Temporal Variability in Primary and Copepod Production in Sagami Bay, Japan

JOURNAL OF PLANKTON RESEARCH j VOLUME 29 j SUPPLEMENT 1 j PAGES i85–i96 j 2007

Temporal variability in primary and copepod production in Sagami Bay, Japan

KOICHI ARA* AND JURO HIROMI Downloaded from https://academic.oup.com/plankt/article/29/suppl_1/i85/1467583 by guest on 28 September 2021 DEPARTMENT OF MARINE SCIENCE AND RESOURCES, COLLEGE OF BIORESOURCE SCIENCES, NIHON UNIVERSITY, KAMEINO 1866, FUJISAWA, KANAGAWA 252-8510, JAPAN

*CORRESPONDING AUTHOR: [email protected]

Received November 15, 2005; accepted in principle September 19, 2006; accepted for publication October 26, 2006; published online December 6, 2006

Communicating editor: R.P. Harris

Seasonal variations in primary production and in abundance, biomass and production of the planktonic copepod community were investigated in the neritic area of Sagami Bay, Kanagawa, Japan, from January 2002 to December 2004. Primary production (PP) determined by 13C in situ incubation was ca. 0–1321.4 mgCL21 day21 (or 0.044– 4.643 g C m22 day21). Copepod abundance, biomass and production rates showed remarkable seasonal and interannual variations, being highest in March 2002, with an overall mean of 3.11 103 ind. m23, 8.85 mg C m23 and 0.94 mg C m23 day,21, respectively. The depth- integrated copepod secondary (SP) and tertiary production (TP) was 0.0038–0.401 and 0.00079–0.048 g C m22 day21, respectively. Transfer efficiencies from PP to SP and TP was 0.3–74.6% (mean: 4.1%) and 0.1–27.5% (mean: 0.8%), respectively. Transfer efficiency of PP–SP and PP–TP decreased exponentially with PP, and there were significant correlations between PP and transfer efficiency of PP–SP and PP–TP, respectively. The depth-integrated food requirement by copepod secondary and tertiary producers was estimated to be 0.012–1.29 and 0.0024–0.185 g C m22 day21, corresponding to 1.1–267.6% (mean: 14.3%) and 0.2–105.6% (mean: 2.6%) of PP, respectively.

INTRODUCTION several hundred years, the bay has been the site of an active fishery. Since at least the 1960s until now, the Sagami Bay, located on the southeastern coast of total annual fishery capture in Sagami Bay has been Honshu, the main island of Japan, is a semi-circular maintained at 30 000 tons wet weight year21, and embayment, facing the western North Pacific Ocean most of this has been caught in the shallow (,250 m (Fig. 1). This bay has an area of 2700 km2, with a depth), coastal and neritic waters. From the viewpoint maximum depth of 1900 m and a mean depth of ca. of interannual variations in the total fishery capture, 750 m. It is situated in the transition zone where water Sagami Bay can be regarded as the most stable ground of Tokyo Bay rich in dissolved inorganic and organic for fishery production in Japan (Kobata, 2003). nutrients and suspended organic matter, one of the Although good water quality has been maintained in most heavily eutrophic semi-enclosed embayments in Sagami Bay compared to that of neighboring Tokyo Japan, opens to the Pacific Ocean. Bay, since the 1980s some signs of eutrophication Sagami Bay is traditionally well known for its beauti- (i.e. deterioration of water quality, outbreaks of red ful natural environment, which is one of the most tides) have occurred in some coastal and/or neritic prominent habitats in Japan noted for a large number waters (Nakata,1982; Saitoh, 1992; Yamada and Iwata, of marine organisms with a high biodiversity. For 1992). Thus, to understand the environmental status of

doi:10.1093/plankt/fbl069, available online at www.plankt.oxfordjournals.org # The Author 2006. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j VOLUME 29 j SUPPLEMENT 1 j PAGES i85–i96 j 2007 Downloaded from https://academic.oup.com/plankt/article/29/suppl_1/i85/1467583 by guest on 28 September 2021

