Long-term Trends of Red Tides by Eutrophication and Toxic Blooms by Oligotrophication in the Seto Inland Sea of Japan

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Long-term Trends of Red Tides by Eutrophication and Toxic Blooms by Oligotrophication in the Seto Inland Sea of Japan Ichiro Imai 1, Masafumi Natsuike 1 Keigo Yamamoto 2 Tetsuya Nishikawa 3 Satoshi Nagai 4 Fish-killing Chattonella red tide 1 : Hokkaido University 2 : Research Institute of Environment, Agriculture and Fisheries, Osaka Prefecture 3 : Fisheries Technology Institute, Hyogo Prefecture 4 : National Research Institute of Fisheries Science

The Seto Inland Sea has experienced extreme eutrophication during the period of high speed economic growth. Strong human impacts were given to the Seto Inland Sea, such as large scale reclamation, heavy inputs of nutrients, etc. Harmful algal blooms have occurred causing mass mortalities of cultured fishes and bivalves. Atada Island, Hiroshima Bay, the Seto Inland Sea, famous for fish and oyster culture Seto Inland Sea is currently in a trend of oligotrophication by the regulation of nutrient inputs, accompanied by frequent occurrences of toxic blooms and Bleaching problems of Nori culture. The toxic alga Alexandrium tamarense was introduced by human activities.

Contents Hime-shima Island, Oita Prefecture (famous for prawn culture) 1) General trends 2) Changes in water quality 3) Red tides and toxic blooms

Seto Inland Sea, Harima-Nada and Osaka Bay Hakodate Seto Inland Sea Japan Akashi Usuki Harima-Nada Osaka Bay

2500 Changes in total COD loading in the Seto Inland Sea COD loads (t d -1 ) 2000 1500 1000 500 Domestic+others Industrial 0 1961 1968 1972 1979 1984 1989 1994 1999 2004 Fiscal year from the Ministry of the Environment Government of Japan & the Association for the Environmental Conservation of Seto Inland Sea

Serious eutrophication of the Seto Inland Sea A B A: Red tide (Noctiluca) B: Bloom of Skeletonema spp. C: Mass mortality of cultured yellowtails in pen cage by HAB C

Countermeasures for eutrophication Special law Law Concerning Special Measures for Conservation of the Environment of the Seto Inland Sea (enacted in 1973) # Control of the total pollutant load # Reduction of the total quantity of organic pollutants in term of COD Control of total P inputs (from 1979) Control of total N inputs (from 1996)

Long-term monitoring: Sampling stations in Harima-Nada O 134 30' E O 135 00' E O 34 40' N O 34 20' N 219 220 154 Harima-Nada Awaji Is. Hyogo pref. Osaka Bay Harima-Nada Area: 3,400 km 2 Mean depth: 25.9 m 345 Kii-Channel

Long-term variations in water temperature (April 1973-Dec 2007, mean of 3 depth at 19 sampling stations) Water temperature ( o C) 30 20 10 0 0.024 y -1 (p>0.05) 0.021 y -1 (p>0.05) 0.042 y -1 (t-test, p<0.05) 1973 1978 1983 1988 1993 1998 2003 Year (Nishikawa et al. 2010)

Long-term variations in salinity (April 1973-Dec 2007, mean of 3 depth at 19 sampling stations) 34 33 Salinity 32 31 30 29 1973 1978 1983 1988 1993 1998 2003 Year (Nishikawa et al. 2010)

Long-term variations in DIN (April 1973-Dec 2007, mean of 3 depth at 19 sampling stations) 15 DIN (µm) 10 5 0 1973 1978 1983 1988 1993 1998 2003 Year (Nishikawa et al. 2010)

Long-term variations in phosphate (April 1973-Dec 2007, mean of 3 depth at 19 sampling stations) 1.5 PO4-P (µm) 1.0 0.5 0.0 1973 1978 1983 1988 1993 1998 2003 Year (Nishikawa et al. 2010)

Long-term variations in silicic acid (April 1973-Dec 2007, mean of 3 depth at 19 sampling stations) 30 Si(OH)4-Si (µm) 20 10 0 1973 1978 1983 1988 1993 1998 2003 Year

Summary of water quality changes Significant long-term changes: 1) Rise in winter water temperature (0.042 y -1 ). 2) Increase in nutrients in 1960s and 1970s. 3) Decrease in dissolved inorganic nitrogen (DIN) (10 µm in the 1970s to ~5µM in the 1990s and thereafter).

Harmful algae in the Seto Inland Sea (Imai et al. 2006) Bars=20µm, E=100µm A-G: Red tide algae A: Chattonella antiqua B: Chattonella marina C: A cyst of Chattonella D: Heterosigma akashiwo E: Noctiluca scintillans F: Karenia mikimotoi G: Heterocapsa circularisquama H-K: Toxic algae H: Dinophysis fortii I: Dinophysis acuminata J: Alexandrium catenella K: Gymnodinium catenatum

* Large scale red tides had been frequent in 1970 s and 1980 (Fisheries Agency, 2009)

Occurrences of red tides in the Seto Inland Sea 300 from 1970 to 2006 (Fisheries Agency, Japan, 2007) Total incidents Fisheries damage Incidents 200 100 0 1970 1975 1980 1985 1990 1995 2000 2005 Year

(Fukuyo et al., 2002) Expansion to western Japan

Identified cells of the toxic dinoflagellate Alexandrium tamarense from the transplanting oyster spats from north to the Seto Inland Sea. <Matsuyama et al. 2008> A: Vegetative cell B: Many temporary cysts including A. tamarense observed in ejected feces from transplanting oyster spats. (Matsuyama et al., 2010)

Distribution of population genetics of A. tamarense From Russia? 0.200 0.150 0.100 0.050 0.000 68 63 53 AKK OKH FUN SEN OFN OHT KUR MIK KOB JIN JIN KUR OHT KOB FUN MIK OKH AKK OFN SEN UPGMA dendrogram constructed using Nei s genetic distance among the ten localities of A. tamarense samples. (Nagai et al., 2006) The dendrogram identified 3 clusters. Transplantation from north to the Seto Inland Sea 21

Long term trends of nutrients and A. tamarense cells (Predominance of A. tamarense in oligotrophic waters) 40 35 30 DIN(μM) 25 20 15 10 5 0 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 1.8 1.6 DIP(μM) 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 (Yamamoto et al., 2010)

Antagonistic relations between maximum densities of A.tamarense andmean diatom densities in 2000s Maximum cell density of A.tamarense (cells ml -1 ) Average cell density of Diatoms (Feb. to May) 1000 100 10 18 10 1 0 10 3 PSP 00 02 05 10 13 (cells ml -1 ) 00 02 05 10 Arrows (and ) indicate occurrences of Paralytoc Shellfish Poisonings (PSP) In Osaka Bay after 2002. other diatoms Pseudonitzscia spp. Leptocylindrus spp. Chaetoceros spp. Thalassiosira spp. Skeletonema spp.

1 In 1960s and 1970s, red tide incidents markedly increased along with serious eutrophication in the Seto Inland Sea. 2 Regulation by law and technical development contributed to decrease nutrient inputs into the Seto Inland Sea. 3 The toxic dinoflagellate Alexandrium tamarense was newly transplanted into the Seto Inland Sea from northern area by human activities of oyster aquaculture industry. 4 PSP problems started in the Seto Inland Sea by A. tamarense from about 1990 and completely established.

Thanks for your attention! My native beach, Usuki Bay, the Seto Inland Sea