Ocean Science Journal (2009) 44(1):21-26 DOI 10.1007/s12601-009-0003-6
Article http://www.springer.com/12601
Species Composition and Seasonal Dynamics of the Population Density and Biomass of the Genus Pyramimonas (Prasinophyceae) from the Russian Waters of East/Japan Sea Inna Valentinovna Stonik* A. V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok 690041, Russia Received 11 November 2008; Revised 14 February 2009; Accepted 5 March 2009 © KSO, KORDI and Springer 2009
Abstract − The species composition and seasonal dynamics of the population density and biomass of the prasinophycean algae of the genus Pyramimonas were investigated in the Russian waters of the East/Japan Sea. According to literature data and the results of our observations, eight species of the prasinophycean algae were identified, and some of them were new for the Russian waters of the East/Japan Sea as follows: P. aff. amylifera Ñonrad, P. aff. cordata McFadden, Hill et Wetherbee, and P. nansenii Braarud. An analysis of their seasonal dynamics showed that the most conspicuous winter peak of the population density of Pyramimonas species in the Amurskii Bay was clearly distinguishable in February. In winter and early spring, the prasinophycean algae made a considerable contribution of 28 to 60% into the total population density on the background of a relatively low biomass, 1.1-14.4% of the total phytoplankton biomass in the Amurskii Bay. In the Golden Horn Bay, the summer peak of the population density of Pyramimonas species was most intensive in June. In summer, during the period of mass development of the algae of the genus Pyramimonas in the Golden Horn Bay, the prasinophycean algae contributed up to 71% of the total population density and up to 84% of the total microalgal biomass. An increase was noted in the density and biomass of the Pyramimonas species in the polluted waters near the sewage water outlets in the Amurskii and Golden Horn bays. Key words – Prasinophyceae, Pyramimonas, seasonal dynamics
1. Introduction The genus Pyramimonas Schmarda (Prasinophyceae) has been reported to include more than 60 marine, brackish*Corresponding author. E-mail:
[email protected]
and fresh-water species; most of them have a wide distribution all over the biogeographical zones (McFadden et al. 1986). Representatives of the genus inhabit mostly the neritic zone of the sea; some of these algae cause “water bloom” (Throndsen 1993). Prasinophytes, along with euglenophytes and cryptophytes, are relatively abundant also in the plankton of Peter the Great Bay of East/Japan Sea (Konovalova et al. 1989). However, Pyramimonas species, like many other unarmored flagellates groups of the Russian waters of the East/Japan Sea, are poorly studied. This is due to the difficulty of the methods of study: these algae are subject to deformations at a common fixation and destruct at a longer preservation of samples (Konovalova 2003). The available data on prasinophycean algae of the genus Pyramimonas refer mostly to species composition (Gail 1950; Konovalova et al. 1989). The previous information on the representatives of the genus Pyramimonas found in the area is limited to morphological descriptions of five species from coastal waters of East/ Japan Sea and is based on evidences of light microscopic study (Gail 1950; Konovalova et al. 1989). Scientific literature gives no data on the quantitative composition and seasonal dynamics of the population density and biomass for this algal group in the Russian waters of East/ Japan Sea. The purpose of this work is to study the seasonal dynamics of the population density and biomass and to review and supplement information on the species composition of the prasinophycean algae of the genus Pyramimonas found in Peter the Great Bay of East/Japan Sea.
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2. Materials and Methods The study used samples collected in Amurskii Bay and in Golden Horn Bay (Fig. 1). The sampling was performed in a half-closed man-made lagoon within the City of Vladivostok in Amurskii Bay (Station 1), in the neighboring Vtoraya Rechka River (Station 2), and in Golden Horn Bay (Station 3). Samples at Station 1 were collected from January to October of 2003. Samples at Stations 2 and 3 were taken from January 1993 through January 1994. Samples for quantitative analysis were taken from the water surface with the use of a 4-liter Molchanov bathometer. The materials were collected twice a month. One-liter sample was fixed with Lugol’s iodine solution and concentrated through sedimentation to a volume of 10-15 ml. Algal cells were counted in a 0.05-1 ml Nojott chamber with respect to the minimal representative sample of the counted cell number (Koltsova et al. 1971). According to Kuosa (1988), enumeration of autotrophic flagellates is most successful with the use of the Utermöhl technique and acid Lugol’s iodine fixation. Although this fixative causes deformation of the Pyramimonas cells, some typical characteristics (inverse pyramidal shape, four (or eight) flagella, the often cup-shaped single chloroplast with four lobes and a basal pyrenoid) are retained which makes it possible to recognize and count the cells. The biomass of algae was expressed as biovolume (mm L ) which is approximately equal to the wet weight (mg m ) (Andersen 3
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Fig. 1. Location of the sampling stations (1-3).
