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Ecological thresholds of hypoxia and sedimentary H2S in coastal soft-bottom habitats: A macroinvertebrate-based assessment
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Ecological thresholds of hypoxia and sedimentary H2S in coastal soft-bottom habitats: A macroinvertebrate-based assessment Gen Kanayaa,∗, Yasuo Nakamuraa, Tomoyoshi Koizumib a b
National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan Corporative Nihon Mikuniya, 3-25-10 Mizonokuchi, Takatsu, Kawasaki, Kanagawa 213-0001, Japan
A R T I C L E I N F O
A B S T R A C T
Keywords: Eutrophication Ecosystem management Dissolved oxygen Sulphide Macrozoobenthic community Polychaete Sediment Coastal zone Tokyo Bay
Ecological thresholds of dissolved oxygen (DO) and sedimentary hydrogen sulfide (H2S) for macrozoobenthos were examined during a 30-month monitoring of two stations in a highly eutrophic canal in inner Tokyo Bay, Japan. Bottom DO and H2S concentrations fluctuated seasonally, and were significantly correlated with water and sediment temperatures. Red tide-derived phytodetritus was a major source of sediment organic matters in the canal bottom, and the sediment became highly reduced and sulfidic condition in warmer months (sedimentary H2S; up to 8.5 mM). Dominant opportunistic taxa, including polychaetes and amphipods, were eliminated under low DO and high H2S conditions (i.e., population thresholds), and devastation of community structure occurred at 2.4–3.3 mg l−1 DO and 1.8–2.7 mM H2S (i.e., community thresholds). To maintain ecosystem function in anthropogenically degraded habitats and ensure colonization by macrozoobenthos throughout the year, DO and H2S levels should be maintained below these thresholds.
1. Introduction In coastal soft-bottom habitats, macrozoobenthos are key components of the benthic community and play important roles at the sediment-water interface. Their activities facilitate the mechanical breakdown of detritus and enhance the transfer of nutrients from the sediment to the overlying water column (Levin et al., 2001). Feeding, burrowing, and bioturbation activities of macrozoobenthos can enhance the cycling of organic matter in sediment (Andersen and Kristensen, 1992; Kinoshita et al., 2008; Josefson et al., 2012). Benthic invertebrates provide important linkages between primary production and mobile predators, facilitating the transfer of energy from benthic to pelagic habitats via predator-prey relationships (Diaz and Rosenberg, 2008). During the last 100 years, anthropogenic disturbances such as reclamation and eutrophication have caused loss of biodiversity and function in marine coastal ecosystems (Lotze et al., 2006). Defaunation in coastal benthic ecosystems often induced drastic changes in material flow, productivity, food-web transfer, and species interactions at the ecosystem scale (Altieri and Witman, 2006; Altieri, 2008; Villnäs et al., 2012; Sturdivant et al., 2013). Accordingly, assuring successful colonization by benthic invertebrates is necessary to maintain ecosystem function in coastal soft-bottom communities. In eutrophic coastal waters, anthropogenic stressors such as bottom
∗
water hypoxia (e.g. < 2.0 O2 mg l−1; Gray et al., 2002) and sedimentary H2S accumulation are significant determinants of macrozoobenthic assemblage structure, through disappearance of less-tolerant taxa, decline in species diversity, and predominant of few smallbodied opportunistic species such as polychaetes (Gamenick et al., 1996; Como and Magni, 2009; Josefson et al., 2012; Kodama et al., 2012; Villnäs et al., 2012). Increasing the loading of labile organic matter enhances oxygen consumption at the sediment-water interface, resulting in the development of an oxygen-deficient water body near the seafloor (Pearson and Rosenberg, 1978). Furthermore, stratification in the water column (e.g. development of thermocline or halocline) also facilitates the development of hypoxia within the stagnant bottom layer (Murphy et al., 2011). As eutrophication proceeds, anaerobic microbial sulfate reduction prevails in the sediment, leading to accumulation of sedimentary H2S (H2S + HS− + S2−; Hargrave et al., 2008). Generally, H2S is highly toxic to most benthic invertebrates even at low concentrations, and its toxicity is enhanced under hypoxic conditions (Gray et al., 2002; Vaquer-Sunyer and Duarte, 2010). A certain groups of macroinvertebrates can cope with H2S toxicity through both of physiological and behavioral adaptations, e.g. detoxification through oxidation in their body fluid and ventilation activities through their burrow (Vismann, 1991; Sturdivant et al., 2012). However, mass mortality of benthic organisms can occur in marine sediments when the
Corresponding author. E-mail address: [email protected] (G. Kanaya).
https://doi.org/10.1016/j.marenvres.2018.02.007 Received 20 September 2017; Received in revised form 30 January 2018; Accepted 11 February 2018 0141-1136/ © 2018 Elsevier Ltd. All rights reserved.
Please cite this article as: Kanaya, G., Marine Environmental Research (2018), https://doi.org/10.1016/j.marenvres.2018.02.007
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concentration of sedimentary H2S exceeds the capability of detoxification by macroinvertebrates (Gamenick et al., 1996; Hargrave et al., 2008; Kanaya et al., 2016b). Opportunistic macrozoobenthos may play an important role as “pioneer species” after a mass-mortality event, and are important components of communities in frequently disturbed soft-bottom habitats (Dauer, 1984; Kanaya et al., 2016a,b; Kodama et al., 2012) because they recolonize quickly after defaunation and rapidly recover their population size (Dauer, 1984; Kinoshita et al., 2008; Kanaya et al., 2016a). These small-sized opportunistic taxa can help conditioning the sediment environment for large and more mature benthic taxa that colonize at later stages of community succession (Pearson and Rosenberg, 1978). These suggest that opportunistic taxa play an important role in maintaining ecosystem function during community recovery in heavily eutrophied coastal waters. Hence, it is important to understand the ecological thresholds of lethal environmental factors including bottom dissolved oxygen (DO) and sedimentary H2S necessary for these opportunistic taxa to maintain their populations and ecosystem functions. Tokyo Bay is a semi-enclosed and highly eutrophic bay located on the Pacific Coast of central Japan. In its inner portion, hypoxic bottom water prevails during the warmer months at a broad scale, leading to change and seasonal defaunation of the benthic community (Kodama et al., 2012). Recently, Yuhara et al. (2013) showed that littoral intertidal zones in the canal networks of inner Tokyo Bay provide substantial habitat for endangered macrozoobenthic species. The bottom habitat of the canal networks provides a potential refuge for macroinvertebrates from the severe hypoxia in the deeper subtidal zone of inner Tokyo Bay (Ando and Kawai, 2007). Hence, shallow littoral habitats contribute to the entire bay's macrozoobenthic biodiversity, and may provide an essential ecosystem function in the anthropogenically degraded bay system. However, anthropogenic disturbances such as sewage overflow, hypoxia, sediment deterioration, and rising water temperature due to thermal discharge are potential threats to the benthic communities in these shallow canal systems (Ando and Kawai, 2007; Maki et al., 2007; Ariji et al., 2008; Nakamura et al., 2012). In this study, a shallow canal system, Keihin Canal, was selected as a study site to conduct a 30-month survey on the relationships between anthropogenic environmental degradation and macrozoobenthic assemblage structure. Two nearby stations (about 100 m apart) were sampled in the littoral zone of the canal, along a steep gradient of DO and sediment redox state. We specifically focused on (1) documenting the seasonal changes in environmental quality of the canal bottom by assessing bottom DO, sedimentary H2S level, and sedimentary organic matter (SOM) content; and (2) resolving ecological thresholds of DO and sedimentary H2S that induced devastation of the macrozoobenthic community. We use this information to discuss the major drivers of seasonal hypoxia and sedimentary H2S accumulation in the canal bottom, with the goal of supporting future mitigation and management strategies for anthropogenically degraded coastal soft-bottom environments.
Fig. 1. Map showing the two sampling stations in the Keihin Canal, inner Tokyo Bay. Sampling was conducted monthly at St. A on the Oi artificial tidal flat (elevation; +0.7 m from Tokyo Peil [T.P.]) and St. B on the canal bottom (−2.7 m from T.P.). Salinity, DO, and water temperature were measured at St. B at two- or four-week intervals.
dissolved inorganic nitrogen (DIN; NH4++NO2−+NO3-) concentration of 226 ± 82 SD μmol l−1 (2010–2011, n = 17, authors' unpublished data). Red tides frequently occur in warmer months (Tokyo Metropolitan Government), and severe hypoxia prevails in the canal bottom from spring to fall (Ariji et al., 2008; Nakamura et al., 2012; Kanaya et al., 2015). In this study, macrozoobenthos and sediment sampling was conducted monthly in the sandy intertidal zone (+0.7 m from Tokyo Pail [T.P.], St. A) of the Oi artificial tidal flat (1.38 ha) and the muddy subtidal zone (−2.7 m from T.P., St. B). Water depth at St. B was 2.5 m during spring low tide, and most of the subtidal zone was covered by sulfidic mud (Kanaya et al., 2015). The benthic community is dominated by multivoltine polychaetes and amphipods that included taxa with opportunistic life history traits, whereas long-lived taxa such as bivalves and decapods are scarce. Massive liquefaction occurred during the 2011 Great East Japan earthquake, which resulted in an increase in the silt-clay contents of the tidal flats for several months but did not significantly affect the abundance of macrozoobenthos (Kanaya et al., 2015). 2.2. Water quality Salinity, DO, and water temperature were only monitored at St. B at 2- or 4-week intervals from April 2010 to October 2012. Measurements were taken from a pontoon during spring low tide on daytime (8: 30 to 10: 30 a.m. in most cases) using a water quality meter (Quanta, Hydrolab) at the surface (10 cm depth) and bottom (10 cm above the sediment). In this study, we defined “hypoxia” as DO < 2.0 mg l−1 and “moderate hypoxia” as DO between 2.0 and 4.0 mg l−1 (Gray et al., 2002). It should be noted here that the intensity of hypoxia at the canal surface were possibly underestimated since DO often shows diurnal fluctuation and could decrease on nighttime in warmer months (Kanaya et al., 2015). During each sampling event, three bottles of surface water were collected at St. B to measure chlorophyll a (chl. a) and phaeopigment (phaeo). In the laboratory, suspended matter in the sample was concentrated onto a GF/F after pre-filtration through a 0.125 mm mesh. Amounts of chl. a and phaeo on the filter were determined via
2. Materials and method 2.1. Study site A 30-month field survey was conducted from May 2010 to October 2012 in a shallow eutrophic brackish canal (water depth < 4 m) in inner Tokyo Bay, Keihin Canal (Fig. 1). The cement-lined canal was constructed in the mid-20th century during reclamation of the surrounding area. Tides are semidiurnal with a spring tidal range of 1.9 m. Salinity fluctuates between 20 and 30, and sometimes falls below 10 (Kanaya et al., 2013). After rainfall, urban surface runoff is discharged into the area through sewage overflow, which provides a significant source of anthropogenically derived nutrients to inner Tokyo Bay (Maki et al., 2007). The canal is highly eutrophic, with an annual average 2
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fluorometry (10-AU, Turner Designs) after extraction in 90% acetone.