Fig. 1. Map showing the sampling station in Sagami Bay.

these waters, it is necessary to investigate the aquatic their community structure and standing stocks may ecosystems (e.g. biological communities, biological pro- respond to environmental changes, and then these vari- duction, energy and/or material ﬂow) in addition to ations may feedback to the environment: zooplankton physico-chemical parameters. may play an important role supplying dissolved in- In marine environments, zooplankton serve as an organic nutrients (N and P) to phytoplankton. important linkage principally as heterotrophic (second- Ecological studies on the planktonic copepods in ary and tertiary) producers by transferring energy and Sagami Bay have dealt principally with aspects of their organic materials from primary producers (phytoplank- diversity and community structure, distribution and ton) to higher trophic levels (planktivorous ﬁsh, carni- temporal (time-to-time, day-to-day or seasonal) vari- vorous invertebrates). In these ecosystems, copepods ations in abundance and/or biomass (e.g. Aizawa and generally represent the most important taxonomic Marumo, 1967; Nakata, 1982; Mitani, 1988a, b; group that comprises the majority (i.e. 70–80% or Shimode et al., 2006). However, no previous estimate more) of the mesozooplankton in terms of both abun- has been made copepod biomass and production rates dance and biomass (e.g. Raymont, 1983). In addition, in relation to phytoplankton primary production. The

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present study provides a quantitative survey of seasonal calculated according to Hama et al. (Hama et al., variations in primary production and in the abundance, 1983). The dark uptake was always corrected for biomass, production rates and food requirement of the primary productivity. The depth-integrated primary planktonic copepods over three years in the neritic area production was calculated as the integral of primary of Sagami Bay. productivities in the photic zone, i.e. from the sea- surface to the depth corresponding to 1% of sea- surface light intensity. METHOD Copepods from sub-samples (0.2–13.3% of the orig- inal samples) were identiﬁed by species, stage (CI–CVI)