and Throndsen 2003). Biovolume can be calculated from measurements of linear dimensions of cells measured under the microscope using appropriate geometric formulae (Edler 1979). Simultaneously with quantitative sampling of phytoplankton, water temperature was recorded for each station. Spearman’s rank correlation coefficient with 5%significance level was applied to determine a relationship between water temperature and population density (R1) and water temperature and biomass (R2) of the prasinophytes. STATISTICA v. 6.0 for Windows (Statsoft, Tulsa, OK, USA) software was used for statistical treatment of the data obtained. The living algal cells as well as the cells preserved with Lugol’s solution were studied, photographed, and measured in a light microscope «Olympus BX41» (Olympus Optical Co. Ltd., Tokyo, Japan) with a UPLanF1 40x/0,75∞/0,17 objective.
3. Results and Discussion According to literature data and the results of our observations, eight species of the genus Pyramimonas were found in the Russian waters of the East/Japan Sea as follows: P. aff. amylifera Conrad, P. aff. cordata McFadden, Hill et Wetherbee, P. delicatula Griffith, P. grossii Parke, P. longicauda Van Meel, P. nansenii Braarud, P. semiglobosa Pascher, P. tetrarhynchus Schmarda (Table 1). As a result of previous studies on the representatives of the genus Pyramimonas in the Russian waters of the East/Japan Sea,
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Pyramimonas species (Prasinophyceae) from the Russian Waters of East/Japan Sea
Table 1. Species composition of the prasinophycean algae of the genus Pyramimonas, found in the plankton of Peter the Great bay of East/Japan Sea Maximum population Species Length, µm Width, µm Reference density, ths. cells L Pyramimonas aff. amylifera Conrad 16-20 11-13 50 Our data Pyramimonas aff. cordata 7-9 6-8 2524 Our data McFadden, Hill et Wetherbee Pyramimonas delicatula Griffith 12-15 Gail 1950 - "Konovalova 2003 Pyramimonas grossii Parke 7-10 5-6 676 Our data - "7.5-8 4.5-6.3 Konovalova et al. 1989 Pyramimonas longicauda Van Meel 16-20 10-12 70 Our data - "18-20 12-14.5 Konovalova et al. 1989 Pyramimonas nansenii Braarud 8.7-13.4 6.1-8.3 96000 Our data Pyramimonas semiglobosa Pascher 5-6 8-10 0.12 Gail 1950 Pyramimonas tetrarhynchus Schmarda 16-18 6-10 0.07 Gail 1950 -1
Note: “-”, no data
Table 2. Total phytoplankton density (ths. cells L ) and population density of Pyramimonas species (ths. cells L ) at stations 1-3 Station 1 Station 2 Station 3 Density of Density of Density of Date Date Total Total Total Pyramimonas Pyramimonas Pyramimonas density density density species species species 03 January 2003 1090 06 January 1993 1500 1300 19 January 2003 431 26 January 1993 1400 350 01 February 2003 342857 96000 13 February 1993 800 50 1800 14 February 2003 2011 100 26 February 1993 1000 1600 9.2 03 March 2003 14980 8800 13 March 1993 500 900 13 March 2003 18750 11200 26 March 1993 700 0.8 1000 0.3 03 April 2003 6631 09 April 1993 1200 3.7 1200 0.3 08 April 2003 4818 27 April 1993 4000 2.9 1000 1.2 15 May 2003 102 06 May 1993 200 0.6 2200 1.9 30 May 2003 74219 14000 30 May 1993 400 1 600 105.7 13 June 2003 19987 18 June 1993 800 3.2 300 100 21 June 2003 215652 30 June 1993 2300 4465 3170.2 06 July 2003 357303 140 14 July 1993 600 11.4 800 1 22 July 2003 122828 31 July 1993 13000 3.1 2500 854.4 04 August 2003 141985 20 August 1993 10000 4.2 500 0.5 17 August 2003 677472 27 August 1993 12500 4200 2.4 02 September 2003 132528 18 September 1993 1300 4.7 9000 1638.4 22 September 2003 21429 30 September 1993 2000 5.6 700 7.9 06 October 2003 17916 12 October 1993 4000 36.4 2500 15.1 28 October 1993 1200 1.9 100 0.4 19 November 1993 2000 1.2 1200 1.2 29 November 1993 1800 1 200 13 December 1993 2000 230 27 December 1993 10000 2 250 18 January 1994 1800 0.6 210 0.5 -1
Note: "-", Pyramimonas species were not found
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five species were found as follows: P. delicatula, P. grossii, P. longicauda, P. semiglobosa, and P. tetrarhynchus (Gail 1950; Konovalova et al. 1989). Our observations indicate that P. aff. amylifera, P. aff. cordata, and P. nansenii are common species in the phytoplankton assemblages on the northwestern East/Japan Sea. These three species of Pyramimonas were found for the first time in the Russian waters of the East/Japan Sea. An analysis of the seasonal dynamics showed that the most significant winter peak for the development of Pyramimonas species is found in February in the Amurskii Bay (Table 2). The peak was clearly distinguished by