2.6. Estimation of threshold levels for macrozoobenthos In this study, lethal levels of DO and sedimentary H2S were elucidated for both at population and community levels. Firstly, lethal concentrations for dominant macrozoobenthic taxa (i.e. population thresholds) were defined from the lowest DO and highest H2S concentration allowing their colonization, based on the 30 months' monitoring data (Fig. 7). For this analysis, six taxa occurring at both stations (polychaetes Pseudopolydora reticulata, Polydora cornuta, and Capitella cf. teleta, cnidarian Edwardsiidae sp., and amphipods Grandidierella japonica and Monocorophium acherusicum) and two taxa occurring at St. B (polychaetes Prionospio pulchra and Schistomeringos cf. rudolphi) were used since their population dynamics was strongly controlled by seasonal hypoxia and H2S accumulation. For the latter two taxa, only the data at St. B were used. Secondly, community thresholds that induced drastic changes in macrozoobenthic community structure on the canal bottom were elucidated from cluster analysis (Fig. 8). We elucidated DO and H2S concentrations that induced drastic changes in community structure from relatively high diversity and density of macrozoobenthos in colder months (group II) to nearly azoic and low diversity conditions in warmer months (group I, see Fig. 9).
2.3. Sediment parameters Sediment parameters including sediment temperature, redox potential (Eh), silt-clay content, chl. a, phaeo, total organic carbon (TOC), total nitrogen (TN), H2S (H2S + HS− + S2−), and acid-volatile sulfide (AVS) were measured monthly from May 2010 to October 2012 at both stations. Four sediment cores were collected at each station with a PVC corer (φ 10 cm, 50 cm length) at St. A and an acryl suspended core sampler (φ 10 cm, 50 cm length, HR type, Rigo-sha) at St. B. From the first core collected at each station, sediment temperature and Eh at a depth of 5 cm were measured immediately in situ using an ORP meter (RM-30P, TOA-DKK), and a sub-core (φ 4 cm, 10 cm deep) was taken for silt-clay analysis. From the other three cores, a sub-core (φ 4 cm, 10 cm deep) was taken from each for chl. a, phaeo, TOC, TN, H2S, and AVS analyses. In the laboratory, silt-clay content (1–4 cm deep, n = 1 for each station) was determined via wet sieving using a 0.063 mm mesh sieve after drying for 48 h at 70 °C. Sediment from 0 to 1 cm depth (n = 3 for each station) was sub-sampled for TOC and TN analysis, acidified with 1 M HCl, and freeze-dried for 24 h. These parameters were determined using an elemental analyzer (NC-2500, Finnigan Mat). Another subsample from each core (0–1 cm deep, n = 3 for each station) was used for chl. a and phaeo analyses, which were quantified by spectrophotometry at wavelengths of 665 and 750 nm (UV-1600, Shimadzu) after extraction in 90% acetone. Sediment from 1 to 4 cm in depth (n = 3 for each station) was subsampled for H2S and AVS analyses. H2S was extracted by purging with pure N2 gas for 20 min and absorbed onto 2.5% zinc acetate. Subsequently, H2S from acid-volatile insoluble sulfide (AViS) was liberated by adding 10 mL 1M HCl; sulfide in the solution was quantified by iodometry. H2S and AViS values were summed and expressed as AVS. H2S was expressed as molar content per interstitial water volume (mM) and AVS was expressed as molar content per sediment volume (mmol l−1).
3. Results 3.1. Water temperature, salinity, DO, and pigments in canal water Water temperature ranged from 11.2 to 32.2 °C (Fig. 2), with a mean value of 21.8 ± 5.4 SD °C at the surface and 22.8 ± 5.5 SD °C at the bottom (n = 46 for each). Temperature was highest in August or September and lowest in January or February of each year. Salinity was high at the canal bottom (mean; 29.1 ± 1.8 SD, n = 46) compared to those at the surface (19.7 ± 5.4 SD, n = 46). Salinity in the surface layer fluctuated widely over time, particularly in the warmer months, and halocline distinctly developed in warmer months. DO was much lower in the bottom water (bottom; 2.5 ± 2.2 SD mg l−1, surface; 5.6 ± 1.7 SD mg l−1, n = 46), which transitioned to moderate hypoxia (DO < 4.0 mg l−1) from May to December, and fell below 2.0 mg l−1 from June to October or November. Surface water also became moderately hypoxic during the warmer months. Chl. a and phaeo in the canal water rose sharply in June to September (chl. a; over 20–30 μg l−1), due to massive blooms of the diatom Skeletonema costatum (authors' unpublished data). The bloom lasted for several months, after which chl. a concentrations were low (< 5 μg l−1) from November to February.
2.4. Macrozoobenthos Macrozoobenthos were collected during each sediment sampling event. Three cores of sediment (φ 10 cm by 30 cm deep) were collected from each station (n = 3), sieved through a 1 mm mesh, and fixed in 5% neutralized formalin containing rose bengal. In the laboratory, macrozoobenthos were sorted, identified, and counted under a stereoscopic dissecting microscope. The use of 1 mm mesh sieve may underestimate the macrozoobenthic density, compared with previous studies using a 0.5 mm mesh (Sturdivant et al., 2012; Villnäs et al., 2012), since small sized opportunists often prevail in community under eutrophication (Diaz and Rosenberg, 1995).
3.2. Sediment characteristics Sediment properties at the sampling stations are summarized in Table 1. Sediment at St. A was characterized by oxidized sand (silt-clay; 11.5%), while that at St. B was highly reduced mud (silt-clay; 81.0%). At St. B, sedimentary chl. a and phaeo were about three to six times higher, and TOC, TN, and AVS were 12–13 times higher than those at St. A. High levels of H2S were detected at St. B throughout the study period (maximum; 8.5 mM), but not at St. A.
2.5. Statistical analyses Relationships between temperature and DO concentration, DO saturation, or sedimentary H2S at the canal bottom (St. B) were examined using linear regression. Spatiotemporal changes in community structure were examined through cluster analysis using the software PRIMER ver. 6.2 (Clarke and Gorley, 2006). Square-root-transformed densities of macrozoobenthos were used for analysis. Samples were clustered with a group average linkage method based on a Bray–Curtis similarity matrix, in which five sample groups were defined. Total macrozoobenthic density, number of taxa, sedimentary H2S content, and DO were averaged for each group. Surface- and bottom-DO data were used in analyses for St. A and B, respectively.
3.3. Temporal fluctuation in pigments, organic matter, and sulfides in sediment Sedimentary chl. a and phaeo contents at the canal bottom and intertidal zone corresponded well to those in the water column (Fig. 3). Sedimentary phaeo reached its annual peak in summer to fall (16–63 μg cm−2 at St. A, 100–250 μg cm−2 at St. B), shortly after the phytoplankton bloom. Seasonal changes in sedimentary TOC at St. B corresponded well to changes in sedimentary phaeo content. TOC was highest in August to October (over 50–75 mg g−1) and gradually 3
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Fig. 2. Seasonal changes in (a) water temperature, (b) salinity, and (c) DO at the surface and bottom (−2.6 m from T.P.) of the Keihin Canal (St. B). (d) Concentrations of pigments (chl. a and phaeo) in surface water at St. B were also shown. Bars in (d) mean SD (n = 3). n = 1 for other plots.
with its highest annual values in summer (5.3–8.5 mM) and lowest in winter to spring (< 0.5 mM). At St. A, H2S was not detected, and AVS was low over most of the study period. At St. A, pulsed increases in AVS occurred after March 2011 due to mud boiling during the 2011 earthquake (see Kanaya et al., 2015). At St. B, AVS was much higher than at St. A and increased sharply in the warmer months, corresponding to the increase in sedimentary H2S.
Table 1 Sediment characteristics at St. A and B. Mean, standard deviation (SD), and maximum (max.) values are calculated from data collected from May 2010 to October 2012. Variables
Silt-clay (%) Eh (mV) Chl. a (μg cm−2) phaeo (μg cm−2) TOC (mg g−1) TN (mg g−1) C/N atom H2S (mM) AVS (mmol l−1)
Intertidal zone (St. A)
Subtidal zone (St. B)
mean
max.
mean
(SD)
max.
69.5 421 18.3 79.2 17.1 1.46 17.6
81.0 −164 15.9 96.0 50.9 5.9 10.3 2.7 27.1
(8.4) (67) (13.9) (75.2) (12.3) (2.2) (1.6) (2.3) (9.2)
93.6 93.1 64.8 356 87.2 13.1 16.8 8.5 44.9
(SD)
11.5 (15.9) 235 (104) 5.6 (4.3) 15.8 (14.9) 3.9 (2.5) 0.43 (0.20) 10.1 (2.3) not detected 2.2 (3.8)
12.9
n
30 29 29 29 29 29 29 30 30
3.4. Relationships of water temperature to bottom DO and sedimentary H2S DO and sedimentary H2S in the canal bottom were significantly correlated with temperature (Fig. 4). Bottom DO concentration was negatively correlated with bottom water temperature (BWT), as expressed in Equation (1):
Bottom DO (mg l−1) = −0.354 BWT + 10.5 decreased into winter. The C/N ratio at St. B fluctuated seasonally, showing an inverse trend to sedimentary TOC. This ratio was below 10 in summer to fall when the TOC content increased, and gradually increased toward winter as TOC decreased. On the other hand, seasonal changes in sedimentary TOC at St. A was different from those at St. B. This should be due to the deposition of muddy sediment onto the tidalflat through massive liquefaction during the 2011 Great East Japan earthquake in March 2011. At St. B, sedimentary H2S exhibited a clear seasonal fluctuation,
(1)
Bottom water in the canal reached moderate hypoxia (DO < 4.0 mg l−1) when BWT exceeded 18.4 °C and hypoxia (DO < 2.0 mg l−1) when BWT exceeded 24.0 °C. Negative relationship was also found between bottom DO saturation and BWT as:
Bottom DO saturation (%) = −3.91 BWT + 120
(2)
Sedimentary H2S was positively correlated with sediment temperature (ST), as described by Equation (3): 4
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Fig. 3. Seasonal changes in sediment parameters including (a) pigments (chl. a and phaeo), (b) TOC and C/N, (c) H2S, and (d) AVS at St. A and B. Bars indicate SD (n = 3). H2S was not detected at St. A throughout the period. H2S and AVS are respective denoted as molar content per interstitial water volume (mM) and per sediment volume (mmol l−1).
