Plankton Benthos Res 9(1): 42–50, 2014
Plankton & Benthos
Research
© The Plankton Society of Japan
Effects of salinity on diel vertical migration behavior in
two red-tide algae, Chattonella antiqua and
Karenia mikimotoi
TOMOYUKI SHIKATA1,*, SETSUKO SAKAMOTO1, GOH ONITSUKA1, K AZUHIRO AOKI2 &
MINEO YAMAGUICHI1
1
National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, Maruishi 2–17–5,
Hatsukaichi, Hiroshima 739–0452, Japan.
2
National Research Institute of Fisheries Science, Fisheries Research Agency, 2–12–4 Fukuura, Kanazawa, Yokohama,
Kanagawa 236–8648, Japan.
Received 17 May 2013; Accepted 4 December 2013
Abstract: We examined the effects of salinity on diel vertical migration (DVM) of two coastal flagellates, Chattonella
antiqua and Karenia mikimotoi, in 90-cm-high columnar aquariums. Experiments were performed with surface salinities from 5 to 32 and bottom salinity constant at 32. Cells of each flagellate were injected into the bottom of the
aquarium at night and the vertical distribution of cells was monitored every 4 h for 36 h in one series of experiments,
or twice daily (day and night) for 5 days in another. Ascent and descent started at approximately the same time in all
water columns, indicating that difference in surface salinity does not substantially affect DVM rhythm in the two
flagellates. During daytime, C. antiqua and K. mikimotoi transited haloclines with surface salinities ≥ 15 and accumulated at the surface, although K. mikimotoi required 2 days to transit the halocline with surface salinity of 20 and 4
days for surface salinity of 15. However, neither flagellate could transit haloclines with surface salinities of 5 or 10;
instead they accumulated in the halocline during daytime. At night, most cells of both species accumulated at the bottom in all water columns, although the distribution of K. mikimotoi gradually expanded to the upper layers on successive days when surface salinity was 5 or 10. We demonstrated that low salinity in the surface layer blocks upward migration in two flagellate species and delays surface accumulation and weakens population synchrony of DVM at night
in K. mikimotoi.
Key words: acclimation, accumulation, flagellate, halocline
Introduction
Some flagellate algae display diel vertical migration
(DVM) behavior. They start to swim toward the surface
before dawn and to deeper layers at dusk (Yamochi & Abe
1984, Olsson & Granéli 1991, Koizumi et al. 1996, Park et
al. 2001). This DVM enables flagellates to optimize photosynthesis regardless of weather or water clarity (Ault
2000), to acquire nutrients over a wide depth-range (Watanabe et al. 1991, Hall & Paerl 2011), and to avoid predation
by zooplankton, which swim to the surface at night and return to deeper layers in the daytime (Lampert 1989). Diel
vertical migration thus aids in competition with other microalgae such as diatoms, which do not have this ability
* Corresponding author: Tomoyuki Shikata; E-mail, [email protected]
(Watanabe et al. 1995, Smayda 1997, Kamykowski et al.
1998, Salonen & Rosenberg 2000). Diel vertical migration
is therefore one of the most important physiological adaptations for survival and growth of flagellate algae.
Diel vertical migration behavior should be less subject to
the external environment because its rhythm is controlled
by an endogenous clock (Roenneberg et al. 1989, Shikata
et al. 2013). However, some environmental conditions such
as nutrient concentrations and light levels can sometimes
affect this physiological behavior (Heaney & Eppley 1980,
Richter et al. 2002). Salinity is also an important environmental condition for completion of DVM in coastal flagellates. In coastal areas, freshwater inflow from rivers causes
dramatic decreases in surface salinity, thereby forming
strong haloclines (Shikata et al. 2008b). Therefore, flagellates performing DVM there often have to transit the halo-
Migration of red-tide algae in halocline
cline. However, the rapid salinity changes that migrating
flagellates must experience in the halocline can inhibit
their swimming ability (Shikata et al. 2008a) and their survival (Mahoney & McLaughlin 1979, Shimura et al. 1979).
In fact, the halocline can block the DVM ascent and descent of some flagellates (Legovi et al. 1991, Bearon et al.
2006, Jephson & Carlsson 2009, Jephson et al. 2011).
