spatial changes in a macrozoobenthic community along environmental gradients in a shallow brackish...

Available online at www.sciencedirect.com

Estuarine, Coastal and Shelf Science 78 (2008) 674e684www.elsevier.com/locate/ecss

Spatial changes in a macrozoobenthic community along environmentalgradients in a shallow brackish lagoon facing Sendai Bay, Japan

Gen Kanaya*, Eisuke Kikuchi

The Center for Northeast Asian Studies, Tohoku University, Kawauchi, Aoba-ku, Sendai 980-8576, Japan

Received 16 January 2008; accepted 18 February 2008

Available online 23 February 2008

Abstract

The spatial distribution, abundance, and assemblage structure of macrozoobenthos were examined at 45 stations in a brackish lagoon (IdouraLagoon, Japan) to examine the animaleenvironmental relations in estuarine soft-bottom habitats. We found a total of 23 taxa; the polychaetesHeteromastus sp., Hediste spp., and Prionospio japonica and the isopod Cyathura muromiensis numerically dominated the community. Clusteranalysis and one-way analysis of similarity (ANOSIM) identified seven groups of stations that had significantly different macrozoobenthic com-munities; these were subsequently consolidated into five habitat groups according to their association with environmental characteristics.Canonical correspondence analysis (CCA) showed that salinity, silt-clay content, and the oxidationereduction potential (ORP) of the sedimentstrongly affected the macrozoobenthos distribution pattern in the lagoon, whereas other factors (e.g., relative elevation of the habitat and sed-iment organic content) had much weaker effects. Similarity percentages (SIMPER) procedures indicated that the polychaete Notomastus sp. andthe bivalve Macoma contabulata were specific to habitats with low salinity and reduced mud, whereas the bivalve Nuttallia olivacea was specificto sandy bottoms. Heteromastus sp. and Hediste spp. achieved their highest densities in rather oxidized sediments. The acid-volatile sulfide(AVS) content in the sediment was suggested as another possible factor affecting macrozoobenthic density. Our results clearly demonstratethat macrozoobenthic assemblages in estuarine soft-bottoms have high spatial heterogeneity on a small scale (e.g., hundreds of meters) relatedto physical and chemical environmental changes. Our data also suggested the importance of sediment redox condition (e.g., ORP and AVScontent) and sediment grain size as structuring factors in estuarine soft-bottom communities as well as the salinity in the habitat.� 2008 Elsevier Ltd. All rights reserved.

Keywords: zoobenthos; community composition; salinity gradients; sediment properties; multivariate analysis; brackish lagoon

Regional index terms: Japan; Honshu Island; Sendai Bay; Idoura Lagoon

1. Introduction

Estuaries provide diverse habitats with different physicaland chemical characteristics within a relatively small scale(e.g., hundreds to thousands of meters). Macrozoobenthos arean important component of estuarine soft-bottom ecosystemsand play an important role in system dynamics (Heip et al.,1995). Most of the species comprising the macrozoobenthosare primary consumers that incorporate organic matter from

* Corresponding author.

E-mail addresses: [email protected] (G. Kanaya), ekikuchi@cneas.

tohoku.ac.jp (E. Kikuchi).

0272-7714/$ - see front matter � 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2008.02.005

different sources into the system (e.g., Doi et al., 2005; Kanget al., 2007; Kanaya et al., in press) and may act as intermediateprey for predatory animals such as large crustaceans, fish, andbirds.

Estuarine ecosystems are, in general, characterized bywidely fluctuating and often unpredictable hydrological andchemical conditions, both at temporal and spatial scales (e.g.,Yamamuro et al., 1990; Ysebaert and Herman, 2002; Kanayaand Kikuchi, 2004; Kang et al., 2007), because they are transi-tional environments between riverineeterrestrial and marineecosystems. In particular, high fluctuation in salinity is oftena lethal factor for marine and freshwater organisms that cannotcope with changes in environmental salinity (e.g., Sanders

mailto:[email protected]



http://www.elsevier.com/locate/ecss

Fig. 1. Locations of the 45 sampling stations in Idoura Lagoon. White and

black circles represent intertidal and subtidal stations, respectively. The white

arrow indicates freshwater discharge from Idoura River during ebb tides. The

black arrow indicates seawater inflow during high tides. The þ indicates la-

goon mouth used as the zero point for the distance measure.

675G. Kanaya, E. Kikuchi / Estuarine, Coastal and Shelf Science 78 (2008) 674e684

et al., 1965; Yamamuro, 1996; Pechenik et al., 2000; Teske andWooldridge, 2003). Thus, estuaries are considered to be areas oflow diversity with high abundances of few estuarine organismscompared to marine systems (e.g., Sanders et al., 1965; Dayet al., 1989; Atrill et al., 1996).

Estuarine macrozoobenthos is commonly thought to bedistributed along gradients of several physiological stresses(e.g., salinity) according to their environmental tolerances(Sanders et al., 1965; Yamamuro et al., 1990; Gamenicket al., 1996; Teske and Wooldridge, 2003). Accordingly,they are often restricted to particular habitat types, resultingin a well-developed distribution pattern of assemblage struc-tures (e.g., Yamamuro et al., 1990; Bachelet et al., 1996; Yse-baert and Herman, 2002; Ysebaert et al., 2003; Nanami et al.,2005). For example, sediment characteristics (e.g., sedimentgrain size), as well as salinity, have long been reported as sig-nificant factors affecting the spatial distributions of estuarinemacrozoobenthos (e.g., Sanders, 1958; Sanders et al., 1965;Bachelet et al., 1996; Teske and Wooldridge, 2003; Ysebaertet al., 2003; Nanami et al., 2005). Teske and Wooldridge(2003) examined the spatial distribution pattern of macrozoo-benthos in 13 estuaries along the coast of South Africaand found that the distribution of estuarine endemic faunawas primarily altered by the nature of the substratum, whereasthe distributions of marine and oligohaline fauna were re-stricted mainly by salinity. Several studies had also offeredthat sulfide accumulation in reduced sediment sometimesacts as a lethal factor for benthic invertebrates in eutrophi-cated brackish waters (e.g., Gamenick et al., 1996). Neverthe-less, the effects of sediment redox conditions for themacrozoobenthic community structure are rarely mentionedin studies of soft-bottom habitats in brackish waters (Yama-muro et al., 1990; Ysebaert and Herman, 2002; Teske andWooldridge, 2003; Nanami et al., 2005; but see Gamenicket al., 1996).

