Distribution and modification of diatom assemblages in and around a ...

Journal of Plankton Research Vol.22 no.11 pp.2061–2074, 2000

Distribution and modification of diatom assemblages in and around a warm core ring in the western North Pacific Frontal Zone east of Hokkaido Kuo-Ping Chiang1 and Akira Taniguchi Laboratory of Biological Oceanography, Faculty of Agriculture, Tohoku University, Sendai 981, Japan 1Present

address: Department of Fishery Science, National Taiwan Ocean University, Keelung 20224, Taiwan, R.O.C.

Abstract. Spatial distribution relationships between diatom assemblages and water types were investigated in and around a 2-year-old warm core ring in the western North Pacific Polar Frontal Zone off Hokkaido, Japan. From the oceanographic and diatom data, principal component analysis and a clustering technique identified four water types and four diatom assemblages. The Background Assemblage had a low standing stock and was distributed over the entire study area, including the core water of the ring. This assemblage was associated with water conditions that were not highly suitable for diatom growth. A Cold Assemblage, probably linked to submerging Oyashio Water, was found in sub-surface waters. Its standing crop was rather high. The two other assemblages also had relatively high standing stocks: one, the Stratified Assemblage, was found around the nutricline in the sub-surface layer and the other, the Warm Streamer Assemblage, in a warm streamer flowing along the outer edge of the warm core ring. We argue here that the Stratified Assemblage emerged from the Background Assemblage because of favorable local conditions (nutrient level), and, conversely, that in the downstream of the warm streamer, the Warm Streamer Assemblage reversed to the Background Assemblage because the nutrient supply was depleted.

Introduction The main oceanographic regimes in the Western North Pacific are the subarctic Oyashio in the north, the subtropical Kuroshio (and its Extension) in the south, and the Polar Frontal Zone in between. Water masses from these regimes interact in ways that are dynamic and quite complex. In particular, the Kuroshio introduces warm streamers into the frontal zone, and as the Kuroshio Extension meanders northward, warm core rings are often pinched off (Kawai, 1972; Kawai and Saitoh, 1986; Nagata et al., 1992). These rings usually shift further north and eventually arrive in the northern part of the frontal zone east of Hokkaido. Rings found east of Hokkaido are usually >1 year old (Tomosada, 1986) and take the form of weak warm core rings in the sub-surface layer [50–150 m (Endo, 1993; Tameishi and Sugimoto, 1993)]. Warm surface (0–50 m) streamers from the south are often deflected and flow clockwise around the warm core ring before heading further east. Several diatom assemblages which are characteristic of different water masses in the southern half of the Polar Frontal Zone have previously been identified using principal component analysis (Chiang and Taniguchi, 1993; Chiang et al., 1994). Among these, a Background Assemblage characterized by a small standing stock and wider distribution range is defined by dominance of several neritic cosmopolitan species. We suggest that this assemblage is formed by the winter © Oxford University Press 2000

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convection of water, which selects a few species tolerant to winter conditions (Chiang and Taniguchi, 1993). Hence, the Background Assemblage is almost homogeneously distributed into depths over the entire Polar Frontal Zone. Some assemblages with larger standing stocks can emerge from the Background Assemblage when environmental conditions turn favorable for the active growth of particular species. Other assemblages are introduced by intruding water masses as well. Similar formation of the Background Assemblage in winter, and its modification into more productive assemblages due to environmental improvement, have also been suggested for diatoms in the East China Sea (Chiang et al., 1997, 1999). This is analogous to the seasonal succession of phytoplankton assemblages observed in rather enclosed regions like Chesapeake Bay (Marshall, 1994; Marshall and Nesius, 1996). In this paper, we use principal component analysis and a clustering technique (Pielou, 1984) to identify the diatom assemblages in the vicinity of a 2-year-old warm core ring, and to show that these assemblages are associated with different water types. From the spatial data, we then attempt to explain how these assemblages might have arisen over time. Method Sampling Between 24 May and 10 June 1991, during Cruise KT-91-7 of R/V Tansei Maru of the Ocean Research Institute, University of Tokyo, water samples were collected at various depths from the surface to 150 m at seven stations in and around a warm core ring (Figure 1). A CTD-Rosette assembly (General Oceanics) equipped with 5 l Go-Flo bottles was employed to record temperature and salinity down to 200 m, as well as to collect the water samples. Diatom species composition Diatom assemblages were determined by microscopic examination following the method of Chiang and Taniguchi (Chiang and Taniguchi, 1993). Briefly, a 500 ml water sample was preserved with 25 ml neutralized formalin. A 100 ml aliquot was taken and left to stand in a plastic bottle for 24 h. After removing supernatant water with a glass siphon, the plankton, now concentrated into about 10 ml water, were transferred to a counting chamber and again left to stand for 24 h. Identification and cell counts were then made under a Nikon-MSDR inverted microscope at a magnification of 200 or 400. Diatom identification was based on Kokubo (Kokubo, 1960), Marumo et al. (Marumo et al., 1966) and Yamaji (Yamaji, 1984), and the species are reported according to the naming convention of Hasle and Syvertsen (Hasle and Syvertsen, 1996). Only cells with a size larger than 10 µm were enumerated.