Sedimentary H2 S (mM) = 0.308 ST − 3.90
14830 ind. m−2, St. B; 4806 ind. m−2). The polychaetes Prionospio japonica, Hediste diadroma, P. reticulata, and Streblospio benedicti japonica were the first to fourth dominant taxa at St. A, while the polychaetes C. cf. teleta and P. pulchra and the amphipods G. japonica and M. acherusicum were the most dominant taxa at St. B. Several dominant taxa occurred at both stations, including Edwardsiidae sp., P. reticulata, P. cornuta, C. cf. telata, G. japonica, and M. acherusicum. Polychaetes S. cf. rudolphi and P. pulchra occurred only at St. B, while seven taxa in Table 2 including H. diadroma, P. japonica, and S. benedicti japonica were unique to St. A. Of the dominant taxa in Table 2, only two species, H. diadroma (dominant at St. A) and N. succinea (dominant at St. B), are univoltine (Hardege et al., 1990; Kikuchi and Yasuda, 2006), while all other dominant taxa appear to have multivoltine life cycles. Several of them had been reported as an opportunistic species that commonly occurred in frequently disturbed soft-bottom habitats including organically
(3)
A 1 °C increase in ST corresponded to a 0.308 mM increase in sedimentary H2S. We also found a significant positive correlation (r = 0.976, n = 30, p < 0.001, data not shown in figure) between ST and BWT, as shown in Equation (4):
ST (°C) = 0.925 BWT + 1.30
(4)
3.5. Composition of macrozoobenthos A total of 48 and 36 taxa occurred during the study period at St. A and B, respectively (Table 2). Polychaetes dominated the community numerically at both stations (86–93%), followed by amphipods (4.3–6.2%) and bivalves (0.3–5.3%). The mean density of total macrozoobenthos was about three times higher at the intertidal zone (St. A; 5
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Table 2 Average density (ind. m−2) and proportion (%) of dominant macrozoobenthos at St. A and B during the study period. Average density for each taxonomic group and all taxa are also shown. Taxa
Cnidaria Edwardsiidae sp. Nemertinea Nemertinea sp. Bivalva Musculus senhousia Arthritica reikoae Ruditapes philippinarum Polychaeta Sigambra tentaculata Eteone longa Hediste diadroma Neamthes succinea Schistomeringos cf. rudolphi Prionospio japonica P. pulchra Streblospio benedicti japonica Rhynchospio glutaea Pseudopolydora reticulata Polydora cornuta Armandia lanceolata Capitella cf. teleta Heteromastus sp. Amphipoda Ampithoe valida Grandidierella japonica Monocorophium acherusicum Bivalva Polychaeta Amphipoda Other Total macrozoobenthos Taxa occurred
Density/% St. A
St. B
191/13
69/1.4
105/0.7
6/0.13
285/1.9 265/1.8 88/0.6
2/0.0 – 2/0.0
14/0.1 111/0.7 2855/19.2 6/0.9 – 3287/22.2 – 1202/8.1 185/1.2 2475/16.7 789/5.3 304/2.1 1071/7.2 390/2.6
37/0.8 3/0.1 – 45/0.9 54/1.1 – 272/5.7 – – 14/0.3 26/0.5 – 3929/81.8 –
1/0.0 479/3.2 441/3.0 784/5.3 12774/86 924/6.2 301/2.4 14830 48
26/0.5 89/1.9 86/1.8 17/0.3 4469/93 207/4.3 77/2.4 4806 36
−; not observed. Common taxa in each station (> 0.5% to total) are listed with eight dominant taxa for each station bolded.
density sharply declined in the warmer months. At St. B, macrozoobenthos were nearly absent from June to December when sedimentary H2S exceeded 2 mM (Fig. 3c). Their density increased sharply in winter to spring, and reached its annual maximum in March or April (up to 46180 ind. m−2). Species richness at St. A fluctuated from 11 to 23 taxa, and declined in the warmer months. At St. B, species richness declined sharply in June to November (< 5 taxa), and increased from November to May (up to 17 taxa). Temporal changes in the densities of dominant taxa are shown in Fig. 6. At St. B, these taxa exhibited a clear seasonal defaunation-recolonization cycle. They almost disappeared from early summer to late fall, and then recolonized and rapidly increased their population sizes in winter to spring, achieving their highest densities in February to May. At St. A, long-term defaunation did not occur despite densities declining during May to September. The population sizes of several taxa including Edwardsiidae sp., C. cf. teleta, Polydora cornuta, and P. japonica recovered in fall, while recolonization by G. japonica, M. acherusicum, Armandia lanceolata, and S. benedicti japonica started later. The univoltine polychaete H. diadroma that reproduces during spring (Kikuchi and Yasuda, 2006) achieved its annual highest density in May to July, while after that the density sharply declined. Population dynamics of the polychaete P. reticulata differed from those of sympatric taxa, possibly due to negative interaction with other colonizing species (see Kanaya et al., 2015).
Fig. 4. Relationships between (a) water temperature and DO, (b) water temperature and DO saturation, and (c) sediment temperature and sedimentary H2S content at the bottom of the canal, St. B.
polluted areas (Pearson and Rosenberg, 1978; Llansó, 1991; Kodama et al., 2012; Kanaya et al., 2016b).
3.6. Seasonal changes in macrozoobenthos density and species richness At St. A, total macrozoobenthos density fluctuated from 1783 to 31237 ind. m−2 (Fig. 5). Complete defaunation did not occur, although 6
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Fig. 5. Seasonal changes in (a) the density of total macrozoobenthos and (b) species richness at St. A and B. Bars in (a) indicate SD (n = 3). n = 1 for species richness. Black ellipses indicate “not found”.
3.7. Population-level thresholds of DO and sedimentary H2S
4. Discussion
Fig. 7 shows the relationships between the density of eight macrozoobenthic taxa and DO or sedimentary H2S. Lowest concentrations of DO that allowed colonization for each species ranged from 0.3 to 2.7 mg l−1, with an average of 1.9 ± 0.9 SD mg l−1 (n = 8). Highest concentration of sedimentary H2S allowing the colonization of each species ranged from 2.5 to 5.4 mM, with an average of 3.4 ± 1.1 SD mM (n = 8).
Our study elucidated the ecological thresholds of DO and sedimentary H2S levels for opportunistic macrozoobenthos in a highly eutrophic canal, both at the population and community levels. Macrozoobenthic community structure changed distinctively in warmer months when bottom water hypoxia and sedimentary H2S accumulation were prevalent. In the Keihin canal, stratification in the water column due to the salinity gradient should significantly contribute to the development of oxygen-deficient bottom water during warmer months. High sedimentary H2S levels under the bottom water hypoxia likely caused mass mortality of sulfide-sensitive organisms (Gamenick et al., 1996; Gray et al., 2002; Hargrave et al., 2008), leading to devastation of the benthic community structure. Although many scientists have experimentally tested the toxicity of H2S on aquatic organisms under controlled rearing conditions (Gray et al., 2002), ecological thresholds of sedimentary H2S levels had not fully been assessed at the community level using field-based monitoring data. Therefore, our findings provide novel information for management and conservation of marine soft-bottom communities exposed to ongoing eutrophication. The sedimentary H2S levels at our study site (up to 8 mM in interstitial water) were comparable with or much higher than those reported from other eutrophic coastal areas (Gamenick et al., 1996; MarvinDiPasquale and Capone, 1998; Kanaya et al., 2016b). Generally, microbial sulfate reduction activity is controlled by environmental factors including temperature, sulfate supply, and the quantity and quality of organic matter in the sediment (Marvin-DiPasquale and Capone, 1998; Marvin-DiPasquale et al., 2003). However, sulfate availability is not a major limiting factor in marine-influenced estuarine sediments, due to plentiful sulfate supplied from the overlying seawater (MarvinDiPasquale and Capone, 1998). High salinity in the canal bottom (mean; 29.1 ± 1.8 SD) implies a sufficient supply of sulfate ion to support microbial sulfate reduction in the upper sediment. At our study site, sedimentation of red tide-derived phytodetritus appears to be one major causal factor for the highly reduced sediment environment. Synchronized changes in sedimentary chl. a, phaeo, and TOC contents after the phytoplankton bloom (see Fig. 3) suggest that settling phytodetritus was a major source of SOM in the canal bottom. The low (< 10) C/N ratios during warmer months also indicate the importance of microalgae-derived labile organic matter (Lamb et al., 2006). High loads of labile organic matter lead to rapid consumption of
3.8. Spatiotemporal changes in macrozoobenthic community structure Fig. 8 shows distinct seasonal changes in macrozoobenthic community structure at each station. Groups I and II consisted of samples from St. B from warmer and colder months, respectively. Group I consisted of 16 samples from June to December including six azoic samples, characterized by high H2S (4.4 mM), low DO (1.3 mg l−1), low diversity (1.3 taxa), and low density (120 ind. m−2), while group II consisted of 14 samples taken at St. B from October to May, during environmental recovery (H2S; 0.8 mM, DO; 4.9 mg l−1). The community was characterized by high diversity and population density (10.5 taxa and 10178 ind. m−2, respectively), and dominated by C. cf. teleta, P. pulchra, and G. japonica. Groups III to V consisted of samples from St. A. Group III consisted of one sample taken in August 2011, characterized by the highest density (24616 ind. m−2). Group IV consisted of 14 samples from warmer months (April to October), dominated by H. diadroma, P. reticulata, and P. japonica. Group V consisted of 15 samples from colder months (September to May), in which P. japonica, S. benedicti japonica, and C. cf. teleta dominated.
3.9. Community-level thresholds of DO and sedimentary H2S The five groups were clearly separated along DO and H2S gradients (Fig. 9). Samples from group I were characterized by low DO (0.2–2.9 mg l−1) and high H2S (1.8–8.5 mM) conditions. Samples from group II had intermediate DO (2.4–8.6 mg l−1) and low H2S (0–2.7 mM) levels. Thresholds of DO and sedimentary H2S of samples in groups I and II were 2.4–3.3 mg l−1 and 1.8–2.7 mM, respectively. Samples from groups III, IV, and V had no H2S, but fell into different DO ranges (group III; 4.7 mg l−1, group IV; 2.8–7.3 mg l−1, group V; 4.3–10.2 mg l−1). 7
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Fig. 6. Seasonal changes in the densities of 13 dominant macrozoobenthos (a) to (m) at St. A and/or St. B. Bars indicate SD (n = 3). White circles indicate absence. Scales for Y-axis were different for each plot.
duration, frequency, and intensity of red tides was a major driver of labile organic matter in the SOM pool, which supported microbial sulfate reduction activity in the canal bottom. Concentration of sedimentary H2S was positively correlated with
dissolved oxygen through aerobic degradation and acceleration of anaerobic metabolic processes in the sediment, including sulfate reduction (Hargrave et al., 2008). It would also induce oxygen-deficiency in the stagnant water body below the halocline. Therefore, the 8
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Fig. 7. Relationships between DO, sedimentary H2S, and density of eight selected macrozoobenthic taxa. Bubble size indicates density. Broken lines indicated the lowest DO and highest H2S concentration, which they could colonized (i.e. population thresholds). For Prionospio pulchra and Schistomeringos cf. rudolphi, only the data at St. B were used since they were absent from St. A.
