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Journal of Oceanography, Vol. 61, pp. 645 to 654, 2005

Seasonal Variations of Plankton Food Web Structure in the Coastal Water off Usujiri Southwestern Hokkaido, Japan A KIYOSHI SHINADA 1,2*, SYUHEI BAN1,3, Y UICHIRO YAMADA1,4 and TSUTOMU IKEDA1 1

Graduate School of Fisheries Sciences, Hokkaido University, Minato-cho, Hakodate, Hokkaido 041-8611, Japan 2 Hokkaido Prefectural Abashiri Fisheries Experiment Station, Masuura, Abashiri, Hokkaido 099-3119, Japan 3 School of Environmental Science University of Shiga Prefecture, Hassaka-cho, Hikone, Shiga 522-8533, Japan 4 Ocean Research Institute, The University of Tokyo, Minamidai, Nakano-ku, Tokyo 164-8639, Japan (Received 13 January 2004; in revised form 1 September 2004; accepted 1 September 2004)

The planktonic food web structure in the subarctic coastal water off Usujiri southwestern Hokkaido, Japan was investigated from June 1997 to June 1999, based on seasonal biomass data of pico- (200 µ m), and path analysis using the structural equation model (SEM). In spring, microphytoplankton predominated due to diatom bloom, while picoand nanophytoplankton predominated in the other seasons, except November and December 1997. The seasonal change in size distribution of heterotrophic plankton was almost similar to that of phytoplankton, and mesozooplankton biomass was high in spring. The path analyses suggest that the main channel in the microbial food web could vary according to phytoplankton size composition, indicating not only the classical food chain (microphytoplankton - copepods) but also the indirect route (microphytoplankton - naked dinoflagellates - copepods).

Keywords: ⋅ Planktonic food web, ⋅ classical food chain, ⋅ microbial food web, ⋅ structural equation model.

as oligotrophic waters (Sherr and Sherr, 1988; Cushing, 1989). Although the classical food chain could efficiently transfer organic carbon from low to high trophic levels (Cushing, 1989), the microbial food web contributes less to high trophic levels since there are many trophic levels and protozooplankton have higher metabolic costs (Roman et al., 1995; Rousseau et al., 2000). The study of the plankton food web is therefore important to understand the biological productivity of marine systems in terms of their efficiencies and final yields. In Japanese coastal area, a few studies of the plankton food web have been conducted in the Inland Sea (Uye et al., 1996) and Funka Bay (Ban, 2000). On the other hand, many studies have been reported concerning the plankton food web in the world coastal area, such as the Gulf of St. Lawrence (Savenkoff et al., 2000), the Limfjorden in Denmark (Andersen and Sørensen, 1986), the Australian Antarctic station (Leakey et al., 1996), the coastal zone in the Baltic Sea (Lignell et al., 1993; Uitto et al., 1997) and the North Sea (Nielsen and Richardson, 1989; van Boekel et al., 1992; Nielsen et al., 1993;

1. Introduction In marine plankton food webs, the solar energy fixed photosynthetically in organic matter by phytoplankton is channeled to higher trophic levels via two routes. One is the “classical food chain”, which is the route from microphytoplankton (10–200 µ m) to mesozooplankton (>200 µm) (e.g. Riley, 1947). The other is the “microbial food web”, which includes a “microbial loop” consisting of heterotrophic bacteria and protozoans (Azam et al., 1983), and all pro- and eukaryotic unicellular phytoplankton such as pico- (30 cells per filter, using an ocular


Latitude (°N)

Funka Bay 80 m 100 m 300


St.60 Usujiri 20′




Fig. 2. Path diagram summarizing the microbial food web structure of “bottom-up” (solid lines) and “top-down” models (dashed lines). HNF is heterotrophic nanoflagellates.

