Journal of Environmental Quality 30:291-302 (2001)
© 2001 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
ARTICLE
SYMPOSIUM PAPER
Oxygen-Deficient Waters along the Japanese Coast and Their Effects upon the Estuarine Ecosystem
Teruaki Suzuki
Aichi Fisheries Research Institute, 97, Wakamiya, Miya-cho, Gamagori, 443, Japan
Corresponding author (suishi{at}pref.aichi.jp)
Received for publication July 14, 2000.
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ABSTRACT
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Development of hypoxia in Japan has been confirmed in the inner part of almost every major bay of Japan on the Pacific Coast from Tokyo southward. This paper presents multiple aspects (present condition, hydraulic mechanism, effect upon fisheries, historical progress and nutrient budget between sediment and water) using Mikawa Bay, where Japan's most serious hypoxia occurs, as an example. Although hypoxia basically results from the increase of nutrient load input from domestic and livestock sources, the intense reclamation of shallows (including tidal flats) and the large reduction in river flow due to farmland irrigation drastically accelerated dissolved oxygen deficiency. Oxygen-deficient waters in Mikawa Bay are large enough to strip the water purification capacity of the remaining shallows. Unfortunately, the shallows have turned from a purifier to a source of nutrient load. These conditions are more or less common in all bays where the dissolved oxygen–deficient waters have been reported. To break this cycle, dissolved oxygen deficiency must be contained to the extent that the purification capacity of the shallows can be restored to an efficient level. For this purpose, the first thing to do is to restore tidal flats over an extensive area and to recover sufficient water flow, which may be a more urgent imperative than reducing the nutrient load input.
Abbreviations: DIN, dissolved inorganic nitrogen • PON, particulate organic nitrogen • TN, total nitrogen
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INTRODUCTION
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SINCE THE 1970s, there have been reports about severe damages to fisheries caused by hypoxia in various coastal waters of Japan. Figure 1
shows the major sea areas where oxygen-deficient water masses occur and have been reported with descriptions of the mechanism causing their development (Joh, 1986, 1989; Ochi and Takeoka, 1986; Suzuki and Matsukawa, 1987; Iizuka and Min, 1989; Onizuka, 1989; Sasaki, 1989; Yuasa, 1994; Hara et al., 1995; Ishida and Hara, 1996; Takasugi et al., 1996; Kamizono et al., 1996). Development of oxygen-deficient waters has been confirmed in the inner part of almost every major bay of Japan on the Pacific Coast from Tokyo southward.
Oxygen-deficient waters deal a deadly blow not only to benthic organisms, but also to several aquaculture species. Oxygen-deficient waters sometimes upwell in coastal areas and totally destroy fishery resources such as bivalves. This phenomenon is known as Niga-shio ("bitter tide") in Mikawa Bay or Ao-shio ("blue tide") in Tokyo Bay.
The following is a report on several aspects of hypoxia in bays of Japan.
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CAUSES OF OXYGEN-DEFICIENT WATER MASS DEVELOPMENT
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There are three major artificial causes that can produce oxygen-deficient water masses:- increase of nutrient load input that raises primary production (red tide);
- reclamation of shallow water areas, including tidal flats, that impairs their water purification functionality; and
- reduction of fresh water inflow to sea areas and the resulting lower rate of exchange with sea water.
The importance of these factors varies with sea area. However, in some areas, such as Omura Bay and Beppu Bay, the chief cause is not artificial eutrophication but topographical features.
In regard to (i), quantitative correlation between the development of oxygen-deficient water masses and nutrient load varies significantly from bay to bay. This is because the supply of oxygen is chiefly dependent on the inflow of external sea water in the lower layer through the bay mouth, and that inflow is determined largely by the inherent hydraulic structure of individual bays. An extreme example of this occurs in Mikawa Bay, where Japan's most serious dissolved oxygen deficiency occurs in spite of having the least nutrient load input, as shown in Fig. 2
. This is attributable to the effect of reclamation (ii) and a reduction of fresh water inflow (iii), which has turned out to be more serious than in other sea areas.
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Fig. 2. Nutrient load input to major bays (Tokyo, Osaka, Ise, and Mikawa) where dissolved oxygen–deficient water masses are known to develop
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Breakdown of the nutrient load composition is also important. Figure 3
shows the breakdown of nitrogen and phosphorus input into four major bays in Japan (Tokyo Bay, Osaka Bay, Ise Bay, and Mikawa Bay). In the legend, dom. and ind. show the input load from domestic and industrial sources, respectively. The main subject of this workshop (that is, load coming from agricultural sources including livestock) is classified as agri. etc in the statistics, but strictly speaking, this category includes inputs from forests and other land use.
