- Email: [email protected]
Benthic quality assessment using M-AMBI in the Seto Inland Sea, Japan
Marine Environmental Research 148 (2019) 67–74
Contents lists available at ScienceDirect
Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev
Benthic quality assessment using M-AMBI in the Seto Inland Sea, Japan a,∗
b
c
a
Akira Umehara , Satoshi Nakai , Tetsuji Okuda , Masaki Ohno , Wataru Nishijima a b c
T
a
Environmental Research and Management Center, Hiroshima University, 1-5-3 Kagamiyama, Higashi-hiroshima, Hiroshima, 739-8513, Japan Graduate School of Science and Engineering, Hiroshima University, 1-4-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8527, Japan Department of Environmental Solution Technology, Faculty of Science and Technology, Ryukoku University, 1-5 Yokoya, Seta Oe-cho, Otsu, Shiga, 520-2194, Japan
A R T I C LE I N FO
A B S T R A C T
Keywords: Biotic index Coastal management Ecological status Enclosed sea Macrobenthos
Benthic invertebrates that inhabit the seafloor respond to anthropogenic and natural stresses, and are good indicators for assessing the benthic ecological status. We evaluated the ecosystem health of the Seto Inland Sea based on the multivariate AZTI Marine Biotic Index (M-AMBI), being its first application in a Japanese coastal sea with numerous endemic species. From the 415 locations studied, we were able to use M-AMBI in 384 sites (92.5% in all sites). The result revealed a statistically significant correlation among biotic indices including AMBI, M-AMBI, Richness, and H’ (p < 0.01). Most of the physico-chemical parameters of the sediment (water content, total organic carbon (TOC) content, sulfide content, mud content, and oxidation–reduction potential (ORP)) were significantly correlated with each other excluding sediment temperature. The M-AMBI was significantly correlated with physico-chemical variables including water content, TOC content, sulfide content, and ORP. We found that the sites classified into the organically enriched cluster, and having high contents of TOC, mud, and sulfide and negative ORP, corresponded with sites that had significantly low M-AMBI values (bad-poor ecological status). Conversely, sites in the unpolluted sandy cluster were assigned high M-AMBI values (highgood ecological status). Therefore, M-AMBI would be a useful biotic index in Japanese coasts due to the representation of the comprehensive sediment quality.
1. Introduction
importance of biological indicators has been emphasised in legislation around the world (Borja et al., 2008a), and especially in Europe, under the Water Framework Directive (WFD, European Commission, 2000) and the Marine Strategy Framework Directive (MSFD, European Commission, 2008), which have resulted in multiple indices to assess the status of marine waters (Birk et al., 2012; Borja et al., 2016). In shallow coastal areas, anthropogenic impacts arising mostly from land affect both pelagic and benthic ecosystems, which are also strongly interrelated. Compared with the pelagic environment, the negative effects of these anthropogenic impacts can remain present in coastal areas for a long time after removal of the impacts (Borja et al., 2010a; Verdonschot et al., 2013; Duarte et al., 2015). Although dilution and dispersion were important natural phenomenon that reduces the concentrations of pollutants in the environment, it was insufficient for reducing concentrations in the sediment; therefore, hazardous trace contaminants, such as heavy metals and persistent organic pollutants, could easily remain in sediments (Pitacco et al., 2018). Benthic invertebrates provide useful indicators for assessing the environment of these contaminated sediments. Many ecological status indices were calculated based on the macrobenthic community structure, including the Benthic Condition Index,
Rapid industrial development, urbanization, and increased tourism have had deleterious impacts on coastal marine ecosystems over the last four decades (Islam and Tanaka, 2004). In coastal areas, the frequency, magnitude and geographic extent of red tides and hypoxia have increased, and fisheries have declined throughout the world (Worm et al., 2006; Díaz and Rosenberg, 2008). Many efforts have been made to restore these deteriorated ecological conditions, including the reduction of anthropogenic impacts such as excessive nutrient loads (Kronvang et al., 2005; Kemp et al., 2009). Environmental management should include an assessment of the present conditions of the environment (Borja et al., 2010b). Physicochemical and biological water and sediment parameters are generally analyzed and assessed. An ecological approach based on biological indicators with different sensitivities to environmental stress is an effective tool for assessing the environment. Hence, Dauer (1993) noted the importance of biological indicators, as (1) they constitute direct measures of the condition of the biota, (2) they may uncover problems that were undetected or underestimated through other methods, and (3) they allow assessment of the progress of restoration efforts. The
∗
Corresponding author. E-mail address: [email protected] (A. Umehara).
https://doi.org/10.1016/j.marenvres.2019.05.007 Received 17 December 2018; Received in revised form 7 May 2019; Accepted 7 May 2019 Available online 11 May 2019 0141-1136/ © 2019 Elsevier Ltd. All rights reserved.
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Fig. 1. Investigation sites in the Seto Inland Sea, Japan. Samples of the sediments and macrobenthos were collected by the Ministry of the Environment during summer 2001–2005. Curved lines on the land in the figure show the large rivers that the annual averaged discharge were more than 10 m3 s−1 (Japan River Association, 2018).
parameters of the sediments, we expect a more accurate understanding of environmental conditions to be achieved. In the present study, benthic quality assessment was conducted using the M-AMBI with macrobenthos data collected in the Seto Inland Sea during 2001–2005 by MOE. For evaluation of the applicability of the index in coastal areas of Japan, the M-AMBI values were compared to physico-chemical parameters of the sediment.
North Carolina Biotic Index (NCBI), AZTI Marine Biotic Index (AMBI), Benthic Quality Index, and Multivariate AZTI Marine Biotic Index (MAMBI) (Díaz et al., 2004; Borja et al., 2015). These indices are constructed based on information about the sensitivity of macrobenthos to an environmental stress gradient, and serve as tools for evaluation of the health of benthic ecosystems. These indices have been applied in many regions, including European estuarine and coastal environments, the Atlantic region, and the Indian Ocean (Borja et al., 2015; Pitacco et al., 2018). Japan is an island country with many endemic species, which limits the effective application of the indices. To date, no evaluation of ecological quality using AMBI and M-AMBI has been conducted in Japan. The Seto Inland Sea is the largest semi-enclosed coastal sea in Japan (23,203 km2). This sea is located in the western part of Japan and is connected to the Pacific Ocean via its western and eastern channels (Fig. 1). In the Seto Inland Sea, policies for reduction of organic matter and nutrient loads from land have been enforced since the period of high economic growth in the 1950s–70s, namely the Water Pollution Control Law (1970) and the Law Concerning Special Measures for Conservation of the Environment of the Seto Inland Sea (1973). Since 1979, Total Pollutant Load Control System (TPLCS) has been implemented (http://www.env.go.jp/en/water/ecs/guidance_tplcs_ summary.pdf), and the pollutant loads including chemical oxygen demand (COD), total nitrogen, and total phosphorus from lands have been reduced. The pollutant load sources include not only industrial effluent, but also household discharge, agricultural wastewater and so on. Consequently, the TPLCS has successfully prevented the increase in the total discharge of pollutant, and the deterioration of water quality has been brought under control, with some evidence of water quality improvement, such as the reduced number of occurrences of red tide. Although the relationship between the sediment quality and distribution of Annelida was studied by Murakami et al. (1998), the sediment quality and macrobenthic community structure of the Seto Inland Sea have not been thoroughly characterized. Therefore, Nishijima et al. (2015) attempted to characterize the macrobenthic community structure in sediments using cluster analysis based on physico-chemical parameters of the sediments. Large-scale monitoring data (425 sites) related to sediment quality and macrobenthos populations in the Seto Inland Sea during 2001–2005, collected by the Ministry of the Environment (MOE) were used. The monitoring sites were located throughout the whole sea to provide a representative dataset with high spatial resolution. It was revealed that important parameters, such as total organic carbon (TOC) and mud contents, influence macrobenthic population size and biodiversity, and identified the typical macrobenthos in the clusters representing organically enriched or un-enriched sediments. On the other hand, no assessment of benthic invertebrates from each region in the Seto Inland Sea has been conducted. If biotic indices such as M-AMBI are used along with physico-chemical
2. Materials and methods 2.1. Study area The Seto Inland Sea is a shallow enclosed coastal sea (mean depth ca. 38 m; water volume ca. 816 km3) divided into 13 sub-areas based on geographical and topographical features (Fig. 1). Each sub-area has a different degree of closure and unique environmental conditions. Sampling of sediments and macrobenthos was carried out by MOE at 415 locations in the Seto Inland Sea during the summers (July–August) of 2001–2005. 2.2. Sample collection and analysis Samples for assessing the physico-chemical parameters of the sediment (water depth, sediment temperature, grain size, TOC, oxidation–reduction potential (ORP), and sulfide content) and macrobenthos were collected from the sediment surface using a Smith-McIntyre grab sampler (0.1 m2). The number of replicates for the physico-chemical parameters of the sediment and macrobenthos were three and two, respectively. Sediment analysis was carried out according to the sediment test method (Ministry of the Environment, 2001). Details of the analyses of sediment and macrobenthos were provided in Nishijima et al. (2015). After removal of carbonates from the sample with 2 N HCl, TOC content of the dried sediment was determined with an elemental analyzer. The grain size composition (pebble, > 2.0 mm; sand, 0.063–2.0 mm; mud, < 0.063 mm) of the sediment was determined using the wet sieving method. Sulfide content was defined as the amount of hydrogen sulfide produced under acidic conditions, which was determined using a Hydrotec-s kit (Gastec Corp.). The samples for macrobenthos were fixed with 10% formalin or 70% alcohol on the ship. In the laboratory, macrobenthos were identified to the species or the lowest possible taxon, and counted. 2.3. Data analysis Soft-bottom macrobenthos were analyzed using the AMBI program (http://ambi.azti.es, v.5.0, species list updated in June 2017), and biotic indices such as richness (number of species or taxa), ShannonWiener diversity (H’), AMBI, and M-AMBI were calculated. We carefully 68
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
most common taxa in all ecological groups. All species or taxa that were among the five most common taxa of the G4 and G5 groups (opportunistic species) fell into the Annelida, except for the pollution indicator, Theora lubrica, Mollusca (15.7% in all sites) and Nebalia japonensis, Arthropoda (0.5%). Although Capitellidae sp. (10.6%), and Capitella sp. (2.4%) were observed at only a small number of sites, they accounted for 25.8% and 2.8%, respectively, of the taxon density relative to total density in G5. The spatial distributions of each ecological group (G1–5) of macrobenthos in Seto Inland Sea are shown in Fig. 2. G1, G2, and G3 tended to dominate the offshore area. In contrast, G4, consisting of secondorder opportunistic species, tended to inhabit coastal regions strongly affected by anthropogenic stresses. Typical regions inhabited by G4 were the enclosed Osaka Bay, where G4 species or taxa dominated > 50% of the macrobenthos sampled in 12 out of 29 sites. G5 consisted of first-order opportunistic species, which were observed at 163 out of 384 total sites (42.4%), and sites at which the combined percentage of Capitellidae sp. and Capitella sp. accounted for more than 10% of the species composition were mainly distributed in eastern region of Suo Nada.
