Journal of Plankton Research Vol.22 no.2 pp.363–380, 2000
Effects of diffusion and upwelling on the formation of red tides
Tamiji Yamamoto and Mitsuru Okai
Faculty of Applied Biological Science, Hiroshima University, Higashi-Hiroshima
739-8528, Japan
Abstract. In this paper, records on the timing and location of specific red tides monitored once or
twice a week in Mikawa Bay, Japan, are related to horizontal and vertical mixing rates determined
from a numerical model. Horizontal (Kh) and vertical (Kz) diffusion coefficients, and upwelling velocities, were estimated using a box model analysis. In the wind-mixed period and in the upper layer
during the stratified period, Kh was estimated to be of the order of 102 m2 s–1. During the stratified
period, Kz was estimated to be of the order of 10–5 m2 s–1. The upwelling velocity was calculated to
be in the range 0.35–5.1 m day–1 with an average of 1.5 m day–1. Comparison between the literature
values of the specific growth rate (µ) of the red tide-forming diatoms and calculated Kh values during
the red tides show that diatoms which have a low µ cannot form red tides in a strongly diffusive
environment, while species having a high µ can form red tides even in a strong diffusive environment.
On the other hand, no clear relationship was found between µ of the flagellate group and Kh, although
the flagellate group formed red tides even in severe diffusive conditions. From the comparison
between the literature values of sinking rate and swimming speed and the physical parameters associated with vertical processes, it was concluded that flagellates will form red tides, even in severe
diffusive conditions, by using their swimming ability, while diatoms form red tides by their high growth
rates with the aid of vertical diffusion and the upwelling movement of water.
Introduction
Spatial and temporal distribution of phytoplankton is fundamentally governed by
the movement of water, because they are lacking in mobility or have only weak
mobility. In other words, turbulence of the water greatly affects the distribution
of phytoplankton (Margalef, 1978). This leads to the concept that the formation
of phytoplankton patches depends on the balance between phytoplankton
growth rate and diffusion of the water (Okubo, 1982).
In shallow coastal areas including embayments and estuaries, dispersion of
material is considered to be two-dimensional for x–y axes due to the existence of
the sea floor, while in the open ocean it is three-dimensional (Yamamoto, 1992).
Therefore, horizontal diffusion would be the most important physical process
influencing the formation of red tides in shallow seas. Vertical diffusion also influences the vertical distribution of phytoplankton, along with the vertical movement of water such as upwelling and downwelling. Since it is necessary for
phytoplankters to reside in the euphotic zone to carry on photosynthesis, vertical water movement would play a significant role for diatoms which are susceptible to water movement, while some flagellates may vertically migrate in weak
upwelling or downwelling conditions.
Mikawa Bay, a part of Ise Bay, is a semi-enclosed estuary located in mid Japan,
and has a surface area of 604 km2 and an average depth of 9.2 m. Two major rivers,
the Yahagi and Toyo Rivers, empty into the bay from the northwest and the
northeast, respectively. While both inorganic and organic loadings from these
rivers have made Mikawa Bay a rich fishery area, high economic growth during
the last two decades has caused it to be one of the most eutrophicated bays in
© Oxford University Press 2000
363
T.Yamamoto and M.Okai
Japan. For example, the occurrence of red tides in Mikawa Bay has been chronic;
the number of blooms monitored sometimes exceeds 365 per year, which means
red tides of different species are observed at different sites on certain days
(Yamamoto et al., 1997).
To understand the mechanisms of the formation of red tides from the field data,
we need sufficient data on the surrounding environments as well as records on
red tides. In Mikawa Bay, administratively-guided monitoring of red tides has
been conducted on a one or twice weekly basis. Routine monitoring of environmental parameters has also been carried out monthly for the last two decades. In
the present study, we relate the literature values of growth rates, sinking velocities and swimming speeds of red tide-forming phytoplankton to the calculated
values of the horizontal and vertical diffusion coefficients and upwelling velocities for local segments of Mikawa Bay, and reveal the characteristic ecological
differences between diatoms and dinoflagellates.
Method
Box model analysis
Mikawa Bay was divided into eight boxes according to the configuration of the
coastline and the depth (Figure 1). Judging from the vertical density structure in
Boxes 3 and 6 (Figure 2), a two-layer model divided at 6 m depth (pycnocline)
was applied for the stratified period of May through October, and a one-layer
model was applied for the wind-mixed period of November through April.