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Fig. 3. Breakdown by source of nutrient loads to major bays (Tokyo, Osaka, Ise, and Mikawa) where dissolved oxygen–deficient water masses occur
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In regard to nitrogen, the chief source in Tokyo Bay is from domestic waste, which accounts for 66% of inputs. In Osaka Bay, industrial input (43%) is as important as domestic input (46%). In Ise Bay, domestic (37%), industrial (27%), and agriculture (36%) inputs nearly match. In Mikawa Bay, domestic (41%) and agriculture (40%) are the two chief sources of nutrients, while the portion of nitrogen originating from industry is considerably lower in comparison with other areas. Within the agri. etc category of Mikawa Bay, livestock accounts for 66%, while the contribution from agricultural sources such as vegetable, fruit, and rice production is estimated to be about 21%.
In regard to phosphorus, input source breakdowns for Tokyo, Osaka, and Ise Bays are not much different than those of nitrogen; however, in Mikawa Bay, agri. etc contributes a much higher phosphorus load than it does for nitrogen. The agri. etc category of Mikawa Bay is further broken down to an estimated 50% for livestock and 40% for agriculture. Thus, the agriculture factor is significant here.
In the following, I report details of the effect from dissolved oxygen–deficient water upon fisheries, the hydraulic mechanism of dissolved-oxygen deficiency and its historical progress, and the effect upon nitrogen circulation in the sediment and nitrogen budget between sediment and water column that intensify eutrophication, with Mikawa bay as an example.
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DISSOLVED OXYGEN DEFICIENCY IN MIKAWA BAY
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Mikawa Bay is a typical, partially mixed estuary located in the central part of Japan, as shown in Fig. 4
. Mikawa Bay consists of two inlets. The northwest part is Chita Bay, into which the Yahagi-gawa River flows. The eastern part is Atsumi Bay, into which the Toyokawa River flows. In its entirety, Mikawa Bay measures about 500 km2 and is very shallow, with an average depth of 10 m.
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OCEANOGRAPHIC CONDITIONS INVOLVED IN THE DEVELOPMENT OF OXYGEN-DEFICIENT WATER MASSES
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Figure 5
shows the vertical distribution of the residual currents along the longer axis of Mikawa Bay. The figure was calculated using data collected in the summer and without incorporating wind conditions using a multilevel hydrodynamic model (Suzuki and Terasawa, 1997). Surface water above the pycnocline, which exists at about 5 m below the surface, flows out from the inner part of the bay toward the mouth, while below the pycnocline, water flows into the bay from the mouth. From the middle to the inner part of the bay, an upwelling area occurs, whereas a notable downwelling area exists at the mouth of the bay, forming a remarkable vertical circulation. The vertical circulation is basically maintained by the density flow, which is formed by river water flowing into the bay. In the upwelling area, inorganic nutrients supplied from the bottom layer accelerate photosynthesis, which produces particulate organic matter.
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Fig. 5. Vertical distribution of residual currents in Mikawa Bay in summer calculated by a hydrodynamic model
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In the downwelling area, sedimentation and decomposition of the particulate organic matter is accelerated. Although such oceanographic conditions are common in estuaries, in Mikawa Bay, the tendency towards a semi-enclosed circulation of nutrient matter is more significant than in other sea areas. The existence of the downwelling area near the bay mouth is also confirmed by the box model analysis of the salt budget (Suzuki and Matsukawa, 1987). Also, the downwelling area was shown to have the highest dissolved oxygen consumption rate under the pycnocline in Mikawa Bay, according to the analysis of dissolved oxygen budget (Suzuki and Matsukawa, 1987). The mechanism of severe eutrophication in Mikawa Bay was also studied in detail by the analysis of the budget and circulation of nitrogen and phosphorus by Matsukawa and Suzuki (1985).
Figure 6
shows an example of the vertical distribution of dissolved oxygen concentration in summer in Mikawa Bay (Suzuki and Terasawa, 1997). Figure 6 shows that seawater, rich in dissolved oxygen, flows in from the bay mouth, but the lower layer of the middle to the inner part of the bay consumes that oxygen during decomposition of organic matter derived from the upper layers and bottom sediment.