checked the AMBI values of the sites with low richness, low density, or with non-listed species more than 20% of the total in physically stressed areas, according to the AMBI guidelines (Borja and Muxika, 2005). For application in coastal areas of Japan, we attempted to further assign the species that were observed frequently but not listed into ecological groups, as follows; (a) if all listed species in the taxon and the unlisted species were in the same ecological group, the unlisted species were assigned to that ecological group; (b) when there were some species assigned to different ecological groups in the taxon, including the unlisted species, the unlisted species were assigned to the same ecological group as species inhabiting sites with similar pollution disturbance levels to the unlisted species in previous studies (Conway et al., 1992; Matsuo et al., 2007; Uede, 2008; Tsujino et al., 2016). M-AMBI values were computed using Factor Analysis of AMBI, richness, and H’. Low AMBI and high M-AMBI values are indicative of high-quality bottom environments, whereas high AMBI and low MAMBI values indicate low-quality environments. The benthic communities are extremely varied due to the differences in natural conditions such as grain size and salinity. Therefore, reference conditions in the Seto Inland Sea were derived from the cluster analysis of sediment quality described by Nishijima et al. (2015). We set two reference conditions in Cluster 1 and Cluster 2–6 in the Seto Inland Sea for MAMBI analysis. Cluster 1 was characterized by high mud, TOC, and sulfide contents, negative ORP, and extremely small population size among clusters and differed significantly from those in other clusters (p < 0.01). Although the benthic communities were drastically changed in different salinity levels (freshwater, brackish water, and seawater species) according to Borja et al. (2008b) and Pelletier et al. (2018), the present study did not remove the salinity bias because the observation sites did not include the estuary in low salinity. ‘High’ status of the reference conditions of richness, H′, and AMBI in Cluster 1 and Cluster 2–6 were defined as 43, 4.44, and 0 for Cluster 1, and 66, 5.67, and 0 for Cluster 2–6 respectively, based on the maximum values obtained at the reference sites. ‘Bad’ status was defined as richness = 0, H’ = 0, and AMBI = 7. The threshold values for M-AMBI classification are as follows: ‘High’ status, > 0.77; ‘Good’, 0.53–0.77; ‘Moderate’, 0.39–0.53; ‘Poor’, 0.20–0.39; and ‘Bad’, < 0.20.
3.2. M-AMBI Fig. 3 shows the relationship between richness, Shannon's index (H′) and M-AMBI in the Seto Inland Sea. The stations with less than 6 number of individuals and 1–3 species per sample ranged from 0 to 5 and from 0 to 2.3, respectively. Therefore, the M-AMBI values in these sites were carefully checked for validation because the M-AMBI values would be low (approximately less than 0.3). The M-AMBI values were estimated for 384 out of 415 locations (92.5%). The low M-AMBI values were distributed in coastal regions including the inner part of the bays such as Osaka Bay (Fig. 4). In contrast, M-AMBI values tended to be high in straits and offshore areas including Iyo Nada. 3.3. Relationship between M-AMBI and sediment quality Pearson correlation coefficients between physico-chemical parameters of the sediment (water depth, sediment temperature, water content, TOC content, sulfide content, mud content, and ORP) and biotic indices (AMBI, M-AMBI, Richness, and H′), and in Cluster 1 and Cluster 2–6 are shown in Table 3. The result revealed a statistically significant correlation (p < 0.01) among biotic indices in each cluster region excluded between AMBI and H’ in Cluster 2–6 (r = −0.14). Most of the physico-chemical parameters of the sediment were significantly correlated with each other excluded sediment temperature in each cluster region. On the other hands, relatively high correlation between water depth and sediment temperature were obtained (Cluster 1, r = −0.54; Cluster 2–6, r = −0.74). The M-AMBI was significantly correlated with physico-chemical variables including water content (Cluster 1, r = −0.33; Cluster 2–6, r = -0.44), TOC content (Cluster 1, r = −0.33; Cluster 2–6, r = -0.42), sulfide content (Cluster 1, r = −0.27; Cluster 2–6, r = −0.28), ORP (Cluster 1, r = 0.39; Cluster 2–6, r = 0.41), and mud content (Cluster 1, n.s.; Cluster 2–6, r = −0.47).
3. Results 3.1. AMBI At 415 locations, 492 species or taxa were observed and 342 species or taxa (69.5%) were documented in the AMBI list. Based on our criteria, the endemic species Heteroplax transversa was assigned to the same ecological group as Eucrate crenata (G2) belonging to the same family (Euryplacidae). In this way, five unlisted species or taxa were classified in the present study (Table 1). The AMBI values were estimated for 384 of 415 locations (92.5%) and the estimated number of sites was not changed before and after the new assignment. Table 2 shows the five most common taxa of the macrobenthic animals in each ecological group observed in the Seto Inland Sea. Echinodermata (Synaptidae sp., Ophiophragmus japonicus, and Ophiuroidea sp.,) and Sipuncula (Apionsoma sp.) were observed only in G1 and G2 of stress-sensitive species. Annelida was observed among the five
Table 1 Appearance frequencies of the macrobenthos not listed in the AMBI list and their ecological group assignation. Superscripts (a and b) in the table indicate the classification methods for the ecological groups described in Materials and Methods. Phylum
Species or taxa
Appearance frequency (Number of sites)
Ecological groups used for this study
Arthropoda Hemichordata Arthropoda Mollusca Mollusca
Nippopisella nagatai Balanoglossida sp. Heteroplax transversa Solemya pusilla Leptomya sp.
56 49 26 21 11
G1b G1a G2b G3b G2a
69
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Table 2 Five most common macrobenthic species of each ecological group observed in the Seto Inland Sea. Ecological groups
1
2
3
4
5
G1
Maldanidae sp. AN (24.3/4.2) Glycera sp. AN (38.8/12.3) Nemertea sp. NE (45.8/6.2) Theora lubrica MO (15.7/33.4) Notomastus sp. AN (31.6/69.6)
Synaptidae sp. EC (22.2/2.6) Ophiophragmus japonicus EC (19.5/9.4) Callianassa sp. AR (16.9/2.4) Lumbrineris longifolia AN (11.3/23.6) Capitellidae sp. AN (10.6/25.8)
Apionsoma sp. SI (15.7/5.3) Lumbrineris sp. AN (18.8/10.9) Leptochela gracilis AR (10.6/2.2) Paraprionospio sp. (form B) AN (9.6/4.8) Capitella sp. AN (2.4/2.8)
Magelonidae sp. AN (14.0/1.7) Ophiuroidea sp. EC (16.1/7.6) Corophium sp. AR (9.9/4.0) Paraprionospio sp. (form CI) AN (8.0/4.1) Leiochrides sp. AN (1.0/0.8)
Nippopisella nagatai AR (13.5/3.1) Alpheus sp. AR (14.7/2.5) Spiophanes sp. AN (9.6/1.2) Chaetozone sp. AN (5.8/2.8) Nebalia japonensis AR (0.5/0.4)
G2 G3 G4 G5
AN, Annelida; AR, Arthropoda; MO, Mollusca; NE, Nemertea; EC, Echinodermata; SI, Sipuncula. ( ); Proportion of sites observed (%)/percentage of species to total densities in each group (%).
Fig. 2. Spatial distributions of ecological groups of the macrobenthos (G1 to G5). Plot size in the figures represent the proportions of each group in species composition. Dark plots in the distribution of G5 indicate that total percentage of Capitellidae sp. and Capitella sp. was more than 10% in species composition.
