Journal of Plankton Research Vol.22 no.7 pp.1221–1235, 2000
Size and species-specific primary productivity and community
structure of phytoplankton in Tokyo Bay
Myung-Soo Han and Ken Furuya1
Department of Life Science, College of Natural Sciences, Hanyang University,
Seoul 133–791, Korea and 1Department of Aquatic Bioscience, Graduate School
of Agricultural and Life Sciences, University of Tokyo, Yayoi, Bunkyo, Tokyo
113-8657, Japan
Abstract. Combined methods of size fractionation and single-cell isolation were used to investigate
the seasonal variation of phytoplankton dynamics in Tokyo Bay with an emphasis on primary productivity. Red tides occurred in Tokyo Bay from spring to autumn; a diatom, Skeletonema costatum, and
a raphidophycean, Heterosigma akashiwo, were the most important primary producers. Small diatoms
and flagellates, including these species, were dominant and showed rapid changes of phytoplankton
community structure within several days in summer. The nanoplankton (3–20 µm) fraction
contributed most to chlorophyll a concentration and primary productivity during spring to autumn,
whereas the microplankton (>20 µm) contribution was remarkable in winter. Picoplankton (<3 µm
phytoplankton) remained relatively constant throughout the year. A significant reverse relationship
was obtained between assimilation rate and chlorophyll a content for the total and nanoplankton
population; the assimilation rate was high at the initial phase of the bloom, then decreased to a
minimum level at the peak of the bloom. Factors controlling the reduction of assimilation rates at the
peak, and changes in phytoplankton community structure, are discussed.
Introduction
Classification of plankton by size has received much attention because of the
potential influence of cell size on the response of phytoplankton populations to
their environment, and the fluxes of energy and material through the food web
in both coastal and oceanic waters (Malone, 1980; Sournia, 1982; Furuya and
Marumo, 1983; Elser et al., 1986; Kurupartkina, 1991; Joint et al., 1993;
Piontkovski et al., 1995). Size differences in phytoplankton in response to light
and nutrient availability may reflect photosynthetic characteristics on a seasonal
scale, since photosynthetic rates have been found to vary with size (Taguchi, 1976;
Prezelin et al., 1987; Frenette et al., 1996). Therefore, size distribution of phytoplankton is important for evaluating the effects of environmental conditions on
their growth and metabolic activity. However, the interpretation of experimental
data from size-fractionated phytoplankton was occasionally ambiguous because
of the variability in dependence of eco-physiological activities in size and species.
In recent years, many attempts have been made to evaluate cellular and speciesspecific properties (Rivkin and Seliger, 1981; Carpenter and Chang, 1988; Furuya
and Li, 1992; Han et al., 1992). Combined use of two or more techniques allows
robust data interpretation in order to understand the food web dynamics within
ecosystems.
The present paper aims to show seasonal changes in phytoplankton based on
their size and its effects on primary productivity and species-specific productivity
of dominant species in Tokyo Bay. The Bay is semi-enclosed with a narrow central
part (6 km wide) restricting the exchange of the bay water. Heavy eutrophication
© Oxford University Press 2000
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M.-S.Han and K.Furuya
Fig. 1. Sampling location in the innermost part of Tokyo Bay. Samples were collected at dawn
between 0 and 0.5 m depth.
has accelerated in the inner part since the 1960s. Frequently-occurring red tides
are formed by single or multi-species (Marumo and Murano, 1973; Han et al.,
1992). In July 1979, the major carbon spectra in phytoplankton occurred in larger
classes (8–64 µm) (Furuya and Marumo, 1983), which included Skeletonema
coastatum, Prorocentrum minimum and Dactyliosolen fragilissimus, in the central
part of Tokyo Bay (Nomura and Yoshida, 1997). Recent studies on dynamics of
particulate organic matter in Tokyo Bay further confirmed these results
(Matsukawa and Sasaki, 1990; Yamaguchi et al., 1991; Yu et al., 1995; Ogawa and
Ogura, 1997). However, little is known about the contribution of size classes
and species to primary productivity.
