 33:1-149 McArdle BH, Blackwell RG (1989) Measurement of density vari­ Hewitt JE, Pridmore RD, Thrush SF, Cummings VJ (1997) Assess­ ability in the bivalve Chione stutchburyi using spatial correlation. ing the short-term stability of spatial patterns of macrobenthos M ar Ecol Prog Ser 52:245-252 in a dynamic estuarine system. Limnol Oceanogr 42:282-288 McArdle BH, Anderson MJ (2001) Fitting multivariate models to James RJ, Fairweather PG (1996) Spatial variation of intertidal community data: a comment on distance-based redundancy macrofauna on a sandy ocean beach in Australia. Estuar Coast analysis. Ecology 82:290-297 Shelf Sei 43:81-107 McLachlan A (1996) Physical factors in benthic ecology: effects of Jaramillo E, McLachlan A, Coetzee P (1993) Intertidal zonation changing sand particle size on beach fauna. Mar Ecol Prog Ser patterns of macroinfauna over a range of exposed sandy beaches 131:205-217 in south-central Chile. M ar Ecol Prog Ser 101:105-118 Meksumpun C, Merksumpun S (1999) Polychaete-sediment rela­ Jones AR, Watson-Russell CJ, Murray A (1986) Spatial patterns in tions in Rayong, Thailand. Environ Poll 105:447-456 the macrobenthic communities of the Hawkesbury estuary, New Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens South Wales. Aust J M ar Freshw Res 37:521-543 T, Heip CHR (2000) The fate of intertidal microphytobenthos Kanaya G, Nobata E, Toya T, Kikuchi E (2005) Effects of different carbon: an in situ 1 3 C-labeling study. Limnol Oceanogr 45:1224- feeding habits of three bivalve species on sediment characteris­ 1234 tics and benthic diatom abundance. M ar Ecol Prog Ser 299:67- Miller DC, Bock MJ, Turner EJ (1992) Deposit and suspension feed­ 78 ing in oscillatory flows and sediment fluxes. J M ar Res 50:489- Kasai A, Horie H, Sakamoto W (2004) Selection of food sources by 520 Ruditapes philippinarum and Mactra veneriformis (Bivalva: Mistri M (2004) Effect of Musculista senhousia mats on clam mortal­ Mollusca) determined from stable isotope analysis. Fish Sei ity and growth: much ado about nothing? Aquaculture 241:207- 70:11-20 218 Karrh RR, Miller DC (1996) Effect of flow and sediment transport Montani S, Magni P, Shimamoto M, Abe N, Okutani K (1998) The on feeding rate of the surface-deposit feeder Saccoglossus kowa­ effect of a tidal cycle on the dynamics of nutrients in a tidal estu­ levskii. M ar Ecol Prog Ser 130:125-143 ary in the Seto Inland Sea, Japan. J Oceanogr 54:65-76 1197

Montani S, Magni P, Abe N (2003) Seasonal and interannual patterns Takai N, Yorozu A, Tanimoto T, Hoshika A, Yoshihara K (2004) of intertidal microphytobenthos in combination with laboratory Transport pathways of microphytobenthos-originating organic and areal production estimates. M ar Ecol Prog Ser 249:79-91 carbon in the food web of an exposed hard bottom shore in the Morrisey DJ, Howitt L, Underwood AJ, Stark JS (1992) Spatial var­ Seto Inland Sea, Japan. M ar Ecol Prog Ser 284:97-108 iation in soft-sediment benthos. M ar Ecol Prog Ser 81:197-204 Tamaki A (1987) Comparison of resistivity to transport by wave ac­ Nicotri ME (1977) Grazing effects of four marine intertidal herbi­ tion in several polychaete species on an intertidal sand flat. Mar vores on the microflora. Ecology 58:1020-1032 Ecol Prog Ser 37:181-189 Norkko A, Bonsdorff E (1996a) Altered benthic prey-availability Tanaka M, Kikuchi T (1978) Ecological studies on benthic macro­ due to episodic oxygen deficiency caused by drifting algal mats. fauna in Tomoe Cove, Amakusa. II. Production of Musculista PSZN I: M ar Ecol 17:355-372 senhousia (Bivalvia, Mytilidae). Publ Amakusa Mar Biol Lab Norkko A, Bonsdorff E (1996b) Rapid zoobenthic community re­ Kyushu Univ 4:215-233 sponses to accumulations of drifting algae. M ar Ecol Prog Ser Thrush SF (1991) Spatial patterns in soft-bottom communities. Tree 131:143-157 6:75-70 Oeschger R, Vismann B (1994) Sulphide tolerance inHeteromastus Thrush SF, Hewitt JE, Pridmore RD (1989) Patterns in the spatial filiformis (Polychaeta): mitochondrial adaptations. Ophelia arrangements of polychaetes and bivalves in intertidal sandflats. 