population density and biomass at negative water temperatures in the range from -1.8 to -1 C (Fig. 2). In Golden Horn Bay (Station 3), the most intensive peak of prasinophycean density was recorded in June at a water temperature of 16.5 C. In winter and early spring, the prasinophycean algae made a considerable contribution of 28 to 60% to the total population density on the background of a relatively low biomass, 1.1-14.4% of the total phytoplankton biomass in the Amurskii Bay (Table 3). In winter, P. nansenii predominated at stations 1 and 2 in Amurskii Bay with the population density of 96×10 and 50×10 cells L , respectively. During summer peak of cell density of Pyramimonas species, the fraction of the prasinophycean algae made up to 71% of the population density and up to 84% of the total biomass of microalgae. In summer, P. aff. cordata and P. grossii predominated over the bay with the population density of 2,5×10 and 6,7×10 cells L , respectively. In other seasons, a relative share of the prasinophycean algae in the dynamics of phytoplankton was modest. Many Pyramimonas species are associated with lower temperatures (Gardner and Hargraves 1979). One of them seems to be P. nansenii found previously from arctic (East Greenland) and a water sample collected from underneath the ice of a Danish brackish water fjord (Thomsen 1988). Population density and biomass of the prasinophycean algae in strongly eutrophicated water areas, as in the semiclosed seawater basin within the city of Vladivostok and in Golden Horn Bay, were significantly higher than in the vicinity of the Vtoraya Rechka mouth. Thus, the population density of these algae at Stations 1 and 3 reached 96×10 and 3.2×10 cells L , and the biomass made up to 50 and 1.6 g m , respectively. At the same time, these records for Station 2 in the vicinity of the Vtoraya Rechka river were significantly lower and did not exceed 50×10 cells L and 26.2 mg m (Fig. 2). In a half-closed basin within the city of Vladivostok, the values of population density of the prasinophycean algae were extremely high and reached some dozens of millions cells per liter. The half-closed seawater basin is a man-made lagoon with a limited water exchange. The lagoon is situated at a short distance of 200 m from the Vtoraya Rechka river mouth, the source of pollution from a sewage water outlet. Extremely high quantitative characteristics of phytoplankton development in this lagoon are linked to continuous enrichment of the waters by biogenic elements o
o
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5
6
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5
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6
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Fig. 2. Seasonal changes in population density of Pyramimonas species (A), biomass (B) and water temperature ( C) at stations 1-3. o
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Pyramimonas species (Prasinophyceae) from the Russian Waters of East/Japan Sea
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Table 3. Total phytoplankton biomass (mg m ) and biomass of Pyramimonas species (mg m ) at stations 1-3 Station 1 Station 2 Station 3 Biomass of Biomass of Biomass of Date Date Total Total Total Pyramimonas Pyramimonas Pyramimonas biomass biomass biomass species species species 03 January 2003 6512 06 January 1993 4800 4200 19 January 2003 2524 26 January 1993 4600 900 01 February 2003 345884 50000 13 February 1993 1800 26.2 6100 14 February 2003 4538 5 26 February 1993 3800 4000 4.8 03 March 2003 52273 4600 13 March 1993 200 1000 13 March 2003 527273 5800 26 March 1993 2500 0.4 1500 0.1 03 April 2003 9001 09 April 1993 900 1.9 1800 0.1 08 April 2003 49373 27 April 1993 3200 1.5 1000 0.6 15 May 2003 1093 06 May 1993 100 0.3 1800 1 30 May 2003 15897 7300 30 May 1993 900 0.5 800 55.3 13 June 2003 28330 18 June 1993 5000 1.7 150 52.3 21 June 2003 556515 30 June 1993 2300 1973.8 1658 06 July 2003 35885 7 14 July 1993 2500 5.9 100 0.5 22 July 2003 470841 31 July 1993 12000 1.6 3200 446.8 04 August 2003 6662 20 August 1993 10500 2.2 1000 0.3 17 August 2003 5059 27 August 1993 11000 7400 1.2 02 September 2003 10562 18 September 1993 1500 2.5 5100 856.9 22 September 2003 2377 30 September 1993 2200 2.9 1100 4.1 06 October 2003 2072 12 October 1993 4000 19 7100 7.9 28 October 1993 1200 0.9 400 0.2 19 November 1993 2500 0.6 1700 0.6 29 November 1993 2000 0.5 800 13 December 1993 2300 900 27 December 1993 7000 0.9 1900 18 January 1994 9800 0.3 2500 0.3 -3