A series of field investigations were conducted fort- and sex, and were counted under a microscope. Downloaded from https://academic.oup.com/plankt/article/29/suppl_1/i85/1467583 by guest on 28 September 2021 nightly during the period from January 2002 to Usually, more than 500 copepods were analyzed from December 2004, at a fixed station (Lat. 35816’N, Long. each sub-sample. Measurements of body length 1398 29’E) located in the neritic waters of Sagami Bay (prosome or total body length) were made for all ana- (Fig. 1). Zooplankton samples were collected by vertical lyzed specimens using an eyepiece micrometer. tows from the bottom (at depth of ca. 55 m) to the Biomass was calculated for each individual whose surface, using a plankton net (45 cm in mouth diameter, body was discriminated into prosome (cephalothorax) 200 mm in mesh opening size), equipped with a flow- and abdomen, using the following length–weight meter (Rigosha). Net samples were immediately pre- regression equation (Uye, 1982), expressed as: served in a buffered formalin seawater solution with a 9 3:07 final concentration of 5–10%. Wc ¼ 4:27 10 PL ð1Þ Prior to zooplankton sampling, water temperature and salinity were recorded every 1 m from the surface where Wc is individual weight (mg C) and PL is to the bottom, using a Memory STD (Alec Electronics prosome length (mm). The biomass of the copepods AST-1000/P-64K). Water samples were collected at whose prosome and abdomen are not clearly discrimi- depths of 0, 5, 10, 20, 30, 40 and 50 m, using duplicate nated such as Microsetella, Macrosetella and Euterpina were Van Dorn bottles (10 L 2). Usually, 500 ml aliquots calculated using a regression equation (Hirota, 1981), collected at the seven depths were filtered through a expressed as: Whatman GF/F filter (47 mm). Chlorophyll a concentration of these samples was determined using a fluo- 10 3:26 Wd ¼ 8:51 10 BL ð2Þ rometer (Turner Designs TD-700), after extraction with 90% acetone (Parsons et al., 1984). where W is dry weight (mg) and BL is total body length Primary production was determined by an in situ d (mm). Carbon content was assumed to be 47% of dry 13C method. Water samples were taken from six weight (Hirota, 1981). depths (100, 50, 25, 10, 5 and 1% photon fluxes just The production rate (P ,mgCm23 day21) was esti- above the sea surface), using a 12-L Niskin bottle. c mated by the equation, expressed as: The depths corresponding to these light levels were measured using a flat quantum sensor (Li Cor Model P ¼ SN W G ð3Þ LI-250 Light Meter). After removing large zooplank- c c ton by sieving through a 200 mm mesh, seawater 23 samples were immediately transferred into clean 1-L where N is abundance (ind. m ) and G is individual 21 or 0.5-L polycarbonate bottles (two light bottles and weight-specific growth rate (day ). Here, G was esti- one dark bottle at each depth). After the addition of mated for copepodites and adults of all copepod 13 species, using the simple model proposed by Hirst and NaH CO3 (ca. 10% of the total inorganic carbon in ambient water), the bottles were placed at the same Lampitt (Hirst and Lampitt, 1998), expressed as: depths at which the water samples were taken, and were incubated in situ for 24 h. Then, the samples log10 G ¼ 0:0208T 0:3221 log10 Wc 1:1408 ð4Þ were filtered through precombusted (at 4508C for 4 h) Whatman GF/F filters (47 mm). These filters were where T is ambient temperature (8C). dried at 608C for 1–2 h, fumed with HCl for 3 h to Secondary and tertiary production rates were calcu- remove inorganic carbon, dried at 608C and stored in lated separately on the basis of the feeding habits of a desiccator. The isotopic ratios of 13Cto12C were each genus: herbivorous, Acrocalanus, Calanus, Eucalanus, determined by a quadruple mass-spectrometer (Europe Paracalanus, Rhincalanus, Microsetella, Macrosetella and Scientific ANCA-SL). Primary productivity was Euterpina; omnivorous Acartia, Oithona, Centropages and

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Temora; and carnivorous Oncaea, Corycaeus, Labidocera RESULTS and Euchaeta (Itoh, 1970; Uye et al., 1987; Uye and Shimazu, 1997). The production by typical herbivores Environmental variables and carnivores was assigned to secondary and tertiary production, respectively. The production by Water column temperature and salinity varied from 8 omnivores was halved and added to each production 12.3 to 28.2 C and from 29.27 to 34.68 psu, respect- value (Uye et al., 1987; Uye and Shimazu, 1997), ively. Water temperature and salinity were vertically because many omnivores can shift feeding habit homogeneous from November to April. Thermo- and depending on the ambient food conditions (Anraku haloclines developed at ca. 20–30 m depth from June