40:147-158 M ar Biol 102:529-535 Olafsson EB (1988) Inhibition of larval settlement to a soft bottom Tsutsumi H (1987) Population dynamics ofCapitella capitata (Poly­ benthic community by drifting algal mats: an experimental test. chaeta; Capitellidae) in an organically polluted cove. M ar Ecol M ar Biol 97:571-574 Prog Ser 36:139-149 Parsons TR, Maita M, Lalli CM (1984) A manual of chemical and Tsutsumi H, Kikuchi T (1983) Benthic ecology of a small cove with biological methods for seawater analysis. Pergamon, Oxford seasonal oxygen depletion caused by organic pollution. Publ Reise K (1979) Spatial configurations generated by motile benthic Amakusa Mar Biol Lab Kyushu Univ 7:17-40 polychaetes. Helg Meer 32:55-72 Uchida M, Numagughi K (1996) Formation of protoplasmatic Renshun Z (1992) Suspended sediment transport processes on tidal detritus with characteristics as food for secondary animals dur­ mud flat in Jiangsu Province, China. Estuar Coast Shelf Sei ing microbial decomposition of Ulva pertusa (Chlorophyta) 35:225-233 frond. J M ar Biotechnol 4:200-206 Ricciardi A, Bourget E (1998) Weight to weight conversion factors for Underwood AJ (1997) Experiments in ecology: their logical design marine benthic macroinvertebrates. M ar Ecol Prog Ser 163:245-251 and interpretation using analysis of variance. Cambridge Uni­ Ricciardi A, Bourget E (1999) Global patterns of macroinvertebrate versity Press, Cambridge biomass in marine intertidal communities. Mar Ecol Prog Ser Viaroli P, Christian RR (2003) Description of trophic status, hyper­ 185:21-35 autotrophy and dystrophy of a coastal lagoon through a poten­ Richardson CA, Ibarrola I, Ingham RJ (1993) Emergence pattern tial oxygen production and consumption index-TOSI: trophic and spatial distribution of the common cockle Cerastoderma ed­ Oxygen Status Index. Ecol Indie 3:237-250 ule. M ar Ecol Prog Ser 99:71-81 Winer BJ, Brown DR, Michels KM (1991) Statistical principles in Saiz-Salinas JI, Francés-Zubillaga G (1997) Enhanced growth in experimental design. 3rd edn. McGraw Hill, New York juvenile Nereis diversicolor after its exposure to anaerobic pol­ Whitlatch RB (1981) Animal-sediment relationship in intertidal ma­ luted sediments. M ar Poll Bull 34:437-442 rine benthic habitats: some determinants of deposit-feeding spe­ Sfriso A, Birkemeyer T, Ghetti PF (2001) Benthic macrofauna cies diversity. J Exp M ar Biol Ecol 53:31-45 changes in areas of Venice lagoon populated by seagrasses or Yin K, Harrison PJ, Pond S, Beamish RJ (1995) Entrainment of ni­ seaweeds. M ar Environ Res 52:323-349 trate in the Fraser river estuary and its biological implications. II. Smith D, Hughes RG, Cox EJ (1996) Predation of epipelic diatoms Effects of spring vs. neap tide and river discharge. Estuar Coast by the amphipod Corophium volutator and the polychete Nereis Shelf Sei 40:529-544 diversicolor. M ar Ecol Prog Ser 145:53-61 Ysebaert T, Herman PMJ (2002) Spatial and temporal variation in Sokal RR, Rohlf FJ (1995) Biometry. Freeman & Company, New benthic macrofauna and relationships with environmental vari­ Y ork ables in an estuarine, intertidal soft-sediment environment. Mar Tagliapietra D, Pavan M, Wagner C (1998) Macrobenthic commu­ Ecol Prog Ser 244:105-124 nity changes related to eutrophication in Palude della Rosa Yokoyama H (1998) Three polychaetes indicating different stages of (Venetian lagoon, Italy). Estuar Coast Shelf Sei 47:217-226 organic pollution. J Rech Océanogr 23:67-74 Takai N, Mishima Y, Yorozu A, Hoshika A (2002) Carbon sources Y okoyama H (2002) Impact of fish and pearl farming on the benthic for demersal fish in the western Seto Inland Sea, Japan, examined environment in Gokasho bay: evaluation from seasonal fluctua­ by 8 13C an d 8 15N analyses. Limnol Oceanogr 47:730-741 tions of the macrobenthos. Fish Sei 68:258-268