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Growth Characteristics and Vertical Distribution of Triparma Laevis (Parmales) During Summer in the Oyashio Region, Western North Pacific

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Growth Characteristics and Vertical Distribution of Triparma Laevis (Parmales) During Summer in the Oyashio Region, Western North Pacific Vol. 68: 107–116, 2013 AQUATIC MICROBIAL ECOLOGY Published online January 10 doi: 10.3354/ame01606 Aquat Microb Ecol Growth characteristics and vertical distribution of Triparma laevis (Parmales) during summer in the Oyashio region, western North Pacific Mutsuo Ichinomiya1,*, Miwa Nakamachi2, Yugo Shimizu3, Akira Kuwata2 1Prefectural University of Kumamoto, Tsukide 3−1−100, Higashi, Kumamoto 862−8502, Japan 2Tohoku National Fisheries Research Institute, Shinhamacho 3−27−5, Shiogama, Miyagi 985−0001, Japan 3National Research Institute of Fisheries Science, Fukuura 2−12−4, Kanazawa, Yokohama 236−8648, Japan ABSTRACT: The vertical and regional distribution of Triparma laevis (Parmales), a siliceous pico- sized eukaryotic marine phytoplankton species, was investigated during summer off the south coast of Hokkaido, Japan, in the western North Pacific. Growth characteristics were also studied in the laboratory using a recently isolated culture strain. T. laevis was abundant in the subsurface layer (30 to 50 m), where water temperature was <10°C, but it was absent above the pycnocline when temperatures were >15°C. Growth experiments revealed that T. laevis was able to grow at 0 to 10°C but not higher than 15°C, indicating that its depth distribution mainly depended on tem- perature. High irradiances resulted in increased growth rates of T. laevis, with the highest rates of 0.50 d−1 at 150 µmol m−2 s−1. Using measured daily incident photosynthetically available radiation and in situ light attenuation, the growth rates of T. laevis at 30 and 50 m were calculated as 0.02 to 0.34 and −0.01 to 0.08 d−1, respectively. Distribution of T. laevis was strongly coupled with the occurrence of Oyashio water. The growth rate of T. laevis was lower than that of bolidophytes and diatoms, which are closely related to Parmales. Bloom forming diatoms in this region have higher growth rates and a broader temperature range (0 to 20°C) and, therefore, might be expected to dominate, but Parmales does manage to co-exist in this region, albeit at a moderate abundance compared to the diatoms. KEY WORDS: Triparma laevis · Parmales · Vertical distribution · Growth characteristics · Oyashio region Resale or republication not permitted without written consent of the publisher INTRODUCTION phytoplankton (Guillou et al. 1999b, Not et al. 2005) with growth characteristics determined from culture Photosynthetic pico-eukaryotes (≤3 µm) account for experiments (Timmermans et al. 2005, Lovejoy et al. a large fraction of the biomass and primary produc- 2007). tion in marine ecosystems (Li 1994, Worden et al. Parmales (Heterokonta) is a pico-sized eukaryotic 2004, Massana 2011). They are highly diverse, com- marine phytoplankton group of small solitary cells prising several algal classes (Moon-van der Staay et that are surrounded by variously shaped silica plates al. 2001, Fuller et al. 2006, Vaulot et al. 2008). To (Booth & Marchant 1987). They are widely distrib- understand how environmental factors affect their uted from tropical to polar waters (Nishida 1986, abundance and distribution as well as their ecologi- Takahashi et al. 1986, Booth & Marchant 1987, Kos- cal role in marine environments, an auto-ecological man et al. 1993), but they are more frequently approach is necessary. However, there have been reported from polar and sub-polar waters (Booth et few auto-ecological studies combining measures of al. 1981, 1982, Taniguchi et al. 1995, Komuro et al. the abundance and distributions of pico-eukaryotic 2005, Konno et al. 2007). Phylogenetic information *Email: [email protected] © Inter-Research 2013 · www.int-res.com 108 Aquat Microb Ecol 68: 107–116, 2013 was very limited until we managed to isolate and the Oyashio and Kuroshio-Oyashio transition characterize a Parmales species, Triparma laevis, for regions with laboratory investigations of growth the first time from the western North Pacific (Ichino - characteristics under varying temperatures and miya et al. 2011). The molecular phylogenetic analy- irradiances. ses of SSU rDNA and the rbcL gene revealed that T. laevis belonged to the class Bolidophyceae, which are autotrophic pico-sized naked flagellates that lack MATERIALS AND METHODS silica structures and form a sister group of diatoms (Guillou et al. 1999a). Field study Some morphological features of Parmales, such as the number of plates or plate ornamentation, are spe- Oceanographic observations were carried out from cies-specific (Booth & Marchant 1987, Konno et al. 7 to 22 July 2009 at 21 stations along the monitoring 2007) and can only be observed with a scanning elec- route ‘A-line’, which crosses the Oyashio and tron microscope (SEM). There have been some stud- Kuroshio-Oyashio transition regions, off the south ies on abundance and distributions of Parmales coast of Hokkaido, Japan, in the western