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Seasonal Variability in Phytoplankton Carbon Biomass and Primary Production, and Their Contribution to Particulate Carbon in the Neritic Area of Sagami Bay, Japan

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Seasonal Variability in Phytoplankton Carbon Biomass and Primary Production, and Their Contribution to Particulate Carbon in the Neritic Area of Sagami Bay, Japan Plankton Benthos Res 14(4): 224–250, 2019 Plankton & Benthos Research © The Plankton Society of Japan Seasonal variability in phytoplankton carbon biomass and primary production, and their contribution to particulate carbon in the neritic area of Sagami Bay, Japan 1,2, 2 2 2,3 KOICHI ARA *, SATOSHI FUKUYAMA , TAKESHI OKUTSU , SADAO NAGASAKA & 4 AKIHIRO SHIOMOTO 1 Department of Marine Science and Resources, College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252–0880, Japan 2 Research Division in Biological Environment Studies, Graduate School of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252–0880, Japan 3 Department of Bioenvironmental and Agricultural Engineering, College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252–0880, Japan 4 Department of Ocean and Fisheries Sciences, Faculty of Bioindustry, Tokyo University of Agriculture, Abashiri, Hokkaido 099–2493, Japan Received 27 August 2018; Accepted 6 June 2019 Responsible Editor: Akira Ishikawa doi: 10.3800/pbr.14.224 Abstract: Seasonal variations in environmental variables, chlorophyll a (Chl-a), particulate carbon and nitrogen (PC and PN, respectively), phytoplankton carbon biomass (Ph-C) and primary production were investigated at a neritic sta- tion in Sagami Bay, Kanagawa, from January 2008 to December 2013. Size-fractionated Ph-C was converted from cell volume by microscopic observation, adding valuable data for this area. During spring blooms, the micro-size fraction (>20 µm) comprised the majority of the total Chl-a and total Ph-C, whereas during other periods the pico- and nano- size fraction (<20 µm) comprised a larger proportion, indicating that phytoplankton standing crops were affected by sunlight conditions and physicochemical properties of the water. In February–March, phytoplankton biomass increased and formed the first peak of spring blooms under increasing sunlight intensities (>15.7 MJ m−2 d−1), high nutrient con- centrations and balanced molar ratios. From the regression equations of size-fractionated Ph-C-Chl-a relationships, the mean Ph-C/Chl-a ratio was 5.3–7.7, 29.2–32.6 and 22.1–25.1 for the <20 µm, >20 µm and total fraction, respectively. The Ph-C/Chl-a ratio (1.8–128.8) was regulated by irradiance and nutrients. Growth rate (ca. 0–3.7 d−1) was positively correlated with irradiance and assimilation number, and negatively with the Ph-C/Chl-a ratio. The depth-integrated pri- mary production (DIPP) was 0.15–5.43 g C m−2 d−1. On the basis of the 0–50 m depth-integrated values, the total Ph-C and DIPP accounted for 1.3–34.4% and 1.3–30.9% d−1 of PC, respectively, indicating that PC variations depended on the total Ph-C and DIPP. Key words: growth rate, particulate carbon, phytoplankton carbon biomass, primary production, Ph-C/Chl-a ratio oceanic areas (e.g. Cloern et al. 2014, Costello & Chaud- Introduction hary 2017). The quantity and size composition of phyto- In general, coastal areas are highly productive habitats plankton assemblages are strongly related to food web for aquatic organisms, attributable principally to the great- structure, which influences energy flow and material (car- er phytoplankton standing crops (i.e. Chl-a, Ph-C) and pri- bon) cycles in marine ecosystems, including the amount mary production rates correlated to intermittently higher of higher trophic level productivity (Sommer et al. 2002, concentrations of land-derived nutrients in addition to Friedland et al. 2012). Hence, quantifying phytoplankton those derived from the open ocean, than found in offshore standing crop, size composition and primary production is essential to understand the food web structure and biologi- * Corresponding author: Koichi Ara; E-mail, [email protected] cal productivity of the marine ecosystem, and is significant Phytoplankton carbon biomass and primary production in Sagami Bay 225 in evaluating the role of phytoplankton in marine carbon Studies on the phytoplankton assemblages in the coastal cycles (Llewellyn et al. 2005). waters of Sagami Bay have dealt with aspects of the sea- Seasonal variations in size-fractionated (i.e. pico-, nano- sonal variations in total and size-fractionated Chl-a con- and micro-) phytoplankton standing crop (i.e. Chl-a and/ centrations (Tatara & Kikuchi 2003, Baek et al. 2007, Ara or Ph-C) have been extensively studied in subarctic and & Hiromi 2007, 2008, 2009, Baki et al. 2009, Ara et al. temperate estuarine and coastal waters in Japan, e.g. the 2011a, b, 2013, Okutsu et al. 2012, Fukuyama 2013), size- Oyashio region off Akkeshi (Shinada et al. 2001), Funka fractionated Ph-C (Ara & Hiromi 2009) and primary pro- Bay and adjacent waters (Maita & Odate 1988, Odate et duction (Ara & Hiromi 