Species composition and long-term dynamics of potentially toxic dinoflagellate species in benthic assemblages of Peter the Great Bay, Sea of Japan

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1 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 Morozova National Scientific Center of Marine Biology Far Eastern Brunch of Russian Academy of Sciences Vladivostok, Russia

2 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

3 Materials and methods N S Japan / East Sea Peter the Great Bay - Station 1, epiphytic dinoflagellates, from Stations 2 & 3, sand-dwelling dinoflagellates, from

4 100 µm 20 µm Cell counting Epiphytic dinos abundance - cells/g dry weight of macrophyte Sand-dwelling dinos abundance - cells/cm 3 of sand 4

5 Results 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.,

6 Number of species 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) I II III IV V VI VII VIII IX X XI XII Months The seasonal dynamics of the total species richness of sand-dwelling dinoflagellates ст. Station 3 3 ст. Station2 2 8

67 benthic species of dinoflagellates: 17

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 7

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

8 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. 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.,

9 Potentially toxic benthic dinoflagellates a b c а - Amphidinium оperculatum Claparede et Lachmann, b - A. carterae Hulbert, d e f c - A. gibbosum (Maranda et Shimizu) Murray et Flø Jørgensen, d,e - Ostreopsis ovata complex Fukuyo, f - Prorocentrum foraminosum Faust 9

The seasonal dynamics of cell density of sand-dwelling dinoflagellates and the main dominant species п л о т н о с т ь, кл / см 3 Density, cells/cm 3 3000 2500 2000 1500 1000 500 0 700 600 500 400

10 The seasonal dynamics of cell density of sand-dwelling dinoflagellates and the main dominant species п л о т н о с т ь, кл / см 3 Density, cells/cm I 2008 I 2008 ( а ) St.2 ( б) IV VII X I 2009 St.3 IV VII X I 2009 IV VII X I 2010 Thecadinium kofoidii Общая total IV VII X I 2010 IV VII X Amphidiniopsis uroensis total Общая IV VII X Months месяцы The proportion of the main dominant species during the year: Thecadinium kofoidii % Amphidiniopsis uroensis %. 10

T, oc 22 100000 18 10000 14 1000 10 100 6 10 2 1-2 3/09/08 17/09/08 25/09/08 13/10/08 27/10/08 21/11/08 23/12/08 2/02/09 Density, cells/g dry weight of

21/05/09 25/06/09 27/07/09 24/08/09 4/09/09 24/09/09 other species P.cam pbellii P.fukuyoi Ostreopsis spp.

11 T, oc /09/08 17/09/08 25/09/08 13/10/08 27/10/08 21/11/08 23/12/08 2/02/09 Density, cells/g dry weight of macrophyte The seasonal dynamics of cell density of epiphytic dinoflagellates and the main dominant species number of species 12/03/09 20/04/09 21/05/09 25/06/09 27/07/09 24/08/09 4/09/09 24/09/09 other species P.cam pbellii P.fukuyoi Ostreopsis spp. 2/10/09 7/10/09 16/10/09 23/11/ Temperature, o C & number of species 3/09/08 17/09/08 25/09/08 13/10/08 27/10/08 21/11/08 23/12/08 2/02/09 Water temperature, o C Number of species 11

2015 2016 1 VII VIII VIII VIII IX IX IX X X X XI XI Months Ostreopsis is the only genus of

12 Maximum density, cells/g macrophyte dry weight The long-term dynamics of Ostreopsis spp. density on macrophytes VII VIII VIII VIII IX IX IX X X X XI XI Months Ostreopsis is the only genus of potentially toxic dinoflagellates, which is regularly reported to bloom in waters of Peter the Great Bay 12

, isolated from the Peter the Great Bay, showed three distinctly different ribotypes according to the nucleotide sequences of ribosomal DNA (rdna).

13 Distribution of the Ostreopsis ribotypes registered in Russian waters Pacific Ocean 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). 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 Vol. 5, no. 4. Р

Maximum density, cells/g macrophyte dry weight The

macrophytes 10000 1000 100 10 1 IV VI VII VIII VIII IX X X

foraminosum occurred regularly from April to November in

14 Maximum density, cells/g macrophyte dry weight The long-term dynamics of Prorocentrum foraminosum density on macrophytes IV VI VII VIII VIII IX X X XI p Months P. foraminosum occurred regularly from April to November in the epiphytic assemblages of Peter the Great Bay (Sea of Japan). 14

15 Prorocentrum foraminosum DTX-1 In culture of P. foraminosum containing cell/ml DTX-1 was determined 8.4 ± 2.5 pg/cell 27.9 ± 14.7 µg/ml of cellfree media (HPLC with high-resolution tandem mass-spectrometry) Kameneva P.A. et al. Detection of dinophysistoxin-1 in clonal culture of marine dinoflagellate Prorocentrum foraminosum (Faust M.A., 1993) from the Sea of Japan // Toxins Vol. 7(10). P

16 Concentration of SDTs ug/kg Patrokl Rinda Paris Starka strait Zapadnaya Vostochnaya Station 8 Station 10 Pervaya rechka Screpcova Qualitative composition of DSTs in mussels in Peter the Great Bay (2012) 600,0 500,0 OA DTX1 400,0 300,0 200,0 100,0 0,0 Station Orlova T.Yu, et al. Diarrhetic shellfish toxins in Primorsky Krai, Russia // J. Shellfish Res Vol. 34 (3). P

17 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.

Long-term changes in microalgae communities on the Russian East coast with emphasis on toxic and bloom forming species

Long-term changes in microalgae communities on the Russian East coast with emphasis on toxic and bloom forming species Tatiana Yu. Orlova, Polina A. Kameneva, Tatiana V. Morozova A.V. Zhirmunsky Institute