Longitude (°E)

Fig. 1. Location of sampling station (St. 60) off Usujiri, southwest Hokkaido, Japan. Bathymetric contours (80, 100 and 300 m) are superimposed.

micrometer. Microplankton were counted under an inverted microscope after allowing samples to settle overnight. Although autotrophic and heterotrophic dinoflagellates (including unidentified micro-size flagellates) were discriminated by epifluorescence microscopy, all ciliates were decided to heterotrophic due to a few appearances of Mesodinium ruburm. Biovolumes were estimated from the measurement of length and width of the organisms, assuming simple geometrical shapes. The wet weights of mesozooplankton were determined after the fractionation of samples into 330 µm, 850 µm and 1800 µm sizes by sequential filtration. The wet weight of each fraction was measured, and major systematic groups such as copepods, euphausiids, chaetognaths, amphipods, appendicularians and others were counted. Assuming that the wet weight of each systematic group in the same fraction is equivalent, the wet weight of each systematic group was calculated. The cell volume (V, µm3) of nano- and microplankton and wet weight of mesozooplankton were converted to carbon values using appropriate formulae or conversion factors (Table 1). Mesozooplankton respiration (Rm, µl O2 ind.–1h–1) was calculated as a function of body mass (CW, mg C ind.–1) and temperature (T, °C), i.e. ln Rm = 0.5254 + 0.8354 ln CW + 0.0601 T (Ikeda, 1985). The food requirement of mesozooplankton was calculated from their respiration rates, assuming the respiratory quotient (RQ) to be 0.97 (Gnaiger, 1983), the gross growth efficiency to be 0.3 and the assimilation efficiency to be 0.7 (Ikeda, 1985).

2.3 Statistical analysis Cluster analysis was carried out to group phytoplankton and zooplankton (33.6) were observed in September to December 1998 near the bottom, which had not been seen during the same season in the previous year (1997). The water column stratified from April to November or December. A strong pycnocline was established in the upper 30 m during August and September in both 1997 and 1998. 3.2 Seasonal changes in plankton biomass The biomass of autotrophic plankton (integrated 0– 50 m) in the euphotic zone (37.1 ± 10.8) varied from 6.3 to 245.2 mgC m–3 (Fig. 5). Biomass values exceeding 50 mgC m –3, as observed in December 1997, and in March and April 1998, were due to the predominance of microphytoplankton (>92%) which consisted mainly of diatoms. On the other occasions the autotrophic biomass was relatively low (58%), except in November 1997 and March and April 1999. In regard to the composition of picophytoplankton, although cyanobacteria was dominant from June to December, eukaryotic picophytoplankton was most abundant in all other months. For microphytoplankton, diatoms were the most important component from November to May, ex648

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Fig. 4. Seasonal changes in vertical profiles of water temperature (°C, top), salinity (middle) and sigma-t (bottom) at St. 60. Dots indicate data points.

cept in April 1999. On the other occasions, naked dinoflagellates and thecate dinoflagellates were dominant components in microphytoplankton. The cluster analysis distinguished two major groups at 200 levels of distance (Figs. 5 and 6), e.g. Group1: mainly microphytoplankton (in November and December 1997, in March and April 1998 and in March and April 1999) and Group2: mainly pico- and nanophytoplankton (all other months). The biomass of heterotrophic plankton in the euphotic zone ranged from 10 to 66 mgC m–3 (Fig. 7), with peaks in April 1998 and 1999. Thereafter, the biomass decreased gradually and reached low values in winter. Ranges of seasonal variations of each component were 9–27 mgC m–3 for bacteria, 1–8 mgC m–3 for HNF, 1–40 mgC m–3 for microzooplankton and 1–25 mgC m–3 for mesozooplankton. Naked dinoflagellates and naked ciliates were the most abundant components of microzooplankton throughout the year (50–93%), except in June 1997. The cluster analysis distinguished two major groups at 100 levels of distance (Figs. 6 and 7), e.g. Group3: mainly microzooplankton (in November 1997, in March, April and September 1998 and in March and April 1999) and Group4: mainly bacteria and HNF (all

Fig. 5. Seasonal changes in pico-, nano- and microphytoplankton biomass (upper), and relative abundance of two picophytoplankton (middle) and three microphytoplankton components (lower) at St. 60. nd = no data.