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EFFECT UPON FISHERIES
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Oxygen-deficient water occurs in Mikawa Bay on a large scale as seen in the example shown in Fig. 7
(Ishida and Hara, 1996). Deficiencies can last as long as approximately four months or more from the middle of June to mid-October.
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Fig. 7. Example of the distribution of dissolved oxygen–deficient water masses in Mikawa Bay. Four legends denote the level of dissolved oxygen saturation percentage
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Figure 8
shows distribution of benthic fish, shells, and crabs in a summer (late July to early August) in 1986, against the dissolved oxygen saturation percentage in the bottom layer of the water for the same period when an oxygen-deficient water mass appeared. Benthic fish were rarely observed in sea areas where the saturation was below 50%. Shells and crabs were observed at lower saturation rates, but not below 30%. Therefore, since 1970, the major fishing grounds of small trawl fisheries of these species have shifted from the middle of the bay toward the mouth. At present, the Mikawa Bay trawl fishery yield is rapidly declining.
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Fig. 8. Correspondence of the development of oxygen-deficient water masses and catch by small trawl fisheries in Mikawa Bay in the summer of 1986
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The same phenomenon occurs in the neighboring Ise Bay (Nakata et al., 1997). Squilla (mantis shrimp) is one of the most important species caught by trawl fisheries in Ise Bay. The catch of squilla in summer was minimal where the DO concentration was below 2 mg L-1 (about 30% saturation).
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HISTORIC RECORD AND CAUSES OF DISSOLVED OXYGEN DEFICIENCY
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Figure 9
shows the transition of transparency and the nitrogen load input through time. Transparency rapidly decreased from 1955 to 1970, corresponding with the yearly fluctuations of the nitrogen load. During the period, nitrogen loading doubled and phosphorus tripled. In regard to the sources of the nutrient load input, the increase attributable to domestic waste and livestock production is remarkable. However, as shown in Fig. 10 , red tides became a notable feature five years after that period, from about 1975 to 1983. Simultaneously, the development of oxygen-deficient water also increased steeply from about 1975.
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Fig. 10. Transition of the total number of days red tides were observed and the areal proportion of oxygen-deficient water with less than 30% saturation in Mikawa Bay
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Thus, historically, eutrophication in Mikawa Bay can be divided into Phase I (1955–1970), in which transparency deteriorated as a result of the increased nutrient load; and Phase II (1975 and after), in which the fisheries were severely damaged by red tides and oxygen-deficient water. The question now is, apart from the increase of nutrient inputs, what caused the intensified eutrophication between Phase I and Phase II?
One likely cause is the intense reclamation of lands over an extensive area. In Atsumi Bay, in the eastern part of Mikawa Bay, during the 1970s about 1200 ha of shallows including tidal flats were reclaimed for the purpose of ground preparation for constructing a harbor (see Fig. 11)
. The appearance of red tides accompanied by oxygen-deficient water coincides exactly with the reclamation of the shallows. This fact is very important in regard to hypoxia in the estuary. Incidentally, benthic suspension feeders (mainly bivalves) in the tidal flats of Mikawa Bay are estimated to filter seawater at a rate of 3.4 (Aoyama and Suzuki, 1997) to 5.0 m3 m-2 d-1 (Sasaki, 1994). From the reclaimed 1200 ha, this totals about 500 m3 s-1. Since the rate of exchange of seawater in Mikawa Bay is 1600 m3 s-1 to 2600 m3 s-1 in the summer (Sasaki, 1989), the lost seawater filtration rate equals 19 to 31% of the exchange rate of seawater.
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Fig. 11. Transition of the total number of days red tides were observed and the area of reclaimed land in Mikawa Bay
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It seems likely that the lowering of seawater filtration capacity drastically reduced the capacity to remove suspended organic matter from water and consequently accelerated the development of dissolved oxygen deficiencies followed by severe red tides (Ishida and Hara, 1996; Suzuki et al., 1996).
Another possibility is the development of water resources in the catchment basin. In Mikawa Bay, Toyokawa River is the most important river in regard to density flow and seawater exchange of the bay.