Method
Field investigation was carried out at Harumi Pier in the innermost part of Tokyo
Bay from May 1986 to June 1987. Water samples were taken once or twice a week
between May and October 1986, and between May and June 1987 (Figure 1).
Sampling from November 1986 to April 1987 was bi-weekly or monthly. Samples
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Size and species-specific primary productivity
were collected with a PVC Van Dorn water sampler at dawn between 0 m and
0.5 m depth where phytoplankton were most abundant (Han, unpublished data).
Plankton whose sizes were larger than 300 µm were gently removed by reverse
filtration. To facilitate the subsequent isolation procedure, cells smaller than
20 µm were reduced by reverse filtration through a 20 µm mesh net. Cells larger
than the 20 µm fraction were incubated in a Teflon-coated BOD bottle (250 ml)
for 1–3 h with 7.4 MBq NaH14CO3 (NEN, NEC-086H10) at simulated in situ
temperature. Cells were irradiated with 300–355 µmol m–2 s–1 of photosynthetically available radiation (PAR) (Biospherical, QSL-100), a saturation intensity
determined by the photosynthesis irradiance (P-I) curve, and thus, the photosynthetic rates represent photosynthetic capacity. Following incubation, individual cells or chains of S.costatum and of other dominant species were randomly
picked out under a dissecting microscope at a magnification of 100 and transferred to scintillation vials. A constant light intensity of 300–355 µmol m–2 s–1 was
maintained from the beginning of incubation to the single cell isolation using the
dissecting microscope. Samples of isolated cells were then acidified with 20–100
µl of 0.5 N HCl overnight to purge inorganic 14C, and the activity was counted in
Aquasol II by a liquid scintillation counter (LKB Wallack Rackbeta 1215).
Quench correction was made by the external standard channel ratio method.
Carbon uptake for each species was calculated by a regression analysis of activity against number of cells (Figure 2). The regression was statistically significant
throughout the study (r > 0.99). Species-specific photosynthetic rate (SSP) for
each species was determined using the slope of this regression line. Primary
productivity was calculated from SSP and the numerical abundance in the mixed
population. Preliminary investigation showed that when 14C-labeled cells were
rinsed with 14C-free medium, there was occasional loss of activity, mostly from
fragile forms, probably due to the leakage of assimilated carbon caused by
mechanical damage. Therefore, the rinsing procedure described in the original
method (Rivkin and Seliger, 1981) was excluded in the present study. Instead, for
the correction of possible contamination by labeled dissolved compounds and
invisible small organisms in the selected populations, labeled medium without
target cells was randomly selected and analyzed serially in vials in the same
manner. In fact, no significant activity was detected above background in blank
vials (20–30 d.p.m.), and a good linear relationship was obtained between the
corrected carbon uptake and number of cells (Figure 2).
Primary productivity was determined by the light and dark bottle method in
250 ml Teflon-coated bottles with NaH14CO3 at 370 kBq. After 1–2 h of incubation under the conditions described above, the phytoplankton samples were
fractionated by sequentially passing through a Nytal screen with a mesh size of
20 µm and a Nuclepore filter with a pore size of 3 µm. Fractionated phytoplankton
(<3 µm, 3–20 µm and >20 µm) was harvested on Whatman GF/F filters under a
vacuum pressure of <250 mmHg, and transferred to scintillation vials. After addition of 0.5 N HCl to purge inorganic 14C, activity was counted as described above.
The fractionated samples were harvested on Whatman GF/F filters and chlorophyll a was determined after extraction in 90% acetone (Sato et al., 1981). Salinity was measured with a salinometer (Guildline, Autosal 8400A). Phosphate,
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M.-S.Han and K.Furuya
Fig. 2. Examples of 14C uptake as a function of the number of isolated cells per scintillation vial.
nitrate, nitrite and ammonium were analyzed with an AutoAnalyzer AA-II
(Technicon) following the method of Parsons et al. (Parsons et al., 1984). Total
inorganic carbon in sea water was determined by carbonate alkalinity (Parsons et
al., 1984) and used for calculation of carbon uptake. Phytoplankton samples were
preserved in 250 ml plastic bottles with 2% glutaraldehyde. The fixed samples
were concentrated by settling, and species identification and cell counting were
performed using a Nikon Nomarsky microscope at 500 to 1000 magnification.