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Diatom assemblages in the North Pacific Frontal Zone

Fig. 1. Location of the seven sampling stations in the western North Pacific Polar Frontal Zone off Hokkaido, northern Japan. Stations were sampled between 24 May and 10 June 1991.

Nutrient concentrations Only water samples from the top 100 m (11 depths) were used for the determination of nutrient concentrations. Five nutrients (dissolved silica, phosphate, nitrate, nitrite and ammonia) were measured using methods described in Strickland and Parsons (Strickland and Parsons, 1972). Nitrate was reduced to nitrite with cadmium wires activated using a copper sulfate solution, and the nitrite was converted to the pink azo dye for colorimetric determination. Concentrations of reactive phosphate and dissolved silica were measured using the molybdenum blue and silicomolybdenum blue methods, respectively. Ammonia was determined by blue indophernol. Data analysis To analyze the spatial distribution of the water types and the diatom assemblages, principal component analysis (PCAs) and cluster analysis (Pielou, 1984) were applied to both the oceanographic dataset (i.e. temperature, salinity and the five nutrients; PCA-OD) and the diatom dataset (i.e. the cell counts for each species at each sample point; PCA-DD)(Table II). Based on the PCAs, clusters were identified by statistical analysis system’s (SASs) average linkage clustering method using a Euclidean distance of 0.6 for PCA-OD and 1.0 for PCA-DD (Pielou, 1984). For each diatom assemblage, a species was considered dominant if it accounted for 25% 2063


or more of the total diatom abundance in any one of the samples from that assemblage, and it appeared in more than 50% of the samples from that assemblage. Results Hydrography The temperature and salinity profiles (Figures 2A and 2B) suggest the presence of a high temperature and high salinity warm water streamer that flowed first through St. C28 (25–90 m) (>4°C, >33.4 psu) and then through St. C33 (0–60 m; >6°C, >33.6 psu). Evidence of a low temperature and low salinity (1 µg l–1) 2064


found between 20 and 50 m along the entire transect, and there was a good agreement between the (high) diatom count and chlorophyll a levels in this sub-surface layer from St. C29 to St. C32. The low diatom stock in the surface (0–20 m) layer at Sts C27–C30 also coincided with low chlorophyll a levels. However, the high diatom abundance in the sub-surface (20 m) at St. 28 and in the surface layer (0–30 m) at St. C33 were not associated with a high concentration of chlorophyll

Fig. 2. Vertical profiles along the sampling transect for (A) temperature (°C); (B) salinity (psu); (C) nitrate concentration (µmol l–1); (D) dissolved silica (µmol l–1);

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Fig. 2. continued.

Fig. 2. Vertical profiles along the sampling transect for (E) diatom abundance (103 cells l–1); (F) chlorophyll a concentration (µg l–1); and the dominant species (G) Thalassiosira nordenskioeldii (102 cells l–1); and (H) Chaetoceros radicans (102 cells l–1).

a. A higher diatom abundance was also found in the cold streamer below St. 29, but chlorophyll a was the same as that in the other sub-surface water. In PCA-DD, the first three components (PC1, PC2 and PC3 ) accounted for 31.1% of the total variance (Table II). Four clusters were identified (Figure 4), 2066


Fig. 3. PCA-OD showing the four clusters (A–D) identified by the average linkage clustering method.