a Downloaded from https://academic.oup.com/plankt/article/29/suppl_1/i85/1467583 by guest on 28 September 2021 and Omori, 1964; Lonsdale et al., 1979; Landry, to October (Fig. 2). Chlorophyll concentration in the m 21 1981). The depth-integrated secondary and tertiary water column ranged from 0.031 to 20.34 gL . a production was estimated by multiplication of second- Chlorophyll concentrations were high at 0–20 m ary and tertiary production rates and sampling depth during the spring–summer periods, and were depths, respectively. low throughout the water column during the autumn– Transfer efficiency (TE, %) from primary winter period (Fig. 2). production (PP,gCm22 day21) to copepod secondary and tertiary production (SP and TP, respectively, Primary production 22 21 gCm day ) was calculated by the following The depth of the photic zone varied from 4.5 to 51 m, equation: with an overall mean of 23.9 m. Daily primary productivity varied from ca. 0 to 1321.4 mgCL21 day21. SP The depth-integrated primary production varied from TE ¼ 100 ð5Þ 22 21 PPSP PP 0.044 to 4.643 g C m day , with an overall mean of 1.083 g C m22 day21. Larger variations and higher TP TE ¼ 100 ð6Þ rates of primary production were observed from PPTP PP February to October, and the rates were low from December to January (Fig. 2). Food requirement (FR,mgCm23 day21) by copepod secondary and tertiary producers was estimated, using Abundance the following equations (Ikeda and Motoda, 1978), expressed as: Net zooplankton was composed of adult and juvenile stages of various taxonomic groups including holo- and meroplankters. Copepods were the most dominant Res FR ¼ ð7Þ component during the study period, accounting for ðAs GrÞ 21.8–97.4% (overall mean: 65.9%) of the total mesozooplankton abundance. Total copepod abundance (CI–CVI) varied 21 21 where Res is respiration rate (mLO2 ind. h ). As from 4.04 102 ind. m23 in January 2003 to (assimilation efficiency) and Gr (gross growth efficiency) 3.04 104 ind. m23 in March 2002, with an overall were assumed to be 0.7 and 0.3, respectively (Ikeda and mean of 3.11 103 ind. m23. Copepod abundance Motoda, 1978). Res was estimated by the showed no consistent seasonal pattern, and very much multiple-regression model proposed by Ikeda (Ikeda, higher abundances were observed in March and June 1985), expressed as: 2002 (Fig. 3). In total, 67 copepod species were identified during

Res ¼ 0:524 þ 0:8354 ln W c þ 0:0601T ð8Þ the study period. The numerically dominant species (maximum relative abundance: .20% of the total copepods) were Paracalanus (¼Parvocalanus) crassirostris, where Wc is individual weight (mg C). Oxygen respired Paracalanus sp., Acartia omorii, Oithona plumifera, Corycaeus is converted to carbon using a respiratory quotient of catus, Oncaea venusta and Temora turbinata. The genus 0.97 (Gnaiger, 1983), and to daily rates by multiplying Paracalanus was predominant during the study period, by 24 (hours). The depth-integrated food requirement accounting for 24.6–87.9% (overall mean: 59.3%) of was estimated by multiplication of the food requirement the total copepod abundance. Oithona was more import- of secondary and tertiary producers and sampling ant from November to May, comprising 9.5–15.3% depths, respectively. (mean of each month in 2002, 2003 and 2004). Acartia

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Fig. 2. Seasonal variations in vertical proﬁle of water temperature, salinity, chlorophyll a concentration and primary productivity and in depth-integrated primary production in Sagami Bay, from January 2002 to December 2004. was more important from January to July (monthly Although the pattern of biomass variations was generally mean: 8.3–31.3%), Oncaea, Corycaeus and Calanus were similar to that of abundance, an additional peak occurred more important in February–May and August– in November 2002 (Fig. 4), which was attributed mainly November, and Eucalanus and Temora in August and to large-sized Calanus sinicus. The contribution of Calanus September, respectively (Fig. 3). (overall mean: 20.5%) and Eucalanus (overall mean: 8.2%) to the total copepod biomass was higher than compared its contribution to total copepod abundance, whereas the Biomass contribution of Oithona in terms of biomass was only Total copepod biomass ranged from 0.95 to 81.50 mg 18.0–55.8% (overall mean: 28.6%) compared to that in Cm23, with an overall mean of 8.85 mg C m23. terms of abundance.

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Fig. 3. Seasonal variations in abundance of total copepods (upper) and its composition (lower) in Sagami Bay, from January 2002 to December 2004.

Daily production rate (Fig. 5). The higher production rates in March and June The daily production rate of the total copepod commu- 2002 were dominated by Paracalanus (74.8–85.8%). nity varied from 0.097 to 7.77 mg C m23 day21, with Calanus and Temora were the greatest contributors in an overall mean of 0.94 mg C m23 day21. The pro- November and September, comprising 41.5% and duction rate was higher in March, June, September and 30.3% of the total copepod production, respectively November 2002, but lower from January to May 2003 (Fig. 5).

Fig. 4. Seasonal variations in biomass of total copepods (upper) and its composition (lower) in Sagami Bay, from January 2002 to December 2004.