In the present study, a shallow (water depth< 2.5 m) andsmall (1.8 km in the longest length) brackish lagoon, IdouraLagoon, Japan, was selected to examine the animaleenviron-ment relations in estuarine soft-bottom habitats affected byriver effluents. The lagoon receives freshwater effluents atthe inner lagoon during low tides, resulting in highly fluctuat-ing salinity on spatial and temporal scales (Miyagi Prefecture,1988; Kikuchi and Hata, 1999; Kanaya and Kikuchi, 2004;Kanaya et al., in press). Muddy tidal flats appear at both sidesof a narrow tidal channel, and the macrozoobenthic commu-nity is dominated by a few polychaete species (Kikuchi andHata, 1999) that are commonly found in brackish waters of Ja-pan (Yamamuro et al., 1990; Yamamuro, 1996; Nanami et al.,2005). Our aim was to determine the assemblage structure andthe spatial distribution of macrobenthic invertebrates at 45 sta-tions in the Idoura Lagoon along the environmental gradients.In the present study, the relative importance of physical andchemical environmental parameters (e.g., salinity, sedimentcharacteristics, and relative elevation) was tested using multi-and univariate analyses. Especial attention was paid to the sed-iment redox conditions including ORP and sulfide content ineach habitat.

2. Materials and methods

2.1. Study site

A series of surveys were conducted in the shallow brackishIdoura Lagoon (38�120 N, 140�560 E; 0.40 km2 in area), whichlies on the north side of the Natori River mouth, facing SendaiBay, Japan (Fig. 1). The lagoon opens to the Natori River Es-tuary at the southern end and is connected to the Teizan Canalat the northern part (i.e., inner lagoon). It receives seawater viathe lagoon mouth during high tides and freshwater effluentsfrom the Idoura River via the Teizan Canal during ebb tides.

676 G. Kanaya, E. Kikuchi / Estuarine, Coastal and Shelf Science 78 (2008) 674e684

The tidal cycle is synchronized to those in the adjacent sea,with a range of approximately 1.5 m at spring tides (Kanayaand Kikuchi, 2004). The lagoon primarily lacks stagnant waterbodies and is characterized by a high tidal water exchange rate(Kanaya and Kikuchi, 2004; Kanaya et al., in press). Kanayaand Kikuchi (2004) estimated that >90% of the lagoon wateris replaced by adjacent waters in each tidal cycle during springtides.

During low tides, river water flows down the lagoon, andmuddy unvegetated tidal flats (0.26 km2) appear on both sidesof the watercourse (Fig. 1). The salinity in the lagoon fluctu-ates from nearly 0 to >30 in relation to the tidal movementand/or river discharge (Miyagi Prefecture, 1988; Kikuchiand Hata, 1999; Kanaya and Kikuchi, 2004). There is a salinitygradient from the lagoon mouth (higher salinity) to the north-ern end (lower salinity), although the salinity in each areashows wide temporal fluctuations (Miyagi Prefecture, 1988;Kanaya et al., in press). We selected 45 stations (Fig. 1) forthe collection of macrozoobenthic and sediment samples.The stations were chosen to cover the entire area of the lagoonalong environmental gradients of relative elevation, salinity,and sediment characteristics.

2.2. Analyses of environmental parameters

At each station, environmental variables, including oxida-tionereduction potential (ORP), relative elevation, silt-claycontent (particles <0.063-mm mesh), total organic carbon(TOC), total nitrogen (TN), acid-volatile sulfides (AVS, mostlyFeS), and sediment C/N ratio were determined.

In the field, sediment ORP was measured using a hand-heldEh meter (RM-12P, TOA, Japan) at 5 cm below the surfaceon 3 or 7 September 1998. The electrode was inserted intocored sediment (PVC core, 5 cm inner diameter). On thesame occasion, relative elevation was determined by measur-ing the water depth during high tides and was represented asa difference (cm) from the mean seawater level at TokyoBay (Tokyo Peil; T.P.).

For sediment chemical analyses, a core was taken at eachstation using a PVC corer (5 cm inner diameter, 30 cm long).When the station was submerged (water depth >1.0 m), a sam-ple was collected from an inflatable boat with the corer attachedto a steel pipe (2 m long). After the samples were brought to thelaboratory, a surface (0e1 cm deep) and a subsurface (1e3 cmdeep) layer of the core were taken, dried at 60 �C for 48 h, andused to determine the TOC and TN contents (0e1 cm layer),and silt-clay content (1e3 cm layer). TOC and TN were deter-mined using an elemental analyzer (NC-2500, CE Instruments,Italy) after samples were acidified with 1 M HCl to removecarbonates. Silt-clay content was determined by wet sieving(0.063-mm mesh sieve).

In marine and estuarine soft-bottoms, the sulfide content(e.g., AVS) is closely related to the redox condition (ORP) be-cause it is primarily formed by sulfate-reducing bacteria underhighly reduced conditions in which anaerobic metabolism pre-vails (Capone and Kiene, 1988). For the AVS content, a 10-mlaliquot was taken from a 4e5 cm depth layer of the cored

sediment using a small syringe-corer (2.8 cm inner diameter).At first, free H2S was extracted from the sediment in a glassvial containing N2-saturated deionized water (for detailedmethods, see Kanaya and Kikuchi, 2004), however, free H2Swas not detected at most stations (see below). After acidifyingthe samples with 0.5 M H2SO4, AVS was liberated as hydro-gen sulfide (H2S) and purged with pure N2 gas into 2.5%zinc acetate solution. The sulfide content in the solution wasdetermined by iodometry (Suzuki and Shiga, 1953). Of the45 stations, free H2S was only detected at St. 43, and the con-tent (0.82 mmol g�1) represented only a small fraction (0.8%)of the AVS pool at the station (97.0 mmol g�1). Thus, the mea-sured AVS consisted primarily of insoluble sulfides (i.e., FeS).

All sediment parameters were measured within the top 5 cmlayer of the sediment. The depth was chosen since most of thedominant species in this lagoon (e.g., Hediste spp., Prionospiojaponica, Notomastus sp., Cyathura muromiensis, and Macomacontabulata) inhabit mainly top 10 cm depth layer of the sedi-ment (66e99% of total individuals, G. Kanaya, unpublisheddata). Contrastingly, the most dominant polychaete Heteromas-tus sp. is mainly collected from the deeper sediment layer (64%of total occurred at a 10e30 cm depth, G. Kanaya, unpublisheddata). This probably underestimated the effects of sediment re-dox condition on the deep-burrowing species since sedimentbecomes more reduced and sulfide-rich in the deeper sedimentlayer that the worm inhabited (Kanaya and Kikuchi, 2004).