other months). These size groups were almost similar to phytoplankton groups, such as micro-size (Group1 and Group3) and pico/nano-size (Group2 and Group4). Mesozooplankton biomass was high, comprising ca. 30% of the total heterotrophic plankton biomass in April 1998 and 1999. Copepods were the most important component in mesozooplankton throughout the year (50–96%). 3.3 Plankton food web structure In “top-down” models of the microbial food web and the interaction between microplankton and copepods, many significant positive path coefficients from predator to prey organism (e.g. from microzooplankton to microphytoplankton) were observed (data not shown). These positive path coefficients imply that the predator increases induce the prey increases, and these relations can thus not be viewed as realistic. The “top-down” models were therefore rejected. In “bottom-up” microbial food web model, two models were constructed due to the seasonal variations of phytoplankton size composition (pico- and nanophytoplankton predominated, and microphytoplankton predominated; Figs. 5 and 6). The goodness of fit index (GFI) of the pico- and nanophytoplankton-predominated model (n = 75) and the microphytoplankton-predominated model (n = 30) were

high (GFI 0.962 and 0.968, respectively) compared to that of the model using all data (GFI 0.943, n = 105). The first two “bottom-up” microbial food web models were thus adapted in this study. In the pico- and nanophytoplankton-predominanted model, many path coefficients from prey to predator were significantly positive (Fig. 8). On the other hand, the path coefficient from microphytoplankton to microzooplankton was only significantly positive in the microphytoplanktonpredominanted microbial food web model (Fig. 8). In addition, significantly negative path coefficient from microphytoplankton to bacteria was also observed. The GFI of “bottom-up” in the interaction between microplankton and copepods was high (0.902, n = 21), so this model was adopted in this study. Although the path coefficients from microphytoplankton to naked dinoflagellates and naked ciliates, and from naked dinoflagellates to copepods were significantly positive, the others were not significant (Fig. 9). Therefore, the indirect interaction via naked dinoflagellates (microphytoplankton - naked dinoflagellates mesozooplankton) was high (0.52). 4. Discussion In this study, the phytoplankton community structure could be divided into two groups: one being that

Seasonal Variations of Plankton Food Web Structure in the Coastal Water off Usujiri Southwestern Hokkaido, Japan



(a) Autotrophs 0







Mar 99 Apr 99 Group 1

Mar 98 Nov 97 Dec 97 Apr 98 Jul 97 Sep 98 Sep 97 Nov 98 Apr 97 Dec 98

Group 2

Oct 97 Jun 98 Jul 98 Jun 97 Jan 98 Jun 98 May 98 Feb 98 Feb 99

(b) Heterotrophs

Distance 0





Mar 98 Apr 98 Group 3

Mar 99 Sep 98 Nov 97 Apr 99 Oct 97 Feb 99 Nov 98 Dec 98 Jun 99 Jun 98

Group 4

Feb 98 Aug 97 May 98 Dec 97 Jul 98 Jan 98 Sep 97 Jun 97 Jul 97

Fig. 6. Dendrogram of the cluster analysis, showing the phytoplankton (a) and zooplankton (b) community could be grouped to two sub-communities.

microphytoplankton predominated in November and December 1997, in March and April 1998 and 1999, while the other is that pico- and nanophytoplankton predominated in all other months (Fig. 6). In spring (March and April), diatom bloom has been observed regularly in Usujiri coastal water (Yokouchi, 1984; Onishi, 1999), thereby microphytoplankton might be the most dominant component of phytoplankton community in spring every year. On the other hand, dominance of microphytoplankton was not observed in November and December 1998, in spite of the outbreak in November and December 1997 (Fig. 5). From the viewpoint of 650

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hydrographic conditions, although the water column was uniform in November and December 1997, the pycnocline was developed in November and December in 1998 due to the presence of high saline water in the lower layer (Fig. 4). While nutrient observation was not done in the present study, the nutrient input to the euphotic zone might occur in November and December 1997, but not in November and December 1998. The nutrient input could cause microphytoplankton production to accelerate, so that the microphytoplankton might become predominant in November and December 1997. An influence of the water column structure on phytoplankton size structure

