Journal of Oceanography, Vol. 56, pp. 131 to 139. 2000
Middle Layer Intrusion as an Important Factor Supporting Phytoplankton Productivity at a Tidal Front in Iyo
Nada, the Seto Inland Sea, Japan
T AMIJI YAMAMOTO1*, T OSHIYA HASHIMOTO1, HIDETAKA T AKEOKA2,
T ENJI SUGIYAMA1 and O SAMU MATSUDA1
1
Faculty of Applied Biological Science, Hiroshima University,
Higashi-Hiroshima 739-8528, Japan
2
Department of Civil and Ocean Engineering, Faculty of Engineering, Ehime University,
Bunkyo 3, Matsuyama 790-8577, Japan
(Received 30 November 1998; in revised form 10 May 1999; accepted 2 June 1999)
Field observations were conducted to examine the processes governing the
phytoplankton distribution and photosynthetic activity in and around a tidal front
formed in Iyo Nada, the Seto Inland Sea, Japan. The existence of a middle layer intrusion, which, it has been suggested, moves from the mixed region to the stratified
region of the tidal front, was ascertained by the phytoplankton distribution in addition to a T-S diagram. Skeletonema costatum, which originally inhabited the mixed
region, was used as the indicator to reveal the intrusion. However, the tip of water
containing the S. costatum population did not extend deeply into the stratified region.
The velocity of the intrusion seemed to be slow enough to make biological processes,
such as nutrient uptake by phytoplankton and subsequent growth, as well as the decrease in cell density due to zooplankton grazing, dominate during the transportation. The patchy distribution of copepod nauplii implied that grazing has an influence on the distribution pattern of phytoplankton. The location of high photosynthetic activity did not coincide spatially with the center of high phytoplankton biomass,
suggesting the importance of these biological processes. Therefore, it is considered
that the middle layer intrusion plays a role as an inducer of subsequent biological
processes at the tidal front by not only supplying nutrients from the mixed region but
also by increasing the vertical diffusivity.
Keywords:
⋅ Tidal front,
⋅ nutrient,
⋅ phytoplankton,
⋅ photosynthesis,
⋅ stratification,
⋅ mixing,
⋅ Iyo Nada.
low stratified region and the deep mixing region. This is
the opposite case to the fronts formed around England
(Pingree, 1978). The reason is that the strong tidal mixing due to the narrow Hayasui Strait between Iyo Nada
and the Bungo Channel (Fig. 1) causes a three-dimensional mixing there. Since the tidal current velocity at
Hayasui Strait is usually up to 2.5–3.0 m s–1 during spring
tides (Takeoka et al., 1993), continuous erosion has made
Hayasui Strait the deepest part of the Seto Inland Sea (up
to 300 m) (Fig. 1).
With time, nutrients in the surface layer of the stratified region of the front become depleted by the uptake of
phytoplankton. On the other hand, phytoplankton growth
rate is also limited due to the short residence time in the
euphotic layer in the mixed region of the front, whereas
nutrients are continuously brought up to the surface layer
by the mixing process. It has been reported that a chlorophyll peak is often observed at the front (e.g., Pingree,
1. Introduction
In shallow coastal areas, the tidal energy mixes the
water column due to turbulence generated by the friction
at the bottom. On the other hand, an increase in buoyancy of the surface water with increasing solar radiation
during early summer causes stratification of the water
column, which is destroyed by tidal mixing. The tidal
front, which is the top part of the pycnocline, is generally
formed when stratification occurs and is often characteristic of shallow coastal areas. Its location can be predicted
as a function of the depth and amplitude of the tidal excursion (Simpson and Hunter, 1974).
One of the major characteristics specific to the front
formed in Iyo Nada is that it is formed between the shal* Corresponding author. E-mail: [email protected]
Copyright © The Oceanographic Society of Japan.
131
1978). A simple explanation for the formation of a chlorophyll peak at the surface of tidal fronts is that a moderate supply of nutrients by various mechanisms and light
provide suitable conditions for the growth of
phytoplankton (Takeoka et al., 1993).