Salinity in Idoura Lagoon is primarily determined by themixing of two water bodies, freshwater from the Idoura Riverat the inner lagoon (salinity; nearly 0) and seawater inflow viathe lagoon mouth during high tides (salinity> 25) (MiyagiPrefecture, 1988; Kanaya and Kikuchi, 2004; Kanaya et al.,in press). As a result, salinity fluctuates widely in relation tothe tidal movements (nearly 0 to over 25, Miyagi Prefecture,1988; Kanaya and Kikuchi, 2004; Kanaya et al., in press). Pre-vious data also showed that a longitudinal saline gradient isformed in the lagoon, i.e., salinity is lower in the inner portioncompared to the area in the vicinity of the lagoon mouth(Miyagi Prefecture, 1988). In the present study, we failed tomeasure the salinity prior to the macrofaunal sampling mainlydue to the temporal fluctuation of salinity in each station.Accordingly, we used the distance from the lagoon mouth tothe stations as an alternative indicator of salinity though themethod provides only rough estimation. The distance fromthe lagoon mouth (km) was calculated using a caliper aftereach station was plotted onto a map of the lagoon. Larger‘‘distance’’ values indicate that the station is closer to theIdoura River and is more affected by freshwater discharge.

2.3. Macrozoobenthos

Quantitative sampling of the macrozoobenthos was con-ducted on October 7e9, 1998, at the 45 stations. At each station,nine sediment cores (176.7 cm2) from the surface to a depth of30 cm were collected using a PVC core (5 cm inner diameter,80 cm long). At stations with high water depth (>1.0 m atlow tides), samples were taken from a boat as described above.The sediments were sieved in situ through a 1-mm mesh sieve,

Table 1

Macrobenthic invertebrate species found in Idoura Lagoon. The mean (�SD,

n¼ 45) and maximum density (ind. m�2) of each taxon are shown. Proportion

(Prop., %) is the relative density of each species compared to the total macro-

zoobenthic density in the lagoon (i.e., 1509 ind. m�2). Occurrence (Occur.) is

the number of stations at which the species were collected. Species collected

from more than three stations (italicized) were used for the cluster, ANOSIM,

SIMPER, and canonical correspondence analyses


and the retained fraction was fixed in 5% neutralized formalineseawater solution. In the laboratory, animals in the sampleswere sorted, transferred into 70% ethanol, and identified to spe-cies or a higher taxon under a dissecting microscope. The datawere represented as density per square meter (ind. m�2). Nomacrozoobenthos was found at Sts. 43 and 45, which were lo-cated in a small inlet at the innermost lagoon.

Taxa Density (ind. m�2) Prop.

(%)

Occur.

Mean� 1 SD Maximum
2.4. Data analyses
Platyhelminthes

Turbellaria sp. 3� 12 56 0.2 2

Nemertea

Nemertinea sp. 8� 23 113 0.5 5

Polychaeta

Hediste spp. 282� 412 1582 19 36

Tylorrhynchus heterochaetus 5� 27 170 0.3 2

Pseudopolydora kempi japonica 8� 23 113 0.5 5

Prionospio japonica 49� 73 396 3 22

Sigambra tentaculata 1� 8 57 0.1 1

Heteromastus sp. 928� 1063 4633 61 41Notomastus sp. 29� 72 339 2 10

Capitella sp. 4� 14 57 0.2 3

Sabellidae sp. 9� 21 56 0.5 7

Bivalva

Nuttallia olivacea 45� 113 508 3 10

Macoma contabulata 21� 37 113 1 13

Ruditapes philippinarum 1� 8 57 0.1 1

Laternula marilina 3� 12 57 0.2 2

Phoronida

Phoronid sp. 9� 21 57 0.5 7

Crustacea

Cyathura muromiensis 77� 90 339 5 27

Grandidierella japonica 4� 14 57 0.2 3

Ilyoplax pusilla 6� 30 169 0.4 2

Macrophthalmus japonicus 8� 29 169 0.5 4

Paracleistostoma cristatum 4� 19 113 0.2 2

Nihonotrypaea japonica 4� 14 57 0.2 3

Upogebia yokoyai 4� 14 57 0.2 3

All macrozoobenthosa 1509� 1269 5254

a The mean number of species at the 45 stations was 4.7� 1.7.

The macrozoobenthos community structure at the stations(excluding Sts. 43 and 45) was examined using cluster analy-sis, using the software PRIMER (Clarke and Gorley, 2001).A dendrogram was produced using the group average linkagemethod based on the BrayeCurtis similarity calculated fromthe square-root-transformed density of 12 common taxa thatwere found in more than three stations (Table 1). On the den-drogram (Fig. 3), seven groups of stations (groups AeG) wereidentified at a level of similarity of 55%; as an exception, St.33 was incorporated into group D with a slightly lower simi-larity level (54.2%).

The mean densities of the dominant species were calculatedfor each station group. ‘‘Typical species’’ that contributedmost to the within-group similarity were examined using aSIMPER (similarity percentages) procedure, using the soft-ware PRIMER. The differences in macrofaunal communitystructure among the station groups (except for groups F andG, which contained only two stations) were tested usingone-way analysis of similarities (ANOSIM), using the soft-ware PRIMER.

Canonical correspondence analysis (CCA) was used to ex-plore the relationships among the spatial distribution patternsof macrozoobenthos and environmental gradients. CCA wasconducted using the software CANOCO (ter Braak and Smila-uer, 1998), with the software options set for forward selectionto test the significance of environmental variables at a level ofp< 0.1. CCA is a nonlinear eigenvector ordination techniquethat constrains the axes to be linear combinations of the envi-ronmental variables (ter Braak and Smilauer, 1998). Theresults of the CCA were drawn on two biplots: stations and an-imal species were each plotted on a two-dimensional plot withthe environmental parameters represented as vectors. Theseplots can be used to determine the habitat types at each stationand habitat preferences of the species. For the CCA, we useddata sets of square-root-transformed density of 12 commonmacrozoobenthic taxa and eight standardized environmentalvariables (relative elevation, distance from lagoon mouth[i.e., indicative of salinity], silt-clay, ORP, AVS, TOC, TN,and C/N ratio) at each station.

Based on the cluster analysis and CCA results, the sevenstation groups were categorized into five habitat types (A, B,C, Dþ FþG [DFG], and E). Differences in the eight environ-mental variables were tested among the habitats using one-way analysis of variance (ANOVA) followed by a post hocTukeyeKramer test. Mean density of the 12 common animalspecies was compared between the subtidal (n¼ 17) and inter-tidal (n¼ 28) stations using a t-test. The homogeneity of data

was tested using the Bartlett test; when necessary, log(xþ 1)or square-root transformations were performed.