Because there have been few studies on the effects of
environmental factors on the DVM behavior of flagellate
algae, we examined the effects of salinity on DVM in the
raphidophyte Chattonella antiqua (Hada) Ono and the dinoflagellate Karenia mikimotoi (Miyake & Kominami)
Hansen & Moestrup. These two flagellates form harmful
red tides that cause tremendous damage to aquaculture industries along the Japanese coast (Okaichi 2004, Imai &
Yamaguchi 2012). In both species, DVM facilitates the
growth of individual cells and increases in population size
and can lead to fish kills through surface accumulation of
cells (Koizumi et al. 1996, Amano et al. 1998, Honjo
2004).
Materials and Methods
43
Fig. 1. Columnar aquarium used as a culture vessel to observe
diel vertical migration. The aquarium had nine sampling ports
for measurement of cell density and was capped with a daylight
colored-LED lamp.
Culture
We isolated clonal strains of Chattonella antiqua (strain
CHA3) from the Yatsushiro Sea, Japan, in June 2010 and
Karenia mikimotoi (strain KM02) from near the North Kujuku Islands, Japan, in July 2005. The C. antiqua strain
was axenic, but that of K. mikimotoi was not. Cultures
were maintained in 50-mL Erlenmeyer flasks containing
25 mL of modified SWM-3 medium (Shikata et al. 2011)
with a salinity of 32 at 25°C under 300 μmol photons
m–2 sec –1 of white fluorescent irradiation on a 12-h : 12-h
light:dark cycle [light period, 0600–1800 local time (LT)].
Irradiance in the incubator was measured with a Quantum
Scalar Laboratory Irradiance Sensor (QSL-2101, Biospherical Instruments Inc., San Diego, CA, USA).
Monitoring of DVM with different surface salinities
We used a columnar aquarium as a culture vessel to
monitor DVM (Fig. 1). The aquarium (inner diameter,
5 cm; height, 90 cm) was made of acrylic, with nine
sampling ports (diameter, 13 mm) at intervals of 10 cm,
starting from the bottom. Each port was plugged with a
silicone-rubber stopper. The aquarium was placed in a
temperature-controlled room (25°C) and capped with a
disc-shaped LED lamp (daylight color; INREDA, Spotlight LED, Inter IKEA Systems B.V., Netherland). The light
intensity at the surface was 250 μmol photons m−2 sec−1.
The experiments were performed with surface salinities
varying from 5 to 32 and a bottom salinity kept constant at
32. To establish a salinity gradient, we first added 810–
820 mL of modified SWM-3 medium with a salinity of
5–32, depending on the desired halocline. Then the same
volume of medium with a salinity of 32 was slowly added
to the bottom of the aquarium via a long glass tube (length,
1 m; inner diameter, 5 mm) and a funnel. After allowing
the water column to stabilize for 3–4 h, we used a syringe
and needle (gauge, 0.7 mm) to inject 25–50 mL of a cell
suspension containing about 10,000–20,000 cells mL−1 of
Chattonella antiqua or Karenia mikimotoi through the
sampling port at the bottom of the aquarium; the injection
was done at night (2000 LT, Day 0). The final water depth
in the aquarium was about 85 cm. Thereafter, at fixed time
intervals, 3.5 mL of the cell suspension was sampled from
the water surface or from each sampling port, and then the
aquarium was refilled from the surface with 17.5 mL of
fresh medium matching the surface salinity (5–32) and
from the bottom sampling port with 17.5 mL of fresh medium matching the bottom salinity (32).
To determine the vertical distribution of cells, we measured the in vivo fluorescence (Brand et al. 1981) of the
sample from each depth by using a fluorometer (Model
10–005R; Turner Designs, Sunnyvale, California, USA).
Previous studies (Yamaguichi & Honjo 1989, Yamaguchi
et al. 1991) showed that the cell densities of C. antiqua and
K. mikimotoi were positively correlated with in vivo fluorescence. The salinity of each sample was measured at the
same time with an immersion refractometer (IS/Mill-E,
AS ONE Corporation, Japan) to observe the vertical distribution of salinity. For sample collection during the dark