Also, live samples were used for identification of fragile phytoplankton.
Results
Physico-chemical properties
Figure 3 depicts variation in temperature, salinity, nitrate, nitrite, ammonium and
phosphate during May 1986 and July 1987. Water temperature varied from 9.4 (8
January 1987) to 26.4°C (1 September 1986). Salinity changed remarkably from
1224
Size and species-specific primary productivity
Fig. 3. Seasonal variations in temperature (open circles), salinity (closed triangles) and inorganic
nutrients salts: nitrate (closed circles), ammonia (open triangles), nitrite (open squares) and phosphate (closed squares) in the innermost part of Tokyo Bay.
1225
M.-S.Han and K.Furuya
Fig. 4. Variation in the abundance (cells ml–1) of dominant species of phytoplankton in the innermost
Tokyo Bay.
6.6 to 23.2 during summer. However, it was relatively stable during winter
(23.7–29.3). Ambient nutrient values showed wide variations in nitrate, nitrite,
ammonium and phosphate concentration, fluctuating from 22.2 to 118.0, 4.4 to
21.0, 82.6 to 328.0 and 2.8 to 12.4 µM l–1, respectively. The ratio of dissolved inorganic nitrogen to phosphate was much higher than Redfield’s ratio of 16.
Species composition
Dominant species, which contribute more than 10% to the annual cumulative
total cell numbers, are shown in Figure 4. The phytoplankton assemblage was
composed of 13 dominant taxa and was characterized by small chain-forming
1226
Size and species-specific primary productivity
Table I. Changes in dominant species in the innermost part of Tokyo Bay during 28 July to
1 September, 1986
Date (1986)
Dominant species
28
1
6
9
12
15
20
25
29
1
Skeletonema costatum, Dunaliella sp. and coccolithophorid
Skeletonema costatum, Heterosigma akashiwo, Dunaliella sp. and coccolithophorid
Skeletonema costatum, Navicula spp.
Skeletonema costatum
Skeletonema costatum and coccolithophorid
Skeletonema costatum and Eutreptiella sp.
Skeletonema costatum and coccolithophorid
Skeletonema costatum
Thalasiossira binata and Heterosigma akashiwo
Skeletonema costatum and Thalasiossira binata
July
August
August
August
August
August
August
August
August
September
diatoms, unarmored dinoflagellates and other flagellates. The seasonal species
succession progressed as follows: Heterosigma akashiwo, Skeletonema costatum,
Cryptomonas/Chroomonas spp. and Hemiselmis sp. (late spring); S.costatum,
Navicula sp. and Pyraminonas grossii (early summer): S.costatum, Thalassiosira
binata, Navicula spp., H.akashiwo, Dunaliella sp., Eutreptiella sp. and a coccolithophorid sp. (late summer); S.costatum, T.binata and Plagioselmis sp. (autumn);
S.costatum (winter–early spring). Interestingly, S.costatum occurred consistently
during summer and was abundant throughout the seasonal changes, while rapid
succession of other species was noted from spring to autumn, especially in late
summer (Table I). S.costatum was totally absent in winter.
Chlorophyll a and primary productivity
Chlorophyll a content varied between 20 and 638 µg l–1, except in winter when
the concentration remained at around 1–5 µg l–1 (Figure 5). The nanoplankton
fraction contributed most to chlorophyll a among the three size fractions from
summer to autumn 1986 and in spring 1987. The microplankton fraction
contributed largely to total chlorophyll a in summer (10 June, 8 July, 22 July and
11 September), due to the abundance of chain-forming diatoms such as S.costatum and T.binata. On the other hand, the microplankton fraction including
species such as Coscinodiscus granii and Heterocapsa triquetra showed high
chlorophyll a content in winter. In this fraction, chain-forming diatoms such as
Chaetoceros spp. and Pseudonitzschia pungens were numerically unimportant.