Fig. 7. Seasonal changes in bacteria, HNF (heterotrophic nanoflagellates), microzooplankton and mesozooplankton biomass (upper), and the composition of microzooplankton (middle) and mesozooplankton (lower) at St. 60. nd = no data.

has been postulated in the other regions, e.g. southern Kattegat (Nielsen and Kiørboe, 1991), northern Baltic Sea (Uitto et al., 1997) and Gulf of St. Lawrence (Savenkoff et al., 2000). In the present path analyses of the microbial food web models, was observed significantly positive pass coefficients from prey to predator (Fig. 8). These positive coefficients might imply that the increase of prey plankton induced the increase of predator plankton due to their feeding on prey plankton. The autotrophic plankton was divided into two groups (Fig. 6). The pico- and nanophytoplankton predominated model was almost combined with the bacteria and HNF predominated one (Figs. 5, 6 and 7), and significantly positive coefficients from prey to HNF and from phytoplankton to Microzooplankton were obtained in the pico- and nanophytoplankton predominated model (Fig. 8). On the other hand, the significantly positive coefficient was only from microphytoplankton to microzooplankton in the microphytoplankton-predominated model (Fig. 9), when the microzooplankton was dominant in heterotrophic plankton (Figs. 6 and 7). These differences could indicate that the main channel in the microbial food web could vary according to phytoplankton size composition. As for the interaction between microplankton and copepods, the path coefficient from microphytoplankton

to copepods was not significant, but the indirect route from microphytoplankton to naked dinoflagellates and from naked dinoflagellates to copepods was significantly positive, respectively (Fig. 9). These results suggest that the indirect route (microphytoplankton - naked dinoflagellates - copepods) could prevail in the coastal water off Usujiri. A recent studies have reported the microzooplankton grazing on microphytoplankton in the nearby Funka Bay (Odate and Maita, 1990), in the nearby water off Cape Esan (Shinada et al., 2003), in the Kiel Bight (Smetacek, 1981) and in the Kattegat (Hansen, 1991). In addition, protozoans such as naked dinoflagellates and naked ciliates are both qualitatively and quantitatively important in the diets of suspensionfeeding copepods (Stoecker and Capuzzo, 1990), and copepods feeding on microzooplankton have been reported in California coastal water and the Irish Sea (Kleppel et al., 1991), in Oregon coastal waters (Fessenden and Cowles, 1994), in the subarctic Pacific (Gifford, 1993) and a subantarctic site (Atkinson, 1996). In this study, the classical food chain (microphytoplankton - copepods) could not been detected by the path analysis (Fig. 9). However, the food requirement of mesozooplankton (mostly copepods) was high from April to June (median = 6.1 mgC m–3d–1, quartile deviation = 0.6, n = 6, data not shown), compared to other

Seasonal Variations of Plankton Food Web Structure in the Coastal Water off Usujiri Southwestern Hokkaido, Japan


Fig. 9. Path diagram of the interaction between microplankton and copepods at St. 60. Numbers alongside lines represent path coefficients (*P < 0.05, **P < 0.01, ***P < 0.001).

Fig. 8. Path diagram of the microbial food web, showing the pico and nanophytoplankton predominanted model (a) and microphytoplankton predominanted model (b). Numbers alongside lines represent path coefficients (*P < 0.05, **P < 0.01, ***P < 0.001).

months (median = 1.6, quartile deviation = 1.1, n = 15), and microphytoplankton biomass was higher than microzooplankton biomass from April to June, except for April in 1999 (Figs. 5 and 7). In fact, the grazing on phytoplankton by copepods (the classical food chain) has been observed all over the world, such as the nearby Funka Bay (Ban, 2000), the Gironde estuary (Benoît et al., 2000), the California coastal waters and the Irish Sea (Klepper et al., 1991) and the North Sea (Gasparini et al., 2000). Therefore, the classical food chain could exist in the coastal water off Usujiri in particular from April to June. The change in microphytoplankton biomass depends on their growth, their death, grazing by predators and their sinking loss. In particular, the sinking loss might be the most important factor for decreasing their biomass dur652