4. Discussion
respectively (Table 2). In the genus Capitella, Capitella teleta and Capitella capitata inhabit heavily organically enriched sediments throughout the world, and their population dynamics and application to bioremediation of enriched sediments have been investigated in previous studies (e.g. Tsutsumi, 1987; Ito et al., 2016). On the other hand, Capitella minima, which inhabits the coastal area of Japan (Imajima, 2015), was found in coarse sediment at a depth of 70 m in the Andaman Sea of the eastern Indian Ocean (Green, 2002), showing that the genus Capitella could include taxa outside of G5. In the Seto Inland Sea, locations with high percentages of Capitellidae sp. and Capitella sp. (more than 10% of the species composition) were mainly distributed in the eastern part of Suo Nada (Fig. 2). These sites (13 sites) were characterized by being relatively deep (36.0 ± 2.9 m, mean ± standard error (SE)), with low mud (41.8 ± 6.4%) and TOC (8.4 ± 1.3 mg g−1) contents. Fig. 5 shows the relationship between TOC content and percentage of Capitellidae sp. and Capitella sp. in the species composition. These taxa were distributed not only in sediments with high TOC contents, but also in low-TOC sediments (5–10 mg g−1), indicating the presence of stress-sensitive Capitellidae and Capitella species in this area. According to Pitacco et al. (2018), the benthic community showed
4.1. Ecological groups In the present study, five unlisted species or taxa were assigned to ecological groups (see section 2.3, Data analysis). In the Seto Inland Sea, 69.5% of species or taxa were assigned to an ecological group, and 92.5% in all sites were successfully analyzed. Muniz et al. (2005) reported that the mean percentage of organisms not assigned to an ecological group was 0.6–6.9% at five locations in coastal South America, and AMBI values were successfully calculated for all sites investigated, with the addition of 20 species that were typically found in South Atlantic coastal regions. In the tropical Southwest Indian Ocean, 150 out of 242 taxa (62.0%) were unlisted in the AMBI program, and most of the unassigned taxa (except for 18 taxa, including those inhabiting in tropical areas) were assigned to an ecological group in the study by Bigot et al. (2008). Capitellidae sp. and Capitella sp. were assigned to G5 in the current species list (June 2017), and accounted for 25.8% and 2.8% of taxon density as a percentage of total density in G5 and the Seto Inland Sea, 70
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
4.2. Factors determining M-AMBI and sediment quality Nishijima et al. (2015) investigated the sediments at the same monitoring sites used in this study in the Seto Inland Sea, in terms of their physico-chemical properties (water depth, sediment temperature, mud content, TOC content, ORP, and sulfide content), using cluster analysis. Their study revealed that physico-chemical variables, especially TOC and mud content, influenced macrobenthic population size and biodiversity. Therefore, we evaluated the relationship of M-AMBI not only with a single physico-chemical parameter of the sediment, but also with comprehensive sediment quality as the clusters provided by Nishijima et al. (2015) (Fig. 6). The TOC contents, mud contents, Richness, H′, AMBI, and M-AMBI values in each cluster were compared among the clusters using a 1-way ANOVA and the Tukey–Kramer test. The result shows the significant differences between Cluster 1, Cluster 2–4, and Cluster 5–6 in TOC contents and mud contents (p < 0.05). On the other hands, the pattern similar to TOC and mud contents was not observed in Richness, H’, and AMBI, although Cluster 1 was significantly different from other clusters. In M-AMBI, Cluster 2–4 and Cluster 5–6 were significantly different, and the mean value in Cluster 1 was extremely low compared to the other clusters. This could suggest that the difference in the M-AMBI pattern is similar to the physicochemical parameters of the sediment, including TOC and mud contents, although Cluster 1 could not be directly compared because of the different reference conditions between Cluster 1 and Cluster 2–6. The sites that were classified into organically enriched Cluster 1, with high TOC (17.4 ± 0.5 mg g−1) and mud (90.4 ± 2.5%), accounted for 44% of all sites and were mainly located in three bays (Osaka Bay, Hiroshima Bay, and Beppu Bay) and Hiuchi Nada. These sites had significantly high AMBI and low M-AMBI values in the present study (Figs. 4 and 6). Conversely, more than 50% of the sites in Bisan Seto, Aki Nada, Iyo Nada, and Bungo Channel were characterized by unpolluted sandy sediment (Clusters 2–4; 26% of all sites) according to Nishijima et al. (2015) and were assigned high M-AMBI values (Bisan Seto, 0.55 ± 0.032; Aki Nada, 0.72 ± 0.026; Iyo Nada, 0.57 ± 0.013; Bungo Channel, 0.58 ± 0.027), corresponding to Good status. The mean M-AMBI values in secondarily enriched Clusters 5 and 6 were 0.51 ± 0.011 and 0.51 ± 0.023, respectively, corresponding to Moderate status. High status was assigned to ten locations based on M-AMBI classification, which were mainly distributed in Aki Nada (5 sites). Most of the sites were classified as Good (122 sites), Moderate (103 sites), or Poor status (102 sites). 47 sites were classified as Bad status, which was located in coastal regions such as the heavily polluted inner Osaka Bay (Tsujimoto et al., 2008). Locations with better than Moderate status
Fig. 3. Relationships between richness, Shannon's index (H′), and M-AMBI values. The triangles in the figure indicate the stations with the number of individuals were less than 6 and 1–3 species per sample.
a very weak response to chemical contamination such as heavy metals and polycyclic aromatic hydrocarbons (PAHs) in a coastal lagoon in Italy during the 11 year-study period. In the Seto Inland Sea, heavy metals accumulated in the surface sediment (0–2 cm), and high contents were detected in inner Osaka Bay, northern Harima Nada, and inner Hiroshima Bay during 1991–1994 (Komai et al., 1998). Nagaoka et al. (2004) reported that the mean Pb content (Mean, 57.8 μg g−1; Min-Max, 15.6–94.6 μg g−1) in the surface sediment (0–5 cm) in Osaka Bay in 2000 was approximately twice as high as that of the coastal lagoon in Italy (Mean; 21 mg kg−1) (Pitacco et al., 2018), and showed high correlation between heavy metals (Hg, Cd, Cu, Zn, Pb, Ni, Mn, Cr, Fe) and mud contents. These results suggested the possibility that not only the organic pollution, but also chemical contamination such as heavy metals influenced the distribution of Capitellidae and Capitella species. In any case, G5 was assigned the highest weighting coefficient of 6 in the calculation process of biotic coefficients following AMBI value determination in the AMBI program (Borja et al., 2000). Therefore, if the assignment of G5 changed, the calculated AMBI value would also change. However, the impact of such a change on the results could be small due to the low frequency of Capitellidae sp. and Capitella sp. in the case of the Seto Inland Sea.
Fig. 4. Spatial distribution of M-AMBI values. 71
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Table 3 Pearson correlation coefficients between physico-chemical parameters of the sediment and biotic indices in two regions (Cluster 1 and Cluster 2–6) of the Seto Inland Sea. Bold numbers are significant at p < 0.01. Cluster 1 AMBI M-AMBI Richness H′ Depth Temp. W.C. TOC Sulfide Mud ORP Cluster 2-6 AMBI M-AMBI Richness H′ Depth Temp. W.C. TOC Sulfide Mud ORP
AMBI
M-AMBI
Richness
H′
Depth
Temp.
W.C.
TOC
Sulfide
Mud
−0.79 −0.45 −0.72 −0.06 −0.04 0.24 0.35 0.33 0.04 −0.42
0.87 0.96 −0.04 0.08 −0.33 −0.33 −0.27 −0.19 0.39
0.77 −0.12 0.10 −0.33 −0.29 −0.15 −0.23 0.28
−0.02 0.06 −0.29 −0.26 −0.26 −0.19 0.36
−0.54 −0.27 −0.18 −0.37 −0.31 0.31
−0.15 −0.18 0.12 0.08 −0.01
0.75 0.30 0.50 −0.41
0.42 0.48 −0.40
0.22 −0.64
−0.09
AMBI
M-AMBI
Richness
H′
Depth
Temp.
W.C.
TOC
Sulfide
Mud
−0.60 −0.28 −0.14 −0.11 −0.11 0.39 0.35 0.19 0.29 −0.29
0.88 0.81 0.17 0.04 −0.44 −0.42 −0.28 −0.47 0.41
0.69 0.06 0.11 −0.37 −0.38 −0.25 −0.45 0.39
0.23 −0.14 −0.25 −0.25 −0.21 −0.33 0.26
−0.74 −0.18 −0.31 −0.32 −0.29 0.38
−0.06 0.08 0.27 0.04 −0.14
0.74 0.41 0.74 −0.65
0.47 0.80 −0.72
0.45 −0.59
−0.75
ORP
ORP
been implemented by the application of the TPLCS since 1979. Consequently, chlorophyll a concentrations and primary productions of the water in coastal regions have been decreasing since 1981 (Nishijima et al., 2016; Nakai et al., 2018). Therefore, the benthic ecosystems including the sediment quality and benthic communities would be changing with time due to the recovery of the water quality. To clarify the response of the benthic environment, a comprehensive index representing the benthic ecosystems is needed, and the M-AMBI would be a suitable for use in the coastal waters of Japan.
5. Conclusions This study aims to assess benthic quality using the M-AMBI and macrobenthic data collected in the Seto Inland Sea during 2001–2005 by MOE. The M-AMBI values were compared to the physico-chemical parameters of the sediment for evaluation of the applicability of the index in the coastal areas of Japan. The conclusions obtained were as follows:
Fig. 5. Relationship between TOC contents and percentages of Capitellidae sp. and Capitella sp. in species composition. Stations with non-appearance of these taxa (0%) were removed.
were mainly distributed from the Bungo Channel, which is strongly affected by the open sea, to Aki Nada in the eastern part of the Seto Inland Sea. Moreover, locations with better than Moderate status were observed near straits such as Bisan Seto and Akashi Strait, which is located between northeastern Harima Nada and northwestern Osaka Bay (Fig. 1). Thus, the distribution pattern of the M-AMBI depended on geographic features and the strength of anthropogenic stress, much greater than did AMBI. Osaka Bay and Bisan Seto are the areas receiving the highest COD and nutrient loads from land in the Seto Inland Sea. For example, Osaka Bay and Bisan Seto received 81 and 55 kg COD km−2 d−1, respectively, whereas other areas received 8–42 kg COD km−2 d−1. Nevertheless, Bisan Seto and Akashi Strait, which are connected to Osaka Bay, showed high M-AMBI values. Bisan Seto and Akashi Strait are characterized as areas with high tidal currents, as is Aki Nada, while Osaka Bay is not (Matsuura et al., 2006). Therefore, the distributions of M-AMBI and sediment quality are controlled not only by anthropogenic pollution, but also by physical forces driven by the geographical features of each region. Because, higher current speed would be produce better dispersion and dilution of pollutants and organic matters, thereby increasing the quality of the area (Borja et al., 2009; Orita et al., 2015). The reduction of the nutrient loading to the Seto Inland Sea has
(1) In the Seto Inland Sea, 69.5% of species or taxa were assigned to an ecological group, and 92.5% in all sites were successfully analyzed using the AMBI program. (2) Capitellidae and Capitella species assigned to G5 in the current species list (June 2017) observed were distributed not only in sediments with high TOC contents, but also in low-TOC sediments in the Seto Inland Sea. (3) M-AMBI would be a useful biotic index in Japanese coasts owing to representation of the comprehensive sediment quality.
Acknowledgments We would like to express our gratitude to the Ministry of the Environment, Japan, for supplying data from their investigation of the Seto Inland Sea. This research was supported by the Environment Research and Technology Development Fund (S-13) granted by the Ministry of the Environment. We acknowledge Dr. Joana Patrício of the European Commission and Dr. Ángel Borja of AZTI・Marine Research Division for valuable advices. We express our gratitude to Dr. Cervinia V. Manalo for her English language proofreading. 72
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Fig. 6. Mean values of (a) TOC and (b) Mud contents in the surface sediments and biotic indices including (c) Richness, (d) H′, (e) AMBI, and (f) M-AMBI in six clusters reported by Nishijima et al. (2015). Different letters indicate significant differences among clusters (Tukey–Kramer test, p < 0.05). Error bars show the standard error (SE).