Temperature and salinity data were obtained from the Report on the Water
Quality of the Areas for Public Use (Department of Environmental Science, Aichi
Prefecture, 1990, 1991, 1992). For Boxes 1, 2 and 8, the one-layer model was
applied all year because the average depth of these boxes was lower than 6 m.
The dimensions of the boxes are summarized in Table I.
In the box model, water exchange was fundamentally expressed as a combination of advection and diffusion. We also took the estuarine circulation driven
by river discharge into account. The two major rivers (the Yahagi and the Toyo
Rivers) empty into Boxes 2 and 8, contributing 73% to the total river discharge
(Saijo, 1984). We assume that this inflow is creating strong upwelling only at the
junction of the bay and the river, not the entire bay, because the Mikawa Bay has
a broader area at the junction, unlike Chesapeake Bay. As we took only one layer
for Boxes 2 and 8 because of their shallowness, upwelling was put in Boxes 3 and
7. In the present study, the magnitude of the estuarine circulation was determined
from the relationship between the riverine inflow and observed current velocity
in the lower layer (Suzuki and Matsukawa, 1987; Matsukawa 1989). Monthly
freshwater discharge data from the two major rivers were taken from the Annual
Report on the Major River Discharge in Japan (Japan River Association, 1991,
1992, 1993). Data for minor rivers were recalculated from the Report on the Water
Quality of the Areas for Public Use (Department of Environmental Science, Aichi
Prefecture, 1990, 1991, 1992).
The budget of water in the upper layer (subscript 1) during the stratified period
364
Effects of advection and upwelling on red tides
Fig. 1. Map showing the location of Mikawa Bay, and a horizontal view of the box arrangement with
sampling stations. Discharge sites of the main rivers are also indicated with arrows.
was determined as follows. As an example the balance of water in Boxes 6–8 is
shown in Figure 3a for the mixed period and Figure 3b for the stratified period.
Ai1Ui1 = (Qr + Qp – Qe) + Aj1Uj1 + Ai0Wi0, (j = i + 1)
(1)
where Ai1, Aj1 are areas of the interfaces between two neighboring boxes (m2),
Ai0 is area of the interface between the upper layer and the lower layer (m2), Qr,
365
Fig. 2. Seasonal changes in vertical profiles of temperature, salinity and sigma-t in Box 3 and 6.
T.Yamamoto and M.Okai
366
Effects of advection and upwelling on red tides
Table I. Dimensions of boxes in Mikawa Bay used in the box model analysis. Surface area (As), mean
depth (D), and volume (V) of each box, and the distance between two neighboring boxes (L) and areas
of the downstream cross-section (A). The first subscript denotes the box number or the downstream
cross-section and the second subscript denotes the layer (1 denotes the upper layer and 2 the lower)
Box
Ais
(3107 m2)
Di
(m)
Vi1
Vi2
–––––––––––––––––––
(3108 m3)
Li
(3103 m)
Ai1
(3104 m2)
1
2
3
4
5
6
7
8
2.30
3.90
4.00
8.85
10.45
9.10
6.60
5.70
8.9
7.1
9.2
15.0
12.8
11.4
9.3
6.3
2.05
2.78
2.40
5.31
6.27
5.46
3.96
3.61
5.83
5.00
8.25
6.00
7.62
6.32
6.18
6.18
3.96
9.32
5.40
6.00
7.25
9.00
5.40
9.05
1.28
7.94
7.14
4.87
2.15
Ai2
2.90
12.60
9.57
10.10
4.52
Fig. 3. A schematic diagram of freshwater and salt balance in the box model. (a) A one-layer model
for the mixed period and (b) a two-layer model for the stratified period. Q: the freshwater inflow
through the box surface (river, precipitation and evaporation). V: the volume of the box. S: salinity
in the box. U and W: horizontal and vertical flows due to advection. Kh and Kz: the horizontal and
vertical diffusion coefficients. A: the area of the interface. The first subscript denotes the box no. or
the cross-section no. The second subscript denotes the layer no. or interface no. The drawing is an
example for the Box 6–8 in the innermost of the eastern part of Mikawa Bay.
367
T.Yamamoto and M.Okai
Qp, Qe are freshwater input by the river, precipitation and evaporation to the
surface of the box (m3 s–1), Ui1, Uj1 are horizontal current velocity across the interface between two neighboring boxes (m s–1) and Wi0 is upwelling velocity across
the interface between the upper layer and the lower layer (m s–1).