3. Results

In total, 23 macrozoobenthic taxa were identified in IdouraLagoon (Table 1). The polychaetes Heteromastus sp. (61% ofthe total macrozoobenthos) and Hediste spp. (19%) were themost abundant taxa in the lagoon. The isopod Cyathura mur-omiensis (5%), polychaetes Prionospio japonica (3%) and No-tomastus sp. (2%), and bivalves Nuttallia olivacea (3%) andMacoma contabulata (1%) also commonly occurred in thelagoon (occurrence; >9 stations). Four taxa, i.e., Heteromastussp., Hediste spp., P. japonica, and C. muromiensis, were dis-tributed widely in the lagoon (>21 stations). No animalswere collected at Sts. 43 and 45 in the small inlet at the inner-most lagoon (see Fig. 1).


In the lagoon, the Hediste spp. complex consisted of twospecies, Hediste atoka and Hediste diadroma (E. Kikuchi, un-published data). Though they may have slightly different eco-logical niches (e.g., Sato and Nakashima, 2003; Nanami et al.,2005; Kikuchi and Yasuda, 2006), we did not analyze themseparately in the present study since the two species couldnot be distinguished morphologically during their postlarvalstages (Sato and Nakashima, 2003).

3.1. Distribution patterns of macrozoobenthos in thelagoon

The most dominant species, Heteromastus sp., was widelydistributed in the lagoon (41 stations; Table 1). This speciesoccurred with high density (>1000 ind. m�2) in the vicinityof the lagoon mouth and in the watercourse (Fig. 2). In con-trast, it was found in lower densities (<500 ind. m�2) in tidalflats at the central and innermost lagoons. Hediste spp., Prio-nospio japonica, and Cyathura muromiensis were also com-monly found in the lagoon (>21 stations) and occurred withhigher densities near the lagoon edge and mouth. Notomastussp. and Macoma contabulata were specific to the inner lagoon,which receives freshwater from the Idoura River, althoughseveral individuals were collected from the upper tidal zonein the southern lagoon. Nuttallia olivacea was found in sandyhabitats close to the lagoon mouth and near the lagoon edge.

3.2. Classification of the macrozoobenthic communityat the stations

Fig. 2. Spatial distribution of the seven dominant macrozoobenthic species

found at 45 stations in Idoura Lagoon. The column length indicates density

(ind. m�2). Note that scales differ for different species as indicated in the

boxes.

The cluster analysis classified the macrobenthic assem-blages into seven groups (Fig. 3). One-way ANOSIM indicatedsignificant differences in community structure among thegroups ( p< 0.05, groups F and G were not tested; Table 2).

Group A consisted of 15 stations that were located at thecentral part of the lagoon (Fig. 4); the dominant specieswere Heteromastus sp., Cyathura muromiensis, and Hedistespp. (mean density: 870, 113, and 79 ind. m�2, respectively;Fig. 3). The SIMPER procedure indicated that Heteromastussp. and Prionospio japonica were the most typical speciesfor group A, respectively, contributing 62.4 and 14.3% to thewithin-group similarity. Group B consisted of nine stationslocated in the vicinity of the lagoon mouth and was character-ized by high macrofaunal density (3653 ind. m�2) with a dom-inance of Heteromastus sp. and Hediste spp. (2637 and665 ind. m�2, respectively). These two species contributed90.2% to the within-group similarity. Group C consisted ofsix stations in the upper tidal zone in the central lagoon andwas characterized by low macrofaunal density (593 ind. m�2).Heteromastus sp., Hediste spp., and C. muromiensis were thedominant species (188, 151, and 103 ind. m�2, respectively),contributing 88.2% to the within-group similarity. Group Dconsisted of six stations that were mainly located in the areanear the freshwater input. The dominant species were Hetero-mastus sp., Hediste spp., and Macoma contabulata (574, 235,and 66 ind. m�2, respectively). They contributed 90.2% to thewithin-group similarity. Group E consisted of three stations

located on sandy tidal flats and was characterized by high oc-currences of the bivalve Nuttallia olivacea, as well as Hedistespp. (320 and 1036 ind. m�2, respectively). These two speciescontributed 75.8% to the within-group similarity. Group Fconsisted of two stations in the inner and central part ofthe lagoon. This group was characterized by low macrofaunaldensity (198 ind. m�2) and the dominance of Heteromastus sp.and C. muromiensis (85 and 57 ind. m�2, respectively). GroupG consisted of two stations in the innermost part of the lagoon,with the dominance of Notomastus sp. and Hediste spp. (226

A

B

C

D

E

F

G

Fig. 3. Dendrogram showing the hierarchical clustering of 43 stations in Idoura

Lagoon using the group average linkage method. Sts. 43 and 45 were excluded

from the analysis. The BrayeCurtis similarity index was calculated from the

square-root-transformed abundances of 12 dominant taxa (Table 1). For each

station group (groups AeG), the mean densities (ind. m�2) of the total macro-

zoobenthos and of the dominant species were calculated. The SIMPER proce-

dure was used to examine the contribution (%) of typical species to within-

group similarity until the cumulative percentage reached 80% of the total. Ab-

breviations: Cya, Cyathura muromiensis, Hed, Hediste spp.; Het, Heteromastus

sp.; Mac, Macoma contabulata; Not, Notomastus sp.; Nut, Nuttallia olivacea;

Pri, Prionospio japonica.

Table 2

One-way analysis of similarities showing significant differences in macrozoo-

benthic community structure among the five station groups found in the cluster

analysis (A: n¼ 15, B: n¼ 9, C: n¼ 6, D: n¼ 6, E: n¼ 3; see Fig. 3). Groups

F and G were not examined because they included only two stations each. The

number of permutations was 999

1-way ANOSIM

R-value p Value

Treatment effect 0.71 <0.001

Pairwise comparison

A, B 0.57 <0.001

A, C 0.64 <0.001

A, D 0.57 <0.001

A, E 0.93 <0.001

B, C 0.96 <0.01

B, D 0.84 <0.01

B, E 0.85 <0.01

C, D 0.64 <0.01

C, E 0.81 <0.05

D, E 0.96 <0.05


and 57 ind. m�2, respectively). Notomastus sp. contributed58.6% to the within-group similarity.

3.3. Distribution of species along environmentalgradients

In the forward selection procedure of the CCA, AVS, TOC,TN, and the C/N ratio were insignificant at a level of p< 0.1.Accordingly, four variables (distance from lagoon mouth,ORP, elevation, and silt-clay content) were used as environmen-tal parameters in the CCA (Table 3). The variables explained78.5% of the variance of the first two CCA axes. The firstaxis showed the highest positive correlation with distancefrom the lagoon mouth (i.e., salinity; r¼ 0.987, p< 0.001)

and a weaker negative correlation with sediment ORP (r¼�0.704, p< 0.001). This axis seemed to mainly reflect the en-vironmental salinity, which was closely related to the locationof each station. The second axis showed the highest correlationswith silt-clay content (r¼�0.761, p< 0.001) and ORP(r¼ 0.670, p< 0.001). In this lagoon, the silt-clay content ispositively correlated with other sediment parameters, includingAVS, TOC, and TN (G. Kanaya, unpublished data). Therefore,the second axis would be closely related to the bottom charac-teristics at each station.