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Fig. 5. Seasonal variations in daily production rate of total copepods (upper) and its composition (lower) in Sagami Bay, from January 2002 to December 2004.

The ratio of daily production to biomass (daily P/B Transfer efficiency from primary production to ratio) varied from 0.07 day21 in November 2002 to copepod tertiary production (PP–TP) varied from 0.1 0.16 day21 in May 2003, with an overall mean of to 27.5%, with an overall mean of 0.8%. The transfer 0.12 day21. efficiencies of PP–TP were higher in September– Copepod secondary production varied from 0.069 to October 2002 (9.7–27.5%), and October–November 7.39 mg C m23 day21 (overall mean: 0.78 mg C m23 2003 (9.5–16.1%), but were low (ca. ,1%) during day21). The depth-integrated copepod secondary pro- most of other periods (Fig. 6). duction varied from 0.0038 to 0.401 g C m22 day21 The transfer efficiencies of PP–SP and PP–TP (overall mean: 0.044 g C m22 day21). The secondary decreased exponentially with increasing primary pro- production constituted 56.8–97.3% (overall mean: duction. There were significant correlations between 81.9%) of the total copepod production (Figs. 5 and 6). primary production and transfer efficiency of PP–SP The copepod tertiary production varied from 0.013 and PP–TP, respectively (Fig. 7). Although the transfer to 0.84 mg C m23 day21 (overall mean: 0.15 mg C m23 efficiency from copepod secondary production to ter- day21). The depth-integrated copepod tertiary pro- tiary production (SP–TP) decreased with copepod sec- duction varied from 0.00079 to 0.048 g C m22 day21 ondary production, there was no significant correlation (overall mean: 0.0085 g C m22 day21). The depth- between copepod secondary production and transfer integrated tertiary production was higher (0.029–0.048 g efficiency of SP–TP (Fig. 7). Cm22 day21) in September and October 2002, but lower (ca. ,0.01 g C m22 day21) during most other periods (Figs. 5 and 6). Food requirement Thedepth-integratedfoodrequirementofcopepodsec- ondary and tertiary producers varied from 0.012 to Transfer efficiency 1.29 g C m22 day21 (overall mean: 0.155 g C m22 day21) Transfer efficiency from primary production to copepod and from 0.0024 to 0.185 g C m22 day21 (overall mean: secondary production (PP–SP) varied from 0.3 to 0.028 g C m22 day21), respectively (Fig. 8). The ratio of 74.6%, with an overall mean of 4.1%. The higher food requirement by copepod secondary producers transfer efficiencies of PP–SP were observed in to primary production was higher (.100%) in March 2002 (74.6%) and October–November 2003 March 2002 (119.8–256%), September–November (52.3–66.2%) (Fig. 6). 2002 (134.1–164%) and October–November 2003

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Fig. 6. Seasonal variations in depth-integrated copepod secondary and tertiary production (upper) and in transfer efﬁciency from primary production to copepod secondary and tertiary production (lower) in Sagami Bay, from January 2002 to December 2004. TE: transfer efﬁciency; PP: primary production; SP: secondary production; TP: tertiary production.

(100.2–267.6%), and very low in February–March 2003 (1.9–3.6%) and May–September 2003 (1.1– 18.6%) and April–September 2004 (1.3–14.4%) (Fig. 8). The ratio of food requirement of copepod tertiary producers to primary production was higher in September–October 2002 (35.7–105.8%) and October–November 2003 (30.8–57.2%), and low during most of other periods (Fig. 8).