Appendix A. Supplementary data
human pressures? Mar. Pollut. Bull. 97, 85–94. Borja, Á., Elliott, M., Andersen, J.H., Berg, T., Carstensen, J., Halpern, B.S., Heiskanen, A.S., Korpinen, S., Stewart Lowndes, J.S., Martin, G., Rodriguez-Ezpeleta, N., 2016. Overview of integrative assessment of marine systems: the ecosystem approach in practice. Front. Mar. Sci. 3, 1–20. Conway, N.M., Howes, B.L., McDowell Capuzzo, J.E., Turner, R.D., Cavanaugh, C.M., 1992. Characterization and site description of Solemya borealis (Bivalvia: Solemyidae), another bivalve-bacteria symbiosis. Mar. Biol. 112, 601–613. Dauer, D.M., 1993. Biological criteria, environmental health and estuarine macrobenthic community structure. Mar. Pollut. Bull. 26, 249–257. Díaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929. Díaz, R.J., Solan, M., Valente, R.M., 2004. A review of approaches for classifying benthic habitats and evaluating habitat quality. J. Environ. Manage. 73, 165–181. Duarte, C.M., Borja, Á., Carstensen, J., Elliott, M., Krause-Jensen, D., Marbà, N., 2015. Paradigms in the recovery of estuarine and coastal ecosystems. Est. Coast. 38, 1202–1212. European Commission, 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. Off. J. Eur. Union L327, 1–72. European Commission, 2008. Directive 2008/56/EC of the European Parliament and of the Council establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Off. J. Eur. Union L164, 19–40. Green, K.D., 2002. Capitellidae (Polychaeta) from the Andaman Sea, vol. 24. Phuket Marine Biological Center Special Publication, pp. 249–343. Imajima, M., 2015. Kankeidoubutsu Tamourui IV (Annelida, Polychaeta). Seibutsu Kenkyusha Co., Ltd., Tokyo, pp. 530 in Japanese. Islam, M.S., Tanaka, M., 2004. Impact of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar. Pollut. Bull. 48, 624–649. Ito, M., Ito, K., Ohta, K., Hano, T., Onduka, T., Mochida, K., Fujii, K., 2016. Evaluation of bioremediation potential of three benthic annelids in organically polluted marine sediment. Chemosphere 163, 392–399. Japan River Association, 2018. River in Japan (in Japanese). (Available on line at. http://www.japanriver.or.jp/river_law/kasenzu/chugoku_zu/chugoku_zu.htm. Kemp, W.M., Testa, J.M., Conley, D.J., Gilbert, D., Hagy, J.D., 2009. Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6, 2985–3008. Komai, Y., Kobuke, Y., Seiki, T., Nagafuchi, O., Murakami, K., Koyama, T., Kakibaya, T., 1998. Distribution of heavy metals and its change in the sediment of the Seto Inland Sea. J. Jpn. Soc. Water Environ. 21, 743–750 in Japanese. Kronvang, B., Jeppesen, E., Conley, D.J., Søndergaard, M., Larsen, S.E., Ovesen, N.B.,
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marenvres.2019.05.007. References Bigot, L., Grémare, A., Amouroux, J.M., Frouin, P., Maire, O., Gaertner, J.C., 2008. Assessment of the ecological quality status of soft-bottoms in Reunion Island (tropical Southwest Indian Ocean) using AZTI marine biotic indices. Mar. Pollut. Bull. 56, 704–722. Birk, S., Bonne, W., Borja, Á., Brucetm, S., Courratm, A., Poikane, S., Solimini, S., van de Bund, W., Zampoukas, N., Hering, D., 2012. Three hundred ways to assess Europe's surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecol. Indic. 18, 31–41. Borja, Á., Franco, J., Pérez, V., 2000. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 40, 1100–1114. Borja, Á., Muxika, I., 2005. Guidelines for the use of AMBI (AZTI's Marine Biotic Index) in the assessment of the benthic ecological quality. Mar. Pollut. Bull. 50, 787–789. Borja, Á., Bricker, S.B., Dauer, D.M., Demetriadis, N.T., Ferreira, J.G., Forbes, A.T., Hutchings, P., Jia, X., Kenchington, R., Marques, J.C., Zhu, C., 2008a. Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. Mar. Pollut. Bull. 56, 1519–1537. Borja, Á., Dauer, D.M., Díaz, R., Llansó, R.J., Muxika, I., Rodríguez, J.G., Schaffner, L., 2008b. Assessing estuarine benthic quality conditions in Chesapeake Bay: a comparison of three indices. Ecol. Indic. 8, 395–403. Borja, Á., Rodríguez, J.G., Black, K., Bodoy, A., Emblow, C., Fernandes, T.F., Forte, J., Karakassis, I., Muxika, I., Nickell, T.D., Papageorgiou, N., Pranovi, F., Sevastou, K., Tomassetti, P., Angel, D., 2009. Assessing the suitability of a range of benthic indices in the evaluation of environmental impact of fin and shellfish aquaculture located in sites across Europe. Aquaculture 293, 231–240. Borja, Á., Dauer, D.M., Elliott, M., Simenstad, 2010a. Medium- and long-term recovery of estuarine and coastal ecosystems: patterns, rates and restoration effectiveness. Est. Coast. 33, 1249–1260. Borja, Á., Elliott, M., Carstensen, J., Heiskanen, A.S., van de Bund, W., 2010b. Marine management - towards an integrated implementation of the European marine Strategy framework and the water framework directives. Mar. Pollut. Bull. 60, 2175–2186. Borja, Á., Marín, S.L., Muxika, I., Pino, L., Rodríguez, J.G., 2015. Is there a possibility of ranking benthic quality assessment indices to select the most responsive to different
73
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Seto Inland Sea Japan, exposed to anthropogenic nutrient loading. Sci. Total Environ. 571, 543–550. Orita, R., Umehara, A., Komorita, T., Choi, J.W., Montani, S., Komatsu, T., Tsutsumi, H., 2015. Contribution of the development of the stratification of water to the expansion of dead zone: a sedimentological approach. Est. Coast. Shelf Sci. 164, 204–213. Pelletier, M.C., Gillett, D.J., Hamilton, A., Grayson, T., Hansen, V., Leppo, E.W., Weisberg, S.B., Borja, A., 2018. Adaptation and application of multivariate AMBI (M-AMBI) in US coastal waters. Ecol. Indic. 89, 818–827. Pitacco, V., Mistri, M., Ferrari, C.R., Munari, C., 2018. Heavy metals, OCPs, PAHs, and PCDD/Fs contamination in surface sediments of a coastal lagoon (Valli di Comacchio, NW Adriatic, Italy): long term trend (2002−2013) and effect on benthic community. Mar. Pollut. Bull. 135, 1221–1229. Tsujimoto, A., Yasuhara, M., Nomura, R., Yamazaki, H., Sampei, Y., Hirose, K., Yoshikawa, S., 2008. Development of modern benthic ecosystems in eutrophic coastal oceans: the foraminiferal record over the last 200 years, Osaka Bay, Japan. Mar. Micropaleontol. 69, 225–239. Tsujino, M., Abo, K., Tarutani, K., 2016. The bottom environment and macrobenthic community of Osaka Bay, Japan in 2003 and 2011. Nippon Suisan Gakkaishi 82, 330–341 (in Japanese with English abstract). Tsutsumi, H., 1987. Population dynamics of Capitella capitata (Polychaeta; Capitellidae) in an organically polluted cove. Mar. Ecol. Prog. Ser. 36, 139–149. Uede, T., 2008. Validity of acid volatile sulfide as environmental index and experiment for fixing its standard value in aquaculture farms along the coast of Wakayama Prefecture, Japan. Nippon Suisan Gakkaishi 74, 402–411 (in Japanese with English abstract). Verdonschot, P.F.M., Spears, B.M., Feld, C.K., Brucet, S., Keizer-Vlek, H., Borja, Á., Elliott, M., Kernan, M., Johnson, R.K., 2013. A comparative review of recovery processes in rivers, lakes, estuarine and coastal waters. Hydrobiologia 704, 453–474. Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke, C., Halpern, B.,S., Jackson, J.B.C., Lotze, H.K., Micheli, F., Palumbi, S.R., Sala, E., Selkoe, K.A., Stachowicz, J.J., Watson, R., 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790.
Carstensen, J., 2005. Nutrient pressures and ecological responses to nutrient loading reductions in Danish streams, lakes and coastal waters. J Hydrol 304, 274–288. Matsuo, M., Sudo, H., Azuma, M., Kondo, H., Tamaki, A., 2007. Division substrate groups and gammaridean amphipod assemblages in sublittoral Ariake Sound-a comparison between 1997 and 2002. Bull. Fac. Fish. Nagasaki Univ. 88, 1–42 in Japanese with English abstract. Matsuura, N., Sasaki, T., Suzuyama, H., Kuwakino, F., Nagashima, H., 2006. High accuracy tidal current Forecasting on the basis of harmonic analysis of model Simulation in the Seto Inland Sea. J. Jpn Soc. Mar. Surv. Technol. 18, 1–10 (in Japanese with English abstract). Ministry of the Environment, Japan, 2001. Sediment test method (in Japanese). (Available on line at. http://db-out.nies.go.jp/emdb/pdfs/water/teisitutyousa/ 0103teisitutyousahouhou.pdf. Muniz, P., Venturini, N., Pires-Vanin, A.M.S., Tommasi, L.R., Borja, Á., 2005. Testing the applicability of a marine biotic index (AMBI) to assessing the ecological quality of soft- bottom benthic communities, South America Atlantic region. Mar. Pollut. Bull. 50, 624–637. Murakami, K., Imatomi, Y., Komai, Y., Nagafuchi, O., Seiki, T., Koyama, T., 1998. Relationship between distribution of Annelida and sediment condition in the Seto Inland Sea. J. Jpn. Soc. Water Environ. 21, 757–764 (in Japanese with English abstract). Nagaoka, C., Yamamoto, Y., Eguchi, S., Miyazaki, N., 2004. Relationship between distribution of heavy metals and sedimental condition in the sediment of Osaka Bay. Nippon Suisan Gakkaishi 70, 159–167 (in Japanese). Nakai, S., Soga, Y., Sekito, S., Umehara, A., Okuda, T., Ohno, M., Nishijima, W., Asaoka, S., 2018. Historical changes in primary production in the Seto Inland Sea, Japan, after implementing regulations to control the pollutant loads. Water Pol. 20, 855–870. Nishijima, W., Umehara, A., Okuda, T., Nakai, S., 2015. Variations in macrobenthic community structures in relation to environmental variables in the Seto Inland Sea, Japan. Mar. Pollut. Bull. 92, 90–98. Nishijima, W., Umehara, A., Sekito, S., Okuda, T., Nakai, S., 2016. Spatial and temporal distributions of Secchi depths and chlorophyll a concentrations in the Suo Nada of the
74
Contents lists available at ScienceDirect
Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev
Benthic quality assessment using M-AMBI in the Seto Inland Sea, Japan a,∗
b
c
a
Akira Umehara , Satoshi Nakai , Tetsuji Okuda , Masaki Ohno , Wataru Nishijima a b c
T
a
Environmental Research and Management Center, Hiroshima University, 1-5-3 Kagamiyama, Higashi-hiroshima, Hiroshima, 739-8513, Japan Graduate School of Science and Engineering, Hiroshima University, 1-4-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8527, Japan Department of Environmental Solution Technology, Faculty of Science and Technology, Ryukoku University, 1-5 Yokoya, Seta Oe-cho, Otsu, Shiga, 520-2194, Japan
A R T I C LE I N FO
A B S T R A C T
Keywords: Biotic index Coastal management Ecological status Enclosed sea Macrobenthos
Benthic invertebrates that inhabit the seafloor respond to anthropogenic and natural stresses, and are good indicators for assessing the benthic ecological status. We evaluated the ecosystem health of the Seto Inland Sea based on the multivariate AZTI Marine Biotic Index (M-AMBI), being its first application in a Japanese coastal sea with numerous endemic species. From the 415 locations studied, we were able to use M-AMBI in 384 sites (92.5% in all sites). The result revealed a statistically significant correlation among biotic indices including AMBI, M-AMBI, Richness, and H’ (p < 0.01). Most of the physico-chemical parameters of the sediment (water content, total organic carbon (TOC) content, sulfide content, mud content, and oxidation–reduction potential (ORP)) were significantly correlated with each other excluding sediment temperature. The M-AMBI was significantly correlated with physico-chemical variables including water content, TOC content, sulfide content, and ORP. We found that the sites classified into the organically enriched cluster, and having high contents of TOC, mud, and sulfide and negative ORP, corresponded with sites that had significantly low M-AMBI values (bad-poor ecological status). Conversely, sites in the unpolluted sandy cluster were assigned high M-AMBI values (highgood ecological status). Therefore, M-AMBI would be a useful biotic index in Japanese coasts due to the representation of the comprehensive sediment quality.