In 1968, Toyokawa Canal was completed, which diverts about 20 (in an average year) to 40% (in a dry year) of the total flow of Toyokawa River. The chief purpose of the canal is irrigation of farmlands, for which 72% of the diversion is used. There is speculation that this large reduction in the river flow due to this canal diversion reduces the density flow in the bay and exchange of seawater by 20 to 40%. Hindrance of seawater exchange slows down ejection of suspended organic matter in seawater to the exterior of the bay, and reduces supply of dissolved oxygen from the mouth of the bay. However, this subject needs further study, since a lower estimation of the decline rate of exchange of seawater has been made by an analysis with the use of numerical model (Suzuki et al., 1986). We surmise that the lowering of the rate of exchange of seawater resulting from reduced river flow, and the lowering of the rate of filtration of seawater caused by reclamation of the shallows after about 1970, accelerated the dissolved oxygen deficiency.
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EFFECT OF DISSOLVED OXYGEN–DEFICIENT WATER ON THE BENTHIC COMMUNITY AND CHANGES IN THE SEDIMENT–SEA WATER NUTRIENT BUDGET
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A deficiency of dissolved oxygen has not only affected the structure of the benthic community but also its functionality. We observed the temporal development of dissolved oxygen–deficient waters and the resulting benthic community changes (Suzuki et al., 1998b). We also studied how the nitrogen balance between the benthic sediment and sea water was affected using a benthic ecosystem model (Suzuki et al., 1998a) that has been developed for the quantification of the nitrogen cycle on tidal flats in Mikawa Bay (Suzuki et al., 1997). Those results are outlined below.
Figure 12
shows the temporal changes in water temperature, salinity, and dissolved oxygen saturation percentage immediately above the bottom sediment in shallow areas (4 m depth expressed by chart datum), which were recorded in the inner part of Mikawa Bay, from June to the end of July 1996, and compared with changes in the benthic community (bacteria, benthic micro algae, meiobenthos, and macrobenthos). A deficiency in dissolved oxygen was observed on 25 and 26 June, 28 and 29 June, and 10 July, but each time the occurrence was brief and the saturation level stayed at about 50% until at least 20 July. Then a deficiency in dissolved oxygen lasted through the period from 20 to 29 July and the frequency of anoxic conditions increased. Different species reacted in different ways to low oxygen concentrations according to their tolerance, but eventually on July 29 the biomass of every species dropped sharply.
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Fig. 12. Time-series changes of water temperature, salinity, and degree of dissolved oxygen concentration immediately above the bottom sediment in shallow areas of Mikawa Bay and changes in the benthic community (bacteria, benthic micro algae, meiobenthos, and macrobenthos) from June to the end of July in 1996
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Figure 13
shows the nitrogen circulation and budget for 1 June, when there was no dissolved oxygen deficiency. The unit of flux is expressed by mg N m-2 d-1. The major points observed from the figure are listed in the following:- The particulate organic nitrogen (PON) supplied from the outside of the modeled system was removed at a high rate (561 mg N m-2 d-1) through the filtering intake of suspension feeders.
- The rate of sedimentation of PON from water was 109 mg N m-2 d-1 for the total of phytoplankton and detritus and nearly balanced with the feeding rate of detritus from bottom sediment by surface deposit feeders (103 mg N m-2 d-1).
- The largest nutrient input to the pore water was caused by bacterial decomposition (255 mg N m-2 d-1), which nearly equaled the total excretion by suspension feeders (188 mg N m-2 d-1), surface deposit feeders (57 mg N m-2 d-1), and meiobenthos (16 mg N m-2 d-1). The largest nutrient output from the pore water was elution of ammonium nitrogen into the water column (159 mg N m-2 d-1), which was 14 times the total absorption by photosynthesis of benthic micro algae (11 mg N m-2 d-1) and sea weed and sea grass (0.3 mg N m-2 d-1).
- In the nutrient flux of seawater and sediment alone (excluding sedimentation), PON in the water column was taken into the sediment at a rate of 561 mg N m-2 d-1, phytoplankton and detritus in total. On the other hand, dissolved inorganic nitrogen (DIN), as a total of ammonium and nitrate nitrogen, eluted into the water at a rate of 160 mg N m-2 d-1. On balance, total nitrogen (TN) was removed from seawater at 401 mg N m-2 d-1.
Figure 14
shows the average nitrogen circulation and budget for 29 July, when biomass fell because of the deficiency in dissolved oxygen. Major differences from 1 June are as follows:- Because of the fall in biomass of suspension feeders, intake of PON from the water was very low.
- The rate of sedimentation of PON from the water column was 113 mg N m-2 d-1 for the total of phytoplankton and detritus, but the consumption of bottom sediment detritus by deposit feeders, which was balanced against the sedimentation before, was reduced to about zero.