DISCUSSION In Sagami Bay, the coastal and neritic waters, especially near Enoshima Island including our sampling station, have higher levels of biological productivity (i.e. phytoplankton primary production, copepod production) than other areas of the bay, because of their higher nutrient concentrations and phytoplankton standing stocks (Saitoh, 1992; Yamada and Iwata, 1992). For this reason, the present study was carried out at one sampling station off Enoshima Island in order to investigate the seasonal variations in primary production and copepod production in the most productive area of this bay, although primary and copepod production can also vary spatially. 13 Fig. 7. Relationships between primary production and transfer The C method employed in the present study esti- efficiency from primary production to copepod secondary and tertiary mates primary productivity from uptake rate of dis- production (upper and middle, respectively) and between secondary solved inorganic carbon by phytoplankton, which is production and transfer efficiency from secondary to tertiary 14 production (lower). TF: transfer efficiency; PP: primary production; similar to the C method that estimate close to actual SP: secondary production; TP: tertiary production. net primary production in natural environments when

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Fig. 8. Seasonal variations in depth-integrated food requirement by copepod secondary and tertiary producers (upper) and in the ratios of food requirement to primary production in Sagami Bay, from January 2002 to December 2004. FR: food requirement. samples are incubated for .12 h, though the utilization phytoplankton standing stock (chlorophyll a) and of the radio-isotope 14C in natural environments has primary production were low. been restricted in Japan (Hashimoto and Saino, 2004). The present study focused on copepods of the meso- Although with the 13C method, it is necessary to use a zooplankton (.200 mm), not including eggs and nau- longer incubation period than the 14C method because pliar stages. The copepodite stages of small species were of the lower sensitivity compared with the 14C method, rare in our samples, suggesting insufficient collection of chlorophyll a-specific carbon assimilation rates deter- the smaller copepods, which would have passed through mined by the 13C and 14C methods were quite similar the plankton net used in the present study. Nonetheless, to each other for marine phytoplankton (Hama et al., the highest biomass and production rates obtained in 1983). Primary production measured in the present the present study were comparable to those in other study was higher than that formerly observed in other high-productive waters, e.g. Osaka Bay, Japan coastal and offshore waters of Sagami Bay (0.18– (74.44 mg C m23 and 18.29 mg C m23 day21, Koga, 4.09 g C m22 day21, Noda and Ichimura, 1967; 1987), the Inland Sea of Japan (44.64 mg C m23 and Shimura and Ichimura, 1972; Kudo and Yamaguchi, mean 5.28 mg C m23 day21, Koga, 1986; 74.0 mg 2000; Hashimoto et al., 2005). The highest primary pro- Cm23 and 14.3 mg C m23 day21,Uyeet al., 1987), duction in Sagami Bay was relatively high compared to Fukuyama Harbor, Japan (147 mg C m23 and other bays, coastal and neritic waters in Japan, which 45.2 mg C m23 day21, Uye and Liang, 1998), Kingston followed that in hyper-eutrophic waters such as Tokyo Harbour, Jamaica (50 mg AFDW m23 and mean Bay (14.61 and 16.42 g C m22 day21, Yamaguchi et al., 12.3 mg AFDW m23 day21, Hopcroft et al., 1998) and 1991), Mikawa Bay (13.6 g C m22 day21, Tanaka and the Cananeía Lagoon estuarine system, Brazil Sano, 1980) and the Inland Sea of Japan (30.66 mg C m23 and 11.11 mg C m23 day21,Ara, (9.5 g C m22 day21,Uyeet al., 1987). 2004), although the annual mean values in the present In the present study, the total copepod abundance study were somewhat lower than in these waters, in showed no consistent seasonal variations, nor did which smaller mesh sizes (62–100 mm) were employed biomass and production rate (Figs. 3–5). This was for sample collections. unexpected, since it is common that zooplankton One of the most characteristic aspects of primary and (copepod) abundance, biomass and production rate are copepod production in Sagami Bay is transfer efficiency. much higher in warm months than in cold months in Transfer efficiency from primary production to copepod temperate waters (e.g. Raymont, 1983). In particular, we secondary and tertiary production decreased with cannot explain the notably high abundance, biomass increase in primary production (Fig. 7), as similarly and production rate in March 2002 when temperature, observed by Greze (Greze, 1970) and Cushing