On the CCA plot (Fig. 5a), stations belonging to groups D,F, and G were plotted mainly on the right side, whereasstations in group B were located on the left side and stationsin groups A and C were near the center. These placements in-dicate that the groups had different environmental parametersalong axis 1 (i.e., salinity and possibly ORP). Stations in groupE were plotted on the upper part of the plot, suggesting that thegroup was distinguished from the other groups along axis 2(i.e., sediment characteristics).

Based on the plot, the seven station groups were consoli-dated into five habitat types: A, B, C, Dþ FþG [DFG], andE. Distance from the lagoon mouth, silt-clay content, ORP,and AVS content differed significantly among the five habitattypes (one-way ANOVA, p< 0.05; Fig. 6), whereas relative el-evation, TOC, TN, and the C/N ratio did not ( p> 0.05). GroupB was closer to the lagoon mouth (distance from lagoon mouth;0.38� 0.24 km) than were groups A and DFG (0.97� 0.38 and1.42� 0.43 km, respectively; TukeyeKramer test, p< 0.05).The sediment at group E sites was sandier and more oxidized(silt-clay: 4.7� 3.6%, ORP: 237� 84 mV) compared to thatat groups A, C, and DFG sites (TukeyeKramer test,p< 0.05). Group E sites were also characterized by low AVScontent (1.46� 2.10 mmol g�1 dw) relative to those of groupsA, C, and DFG, although the difference was not statistically sig-nificant (TukeyeKramer test, p> 0.05). Although groups A, B,and DFG sites contained muddy sediments (silt-clay: 44� 26,25� 24, and 38� 21%, respectively), group B sites were

Fig. 4. Spatial distribution of the seven station groups (groups AeG) in Idoura Lagoon identified using cluster analysis (Fig. 3). Stations in groups B, C, and

Dþ FþG [DFG] are indicated by broken lines, black triangles, and gray-colored areas, respectively.


characterized by having much more oxidized sediment (ORP:157� 84 mV, AVS: 0.94� 1.2 mmol g�1 dw) than those ofgroups A (70� 70 mV, 9.58� 14.2 mmol g�1 dw) and DFG(25� 34 mV, 9.76� 9.43 mmol g�1 dw; TukeyeKramer test,p< 0.05). Group C sites were characterized by muddy sedi-ments (silt-clay: 58� 18%), moderate ORP (66� 60 mV),and high AVS content (8.8� 7.8 mmol g�1 dw). Stations withno macrozoobenthic animals (Sts. 43 and 45) were character-ized by having much higher AVS contents in the sediments(97.0 and 82.1 mmol g�1 dw, data are not shown) compared tothe other stations (<32.5 mmol g�1 dw).

The CCA also revealed relationships among 12 macrozoo-benthic species and environmental variables (Fig. 5b). The bi-valve Macoma contabulata, polychaetes Notomastus sp. andSabellidae sp., and the crab Macrophthalmus japonicus were

Table 3

Summarized results of canonical correspondence analysis using four environ-

mental parameters and macrozoobenthic abundance data for 43 stations (Sts.

43 and 45 were excluded). Inter-set correlations between the first three canon-

ical axes and the environmental variables are presented. Significant correla-

tions between each environmental variable and the axes are indicated with

asterisks: ***p< 0.001

Axis 1 Axis 2 Axis 3

Eigenvalue 0.159 0.122 0.046

Specieseenvironment correlation 0.799 0.770 0.589

Cumulative % variance

Of species data 11.7 20.6 24.0

Of specieseenvironmental relation 44.4 78.5 91.3

Inter-set correlation

with environmental variablesa

Distance from lagoon mouth 0.987*** 0.061 0.120

ORP �0.704*** 0.670*** �0.087

Relative elevation 0.260 0.192 �0.795***

Silt-clay 0.253 �0.761*** �0.513***

a During the forward selection procedure, four sediment variables, i.e., acid-

volatile sulfides (AVS), total nitrogen (TN), total organic carbon (TOC), and

the carbon/nitrogen ratio (C/N ratio), were excluded from the analysis at a sig-

nificance level of p< 0.1.

clustered on the right side of the plot. This indicates thatthey were mainly distributed at stations in the inner lagoon(i.e., lower salinity). The bivalve Nuttallia olivacea was foundmainly on the upper left side of the plot (i.e., sandy and oxi-dized habitat), whereas M. contabulata, M. japonicus, Phoro-nid sp., and the polychaete Pseudopolydora kempi japonicawere on the lower part of the plot (i.e., muddy habitat). TheCCA implied that the other dominant species, i.e., Heteromas-tus sp., Hediste spp., Prionospio japonica, and Cyathura mur-omiensis, were widely distributed along the environmentalvariables because they were clustered near the origin. How-ever, the cluster and univariate (one-way ANOVA) analysesshowed that Hediste spp. achieved the highest densities inboth groups E (1036 ind. m�2) and B (665 ind. m�2; Fig. 3),which were found in sites that were characterized by oxidizedsediments (Fig. 6). Heteromastus sp. also occurred with muchhigher density in group B, which sites had oxidized mud(2637 ind. m�2), compared to group A, which sites had re-duced mud (870 ind. m�2), although the silt-clay content wasnot significantly different between the groups’ sites.

The effects of emergence on the animals were tested by com-paring the mean densities of 12 common taxa (see Table 1) be-tween the subtidal and intertidal stations. Only two speciesshowed significant difference in density between the two habi-tats (df¼ 43, t¼ 2.16 for Notomastus sp. and �2.05 for Phoro-nid sp., p< 0.05, t-test), while the others did not ( p> 0.05).Phoronid sp. exhibited higher density in the subtidal habitat(17� 27 ind. m�2, n¼ 17) than in the intertidal habitat(4� 15 ind. m�2, n¼ 28), while Notomastus sp. showed aninversive trend (subtidal; 3� 14 ind. m�2, intertidal; 44�87 ind. m�2).