- The largest nutrient input to the pore water was caused by bacterial decomposition (146 mg N m-2 d-1). Total excretion by suspension feeders, surface deposit feeders, and meiobenthos was less than 1% of the bacterial decomposition. Because the bacterial biomass decreased to one quarter (from 1.23 to 0.33 g N m-2), bacterial decomposition also slowed by about 50% in spite of an increase in the detritus mass (from 154 to 165 g N m-2). As for the nutrient output, the increase in the ammonium nitrogen concentration in the pore water raised elution into the water by about 25% (to 200 mg N m-2 d-1), whereas intake by deposit algae (6 mg N m-2 d-1) and absorption by sea weed and grass for photosynthesis decreased further.
- For the nutrient flux of sea water and sediment alone (excluding sedimentation), intake of PON from the water column into the sediment fell drastically to about 1 mg N m-2 d-1, for the total of phytoplankton and detritus. On the other hand, elution of DIN increased by 26%, at a rate of 202 mg N m-2 d-1. On balance, TN was supplied from the sediment to seawater at 201 mg N m-2 d-1.
Figure 15
shows a time series chart of the nutrient flux between seawater and sediment. On the vertical axis, the flux from seawater to sediment is indicated as negative quantities. Before 16 July, PON was being removed from the water at -561 to -962 mg N m-2 d-1 (-785 mg N m-2 d-1 on average). Dissolved inorganic nitrogen was eluting at 159 to 757 mg N m-2 d-1 (535 mg N m-2 d-1 on average). On balance, TN was removed from the water at -43 to -401 mg N m-2 d-1 (-250 mg N m-2 d-1 on average). Then, from 16 to 22 July, both the PON removal rate and the DIN elution rate dropped rapidly, and on 29 July PON removal practically stopped. Thus, after 22 July, the TN budget turned from negative to positive to about 240 mg N m-2 d-1.
An oxygen-deficient water mass is formed when oxygen consumption exceeds oxygen supply. The main cause of overconsumption of oxygen is the increase in the amount of particulate organic matter or organic sediments.
The analytical results from the benthic ecosystem model indicate that the shallows usually have the capability of reducing particulate organic matter at higher rate of efficiency than the rate of elution of inorganic nutrient salts. However, the so-called water self-purification ability functions only if ambient oxygen conditions are normal. If a huge oxygen-deficient water mass develops in the offshore sea bottom to a scale that can affect the shallows under certain wind and tide conditions, the situation totally changes. First, the biomass of suspension-feeder macrobenthos is reduced, resulting in a lower rate of removal of particulate organic matter from the water. Then, the rate of removal of organic sediment matter by deposit-feeder macrobenthos also drops. Deteriorated transparency near the sea bottom hinders growth of benthic microalgae and seaweeds, slowing down the rate of absorption of inorganic nutrient salts. Then the amount of oxygen generated by photosynthesis also falls, accelerating development of the anaerobic condition near the sea bottom.
Material circulation within the bottom sediment becomes heavily dependent on bacteria, although this last system is also hindered by a reduction in the bacteria biomass. Although this means a reduction of nutrient elution from sediment to sea water, the TN budget of PON and DIN swings from a sink (-) to a source (+). Consequently, the shallows that used to be a highly efficient purifier turn into the source of nutrients, which further exacerbates the dissolved oxygen deficiency.
In shallow sea areas above a depth of 10 m, where benthic organisms are abundant, it is estimated that benthic organisms are wiped out by the deficiency of dissolved oxygen throughout about one-fifth of the total area. This results in nitrogen elution of 12 Mg d-1, which amounts to about 30% of the load to Mikawa Bay.
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THE FUTURE
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This report presents multiple aspects of water bodies with a dissolved oxygen deficiency in Japan, using Mikawa Bay as an example. Although dissolved oxygen deficiency in Mikawa Bay basically results from the increased nutrient load from domestic waste and livestock sources, reclamation of shallows including tidal flats and reduction of river flow for irrigation of farm lands also drastically accelerate the dissolved oxygen deficiency. These days, oxygen-deficient water masses in Mikawa Bay develop to a size such that they can strip the precious water purification capacity of the remaining shallows. The worst thing is that the shallows have turned from the purifier to a contributor of the nutrient load. These conditions are more or less common in all bays where the dissolved oxygen–deficient water masses have been reported.