There are three mechanisms that supply nutrients to
the phytoplankton assemblage at the front, as follows: (1)
vertical diffusion through the pycnocline; (2) upwelling
accompanied by the frontal eddies; and (3) water exchange
by wind-induced turbulence in the surface layer (Loder
and Platt, 1985). Of these, mechanism (1) seems less effective judging from the small diffusivity, unless there
are no other processes such as an internal wave (Loder
and Platt, 1985). On the other hand, Pingree et al. (1979)
observed the frontal eddies (mechanism (2)) at the Ushant
front and discussed their importance as one of the nutrient supply mechanisms at tidal fronts. Stimulation of photosynthetic activity by the mixing of surface waters
(mechanism (3)) between the stratified region and the
mixed region was demonstrated by Savidge (1976) experimentally for phytoplankton at the Irish Sea front.
Recently, from the analysis of T-S diagrams in and
around the tidal front formed in Iyo Nada, the Seto Inland Sea, Japan, Takeoka et al. (1993) have suggested
that intrusion from the mixed region to the middle layer
of the stratified region must be the most important process that supplies nutrients to the subsurface of the frontal
region, producing an intense subsurface chlorophyll a
maximum. In the present study we document the intrusion of the middle layer by the distribution of
phytoplankton assemblages in and around the front, along
with the physical structure, and clarify the relative photosynthetic activities of phytoplankton assemblages at the
tidal front formed in Iyo Nada, the Seto Inland Sea,
Japan.
2. Materials and Methods
Observations were carried out on two lines across
the tidal front formed in Iyo Nada, the Seto Inland Sea,
Japan during June 21–22, 1995 (Fig. 1). The tidal range
was expected to be relatively small because it was a neap
tide during the sampling period, and the observation times,
0900–1410 21 June for Line A and 1010–1350 22 June
for Line B, corresponded to the flood tide (Maritime
Safety Agency, 1994). At all stations, CTD casts (SBE-9/
11, Sea-Bird Electronics Inc. plus Sea-Tech Fluorometer,
Sea-Tech Inc.) were done to measure water temperature,
salinity and underwater fluorescence prior to water sampling. From the profiles of these parameters, five water
sampling depths were chosen for each station: at the surface, between the surface and fluorescence maximum, at
the fluorescence maximum, below the fluorescence maximum, and just above the bottom. Dissolved oxygen (DO)
concentration was determined for the seawaters collected
from these depths by the Winkler method (Strickland and
Parsons, 1972) immediately after the sampling.
The water samples were filtered (Type HA,
Millipore) and the filtrate was used to measure nitrate- +
nitrite-N (hereafter referred to as NO 3) according to the
methods of Strickland and Parsons (1972). Since phos-
Fig. 1. Map showing the locations of sampling stations across the tidal front formed in Iyo Nada, the Seto Inland Sea, Japan.
132
T. Yamamoto et al.
phate-P and silicate-Si were supposed to show similar
spatial patterns to nitrate-N, considering the supply and
consumption processes in an offshore area, we did not
measure them in the present study. Although ammoniumN was measured for the water samples, we do not show
the results because no significant trend was found in the
spatial pattern. Samples for particulate organic carbon
(POC) and particulate organic nitrogen (PON) were collected on a precombusted (450°C, 2 h) glass fiber filter
(GF/F, Whatman) and measured with a CHN analyzer
(MT-3, Yanaco Co.). Chlorophyll a (Chl a) was determined by the spectrophotometric method of Jeffrey and
Humphrey (1975) using cellulose nitrate filters (Sartorius, 0.45 µm pore size) to calibrate the underwater fluo-
rescence values.
