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(particularly nanoplankton), which has been commonly found in coastal .... microzooplankton consume most of the primary production by nanophytoplankton.

Journal of Oceanography Vol. 52, pp. 689 to 703. 1996

Geographical and Seasonal Variations in Abundance, Biomass and Estimated Production Rates of Microzooplankton in the Inland Sea of Japan SHIN-ICHI UYE, NAOKI NAGANO and HIDENORI TAMAKI Faculty of Applied Biological Science, Hiroshima University, Higashi-Hiroshima 724, Japan (Received 22 December 1995; in revised form 19 March 1996; accepted 22 March 1996)

We measured abundance and biomass of 3 major groups of microzooplankton, i.e. tintinnids, naked ciliates and copepod nauplii, at 21 stations in the Inland Sea of Japan in October 1993, January, April and June 1994. The average abundance of the microzooplankton over the entire Inland Sea of Japan ranged from 2.39 × 105 indiv. m–3 in January to 4.00 × 105 indiv. m–3 in April. Ciliated protozoans, i.e. tintinnids plus naked ciliates, numerically dominated the microzooplankton. The average biomass of the microzooplankton was exceedingly high in October (8.62 mg C m–3) compared to that in the other months (2.06, 2.79 and 2.68 mg C m–3 in January, April and June, respectively). The ciliated protozoans also dominated in terms of biomass except in October, when copepod nauplii were more important. Estimated production rate of the microzooplankton was highest in October (average: 6.02 mg C m–3d–1) and followed in order by June, April and January (1.94, 1.14 and 0.54 mg C m–3d–1, respectively). Due to higher specific growth rate, the production rate by the ciliated protozoans far exceeded that by the copepod nauplii. The trophic importance of the microzooplankton in the pelagic ecosystem of the Inland Sea of Japan was assessed by estimating carbon flow through the microzooplankton community. 1. Introduction The importance of microzooplankton (body dimensions between 20 and 200 µm) in the marine ecosystem have been increasingly evident in the past decade. Despite smaller biomass relative to meso- and macrozooplankton, microzooplankton (particularly ciliated protozoans) may have higher weight-specific metabolic rates than metazoan competitors (Heinbokel, 1978; Verity, 1985, 1986a, b). By virtue of small body size, microzooplankton can exploit small food particles which may be unavailable to larger animals, and they may thus act as a significant food source for larger metazoan predators (Robertson, 1983; Stoecker and Egloff, 1987; Stoecker and Capuzzo, 1990). The Inland Sea of Japan is a semi-closed narrow sea, being divided into 9 sub-areas, i.e. from east to west, Kii Channel, Osaka Bay, Harima Nada, Bisan Seto Strait, Hiuchi Nada, Aki Nada, Hiroshima Bay, Iyo Nada and Suo Nada, according to the geographical and topographical features (Fig. 1). Several estimates of the rates of primary production and meso- and macrozooplankton production have been made (Endo, 1970; Endo and Okaichi, 1977; Hirota, 1977; Joh and Uno, 1983; Uye et al., 1987, and others) in order to understand the transfer of organic matter to fish production, since the annual catch of fish per unit area is one of the world’s highest in this area (21 m. tons km–2yr–1, Tatara, 1981). To our knowledge, microzooplankton have been quantified only in 3 sub-areas of the Inland Sea of Japan, i.e. Suo Nada (Aizawa, 1985),


S. Uye et al.

Fig. 1. Map of the Inland Sea of Japan with the locations of sampling stations.

Osaka Bay (Aizawa, 1987) and Hiroshima Bay (Kamiyama, 1994); their geographical distribution over the entire Inland Sea of Japan has never been studied. In this study, the geographical and seasonal variations in abundance, biomass and production rate of microzooplankton over the entire Inland Sea of Japan were investigated during 4 cruises between October 1993 and June 1994. Other collaborative studies have focused on physicochemical parameters, phytoplankton biomass and primary production rate, meso- and macrozooplankton biomass and production rate. Here, we present the data for microzooplankton along with some environmental and biological properties with which the microzooplankton may interact. In addition, the role of the microzooplankton community in pelagic carbon flow in the Inland Sea of Japan is evaluated. 2. Materials and Methods Microzooplankton sampling and general oceanographic surveys were conducted at 21 stations (Fig. 1) during 4 cruises (12–22 October 1993, 8–21 January 1994, 12–22 April 1994, 20–30 June 1994) of T & R/V Toyoshio Maru, Hiroshima University. At each station, a hydrographic cast was made using a Sea Bird STD with a Sea Tech fluorometer attached, which provided continuous records of temperature, salinity and in vivo fluorescence. Water samples were collected with a pair of 10-l Van Dorn bottles at 3 to 5 depths (0.5, 5, 10, 20 m and 2 m above the sea-bottom) depending on the depth of station. For microzooplankton samples, 250 to 500 ml of water at each depth was taken in a plastic bottle, to which neutralized formalin was added at a final concentration of 1%. These samples were kept refrigerated at ca. 3°C in darkness until later examination. 500 to 1000 ml of water from each depth was filtered through glassfiber filters (Whatman GF/F), which were then transferred to plastic bottles containing 10 ml of N,Ndimethylformamide (Suzuki and Ishimaru, 1992) and kept at ca. –20°C in darkness. Later, chlorophyll a concentration was determined spectrophotometrically according to the method