4. Discussion

Many studies have demonstrated that salinity and sedimentcharacteristics are significant factors that limit the distributionof macrozoobenthos in estuarine and coastal waters (e.g.,

a

b

Fig. 5. Canonical correspondence analysis biplots: (a) station scores and (b)

species scores. Arrows indicate environmental variables. Allowance for eleva-

tion is not shown because it was not significantly correlated with axes 1 or 2

(see Table 3). Station groups identified using cluster analysis (Fig. 3) are indi-

cated by different symbols in plot (a). The first three to seven characters of

each taxon name of the macrozoobenthos (see Table 1 for full names) are pro-

vided in plot (b).


Sanders, 1958; Sanders et al., 1965; Bachelet et al., 1996;Teske and Wooldridge, 2003; Ysebaert et al., 2003; Nanamiet al., 2005). In soft-bottom habitats, however, sediment grainsize is often correlated with other environmental parameters(e.g., organic content, Yamamuro et al., 1990; Snelgrove andButman, 1994). This often makes it difficult to infer which en-vironmental variables are more responsible for the distributionpattern of a species (Yamamuro et al., 1990). Integrated inter-pretations of multivariate and univariate analyses providedetailed information about environmenteanimal relations inestuarine soft-bottom habitats.

Of the 23 macrozoobenthic taxa that occurred in IdouraLagoon, the deep-burrowing capitellid polychaete Heteromas-tus sp. and a few other species dominated the community nu-merically (Table 1). The dominant species in the lagoon (i.e.,Heteromastus sp., Notomastus sp., Hediste spp., and Prionospiojaponica) are commonly found in mesohaline to polyhalinebrackish waters along the coast of Japan (Yamamuro et al.,1990; Yamamuro, 1996; Doi et al., 2005; Nanami et al.,2005). The densities of the dominant species showed markedspatial variation (Fig. 2), resulting in highly heterogeneous mac-rozoobenthic assemblages in the lagoon (Fig. 4). The forwardselection procedure of the CCA found that the four environmen-tal variables (AVS, TOC, TN, and the C/N ratio) were the insig-nificant factors (Table 3). The CCA indicated that salinity, thesilt-clay content, and ORP contributed mostly to the spatialdistribution patterns of macrozoobenthic species, whereasrelative elevation exhibited a much weaker contribution. Theseresults suggest that sediment characteristics (silt-clay contentand redox condition) and salinity are the major structuringfactors for macrozoobenthic assemblages in Idoura Lagoon.

Relative elevation (or water depth) sometimes acts as a sig-nificant factor, creating a zonation pattern of macrozoobenthicassemblages in estuarine soft-bottom habitats (Ono, 1967;Bachelet et al., 1996; Ysebaert et al., 2003). At Idoura Lagoon,however, both multivariate (CCA) and univariate (one-way AN-OVA) analyses demonstrated that the macrozoobenthic commu-nity structure was hardly affected by the relative elevation of thehabitat (Table 3; Fig. 6). We had also made comparisons formean densities of the 12 common macrozoobenthic taxa (seeTable 1) between intertidal and subtidal stations. The resultsshowed that only two taxa exhibited a significant differencebetween the habitats (df¼ 43, t¼ 2.16 for Notomastus sp. and�2.05 for Phoronid sp., p< 0.05, t-test), whereas the other 10taxa did not ( p> 0.05). Phoronid sp. exhibited higher densityin the subtidal habitat (17� 27 ind. m�2, n¼ 17) than in the in-tertidal habitat (4� 15 ind. m�2, n¼ 28). In contrast, density ofNotomastus sp. was much higher in the intertidal habitat(44� 87 ind. m�2) than in the subtidal habitat (3� 14-ind. m�2). These suggest that the physical stresses from desic-cation and high temperatures played only minor role instructuring the macrozoobenthic assemblage at these stations.The reason for this may be that most of the sampling stationswere located in the subtidal or lower intertidal zones, whichhad short emergence periods (Fig. 6a).

Based on these results, the macrozoobenthic communitiesat the stations were classified into five types along the environ-mental gradients (Fig. 3). (1) Group B, habitat with highersalinity and oxidized mud characterized by the high densitiesof Heteromastus sp. and Hediste spp. (2) Group A, habitat inthe middle lagoon that had reduced mud. Heteromastus sp.(moderate density), Prionospio japonica, and Cyathura muro-miensis were the typical species. (3) Group C, habitat near thelagoon edge (Fig. 4) that had reduced mud. This group wascharacterized by the low densities of dominant species, Heter-omastus sp., Hediste spp., and C. muromiensis. (4) Group E,habitat with oxidized sand inhabited mainly by Hediste spp.Nuttallia olivacea was specific to this group. (5) Group

a

b

c

d

f

e

Fig. 6. Comparison of the mean environmental parameters among the five station groups, i.e., A, B, C, Dþ FþG [DFG], and E, that were categorized using the

results of canonical correspondence analysis (Fig. 5). (a) Relative elevation, (b) distance from the lagoon mouth (i.e., decreasing salinity), (c) silt-clay content, (d)

ORP and AVS content, (e) TOC and TN contents, and (f) C/N ratio. The F-value (df¼ 4, 38) for one-way ANOVA is shown with the significance level (**p< 0.01,

***p< 0.001, n.s., not significant). Different letters indicate significant differences among the groups (TukeyeKramer test, p< 0.05).


DFG, habitat with low salinity (i.e., inner lagoon) and reducedmud characterized by the appearance of Macoma contabulata(group D) and Notomastus sp. (group G). These results suggestthat the spatial heterogeneity in the macrozoobenthic assem-blages was closely related to the habitat preferences of eachmacrozoobenthic species along the environmental gradients.

Tolerance to changing environmental salinity would partiallyexplain the observed distribution pattern for the macrozoo-benthic species in Idoura Lagoon. Yamamuro (1996) reviewedprevious studies conducted in brackish waters of Japan, includ-ing her own researches, and concluded that the distributions ofestuarine macrozoobenthos are primarily determined by envi-ronmental salinity. For example, the oligohaline polychaete No-tomastus sp. is distributed mainly in upper estuarine habitats(sal.<5.5), whereas mesohaline to polyhaline polychaetes Het-eromastus sp., Hediste spp., and Prionospio japonica inhabitlower estuarine to marine habitats that have higher salinity(sal. >5.5). The classification by Yamamuro (1996) wouldpartly explain the distribution patterns of these species in our

study site. In Idoura Lagoon, the oligohaline species Notomas-tus sp. was specific to the inner lagoon habitat that receivesfreshwater from the Idoura River (Fig. 2) although the mesoha-line to polyhaline species (Heteromastus sp., Hediste spp., andP. japonica) were widely distributed in the lagoon. This sug-gests that the low salinity in the innermost lagoon (Miyagi Pre-fecture, 1988; Kanaya et al., in press) positively affected therecruitment and/or post-settlement survival of Notomastus sp.In contrast, environmental salinity would not be the lethal factorfor most of the mesohaline to polyhaline species in the lagoonalsystem. Our data also showed that the bivalve Macoma contabu-lata was specific to the inner lagoon habitat as well as Notomas-tus sp. However, this bivalve species is commonly found in moreseaward habitats along Sendai Bay that have much higher salin-ity (e.g., Kikuchi and Hata, 1999; Kanaya et al., 2005; G. Ka-naya, unpublished data). Other environmental factors that wedid not measure are possibly responsible for the spatial distribu-tion pattern of this species in Idoura Lagoon. Further studies ofthe ecological distribution of M. contabulata are needed.