As well as rainfall data, wind speed and humidity data used for the estimation
of surface evaporation were obtained from the Irago Meteorological Station
which is located at the tip of Atsumi Peninsula (Japan Weather Association, 1989,
1990, 1991). Then, Ui1 was obtained from equation (1).
The salt exchange in the upper layer (subscript 1) and lower layer (subscript 2)
during the stratified period was balanced using the following equations, respectively:
Vi1(∂Si1/∂t) = Aj1{Uj1Sj1 – Khj1(∂S/∂x)j1} –
Ai1{Ui1Si1 – Khi1(∂S/∂x)i1} + Ai0{Wi0Si2 – Kzi(∂S/∂z)i}
(2–1)
Vi2(∂Si2/∂t) = Ai2{Ui2Si2 – Khi2(∂S/∂x)i2} –
Aj2{Uj2Sj2 – Khj2(∂S/∂x)j2} – Ai0{Wi0Si2 – Kzi(∂S/∂z)i}
(2–2)
where, Vi1, Vi2 are volumes of the upper and lower boxes, respectively (m3), Si1,
Si2 are salinity in the upper and lower boxes, respectively (p.s.u.), Khi1, Khi2 are
horizontal diffusion coefficients between the neighboring boxes in the upper and
lower layers, respectively (m2 s–1), Kzi is vertical diffusion coefficient between the
upper and lower boxes (m2 s–1), x is the horizontal distance between the two
neighboring boxes (m), z is the vertical distance between the centers upper layer
and the lower layer (m) and t is time (s).
Incorporating the array of equations for all boxes into the computer program,
horizontal and vertical diffusion coefficients (Khi, Khj and Kzi) were determined
by iteration, changing Kh from 1.0 3 100 to 1.0 3 104 m2 s–1 and Kz from 1.0 3
10–5 to 1.0 3 10–3 m2 s–1 with an interval of 1.0 in each order for both Kh and Kz,
so that the salinity difference between the calculated and measured values
becomes minimum for all boxes. These calculations were carried out for every
month from April 1989 to December 1991 using the measured value at the central
point in each box (Figure 1) as the initial value. The time step of the computation was 600 s.
Comparison between biological parameters and physical parameters
Biological parameters of the red tide-forming species were related to the physical parameters described above. Red tide data from April 1989 to December 1991
were taken from Records on Red Tide Occurrence in Ise Bay and Mikawa Bay
(Yamamoto et al., 1989, 1991; Yamamoto and Tsuchiya, 1990), which are the
reports of the government-guided systematic monitoring conducted once or twice
a week. In these reports, species name, cell density and the spreading area of all
red tides that occurred in Mikawa Bay were recorded. To match the biological
and physical parameters, red tide records lasting for <5 days were omitted
368
Effects of advection and upwelling on red tides
because the interval of calculation for physical parameters was monthly (Table
II). Furthermore, records of unidentified species were also omitted because their
biological parameters could not be specified.
The formation of patches (red tide) is a function of length scale, as documented
by Okubo (Okubo, 1971). Steele (Steele, 1976) and Denman and Platt (Denman
and Platt, 1976) also showed that the critical size of patches would be 1–2 km,
which means a phytoplankton patch below this scale would never be formed. Our
choice of the length scale in the box model (the distance between the boxes is
5.0–8.25 km; Table I) is appropriate from this point of view.
The literature-cited maximum specific growth rate (µ, [T–1]) of those red tideforming species in Mikawa Bay (Table III) was compared with the physical index
having the same dimension Kh/x2 [T–1]. For the stratified period, the sinking rate
of diatoms (SR, [L T–1]) and the swimming speed of flagellates (SS, [L T–1]) were
also compared with upwelling velocity (Wo, [L T–1]) and Kz/z [L T–1].