The photosynthetic activity of phytoplankton was
estimated using a fluorometer (Model 10, Turner Designs
Inc.) to measure the difference in the intensity of in vivo
fluorescence before (FN) and after (FD) the addition of a
herbicide DCMU (dichlorophenyl dimethylurea) to a final concentration of 10–5 M, according to the method of
Samuelsson and Öquist (1977). In a normal system of
photosynthesis, the light energy is used for the photochemical processes, and some of the energy is dissipated
as fluorescence. However, the presence of DCMU enhances the fluorescence to the maximum level due to
blockage of the electron transport in the photochemical
processes. Therefore, the difference in the intensity of in
Fig. 2. Vertical profiles of various parameters observed along Line A across the tidal front formed in Iyo Nada, the Seto Inland
Sea, Japan, on 21 June, 1995. From top to bottom, temperature (Temp.), salinity, density (sigma-t), nitrate + nitrite, particulate
organic carbon (POC), particulate organic nitrogen (PON), POC/PON (C/N) ratio and dissolved oxygen (DO) % saturation
(H = high and L = low).
Phytoplankton Productivity at a Tidal Front
133
vivo fluorescence before (FN) and after (FD) the addition
of DCMU is an estimate of the gross production. In addition to this, FD is a much better function of cellular Chl a
regardless of growth condition and species difference
(Slovacek and Hannan, 1977), then (F D–FN)/F D was used
as an index of the assimilation number, ranging from 0 of
no photosynthetic activity to ideally 1, when all electrons
are supposed to be used for the photosynthesis (no fluorescence).
The identification of phytoplankton species and cell
counts were done under a light microscope (S-Ke, Nikon)
for water samples preserved with 1% glutaraldehyde (final concentration). Total number of copepods was also
counted for water bottle samples. However, since nets
were not used to catch zooplankton, the number of
copepods may be underestimated because the larger
copepodite and adult stages probably escaped the water
bottle sampling.
3. Results
3.1 Characteristics of environmental parameters
From the temperature, salinity and density profiles
shown in Fig. 2, it can be seen that there was a transition
zone (Stns A4–A5) between the stratified region (Stns
A1–A3) and the mixed region (Stns A6–A7). The greater
Fig. 3. Vertical profiles of various parameters observed along Line B across the tidal front formed in Iyo Nada, the Seto Inland
Sea, Japan, on 22 June, 1995. From upper to lower, temperature (Temp.), salinity, density (sigma-t), nitrate + nitrite, particulate
organic carbon (POC), particulate organic nitrogen (PON), POC/PON (C/N) ratio and dissolved oxygen (DO) % saturation
(H = high and L = low).
134
T. Yamamoto et al.
range in temperature than salinity shows that this transition zone is the tidal front which is formed from the balance of heat and tidal mixing.
The concentration of NO 3 was low between the 20–
30 m layer of Stns A1–A5 (<0.5 µg-at l–1) and high in the
bottom layer of Stns A1–A2 (>2.0 µg-at l–1) (Fig. 2). On
the other hand, NO3 at the mixed station (A7) was homogeneous from the surface to the bottom at ~1.7 µg-at l –1.
Both POC and PON were high in the thermocline of the
stratified region, with a maximum of 146 and 46 µg l –1
respectively at 20–30 m at Stn A1 (Fig. 2). The POC/
PON ratio showed more than a two-fold difference, being high (~11) in the surface layer of Stn A1 and low (<4)
in the mixed region through the middle layer of the stratified region. DO concentration was supersaturated at the
surface of Stns A4–A5 and in the thermocline of the stratified region, while it was comparatively low in the mixed
region.
Along Line B, weak stratification of the water column was seen in the whole cross-section (Fig. 3). The
concentration of NO3 was low in the surface layer (~0.5
µg-at l–1) and high in the bottom layer of Stns B5–B6
(>2.0 µg-at l–1). POC and PON was maximum at the surface of Stn B5 (336 and 59 µg l–1). The POC/PON ratio
along Line B was relatively high in the bottom layer (occasionally > 14), and low (~6) at the surface of Stn B6
and the middle layer of Stn B1 (Fig. 3). DO concentration was saturated in the surface layer with the maximum
value (104.3%) at 24 m of Stn B3.