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ing the spring bloom (Nielsen and Richardson, 1989; Lignell et al., 1993). Unfortunately, the sinking loss was not observed in this study, and this could be one of the factors why the existence of the classical food chain was not detected by the path analysis. In conclusion, in the coastal water off Usujiri, the main channel in the microbial food web could vary according to phytoplankton size composition, and the indirect route of microphytoplankton - naked dinoflagellates - copepods could prevail. However, these results were derived from the analysis of plankton biomass data only. For more detailed analysis, including production, grazing and feeding between the size and trophic components of plankton community, experimental studies (such as the “dilution” technique) are needed in the future. Acknowledgements We are grateful to Mr. Y. Harada and Mr. K. Miyazaki for their assistance in sampling at sea and valuable discussions in the course of this study. Thanks are extended to the captains and crew of R/V Ushio Maru for their cooperation at sea. We also thank two anonymous reviewers for their valuable comments and suggestions. Appendix (see p. 654) References Andersen, P. and H. M. Sørensen (1986): Population dynamics and trophic coupling in pelagic microorganisms in eutrophic coastal waters. Mar. Ecol. Prog. Ser., 33, 99–109. Atkinson, A. (1996): Subantarctic copepods in an oceanic, low chlorophyll environment: ciliate predation, food selectivity and impact on prey population. Mar. Ecol. Prog. Ser., 130, 85–96. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil and F. Thingstad (1983): The ecological role of water-col-

umn microbes in the sea. Mar. Ecol. Prog. Ser., 10, 257– 263. Ban, S. (2000): Grazing and microbial food chains during diatom blooming and post-diatom-blooming period. Bull. Coast. Oceanogr., 38, 23–28 (in Japanese with English abstract). Benoît, S., L. F. Artigas, D. Delmas, A. Herbland and P. Laborde (2000): Grazing impact of micro- and mesozooplankton during a spring situation in coastal waters off the Gironde estuary. J. Plankton Res., 22, 531–552. Børsheim, K. Y. and G. Bratbak (1987): Cell volume to carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Mar. Ecol. Prog. Ser., 36, 171–175. Brussaard, C. P. D., R. Riegman, A. A. M. Noordeloos, G. C. Cadée, H. Witte, A. J. Kop, G. Nieuwland, F. C. van Duyl and R. P. M. Bak (1995): Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar. Ecol. Prog. Ser., 123, 259–271. Brussaard, C. P. D., G. J. Gast, F. C. van Duyl and R. Riegman (1996): Impact of phytoplankton bloom magnitude on a pelagic microbial food web. Mar. Ecol. Prog. Ser., 144, 211– 221. Cushing, D. H. (1989): A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J. Plankton Res., 11, 1–13. Fessenden, T. and T. J. Cowles (1994): Copepod predation on phagotrophic ciliates in Oregon coastal waters. Mar. Ecol. Prog. Ser., 107, 103–111. Gasparini, S., M. H. Daro, E. Antajan, M. Tackx, V. Rousseau, J.-Y. Parent and C. Lancelot (2000): Mesozooplankton grazing during the Phaeocystis globosa bloom in the southern bight of the North Sea. J. Sea Res., 43, 345–356. Gifford, D. J. (1993): Protozoa in the diets Neocalanus spp. in the oceanic subarctic Pacific Ocean. Prog. Oceanogr., 32, 223–237. Gnaiger, E. (1983): Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. p. 337–347. In Polarographic Oxygen Sensors, ed. by E. Gnaiger and H. Horstner, Springer-Verlag, Berlin. Hansen, P. J. (1991): Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar. Ecol. Prog. Ser., 73, 253–261. Hass, L. W. (1982): Improved epifluorescence microscopy for observing planktonic micro-organisms. Ann. Inst. Oceanogr. Paris, 58, 261–266. Ikeda, T. (1985): Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature. Mar. Biol., 85, 1–11. Kano, Y. (2002): Does structural equation modeling outperform classical factor analysis, analysis of variance and path analysis? Jpn. J. Behaviormetrics., 29, 138–159 (in Japanese). Kirchman, D. L., R. G. Kell, M. Simon and N. A. Welschmeyer (1993): Biomass and production of heterotrophic bacterioplankton in the oceanic subarctic Pacific. Deep-Sea Res. I, 40, 967–988. Kleppel, G. S., D. V. Holliday and R. E. Pieper (1991): Trophic interactions between copepods and microplankton: a question about the role of diatoms. Limnol. Oceanogr., 36, 172– 178.