2007, 2009, Ara et al. 2011b, 2013). al. 1993, Shinada et al. 2005, 2008), Oginohara Bay (Ishi- There has been no attempt, however, to assess the sea- nomaki Bay) (Kamiyama et al. 2005), Tokyo Bay (Han sonal variations in phytoplankton standing crop in terms & Furuya 2000), Sagami Bay (Ara & Hiromi 2009), Ago of Chl-a and Ph-C and in primary production rate in rela- Bay (Tanimura et al. 2008), Hiroshima Bay (Lee et al. tion to environmental parameters (i.e. weather conditions, 1996, Kamiyama et al. 2005), Tosa Bay (Ichikawa & Hiro- physicochemical properties), and their contribution to PC ta 2004) and Uchiumi Bay (Tomaru et al. 2002), as well as in these waters. In the present study, we aimed to elucidate primary production (references in Ara et al. 2011b). These (1) the seasonal variations in size-fractionated phytoplank- studies found drastic seasonal variations with consider- ton standing crop in terms of Chl-a and Ph-C, PC and PN able peaks of Chl-a, Ph-C and primary production rate in concentration and primary production, (2) the size-frac- spring–autumn, depending on the trophic state; in oligo- tionated and total Ph-C/Chl-a ratio (i.e. conversion factor trophic open coastal waters, their peaks occurred only in to estimate carbon biomass from Chl-a), (3) growth rate of spring, whereas in eutrophic estuarine waters the peaks the phytoplankton assemblage, and (4) the contribution of occurred intermittently in summer–autumn in addition to Ph-C and primary production to PC, over 6 years (2008– in spring. However, almost all of these studies were based 2013) in the neritic area of Sagami Bay. on the determination of size-fractionated Chl-a, with stud- ies on size-fractionated Ph-C being limited, except in Fun- Materials and Methods ka Bay and adjacent waters (Maita & Odate 1988, Odate et al. 1993, Shinada et al. 2005, 2008), the Oyashio region off Field investigation Akkeshi (Shinada et al. 2001) and Sagami Bay (Ara & Hi- romi 2009). In addition, many of those studies were based A series of field investigations were conducted mostly on field investigations conducted only once in a month or every two weeks (i.e. twice a month) on 144 occasions in a season, except Ara & Hiromi (2007, 2009) and Ara from January 2008 to December 2013, at a station (Lat. et al. (2011b, 2013), which investigated size-fractionated 35°16.3′N, Long. 139°29.6′E; local depth: ca. 56 m) located Ph-C and/or primary production twice a month for mul- in the neritic area off Enoshima Island (ca. 4 km off the tiple years in the innermost open area, near Enoshima Is- coastline), Fujisawa, Kanagawa, of Sagami Bay (Fig. 1). land, of Sagami Bay. On each date, sampling was always done during daytime Sagami Bay is a semi-circular embayment, located on (07:30–12:00 a.m.). the southern coast of central Honshu, the main island of The procedure for measuring physicochemical proper- Japan, and facing the western North Pacific Ocean (Fig. ties (i.e. water temperature, salinity and dissolved inor- 1). It is located in a transition zone where hyper-eutrophic ganic nutrients), Chl-a concentration and primary produc- Tokyo Bay Water flows out to the Pacific Ocean. The water tion at this station have been previously published by e.g. quality environment in the wide-mouthed Sagami Bay has Ara & Hiromi (2008, 2009) and Ara et al. (2011a, b), an maintained much better conditions than in the neighboring outline of which is briefly given as follows. Prior to sample semi-closed Tokyo Bay (Ara & Hiromi 2008, Ara et al. collection, water temperature and salinity were measured, 2011a, b), which is attributed to less freshwater discharge using a Memory STD (AST-1000/P-64K, Alec Electronics, with smaller nutrient and pollutant load from rivers, and Japan). Transparency was measured using a Secchi disk. their shorter residence time in estuarine areas due to much Water samples for assessments of cyanobacteria (size: 0.2– more frequent exchange between estuarine and offshore 2 µm) and autotrophic nanoplankton (ANP, size: 2–20 µm) ocean waters, compared to Tokyo Bay (Kawabe & Yoneno were taken at depths of 0, 10, 20, 30, 40 and 50 m, using 1987, Iwata & Matsuyama 1989, Yamada & Matsushita a Kitahara bottle. Water samples for microphytoplankton 2006). In the innermost open waters of Sagami Bay, es- (size: >20 µm), Chl-a, particulate matter (PM) and dis- pecially in the upper layer around Enoshima Island, Chl- solved inorganic nutrients were taken at depths of 0, 5, 10, a concentrations and primary production rates have been 20, 30, 40 and 50 m, using duplicate Van Dorn bottles. higher than in any other open area of this bay, and these The samples for cyanobacteria (40 ml) and ANP (100 ml) have been attributed to higher nutrient concentrations due were transferred into γ-ray-sterilized polypropylene bottles to nutrient-rich freshwater discharge from the Sakai and and HCl-sterilized glass bottles, respectively. For micro- Hikiji Rivers (Yamada & Matsushita 2005, 2006, Ara & phytoplankton, 10 or 20 L of water samples were concen- Hiromi 2007, 2008, 2009, Ara et al.
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