Results and Discussion
Physical processes
Estimated horizontal diffusion coefficients (Kh) in the upper layer during the
stratified period were of the order of 102 m2 s–1 except those in Box 1, which were
of the order of 101 m2 s–1 (Figure 4, Table IV). The low Kh in Box 1 is due to the
Table II. List of species which formed red tides for >5 days, and their periods and boxes (parentheses)
observed
Species
Diatoms
Cylindrotheca closterium
Eucampia zodiacus
Leptocylindrus danicus
Rhizosolenia delicatula
Rhizosolenia fragilissima
Skeletonema costatum
Flagellates
Alexandrium tamarense
Ceratium furca
Ceratium fusus
Gymnodinium sanguineum
Prorocentrum minimum
Prorocentrum micans
Ciliate
Mesodinium rubrum
Periods and boxes
1989: 13–18 July (1–3)
1990: 22–28 June (7,8)
1990: 23–30 Jan (1–4)
1990–1991: 15 Dec–5 Feb (1–4), 18 Dec–5 Feb (5–8)
1991: 10–17 Apr (3,4), 20–25 Apr (6–8)
1990: 10–16 Sept (8)
1990: 24–29 Aug (6–8)
1989: 9–11 Oct (8),
1991: 29 July–2 Aug (5–8)
1989: 27 June–20 July (5,6), 8–13 Sept (3,4), 2–9 Oct (1–4)
1990: 13–31 Jan (5–8), 3–14 Feb (8), 20–28 May (5–8),
11–20 June (6–8), 17–25 June (1–3), 11–16 July (1–3),
13–17 July (7,8), 11–20 Aug (1,2), 11–23 Aug (6–8),
22–29 Sept (1–8), 2–8 Oct (1–8)
1991: 1–5 Mar (7,8), 10–17 Apr (3,4), 20–27 June (1),
29 July–2 Aug (5–8), 21–30 Sept (4–8), 5–12 Dec (7,8)
1991: 28 Mar–22 Apr (6–8)
1990: 1–5 July (7,8), 2–7 July (1–4)
1990: 1–5 July (7,8), 2–7 July (1–4)
1990: 15 Oct–11 Dec (4–8), 9–13 Dec (3)
1989: 9 May–7 June (1–4), 12 May-6 June (5–8)
1990: 9–13 Dec (3)
1991: 5–19 Nov (5–7)
369
T.Yamamoto and M.Okai
Table III. Literature cited maximum specific growth rates for the red tide-forming species in Mikawa
Bay, Japan
Species
Maximum
specific growth rate (µ)
References
Diatoms
Cylindrotheca closterium
Leptocylindrus danicus
Rhizosolenia fragilissima
Skeletonema costatum
1.7–2.0
1.2–1.4
1.2
1.6–3.0
Tokuda (1968)
Fred et al. (1986)
Ignatiades and Smayda (1970)
Chan (1978)
Curl and McLeod (1961)
Jitts et al. (1964)
Smayda (1973)
Flagellates
Alexandrium tamarense
0.4
Ceratium furca
Ceratium fusus
Gymnodinium sanguineum
0.4
0.3
0.2–0.4
Prorocentrum minimum
Prorocentrum micans
0.4
0.3–1.4
Yamamoto et al. (1995)
Yamamoto and Tarutani (1997)
Nordli (1957)
Nordli (1957)
Hellebust (1965)
Hochachka and Teal (1964)
Watanabe et al. (1980)
Barker (1935)
Brand and Guillard (1981)
Chan (1978)
Lanskaya (1963)
Moshkina (1961)
Sweeney (1975)
Ciliate
Mesodinium rubrum
0.4–0.7
Montagnes et al. (1989)
breakwater between Box 1 and Box 2. This is also apparent from the large difference in salinity (max. 14.4 p.s.u.) between these boxes. According to the spectral analyses by Matsukawa, who also worked on a box model analysis in the
eastern half of Mikawa Bay, shear dispersion due to density-driven currents,
which has an order of 102 m2 s–1, is overwhelming compared with wind-driven
currents (101 m2 s–1) and tidal currents (100–101 m2 s–1) (Matsukawa, 1989).
Therefore, the surface layer of Mikawa Bay is considered to be largely influenced by density-driven currents forced by freshwater inflow from the Yahagi
and Toyo Rivers.
Kh in the lower layer was estimated to be one order of magnitude smaller
(101 m2 s–1) than in the upper layer (Figure 4, Table IV). In the lower layer, shear
dispersion by tidal currents might predominate. It is logical that the order of
magnitude of estimated Kh in the lower layer is in accordance with the estimate
by Matsukawa (Matsukawa, 1989).