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(Cushing, 1971). This indicates that in Sagami Bay, transfer efficiency was controlled principally by primary production, when primary production was lower than ca. 0.5 g C m22 day21. Additionally, when primary production was higher than ca. 1 g C m22 day21, transfer efficiency was constant, independent of copepod production. Estimations of transfer efficiency are time-consuming because they involve calculation from separately estimated primary production and copepod production rates. In particular, estimations of copepod Downloaded from https://academic.oup.com/plankt/article/29/suppl_1/i85/1467583 by guest on 28 September 2021 production needs several parameters (i.e. abundance, individual weight, growth rate, water temperature), compared to primary production measurements. For a general estimate for copepods in Sagami Bay, transfer efficiency as well as copepod production can be estimated from primary production, using regression equations of primary production–transfer efficiency relationships obtained in the present study. Although on most of the sampling dates, primary production was sufficient for copepod food requirement, Fig. 9. Trophodynamics of lower trophic levels in Sagami Bay based on eight dates copepod food requirement greatly on three-year carbon flow through three components from phytoplankton primary production to copepod secondary and tertiary exceeded primary production (Fig. 8). On these production. occasions, herbivorous copepods must feed on not only newly produced phytoplankton, but also on phytoplankton standing stocks. On the other hand, omnivorous et al., 1997), Dokai Inlet (in summer: ca. 43%, Uye copepods might shift their feeding habit from herbivory et al., 1998) and Ise Bay (in winter: ca. 27%, Uye et al., to carnivory (e.g. Anraku and Omori, 1964; Lonsdale 2000). The present study focused on carbon flow from et al., 1979; Landry, 1981). In pelagic ecosystems, in phytoplankton primary production to secondary and addition to copepods, there are other many hetero- tertiary production of copepods of the mesozooplankton trophic organisms, such as microzooplankton (e.g. (CI–CVI), which would be the principal carbon flow in copepod nauplii, tintinnids, naked ciliates) and hetero- classical food chains. The relative role and importance trophic nanoflagellates, that feed on phytoplankton (e.g. of copepods in the Sagami Bay ecosystem may be Azam et al., 1983). Thus, in Sagami Bay, sometimes further understood in future studies with additional primary production would be insufficient for hetero- focus on the microplankton (e.g. bacteria, microflagel- trophic organisms such as copepods that feed directly lates, microzooplankton: Ara unpublished data), consid- on phytoplankton. ering also microbial food webs (e.g. Uye and Shimazu, Although transfer efficiency showed large seasonal 1997; Uye et al., 1998, 2000). variations, the trophodynamics of lower trophic levels in Sagami Bay is assessed by carbon flow through three components from phytoplankton primary production to ACKNOWLEDGEMENTS copepod secondary and tertiary production (Fig. 9). On the basis of a three-year mean, annual transfer effi- We thank Mr Kazuharu Yuasa, captain/owner of the ciency from primary production to copepod secondary fishery boat ‘Genshun-maru’, for continuously helpful production in Sagami Bay was estimated to be 4.1%. assistance in fieldwork. We thank Drs Akihiro Shiomoto This was equivalent to that in Ise Bay (in winter: 4.4%, and Katsuyuki Sasaki, National Research Institute of Uye et al., 2000), Osaka Bay (3.8%, Joh and Uno, 1983; Fisheries Science, for helping determination of primary 0.8–5.8%, Koga, 1987) and Dokai Inlet (in summer: productivity. Thanks are also due to all members 4.2%, Uye et al., 1998), and was lower than in the who participated in ‘Project SHONAM’ for helping Inland Sea of Japan (21.7%, Uye et al., 1987; 14.4%, fieldwork and analyzing samples. This research was Hashimoto et al., 1997). The annual transfer efficiency financially supported in parts by the Ministry of from copepod secondary to tertiary production in Education, Culture, Sports Science and Technology Sagami Bay, estimated to be 19.5%, was lower than of Japan through ‘Open Research Center Project’ of in the Inland Sea of Japan (ca. 29%, Hashimoto Nihon University.

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