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 Weld surveys were conducted in an estu- sation of macrofauna, initiated by few opportunistic arine intertidal sandXat 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 Wrst evidence of signiWcant 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 Xat were used as a com- in an estuarine intertidal Xat 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 Xats. (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 Wlter-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 aVecting macrofaunal distribution Communicated by R. Cattaneo-Vietti, Genova (Dexter 1984; Allen and Moore 1987; Jaramillo et al. 1993; Brazeiro and Defeo 1996; James and Fairweather P. Magni (&) · S. Como IMC – International Marine Centre, Località Sa Mardini, 1996; McLachlan 1996; Defeo and McLachlan 2005). In Torregrande, 09072 Oristano, Italy tidally dominated estuarine Xats, 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. Montani Graduate School of Environmental Science, ment morphodynamics (Grant 1981; Renshun 1992; Hokkaido University, Kita 13 Nishi 8, Dyer et al. 2000; Magni and Montani 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 eVect 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-speciWc 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; Montani et al. 2003), water chemistry 1991; Morrisey et al. 1992; Crooks 1998) and may (Montani et al. 1998; Magni and Montani 2000), and remain relatively stable in terms of their spatial distribu- benthic macrofauna (Magni and Montani 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 inXuence of environmental variables (e.g., Montani 1998). Duration of sediment emersion varies mud content, chlorophyll a (chl 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- Montani 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- niWcantly with the environmental variables that are Field sampling inXuenced 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 Xats, re-suspension and deposition of organic 50£100 m and were repeated on Wve diVerent 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 Xuctuating throughout the and 20 January (winter, W) 1994, and 15 April 1995 year (Heip et al. 1995; Magni and Montani 2000; (spring 95, Sp95). At each sampling station, emerged Montani 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 Weld studies are available in this regard (Castel et al. were carefully sliced oV the sediment. Sediment samples 1989), especially on a year-round basis in estuarine from the same layer were pooled together and brought intertidal sandXats. 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; Montani et al. 1998; Magni and Montani 2000). In mesh size of 1 mm. The residue of each replicate was the present work, we investigated the year-round distri- separately Wxed in a 10% buVered 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 Xat was assemblages in the lower part of the sandXat. 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 chl 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), NH4-N, chl 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 sandXat on water sample treatment and analysis to our compan- occurring on a year-round basis at a small spatial scale ion paper (Magni and Montani 2000). (i.e., tens of meters). Sediment sample treatment and analysis
In the laboratory, chl 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 sandXat of the for 10 min, and extracts were spectrophotometrically Seto Inland Sea, southwestern Japan (Fig. 1). The Xat is analysed (Jasco, Uvidec¡320). Chl a and pheopigment located in a mixed-semidiurnal type estuary (mean tidal values were obtained before and after acidiWcation with range of about 2 m) where we have previously conducted 1 N HCl, respectively, according to Lorenzen’s (1967) 1187
2000). From the same pool of fresh sediments, the AVS concentrations, as a measure of reducing conditions of sediments, were determined simultaneously in duplicate subsamples (about 1 g) using a H2S-absorbent column (GASTEC, Kanagawa, Japan). Phyto-pigment and AVS values were expressed as gg¡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 acidiWcation with 2 N HCl and neu- tralization with NaOH, using a CHN analyser (Yanako). Macrofauna was sorted, identiWed to the species level, when possible, counted under a stereo-microscope (Olympus, Wild M3Z) and preserved in 75% ethanol and 2.5% ethylene-glycol. All individuals of a species in a given core were grouped for biomass measurements. The wet weights (WW) of polychaetes and minor and/or uncommon taxa were obtained from each sample after carefully blotting oV any excess Xuid. 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 diVerent 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=0.320£TW ¡0.002 (r2=0.885, P<0.001) for M. senhousia and WW=0.167£TW+0.025 (r2=0.886, P<0.001) for R. phil- ippinarum.