North species (Booth et al. 1980, Bravo-Sierra & Hernán- Pacific (Fig. 1A). Temperature and salinity were dez-Becerril 2003, Konno & Jordan 2007), but only 2 recorded with a CTD. Water samples for quantifying studies have assessed growth characteristics using nutrients and chlorophyll a concentrations were col- natural Parmales assemblages (Taniguchi et al. 1995, lected with a bucket at the surface and Niskin sam- Ichinomiya et al. 2010) and no laboratory growth pling bottles from 7 depths from 10 to 100 m at every studies using cultures. station of A1 to A4 and odd stations of A5 to A21. The The Oyashio Current is located in the southwest- samples for quantifying the abundance of Triparma ern part of the western subarctic gyre in the North laevis were collected from 7 depths at 0, 10, 20, 30, Pacific, flowing southwestward along the Kuril Is - 50, 80 and 100 m at the same stations collected for lands and Hokkaido. The flow turns to the east off nutrient analysis. At Stn A1, the water was collected Honshu, becoming an extension flow. The area sur- at 90 m but not at 100 m because the depth at this rounded by the Oyashio Current and its extension is station was <100 m. Aliquots (500 ml) of water sam- called the Oyashio region. The Oyashio region is ples were fixed with acid Lugol’s solution (final conc. colder and less-saline than the southern areas, i.e. 1%) and stored in a dark cold room (5°C) until SEM the subtropical Kuroshio region and Kuroshio- analysis. Oyashio transition region, where warm and cold Incident photosynthetically available radiation eddies frequently detach from the Kuroshio and (PAR, 400 to 700 nm) above the sea surface was Oyashio regions, respectively (Itoh & Yasuda 2010). continuously measured on deck with a PAR sensor In the Oyashio region, a massive phytoplankton (ML-020P, EKO Instruments) and recorded in a data bloom (mainly diatoms) normally occurs in spring logger during the investigation period. During day- due to the nutrient-rich Oyashio water, but this ter- time sampling, vertical profiles of water PAR were minates with the development of water stratification obtained with a profiling reflectance radiometer in summer (Isada et al. 2009). Parmales abundance PRR-600/610 (Biospherical Instruments). From the increases from late spring, reaching a peak in vertical profiles, attenuation coefficients (k, m−1) summer–autumn in the Oyashio region (H. Hattori were determined to approximate the following pers. comm.). However, the spatial distribution of equation: Parmales across the Kuroshio-Oyashio transition I = I exp−kz (1) region as well as the effects of hydrographic features z 0 are still unknown. where Iz and I0 are the irradiance at each depth (z, m) Triparma laevis belongs to the family Triparma- and the surface. ceae and is widely distributed in the North Pacific The concentrations of nitrate and silicate were (Booth et al. 1982, Konno et al. 2007). In the Oya - determined with a TRAACS 800 autoanalyzer follow- shio region, Ichinomiya et al. (2010) reported that ing the methods of Strickland & Parsons (1972). For this species was dominant (>90%) among the Par- chlorophyll a analysis, 128 ml aliquots of sea water males assemblage in winter. The aim of the present were filtered using glass-fiber filters. The filters were study was to investigate what controls the vertical soaked in N, N-dimethylformamide to extract chloro- and horizontal distributions of T. laevis during sum- phyll a (Suzuki & Ishimaru 1990) and determined mer by combining field data collected from across with a Turner Designs fluorometer (10-AU-005). Ichinomiya et al.: Growth characteristics and distribution of Parmales 109 A B 45° 45° N Okhotsk Sea N 44° 200 m 44° Hokkaido Hokkaido 43° 45° N 1000 m 43° 45° N A1 42° 2000 m 42° WCR 41° 3000 m 41° CWR1 A-line 40° 4000 m 40° Latitude Latitude 39° 5000 m 39° Honshu Honshu 38° 6000 m 38° A21 37° 6500 m 37° CWR2 36° 36° 140°E 142° 144° 146° 148° 150° 140°E 142° 144° 146° 148° 150° Longitude Longitude Fig. 1. (A) Sampling stations along the monitoring section A-line with the bottom topography and (B) the isotherms (°C) at 100 m depth in July 2009. The temperature map was the color-modified one of the monthly publication by Tohoku National Fisheries Research Institute (http://tnfri.fra.affrc.go.jp/kaiyo/temp/data/200907_100.gif), which was drawn based on present observations and the other cooperative organizations’ data. The area with temperature <6°C at 100 m depth, which was re- garded as the Oyashio region according to Kawai’s (1972) indicator isotherm, is shaded, and the locations of a warm core ring (WCR) and the cold water regions (CWR1 and CWR2) along the A-line are denoted in panel B The counting method for Triparma laevis was sim- Culture experiments in the laboratory ilar to that used by Booth at al. (1981) and Taniguchi et al. (1995). To quantify T. laevis abundance, Incubation experiments used the Triparma laevis 286 ml aliquots of the fixed samples were filtered strain that was isolated from the Oyashio region and through 0.6 µm polycarbonate filters using low vac- deposited in the culture collection of the National In- uum pressure (<10 kPa).
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