In order to break the vicious cycle, dissolved oxygen deficiency must be contained to the extent that the purification capacity of the shallows can be restored to an efficient level. For this purpose, the first thing to do is to restore tidal flats over an extensive area that is free from the effects of oxygen-deficient water masses, and to recover sufficient water flow, which may be a more urgent imperative than reducing the nutrient load input.
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REFERENCES
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- Aoyama, H., and T. Suzuki. 1997. In situ measurement of particulate organic matter removal rates by a tidal flat macrobenthic community. Bull. Jpn. Fish. Oceanogr. 61:256–274.
- Hara, T., R. Mukai, and N. Kuroda. 1995. The progress of oxygen deficient water mass in Mikawa Bay. Bull. Aichi Fish. Res. Inst. 2:47–50.
- Iizuka, S., and S.H. Min. 1989. Formation of anoxic bottom waters in Omura Bay. Bull. Coast. Oceanogr. 26:75–86.
- Ishida, M., and T. Hara. 1996. Changes in water quality and eutrophication in Ise and Mikawa Bays. Bull. Aichi Fish. Res. Inst. 3:20–42.
- Joh, H. 1986. Studies on the mechanism of eutrophication and the effect of it on fisheries production in Osaka Bay. Bull. Osaka Prefect. Fish. Exp. Stn. 7., Osaka, Japan.
- Joh, H. 1989. Oxygen-deficient water in Osaka Bay. Bull. Coast. Oceanogr. 26:87–98.
- Kamizono, M., T. Etoh, and H. Satoh. 1996. Oxygen budget of the bottom layer in the southwestern part of Suo-Nada. Umi no Kenkyu 5:87–96.
- Matsukawa, Y., and T. Suzuki. 1985. Box model analysis of hydrography and behavior of nitrogen and phosphorus in a eutrophic estuary. J. Oceanogr. Soc. Jpn. 41:407–426.
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- Ochi, T., and H. Takeoka. 1986. The anoxic water mass in Hiuchi-Nada. Part 1. Distribution of the anoxic water mass. J. Oceanogr. Soc. Jpn. 42:1–11.
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- Sasaki, K. 1994. Material circulation and production in estuary and tidal flat-12. Aquabiology 16:487–492.
- Suzuki, T., H. Aoyama, and K. Hata. 1996. Environmental bioremediation of eutrophic estuaries by biological processes in tidal flats. p. 109–134. In Environmental bioremediation by biological processes. The possibility of bioremediation in fisheries environments. Kouseisha-Kouseikaku, Tokyo.
- Suzuki, T., H. Aoyama, and K. Hata. 1997. The quantification of nitrogen cycle on tidal flat by ecosystem model—In the case of Isshiki tidal flat in Mikawa bay. J. Adv. Mar. Sci. Tech. Soc. 3:63–80.
- Suzuki, T., H. Aoyama, M. Kai, and K. Hata. 1998a. The effect of change in the benthic community, due to the development of dissolved oxygen deficiency, on the nitrogen budget between the sediment and overlying water. J. Adv. Mar. Sci. Tech. Soc. 4:65–80.
- Suzuki, T., H. Aoyama, M. Kai, and K. Imao. 1998b. Effect of dissolved oxygen deficiency on a shallow benthic community in an embayment. Umi no Kenkyu 7:223–236.
- Suzuki, T., Y. Hirasawa, and Y. Seko. 1986. Syouwa 60 nendo Akashio Taisaku Gizyutsu Kaihatsu Shiken Houkokusyo, Aichiken Suisan Shikenzyou.
- Suzuki, T., and Y. Matsukawa. 1987. Hydrography and budget of dissolved total nitrogen and dissolved oxygen in the stratified season in Mikawa Bay, Japan. J. Oceanogr. Soc. Jpn. 43:37–48.
- Suzuki, T., and T. Terasawa. 1997. A simulated numerical reproduction of an oxygen-depleted water mass in an eutrophic estuary; an examination of methods to increase the oxygen concentration in depleted waters. The case of Ise and Mikawa Bays. J. Adv. Mar. Sci. Tech. Soc. 3:81–102.
- Takasugi, Y., T. Higo, and H. Yasuda. 1996. The role of bottom current in occurrence of oxygen-deficient water mass. Umi no Kenkyu 5:1–12.
- Yuasa, I. 1994. Residual circulation, coastal fronts and behavior of nutrients in the inland sea. Bull. Chugoku Natl. Ind. Res. Inst, AIST, MITI, Kure, Japan.
TOP
ABSTRACT
INTRODUCTION