period, we used a red LED flashlight (peak wavelength,
640 nm) for illumination, because red light has little effect
on the DVM rhythm of C. antiqua (Shikata et al. 2013) or
K. mikimotoi (Shikata et al. unpublished).
44
T. Shikata et al.
Design of the two experiments
We conducted two experiments. In the first experiment
(hereafter, the short-term experiment), variations in the
vertical distribution of cells were monitored in water columns with six different surface salinities (5, 10, 15, 20, 25
or 32). Samples were collected every 4 h for 36 h starting
from 0000 LT on Day 1. In the second experiment (hereafter, the long-term experiment), variations in the vertical
distribution of cells were monitored in water columns of
two or three different surface salinities (for Chattonella
antiqua: surface salinity 5 or 10, bottom salinity 32; for
Karenia mikimotoi: surface salinity 5, 10, or 15, bottom salinity 32). Samples were collected twice a day (daytime,
1230–1330 LT; nighttime, 1900–2000 LT) every day, from
daytime on Day 1 to daytime on Day 5. Both experiments
were performed in triplicate. Water temperature at the surface (1 cm water depth) measured with a temperature data
logger (RTR-52A, T&D Corporation, Japan) remained almost constant (25±0.3°C). The halocline is defined as the
layer in which the difference in average salinity between
neighboring sampling ports is ≥2. There was minimal disturbance of salinity gradients in all water columns
throughout the experimental periods. For example, the surface and bottom salinities in the most stratified column
ranged from 4 to 7 and from 30 to 34, respectively, in the
two experiments.
Results
Short-term experiment
The vertical distributions of Chattonella antiqua and
Karenia mikimotoi in water columns with different surface
salinities were monitored every 4 h for 36 h to examine
how low salinity in the surface layer affected the DVM behavior of the two flagellates over a short time-period. Average in vivo fluorescence of C. antiqua and K. mikimotoi
at the 10 sampling depths in the water column generally
fluctuated in the range of 101–102 over the experimental period, but there was no clear increasing or decreasing trend
under any experimental conditions (Figs. 2a, 3a). This
means that total cell numbers in the water column were
roughly constant, indicating that noticeable death and
growth did not occur over the experimental period in any
of the haloclines. In all salinity gradients, C. antiqua
started to ascend at 0000–0400 and to descend at 1600–
2000 (Fig. 2b–g); K. mikimotoi started to ascend at 0400–
0800 and to descend at 1200–1600 (Fig. 3b–g). This indicated that the DVM rhythms of both species were approximately constant regardless of surface salinity. However,
the layers of maximum in vivo fluorescence during the
daytime differed for different surface salinities. For C.
antiqua, most cells accumulated at the surface (0 cm water
depth) in water columns with surface salinities greater
than 15 but remained in the upper part of the halocline dur-
ing the daytime (35 cm water depth; salinity, 9–11) in
water columns with surface salinity of 5 or 10 (Fig. 2b, c).
The results were more complicated for K. mikimotoi (Fig.
3b–g). From daytime on Day 1, most cells accumulated at
the surface (0 cm water depth) in water columns with surface salinities of 25 and 32. In the water column with a
surface salinity of 20, most K. mikimotoi cells accumulated
in the upper part of the halocline (35 cm water depth; salinity, 21) on Day 1 but reached the surface on the following day. When the surface salinity was 15, the maximumdensity layer for K. mikimotoi during the daytime shifted
from the middle of the halocline (45 cm water depth; salinity, 25) on Day 1 to the upper halocline (35 cm water
depth; salinity, 15) on Day 2. When the surface salinity
was 5 and 10, most K. mikimotoi cells accumulated in the
middle of the halocline (45 cm water depth; salinity, 20–
22) during the daytime on both days. At night, most cells
of both species accumulated at or near the bottom regardless of halocline strength (Figs. 2b, 3b).
Long-term experiment
We followed the DVM behaviors of Chattonella antiqua
and Karenia mikimotoi for 5 days in the water columns
with quite low salinity in the upper layers, in which they
could not reach the surface in the short-term experiment,
to see whether they could transit the haloclines and reach
the surface given more time. Average in vivo fluorescence
of C. antiqua and K. mikimotoi at 10 sampling depths in
the water column fluctuated in the range of 101–102 over 5
days, and increased only little by little at any of the surface
salinities (Figs. 4a, 5a), indicating that the two species
grew only slightly over the experimental period at any of
the surface salinities. Most C. antiqua cells could not transit the haloclines and instead accumulated in the upper and
middle parts of the haloclines (35–45 cm water depth; salinity, 7–22) in the daytime and at the bottom at night for
all 5 days (Fig. 4b, c). Karenia mikimotoi also could not
transit the haloclines and accumulated in the upper or middle part of the haloclines (35–45 cm water depth; salinity,
12–21) in the daytime when the surface salinity was 5 or
10 (Fig. 5b, c). When the surface salinity was 15, however,
most K. mikimotoi cells were found in the upper part of the
halocline in the daytime until Day 2, but thereafter the percentage of cells at the surface in the daytime increased
daily and exceeded 50% on Day 4 (Fig. 5d). At night, most
K. mikimotoi cells accumulated at the bottom for all surface salinities over 5 days, but the percentage of cells at the
bottom gradually decreased and those in the upper layers
increased when the surface salinity was 5 or 10 (Fig. 5b, c).