1. Introduction
importance of biological indicators has been emphasised in legislation around the world (Borja et al., 2008a), and especially in Europe, under the Water Framework Directive (WFD, European Commission, 2000) and the Marine Strategy Framework Directive (MSFD, European Commission, 2008), which have resulted in multiple indices to assess the status of marine waters (Birk et al., 2012; Borja et al., 2016). In shallow coastal areas, anthropogenic impacts arising mostly from land affect both pelagic and benthic ecosystems, which are also strongly interrelated. Compared with the pelagic environment, the negative effects of these anthropogenic impacts can remain present in coastal areas for a long time after removal of the impacts (Borja et al., 2010a; Verdonschot et al., 2013; Duarte et al., 2015). Although dilution and dispersion were important natural phenomenon that reduces the concentrations of pollutants in the environment, it was insufficient for reducing concentrations in the sediment; therefore, hazardous trace contaminants, such as heavy metals and persistent organic pollutants, could easily remain in sediments (Pitacco et al., 2018). Benthic invertebrates provide useful indicators for assessing the environment of these contaminated sediments. Many ecological status indices were calculated based on the macrobenthic community structure, including the Benthic Condition Index,
Rapid industrial development, urbanization, and increased tourism have had deleterious impacts on coastal marine ecosystems over the last four decades (Islam and Tanaka, 2004). In coastal areas, the frequency, magnitude and geographic extent of red tides and hypoxia have increased, and fisheries have declined throughout the world (Worm et al., 2006; Díaz and Rosenberg, 2008). Many efforts have been made to restore these deteriorated ecological conditions, including the reduction of anthropogenic impacts such as excessive nutrient loads (Kronvang et al., 2005; Kemp et al., 2009). Environmental management should include an assessment of the present conditions of the environment (Borja et al., 2010b). Physicochemical and biological water and sediment parameters are generally analyzed and assessed. An ecological approach based on biological indicators with different sensitivities to environmental stress is an effective tool for assessing the environment. Hence, Dauer (1993) noted the importance of biological indicators, as (1) they constitute direct measures of the condition of the biota, (2) they may uncover problems that were undetected or underestimated through other methods, and (3) they allow assessment of the progress of restoration efforts. The
∗
Corresponding author. E-mail address: [email protected] (A. Umehara).
https://doi.org/10.1016/j.marenvres.2019.05.007 Received 17 December 2018; Received in revised form 7 May 2019; Accepted 7 May 2019 Available online 11 May 2019 0141-1136/ © 2019 Elsevier Ltd. All rights reserved.
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Fig. 1. Investigation sites in the Seto Inland Sea, Japan. Samples of the sediments and macrobenthos were collected by the Ministry of the Environment during summer 2001–2005. Curved lines on the land in the figure show the large rivers that the annual averaged discharge were more than 10 m3 s−1 (Japan River Association, 2018).
parameters of the sediments, we expect a more accurate understanding of environmental conditions to be achieved. In the present study, benthic quality assessment was conducted using the M-AMBI with macrobenthos data collected in the Seto Inland Sea during 2001–2005 by MOE. For evaluation of the applicability of the index in coastal areas of Japan, the M-AMBI values were compared to physico-chemical parameters of the sediment.
North Carolina Biotic Index (NCBI), AZTI Marine Biotic Index (AMBI), Benthic Quality Index, and Multivariate AZTI Marine Biotic Index (MAMBI) (Díaz et al., 2004; Borja et al., 2015). These indices are constructed based on information about the sensitivity of macrobenthos to an environmental stress gradient, and serve as tools for evaluation of the health of benthic ecosystems. These indices have been applied in many regions, including European estuarine and coastal environments, the Atlantic region, and the Indian Ocean (Borja et al., 2015; Pitacco et al., 2018). Japan is an island country with many endemic species, which limits the effective application of the indices. To date, no evaluation of ecological quality using AMBI and M-AMBI has been conducted in Japan. The Seto Inland Sea is the largest semi-enclosed coastal sea in Japan (23,203 km2). This sea is located in the western part of Japan and is connected to the Pacific Ocean via its western and eastern channels (Fig. 1). In the Seto Inland Sea, policies for reduction of organic matter and nutrient loads from land have been enforced since the period of high economic growth in the 1950s–70s, namely the Water Pollution Control Law (1970) and the Law Concerning Special Measures for Conservation of the Environment of the Seto Inland Sea (1973). Since 1979, Total Pollutant Load Control System (TPLCS) has been implemented (http://www.env.go.jp/en/water/ecs/guidance_tplcs_ summary.pdf), and the pollutant loads including chemical oxygen demand (COD), total nitrogen, and total phosphorus from lands have been reduced. The pollutant load sources include not only industrial effluent, but also household discharge, agricultural wastewater and so on. Consequently, the TPLCS has successfully prevented the increase in the total discharge of pollutant, and the deterioration of water quality has been brought under control, with some evidence of water quality improvement, such as the reduced number of occurrences of red tide. Although the relationship between the sediment quality and distribution of Annelida was studied by Murakami et al. (1998), the sediment quality and macrobenthic community structure of the Seto Inland Sea have not been thoroughly characterized. Therefore, Nishijima et al. (2015) attempted to characterize the macrobenthic community structure in sediments using cluster analysis based on physico-chemical parameters of the sediments. Large-scale monitoring data (425 sites) related to sediment quality and macrobenthos populations in the Seto Inland Sea during 2001–2005, collected by the Ministry of the Environment (MOE) were used. The monitoring sites were located throughout the whole sea to provide a representative dataset with high spatial resolution. It was revealed that important parameters, such as total organic carbon (TOC) and mud contents, influence macrobenthic population size and biodiversity, and identified the typical macrobenthos in the clusters representing organically enriched or un-enriched sediments. On the other hand, no assessment of benthic invertebrates from each region in the Seto Inland Sea has been conducted. If biotic indices such as M-AMBI are used along with physico-chemical
2. Materials and methods 2.1. Study area The Seto Inland Sea is a shallow enclosed coastal sea (mean depth ca. 38 m; water volume ca. 816 km3) divided into 13 sub-areas based on geographical and topographical features (Fig. 1). Each sub-area has a different degree of closure and unique environmental conditions. Sampling of sediments and macrobenthos was carried out by MOE at 415 locations in the Seto Inland Sea during the summers (July–August) of 2001–2005. 2.2. Sample collection and analysis Samples for assessing the physico-chemical parameters of the sediment (water depth, sediment temperature, grain size, TOC, oxidation–reduction potential (ORP), and sulfide content) and macrobenthos were collected from the sediment surface using a Smith-McIntyre grab sampler (0.1 m2). The number of replicates for the physico-chemical parameters of the sediment and macrobenthos were three and two, respectively. Sediment analysis was carried out according to the sediment test method (Ministry of the Environment, 2001). Details of the analyses of sediment and macrobenthos were provided in Nishijima et al. (2015). After removal of carbonates from the sample with 2 N HCl, TOC content of the dried sediment was determined with an elemental analyzer. The grain size composition (pebble, > 2.0 mm; sand, 0.063–2.0 mm; mud, < 0.063 mm) of the sediment was determined using the wet sieving method. Sulfide content was defined as the amount of hydrogen sulfide produced under acidic conditions, which was determined using a Hydrotec-s kit (Gastec Corp.). The samples for macrobenthos were fixed with 10% formalin or 70% alcohol on the ship. In the laboratory, macrobenthos were identified to the species or the lowest possible taxon, and counted. 2.3. Data analysis Soft-bottom macrobenthos were analyzed using the AMBI program (http://ambi.azti.es, v.5.0, species list updated in June 2017), and biotic indices such as richness (number of species or taxa), ShannonWiener diversity (H’), AMBI, and M-AMBI were calculated. We carefully 68
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
most common taxa in all ecological groups. All species or taxa that were among the five most common taxa of the G4 and G5 groups (opportunistic species) fell into the Annelida, except for the pollution indicator, Theora lubrica, Mollusca (15.7% in all sites) and Nebalia japonensis, Arthropoda (0.5%). Although Capitellidae sp. (10.6%), and Capitella sp. (2.4%) were observed at only a small number of sites, they accounted for 25.8% and 2.8%, respectively, of the taxon density relative to total density in G5. The spatial distributions of each ecological group (G1–5) of macrobenthos in Seto Inland Sea are shown in Fig. 2. G1, G2, and G3 tended to dominate the offshore area. In contrast, G4, consisting of secondorder opportunistic species, tended to inhabit coastal regions strongly affected by anthropogenic stresses. Typical regions inhabited by G4 were the enclosed Osaka Bay, where G4 species or taxa dominated > 50% of the macrobenthos sampled in 12 out of 29 sites. G5 consisted of first-order opportunistic species, which were observed at 163 out of 384 total sites (42.4%), and sites at which the combined percentage of Capitellidae sp. and Capitella sp. accounted for more than 10% of the species composition were mainly distributed in eastern region of Suo Nada.