Statistical analysis
Temporal changes in the chemical characteristics of sedi- ments (i.e., chl a, pheopigments, pheopigments to chl a ratio, TOC and AVS) were analysed using one-factor model ANOVA (Underwood, 1997). Factor “dates” (D; 5 levels) was Wxed and there were 15 replicates for each date. DiVerences 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 sandXat of the Seto Inland Sea, southwestern Japan. On the Xat, 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 diVerences among dates (Clarke 1993). Changes in total abundance (N), total number of species (S), Shannon–Weiner diversity (HЈ), and total biomass, and abundance and biomass of the taxa identi- method, as described by Parsons et al. (1984), where the Wed 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 Wxed and of the sediment expressed in grams. Acetone-extract- there were 15 replicates for each date. When signiWcant able chl a estimates, obtained after correction for deg- diVerences 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(x+1) ments which gave similar chl 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 36 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 (psu) Salinity ¡1 was an opposite trend of DO (range 3.2–12.6 mg l ) and 18 18 + NH4-N (range 11.7–89.4 M) concentrations, with a major + (˚C)Temperature increase of NH4-N in October, in coincidence with the low- est DO values. Subsequently, DO increased throughout + 0 0 winter and spring, while NH4-N peaked in winter and sharply decreased in the next spring. With regard to the ) 18 100 temporal distribution of particulate compounds, two -1 major peaks occurred in August and October (Fig. 2). They most noticeably diVered from each other in that chl NH 4 DO (mg l
9 50 + a concentration was highest in August, while pheopig- (µM) -N ments, POC and TSM were highest in October. Consistent with this trend, chl a was poorly correlated with pheopig- ments and POC, and not signiWcantly correlated with 0 0 TSM, while pheopigments, POC and TSM were strongly correlated with each others (Table 1). In addition, salinity ) 90 120 was not signiWcantly correlated with chl a, while it was -1 ho (µg l Pheop correlated positively with DO and negatively with NH +-N, (µg l 4 a pheopigments, POC and TSM (Table 1). 45 60 Chl
Sediment characteristics -1 ) 0 0 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) -1 (Magni et al. 2000). There were also strong changes in the S m l (mg TSM chemical characteristics of sediments among dates (Fig. 3, 280 Table 2). Chl a ranged from 2.9§0.4 (subsurface, A) to 10 ¡1 W l POC (mg 8.7§0.5 gg (surface, Sp95) and was signi cantly lower -1 in the autumn date (A) than in all other sampling dates in ) both surface and subsurface layers. Pheopigments showed 0 0 a diVerent trend from that of chl a. At the surface pheopig- A MJ JAS ONJFMAD ments were higher in the summer date (Su, 22.5§1.7 94 95 ¡1 gg ) than in all other sampling dates (minimum of Fig. 2 Temporal variations (mean § SE) of hydrological variables 8.2§0.7 gg¡1 in W), while at the subsurface they tended in low-tide water of a creek located near the emerged tidal Xat (see Fig. 1). From top to bottom: temperature and salinity, dissolved oxy- to increase progressively from the spring (Sp94) to the + gen (DO) and ammonium (NH4-N), chlorophyll a (Chl a) and pheo- autumn (A) dates. Consistent with these temporal pigments (pheop), and particulate organic carbon (POC) and total changes, the pheopigments to chl a ratio showed an oppo- suspended matter (TSM). Interrupted lines: data not available be- site trend to that of chl a, being highest in the autumn date tween 2 months
Table 1 Correlation coeYcient R among hydrological variables
Temp Sal DO Chl a Pheop POC
DO 0.68** (n=19) + NH4-N ¡0.62** (n=23) ¡0.52** (n=27) ¡0.56** (n=21) Pheop ¡0.62** (n=26)0.42* (n=35) POC ¡0.61** (n=27)0.40* (n=35) 0.99*** (n=35) TSM ¡0.52** (n=27) 0.95*** (n=35) 0.96*** (n=36) Only statistically signiWcant correlations are indicated: *P<0.05, **P<0.01, ***P<0.001; in bold: negative correlations DO dissolved oxygen, Chl a chlorophyll a, Pheop pheopigments, POC particulate organic carbon, TSM total suspended matter, n number of 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 signiWcantly 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), although the biomass, respectively. SNK test failed to discriminate alternative hypothesis Macrofaunal assemblages were diVerent in the Wve (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 (HЈ) and total biomass, are reported in most abundant (i.e., 75% of the total abundances of Table 4. S, N and HЈ 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 Wve taxa, respectively, contributed most for the diVerences among dates in terms of abundances and biomass (SIMPER analysis, cut-oV 70%; see Table 5 Surface (0-0.5 cm) Subsurface (0.5-2 cm) for the reference list). The analyses of variance and the