As mentioned above, a simple model had been proposed byYamamuro (1996), that macrozoobenthic assemblages in Japa-nese brackish waters are determined primarily by salinity in thehabitat. However, the distribution patterns of several animalspecies in Idoura Lagoon seemed to be influenced more by sed-iment characteristics (i.e., sediment grain size and redox condi-tion) than salinity. This strongly suggests that sedimentcharacteristics should be considered as additional (or some-times more significant) factors that define the macrozoobenthiccommunity structure in Japanese brackish waters. It has longbeen mentioned that the spatial distributions of suspension-and deposit-feeders are strongly affected by sediment grainsize (e.g., Sanders, 1958; Rhoads and Young, 1970). In general,suspension-feeders are more abundant at sites that have sandybottoms, whereas deposit-feeders attain high densities on softmuddy substrata that are rich in fine organic particles (Sanders,1958; Rhoads and Young, 1970). Our results are partly consis-tent with this idea. For example, the bivalve Nuttallia olivacea,which was typical of the sandy habitat in Idoura Lagoon (GroupE, silt-clay: 4.7%), is a facultative suspension feeder (Kanayaet al., 2005). In contrast, the dominant species in the muddyhabitat groups, including Heteromastus sp., Notomastus sp.,Hediste spp., Prionospio japonica, Cyathura muromiensis,and Macoma contabulata (Fig. 3), are surface- or deep-de-posit-feeders (Fauchald and Jumars, 1979; Yamamuro et al.,1990; Kikuchi and Wada, 1996; Kanaya et al., 2005; G. Kanaya,unpublished data). This suggests that a smaller grain size wouldallow the predominance of deposit-feeders while having a neg-ative effect on the recruitment and/or post-settlement survivalof the suspension-feeder N. olivacea.

Sulfide accumulation in the sediment sometimes acts as alethal factor for estuarine benthic invertebrates at both spatialand temporal scales (e.g., Gamenick et al., 1996). Neverthe-less, the relationships between sediment redox conditions(i.e., ORP and sulfide content) and the spatial distribution ofmacrozoobenthos are rarely mentioned in studies of estuarinesoft-bottom habitats (Yamamuro et al., 1990; Ysebaert andHerman, 2002; Teske and Wooldridge, 2003; Nanami et al.,2005; but see Gamenick et al., 1996). At our study site, spatialextinction of macrozoobenthos was observed at the two sta-tions (Sts. 43 and 45) that were characterized by distinctivelyhigh AVS contents (97.0 and 82.1 mmol g�1 dw) relative to theother stations (<32.5 mmol g�1 dw; data are not shown). Ourdata also showed that the dominant species, Heteromastussp., occurred with much higher density in group B (2637 in-d. m�2; high ORP and low AVS) than in group A (870 in-d. m�2; low ORP and high AVS) although both groupsoccurred on muddy sediments (Fig. 6). This worm seems tobe sensitive to sulfide accumulation and hypoxia in muddyreduced habitats because of its deep-burrowing behavior andlow ventilation activity (G. Kanaya, unpublished data). There-fore, prevalence of anaerobic condition in the sediment maynegatively affect the survival of Heteromastus sp. in the habi-tat. Our data also suggest that Hediste spp. prefer oxidized sed-iment because they achieved the highest densities in groups Band E sites (665e1036 ind. m�2), which had more oxidizedsediment regardless of the silt-clay content (Fig. 6). These

results support the idea that sediment redox conditions (i.e.,ORP and sulfide content) are one of the lethal factors thataffect the spatial distribution of macrozoobenthic invertebratesin estuarine soft-bottom habitats.

Our data clearly demonstrate that the macrozoobenthicassemblages in the shallow brackish lagoon changed signifi-cantly along environmental gradients. At Idoura Lagoon,the spatial distribution patterns of the macrozoobenthos werestrongly affected by environmental parameters, includingsalinity (distance from lagoon mouth), sediment grain size(silt-clay content), and the redox condition of the sediment(ORP and AVS content) within a relatively small spatial scale(e.g., hundreds of meters). Above all, our results emphasizethe importance of the sediment redox condition (ORP andAVS) in assessing the spatial distribution patterns of macro-zoobenthos in estuarine soft-bottom habitats, in which the sed-iment redox condition shows dramatic spatial differences(Kanaya and Kikuchi, 2004). Our results clearly show thatthe highly fluctuating physical and chemical environments inestuaries provide macrozoobenthic animals with diverse typesof habitats and thus may result in the coexistence of animalswith different habitat selectivity within a relatively small scale(e.g., hundreds of meters).

Acknowledgements

We would like to thank T. Masuda, E. Nobata, and N. Iso-mura for their help in the field samplings. Special thanks to Dr.T. Suzuki for his aid in identification of the macrozoobenthos.We are also grateful to two anonymous referees for theirreviewing, advising, and critical comments on the manuscript.

References

Atrill, M., Ramsay, P., Thomas Myles, R., Trett, M., 1996. An estuarine

biodiversity hot-spot. Journal of the Marine Biological Association of

the United Kingdom 76, 161e175.

Bachelet, G., de Montaudouin, X., Dauvin, J.-C., 1996. The quantitative

distribution of subtidal macrozoobenthic assemblages in Arcachon Bay

in relation to environmental factors: a multivariate analysis. Estuarine,

Coastal and Shelf Science 42, 371e391.

ter Braak, C.J.F., Smilauer, P., 1998. CANOCO Reference Manual and User’s

Guide to Canoco for Windows: Software for Canonical Community Ordi-

nation (Version 4). Microcomputer Power, Ithaca, New York, 351 pp.

Capone, D.G., Kiene, R.P., 1988. Comparison of microbial dynamics in

marine and freshwater sediments. Limnology and Oceanography 33,

725e749.

Clarke, K.R., Gorley, R.N., 2001. Primer (Plymouth Routines In Multivariate

Ecological Research) v5: User Manual/Tutorial. PRIMER-E Ltd.,

Plymouth, 91 pp.