Although the same order of magnitude of Kh was estimated for both the windmixed and stratified periods, during the mixed period higher values (5.8 3
102 m2 s–1 on average) were obtained in the western part of the bay (Boxes 1–4)
compared with those (2.5 3 102 m2 s–1) in the eastern part (Boxes 5–8) (Figure 4,
Table IV). The average wind velocity in winter (5.0 m s–1) is stronger than that in
summer (3.8 m s–1), and the wind direction in winter is from the northwest and
in summer from the southeast (Figure 5). Therefore, it seems that the western
370
Effects of advection and upwelling on red tides
Fig. 4. Estimated horizontal and vertical diffusion coefficients (Kh and Kz) in each box. (a) Kh in the
upper layer (n = 18) and the lower layer (n = 18) in the stratified season (May–Oct). (b) Kh in the
mixed season (Nov–Apr) (n = 14). (c) Kz in the stratified season (n = 18). Error bars show the standard error.
arm of the bay, oriented in the northwest–southeast direction, may be affected
more in winter with northwesterly winds which drag the surface water toward the
mouth of the bay. This might be a major reason why Kh in the western half was
higher in winter than that in the eastern half.
Estimated vertical diffusion coefficients during the stratified period showed no
significant difference among boxes (Boxes 3–7), and the average was 4.5 3
10–5 m2 s–1 (Figure 4c, Table V). This value seems to be reasonable compared with
those values (10–6–10–4 m2 s–1) proposed for a typically stratified layer by Okubo
(Okubo, 1970).
Upwelling velocities of 4.2–59 3 10–6 m s–1 (0.35–5.1 m day–1) with an average
of 17 3 10–6 m s–1 (1.5 m day–1) were estimated for Boxes 3 and 7 (Table V). The
reported average upwelling velocity of neighboring Ise Bay during the stratified
371
T.Yamamoto and M.Okai
Table IV. Estimated horizontal diffusion coefficient (3102 m2 s–1). For the stratified period
(May–Oct), values both in the upper layer (upper line) and the lower layer (lower line) were shown
Cross-section (Ai)
–––––––––––––––––––––––––––––––––––––––––––––––––––––
Date
1
2
3
4
5
6
7
8
April 1989
May 1989
0.3
0.08
ND
0.1
ND
0.2
ND
0.1
ND
4.0
ND
0.7
ND
1.0
0.7
0.3
0.1
0.5
20
ND
ND
0.09
ND
0.1
ND
0.1
ND
0.04
ND
0.4
ND
0.3
2.0
1.0
0.8
ND
0.2
ND
ND
0.2
ND
0.09
ND
0.07
ND
0.1
ND
ND
ND
10
1.0
0.2
ND
0.2
ND
0.5
ND
0.06
ND
2.0
ND
10
ND
10
10
1.0
10
10
ND
0.6
ND
0.6
ND
0.2
ND
2.0
ND
10
ND
4.0
ND
3.0
20
10
10
1.0
10
ND
ND
0.4
ND
ND
ND
0.04
ND
3.0
ND
0.1
ND
0.7
9.0
5.0
0.1
ND
ND
1.0
0.2
10
1.0
10
0.5
20
0.5
8.0
3.0
7.0
2.0
10
ND
1.0
0.1
4.0
5.0
0.5
1.0
3.0
0.1
0.1
0.1
4.0
1.0
3.0
10
10
6.0
10
10
1.0
0.1
1.0
0.1
3.0
0.1
ND
ND
3.0
0.5
5.0
0.1
10
8.0
2.0
0.1
50
0.5
2.0
0.2
2.0
0.1
20
0.5
0.2
0.5
6.0
2.0
10
0.8
1.0
ND
5.0
0.1
5.0
1.0
5.0
1.0
1.0
0.1
ND
ND
0.7
0.5
1.0
10
10
2.0
0.1
10
1.0
0.1
2.0
0.1
0.8
0.1
ND
ND
10
0.5
0.7
0.1
10
2.0
0.1
0.1
10
0.2
1.0
0.3
0.5
0.1
10
0.5
0.1
0.1
0.5
0.4
0.01
2.0
1.0
6.0
10
0.1
0.1
1.0
1.0
1.0
0.5
0.1
0.5
0.1
1.0
0.5
0.7
1.0
0.4
0.1
0.1
10
1.0
0.1
20
0.1
0.5
0.1
ND
ND
5.0
0.5
1.0
0.1
1.0
4.0
0.1
0.1
10
0.2
0.8
0.3
1.0
0.1
10
0.5
0.1
0.1
0.5
0.4
0.04
2.0
0.4
7.0
10
0.1
0.1
1.0
1.0
1.0
0.1
0.1
1.0
0.1
1.0
1.0
0.8
1.0
1.0
5.0
0.1
10
1.0
0.1
20
0.1
ND
ND
0.01
0.1
1.0
0.6
2.0
0.1
1.0
5.0
0.1
0.1