checked the AMBI values of the sites with low richness, low density, or with non-listed species more than 20% of the total in physically stressed areas, according to the AMBI guidelines (Borja and Muxika, 2005). For application in coastal areas of Japan, we attempted to further assign the species that were observed frequently but not listed into ecological groups, as follows; (a) if all listed species in the taxon and the unlisted species were in the same ecological group, the unlisted species were assigned to that ecological group; (b) when there were some species assigned to different ecological groups in the taxon, including the unlisted species, the unlisted species were assigned to the same ecological group as species inhabiting sites with similar pollution disturbance levels to the unlisted species in previous studies (Conway et al., 1992; Matsuo et al., 2007; Uede, 2008; Tsujino et al., 2016). M-AMBI values were computed using Factor Analysis of AMBI, richness, and H’. Low AMBI and high M-AMBI values are indicative of high-quality bottom environments, whereas high AMBI and low MAMBI values indicate low-quality environments. The benthic communities are extremely varied due to the differences in natural conditions such as grain size and salinity. Therefore, reference conditions in the Seto Inland Sea were derived from the cluster analysis of sediment quality described by Nishijima et al. (2015). We set two reference conditions in Cluster 1 and Cluster 2–6 in the Seto Inland Sea for MAMBI analysis. Cluster 1 was characterized by high mud, TOC, and sulfide contents, negative ORP, and extremely small population size among clusters and differed significantly from those in other clusters (p < 0.01). Although the benthic communities were drastically changed in different salinity levels (freshwater, brackish water, and seawater species) according to Borja et al. (2008b) and Pelletier et al. (2018), the present study did not remove the salinity bias because the observation sites did not include the estuary in low salinity. ‘High’ status of the reference conditions of richness, H′, and AMBI in Cluster 1 and Cluster 2–6 were defined as 43, 4.44, and 0 for Cluster 1, and 66, 5.67, and 0 for Cluster 2–6 respectively, based on the maximum values obtained at the reference sites. ‘Bad’ status was defined as richness = 0, H’ = 0, and AMBI = 7. The threshold values for M-AMBI classification are as follows: ‘High’ status, > 0.77; ‘Good’, 0.53–0.77; ‘Moderate’, 0.39–0.53; ‘Poor’, 0.20–0.39; and ‘Bad’, < 0.20.
3.2. M-AMBI Fig. 3 shows the relationship between richness, Shannon's index (H′) and M-AMBI in the Seto Inland Sea. The stations with less than 6 number of individuals and 1–3 species per sample ranged from 0 to 5 and from 0 to 2.3, respectively. Therefore, the M-AMBI values in these sites were carefully checked for validation because the M-AMBI values would be low (approximately less than 0.3). The M-AMBI values were estimated for 384 out of 415 locations (92.5%). The low M-AMBI values were distributed in coastal regions including the inner part of the bays such as Osaka Bay (Fig. 4). In contrast, M-AMBI values tended to be high in straits and offshore areas including Iyo Nada. 3.3. Relationship between M-AMBI and sediment quality Pearson correlation coefficients between physico-chemical parameters of the sediment (water depth, sediment temperature, water content, TOC content, sulfide content, mud content, and ORP) and biotic indices (AMBI, M-AMBI, Richness, and H′), and in Cluster 1 and Cluster 2–6 are shown in Table 3. The result revealed a statistically significant correlation (p < 0.01) among biotic indices in each cluster region excluded between AMBI and H’ in Cluster 2–6 (r = −0.14). Most of the physico-chemical parameters of the sediment were significantly correlated with each other excluded sediment temperature in each cluster region. On the other hands, relatively high correlation between water depth and sediment temperature were obtained (Cluster 1, r = −0.54; Cluster 2–6, r = −0.74). The M-AMBI was significantly correlated with physico-chemical variables including water content (Cluster 1, r = −0.33; Cluster 2–6, r = -0.44), TOC content (Cluster 1, r = −0.33; Cluster 2–6, r = -0.42), sulfide content (Cluster 1, r = −0.27; Cluster 2–6, r = −0.28), ORP (Cluster 1, r = 0.39; Cluster 2–6, r = 0.41), and mud content (Cluster 1, n.s.; Cluster 2–6, r = −0.47).
3. Results 3.1. AMBI At 415 locations, 492 species or taxa were observed and 342 species or taxa (69.5%) were documented in the AMBI list. Based on our criteria, the endemic species Heteroplax transversa was assigned to the same ecological group as Eucrate crenata (G2) belonging to the same family (Euryplacidae). In this way, five unlisted species or taxa were classified in the present study (Table 1). The AMBI values were estimated for 384 of 415 locations (92.5%) and the estimated number of sites was not changed before and after the new assignment. Table 2 shows the five most common taxa of the macrobenthic animals in each ecological group observed in the Seto Inland Sea. Echinodermata (Synaptidae sp., Ophiophragmus japonicus, and Ophiuroidea sp.,) and Sipuncula (Apionsoma sp.) were observed only in G1 and G2 of stress-sensitive species. Annelida was observed among the five
Table 1 Appearance frequencies of the macrobenthos not listed in the AMBI list and their ecological group assignation. Superscripts (a and b) in the table indicate the classification methods for the ecological groups described in Materials and Methods. Phylum
Species or taxa
Appearance frequency (Number of sites)
Ecological groups used for this study
Arthropoda Hemichordata Arthropoda Mollusca Mollusca
Nippopisella nagatai Balanoglossida sp. Heteroplax transversa Solemya pusilla Leptomya sp.
56 49 26 21 11
G1b G1a G2b G3b G2a
69
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Table 2 Five most common macrobenthic species of each ecological group observed in the Seto Inland Sea. Ecological groups
1
2
3
4
5
G1
Maldanidae sp. AN (24.3/4.2) Glycera sp. AN (38.8/12.3) Nemertea sp. NE (45.8/6.2) Theora lubrica MO (15.7/33.4) Notomastus sp. AN (31.6/69.6)
Synaptidae sp. EC (22.2/2.6) Ophiophragmus japonicus EC (19.5/9.4) Callianassa sp. AR (16.9/2.4) Lumbrineris longifolia AN (11.3/23.6) Capitellidae sp. AN (10.6/25.8)
Apionsoma sp. SI (15.7/5.3) Lumbrineris sp. AN (18.8/10.9) Leptochela gracilis AR (10.6/2.2) Paraprionospio sp. (form B) AN (9.6/4.8) Capitella sp. AN (2.4/2.8)
Magelonidae sp. AN (14.0/1.7) Ophiuroidea sp. EC (16.1/7.6) Corophium sp. AR (9.9/4.0) Paraprionospio sp. (form CI) AN (8.0/4.1) Leiochrides sp. AN (1.0/0.8)
Nippopisella nagatai AR (13.5/3.1) Alpheus sp. AR (14.7/2.5) Spiophanes sp. AN (9.6/1.2) Chaetozone sp. AN (5.8/2.8) Nebalia japonensis AR (0.5/0.4)
G2 G3 G4 G5
AN, Annelida; AR, Arthropoda; MO, Mollusca; NE, Nemertea; EC, Echinodermata; SI, Sipuncula. ( ); Proportion of sites observed (%)/percentage of species to total densities in each group (%).
Fig. 2. Spatial distributions of ecological groups of the macrobenthos (G1 to G5). Plot size in the figures represent the proportions of each group in species composition. Dark plots in the distribution of G5 indicate that total percentage of Capitellidae sp. and Capitella sp. was more than 10% in species composition.