Leakey, R. J. L., S. D. Archer and J. Grey (1996): Microbial dynamics in coastal waters of East Antarctica: bacterial production and nanoflagellate bacterivory. Mar. Ecol. Prog. Ser., 142, 3–17. Li, W. K. W., P. M. Dickie, W. G. Harrison and B. D. Irwin (1992): Biomass and production of bacteria and phytoplankton during the spring bloom in the western North Atlantic Ocean. Deep-Sea Res. II, 40, 307–327. Lignell, R., A.-S. Heiskanen, H. Kuosa, K. Gundersen, P. Kuuppo-Leinikki, R. Pajuniemi and A. Uitto (1993): Fate of a phytoplankton spring bloom: sedimentation and carbon flow in the planktonic food web in the northern Baltic. Mar. Ecol. Prog. Ser., 94, 239–252. Menden-Deuer, S. and E. J. Lessard (2000): Carbon to volume relationships for dinoflagellates, diatoms, and other protest plankton. Limnol. Oceanogr., 45, 569–579. Mullin, M. M. (1969): Production of zooplankton in the ocean: the present status and problems. Oceanogr. Mar. Biol. Ann. Rev., 7, 293–310. Mullin, M. M., P. R. Sloan and R. W. Eppley (1966): Relationship between carbon content, cell volume and area in phytoplankton. Limnol. Oceanogr., 11, 307–311. Nielsen, T. G. and T. Kiørboe (1991): Effects of a storm event on the structure of the pelagic food web with special emphasis on planktonic ciliates. J. Plankton Res., 13, 35–51. Nielsen, T. G. and K. Richardson (1989): Food chain structure of the North Sea plankton communities: seasonal variations of the role of the microbial loop. Mar. Ecol. Prog. Ser., 56, 75–87. Nielsen, T. G., B. Løkkegaard, K. Richardson, F. B. Pedersen and L. Hansen (1993): Structure of plankton communities in the Dogger Bank area (North Sea) during a stratified situation. Mar. Ecol. Prog. Ser., 95, 115–131. Odate, T. and Y. Maita (1990): Phagotrophic grazing by dinoflagellates on diatoms during the spring phytoplankton bloom in Funka Bay. Bull. Plankton Soc. Japan, 36, 142– 144. Onishi, T. (1999): A short term and seasonal changes in applendicularians, and production of applendicularians in coastal water, southwest part of Hokkaido, Japan. Ms Thesis, Hokkaido Univ., 51 pp. (in Japanese). Putt, M. and D. K. Stoecker (1989): An experimentally determined carbon:volume ratio for marine “oligotrichous” ciliates from estuarine and coastal water. Limnol. Oceanogr., 34, 1097–1103. Richardson, K., T. G. Nielsen, F. B. Pedersen, J. P. Heilmann, B. Løkkegaard and H. Kaas (1998): Spatial heterogeneity in the structure of the planktonic food web in the North Sea. Mar. Ecol. Prog. Ser., 169, 197–211. Riley, G. A. (1947): A theoretical analysis of the zooplankton population of Georges Bank. J. Mar. Res., 6, 104–113. Roman, M. R., D. A. Caron, P. Kremer, E. J. Lessard, L. P. Madin, T. C. Malone, J. M. Napp, E. R. Peele and M. J. Youngbluth (1995): Spatial and temporal changes in the partitioning of organic carbon in the plankton community of the Sargasso Sea off Bermuda. Deep-Sea Res. I, 42, 973– 992. Rousseau, V., S. Becquevort, J.-Y. Parent, S. Gasparini, M.-H. Daro, M. Tackx and C. Lancelot (2000): Trophic efficiency