10
0.2
0.3
0.3
ND
ND
30
0.5
0.1
0.1
10
0.5
3.0
10
5.0
10
10
0.1
0.5
5.0
3.0
1.0
0.1
0.1
0.5
1.0
5.0
1.0
0.3
5.0
3.0
1.0
2.0
1.0
1.0
0.1
ND
ND
1.0
0.1
0.5
0.2
5.0
0.6
2.0
0.1
2.0
1.0
0.8
ND
5.0
ND
0.5
ND
0.3
ND
1.5
ND
0.5
ND
0.7
0.2
0.05
2.0
1.0
5.0
2.0
ND
4.0
ND
0.5
ND
1.0
ND
1.0
ND
40
ND
0.1
0.4
4.0
1.0
0.5
10
0.3
ND
0.3
ND
1.0
ND
0.3
ND
5.0
ND
7.0
ND
1.0
June 1989
July 1989
August 1989
September 1989
October 1989
November 1989
December 1989
January 1990
February 1990
March 1990
April 1990
May 1990
June 1990
July 1990
August 1990
September 1990
October 1990
November 1990
December 1990
January 1991
February 1991
March 1991
April 1991
May 1991
June 1991
July 1991
August 1991
September 1991
October 1991
November 1991
372
Effects of advection and upwelling on red tides
Fig. 5. (a) Daily variations of the mean wind velocity and the prevailing wind direction during
1989–1991 which were observed at Irago meteorological observatory located at the tip of the Atsumi
Peninsula. (b) Wind roses for monthly data. Symbol shows the monthly mean wind velocity and the
prevailing direction.
period [6.9 3 10–6 m s–1 (Fujiwara et al., 1996)] is about two times smaller than
those obtained for Mikawa Bay in the present study. This may be attributed to a
smaller vertical salinity difference in Mikawa Bay, due to its shallowness, which
has less resistance to upwelling.
Red tides and horizontal diffusion
The relationship between maximum specific growth rates (µ) of red tide-forming
species and estimated horizontal diffusion coefficients (Kh) during red tide
formation are shown in Figure 6. In the case of the diatom group, a significant
increasing trend in µ with increasing Kh was found (Kendall’s rank correlation
test, P < 0.05). This indicates that species with a low µ could not form red tides
373
T.Yamamoto and M.Okai
Table V. Estimated vertical diffusion coefficient (310–4 m2 s–1) for Boxes 3–7, and estimated
upwelling velocity (310–4 m s–1) for Boxes 3 and 7
Date
Vertical diffusion coefficient box no.
–––––––––––––––––––––––––––––––
3
4
5
6
7
Upwelling velocity box no.
–––––––––––––––––––––––––––
3
7
May 1989
June 1989
July 1989
August 1989
September 1989
October 1989
May 1990
June 1990
July 1990
August 1990
September 1990
October 1990
May 1991
June 1991
July 1991
August 1991
September 1991
October 1991
0.2
ND
0.8
0.4
2.0
0.7
0.3
0.1
0.1
0.1
0.5
0.5
0.1
0.3
0.1
ND
1.0
0.5
0.2
0.4
0.5
ND
1.0
0.1
1.0
0.6
0.5
0.1
1.0
1.0
0.1
ND
0.1
0.2
1.0
0.4
0.09
0.16
0.18
0.09
0.59
0.14
0.14
0.11
0.07
0.06
0.17
0.13
0.05
0.12
0.12
0.10
0.27
0.18
0.1
0.2
0.7
0.1
0.1
0.7
0.2
0.1
0.5
0.1
ND
0.7
0.1
0.1
0.1
ND
1.0
0.6
0.1
0.3
0.1
0.2
0.4
0.1
0.1
0.2
0.1
0.1
3.0
0.2
0.1
0.1
0.1
ND
1.0
2.0
0.1
0.1
0.1
0.1
0.1
0.1
0.2
0.2
0.1
0.1
2.0
0.7
0.1
0.1
ND
0.1
1.0
1.0
0.08
0.23
0.15
0.13
0.55
0.08
0.29
0.16
0.07
0.08
0.37
0.24
0.04
0.18
0.13
0.07
0.32
0.14
in a strong diffusive environment, while species with a high µ could form red tides
even in a strong diffusive environment. A significant difference was also found
between the average µ values of each of two species (t-test, P < 0.05) except for
Leptocylindrus danicus and Rhizosolenia fragilissima. However, the t-test showed
no significant difference among the average Kh values.