The picoplankton fraction remained low throughout the year and did not
contribute significantly to total chlorophyll a content.
Primary productivity varied considerably from 3.9 (8 June 1987) to 991.3 µgC
1–1 h–1 (8 May 1987) (Figure 6). The nanoplankton and microplankton fractions
showed high productivity during the spring–autumn period and winter, respectively. Primary productivity of picoplankton remained low throughout the year,
except in May 1987. These seasonal trends were similar to those observed for
chlorophyll a content.
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M.-S.Han and K.Furuya
Fig. 5. Chlorophyll a content and relative contribution (%) of different size-fractionated phytoplankton in the innermost part of Tokyo Bay.
Fig. 6. Primary productivity and contribution (%) of different size-fractionated phytoplankton in the
innermost part of Tokyo Bay.
Relative abundance and species-specific primary productivity
Figure 7 compares relative abundance and primary productivity of dominant
species with the total population. S.costatum was the most abundant species,
accounting for 28–98% of total cell numbers, and made a consistently major
1228
Size and species-specific primary productivity
1229
Fig. 7. Comparison of relative abundance and species-specific primary productivity of dominant species to the total phytoplankton in the innermost part of
Tokyo Bay.
M.-S.Han and K.Furuya
Table II. One-way ANOVA analysis of the assimilation rates of total and size-fractionated
phytoplankton in different seasons in Tokyo Bay
Period
Mean assimilation rates (µgC µgChl a–1 h–1 )
———————————————————–
Total
>20 µm
3–20 µm
<3 µm
Summer (3 June–29 September 1986)
Spring and autumn (14–28 May; 6–27 October 1986;
24 April–1 June 1987)
Winter (7 November 1986–10 February 1987)
F0.05[2,35] = 3.28
Fs
5.72
8.24
5.77
3.83
3.41
3.94
6.86
4.26
2.99
3.50
4.97
7.18
7.52
0.63
5.91
2.49
contribution to total primary productivity. However, its contribution to primary
productivity was relatively lower compared with numerical abundance. Although
this species accounted for >90% of numerical abundance, productivity accounted
for only <40% of the total in June 1986. In contrast, relative productivity in the
total population of T.binata, Dunaliella sp., Eutreptiella sp. and coccolithophorids
was similar to relative numerical abundance in summer. Percentage productivity
of H.akashiwo was high in spite of minor numerical abundance, and total primary
productivity was ascribed exclusively to this species in May 1987. In winter, the
contribution of S.costatum, as well as C.granii, Chaetoceros affine and H.triquetra, was important for their numerical abundance.
Assimilation rate
Assimilation rates fluctuated widely by a factor of 20–70 in the three different
fractions (Table II). Among the three fractions, the assimilation rate was highest
in the microplankton and fluctuated from 0.6 µgC µgChl a–1 h–1 (July 1987) to
22.8 µgC µgChl a–1 h–1 (October 1986), except in July 1987 when it was abnormally high (40.4 µgC µgChl a–1 h–1). Assimilation rates of nanoplankton and
picoplankton varied from 0.5 (February 1987) to 11.6 µgC µgChl a–1 h–1 (September 1986), and from 0.2 (May 1987) to 13.4 µgC µgChl a–1 h–1 (January 1987),
respectively.
Although the assimilation rate of the total and nanoplankton fraction was
consistently more stable than that of the microplankton on a seasonal scale, it
showed considerable variations on short time scales (Figure 8). The temporal
phase of chlorophyll a values and assimilation rates was inversely correlated in
both total and nanoplankton. There was a reverse relationship between fractionated chlorophyll a values and assimilation rate, as mentioned above. The assimilation rate showed an increase when fractionated chlorophyll a content decreased
to a minimum. On the other hand, assimilation rates tended to be low around the
period showing the maximum content of chlorophyll a in the total and nanoplankton fraction. As the bloom progressed towards its peak, the assimilation rate
decreased from a factor of 7 to 23.