we found that the ecological thresholds of DO and sedimentary H2S for colonization by dominant macrozoobenthic taxa (i.e., the population thresholds) were 0.3–2.8 mg l−1 and 2.5–5.4 mmol l−1, respectively (Fig. 7). Gray et al. (2002) concluded that the metabolism of marine organisms is affected by DO concentrations below 4.0 mg O2 l−1 and that mortality begins to occur in sensitive taxa below 2.0 mg O2 l−1. Vaquer-Sunyer and Duarte (2008) also provided a comprehensive review of how hypoxia affects marine organisms, and reported that ninety percent of previous experiments showed median lethal concentration (LC50) values below 4.59 mg O2 l−1. Other studies have reported similar threshold values of bottom DO for colonization by opportunistic macroinvertebrates (Ando and Kawai, 2007; Kodama et al., 2012; Villnäs et al., 2012). On the other hand, knowledge of the lethal levels of sedimentary H2S for benthic invertebrates remains scarce. Kanaya et al. (2016b) showed experimentally that 0.4–1.4 mmol l−1 of sedimentary H2S had strong negative effects on recolonization by opportunistic polychaetes using sediment-filled enclosures deployed in the field. They also discovered that a defaunation-recolonization cycle of opportunistic taxa in a eutrophic brackish lagoon (Gamo Lagoon) occurred at a H2S level of ca. 1 mmol l−1 sediment. Gamenick et al. (1996) conducted a rearing experiment and reported that the polychaete Hediste diversicolor died (median lethal time; LT50) within 10 h to 3 days in the presence of 0.27–1.0 mmol−1 H2S under hypoxic condition. Contrastingly, more sensitive taxa including oligochaetes, amphipods, and echiurans experienced mortality when reared under H2S conditions of less than 100 μmol l−1 (Gray et al., 2002). The population thresholds of sedimentary H2S identified in this study (2.5–5.4 mM) are higher than those in the previous studies. This suggests that the dominant taxa on the
mud temperature, and bottom DO was negatively correlated with bottom water temperature (see Fig. 4). These results indicate that temperature is a significant factor controlling the temporal fluctuations of DO and sedimentary H2S content. This seemed to be due to the enhanced microbial metabolism including aerobic and anaerobic degradation of organic matters in the canal bottom (Marvin-DiPasquale and Capone, 1998; Marvin-DiPasquale et al., 2003). In Keihin Canal, the mean water temperature (21.8–22.8 °C) was much higher than in Tokyo Bay (17.4–17.9 °C at surface, 15.9–16.5 °C at bottom, Ishii et al., 2008) due to the shallow and enclosed characteristics of the canal. Inflow of heated seawater from the Oi Thermal Power Station, which is about 3 km north of the study site, is other possible factor that induced high water temperature in the canal system (Nakamura et al., 2012). Ariji et al. (2008) estimated that thermal discharge may have contributed to a 2 °C increase in surface water (< 5 m deep) in the southern portion of Keihin Canal. Such anthropogenic increases in water temperature may also increase the duration and intensity of hypoxia and accelerate microbial sulfate reduction in the canal. These findings imply that increasing water temperatures associated with future climatic change (IPCC, 2013), as well as an increase in local inputs such as anthropogenic thermal discharge, may modify the duration and intensity of bottom water hypoxia and sedimentary H2S accumulation, which seemed as potential threats for soft-bottom communities in highly eutrophic coastal areas. The density of macrozoobenthos exhibited a clear seasonal fluctuation, reflecting changes in environmental quality in the canal. A sharp increase in the density and diversity of macrozoobenthos during colder months implies that post-settlement survival increases under normoxic and low-H2S conditions. Based on a 30-month field survey, 9
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Fig. 9. Relationships between monthly mean DO (mg l−1), sedimentary H2S (mM), and the five community groups, I, II, III, IV, and V, defined on the cluster dendrogram (Fig. 8). Concentrations of H2S and DO (i.e., community thresholds) that induced changes in community structure on the canal bottom, from higher diversity and density (group II) to nearly azoic and low diversity conditions (group I), are indicated by broken lines. Greyshaded areas indicate transition zone between groups I and II since samples from the two groups were overlapped along the DO and H2S gradients.
bivalves including Ruditapes philippinarum and Mactra veneriformis (common bivalves of tidalflats in inner Tokyo Bay) on the Oi artificial tidalflat using cages, and found the high mortality rates during summer hypoxia. Therefore, absence of long-lived taxa on the intertidal zone, including bivalves and decapods, may be due to the hypoxia-induced mortality during warmer months. Contrastingly, the dominant taxa in the canal bottom seemed to have ecophysiological tolerances to oxygen deficiency and sedimentary H2S. The taxon-specific responses toward H2S accumulation and hypoxia may lead to changes in macrozoobenthic community structure along gradients of DO and H2S, resulting in spatiotemporal variation in macrozoobenthic community structure in the canal system. In our study site, the community thresholds of bottom DO and sedimentary H2S were estimated as 2.4–3.3 mg l−1 and 1.8–2.7 mM (see Fig. 9), respectively, as crossing these values induced a drastic loss of macroinvertebrate diversity and abundance. Once environmental conditions exceeded these thresholds, the community became nearly azoic and few taxa were present. Vaquer-Sunyer and Duarte (2008) showed that hypoxia thresholds vary greatly across marine benthic organisms and that the use of conventional threshold (2 mg O2 l−1) is inadequate to conserve coastal biodiversity, because significant mortality could occur in many species even at higher DO levels. Among the taxa they analysed, cnidarians and annelids exhibited the highest tolerance toward hypoxia, median sublethal concentration (SLC 50) of 0.69 and 1.20 mg l−1. These agreed with the DO thresholds estimated in the present study and well explained the dominance of few polychaetes and cnidarians in the canal bottom. Shortly after environmental recovery in the canal bottom, the community was recolonized and dominated by several multivoltine taxa including polychaetes and amphipods, which resulted in the rapid recovery of density and biodiversity during colder months. Dense recolonization by opportunistic macrozoobenthos such as C. cf. teleta may facilitate the degradation of accumulated labile organic matter in the sediment through bioturbation and feeding activities (Diaz and Rosenberg, 2008; Kinoshita et al., 2008; Josefson et al., 2012). This
Fig. 8. Dendrogram created using the group average linkage method based on a BrayCurtis similarity matrix calculated from 60 samples at St. A and B from May 2010 to October 2012. Groups III to V were separated at a similarity of 55%, and group II was defined at a similarity of 75%. Other 16 samples characterized by low macrozoobenthic diversity and density, including 6 azoic samples, were defined as group I. Mean DO and sedimentary H2S contents are calculated and three dominant taxa are listed for each group.
canal bottom (Fig. 7) are potentially tolerant to sulfide toxicity, possibly through their physiological or behavioral adaptation (Vismann, 1991). At our study site, long-lived invertebrates such as bivalves and decapods were scarce, while small multivoltine taxa such as polychaetes and amphipods predominated. Vaquer-Sunyer and Duarte (2008) reported that crustaceans and bivalves were more sensitive to hypoxia than other macroinvertebrates including polychaetes, echinoderms, and cnidarians. In our study site, it had been reported that periodic hypoxia (< 2 mg l−1) occurred even at the intertidal zone in spring to fall (Kanaya et al., 2015). Nakamura et al. (2012) reared 10
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mechanism is consistent with the decrease in sediment TOC content during colder months, and thus may contribute to environmental remediation of the canal bottom. In spring, these organisms became completely absent when the sedimentary H2S and bottom DO levels exceeded community thresholds. This indicates that the benthic community in the canal bottom retains an early stage of community succession (i.e., predominance of opportunists) due to the eutrophication gradient (see Pearson and Rosenberg, 1978; Diaz and Rosenberg, 2008). Long-lived and less tolerant benthic taxa such as bivalves, gastropods, and decapods will only recolonize the canal bottom if much longer periods of normoxic and non-sulfidic conditions were assured. In Tokyo Bay, nutrient inputs from the catchment have decreased due to regulations on nutrient loading enacted based on the Guiding Principle in Countermeasures for Eutrophication in Tokyo Bay in 1982 and revision of the Water Pollution Control Law in 1993 (Kodama and Horiguchi, 2011). These measures resulted in reduction of total nitrogen and phosphorus inputs to the bay. However, loss of biodiversity associated with sediment deterioration has been an ongoing issue in inner Tokyo Bay (Kodama et al., 2012). Suppression of the frequency and intensity of phytoplankton blooms in the study area is one possible way to mitigate sediment deterioration, as settling phytoplankton were a major source of organic enrichment in bottom sediments. For future mitigation and management of such anthropogenically degraded ecosystems, ensuring DO and H2S levels stay below the community thresholds is necessary, and is particularly important for the maintenance of biodiversity and function in the shallow coastal habitats of inner Tokyo Bay.
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Acknowledgements We thank staffs at Cooperative Nihon Mikuniya provided help in field, staffs in Cooperative Nihon Kaiyo Seibutu Kenkyujyo, S Takagi, and A Oishi provided help in laboratory works. The office of Oi Central Seaside Park was acknowledged for allowing us to use the facilities. Dr. T Kondoh and Dr. W Sato-Okoshi were acknowledged for their help in idenfication of Polydora cornuta and Pseudopolydora reticulata. We are also grateful for editors and three anonymous referees for their reviewing, advising, and critical comments to the manuscript. This study was partly supported by NIES research project from National Institute for Environmental Studies (NIES) and KAKENHI (No. 21770013, 17K07580) from JSPS. References Altieri, A.H., 2008. Dead zones enhance key fisheries species by providing predation refuge. Ecology 89, 2808–2818. Altieri, A.H., Witman, J.D., 2006. Local extinction of a foundation species in a hypoxic estuary: integrating individuals to ecosystem. Ecology 87, 717–730. Andersen, F.Ø., Kristensen, E., 1992. The importance of benthic macrofauna in decomposition of microalgae in a coastal marine sediment. Limnol. Oceanogr. 37, 1392–1403. Ariji, R., Tanaka, Y., Morohoshi, K., Matsuzaka, S., Suzuki, K., 2008. Field survey on water quality and currents in southern part of Keihin Canal. Proc. Civ. Eng. Ocean 24, 627–632 (in Japanese with English abstract). Ando, H., Kawai, T., 2007. Data analysis of habitat environment of benthos in the coastal sea of Tokyo. Annual Report of the Tokyo Metropolitan Research Institute for Environmental Protection 2007, pp. 77–84 (in Japanese). Clarke, K.R., Gorley, R.N., 2006. PRIMER V6: User Manual/Tutorial. PRIMER-E, Plymouth. Como, S., Magni, P., 2009. Temporal changes of a macrobenthic assemblage in harsh lagoon sediments. Estuar. Coast Shelf Sci. 83, 638–646. Dauer, D.M., 1984. High resilience to disturbance of an estuarine polychaete community. Bull. Mar. Sci. 34, 170–174. Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33, 245–303. Diaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929. Gamenick, I., Jahn, A., Vopel, K., Giere, O., 1996. Hypoxia and sulfide as structuring factors in a macrozoobenthic community on the Baltic Sea shore: colonisation studies and tolerance experiments. Mar. Ecol. Prog. Ser. 144, 73–85. Gray, J.S., Wu, R.S., Or, Y.Y., 2002. Effects of hypoxia and organic enrichment on the coastal
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Ecological thresholds of hypoxia and sedimentary H2S in coastal soft-bottom habitats: A macroinvertebrate-based assessment Gen Kanayaa,∗, Yasuo Nakamuraa, Tomoyoshi Koizumib a b
National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan Corporative Nihon Mikuniya, 3-25-10 Mizonokuchi, Takatsu, Kawasaki, Kanagawa 213-0001, Japan
A R T I C L E I N F O
A B S T R A C T
Keywords: Eutrophication Ecosystem management Dissolved oxygen Sulphide Macrozoobenthic community Polychaete Sediment Coastal zone Tokyo Bay
Ecological thresholds of dissolved oxygen (DO) and sedimentary hydrogen sulfide (H2S) for macrozoobenthos were examined during a 30-month monitoring of two stations in a highly eutrophic canal in inner Tokyo Bay, Japan. Bottom DO and H2S concentrations fluctuated seasonally, and were significantly correlated with water and sediment temperatures. Red tide-derived phytodetritus was a major source of sediment organic matters in the canal bottom, and the sediment became highly reduced and sulfidic condition in warmer months (sedimentary H2S; up to 8.5 mM). Dominant opportunistic taxa, including polychaetes and amphipods, were eliminated under low DO and high H2S conditions (i.e., population thresholds), and devastation of community structure occurred at 2.4–3.3 mg l−1 DO and 1.8–2.7 mM H2S (i.e., community thresholds). To maintain ecosystem function in anthropogenically degraded habitats and ensure colonization by macrozoobenthos throughout the year, DO and H2S levels should be maintained below these thresholds.