Microzooplankton Biomass and Production in the Inland Sea of Japan


described by Parsons et al. (1984). The preserved microzooplankton sample was subsampled and concentrated by settling to a final volume of ca. 10 ml, and this was transferred to a settling chamber for examination under an inverted microscope. We enumerated 3 major microzooplankton categories, i.e. tintinnids, naked ciliates (excluding functionally autotrophic ciliate Mesodinium rubrum) and copepod nauplii. Animals of other taxa such as radiolarians, rotifers, larvaceans and benthic invertebrate larvae were usually much lower in numbers, and hence, were excluded from our study. Lengths of appropriate body dimensions were measured to the nearest 1 µm by an eye-piece micrometer, and lorica volume of tintinnids and cell volume of naked ciliates were determined according to their geometric configurations. From lorica volume (LV, µm3), body carbon weight of a tintinnid (Ct, pg) was calculated using the regression equation: Ct = 444.5 + 0.053LV (Verity and Langdon, 1984). Lorica occupancy was assumed to be 100%. Carbon weight of a naked ciliate was converted from cell volume using a factor of 0.14 pg µm–3 (Putt and Stoecker, 1989). Carbon content of a copepod nauplius (Cc, ng) was calculated from body length (BL, µm) with the regression equation: Cc = 1.51 × 10–5BL2.94 (Uye, unpublished). The production rate of each taxonomic group (P, mg C m–3d–1) was estimated from biomass (B, mg C m–3) and empirically-determined instantaneous growth rate (g, d–1): P = B × g. For copepod nauplii, we used the following regression equation to describe the composite relationship between instantaneous growth rate and temperature (T, °C) for 8 copepod species from the Inland Sea of Japan (Uye, 1980, 1982, 1988, 1991; Uye et al., 1983, unpublished; Kimoto et al., 1986; Liang et al., 1996): g = 0.057e0.069T. For ciliated protozoans, we used the following multiple regression proposed by Montagnes et al. (1988): lng = 0.1438T – 0.3285ln(V × 10–3) – 1.3815, where V is cell volume (µm3 ). The cell volume of tintinnids was calculated back from their body carbon weight using the conversion factor (0.14 pg µm–3) similar to naked ciliates. The growth rates estimated from above methods are considered to be close to potential, because copepod nauplii were reared under food-satiated conditions and the growth data of ciliates were derived from maximal values from laboratory culturing experiments by Fenchel (1968) and Finlay (1978). Since our study emphasized the geographical or horizontal variations rather than the vertical variations, environmental parameters and microzooplankton quantity at each station were represented by the depth weighted water column averages, calculated by dividing the integrated values through water column by the depth of the water column. A mean value was calculated for each sub-area with more than 2 stations, and then the average over the entire Inland Sea of Japan was calculated based on the water volumes of respective sub-areas (Environmental Agency, 1995). In this calculation, the values from St. 21 were excluded, since officially Bungo Channel is not a part of the Inland Sea of Japan.


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3. Results 3.1 Environmental variables Due to complicated geomorphology and hydrography of the Inland Sea of Japan, envi-

Fig. 2. Geographical variations in temperature and chlorophyll a concentration in the Inland Sea of Japan in October 1993, January, April and June 1994. Values are water-column averages. St. 15 could not be occupied in January because of bad weather.

Microzooplankton Biomass and Production in the Inland Sea of Japan


ronmental parameters showed considerable geographical variations. The seasonal water column stratification was lacking at St. 7 in Bisan Seto Strait due to strong tidal current, while it was prominent at stations in bays and Nadas, where the tidal current is relatively weak. The water-column average temperature ranged from 20.7–23.9, 10.1–15.3, 11.4–16.0 and 18.1–22.3°C in October, January, April and June, respectively (Fig. 2). Average salinity ranged from 28.8 to 34.4 during the present study (not figured). It was always high at stations in and near

Fig. 3. Geographical variation in abundance of microzooplankton (tintinnids: open column, naked ciliates: shaded column, and copepod nauplii: filled column) in the Inland Sea of Japan in October 1993, January, April and June 1994. Values are depth-weighted water-column averages.