4. Discussion
respectively (Table 2). In the genus Capitella, Capitella teleta and Capitella capitata inhabit heavily organically enriched sediments throughout the world, and their population dynamics and application to bioremediation of enriched sediments have been investigated in previous studies (e.g. Tsutsumi, 1987; Ito et al., 2016). On the other hand, Capitella minima, which inhabits the coastal area of Japan (Imajima, 2015), was found in coarse sediment at a depth of 70 m in the Andaman Sea of the eastern Indian Ocean (Green, 2002), showing that the genus Capitella could include taxa outside of G5. In the Seto Inland Sea, locations with high percentages of Capitellidae sp. and Capitella sp. (more than 10% of the species composition) were mainly distributed in the eastern part of Suo Nada (Fig. 2). These sites (13 sites) were characterized by being relatively deep (36.0 ± 2.9 m, mean ± standard error (SE)), with low mud (41.8 ± 6.4%) and TOC (8.4 ± 1.3 mg g−1) contents. Fig. 5 shows the relationship between TOC content and percentage of Capitellidae sp. and Capitella sp. in the species composition. These taxa were distributed not only in sediments with high TOC contents, but also in low-TOC sediments (5–10 mg g−1), indicating the presence of stress-sensitive Capitellidae and Capitella species in this area. According to Pitacco et al. (2018), the benthic community showed
4.1. Ecological groups In the present study, five unlisted species or taxa were assigned to ecological groups (see section 2.3, Data analysis). In the Seto Inland Sea, 69.5% of species or taxa were assigned to an ecological group, and 92.5% in all sites were successfully analyzed. Muniz et al. (2005) reported that the mean percentage of organisms not assigned to an ecological group was 0.6–6.9% at five locations in coastal South America, and AMBI values were successfully calculated for all sites investigated, with the addition of 20 species that were typically found in South Atlantic coastal regions. In the tropical Southwest Indian Ocean, 150 out of 242 taxa (62.0%) were unlisted in the AMBI program, and most of the unassigned taxa (except for 18 taxa, including those inhabiting in tropical areas) were assigned to an ecological group in the study by Bigot et al. (2008). Capitellidae sp. and Capitella sp. were assigned to G5 in the current species list (June 2017), and accounted for 25.8% and 2.8% of taxon density as a percentage of total density in G5 and the Seto Inland Sea, 70
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
4.2. Factors determining M-AMBI and sediment quality Nishijima et al. (2015) investigated the sediments at the same monitoring sites used in this study in the Seto Inland Sea, in terms of their physico-chemical properties (water depth, sediment temperature, mud content, TOC content, ORP, and sulfide content), using cluster analysis. Their study revealed that physico-chemical variables, especially TOC and mud content, influenced macrobenthic population size and biodiversity. Therefore, we evaluated the relationship of M-AMBI not only with a single physico-chemical parameter of the sediment, but also with comprehensive sediment quality as the clusters provided by Nishijima et al. (2015) (Fig. 6). The TOC contents, mud contents, Richness, H′, AMBI, and M-AMBI values in each cluster were compared among the clusters using a 1-way ANOVA and the Tukey–Kramer test. The result shows the significant differences between Cluster 1, Cluster 2–4, and Cluster 5–6 in TOC contents and mud contents (p < 0.05). On the other hands, the pattern similar to TOC and mud contents was not observed in Richness, H’, and AMBI, although Cluster 1 was significantly different from other clusters. In M-AMBI, Cluster 2–4 and Cluster 5–6 were significantly different, and the mean value in Cluster 1 was extremely low compared to the other clusters. This could suggest that the difference in the M-AMBI pattern is similar to the physicochemical parameters of the sediment, including TOC and mud contents, although Cluster 1 could not be directly compared because of the different reference conditions between Cluster 1 and Cluster 2–6. The sites that were classified into organically enriched Cluster 1, with high TOC (17.4 ± 0.5 mg g−1) and mud (90.4 ± 2.5%), accounted for 44% of all sites and were mainly located in three bays (Osaka Bay, Hiroshima Bay, and Beppu Bay) and Hiuchi Nada. These sites had significantly high AMBI and low M-AMBI values in the present study (Figs. 4 and 6). Conversely, more than 50% of the sites in Bisan Seto, Aki Nada, Iyo Nada, and Bungo Channel were characterized by unpolluted sandy sediment (Clusters 2–4; 26% of all sites) according to Nishijima et al. (2015) and were assigned high M-AMBI values (Bisan Seto, 0.55 ± 0.032; Aki Nada, 0.72 ± 0.026; Iyo Nada, 0.57 ± 0.013; Bungo Channel, 0.58 ± 0.027), corresponding to Good status. The mean M-AMBI values in secondarily enriched Clusters 5 and 6 were 0.51 ± 0.011 and 0.51 ± 0.023, respectively, corresponding to Moderate status. High status was assigned to ten locations based on M-AMBI classification, which were mainly distributed in Aki Nada (5 sites). Most of the sites were classified as Good (122 sites), Moderate (103 sites), or Poor status (102 sites). 47 sites were classified as Bad status, which was located in coastal regions such as the heavily polluted inner Osaka Bay (Tsujimoto et al., 2008). Locations with better than Moderate status
Fig. 3. Relationships between richness, Shannon's index (H′), and M-AMBI values. The triangles in the figure indicate the stations with the number of individuals were less than 6 and 1–3 species per sample.
a very weak response to chemical contamination such as heavy metals and polycyclic aromatic hydrocarbons (PAHs) in a coastal lagoon in Italy during the 11 year-study period. In the Seto Inland Sea, heavy metals accumulated in the surface sediment (0–2 cm), and high contents were detected in inner Osaka Bay, northern Harima Nada, and inner Hiroshima Bay during 1991–1994 (Komai et al., 1998). Nagaoka et al. (2004) reported that the mean Pb content (Mean, 57.8 μg g−1; Min-Max, 15.6–94.6 μg g−1) in the surface sediment (0–5 cm) in Osaka Bay in 2000 was approximately twice as high as that of the coastal lagoon in Italy (Mean; 21 mg kg−1) (Pitacco et al., 2018), and showed high correlation between heavy metals (Hg, Cd, Cu, Zn, Pb, Ni, Mn, Cr, Fe) and mud contents. These results suggested the possibility that not only the organic pollution, but also chemical contamination such as heavy metals influenced the distribution of Capitellidae and Capitella species. In any case, G5 was assigned the highest weighting coefficient of 6 in the calculation process of biotic coefficients following AMBI value determination in the AMBI program (Borja et al., 2000). Therefore, if the assignment of G5 changed, the calculated AMBI value would also change. However, the impact of such a change on the results could be small due to the low frequency of Capitellidae sp. and Capitella sp. in the case of the Seto Inland Sea.
Fig. 4. Spatial distribution of M-AMBI values. 71
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Table 3 Pearson correlation coefficients between physico-chemical parameters of the sediment and biotic indices in two regions (Cluster 1 and Cluster 2–6) of the Seto Inland Sea. Bold numbers are significant at p < 0.01. Cluster 1 AMBI M-AMBI Richness H′ Depth Temp. W.C. TOC Sulfide Mud ORP Cluster 2-6 AMBI M-AMBI Richness H′ Depth Temp. W.C. TOC Sulfide Mud ORP
AMBI
M-AMBI
Richness
H′
Depth
Temp.
W.C.
TOC
Sulfide
Mud
−0.79 −0.45 −0.72 −0.06 −0.04 0.24 0.35 0.33 0.04 −0.42
0.87 0.96 −0.04 0.08 −0.33 −0.33 −0.27 −0.19 0.39
0.77 −0.12 0.10 −0.33 −0.29 −0.15 −0.23 0.28
−0.02 0.06 −0.29 −0.26 −0.26 −0.19 0.36
−0.54 −0.27 −0.18 −0.37 −0.31 0.31
−0.15 −0.18 0.12 0.08 −0.01
0.75 0.30 0.50 −0.41
0.42 0.48 −0.40
0.22 −0.64
−0.09
AMBI
M-AMBI
Richness
H′
Depth
Temp.
W.C.
TOC
Sulfide
Mud
−0.60 −0.28 −0.14 −0.11 −0.11 0.39 0.35 0.19 0.29 −0.29
0.88 0.81 0.17 0.04 −0.44 −0.42 −0.28 −0.47 0.41
0.69 0.06 0.11 −0.37 −0.38 −0.25 −0.45 0.39
0.23 −0.14 −0.25 −0.25 −0.21 −0.33 0.26
−0.74 −0.18 −0.31 −0.32 −0.29 0.38
−0.06 0.08 0.27 0.04 −0.14
0.74 0.41 0.74 −0.65
0.47 0.80 −0.72
0.45 −0.59
−0.75
ORP
ORP
been implemented by the application of the TPLCS since 1979. Consequently, chlorophyll a concentrations and primary productions of the water in coastal regions have been decreasing since 1981 (Nishijima et al., 2016; Nakai et al., 2018). Therefore, the benthic ecosystems including the sediment quality and benthic communities would be changing with time due to the recovery of the water quality. To clarify the response of the benthic environment, a comprehensive index representing the benthic ecosystems is needed, and the M-AMBI would be a suitable for use in the coastal waters of Japan.
5. Conclusions This study aims to assess benthic quality using the M-AMBI and macrobenthic data collected in the Seto Inland Sea during 2001–2005 by MOE. The M-AMBI values were compared to the physico-chemical parameters of the sediment for evaluation of the applicability of the index in the coastal areas of Japan. The conclusions obtained were as follows:
Fig. 5. Relationship between TOC contents and percentages of Capitellidae sp. and Capitella sp. in species composition. Stations with non-appearance of these taxa (0%) were removed.
were mainly distributed from the Bungo Channel, which is strongly affected by the open sea, to Aki Nada in the eastern part of the Seto Inland Sea. Moreover, locations with better than Moderate status were observed near straits such as Bisan Seto and Akashi Strait, which is located between northeastern Harima Nada and northwestern Osaka Bay (Fig. 1). Thus, the distribution pattern of the M-AMBI depended on geographic features and the strength of anthropogenic stress, much greater than did AMBI. Osaka Bay and Bisan Seto are the areas receiving the highest COD and nutrient loads from land in the Seto Inland Sea. For example, Osaka Bay and Bisan Seto received 81 and 55 kg COD km−2 d−1, respectively, whereas other areas received 8–42 kg COD km−2 d−1. Nevertheless, Bisan Seto and Akashi Strait, which are connected to Osaka Bay, showed high M-AMBI values. Bisan Seto and Akashi Strait are characterized as areas with high tidal currents, as is Aki Nada, while Osaka Bay is not (Matsuura et al., 2006). Therefore, the distributions of M-AMBI and sediment quality are controlled not only by anthropogenic pollution, but also by physical forces driven by the geographical features of each region. Because, higher current speed would be produce better dispersion and dilution of pollutants and organic matters, thereby increasing the quality of the area (Borja et al., 2009; Orita et al., 2015). The reduction of the nutrient loading to the Seto Inland Sea has
(1) In the Seto Inland Sea, 69.5% of species or taxa were assigned to an ecological group, and 92.5% in all sites were successfully analyzed using the AMBI program. (2) Capitellidae and Capitella species assigned to G5 in the current species list (June 2017) observed were distributed not only in sediments with high TOC contents, but also in low-TOC sediments in the Seto Inland Sea. (3) M-AMBI would be a useful biotic index in Japanese coasts owing to representation of the comprehensive sediment quality.
Acknowledgments We would like to express our gratitude to the Ministry of the Environment, Japan, for supplying data from their investigation of the Seto Inland Sea. This research was supported by the Environment Research and Technology Development Fund (S-13) granted by the Ministry of the Environment. We acknowledge Dr. Joana Patrício of the European Commission and Dr. Ángel Borja of AZTI・Marine Research Division for valuable advices. We express our gratitude to Dr. Cervinia V. Manalo for her English language proofreading. 72
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Fig. 6. Mean values of (a) TOC and (b) Mud contents in the surface sediments and biotic indices including (c) Richness, (d) H′, (e) AMBI, and (f) M-AMBI in six clusters reported by Nishijima et al. (2015). Different letters indicate significant differences among clusters (Tukey–Kramer test, p < 0.05). Error bars show the standard error (SE).