1. Introduction In coastal soft-bottom habitats, macrozoobenthos are key components of the benthic community and play important roles at the sediment-water interface. Their activities facilitate the mechanical breakdown of detritus and enhance the transfer of nutrients from the sediment to the overlying water column (Levin et al., 2001). Feeding, burrowing, and bioturbation activities of macrozoobenthos can enhance the cycling of organic matter in sediment (Andersen and Kristensen, 1992; Kinoshita et al., 2008; Josefson et al., 2012). Benthic invertebrates provide important linkages between primary production and mobile predators, facilitating the transfer of energy from benthic to pelagic habitats via predator-prey relationships (Diaz and Rosenberg, 2008). During the last 100 years, anthropogenic disturbances such as reclamation and eutrophication have caused loss of biodiversity and function in marine coastal ecosystems (Lotze et al., 2006). Defaunation in coastal benthic ecosystems often induced drastic changes in material flow, productivity, food-web transfer, and species interactions at the ecosystem scale (Altieri and Witman, 2006; Altieri, 2008; Villnäs et al., 2012; Sturdivant et al., 2013). Accordingly, assuring successful colonization by benthic invertebrates is necessary to maintain ecosystem function in coastal soft-bottom communities. In eutrophic coastal waters, anthropogenic stressors such as bottom
∗
water hypoxia (e.g. < 2.0 O2 mg l−1; Gray et al., 2002) and sedimentary H2S accumulation are significant determinants of macrozoobenthic assemblage structure, through disappearance of less-tolerant taxa, decline in species diversity, and predominant of few smallbodied opportunistic species such as polychaetes (Gamenick et al., 1996; Como and Magni, 2009; Josefson et al., 2012; Kodama et al., 2012; Villnäs et al., 2012). Increasing the loading of labile organic matter enhances oxygen consumption at the sediment-water interface, resulting in the development of an oxygen-deficient water body near the seafloor (Pearson and Rosenberg, 1978). Furthermore, stratification in the water column (e.g. development of thermocline or halocline) also facilitates the development of hypoxia within the stagnant bottom layer (Murphy et al., 2011). As eutrophication proceeds, anaerobic microbial sulfate reduction prevails in the sediment, leading to accumulation of sedimentary H2S (H2S + HS− + S2−; Hargrave et al., 2008). Generally, H2S is highly toxic to most benthic invertebrates even at low concentrations, and its toxicity is enhanced under hypoxic conditions (Gray et al., 2002; Vaquer-Sunyer and Duarte, 2010). A certain groups of macroinvertebrates can cope with H2S toxicity through both of physiological and behavioral adaptations, e.g. detoxification through oxidation in their body fluid and ventilation activities through their burrow (Vismann, 1991; Sturdivant et al., 2012). However, mass mortality of benthic organisms can occur in marine sediments when the
Corresponding author. E-mail address: [email protected] (G. Kanaya).
https://doi.org/10.1016/j.marenvres.2018.02.007 Received 20 September 2017; Received in revised form 30 January 2018; Accepted 11 February 2018 0141-1136/ © 2018 Elsevier Ltd. All rights reserved.
Please cite this article as: Kanaya, G., Marine Environmental Research (2018), https://doi.org/10.1016/j.marenvres.2018.02.007
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concentration of sedimentary H2S exceeds the capability of detoxification by macroinvertebrates (Gamenick et al., 1996; Hargrave et al., 2008; Kanaya et al., 2016b). Opportunistic macrozoobenthos may play an important role as “pioneer species” after a mass-mortality event, and are important components of communities in frequently disturbed soft-bottom habitats (Dauer, 1984; Kanaya et al., 2016a,b; Kodama et al., 2012) because they recolonize quickly after defaunation and rapidly recover their population size (Dauer, 1984; Kinoshita et al., 2008; Kanaya et al., 2016a). These small-sized opportunistic taxa can help conditioning the sediment environment for large and more mature benthic taxa that colonize at later stages of community succession (Pearson and Rosenberg, 1978). These suggest that opportunistic taxa play an important role in maintaining ecosystem function during community recovery in heavily eutrophied coastal waters. Hence, it is important to understand the ecological thresholds of lethal environmental factors including bottom dissolved oxygen (DO) and sedimentary H2S necessary for these opportunistic taxa to maintain their populations and ecosystem functions. Tokyo Bay is a semi-enclosed and highly eutrophic bay located on the Pacific Coast of central Japan. In its inner portion, hypoxic bottom water prevails during the warmer months at a broad scale, leading to change and seasonal defaunation of the benthic community (Kodama et al., 2012). Recently, Yuhara et al. (2013) showed that littoral intertidal zones in the canal networks of inner Tokyo Bay provide substantial habitat for endangered macrozoobenthic species. The bottom habitat of the canal networks provides a potential refuge for macroinvertebrates from the severe hypoxia in the deeper subtidal zone of inner Tokyo Bay (Ando and Kawai, 2007). Hence, shallow littoral habitats contribute to the entire bay's macrozoobenthic biodiversity, and may provide an essential ecosystem function in the anthropogenically degraded bay system. However, anthropogenic disturbances such as sewage overflow, hypoxia, sediment deterioration, and rising water temperature due to thermal discharge are potential threats to the benthic communities in these shallow canal systems (Ando and Kawai, 2007; Maki et al., 2007; Ariji et al., 2008; Nakamura et al., 2012). In this study, a shallow canal system, Keihin Canal, was selected as a study site to conduct a 30-month survey on the relationships between anthropogenic environmental degradation and macrozoobenthic assemblage structure. Two nearby stations (about 100 m apart) were sampled in the littoral zone of the canal, along a steep gradient of DO and sediment redox state. We specifically focused on (1) documenting the seasonal changes in environmental quality of the canal bottom by assessing bottom DO, sedimentary H2S level, and sedimentary organic matter (SOM) content; and (2) resolving ecological thresholds of DO and sedimentary H2S that induced devastation of the macrozoobenthic community. We use this information to discuss the major drivers of seasonal hypoxia and sedimentary H2S accumulation in the canal bottom, with the goal of supporting future mitigation and management strategies for anthropogenically degraded coastal soft-bottom environments.
Fig. 1. Map showing the two sampling stations in the Keihin Canal, inner Tokyo Bay. Sampling was conducted monthly at St. A on the Oi artificial tidal flat (elevation; +0.7 m from Tokyo Peil [T.P.]) and St. B on the canal bottom (−2.7 m from T.P.). Salinity, DO, and water temperature were measured at St. B at two- or four-week intervals.
dissolved inorganic nitrogen (DIN; NH4++NO2−+NO3-) concentration of 226 ± 82 SD μmol l−1 (2010–2011, n = 17, authors' unpublished data). Red tides frequently occur in warmer months (Tokyo Metropolitan Government), and severe hypoxia prevails in the canal bottom from spring to fall (Ariji et al., 2008; Nakamura et al., 2012; Kanaya et al., 2015). In this study, macrozoobenthos and sediment sampling was conducted monthly in the sandy intertidal zone (+0.7 m from Tokyo Pail [T.P.], St. A) of the Oi artificial tidal flat (1.38 ha) and the muddy subtidal zone (−2.7 m from T.P., St. B). Water depth at St. B was 2.5 m during spring low tide, and most of the subtidal zone was covered by sulfidic mud (Kanaya et al., 2015). The benthic community is dominated by multivoltine polychaetes and amphipods that included taxa with opportunistic life history traits, whereas long-lived taxa such as bivalves and decapods are scarce. Massive liquefaction occurred during the 2011 Great East Japan earthquake, which resulted in an increase in the silt-clay contents of the tidal flats for several months but did not significantly affect the abundance of macrozoobenthos (Kanaya et al., 2015). 2.2. Water quality Salinity, DO, and water temperature were only monitored at St. B at 2- or 4-week intervals from April 2010 to October 2012. Measurements were taken from a pontoon during spring low tide on daytime (8: 30 to 10: 30 a.m. in most cases) using a water quality meter (Quanta, Hydrolab) at the surface (10 cm depth) and bottom (10 cm above the sediment). In this study, we defined “hypoxia” as DO < 2.0 mg l−1 and “moderate hypoxia” as DO between 2.0 and 4.0 mg l−1 (Gray et al., 2002). It should be noted here that the intensity of hypoxia at the canal surface were possibly underestimated since DO often shows diurnal fluctuation and could decrease on nighttime in warmer months (Kanaya et al., 2015). During each sampling event, three bottles of surface water were collected at St. B to measure chlorophyll a (chl. a) and phaeopigment (phaeo). In the laboratory, suspended matter in the sample was concentrated onto a GF/F after pre-filtration through a 0.125 mm mesh. Amounts of chl. a and phaeo on the filter were determined via
2. Materials and method 2.1. Study site A 30-month field survey was conducted from May 2010 to October 2012 in a shallow eutrophic brackish canal (water depth < 4 m) in inner Tokyo Bay, Keihin Canal (Fig. 1). The cement-lined canal was constructed in the mid-20th century during reclamation of the surrounding area. Tides are semidiurnal with a spring tidal range of 1.9 m. Salinity fluctuates between 20 and 30, and sometimes falls below 10 (Kanaya et al., 2013). After rainfall, urban surface runoff is discharged into the area through sewage overflow, which provides a significant source of anthropogenically derived nutrients to inner Tokyo Bay (Maki et al., 2007). The canal is highly eutrophic, with an annual average 2
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fluorometry (10-AU, Turner Designs) after extraction in 90% acetone.
