Long-term Trends of Red Tides by Eutrophication and Toxic Blooms by Oligotrophication in the of Ichiro Imai1, Fish-killing Chattonella red tide Masafumi Natsuike1 Keigo Yamamoto2 Tetsuya Nishikawa3 Satoshi Nagai4

1: Hokkaido University 2: Research Institute of Environment, Agriculture and Fisheries, 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. Hime-shima Island, Oita Prefecture Contents (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 Osaka Bay Harima-Nada Changes in total COD loading in the Seto Inland Sea

2500

Domestic+others

) 2000

-1 Industrial

1500

1000

COD loads (t d (t CODloads 500

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

C A: Red tide (Noctiluca) B: Bloom of Skeletonema spp. C: Mass mortality of cultured yellowtails in pen cage by HAB 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 134 O 30' E 135 O 00' E

● ● ● Hyogo pref. ● ● ● ● 34 O 40' N ● ● ● ● ● ● ● ● Osaka Bay Harima-Nada ● ● ● O ● 34 20' N 219 220 Awaji Is.

154 Harima-Nada 345 ・Area: 3,400 km2 Kii-Channel ・Mean depth: 25.9 m Long-term variations in water temperature (April 1973-Dec 2007, mean of 3 depth at 19 sampling stations)

30 0.024 ℃ y-1 (p>0.05) C) o

-1 20 0.021 ℃ y (p>0.05)

10

0.042℃ y-1

Water temperatureWater ( (t-test, p<0.05) 0 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

32

31 Salinity

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

10 DIN (µM) DIN 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

1.0 -P (µM) 4

PO 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

20 -Si (µM) 4

10 Si(OH)

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 from 1970 to 2006 (Fisheries Agency, Japan, 2007) 300

Total incidents Fisheries damage

200 Incidents 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.

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 OKH 68 AKK OKH FUN SEN FUN AKK OFN OHT 53 KUR OFN 63 MIK KOB SEN JIN KUR OHT JIN MIK KOB

UPGMA dendrogram constructed using Nei’s genetic distance The dendrogram identified among the ten localities of 3 clusters. A. tamarense samples. Transplantation from north

(Nagai et al., 2006) 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

) 25

20 μM 15

10 DIN( 5

0 2011 1981 1991 1972 1977 1973 1975 1974 1992 1982 2001 2010 1979 1997 1976 1978 1987 1993 1983 1985 1995 1994 1984 1989 1990 1998 1999 1980 1988 1996 1986 2002 2007 2003 2005 2004 2009 2000 2008 2006

1.8 1.6 1.4

) 1.2 1.0

μM 0.8 0.6

DIP( 0.4 0.2 0.0 2011 1991 1981 1972 1977 1973 1975 1974 1992 1982 2001 2010 1978 1979 1987 1997 1976 1993 1983 1995 1985 1994 1984 1999 1980 1989 1990 1998 1988 1996 1986 2002 2007 2003 2005 2004 2000 2009 2006 2008

(Yamamoto et al., 2010) Antagonistic relations between maximum densities of A.tamarense andmean diatom densities in 2000s

1000

)

-1 Arrows (and ) PSP indicate 100 occurrences of

(cellsml Paralytoc Shellfish Poisonings (PSP) 10 In Osaka Bay after 2002. tamarense . A

Maximum cell density of Maximumdensity cell 1 00 02 05 10 13 ×103 (cells ml-1)

18

other diatoms Pseudonitzscia spp. 10 Leptocylindrus spp. Chaetoceros spp. Thalassiosira spp. Skeletonema spp. Diatoms (Feb. to May) to Diatoms(Feb. Average cell density of density cell Average 0 00 02 05 10 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