Fig. 4. Three dimensional PCA-DD scatter diagram showing the four clusters (A–D) identified by an average linkage clustering analysis.

and the distribution patterns of these diatom assemblages were generally consistent with those of the water types. As shown in Figures 5B and 6, Cluster A corresponds to the Background Assemblage. This assemblage was widely distributed over the study area and was found in the warm core ring as well as down-stream 2067


Fig. 5. Vertical distribution pattern of (A) water types and (B) diatom assemblages.

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Table I. PC1 and PC2 eigenvectors from the principal component analysis of the oceanographic data (PCA-OD). Percentage of variance accounted for by each component is shown in parentheses Variables

PC1 (55.38%)

PC2 (22.65%)

Temperature Salinity Dissolved silica Reactive phosphate Nitrate Nitrite Ammonia

–0.456 0.054 0.461 0.498 0.485 0.237 0.190

0.155 0.152 –0.227 –0.070 –0.164 0.662 0.656

Table II. PC1, PC2, and PC3 eigenvectors for the 21 (out of 87) most influential species used in the PCA-DD. Only species whose eigenvector value exceeded 0.2 (indicated with an asterisk) for at least one principle component are shown here. Percentage of variance accounted for by each component is shown in parentheses Variables Bacteriastrum delicatulum Cleve Ceratulina pelagica (Cleve) Hendey Chaetoceros curvisetus Cleve Chaetoceros decipiens Cleve Chaetoceros frichei Hustedt Eucampia zodiacus Ehrenberg Fragilariopsis oceanica (Cleve) Hasle Guinarida striata (Stolterfoth) Hasle com. nov. Melosira moniliformis Mller Meuniera membranacea (Cleve) P.C.Silva comb. nov. Navicula distans (W.Smith) Ralfs in Pritchard Neodenticula seminae (Simonsen & Kanaya) Akiba & Yanagisawa Proboscia alata f. gracillima (Cleve) Grunow Proboscia alata f. inermis (Castracane) Hustedt Rhizosolenia setigera Brightwell Surirella sp. Turpin Thalassiosira angulata (Gregory) Hasle Thalassiosira gravida Cleve Thalassiosira nordenskioeldii Cleve Thalassiosira pacifica Gran Angst Thalassiosira sp. Cleve

PC1 (13.72%)

PC2 (9.43%)

PC3 (8.00%)

0.132 0.202* 0.240* 0.241* 0.205* 0.206* 0.069 0.173 0.061 0.110 0.246*

0.265* 0.175 –0.092 –0.035 –0.035 –0.116 –0.168 0.212* 0.220* 0.210* 0.013

0.067 –0.010 –0.057 –0.012 –0.101 –0.116 0.292* 0.027 0.075 0.006 –0.089

–0.111 0.270* 0.231* 0.210* –0.017 –0.110 –0.024 –0.057 0.035 –0.029

0.234* 0.080 0.093 0.061 0.203* 0.225* 0.237* 0.262* 0.269* 0.247*

–0.033 0.101 0.122 0.067 –0.019 0.115 –0.017 –0.049 0.034 –0.029

of the warm streamer. Although there was no single dominant species, this assemblage was characterized by many cold neritic species such as Chaetoceros radicans. The population density was generally low (≤5.0 104 cells l–1), except above the warm core ring and down-stream of the warmer stream (St. C33) where the density exceeded 105 cells l–1 (Figure 2E). Cluster B, the Stratified Assemblage, was found in the sub-surface layer of Sts C29 and C32. This assemblage appeared around the nutricline and was characterized by the smallest value of PC2. The largest standing stock, 3.5 105cells l–1, was recorded in this assemblage (30 m at 2069