-3
Note: "-", Pyramimonas species were not found
and dissolved organic matter from anthropogenic sources, the industrial and municipal wastewater discharge (Begun et al. 2004). Isolation of this lagoon, resulting in stabilization of the water column, is also regarded as an important physical factor favouring algal blooms. As a rule, a rise in the abundance of unarmoured flagellates (prasinophytes, euglenophytes, and haptophytes) is usually observed in areas of increased eutrophication and is favoured either directly by higher nutrient availability or indirectly through increased microbial activity (Hajdu et al. 1996; Mihnea 1997). A change in the qualitative relationship among species in favor of the prasinophycean algae was reported earlier for the Gulf of Finland and for other highly productive areas of the Baltic Sea (Kononen et al. 1993). Data of some authors (Gardner and Hargraves 1979; Hajdu et al. 1996) shows that temperature is a factor
affecting the seasonal dynamics of growth of the genus Pyramimonas and other groups of unarmoured flagellates in coastal marine ecosystems. For Amurskii Bay, no statistically significant correlations were revealed between the variations in water temperature and population density/ biomass of the prasinophytes. But in Golden Horn Bay, we have found a reliable correlation between variations in water temperature and population density (R1=0.68, p= 0.00017) and biomass (R2=0.67, p=0.00021) of the prasinophytes. However, this positive correlation between the temperature rise and the increased population density and biomass of the prasinophytes may be linked also to an impact of some other physical, chemical, and/or biological variables (stratification of the water column, availability of biogenic elements, zooplankton grazing, etc.) related to temperature.
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We can expect that application of special methods of fixation and electron microscopy will allow researchers to considerably extend scientific knowledge on flora of the prasinophycean algae in the plankton of the East/Japan Sea.
Acknowledgements This research was supported by the Far Eastern Branch of the Russian Academy of Sciences (FEB RAS) through grants No.06-III-B-06-213, and grant FEB RAS/RFBR No. 09-04-98570-p_vostok_a). The author is greatly indebted to A.A. Begun for providing the material for this research (samples of 2003).
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(Prasinophyceae): seasonal dynamics of a wild population, and the effects of temperature and salinity on growth and survival in culture. J Plankton Res 1:291-299 Hajdu S, Larsson U, Moestrup Ø (1996) Seasonal dynamics of Chrysochromulina species (Prasinophyceae) in a coastal area and a nutrient-enriched inlet of the Northern Baltic Proper. Botanica Marina 39:281-295 Koltsova TI, Konoplya LA, Maksimov VN, Fedorov VD (1971) On the representativeness of samples in phytoplankton research. Gidrobiol Zhurn (Russ J Hydrobiol) 7:109-117 (In Russian) Kononen K, Laholes EO, Gronlund L (1993) Physiological and community responses of summer plankton to nutrient manipulation in the Gulf of Finland (Baltic Sea) with special reference to phosphorus. Sarsia 78:243-253 Konovalova GV (2003) State of research on flagellate algae in the Russian waters of the Far Eastern seas. Int J Algae 5:3346 Kuosa H (1988) Enumeration of autotrophic and heterotrophic flagellates in Baltic Sea samples – a comparison of microscopical methods. Arch Hydrobiol Beih 31:301-306 McFadden GI, Hill DRA, Wetherbee R (1986) A study of genus Pyramimonas (Prasinophyceae) from south-eastern Australia. Nord J Bot 6:209-234 Mihnea PE (1997) Major shifts in the phytoplankton community (1980-1994) in the Romanian Black Sea. Oceanologica Acta 20:119-129 Throndsen J (1993) The planktonic marine flagellates. In: Tomas CR (ed) Marine phytoplankton: a guide to naked flagellates and coccolithophorids, Academic Press, pp 591-729 Thomsen HA (1988) Fine structure of Pyramimonas nansenii (Prasinophyceae) from Danish coastal waters. Nord J Bot 8:305-318