2.6. Estimation of threshold levels for macrozoobenthos In this study, lethal levels of DO and sedimentary H2S were elucidated for both at population and community levels. Firstly, lethal concentrations for dominant macrozoobenthic taxa (i.e. population thresholds) were defined from the lowest DO and highest H2S concentration allowing their colonization, based on the 30 months' monitoring data (Fig. 7). For this analysis, six taxa occurring at both stations (polychaetes Pseudopolydora reticulata, Polydora cornuta, and Capitella cf. teleta, cnidarian Edwardsiidae sp., and amphipods Grandidierella japonica and Monocorophium acherusicum) and two taxa occurring at St. B (polychaetes Prionospio pulchra and Schistomeringos cf. rudolphi) were used since their population dynamics was strongly controlled by seasonal hypoxia and H2S accumulation. For the latter two taxa, only the data at St. B were used. Secondly, community thresholds that induced drastic changes in macrozoobenthic community structure on the canal bottom were elucidated from cluster analysis (Fig. 8). We elucidated DO and H2S concentrations that induced drastic changes in community structure from relatively high diversity and density of macrozoobenthos in colder months (group II) to nearly azoic and low diversity conditions in warmer months (group I, see Fig. 9).
2.3. Sediment parameters Sediment parameters including sediment temperature, redox potential (Eh), silt-clay content, chl. a, phaeo, total organic carbon (TOC), total nitrogen (TN), H2S (H2S + HS− + S2−), and acid-volatile sulfide (AVS) were measured monthly from May 2010 to October 2012 at both stations. Four sediment cores were collected at each station with a PVC corer (φ 10 cm, 50 cm length) at St. A and an acryl suspended core sampler (φ 10 cm, 50 cm length, HR type, Rigo-sha) at St. B. From the first core collected at each station, sediment temperature and Eh at a depth of 5 cm were measured immediately in situ using an ORP meter (RM-30P, TOA-DKK), and a sub-core (φ 4 cm, 10 cm deep) was taken for silt-clay analysis. From the other three cores, a sub-core (φ 4 cm, 10 cm deep) was taken from each for chl. a, phaeo, TOC, TN, H2S, and AVS analyses. In the laboratory, silt-clay content (1–4 cm deep, n = 1 for each station) was determined via wet sieving using a 0.063 mm mesh sieve after drying for 48 h at 70 °C. Sediment from 0 to 1 cm depth (n = 3 for each station) was sub-sampled for TOC and TN analysis, acidified with 1 M HCl, and freeze-dried for 24 h. These parameters were determined using an elemental analyzer (NC-2500, Finnigan Mat). Another subsample from each core (0–1 cm deep, n = 3 for each station) was used for chl. a and phaeo analyses, which were quantified by spectrophotometry at wavelengths of 665 and 750 nm (UV-1600, Shimadzu) after extraction in 90% acetone. Sediment from 1 to 4 cm in depth (n = 3 for each station) was subsampled for H2S and AVS analyses. H2S was extracted by purging with pure N2 gas for 20 min and absorbed onto 2.5% zinc acetate. Subsequently, H2S from acid-volatile insoluble sulfide (AViS) was liberated by adding 10 mL 1M HCl; sulfide in the solution was quantified by iodometry. H2S and AViS values were summed and expressed as AVS. H2S was expressed as molar content per interstitial water volume (mM) and AVS was expressed as molar content per sediment volume (mmol l−1).
3. Results 3.1. Water temperature, salinity, DO, and pigments in canal water Water temperature ranged from 11.2 to 32.2 °C (Fig. 2), with a mean value of 21.8 ± 5.4 SD °C at the surface and 22.8 ± 5.5 SD °C at the bottom (n = 46 for each). Temperature was highest in August or September and lowest in January or February of each year. Salinity was high at the canal bottom (mean; 29.1 ± 1.8 SD, n = 46) compared to those at the surface (19.7 ± 5.4 SD, n = 46). Salinity in the surface layer fluctuated widely over time, particularly in the warmer months, and halocline distinctly developed in warmer months. DO was much lower in the bottom water (bottom; 2.5 ± 2.2 SD mg l−1, surface; 5.6 ± 1.7 SD mg l−1, n = 46), which transitioned to moderate hypoxia (DO < 4.0 mg l−1) from May to December, and fell below 2.0 mg l−1 from June to October or November. Surface water also became moderately hypoxic during the warmer months. Chl. a and phaeo in the canal water rose sharply in June to September (chl. a; over 20–30 μg l−1), due to massive blooms of the diatom Skeletonema costatum (authors' unpublished data). The bloom lasted for several months, after which chl. a concentrations were low (< 5 μg l−1) from November to February.
2.4. Macrozoobenthos Macrozoobenthos were collected during each sediment sampling event. Three cores of sediment (φ 10 cm by 30 cm deep) were collected from each station (n = 3), sieved through a 1 mm mesh, and fixed in 5% neutralized formalin containing rose bengal. In the laboratory, macrozoobenthos were sorted, identified, and counted under a stereoscopic dissecting microscope. The use of 1 mm mesh sieve may underestimate the macrozoobenthic density, compared with previous studies using a 0.5 mm mesh (Sturdivant et al., 2012; Villnäs et al., 2012), since small sized opportunists often prevail in community under eutrophication (Diaz and Rosenberg, 1995).
3.2. Sediment characteristics Sediment properties at the sampling stations are summarized in Table 1. Sediment at St. A was characterized by oxidized sand (silt-clay; 11.5%), while that at St. B was highly reduced mud (silt-clay; 81.0%). At St. B, sedimentary chl. a and phaeo were about three to six times higher, and TOC, TN, and AVS were 12–13 times higher than those at St. A. High levels of H2S were detected at St. B throughout the study period (maximum; 8.5 mM), but not at St. A.
2.5. Statistical analyses Relationships between temperature and DO concentration, DO saturation, or sedimentary H2S at the canal bottom (St. B) were examined using linear regression. Spatiotemporal changes in community structure were examined through cluster analysis using the software PRIMER ver. 6.2 (Clarke and Gorley, 2006). Square-root-transformed densities of macrozoobenthos were used for analysis. Samples were clustered with a group average linkage method based on a Bray–Curtis similarity matrix, in which five sample groups were defined. Total macrozoobenthic density, number of taxa, sedimentary H2S content, and DO were averaged for each group. Surface- and bottom-DO data were used in analyses for St. A and B, respectively.
3.3. Temporal fluctuation in pigments, organic matter, and sulfides in sediment Sedimentary chl. a and phaeo contents at the canal bottom and intertidal zone corresponded well to those in the water column (Fig. 3). Sedimentary phaeo reached its annual peak in summer to fall (16–63 μg cm−2 at St. A, 100–250 μg cm−2 at St. B), shortly after the phytoplankton bloom. Seasonal changes in sedimentary TOC at St. B corresponded well to changes in sedimentary phaeo content. TOC was highest in August to October (over 50–75 mg g−1) and gradually 3
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Fig. 2. Seasonal changes in (a) water temperature, (b) salinity, and (c) DO at the surface and bottom (−2.6 m from T.P.) of the Keihin Canal (St. B). (d) Concentrations of pigments (chl. a and phaeo) in surface water at St. B were also shown. Bars in (d) mean SD (n = 3). n = 1 for other plots.
with its highest annual values in summer (5.3–8.5 mM) and lowest in winter to spring (< 0.5 mM). At St. A, H2S was not detected, and AVS was low over most of the study period. At St. A, pulsed increases in AVS occurred after March 2011 due to mud boiling during the 2011 earthquake (see Kanaya et al., 2015). At St. B, AVS was much higher than at St. A and increased sharply in the warmer months, corresponding to the increase in sedimentary H2S.
Table 1 Sediment characteristics at St. A and B. Mean, standard deviation (SD), and maximum (max.) values are calculated from data collected from May 2010 to October 2012. Variables
Silt-clay (%) Eh (mV) Chl. a (μg cm−2) phaeo (μg cm−2) TOC (mg g−1) TN (mg g−1) C/N atom H2S (mM) AVS (mmol l−1)
Intertidal zone (St. A)
Subtidal zone (St. B)
mean
max.
mean
(SD)
max.
69.5 421 18.3 79.2 17.1 1.46 17.6
81.0 −164 15.9 96.0 50.9 5.9 10.3 2.7 27.1
(8.4) (67) (13.9) (75.2) (12.3) (2.2) (1.6) (2.3) (9.2)
93.6 93.1 64.8 356 87.2 13.1 16.8 8.5 44.9
(SD)
11.5 (15.9) 235 (104) 5.6 (4.3) 15.8 (14.9) 3.9 (2.5) 0.43 (0.20) 10.1 (2.3) not detected 2.2 (3.8)
12.9
n
30 29 29 29 29 29 29 30 30
3.4. Relationships of water temperature to bottom DO and sedimentary H2S DO and sedimentary H2S in the canal bottom were significantly correlated with temperature (Fig. 4). Bottom DO concentration was negatively correlated with bottom water temperature (BWT), as expressed in Equation (1):
Bottom DO (mg l−1) = −0.354 BWT + 10.5 decreased into winter. The C/N ratio at St. B fluctuated seasonally, showing an inverse trend to sedimentary TOC. This ratio was below 10 in summer to fall when the TOC content increased, and gradually increased toward winter as TOC decreased. On the other hand, seasonal changes in sedimentary TOC at St. A was different from those at St. B. This should be due to the deposition of muddy sediment onto the tidalflat through massive liquefaction during the 2011 Great East Japan earthquake in March 2011. At St. B, sedimentary H2S exhibited a clear seasonal fluctuation,
(1)
Bottom water in the canal reached moderate hypoxia (DO < 4.0 mg l−1) when BWT exceeded 18.4 °C and hypoxia (DO < 2.0 mg l−1) when BWT exceeded 24.0 °C. Negative relationship was also found between bottom DO saturation and BWT as:
Bottom DO saturation (%) = −3.91 BWT + 120
(2)
Sedimentary H2S was positively correlated with sediment temperature (ST), as described by Equation (3): 4
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Fig. 3. Seasonal changes in sediment parameters including (a) pigments (chl. a and phaeo), (b) TOC and C/N, (c) H2S, and (d) AVS at St. A and B. Bars indicate SD (n = 3). H2S was not detected at St. A throughout the period. H2S and AVS are respective denoted as molar content per interstitial water volume (mM) and per sediment volume (mmol l−1).