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Kii Channel and Bungo Channel where offshore saline water intruded, while it was low at stations in the inner part of Osaka Bay and Hiroshima Bay where the water was diluted with river runoff. Chlorophyll was always high at stations in the inner part of bays because of high nutrient concentrations (not figured). Average chlorophyll ranged from 0.8–9.8, 0.6–7.1, 0.8–11.6 and 0.8–12.4 µg l–1 in October, January, April and June, respectively (Fig. 2). 3.2 Microzooplankton abundance The vertical distribution of microzooplankton abundance varied geographically within the same cruise and seasonally at the same station. The pattern was also different among taxonomic

Fig. 4. Geographical variation in biomass of microzooplankton (column shadings as in Fig. 3) in the Inland Sea of Japan in October 1993, January, April and June 1994. Values are depth-weighted water-column averages.

Microzooplankton Biomass and Production in the Inland Sea of Japan


groups. Both tintinnids and naked ciliates were generally more abundant at shallower depths (i.e. 0.5 and 5 m), although at several stations in April and June, tintinnids showed a prominent numerical peak at near-bottom depth. Copepod nauplii were distributed more homogeneously throughout the water column than these ciliated protozoans. The water-column average of microzooplankton abundance also varied geographically as well as seasonally (Fig. 3). The density varied by 2 orders of magnitude from 3.0 × 104 to 2.19 × 106 indiv. m–3. In October, the average over the Inland Sea of Japan was 3.76 × 105 indiv. m–3, among which naked ciliates were most numerous (51%), followed by copepod nauplii (37%) and tintinnids (12%). In January, April and June, when the average was 2.39 × 105 , 4.00 × 105 and 2.72 × 105 indiv. m–3, respectively, tintinnids represented the largest proportion (59, 83 and 74%, in January, April and June, respectively). 3.3 Microzooplankton biomass The water-column average biomass varied from 0.53 to 28.3 mg C m–3. The average biomass

Fig. 5. Relationships between biomass of various microzooplankton taxonomic groups (mg C m–3) and chlorophyll concentration (µg l–1). Only cases with significant (p < 0.05) positive correlation are presented. Regression equation in each case is as follows. Tintinnids in October (1): B = 0.34 + 0.19Chl (r = 0.61), naked ciliates in October (2): B = –0.27 + 0.73Chl (r = 0.67, filled circles) and January (3): B = –0.19 + 0.41Chl (r = 0.88, open circles), copepod nauplii in October (4): B = 3.74 + 0.46Chl (r = 0.49), and total microzooplankton in October (5): B = 3.95 + 1.28Chl (r = 0.69, filled circles), January (6): B = 1.06 + 0.57Chl (r = 0.71, open circles) and June (7): B = 1.90 + 0.61Chl (r = 0.46, filled squares).


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Fig. 6. Relationship between percent contribution of ciliated protozoan biomass to microzooplankton biomass (P, %) and chlorophyll concentration (Chl, µg l–1). Only cases with significant (p < 0.05) positive correlation are presented: in October (P = 23.6 + 2.7Chl, r = 0.60, filled circles) and January (P = 45.9 + 6.8Chl, r = 0.66, open circles).

over the entire area was higher (8.62 mg C m–3) in October than in any other months (2.06, 2.79 and 2.68 mg C m–3 in January, April and June, respectively, Fig. 4). Copepod nauplii accounted for 60% of the community biomass in October, but ciliated protozoans dominated (64 and 69%) in January and April. In June, micrometazoans and ciliated protozoans were approximately equal (48:52). Within the ciliated protozoans, naked ciliates represented 77% in October, while tintinnids made larger contributions to ciliate biomass in April (72%) and June (82%). In January, the biomass of naked ciliates and tintinnids was nearly equal (49:51). Geographically, the microzooplankton biomass was always low in and near Kii Channel and Bungo Channel (e.g. Sts. 1, 20, 21), while it was often high in the inner part of bays (e.g. Sts. 3, 4, 12). Considering the rapid growth rate of microzooplankton, particularly ciliated protozoans (Heinbokel, 1978; Verity, 1986b), positive relationship between microzooplankton and their food concentration is expected. We examined correlations between average biomass of each of 4 categories (i.e. tintinnids, naked ciliates, copepod nauplii and total microzooplankton) and averaged chlorophyll concentration. Significant (p < 0.05) positive linear correlations were obtained for only 1 or 2 cruises out of 4 for tintinnid, naked ciliates and copepod nauplii (Fig. 5). However, when these taxa were combined, the regression was significant during 3 cruises (Fig. 5). We also examined the relationship between biomass of ciliated protozoans relative to total microzooplankton biomass and chlorophyll concentration. There was a significant (

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