The maximum Kh values should be considered instead of the average values
because the question is which species can maintain the population and at what
level of turbulence. The maximum Kh values during the red tides formed by
Skeletonema costatum, Cylindrotheca closterium, L.danicus and R.fragilissima
were 4.0, 0.04, 0.01 and 0.005 3 102 m2 s–1, respectively. These differences in
values seem to have a large effect on the phytoplankton distribution. The large
range of Kh in S.costatum and R.fragilissima indicates that these species form red
tides even in the calm stratified summer season.
On the other hand, no clear relationship was found between the µ of the flagellate group (including one ciliate species, Mesodinium rubrum) and Kh. However,
it should be noted that they formed red tides in almost the same range of Kh
(101–103 m2 s–1), even though they all have low µ.
Kh/x2 was compared with µ. As x is the distance between the two neighboring
boxes (Figure 7), Kh/x2 has the dimension of [T–1], which represents the
exchange rate of water. In this Figure, the dotted line shows the condition where
µ and Kh/x2 balance. If µ is greater than Kh/x2 (upper part of the dotted line), this
means that the species could expand its population due to its faster growth rates.
On the other hand, the species which are located under the lower part of the
dotted line should disappear by turbulence. According to this concept, all
374
Effects of advection and upwelling on red tides
Fig. 6. Comparison between estimated horizontal diffusion coefficient (Kh) and phytoplankton
specific growth rate (µ). (a) Diatoms and (b) flagellates (including a ciliate species, Mesodinium
rubrum). Horizontal bar shows the range of Kh during red tide formed by each species. Vertical bar
shows the range between the reported minimum and maximum values of µ.
diatoms are generally in the former situation, while flagellates are generally in
the latter situation, although there is no way to test this. It is plausible that since
diatoms can increase their population against dispersion fate, they can form red
tides. However, for flagellates, factors other than µ may cause the formation of
red tides in such diffusive environments.
One possible explanation is the motility of flagellates compared with nonmotile diatoms. White reported that a moderate swirling action made the dinoflagellate, Alexandrium tamarense, aggregate in the center of the flask (White,
1976). On the other hand, there are many references relating to shaking or agitation (Tuttle and Loeblich, 1975; Galleron, 1976; White, 1976; Berdalet and
Estrada, 1993; Gibson and Thomas, 1995). These results suggest that a turbulent
condition is not preferable for the growth of flagellates (Thomas and Gibson,
1990). According to this behavior of flagellates observed in the laboratory, it is
plausible that flagellates might swim down possibly to the benthic boundary layer
to avoid the strong turbulent condition at the surface. Thus, flagellate blooms can
come and go fairly rapidly in shallow coastal areas, depending on the degree of
375
T.Yamamoto and M.Okai
Fig. 7. Comparison between water exchange rate (Kh/x2) and phytoplankton specific growth rate (µ).
Kh/x2 and µ are balanced on the 45° broken line.
wave- and wind-induced turbulence. In fact, Gymnodinium sanguineum, whose
maximum specific growth rate is only 0.2–0.4 day–1, formed a red tide for 3 months
from 15 October to 11 December, 1990 in the eastern arm of the bay.
Sinking of diatoms and vertical physical processes
Since the average specific gravity of diatoms (~2 g ml–1) is greater than that of sea
water (Smayda, 1970), sinking is inevitable for diatoms unless physical processes
counteract the tendency to sink. Sinking, however, plays a role in replenishing cellular nutrients by renewing the surrounding water of the cell (Munk and Riley, 1952).
Some species follow a life cycle strategy where they form dormant cysts that sink
into the deeper aphotic zone and are brought up again to the euphotic zone with
the assistance of physical processes (Smetacek, 1985). Turbulence and upwelling
could be the processes supporting this life cycle strategy of diatoms, in addition to
their role of nutrient supply from the deep (Pitcher, 1990; Varela et al., 1991). From
this point of view, a certain level of vertical diffusivity and/or upwelling would be
required to sustain a diatom population in the surface layer.