St. C32), and the cold neritic species, C.radicans, was dominant. A Warm Streamer Assemblage (Cluster C) was found 15–25 m below St. C28, where the streamer flowed from the south. This assemblage was characterized by the largest values of PC2 and was dominated by Chaetoceros compressus, a neritic cosmopolitan species. Population density was intermediate (3.0 104–1.4 105 cells l–1). Cluster D, the Cold Streamer Assemblage, was found only at 100 m below St. 29, where the cold streamer prevailed. This assemblage had the largest value of PC3, a component influenced by cold neritic species such as Fragilariopsis oceanica, Neodenticula seminae, Thalassiosira angulata, T.gravida, T.nordenskioeldii and T.pacifica. Two cold neritic species, C.radicans and T.nordenskioeldii, were dominant. Population density was intermediate (105 cells l–1). Discussion Earlier studies have used principal component analysis to identify several diatom assemblages that are characteristic of different water masses in the southern half of the Polar Frontal Zone (Chiang and Taniguchi, 1993; Chiang et al., 1994). Above the permanent halcoline, the Background Assemblage is widely and homogeneously distributed over the entire Polar Frontal Zone. As it is characterized by a small standing stock and dominated by several neritic cosmopolitan species, we previously suggested that this assemblage resulted from the winter convection of water, a vertical mixing process, which selects for species that are tolerant to winter conditions (Chiang and Taniguchi, 1993). We have argued elsewhere (Chiang et al., 1997, 1999) that in the East China Sea, more productive assemblages can emerge from the Background Assemblage when environmental conditions become favorable for the active growth of particular species. This environmentally-driven emergence of diatom assemblages is analogous to the seasonal succession of phytoplankton assemblages seen in relatively enclosed regions like Chesapeake Bay (Marshall, 1994; Marshall and Nesius, 1996). In the present study area too, it is reasonable to expect that over time, as the hydrographic conditions in the rings change, so too will the planktonic flora and groups of diatom species associated with the rings [c.f. (Cleve, 1897; Johnstone, 1908; Aikawa, 1936)]. This would explain why, after two winters [i.e. two periods of winter convection; see (Chiang and Taniguchi, 1993)] in the Polar Frontal Zone, the diatoms in the warm core ring reverted to the Background Assemblage, and it also accounts for the emergence of The Stratified Assemblage (the assemblage with the largest standing stock) around the nutricline at Sts C29 and C32 (Figure 6), i.e. in locations where the growth of diatoms would have been enhanced. The Background Assemblage meanwhile persists both above and below the Stratified Assemblage, probably because of limited nutrients in the surface layers (see Figures 2C and 2D) (Marra et al., 1990; Chiang et al., 1997) and limited light in the euphotic layer which is 20–40 m in spring or 60 m in summer and autumn [in the sea area east of Hokkaido; (Taniguchi and Kawamura 1972)] in the deeper waters. The Warm Streamer Assemblage was found in sub-surface waters at St. C28 in the up-stream of the warm streamer (Cluster C, Figure 5B). However, in the 2070


Station C27

C28

C29

C30 C31 C32

C33

0 Surface water (B) ws(D)

Depth (m)

Mixed water(C) 50 Mid-layer water (A)

100

150

Background Assemblage

Stritified Assemblage

Cold Streamer Assemblage

Warm Streamer Assemblage

D: Warm Streamer Water Fig. 6. Distribution of the four water types and the four diatom assemblages.

down-stream of the same streamer (St. C33, 0–60 m), a high density (105 cells l–1) Background Assemblage was found (Figures 5B and 6). Population density was three times higher in the down-stream than in the up-stream (t-test, P > 0.05; Figure 2E), and the populations of some species, such as C.radicans and T.nordenskioeldi, increased by 1–2 orders of magnitude (Figures 2G and 2H). Changes in grazing pressure could not easily account for this increase because a contemporaneous study (Tsuda, 1992) found that copepod biomass, a reliable index of grazing pressure, was similar at both sites. Alternatively, to apply an argument used previously by Chiang et al. (Chiang et al., 1997, 1999) in their interpretation of similar data from the East China Sea, the high nitrate and dissolved silica concentrations in the up-stream and the low concentrations in the down-stream 2071


(Figures 2C and 2D) suggest that the change from the Warm Streamer Assemblage into the Background Assemblage might have been driven by a depletion of nutrients in the warm streamer as it flowed around the north of the warm core ring. Oyashio Water is reported to mix into the intermediate water in this area (Kono, 1996), and we interpret the Cold Streamer Assemblage in sub-surface waters at St. C29 (Figure 6) to indicate the presence of advected subarctic Oyashio Water. However, despite the presence of a low-temperature (