T-S plots from Lines A and B showed fundamentally
the same trend (Fig. 4). Temperature and salinity from
the stratified region (Stns A1 and B1) gave a straight line
showing a wide range both in temperature and salinity
and indicating the resistance to vertical mixing, while the
values from the mixed region (Stn A7) gathered together
at the same site at ca. 18°C and ca. 34, showing homogeneity in the water column. Along the transect from the
stratified to the mixed region, there was more deflection
in the T-S curves in the middle layer toward the point of
the mixed region. In the present case, the deflection occurred at the isopycnal layer of the density 24.4–24.5.
3.2 Phytoplankton distribution and photosynthetic activity
Along Line A, Chl a was present in concentration up
to 2.8 µg l–1 at the surface of Stns A5 and A6 and the
middle layer of Stn A1, and low in the mixed region (<1.6
µg l–1) (Fig. 5). The (FD–FN) values showed a similar
pattern to Chl a and also to DO % saturation (Fig. 2).
However, (FD–FN)/F D showed a slightly different pattern
from Chl a and (FD–FN). It was low at the surface of Stns
A5 and A6 where Chl a and the (FD–FN) were high, and
the maximum of (FD–F N)/F D was found at 20 m at Stn
A4.
Fig. 4. T-S diagram showing the physical characteristics in
and around the tidal front. Line A (upper) and Line B
(lower). Numbers on the T-S plot indicate the depth where
the T-S curve deflected toward the mixing water of Stn A7.
Chlorophyll a along Line B was high in the middle
layer (1.8–2.4 µg l–1) through the entire cross-section (Fig.
5). The maximum value of (FD–FN) was found just above
the Chl a maximum through Stn B3–B6 (Fig. 5), roughly
corresponding to the pattern of DO % saturation (Fig. 3).
On the other hand, the maximum of (FD–FN)/F D was located at the surface of Stn B5, which is above the (FD–
FN) maximum and shifted to the middle layer of the stratified region (Fig. 5).
The distribution pattern of dominant phytoplankton
was divided into three types. Type I was the group which
was distributed from the surface to the thermocline or in
the front. Prorocentrum sp. was found along the
Phytoplankton Productivity at a Tidal Front
135
Fig. 5. Vertical profiles of Chl a, (F D–FN), and (FD–F N)/FD along (a) Line A and (b) Line B across the tidal front formed in Iyo
Nada, the Seto Inland Sea, Japan. Observations of Lines A and B were carried out on 21 and 22 June, 1995, respectively (H =
high and L = low).
thermocline along Line A (Fig. 6), while it was concentrated in the surface along Line B (Fig. 6). Eutreptiella
gymnastica showed a clear preference for the surface, as
shown in both lines. Type II was the group which showed
benthic habitation represented by Melosira sp. Type III
was the group which originally inhabited the mixed region as seen for Skeletonema costatum and it should be
noted that it showed a deflection in distribution from the
mixed layer to the middle layer of the stratified region in
both lines (Fig. 6). This might be an indicator of the middle layer intrusion, as discussed below.
4. Discussion
The deflection of the T-S curves suggests that the
seawater in the middle layer of the stratified region may
be exchangeable with the water of the neighboring mixed
layer (Fig. 4). Takeoka et al. (1993) suggest that the flow
directed from the mixed region to the stratified region is
inevitable due to the gravity balance, which accelerates
the movement of both the light surface water and the
heavy bottom water in the stratified region toward the
mixed region, and this then allows the mixed water to
136
T. Yamamoto et al.
intrude into the middle layer of the stratified region. The
timing of our observations, which corresponded to the
flood tide, might have enhanced the extent of intrusion at
the front in Iyo Nada observed in this study.
The distribution pattern of Type III species represented by S. costatum (Fig. 6), visually indicated and
strongly supported the existence of the middle layer intrusion. This is important information, revealed by laborious microscopic work, and it can not obtained from
physical and chemical analyses. This horizontal water
movement should also drag the water from the surface of
the front toward the middle layer of the stratified region.