Sedimentary H2 S (mM) = 0.308 ST − 3.90
14830 ind. m−2, St. B; 4806 ind. m−2). The polychaetes Prionospio japonica, Hediste diadroma, P. reticulata, and Streblospio benedicti japonica were the first to fourth dominant taxa at St. A, while the polychaetes C. cf. teleta and P. pulchra and the amphipods G. japonica and M. acherusicum were the most dominant taxa at St. B. Several dominant taxa occurred at both stations, including Edwardsiidae sp., P. reticulata, P. cornuta, C. cf. telata, G. japonica, and M. acherusicum. Polychaetes S. cf. rudolphi and P. pulchra occurred only at St. B, while seven taxa in Table 2 including H. diadroma, P. japonica, and S. benedicti japonica were unique to St. A. Of the dominant taxa in Table 2, only two species, H. diadroma (dominant at St. A) and N. succinea (dominant at St. B), are univoltine (Hardege et al., 1990; Kikuchi and Yasuda, 2006), while all other dominant taxa appear to have multivoltine life cycles. Several of them had been reported as an opportunistic species that commonly occurred in frequently disturbed soft-bottom habitats including organically
(3)
A 1 °C increase in ST corresponded to a 0.308 mM increase in sedimentary H2S. We also found a significant positive correlation (r = 0.976, n = 30, p < 0.001, data not shown in figure) between ST and BWT, as shown in Equation (4):
ST (°C) = 0.925 BWT + 1.30
(4)
3.5. Composition of macrozoobenthos A total of 48 and 36 taxa occurred during the study period at St. A and B, respectively (Table 2). Polychaetes dominated the community numerically at both stations (86–93%), followed by amphipods (4.3–6.2%) and bivalves (0.3–5.3%). The mean density of total macrozoobenthos was about three times higher at the intertidal zone (St. A; 5
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Table 2 Average density (ind. m−2) and proportion (%) of dominant macrozoobenthos at St. A and B during the study period. Average density for each taxonomic group and all taxa are also shown. Taxa
Cnidaria Edwardsiidae sp. Nemertinea Nemertinea sp. Bivalva Musculus senhousia Arthritica reikoae Ruditapes philippinarum Polychaeta Sigambra tentaculata Eteone longa Hediste diadroma Neamthes succinea Schistomeringos cf. rudolphi Prionospio japonica P. pulchra Streblospio benedicti japonica Rhynchospio glutaea Pseudopolydora reticulata Polydora cornuta Armandia lanceolata Capitella cf. teleta Heteromastus sp. Amphipoda Ampithoe valida Grandidierella japonica Monocorophium acherusicum Bivalva Polychaeta Amphipoda Other Total macrozoobenthos Taxa occurred
Density/% St. A
St. B
191/13
69/1.4
105/0.7
6/0.13
285/1.9 265/1.8 88/0.6
2/0.0 – 2/0.0
14/0.1 111/0.7 2855/19.2 6/0.9 – 3287/22.2 – 1202/8.1 185/1.2 2475/16.7 789/5.3 304/2.1 1071/7.2 390/2.6
37/0.8 3/0.1 – 45/0.9 54/1.1 – 272/5.7 – – 14/0.3 26/0.5 – 3929/81.8 –
1/0.0 479/3.2 441/3.0 784/5.3 12774/86 924/6.2 301/2.4 14830 48
26/0.5 89/1.9 86/1.8 17/0.3 4469/93 207/4.3 77/2.4 4806 36
−; not observed. Common taxa in each station (> 0.5% to total) are listed with eight dominant taxa for each station bolded.
density sharply declined in the warmer months. At St. B, macrozoobenthos were nearly absent from June to December when sedimentary H2S exceeded 2 mM (Fig. 3c). Their density increased sharply in winter to spring, and reached its annual maximum in March or April (up to 46180 ind. m−2). Species richness at St. A fluctuated from 11 to 23 taxa, and declined in the warmer months. At St. B, species richness declined sharply in June to November (< 5 taxa), and increased from November to May (up to 17 taxa). Temporal changes in the densities of dominant taxa are shown in Fig. 6. At St. B, these taxa exhibited a clear seasonal defaunation-recolonization cycle. They almost disappeared from early summer to late fall, and then recolonized and rapidly increased their population sizes in winter to spring, achieving their highest densities in February to May. At St. A, long-term defaunation did not occur despite densities declining during May to September. The population sizes of several taxa including Edwardsiidae sp., C. cf. teleta, Polydora cornuta, and P. japonica recovered in fall, while recolonization by G. japonica, M. acherusicum, Armandia lanceolata, and S. benedicti japonica started later. The univoltine polychaete H. diadroma that reproduces during spring (Kikuchi and Yasuda, 2006) achieved its annual highest density in May to July, while after that the density sharply declined. Population dynamics of the polychaete P. reticulata differed from those of sympatric taxa, possibly due to negative interaction with other colonizing species (see Kanaya et al., 2015).
Fig. 4. Relationships between (a) water temperature and DO, (b) water temperature and DO saturation, and (c) sediment temperature and sedimentary H2S content at the bottom of the canal, St. B.
polluted areas (Pearson and Rosenberg, 1978; Llansó, 1991; Kodama et al., 2012; Kanaya et al., 2016b).
3.6. Seasonal changes in macrozoobenthos density and species richness At St. A, total macrozoobenthos density fluctuated from 1783 to 31237 ind. m−2 (Fig. 5). Complete defaunation did not occur, although 6
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Fig. 5. Seasonal changes in (a) the density of total macrozoobenthos and (b) species richness at St. A and B. Bars in (a) indicate SD (n = 3). n = 1 for species richness. Black ellipses indicate “not found”.
3.7. Population-level thresholds of DO and sedimentary H2S
4. Discussion
Fig. 7 shows the relationships between the density of eight macrozoobenthic taxa and DO or sedimentary H2S. Lowest concentrations of DO that allowed colonization for each species ranged from 0.3 to 2.7 mg l−1, with an average of 1.9 ± 0.9 SD mg l−1 (n = 8). Highest concentration of sedimentary H2S allowing the colonization of each species ranged from 2.5 to 5.4 mM, with an average of 3.4 ± 1.1 SD mM (n = 8).
Our study elucidated the ecological thresholds of DO and sedimentary H2S levels for opportunistic macrozoobenthos in a highly eutrophic canal, both at the population and community levels. Macrozoobenthic community structure changed distinctively in warmer months when bottom water hypoxia and sedimentary H2S accumulation were prevalent. In the Keihin canal, stratification in the water column due to the salinity gradient should significantly contribute to the development of oxygen-deficient bottom water during warmer months. High sedimentary H2S levels under the bottom water hypoxia likely caused mass mortality of sulfide-sensitive organisms (Gamenick et al., 1996; Gray et al., 2002; Hargrave et al., 2008), leading to devastation of the benthic community structure. Although many scientists have experimentally tested the toxicity of H2S on aquatic organisms under controlled rearing conditions (Gray et al., 2002), ecological thresholds of sedimentary H2S levels had not fully been assessed at the community level using field-based monitoring data. Therefore, our findings provide novel information for management and conservation of marine soft-bottom communities exposed to ongoing eutrophication. The sedimentary H2S levels at our study site (up to 8 mM in interstitial water) were comparable with or much higher than those reported from other eutrophic coastal areas (Gamenick et al., 1996; MarvinDiPasquale and Capone, 1998; Kanaya et al., 2016b). Generally, microbial sulfate reduction activity is controlled by environmental factors including temperature, sulfate supply, and the quantity and quality of organic matter in the sediment (Marvin-DiPasquale and Capone, 1998; Marvin-DiPasquale et al., 2003). However, sulfate availability is not a major limiting factor in marine-influenced estuarine sediments, due to plentiful sulfate supplied from the overlying seawater (MarvinDiPasquale and Capone, 1998). High salinity in the canal bottom (mean; 29.1 ± 1.8 SD) implies a sufficient supply of sulfate ion to support microbial sulfate reduction in the upper sediment. At our study site, sedimentation of red tide-derived phytodetritus appears to be one major causal factor for the highly reduced sediment environment. Synchronized changes in sedimentary chl. a, phaeo, and TOC contents after the phytoplankton bloom (see Fig. 3) suggest that settling phytodetritus was a major source of SOM in the canal bottom. The low (< 10) C/N ratios during warmer months also indicate the importance of microalgae-derived labile organic matter (Lamb et al., 2006). High loads of labile organic matter lead to rapid consumption of
3.8. Spatiotemporal changes in macrozoobenthic community structure Fig. 8 shows distinct seasonal changes in macrozoobenthic community structure at each station. Groups I and II consisted of samples from St. B from warmer and colder months, respectively. Group I consisted of 16 samples from June to December including six azoic samples, characterized by high H2S (4.4 mM), low DO (1.3 mg l−1), low diversity (1.3 taxa), and low density (120 ind. m−2), while group II consisted of 14 samples taken at St. B from October to May, during environmental recovery (H2S; 0.8 mM, DO; 4.9 mg l−1). The community was characterized by high diversity and population density (10.5 taxa and 10178 ind. m−2, respectively), and dominated by C. cf. teleta, P. pulchra, and G. japonica. Groups III to V consisted of samples from St. A. Group III consisted of one sample taken in August 2011, characterized by the highest density (24616 ind. m−2). Group IV consisted of 14 samples from warmer months (April to October), dominated by H. diadroma, P. reticulata, and P. japonica. Group V consisted of 15 samples from colder months (September to May), in which P. japonica, S. benedicti japonica, and C. cf. teleta dominated.
3.9. Community-level thresholds of DO and sedimentary H2S The five groups were clearly separated along DO and H2S gradients (Fig. 9). Samples from group I were characterized by low DO (0.2–2.9 mg l−1) and high H2S (1.8–8.5 mM) conditions. Samples from group II had intermediate DO (2.4–8.6 mg l−1) and low H2S (0–2.7 mM) levels. Thresholds of DO and sedimentary H2S of samples in groups I and II were 2.4–3.3 mg l−1 and 1.8–2.7 mM, respectively. Samples from groups III, IV, and V had no H2S, but fell into different DO ranges (group III; 4.7 mg l−1, group IV; 2.8–7.3 mg l−1, group V; 4.3–10.2 mg l−1). 7
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Fig. 6. Seasonal changes in the densities of 13 dominant macrozoobenthos (a) to (m) at St. A and/or St. B. Bars indicate SD (n = 3). White circles indicate absence. Scales for Y-axis were different for each plot.
duration, frequency, and intensity of red tides was a major driver of labile organic matter in the SOM pool, which supported microbial sulfate reduction activity in the canal bottom. Concentration of sedimentary H2S was positively correlated with
dissolved oxygen through aerobic degradation and acceleration of anaerobic metabolic processes in the sediment, including sulfate reduction (Hargrave et al., 2008). It would also induce oxygen-deficiency in the stagnant water body below the halocline. Therefore, the 8
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Fig. 7. Relationships between DO, sedimentary H2S, and density of eight selected macrozoobenthic taxa. Bubble size indicates density. Broken lines indicated the lowest DO and highest H2S concentration, which they could colonized (i.e. population thresholds). For Prionospio pulchra and Schistomeringos cf. rudolphi, only the data at St. B were used since they were absent from St. A.