Discussion
Diel vertical migration behavior should not only provide
advantages to flagellates by enabling efficient acquisition
of nutrients and light, but would also expose them to the
risk of down- and up-shocks due to salinity changes in
Migration of red-tide algae in halocline
45
Fig. 2. Short-term (36 h) experiments for diel vertical migration of Chattonella antiqua in water columns with various surface salinities (5, 10, 15, 20, 25, and 32) and bottom salinity of 32. (a): Temporal variations in in vivo fluorescence averaged over
the entire water column (mean±SD, n=3). (b–g): Time-series sections of the vertical percentage distribution of cells (mean,
n=3) in the columns and vertical profiles of the average salinity over the experimental period. White and black bars above each
panel represent light and dark periods, respectively. Gray areas in (b)–(f) represent the halocline.
coastal areas where there are frequent inflows of fresh
water to the surface layer. Therefore, coastal flagellates
should have the ability to quickly sense salinity changes
and to control swimming patterns. In some flagellates,
such as Tetraselmis sp. (Prasinophyceae), Heterosigma
akashiwo (Y. Hada) Y. Hada ex Y. Hara & M. Chihara
(Raphidophyceae) and Heterocapsa triquetra (Ehrenberg)
F. Stein (Dinophyceae), cessation of upward swimming
and a decrease in swimming speed have been observed
when they transit a strong halocline in laboratory conditions (Erga et al. 2003, Bearon et al. 2006, Jephson et al.
2011). Some flagellates such as Gyrodinium aureolum
46
T. Shikata et al.
Fig. 3. Short-term (36 h) experiments for diel vertical migration of Karenia mikimotoi in water columns with various surface
salinities (5, 10, 15, 20, 25, and 32) and bottom salinity of 32. (a): Temporal variations in in vivo fluorescence averaged over the
entire water column (mean±SD, n=3). (b–g): Time-series sections of the vertical percentage distribution of cells (mean, n=3) in
the columns and vertical profiles of the average salinity over the experimental period. White and black bars above each panel
represent light and dark periods, respectively. Gray areas in (b)–(f) represent the halocline.
Hulburt form a thick bloom in a strong halocline (Bjørnsen
& Nielsen 1991). We found that Chattonella antiqua and
Karenia mikimotoi stopped ascent in the halocline when
there is low salinity in the upper layer (Figs. 2b, 3b).
According to field observations by Katano et al. (2012),
Chattonella spp. does not migrate into the surface layer
when salinity is low (＜10) after inflow from a large river.
Onitsuka et al. (2011) observed that a maximum layer of
the cell density of C. antiqua was located in the halocline
only at sampling stations where the surface salinity was
quite low.
Some microalgae control intracellular concentrations of
Migration of red-tide algae in halocline
47
Fig. 4. Long-term (5 days) experiments for diel vertical migration of Chattonella antiqua in water columns with surface salinities of 5 and 10, into which C. antiqua did not penetrate in the short-term experiment, and with a bottom salinity of 32. (a):
Daily variations in the in vivo fluorescence (mean±SD, n=3) averaged over the entire water column; white and black bars represent light and dark periods, respectively. (b, c): Time-series sections of the vertical percentage distribution of cells (mean,
n=3) in daytime and at night in the columns with surface salinities of 5 (b) or 10 (c), and vertical profiles of average salinities in
the daytime over the experimental period; gray areas represent the halocline.
organic osmolytes such as glycerol and ribitol, and ions such
as K＋ and Cl− so as to tolerate salinity changes (Hellebust
1985, Kirst 1989, Gustavs et al. 2010). However, osmotic
pressure moves water in or out of the cell across the cell
membrane before osmoregulation is accomplished; therefore the volume and shape of the cell change immediately
after a salinity change (McMillan & Johansen 1988, Kirst
1989). In consequence, salinity changes can cause temporary inactivation of motility and cause cell death (Hellebust 1985, Kirst 1989, Shikata et al. 2008b). In the present
study, however, the average in vivo fluorescence (that is,
total cell numbers) of C. antiqua and K. mikimotoi in the
water column did not decrease over the experimental periods, even when the surface salinity was extremely low.