Day Jr., J.W., Hall, C.A.S., Kemp, W.M., Ya~nez-Arancibia, A., 1989. Estuarine

Ecology. John Wiley & Sons, New York, 558 pp.

Doi, H., Matsumasa, M., Toya, T., Satoh, N., Mizota, C., Maki, Y., Kikuchi, E.,

2005. Spatial shifts in food sources for macrozoobenthos in an estuarine

ecosystem: carbon and nitrogen stable isotope analyses. Estuarine, Coastal

and Shelf Science 64, 316e322.

Fauchald, K., Jumars, P.A., 1979. The diet of worms: a study of polychaete

feeding guilds. Oceanography and Marine Biology: an Annual Review

17, 193e284.

Gamenick, I., Jahn, A., Vopel, K., Giere, O., 1996. Hypoxia and sulphide as

structuring factors in a macrozoobenthic community on the Baltic Sea


shore: colonisation studies and tolerance experiments. Marine Ecology

Progress Series 144, 73e85.

Heip, C.H.R., Goosen, N.K., Herman, P.M.J., Kromkamp, J., Middelburg, J.J.,

Soetaert, K., 1995. Production and consumption of biological particles in

temperate tidal estuaries. Oceanography and Marine Biology: an Annual

Review 33, 1e149.

Kanaya, G., Kikuchi, E., 2004. Relationships between sediment chemical buff-

ering capacity and H2S accumulation: comparative study in two temperate

estuarine brackish lagoons. Hydrobiologia 528, 187e199.

Kanaya, G., Nobata, E., Toya, T., Kikuchi, E., 2005. Effects of different feed-

ing habits of three bivalve species on sediment characteristics and benthic

diatom abundance. Marine Ecology Progress Series 299, 67e78.

Kanaya, G., Takagi, S., Kikuchi, E. Spatial dietary variations in Laternula

marilina (Bivalva) and Hediste spp. (Polychaeta) along environmental

gradients in two brackish lagoons. Marine Ecology Progress Series. doi:

10.3354/meps07356, in press.

Kang, C.-K., Choy, E.J., Paik, S.-K., Park, H.J., Lee, K.-S., An, S., 2007.

Contributions of primary organic matter sources to macroinvertebrate pro-

duction in an intertidal salt marsh (Scirpus triqueter) ecosystem. Marine

Ecology Progress Series 334, 131e143.

Kikuchi, E., Hata, H., 1999. Comparative study of macrofauna and sediment of

two brackish tidal flats located at river mouths facing Sendai Bay. North-

east Asian Studies 3, 39e58.

Kikuchi, E., Wada, E., 1996. Carbon and nitrogen isotope ratios of deposit-

feeding polychaetes in the Nanakita River Estuary, Japan. Hydrobiologia

321, 69e75.

Kikuchi, E., Yasuda, K., 2006. Comparison of the life cycles of two sympatric es-

tuarine polychaetes, Hediste diadroma and H. atoka (Polychaeta: Nereididae),

in the Nanakita River estuary, northeastern Japan. Limnology 7, 103e115.

Miyagi Prefecture, 1988. III Suishitsu chousa. In: Miyagi Prefecture (Ed.),

Idoura Chiku (Kanhai) I-71 gou ‘‘Idoura Gawa kankyou cyousa gyoumu

houkokusho’’. Miyagi Prefecture, Sendai, Japan, pp. 70e120 (in Japanese).

Nanami, A., Saito, H., Akita, T., Motomatsu, K., Kuwahara, H., 2005. Spatial

distribution and assemblage structure of macrobenthic invertebrates in

a brackish lake in relation to environmental variables. Estuarine, Coastal


Ono, Y., 1967. On the ecological distribution of ocypoid crabs in the estuary. Mem-

oirs of the Faculty of Science Kyushu University Series E Biology 4, 1e60.

Pechenik, J.A., Berard, R., Kerr, L., 2000. Effects of reduced salinity on

survival, growth, reproductive success, and energetics of the euryhaline

polychaete Capitella sp. I. Journal of Experimental Marine Biology and

Ecology 254, 19e35.

Rhoads, D.C., Young, D.K., 1970. The influence of deposit-feeding organisms

on sediment stability and community trophic structure. Journal of Marine

Research 28, 150e178.

Sanders, H.L., 1958. Benthic studies in Buzzards Bay. I. Animal sediment

relationships. Limnology and Oceanography 3, 245e258.

Sanders, H.L., Mangelsdorf, P.C.J., Hampson, G.R., 1965. Salinity and faunal

distribution in the Pocasset River, Massachusetts. Limnology and Ocean-

ography 10 (Suppl.), 216e229.

Sato, M., Nakashima, A., 2003. A review of Asian Hediste species complex

(Nereididae, Polychaeta) with descriptions of two new species and a rede-

scription of Hediste japonica (Izuka, 1908). Zoological Journal of the

Linnean Society 137, 403e455.

Snelgrove, P.V.R., Butman, C.A., 1994. Animalesediment relationships revis-

ited: cause versus effect. Oceanography and Marine Biology: an Annual

Review 32, 111e177.

Suzuki, S., Shiga, H., 1953. Studies on behavior of hydrogen sulfide in water-

logged soils. (part 1) Determination of hydrogen sulfide and other sulfides

in soils. Bulletin of the Chugoku National Agricultural Experimental

Station 2, 43e56 (in Japanese).

Teske, P.R., Wooldridge, T.H., 2003. What limits the distribution of subtidal

macrobenthos in permanently open and temporarily open/closed South

African estuaries? Salinity vs. sediment particle size. Estuarine, Coastal


Yamamuro, M., Nakamura, M., Nishimura, M., 1990. A method for detecting

and identifying the lethal environmental factor on a dominant macroben-

thos and its application to Lake Shinji, Japan. Marine Biology 107,

479e483.

Yamamuro, M., 1996. Kanchoiki no teiseidoubutsu. In: Saijo, Y., Okuda, S.

(Eds.), Kasen kanchoiki e Sono shizen to henbou. Nagoya University

Press, Nagoya, Japan, pp. 151e172 (in Japanese).

Ysebaert, T., Herman, P.M.J., 2002. Spatial and temporal variation in benthic

macrofauna and relationships with environmental variables in an estuarine,

intertidal soft-sediment environment. Marine Ecology Progress Series 244,

105e124.

Ysebaert, T., Herman, P.M.J., Meire, P., Craeymeersch, J., Verbeek, H.,

Heip, C.H.R., 2003. Large-scale spatial patterns in estuaries: estuarine

macrobenthic communities in the Schelde estuary, NW Europe. Estuarine,

Coastal and Shelf Science 57, 335e355.

spatial changes in a macrozoobenthic community along environmental gradients in a shallow brackish...

Documents