we found that the ecological thresholds of DO and sedimentary H2S for colonization by dominant macrozoobenthic taxa (i.e., the population thresholds) were 0.3–2.8 mg l−1 and 2.5–5.4 mmol l−1, respectively (Fig. 7). Gray et al. (2002) concluded that the metabolism of marine organisms is affected by DO concentrations below 4.0 mg O2 l−1 and that mortality begins to occur in sensitive taxa below 2.0 mg O2 l−1. Vaquer-Sunyer and Duarte (2008) also provided a comprehensive review of how hypoxia affects marine organisms, and reported that ninety percent of previous experiments showed median lethal concentration (LC50) values below 4.59 mg O2 l−1. Other studies have reported similar threshold values of bottom DO for colonization by opportunistic macroinvertebrates (Ando and Kawai, 2007; Kodama et al., 2012; Villnäs et al., 2012). On the other hand, knowledge of the lethal levels of sedimentary H2S for benthic invertebrates remains scarce. Kanaya et al. (2016b) showed experimentally that 0.4–1.4 mmol l−1 of sedimentary H2S had strong negative effects on recolonization by opportunistic polychaetes using sediment-filled enclosures deployed in the field. They also discovered that a defaunation-recolonization cycle of opportunistic taxa in a eutrophic brackish lagoon (Gamo Lagoon) occurred at a H2S level of ca. 1 mmol l−1 sediment. Gamenick et al. (1996) conducted a rearing experiment and reported that the polychaete Hediste diversicolor died (median lethal time; LT50) within 10 h to 3 days in the presence of 0.27–1.0 mmol−1 H2S under hypoxic condition. Contrastingly, more sensitive taxa including oligochaetes, amphipods, and echiurans experienced mortality when reared under H2S conditions of less than 100 μmol l−1 (Gray et al., 2002). The population thresholds of sedimentary H2S identified in this study (2.5–5.4 mM) are higher than those in the previous studies. This suggests that the dominant taxa on the
mud temperature, and bottom DO was negatively correlated with bottom water temperature (see Fig. 4). These results indicate that temperature is a significant factor controlling the temporal fluctuations of DO and sedimentary H2S content. This seemed to be due to the enhanced microbial metabolism including aerobic and anaerobic degradation of organic matters in the canal bottom (Marvin-DiPasquale and Capone, 1998; Marvin-DiPasquale et al., 2003). In Keihin Canal, the mean water temperature (21.8–22.8 °C) was much higher than in Tokyo Bay (17.4–17.9 °C at surface, 15.9–16.5 °C at bottom, Ishii et al., 2008) due to the shallow and enclosed characteristics of the canal. Inflow of heated seawater from the Oi Thermal Power Station, which is about 3 km north of the study site, is other possible factor that induced high water temperature in the canal system (Nakamura et al., 2012). Ariji et al. (2008) estimated that thermal discharge may have contributed to a 2 °C increase in surface water (< 5 m deep) in the southern portion of Keihin Canal. Such anthropogenic increases in water temperature may also increase the duration and intensity of hypoxia and accelerate microbial sulfate reduction in the canal. These findings imply that increasing water temperatures associated with future climatic change (IPCC, 2013), as well as an increase in local inputs such as anthropogenic thermal discharge, may modify the duration and intensity of bottom water hypoxia and sedimentary H2S accumulation, which seemed as potential threats for soft-bottom communities in highly eutrophic coastal areas. The density of macrozoobenthos exhibited a clear seasonal fluctuation, reflecting changes in environmental quality in the canal. A sharp increase in the density and diversity of macrozoobenthos during colder months implies that post-settlement survival increases under normoxic and low-H2S conditions. Based on a 30-month field survey, 9
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Fig. 9. Relationships between monthly mean DO (mg l−1), sedimentary H2S (mM), and the five community groups, I, II, III, IV, and V, defined on the cluster dendrogram (Fig. 8). Concentrations of H2S and DO (i.e., community thresholds) that induced changes in community structure on the canal bottom, from higher diversity and density (group II) to nearly azoic and low diversity conditions (group I), are indicated by broken lines. Greyshaded areas indicate transition zone between groups I and II since samples from the two groups were overlapped along the DO and H2S gradients.
bivalves including Ruditapes philippinarum and Mactra veneriformis (common bivalves of tidalflats in inner Tokyo Bay) on the Oi artificial tidalflat using cages, and found the high mortality rates during summer hypoxia. Therefore, absence of long-lived taxa on the intertidal zone, including bivalves and decapods, may be due to the hypoxia-induced mortality during warmer months. Contrastingly, the dominant taxa in the canal bottom seemed to have ecophysiological tolerances to oxygen deficiency and sedimentary H2S. The taxon-specific responses toward H2S accumulation and hypoxia may lead to changes in macrozoobenthic community structure along gradients of DO and H2S, resulting in spatiotemporal variation in macrozoobenthic community structure in the canal system. In our study site, the community thresholds of bottom DO and sedimentary H2S were estimated as 2.4–3.3 mg l−1 and 1.8–2.7 mM (see Fig. 9), respectively, as crossing these values induced a drastic loss of macroinvertebrate diversity and abundance. Once environmental conditions exceeded these thresholds, the community became nearly azoic and few taxa were present. Vaquer-Sunyer and Duarte (2008) showed that hypoxia thresholds vary greatly across marine benthic organisms and that the use of conventional threshold (2 mg O2 l−1) is inadequate to conserve coastal biodiversity, because significant mortality could occur in many species even at higher DO levels. Among the taxa they analysed, cnidarians and annelids exhibited the highest tolerance toward hypoxia, median sublethal concentration (SLC 50) of 0.69 and 1.20 mg l−1. These agreed with the DO thresholds estimated in the present study and well explained the dominance of few polychaetes and cnidarians in the canal bottom. Shortly after environmental recovery in the canal bottom, the community was recolonized and dominated by several multivoltine taxa including polychaetes and amphipods, which resulted in the rapid recovery of density and biodiversity during colder months. Dense recolonization by opportunistic macrozoobenthos such as C. cf. teleta may facilitate the degradation of accumulated labile organic matter in the sediment through bioturbation and feeding activities (Diaz and Rosenberg, 2008; Kinoshita et al., 2008; Josefson et al., 2012). This
Fig. 8. Dendrogram created using the group average linkage method based on a BrayCurtis similarity matrix calculated from 60 samples at St. A and B from May 2010 to October 2012. Groups III to V were separated at a similarity of 55%, and group II was defined at a similarity of 75%. Other 16 samples characterized by low macrozoobenthic diversity and density, including 6 azoic samples, were defined as group I. Mean DO and sedimentary H2S contents are calculated and three dominant taxa are listed for each group.
canal bottom (Fig. 7) are potentially tolerant to sulfide toxicity, possibly through their physiological or behavioral adaptation (Vismann, 1991). At our study site, long-lived invertebrates such as bivalves and decapods were scarce, while small multivoltine taxa such as polychaetes and amphipods predominated. Vaquer-Sunyer and Duarte (2008) reported that crustaceans and bivalves were more sensitive to hypoxia than other macroinvertebrates including polychaetes, echinoderms, and cnidarians. In our study site, it had been reported that periodic hypoxia (< 2 mg l−1) occurred even at the intertidal zone in spring to fall (Kanaya et al., 2015). Nakamura et al. (2012) reared 10
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mechanism is consistent with the decrease in sediment TOC content during colder months, and thus may contribute to environmental remediation of the canal bottom. In spring, these organisms became completely absent when the sedimentary H2S and bottom DO levels exceeded community thresholds. This indicates that the benthic community in the canal bottom retains an early stage of community succession (i.e., predominance of opportunists) due to the eutrophication gradient (see Pearson and Rosenberg, 1978; Diaz and Rosenberg, 2008). Long-lived and less tolerant benthic taxa such as bivalves, gastropods, and decapods will only recolonize the canal bottom if much longer periods of normoxic and non-sulfidic conditions were assured. In Tokyo Bay, nutrient inputs from the catchment have decreased due to regulations on nutrient loading enacted based on the Guiding Principle in Countermeasures for Eutrophication in Tokyo Bay in 1982 and revision of the Water Pollution Control Law in 1993 (Kodama and Horiguchi, 2011). These measures resulted in reduction of total nitrogen and phosphorus inputs to the bay. However, loss of biodiversity associated with sediment deterioration has been an ongoing issue in inner Tokyo Bay (Kodama et al., 2012). Suppression of the frequency and intensity of phytoplankton blooms in the study area is one possible way to mitigate sediment deterioration, as settling phytoplankton were a major source of organic enrichment in bottom sediments. For future mitigation and management of such anthropogenically degraded ecosystems, ensuring DO and H2S levels stay below the community thresholds is necessary, and is particularly important for the maintenance of biodiversity and function in the shallow coastal habitats of inner Tokyo Bay.
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Acknowledgements We thank staffs at Cooperative Nihon Mikuniya provided help in field, staffs in Cooperative Nihon Kaiyo Seibutu Kenkyujyo, S Takagi, and A Oishi provided help in laboratory works. The office of Oi Central Seaside Park was acknowledged for allowing us to use the facilities. Dr. T Kondoh and Dr. W Sato-Okoshi were acknowledged for their help in idenfication of Polydora cornuta and Pseudopolydora reticulata. We are also grateful for editors and three anonymous referees for their reviewing, advising, and critical comments to the manuscript. This study was partly supported by NIES research project from National Institute for Environmental Studies (NIES) and KAKENHI (No. 21770013, 17K07580) from JSPS. References Altieri, A.H., 2008. Dead zones enhance key fisheries species by providing predation refuge. Ecology 89, 2808–2818. Altieri, A.H., Witman, J.D., 2006. Local extinction of a foundation species in a hypoxic estuary: integrating individuals to ecosystem. Ecology 87, 717–730. Andersen, F.Ø., Kristensen, E., 1992. The importance of benthic macrofauna in decomposition of microalgae in a coastal marine sediment. Limnol. Oceanogr. 37, 1392–1403. Ariji, R., Tanaka, Y., Morohoshi, K., Matsuzaka, S., Suzuki, K., 2008. Field survey on water quality and currents in southern part of Keihin Canal. Proc. Civ. Eng. Ocean 24, 627–632 (in Japanese with English abstract). Ando, H., Kawai, T., 2007. Data analysis of habitat environment of benthos in the coastal sea of Tokyo. Annual Report of the Tokyo Metropolitan Research Institute for Environmental Protection 2007, pp. 77–84 (in Japanese). Clarke, K.R., Gorley, R.N., 2006. PRIMER V6: User Manual/Tutorial. PRIMER-E, Plymouth. Como, S., Magni, P., 2009. Temporal changes of a macrobenthic assemblage in harsh lagoon sediments. Estuar. Coast Shelf Sci. 83, 638–646. Dauer, D.M., 1984. High resilience to disturbance of an estuarine polychaete community. Bull. Mar. Sci. 34, 170–174. Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33, 245–303. Diaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929. Gamenick, I., Jahn, A., Vopel, K., Giere, O., 1996. Hypoxia and sulfide as structuring factors in a macrozoobenthic community on the Baltic Sea shore: colonisation studies and tolerance experiments. Mar. Ecol. Prog. Ser. 144, 73–85. Gray, J.S., Wu, R.S., Or, Y.Y., 2002. Effects of hypoxia and organic enrichment on the coastal
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