Our microscopic observations revealed that most cells in
the halocline were motile and had a normal shape (data not
shown). These results indicate that both species could
avoid low salinities causing physiological damage.
The lowest salinity into which a flagellate can enter by
DVM varies among species: H. akashiwo, 8 (Bearon et al.
2006); C. antiqua, 7 (this study); and K. mikimotoi, 12 (this
study). These values are usually close to the threshold salinity for their growth: H. akashiwo, 2–5 (Tomas 1978,
Martínez et al. 2010); C. antiqua, 5–10 (Shikata et al.
2010); and K. mikimotoi, 10–15 (Yamaguchi & Honjo
1989). This suggests that coastal flagellates can transit
haloclines as long as the salinity above the halocline is
above the threshold for their growth. From this perspective, C. antiqua can photosynthesize and grow more successfully in shallower layers than K. mikimotoi when surface salinity is quite low. The present study found that,
compared with K. mikimotoi, C. antiqua requires a much
48
T. Shikata et al.
Fig. 5. Long-term (5 days) experiments for diel vertical migration of Karenia mikimotoi in water columns with surface salinities of 5, 10 and 15, into which K. mikimotoi did not penetrate during the short-term experiment, and with a bottom salinity of
32. (a): Daily variations in the in vivo fluorescence (mean±SD, n=3) averaged over the entire water column; white and black
bars represent light and dark periods, respectively. (b–d): Time-series sections of the vertical percentage distribution of cells
(mean, n=3) in daytime and at night in the columns with surface salinities of 5 (b), 10 (c) or 15 (d), and vertical profiles of average salinities in the daytime over the experimental period; gray areas represent the halocline.
shorter period to reach surface layers with low salinities,
and that C. antiqua can concurrently descend to the bottom at night even when the surface salinity is extremely
low during the day, allowing secure nutrient-uptake in
deeper layers. These advantages due to DVM in C. antiqua
may partly explain why C. antiqua frequently blooms in
the Ariake Sea and the Yatsushiro Sea (Matsubara et al.
2009, Aoki et al. 2012), where there are inflows from large
rivers such as the Chikugo River and the Kuma River, respectively, and why C. antiqua blooms can develop when
surface salinity is extremely low (10–15) in these estuaries
(Matsubara et al. 2009). On the other hand, K. mikimotoi
rarely blooms in strongly enclosed bays around Japan, and
the salinity necessary for blooming of this species is rather
high (mainly 28–33) (Matsuoka et al. 1989).
The presence of low-salinity surface layers strengthens
Migration of red-tide algae in halocline
vertical stability of the water column, which promotes cell
accumulation by DVM and thereby increases the likelihood of red tide formation by flagellates (Hershberger et al.
1997). Red tides of C. antiqua and K. mikimotoi also develop under stratified conditions originating from river inflow (Yamaguchi 1994, Matsubara et al. 2009). DVM behavior itself would also promote development of a red tide
under stratified conditions. Moving up to the surface layer
gives flagellates a big advantage in their competition with
diatoms, which do not have DVM ability. This is particularly so under stratified conditions, because nutrient
sources originating from rivers and the intensity of photosynthetically active radiation are higher in the upper layer.
However, if diatoms that have higher tolerance to low salinity than flagellates exist in the low-salinity surface
layer, the advantage for flagellates of DVM may be reduced or disappear. Katano et al. (2012) observed that after
the salinity in water with a mixture of the coastal diatom
Skeletonema spp. and Chattonella spp. decreased drastically, Skeletonema spp., which can grow even at quite low
salinities (Shikata et al. 2008b, 2010, Balzano et al. 2011),
bloomed whereas Chattonella spp. stayed in the halocline,
where light intensity was not enough to sustain its population during daytime, and then it decreased in numbers.
This illustrates how the relationship between growth and
salinity is an important factor in competition between flagellates and diatoms in low-salinity surface waters, as well
as underlining the importance of the relationship between
DVM in flagellates and surface salinity. The relationships
between DVM behavior and surface salinity could influence not only competition among species but also species
succession, the species habitat distributions and growth
dynamics. In the near future, we will examine the synergetic effects of salinity and other environmental conditions
such as light and nutrients, which always coexist in nature,
on DVM behavior to further elucidate the developmental
mechanisms of red tides in these two harmful species.
Acknowledgements
This study was supported by a grant from the Japan Society for the Promotion of Science (25340024).
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