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of the planktonic food web in a coastal ecosystem dominated by Phaeocystis colonies. J. Sea Res., 43, 357–372. Savenkoff, C., A. F. Vézina, S. Roy, B. Klein, C. Lovejoy, J.-C. Therriault, L. Legendre, R. Rivkin, C. Bérubé, J.-É. Tremblay and N. Silverberg (2000): Export of biogenic carbon and structure and dynamics of the pelagic food web in the Gulf of St. Lawrence Part 1. Seasonal variations. DeepSea Res. II, 47, 585–607. Sherr, E. B. and B. F. Sherr (1988): Role of microbes in pelagic food webs: a revised concept. Limnol. Oceanogr., 33, 1225– 1227. Sherr, E. B., D. A. Caron and B. F. Sherr (1993): Staining of heterotrophic protests for visualization via epifluorescence microscopy. p. 231–237. In Handbook of Methods in Aquatic Microbial Ecology, ed. by P. F. Kemp, B. F. Sherr, E. B. Sherr and J. J. Cole, Lewis Pub., Boca Raton. Shinada, A., S. Ban and T. Ikeda (2003): Seasonal changes in nano/micro-zooplankton herbivory and heterotrophic nanoflagellates bacterivory off cape Esan, southwestern Hokkaido, Japan. J. Oceanogr., 59, 609–618. Smetacek, V. (1981): The annual cycle of protozooplankton in the Kiel Bight. Mar. Biol., 63, 1–11. Stoecker, D. K. and J. M. Capuzzo (1990): Predation on protozoa: its importance to zooplankton. J. Plankton Res., 12, 891–908. Strathmann, R. R. (1967): Estimating the organic carbon content of phytoplankton from cell volume of plasma volume.

Limnol. Oceanogr., 12, 411–418. Uitto, A., A.-S. Heiskanen, R. Lignell, R. Autio and R. Pajuniemi (1997): Summer dynamics of the coastal planktonic food web in the northern Baltic Sea. Mar. Ecol. Prog. Ser., 151, 27–41. Uye, S., N. Nagano and H. Tamaki (1996): Geographical and seasonal variations in abundance, biomass and estimated production rates of microzooplankton in the Inland sea of Japan. J. Oceanogr., 52, 689–703. Van Boekel, W. H. M., F. C. Hansen, R. Riegman and R. P. M. Bak (1992): Lysis-induced decline of a Phaeocystis spring bloom and coupling with the microbial food web. Mar. Ecol. Prog. Ser., 81, 269–276. Verity, P. G. and C. Langdon (1984): Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. J. Plankton Res., 6, 859– 868. Verity, P. G., C. Y. Robertson, C. R. Tronzo, M. G. Andrews, J. R. Nelson and M. E. Sieracki (1992): Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol. Oceanogr., 37, 1434– 1446. Yokouchi, K. (1984): Surface distribution of polychaete larvae in Volcano Bay, southern Hokkaido, during the vernal phytoplankton bloom of 1982. Bull. Plankton Soc. Japan, 31, 113–122.

Appendix 1. Correlation matrix of pico- and nanophytoplankton, microphytoplankton, bacteria, HNF (heterotrophic nanoflagellates) and microzooplankton biomass.

Pico- and nanophytoplankton Pico- and nanophytoplankton Microphytoplankton Bacteria HNF Microzooplankton

1.00 −0.35 0.35 0.35 −0.17

Microphytoplankton Bacteria 1.00 −0.29 0.13 0.61

1.00 0.28 −0.01



1.00 0.16


Appendix 2. Correlation matrix of microphytoplankton, naked dinoflagellates, naked ciliates and copepods biomass (bottom up models).

Microphytoplankton Naked dinoflagellates Naked ciliates Copepods


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Naked dinoflagellates

Naked ciliates


1.00 0.42 0.76 −0.17

1.00 0.59 −0.03

1.00 0.12