One-way ANOVA was carried out to determine whether the mean values of
the assimilation rates of each population were dependent on season (Table II).
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Size and species-specific primary productivity
Fig. 8. Seasonal fluctuation in assimilation rate and size-fractionated chlorophyll a content in total
phytoplankton and nanoplankton in the innermost part of Tokyo Bay.
The assimilation rates of total phytoplankton and nanoplankton revealed a
seasonal dependence; the summer population (3 June to 29 September 1986)
exhibited a significantly higher assimilation rate than the spring and autumn
population (14–28 May, 6–27 October 1986 and 24 April–1 June 1987), and the
winter population (7 November 1986–10 February 1987). However, the assimilation rates of the microplankton and picoplankton did not differ significantly
between seasons.
Discussion
It is well established that micro-, pico- and nanoplankton contribute significantly
to biomass and primary productivity in many parts of the coastal and oceanic
waters. Exceptions to this general pattern have been observed in shallow, temperate estuaries and adjacent coastal waters influenced by estuarine run-off
(Malone, 1980). The present study demonstrated the importance of the nano- and
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M.-S.Han and K.Furuya
microplankton fraction in primary productivity of the estuaries. Several
nanoplanktonic species, such as H.akashiwo, S.costatum, T.binata, Dunaliella sp.,
Eutreptiella sp. and coccolithophorids, accounted for a major portion of annual
primary productivity in Tokyo Bay.
Nanoplanktonic species were clearly abundant in summer in Tokyo Bay.
Previous reports (Han et al., 1992) revealed the high species-specific productivity
(SSP) of nanoplankton such as S.costatum, H.akashiwo and T.binata in Tokyo
Bay. In particular, volume-specific SSP of H.akashiwo was higher than any other
species, and its ratio of carbon to chlorophyll a content (C:Chl a) was lower. The
lower C:Chl a ratio might contribute to a higher growth rate of phytoplankton
(Furuya et al., 1986). Similarly, nanoplankton exhibited a significantly higher
assimilation rate in summer than in spring and autumn (Table II). The physiological advantages of nanoplanktonic species in terms of volume-specific SSP,
lower C:Chl a ratio and higher assimilation rate seem to accord well with the
dominance of small species in summer. However, the assimilation rate of the
nanoplankton fraction was lower than that of the total or microplankton fraction. It is important to remember that although the assimilation rate is related
to photosynthetic capacity, there is no direct relationship between assimilation
rate and growth rate. Physiological advantages in terms of photosynthetic capacity cannot fully explain the dominance of nanoplankton in summer. Although
there are limited published data on grazing in Tokyo Bay, the impact of
zooplankton grazing appears to be an important factor for the dominance of
nanoplankton. Hiromi estimated the potential zooplankton grazing rate in
summer by the laboratory-oriented budgetary method and found that Oithona
davisae can compete with microzooplankton for phytoplankton, and that
primary production is heavily depressed by the grazing pressure (Hiromi, 1996).
Oithona davisae prefers large particles over 20 µm in Tokyo Bay throughout the
year (Tsuda and Nemoto, 1988). Malone and Chervin also found grazing to be
an important factor in the New York Bight in summer (Malone and Chervin,
1979).