Appendix A. Supplementary data
human pressures? Mar. Pollut. Bull. 97, 85–94. Borja, Á., Elliott, M., Andersen, J.H., Berg, T., Carstensen, J., Halpern, B.S., Heiskanen, A.S., Korpinen, S., Stewart Lowndes, J.S., Martin, G., Rodriguez-Ezpeleta, N., 2016. Overview of integrative assessment of marine systems: the ecosystem approach in practice. Front. Mar. Sci. 3, 1–20. Conway, N.M., Howes, B.L., McDowell Capuzzo, J.E., Turner, R.D., Cavanaugh, C.M., 1992. Characterization and site description of Solemya borealis (Bivalvia: Solemyidae), another bivalve-bacteria symbiosis. Mar. Biol. 112, 601–613. Dauer, D.M., 1993. Biological criteria, environmental health and estuarine macrobenthic community structure. Mar. Pollut. Bull. 26, 249–257. Díaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929. Díaz, R.J., Solan, M., Valente, R.M., 2004. A review of approaches for classifying benthic habitats and evaluating habitat quality. J. Environ. Manage. 73, 165–181. Duarte, C.M., Borja, Á., Carstensen, J., Elliott, M., Krause-Jensen, D., Marbà, N., 2015. Paradigms in the recovery of estuarine and coastal ecosystems. Est. Coast. 38, 1202–1212. European Commission, 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. Off. J. Eur. Union L327, 1–72. European Commission, 2008. Directive 2008/56/EC of the European Parliament and of the Council establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Off. J. Eur. Union L164, 19–40. Green, K.D., 2002. Capitellidae (Polychaeta) from the Andaman Sea, vol. 24. Phuket Marine Biological Center Special Publication, pp. 249–343. Imajima, M., 2015. Kankeidoubutsu Tamourui IV (Annelida, Polychaeta). Seibutsu Kenkyusha Co., Ltd., Tokyo, pp. 530 in Japanese. Islam, M.S., Tanaka, M., 2004. Impact of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar. Pollut. Bull. 48, 624–649. Ito, M., Ito, K., Ohta, K., Hano, T., Onduka, T., Mochida, K., Fujii, K., 2016. Evaluation of bioremediation potential of three benthic annelids in organically polluted marine sediment. Chemosphere 163, 392–399. Japan River Association, 2018. River in Japan (in Japanese). (Available on line at. http://www.japanriver.or.jp/river_law/kasenzu/chugoku_zu/chugoku_zu.htm. Kemp, W.M., Testa, J.M., Conley, D.J., Gilbert, D., Hagy, J.D., 2009. Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6, 2985–3008. Komai, Y., Kobuke, Y., Seiki, T., Nagafuchi, O., Murakami, K., Koyama, T., Kakibaya, T., 1998. Distribution of heavy metals and its change in the sediment of the Seto Inland Sea. J. Jpn. Soc. Water Environ. 21, 743–750 in Japanese. Kronvang, B., Jeppesen, E., Conley, D.J., Søndergaard, M., Larsen, S.E., Ovesen, N.B.,
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marenvres.2019.05.007. References Bigot, L., Grémare, A., Amouroux, J.M., Frouin, P., Maire, O., Gaertner, J.C., 2008. Assessment of the ecological quality status of soft-bottoms in Reunion Island (tropical Southwest Indian Ocean) using AZTI marine biotic indices. Mar. Pollut. Bull. 56, 704–722. Birk, S., Bonne, W., Borja, Á., Brucetm, S., Courratm, A., Poikane, S., Solimini, S., van de Bund, W., Zampoukas, N., Hering, D., 2012. Three hundred ways to assess Europe's surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecol. Indic. 18, 31–41. Borja, Á., Franco, J., Pérez, V., 2000. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 40, 1100–1114. Borja, Á., Muxika, I., 2005. Guidelines for the use of AMBI (AZTI's Marine Biotic Index) in the assessment of the benthic ecological quality. Mar. Pollut. Bull. 50, 787–789. Borja, Á., Bricker, S.B., Dauer, D.M., Demetriadis, N.T., Ferreira, J.G., Forbes, A.T., Hutchings, P., Jia, X., Kenchington, R., Marques, J.C., Zhu, C., 2008a. Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. Mar. Pollut. Bull. 56, 1519–1537. Borja, Á., Dauer, D.M., Díaz, R., Llansó, R.J., Muxika, I., Rodríguez, J.G., Schaffner, L., 2008b. Assessing estuarine benthic quality conditions in Chesapeake Bay: a comparison of three indices. Ecol. Indic. 8, 395–403. Borja, Á., Rodríguez, J.G., Black, K., Bodoy, A., Emblow, C., Fernandes, T.F., Forte, J., Karakassis, I., Muxika, I., Nickell, T.D., Papageorgiou, N., Pranovi, F., Sevastou, K., Tomassetti, P., Angel, D., 2009. Assessing the suitability of a range of benthic indices in the evaluation of environmental impact of fin and shellfish aquaculture located in sites across Europe. Aquaculture 293, 231–240. Borja, Á., Dauer, D.M., Elliott, M., Simenstad, 2010a. Medium- and long-term recovery of estuarine and coastal ecosystems: patterns, rates and restoration effectiveness. Est. Coast. 33, 1249–1260. Borja, Á., Elliott, M., Carstensen, J., Heiskanen, A.S., van de Bund, W., 2010b. Marine management - towards an integrated implementation of the European marine Strategy framework and the water framework directives. Mar. Pollut. Bull. 60, 2175–2186. Borja, Á., Marín, S.L., Muxika, I., Pino, L., Rodríguez, J.G., 2015. Is there a possibility of ranking benthic quality assessment indices to select the most responsive to different
73
Marine Environmental Research 148 (2019) 67–74
A. Umehara, et al.
Seto Inland Sea Japan, exposed to anthropogenic nutrient loading. Sci. Total Environ. 571, 543–550. Orita, R., Umehara, A., Komorita, T., Choi, J.W., Montani, S., Komatsu, T., Tsutsumi, H., 2015. Contribution of the development of the stratification of water to the expansion of dead zone: a sedimentological approach. Est. Coast. Shelf Sci. 164, 204–213. Pelletier, M.C., Gillett, D.J., Hamilton, A., Grayson, T., Hansen, V., Leppo, E.W., Weisberg, S.B., Borja, A., 2018. Adaptation and application of multivariate AMBI (M-AMBI) in US coastal waters. Ecol. Indic. 89, 818–827. Pitacco, V., Mistri, M., Ferrari, C.R., Munari, C., 2018. Heavy metals, OCPs, PAHs, and PCDD/Fs contamination in surface sediments of a coastal lagoon (Valli di Comacchio, NW Adriatic, Italy): long term trend (2002−2013) and effect on benthic community. Mar. Pollut. Bull. 135, 1221–1229. Tsujimoto, A., Yasuhara, M., Nomura, R., Yamazaki, H., Sampei, Y., Hirose, K., Yoshikawa, S., 2008. Development of modern benthic ecosystems in eutrophic coastal oceans: the foraminiferal record over the last 200 years, Osaka Bay, Japan. Mar. Micropaleontol. 69, 225–239. Tsujino, M., Abo, K., Tarutani, K., 2016. The bottom environment and macrobenthic community of Osaka Bay, Japan in 2003 and 2011. Nippon Suisan Gakkaishi 82, 330–341 (in Japanese with English abstract). Tsutsumi, H., 1987. Population dynamics of Capitella capitata (Polychaeta; Capitellidae) in an organically polluted cove. Mar. Ecol. Prog. Ser. 36, 139–149. Uede, T., 2008. Validity of acid volatile sulfide as environmental index and experiment for fixing its standard value in aquaculture farms along the coast of Wakayama Prefecture, Japan. Nippon Suisan Gakkaishi 74, 402–411 (in Japanese with English abstract). Verdonschot, P.F.M., Spears, B.M., Feld, C.K., Brucet, S., Keizer-Vlek, H., Borja, Á., Elliott, M., Kernan, M., Johnson, R.K., 2013. A comparative review of recovery processes in rivers, lakes, estuarine and coastal waters. Hydrobiologia 704, 453–474. Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke, C., Halpern, B.,S., Jackson, J.B.C., Lotze, H.K., Micheli, F., Palumbi, S.R., Sala, E., Selkoe, K.A., Stachowicz, J.J., Watson, R., 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790.
Carstensen, J., 2005. Nutrient pressures and ecological responses to nutrient loading reductions in Danish streams, lakes and coastal waters. J Hydrol 304, 274–288. Matsuo, M., Sudo, H., Azuma, M., Kondo, H., Tamaki, A., 2007. Division substrate groups and gammaridean amphipod assemblages in sublittoral Ariake Sound-a comparison between 1997 and 2002. Bull. Fac. Fish. Nagasaki Univ. 88, 1–42 in Japanese with English abstract. Matsuura, N., Sasaki, T., Suzuyama, H., Kuwakino, F., Nagashima, H., 2006. High accuracy tidal current Forecasting on the basis of harmonic analysis of model Simulation in the Seto Inland Sea. J. Jpn Soc. Mar. Surv. Technol. 18, 1–10 (in Japanese with English abstract). Ministry of the Environment, Japan, 2001. Sediment test method (in Japanese). (Available on line at. http://db-out.nies.go.jp/emdb/pdfs/water/teisitutyousa/ 0103teisitutyousahouhou.pdf. Muniz, P., Venturini, N., Pires-Vanin, A.M.S., Tommasi, L.R., Borja, Á., 2005. Testing the applicability of a marine biotic index (AMBI) to assessing the ecological quality of soft- bottom benthic communities, South America Atlantic region. Mar. Pollut. Bull. 50, 624–637. Murakami, K., Imatomi, Y., Komai, Y., Nagafuchi, O., Seiki, T., Koyama, T., 1998. Relationship between distribution of Annelida and sediment condition in the Seto Inland Sea. J. Jpn. Soc. Water Environ. 21, 757–764 (in Japanese with English abstract). Nagaoka, C., Yamamoto, Y., Eguchi, S., Miyazaki, N., 2004. Relationship between distribution of heavy metals and sedimental condition in the sediment of Osaka Bay. Nippon Suisan Gakkaishi 70, 159–167 (in Japanese). Nakai, S., Soga, Y., Sekito, S., Umehara, A., Okuda, T., Ohno, M., Nishijima, W., Asaoka, S., 2018. Historical changes in primary production in the Seto Inland Sea, Japan, after implementing regulations to control the pollutant loads. Water Pol. 20, 855–870. Nishijima, W., Umehara, A., Okuda, T., Nakai, S., 2015. Variations in macrobenthic community structures in relation to environmental variables in the Seto Inland Sea, Japan. Mar. Pollut. Bull. 92, 90–98. Nishijima, W., Umehara, A., Sekito, S., Okuda, T., Nakai, S., 2016. Spatial and temporal distributions of Secchi depths and chlorophyll a concentrations in the Suo Nada of the
74