Species composition and long-term dynamics of

potentially toxic dinoflagellate species in benthic

assemblages of Peter the Great Bay, Sea of Japan

Marina Selina & Tatiana Morozovatatiana_morozova@mail.ru

National Scientific Center of Marine Biology

Far Eastern Brunch of Russian Academy of Sciences

Vladivostok, Russia

PICES 2017

Introduction

• Benthic dinoflagellates include about 190 species and 45 genera. About 60

species of all dinoflagellates can produce various toxins. Among them 30

species are benthic.

• Recently the study of benthic dinos focuses on the species diversity.

Abundance, temporal and spatial changes are known mainly for epiphytic

communities, which is basically connected with the ciguatera. Information

about sand-dwelling dinos are limited by some areas of World Ocean.

• The present work represents the species composition, long-term dynamics

and the maximum abundance of benthic dinoflagellates in Peter the Great

Bay (Sea of Japan) including toxic species

2

PICES 2017

Materials and methods

Japan / East

SeaPeter the Great Bay

N

S

- Station 1, epiphytic dinoflagellates, from 2008

- Stations 2 & 3, sand-dwelling dinoflagellates, from 2005

-

3

12

3

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Cell counting

100 µm

20 µm

Epiphytic dinos abundance - cells/g dry weight of macrophyte

Sand-dwelling dinos abundance - cells/cm3 of sand4

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5

World biodiversity of benthic species

Region Number of species Reference

Elba, Italy 90 Hoppenrath et al.,2014

Brittany, France 78 Hoppenrath et al.,2014

Sea of Japan, Russia 67 Selina, 2016

North German Wadden Sea, Germany 67 Hoppenrath et al.,2014

Arabian Gulf, Kuwait 55 Hoppenrath et al., 2014

British Columbia, Canada 52 Hoppenrath et al.,2014

North-Eastern Australia 50 Hoppenrath et al.,2014

Jeju, South Korea 37 Shah et al.,2013

Botany Bay, Australia 36 Hoppenrath et al.,2014

Pacifiс coast of Japan 32 Hoppenrath et al., 2014

Malaysia 24 Hoppenrath et al., 2014

ResultsPICES 2017

Number of species Sand-dwelling dinos Epiphytic dinos

Total 67 species (25 genera) 15 species (7 genera)

Annual fluctuations 18 (winter) – 44 (summer) 1 (winter) – 8 (autumn)

8

The seasonal dynamics of

the total species richness of

sand-dwelling dinoflagellates

0

5

10

15

20

25

30

35

40

45

I II III IV V VI VII VIII IX X XI XII

Nu

mb

er

ofsp

ecie

s

Months

ст. 3

ст. 2

Station 3

Station2

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7

67 benthic species of dinoflagellates:

• 17 taxa - undetermined taxonomic status,

• 31 species – new for the seas of Russia,

• 8 species - new for Far Eastern seas of Russia.

Amphidinium Amphidiniopsis Thecadinium Sinophysis

9 species 9 species 6 species 4 species

PICES 2017

8

а - Amphidiniopsis

hoppenrathae 1,

b - A. konovalovae 2,

c - A. ovalis 1,

d - A. rotundata 3,

e - A. striata 2,

f - A. elongata 1,

g - Cabra levis 4 ,

h - Sinophysis minima 5,

i - Sabulodinium

undulatum var.

glabromarginatum 6

1 – Selina, Morozova, 2016; 2- Selina, Hoppenrath, 2013;3 – Hoppenrath et al., 2012; 4- Selina et al.,

2015; 5- Selina, Hoppenrath, 2004; 6 - :Hoppenrath et al., 2007

Six new species from the genus Amphidiniopsis (а-f), one species from the genera

Cabra (g) and Sinophysis (h), and one intraspecific taxa of Sabulodinium

undulatum (i) were described during the study period.

PICES 2017

9

Potentially toxic benthic dinoflagellates

а - Amphidinium оperculatum

Claparede et Lachmann,

b - A. carterae Hulbert,

c - A. gibbosum (Maranda et Shimizu)

Murray et Flø Jørgensen,

d,e - Ostreopsis ovata complex Fukuyo,

f - Prorocentrum foraminosum Faust

a b c

d e f

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The seasonal dynamics of cell density of sand-dwelling dinoflagellates

and the main dominant species

The proportion of the main

dominant species during the year:

Thecadinium kofoidii - 7799%

Amphidiniopsis uroensis -1998%.