A distorted distribution pattern from the surface front to
the middle layer found in E. gymnastica of Type I (Fig.
6) seems to indicate such a phenomenon. However, no
sign of intruding water movement was found in NO 3 distribution. This is thought to be due to uptake by
phytoplankton during the intrusion process.
The location of the maximum of (FD–FN)/FD, which
would be an index of the assimilation number, shifted
toward the stratified region along both Line A and Line B
(Fig. 5). Takeoka et al. (1993) have given a schematic
Fig. 6. Vertical distributions of dominant phytoplankton species along (a) Line A and (b) Line B across the tidal front formed in
Iyo Nada, the Seto Inland Sea, Japan. Observations of Lines A and B were carried out on 21 and 22 June, 1995, respectively
(H = high and L = low).
explanation of the mechanisms causing intensification of
the Chl a maximum at the tidal front. In their concept,
the horizontal flow not only shifts the location of the Chl
a maximum toward the stratified region but also stimulates photosynthesis by improving both the nutrient and
light conditions. Using computer analyses which simulate the hydrological and biological conditions of the tidal
front of Iyo Nada, Hashimoto et al. (1995) revealed that
an intrusion by the middle layer is necessary to shift the
Chl a maximum and stimulate photosynthesis. This horizontal water movement would also accelerate the vertical diffusion process across the thermocline. Therefore
the middle layer intrusion also plays a role in mixing nutrients across the thermocline.
The maximum copepod density was also found in
the middle layer along Lines A and B (Fig. 7). Almost of
the copepod were those of nauplius stages. Although they
were not identified, they probably belong to Calanus
sinicus and Paracalanus sp., which are reported to be the
dominant copepod species in this region (Uye and
Shimazu, 1997). It is also known that these species start
to feed phytoplankton from the nauplius stage III (Uye,
1988, 1991). A numerical model suggests that the current
velocity of middle layer intrusion must be less than 4 cm
s–1 (Hashimoto et al., 1995). In case of a velocity greater
than 4 cm s–1, Chl a concentration in the stratified region
became higher than that in the front. This small current
velocity of the middle layer intrusion would be slow
Phytoplankton Productivity at a Tidal Front
137
ing stock, indicating that copepods might prefer actively
growing phytoplankton.
In the present study, the distributional pattern of
phytoplankton in addition to the deflection of T-S curve
strongly suggests that the middle layer intrusion occurs
from the mixed region to the stratified region of the tidal
front. Although the current velocity of the middle layer
intrusion may not be high enough to be detectable, we
can conclude that it would be important for the following
reasons (Fig. 8): (i) it supplies nutrients continuously from
the mixed region to the layer just below the thermocline
of the stratified region; (ii) it accelerates the nutrient supply rate to the nutrient-depleted upper layer due to its intensification of the diffusivity across the thermocline; and
then, (iii) it stimulates photosynthetic activities of the
phytoplankton assemblage and biological processes of
higher trophic levels.
Fig. 7. Vertical distribution of copepod nauplii counted in water bottle samples from Line A and Line B.
Fig. 8. Schematic graph showing a chain of processes induced
by the middle layer intrusion at a tidal front in Iyo Nada,
the Seto Inland Sea, Japan. Chlorophyll maximum at the
front is considered to be sustained by the nutrient supply,
which is continuously transported from the mixed region
by the middle layer intrusion. The middle layer intrusion
would also accelerate the nutrient supply from the layer
below the thermocline due to intensifying the vertical diffusivity.
enough to allow grazing of phytoplankton and might be
one of the reasons why Type III species did not extend
their distribution deep into the stratified region. It is also
interesting that the distribution of copepods showed a
good correlation with (FD–FN)/FD rather than Chl a stand138
T. Yamamoto et al.
Acknowledgements
We thank Prof. P. J. Harrison, Dept. of Earth and
Ocean Sciences, Univ. British Columbia, Canada, for his
critical review of the manuscript.
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