A supply of nutrient salts was not a limiting factor as their concentrations were
consistently at saturation throughout the year. However, N/P ratios higher than
Redfield’s ratio of 16 throughout the year suggest that P supply could be limiting
for phytoplankton growth under heavy bloom conditions. Depletion of nutrient
salts in surface water during phytoplankton blooms in eutrophicated estuaries
followed by a large freshwater supply may permit species succession (Malone,
1980; Han et al., 1994). Therefore, changes in the structure and abundance of the
phytoplankton community could be interpreted as a time-dependant response of
nutrient dynamics in a resident water column (Tsunogai and Watanabe, 1983;
Han et al., 1994). However, our results showed that nutrients are rarely depleted
even in summer when the phytoplankton blooms in Tokyo Bay, as reported by
Yu et al. (Yu et al., 1995). Why were nutrient salts rarely depleted even in the
surface layer in summer? One possible explanation could be that nitrogen and
phosphate were regenerated rigorously from the anaerobic bottom water in
summer and in the bottom sediment itself throughout the year (Matsukawa and
Sasaki, 1990; Yu, et al., 1995). Even during the summer stratification period, the
1232
Size and species-specific primary productivity
regenerated nutrients are occasionally advected upwards by wind-induced water
mixing near the coast (Miyata and Hattori, 1986). Another explanation could be
a relatively constant supply from the land.
Table I and figure 4 showed that there were two distinct communities assemblage 1 (H.akashiwo, Cryptomonas/Chroomonas spp., Dunaliella spp., a coccolithophorid sp. and Eutreptiella sp.) and assemblage 2 (T.binata, Plagioselmis spp.
and Hemiselmis spp.), in August to September 1986. Alterations in the two assemblages could be attributed to advection of the populations in and out of the study
site. These assemblages were frequently observed as mosaics around the study
site (data not shown). The subsequent higher biomass of assemblage 2 may not
be due to in situ growth but rather, to advection of the center of a patch of assemblage 2 into the sampling site in summer. In fact, T.binata and Hemiselmis spp.
were sometimes dominant outside the sampling site (Han, 1988). Although our
results do not provide direct evidence, it is suggested that the advective process
could drive the changes in species composition at the study site.
Although S.costatum and H.akashiwo were the most abundant species, their
contribution to total primary production differed. Species-specific productivity of
H.akashiwo was high despite its low abundance, while S.costatum made a minor
contribution to the total considering its numerical predominance (Figure 7). The
difference can be explained by the fact that chlorophyll a content per unit cell
volume was high in small diatoms and flagellates compared with large species
(Han et al, 1992). The chlorophyll a content per unit cell volume in H.akashiwo
was higher than that of S.costatum.
A reverse relationship was found between assimilation rate and phytoplankton
abundance in the total and nanoplankton fractions (Figure 8). The assimilation
rate was often high when abundance was low; it then decreased gradually along
with increasing abundance, and reached a minimum at the peak of the bloom.
This phenomenon was also observed in species-specific productivity of S.costatum in this bay (Han et al., 1992). Using a flow cytometer, Furuya and Li (Furuya
and Li, 1992) showed the same pattern in temporal variations of the fluorescence
response index (FRI); a high FRI was associated with the early phase and the FRI
tended to decrease as the bloom progressed toward the peak. Guasch and Sabater
(Guasch and Sabater, 1995) also found a significant negative correlation between
biomass and biomass-specific photosynthetic activity. Although there is no clear
explanation for the change in photosynthetic activity, self-shading due to dense
accumulation of biomass is a possible factor. Various phytoplankton species are
known to increase the amount of light-harvesting pigments per photosystem in
response to low growth irradiation (Halldal, 1970). This may lead to a decreased
assimilation rate even when cellular photosynthetic activity remains constant.
Further study is needed to examine this hypothesis.
In conclusion, nano- and microplanktonic species were major primary producers in the inner part of Tokyo Bay in summer and winter, respectively. The high
productivity of nanoplanktonic species, and high fraction to total primary productivity, resulted from higher chlorophyll a content per unit cell volume. Both high
photosynthetic capacity and, possibly, low grazing pressure are likely important
factors regulating the dominance of nanoplankton fraction during summer.
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M.-S.Han and K.Furuya
Acknowledgements
We are grateful for valuable suggestions and comments by the late Prof.
T.Nemoto. We are also thankful to Prof. M.Terazaki for his kind co-operation in
14C experiments and to Mr D.-S.Yi for the drawing of pictures. Comments of Drs
B.Asrlow, N.Ramaiah and U.Namgung improved the manuscript.
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Received on April 4, 1999; accepted on October 21, 1999
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