10

0

500

1000

1500

2000

2500

3000

I2008

IV VII X I2009

IV VII X I2010

IV VII X

Thecadinium kofoidii

Общая

0

100

200

300

400

500

600

700

I2008

IV VII X I2009

IV VII X I2010

IV VII X

Amphidiniopsis uroensis

Общая

месяцы

п л

о т

н о

с т

ь, кл

/ с

м3

( а )

( б)

St.2

St.3

total

total

Months

Den

sit

y, cell

s/

cm

3

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11

1

10

100

1000

10000

100000

3/0

9/0

8

17

/09

/08

25

/09

/08

13

/10

/08

27

/10

/08

21

/11

/08

23

/12

/08

2/0

2/0

9

12

/03

/09

20

/04

/09

21

/05

/09

25

/06

/09

27

/07

/09

24

/08

/09

4/0

9/0

9

24

/09

/09

2/1

0/0

9

7/1

0/0

9

16

/10

/09

23

/11

/09

other species

P.campbellii

P.fukuyoi

Ostreopsis spp.

-2

2

6

10

14

18

22

3/0

9/0

8

17

/09

/08

25

/09

/08

13

/10

/08

27

/10

/08

21

/11

/08

23

/12

/08

2/0

2/0

9

12

/03

/09

20

/04

/09

21

/05

/09

25

/06

/09

27

/07

/09

24

/08

/09

4/0

9/0

9

24

/09

/09

2/1

0/0

9

7/1

0/0

9

16

/10

/09

23

/11

/09

T, oC

-2

2

6

10

14

18

22

T, oC

number of species

Water temperature, oC Number of species

Den

sit

y, cell

s/

g d

ry w

eig

ht

of

macro

ph

yte

Tem

peratu

re,oC

& n

um

ber

of

sp

ecie

s

The seasonal dynamics of cell density of epiphytic dinoflagellates

and the main dominant species

PICES 2017

The long-term dynamics of Ostreopsis spp. density on macrophytes

Months

1

10

100

1000

10000

100000

1000000

VII VIII VIII VIII IX IX IX X X X XI XI

Ma

xim

um

de

ns

ity,

cell

s/g

ma

cro

ph

yte

dry

we

igh

t2008

2009

2010

2011

2012

2013

2014

2015

2016

Ostreopsis is the only genus of potentially toxic dinoflagellates, which is regularly

reported to bloom in waters of Peter the Great Bay 12

PICES 2017

Identical ribotypes are depicted in one color.Phylogenetic analysis of clonal cultures and single cells of Ostreopsis spp., isolated from the Peter the Great Bay, showed three distinctly different ribotypes according to the nucleotide sequences of ribosomal DNA (rDNA).

Pacific Ocean

Distribution of the Ostreopsis ribotypes registered in Russian waters

13

Efimova K.V. et al. Phylogenetic characterization of cryptic species of the marine dinoflagellate, Ostreopsis sp. Shmidt, 1902, from Russian coastal waters, the Sea of Japan // J. Biodiversity and Environmental Sciences. 2014. Vol. 5, no. 4. Р. 317–332.

PICES 2017

The long-term dynamics of Prorocentrum foraminosum densityon macrophytes

Months

1

10

100

1000

10000

IV VI VII VIII VIII IX X X XI

Maxim

um

den

sit

y,

cell

s/g

macro

ph

yte

dry

we

igh

t

2008

2009

2010

2011

2012

2013

2014

2015

2016

P. foraminosum occurred regularly from April to November in the epiphytic assemblages of Peter the

Great Bay (Sea of Japan).

14

p

PICES 2017

DTX-1

Kameneva P.A. et al. Detection of dinophysistoxin-1 in clonal culture of marine dinoflagellate Prorocentrumforaminosum (Faust M.A., 1993) from the Sea of Japan // Toxins. 2015. Vol. 7(10). P. 3947–3959.

Prorocentrum foraminosum

In culture of P.

foraminosum containing

3500-5000 cell/mL

DTX-1 was determined

8.4 ± 2.5 pg/cell

27.9 ± 14.7 µg/mL of cell-

free media(HPLC with high-resolution

tandem mass-spectrometry)

15

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Qualitative composition of DSTs in mussels in Peter the Great Bay (2012)

0,0

100,0

200,0

300,0

400,0

500,0

600,0

Patr

okl

Rin

da

Paris

Sta

rka s

trait

Zap

adn

aya

Vosto

chna

ya

Sta

tion 8

Sta

tion 1

0

Perv

aya

rechka

Scre

pco

va

Co

nc

en

tra

tio

n o

f S

DTs

ug

/kg

Station

OA DTX1

Orlova T.Yu, et al. Diarrhetic shellfish toxins in Primorsky Krai, Russia // J. Shellfish Res. 2015. Vol. 34 (3). P. 1-10.16

PICES 2017

Conclusions

• The species richness of benthic dinoflagellates in Peter the Great Bay

exceeds that of many parts of the World Ocean.

• Potentially toxic dinoflagellates are constant and abundant in the

epiphyton during the summer-autumn period.