) 10
-1 post hoc comparisons indicated that the abundances of Cirriphormia tentaculata decreased in the summer date
(µg g 5 (Table 5; Fig. 5), and those of R. philippinarum, Gam- a maridae sp. and Polydora sp. decreased in the autumn
Chl 0 date (Table 5), although it was not possible to identify )
-1 30 this pattern with the SNK test for Polydora sp. (Table 5). As an example, R. philippinarum is illustrated in Fig. 5. 15 Gammaridae sp. was also less abundant in the spring 1994 date (Sp94). On the contrary, the abundances of
Pheop (µg g 0
a 8
4 Table 2 Analyses of variance for chlorophyll a (Chl a) concentra- tions in the surface layer (0–0.5 cm) of sediments for diVerences Pheop/Chl 0 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 -1 Source df MS FP SNK test 0.3 Chl a
AVS (mg g AVS (mg 0.0 Date 4 2.04 18.87 0.0000 A ) 16 MS F4,70 P SNK test -1 Other sediment variables 8 Surface (0–0.5 cm): Pheop 498.33 19.47 0.0000 Su>Sp94=A=W=Sp95 Pheop/Chl a 2.35 30.43 0.0000 A>Su>Sp94=W=Sp95 TOC (mg g 0 Sp AVS 0.09 34.95 0.0000 A>Sp94=Su=W=Sp95 94 Su AWSp95 TOC 0.85 4.05 0.0052 NAH Subsurface (0.5–2 cm) Fig. 3 Mean concentrations (n=15 § SE) of sediment variables in Chl a 0.48 4.81 0.0018 A Table 3 PERMANOVA on Bray–Curtis dissimilarities for diVerences of macrofaunal assemblages among dates in terms of abundances and biomasses Source df MS FP Within dates Among dates Abundances Date 4 5,386.57 4.50 0.001 Sp94 41.35 Sp94 vs. Su 43.74 Residual 70 1,197.59 Su 38.70 Sp94 vs. A 58.22 Total 74 A 60.85 Sp94 vs. W 49.53 W 44.11 Sp94 vs. Sp95 45.27 Sp95 37.60 Su vs. A 60.19 Su vs. W 48.40 Su vs. Sp95 44.05 A vs. W 56.43 A vs. Sp95 58.17 W vs. Sp95 45.77 df MS FP Within dates Among dates Biomasses Date 4 4,497.10 2.92 0.001 Sp94 35.11 Sp94 vs. Su 48.04 Residual 70 1,542.04 Su 39.84 Sp94 vs. A 59.61 Total 74 A 64.25 Sp94 vs. W 49.77 W 55.71 Sp94 vs. Sp95 45.96 Sp95 49.70 Su vs. A 57.42 Su vs. W 52.41 Su vs. Sp95 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 Warwick 2001) Sp94 spring 1994, Su summer, A autumn, W winter, Sp95 spring 1995 Fig. 4 Mean (n=15§SE) abun- 140 16 dances (ind. 100 cm¡2, N), num- ber of species (S), Shannon– Wiener diversity (HЈ) and total 70 8 S biomass (g WW 100 cm¡2) in N each sampling date. Sp94 spring 1994, Su summer, A autumn, W 0 0 winter, Sp95 spring 1995 2 6 1 H' 3 Biomass 0 0 Sp Sp 94 Su A W Sp95 94 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 signiWcant diVerences 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., Wlter-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 signiWcant 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, chl a, pheopigments and TOC in surface 1191 Table 4 Analyses of variance for the total abundance (N) for diVerences among dates, and SNK test. Summary of analyses of variance and SNK test for the total number of species (S), Shannon–Wiener diversity (HЈ), and total biomass Source df MS FP SNK test Total abundance (N) Date 4 28.50 3.01 0.0238 NAH Residual 70 9.47 Total 74 MS F4,70 P SNK test Total no. of species S 75.25 7.72 0.0000 NAH HЈ 0.76 5.72 0.0005 NAH Total biomass 0.67 1.42 0.2358 NS NAH no alternative hypothesis, NS no signiWcant eVects § -2 Fig. 5 Mean (n=15 SE) abun- Abundances (ind. 100 cm-2) Biomass (gWW 100 cm ) dances (left side) and biomass 16 0.6 (right side) of Cirriformia tentac- ulata, Ruditapes philippinarum, Musculista senhousia and Poly- 8 0.3 dora sp. Sp94 spring 1994, Su summer, A autumn, W winter, Sp95 spring 1995 C. tentaculata 0 0.0 40 3.0 20 1.5 R. philippinarum 0 0.0 20 3.0 10 1.5 M. senhousia 0 0.0 50 0.4 sp. 25 0.2 Polydora 0 0.0 Sp94 Su A W Sp Sp 95 94 Su A W Sp95 and/or subsurface sediments were all positively corre- 8 and 13 vs. 10, respectively). By contrast, among chem- lated with the total abundance (N), total number of ical variables of sediments, subsurface AVS alone gave species (S), Shannon–Wiener diversity (HЈ) and the all negative correlations with macrofaunal univariate total biomass (Table 6). The abundances and/or bio- measures, including N, S, HЈ, 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. tentaculata and Polydora sp. (Table 6). strongly M. senhousia with pheopigments and TOC. Finally, temperature of emerged sediments was corre- Among individual variables, subsurface chl a had the lated positively with S, HЈ, total biomass, the abun- highest number of highly signiWcant (P<0.001) correla- dances and biomass of R. philippinarum, and the tions with macrofauna. As to both chl 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 of variance for the abundance of Cirriphormia tentaculata for diVerences among dates, and SNK test and summary of analyses of variance and SNK test for the taxa contributing most for the diVerences among dates in terms of abundances and biomass (SIMPER, cut-oV 