The sinking rates (SR) of C.closterium and L.danicus (0.3–0.5 and 0.2–0.4
m day–1, respectively) were smaller than Kz/z (where z is the distance between
the upper layer and the lower layer) during the red tide formation of these species
(Table VI). This indicates that these species, which have low sinking rates, might
be almost passive to the normal level of turbulence occurring in this bay. Ruiz
et al. have reported that the sinking of organisms whose sinking rates were lower
than ~1 m day–1 would be affected by turbulence (Ruiz et al., 1996). This,
inversely, suggests that diatoms whose sinking rate is higher than ~1 m day–1
cannot be sustained in the upper euphotic zone only by vertical diffusion.
376
Effects of advection and upwelling on red tides
Table VI. Comparison of sinking rates of diatoms (SR) or swimming speeds of flagellates (SS) to the
physical parameters for the specific time periods of the reported blooms (Kz/z and upwelling velocity)
Species
SR or SS
(m day–1)
Diatoms
Cylindrotheca closterium
Eucampia zodiacus
Leptocylindrus danicus
Rhizosolenia delicatula
Rhizosolenia fragilissima
Skeletonema costatum
Flagellates
Gymnodinium sanguineum
Prorocentrum minimum
aSmayda
Kz/z
(m day–1)
Upwelling
(m day–1)
0.3–0.5a
0.4–5a
0.2–0.4a
0.3–0.7a
0.2–3a
0.3–1.2a
1.2
0.75
1.6
0.17
0.21
1.0
1.6
1.2
0.0
0.65
0.87
1.7
26.4b
3.6–5.9c
1.5
0.30
2.1
1.2
(1970); bCullen and Horrigan (1981); cBauerfeind et al. (1986).
Upwelling is another factor which supports diatoms in the upper layer.
Rhizosolenia delicatula and S.costatum can be suspended with the aid of
upwelling (Table VI). However, it does not seem to apply to species with extraordinarily high sinking rates, such as Eucampia zodiacus. Even the combination
of vertical diffusion and upwelling does not appear to be sufficient for these
species to be suspended in the water column. Denman and Gargett suggest that
phenomena such as internal waves and Langmiur circulation are important to
resuspend phytoplankton cells in the euphotic zone (Denman and Gargett, 1983).
As Kz/z and upwelling velocity were calculated on a monthly basis, such high
frequency phenomena would be averaged out in the present study. From our
observations, the red tides of E.zodiacus, which usually grow in the bottom layer
in winter (Table II), occasionally appear in the surface layer because of a strong
wind.
Swimming of flagellates and vertical physical processes
Diel vertical migration has been observed for some flagellate species, which may
allow them to take up nutrients in the lower layer during the night and carry on
photosynthesis in the upper layer during the day. However, when Kz/z is greater
than their swimming speed (SS), the flagellates should be distributed homogeneously in the water column, as is the case for diatoms. Also, if the upwelling
velocity is greater than SS, they would be carried far from the inner area of the
bay. In other words, SS must be greater than the speed of the water movement to
form red tides. The SS of G.sanguineum is reported to be as high as 26.4
m day–1 (Cullen and Horrigan, 1981), which is significantly greater than both the
Kz/z (1.5 m day–1) and upwelling velocity (2.1 m day–1) (Table VI). The SS of
Prorocentrum minimum (3.6–5.9 m day–1) is also greater than both the Kz/z (0.30
m day–1) and upwelling velocity (1.2 m day–1). This indicates that these dinoflagellates are able to concentrate at a comfortable depth due to their motility,
even under the turbulent and upwelling conditions which occur in Mikawa Bay.
377
T.Yamamoto and M.Okai
From the results obtained in the present study, it is concluded that flagellates
would form red tides even in severe diffusive conditions by using their swimming
ability, while diatoms form red tides due to their large growth rates and with the
aid of vertical diffusion and the upwelling movement of water. Although these
conclusions may be a restatement of conventional theory, no confirmation of the
theory has been carried out in the field as far as we know. Accumulation of monitoring data is both time-consuming and expensive, but it is valuable not only to
determine the trend of red tide occurrences, but also to help understand and
predict the spatial and temporal scale of red tides.
Acknowledgements
We thank Profs O.Matsuda and N.Rajendran and Dr T.Hashimoto, Faculty of
Applied Biological Science, Hiroshima Univ., Japan for their valuable discussion.
Thanks are also given to Profs P.J. Harrison and S.Pond, Dept Earth and Ocean
Sciences, Univ. British Columbia, Canada, for their critical review of the manuscript.
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Received on December 1, 1998; accepted on September 3, 1999
380