70%) Source df MS FP SNK test C. tentaculata Date 4 4.14 5.58 0.0006 Su Biomass M. senhousia 1.50 3.99 0.0056 NAH R. philippinarum 1.15 7.88 0.0000 Su>Sp94=A=W=Sp9 C. tentaculata 0.18 7.31 0.0001 Su=A Table 6 Correlation coeYcient R between sediment variables and dominant macrofaunal taxa Temp Chl a surf Chl a subsurf Pheop surf Pheop subsurf TOC surf AVS surf AVS subsurf N 0.31** 0.49*** 0.25* 0.32** 0.31** ¡0.41*** S 0.23* 0.45*** 0.41*** 0.35** 0.23* 0.32** ¡0.40*** HЈ 0.23* 0.36** 0.25* 0.28* 0.27* ¡0.32** Tot-bio 0.25* 0.31** 0.51*** 0.43*** 0.52*** Abundances M. senhousia 0.29* 0.48*** 0.34** 0.47*** 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** ¡0.24* A. oxycephala 0.27* 0.26* 0.31** ¡0.23* Polydora sp. 0.28* 0.46*** 0.25* ¡0.32** Spionidae sp. 0.43*** 0.31** Gammaridae sp. 0.23* 0.26* 0.38** 0.26* 0.24* 0.26* ¡0.24* Dimorphostylis sp. 0.25* ¡0.26* C. muromiensis 0.31** Biomass M. senhousia 0.52*** 0.45*** 0.55*** 0.25* R. philippinarum 0.48*** 0.27* 0.34** C. tentaculata ¡0.28*0.31** ¡0.32** C. erithraeensis 0.41*** 0.48*** 0.31** Polydora sp. 0.24* 0.41*** 0.25* ¡0.29* Only statistically signiWcant correlations are indicated: *P<0.05, **P<0.01, ***P<0.001; in bold: negative correlations; n=75) N total abundance, S total number of species, HЈ Shannon–Wiener index, Tot-bio total biomass, Temp surface sediment temperature, Chl a chlorophyll a, Pheop pheopigments, TOC total organic carbon, AVS acid-volatile sulphide, surf 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 Xat 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 Wlter zone has been emphasized recently (Ysebaert and Her- feeders such as R. philippinarum (Kasai et al. 2004; man 2002). This study provides the Wrst evidence of sig- Kanaya et al. 2005). Recent Weld experiments in Ulva- niWcant 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 signiWcant amounts of TOC and AVS, and macrofaunal assemblages in an estu- macroalgae provided that there are no hypoxic condi- arine intertidal Xat at a small spatial scale (i.e., tens of tions and depending on the seasonal cycles of Ulva itself meters). This demonstrates the high Xexibility 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., Mann 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 eVects of algal favoured the development of conspicuous algal assem- cover on the structure of an intertidal benthic assem- blages (Magni and Montani 1998; Montani et al. 2003). blage. He concluded that increased abundance of small High chl 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 chl 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 warm 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 aVect 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 Xat 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§0.35 g WW 100 cm¡2), 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 chl 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 42.5g AFDWm¡2 (or living and detrital algal materials are important food 311 g WW m¡2), up to a maximum of 60.6 g AFDW 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 chl 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 chl 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 diVerences 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 chl 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 chl 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 Wnd diVerences in the rological conditions, including a drastic reduction of mortality of R. philippinarum at diVerent 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 eVects 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 eVect of macroalgal inarum, the polychaete Cirriphormia tentaculata strongly exudates (Norkko and BonsdorV 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 eVect of sulphide on various benthic et al. 1998). The presence of mats of M. senhousia was animals has been extensively investigated in laboratory thus likely to drive the recruitment after the dystrophic experiments (Lansó 1991; Fueller 1994; Oeschger and event. SpeciWcally, M. senhousia may have facilitated Vismann 1994; Saiz-Salinas and Francés-Zubillaga 1997) opportunistic species and inhibited others by entrapping there are relatively few Weld 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 Xats (Meksumpun and Merksumpun winter with a progressive increase of small-sized, deposit- 1999). This study clearly shows how a signiWcant 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 mark- 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 signiWcantly 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 Wlter-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 Weld 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 beneWcial eVect of bur- (Grant-in-Aid of ScientiWc Research). 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