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Effect of silicate enrichment on ice algae at low salinity in Saroma-ko Lagoon, Hokkaido, Japan
wine Systems 1I ( 1997145-5
b 9
’ Hokkaido National Fisheries Research Institute. Kushiro, Hokkaido 085, Japan ’ Biology Department, Uniljersity qf Waterloo, Waterloo, Ont. N2L 361, Canada ’ Sea Ice Research Laboratoq, Hokkaido Vvirersity, Monbetsu, Hokkaidc 094. Japan
Received 18 September 1994; accepted 11October 1995
Abstract
The response of ice algae to low salinity was determined at three levels of silicate enrichment during the winter of 1992 in Saroma-ko Lagoon, Hokkaido, Japan. Regardless of the silicate concentration, the chlorophyll a content decreased by 50% of its initial value within the first day of exposure to low salinity water (22 psu) and continued to decrease gradually thereafter. The degree of decrease after the first day was a function of silicate concentration. The size distribution of the ice algae at the beginning of the incubation was 52% in the size class > 10 p,rn, 39% in 10-2 pm and 9% in 2-0.2 pm. Within two weeks of silicate enrichment, the 2-0.2 pm fraction decreased to less thti 1% while the > 10 pm fraction increased to more than 90%. Low salinity and low silicate concentrations reduced the chlorophyll a biomass and photosynthetic activity. Silicate enrichmecrts, ewn st th e !ow s&&y, e&nsced phottijynthctic rrctivity cgd the relative abundance of the > 10 pm cells. Our results suggest that ice algae may not survive if trapped in the low salinity lens that is present immediately below the ice during melting because of possible osmotic damage associated with silicate deficiency.
However, ice algal cells may recover from the damage when they sink into the high salinity and silicate-rich underlying water in Saroma-ko Lagoon. The ecological role of low salinity water is discussed in relation to vertical flux of ice algae. Keywords: salinity; silicate; deficiency; cell size; less saline lenses; photosynthesis
1. Introduction Growth of ice algae is vigorous in brine pockets even at salinities as high as 50 psu (Arrigo and Sullivan, 1992). As the ice melts, it produces a low salinity lens immediately below the sea ice. Ice algae
* Corresponding author. Present address: Lab. of Biological Oceanography, Dep. of Rioengineering, Soka University Hachioji, Tokyo 192, Japan. Phone/fax: $1 426 91 8002. E-mail: [email protected].
that are flushed into this layer during melting may go through a drastic change in their physiological condition, particularly in the vicinity of freshwater runoff, where the ice algae are even more likely to encounter a wide range of salinities (Ingram and Larouche, 1987; Lepage and Ingram, 1991; Runge and Ingram, 1991). The presence of ~~~~~entsin brine pockets 0 sea ice is essential for ice algal growth. Unfortunately, it is difficult to dire&y determine nutrient concentrations in brine pockets due to their small size (less than 1 mm diameter; Lake and Lewis,
0924-7963/97/$17.00 Copyright 0 1997 Elsevier Science B.V. All rights reserved. PII SO924-7963(96)00026-7
46
S. Tqpchi et al. / Jowxnl of Mmhe Systems 11 f 1997145-52
1970). However, Smith et al. (1990) observed a close correspondence of dissolved inorganic nutrients (except for silicate) to the approximately exponential vertical increase in the chlorophyll a concentration in fine sections of bottom sea ice in the High Arctic. Nutrient contents of sea ice in Saroma-ko Lagoon were not as low as those reported for the Canadian Arctic (Taguchi et al., 1994), but regardless of the varying amounts of nutrients in sea ice (Smith et al., 1990), the nutrient concentrations in the low salinity lenses are low compared to those in the underlying water column (Cota et al., 1990). The duration of this low salinity and silicatelimited water layer may be a function of the advection of seawater from the water column. When a stable condition lasts longer than one day, low salinity and silicate deficiency are expected to affect the physiology of ice algae at the ice-water interface since silicate deficiency may occur within 24 h (Badour, 1968; Werner, 1970; Taguchi et al., 1987) and may subsequently play a significant role in competition between species (Egge and Aksnes, 1992). Saroma-ko Lagoon is located at the northeast coast of Hokkaido, Japan. It is highly eutrophic with the annual gross primary production by phytoplankton estimated to be 780 g Cm“ yr- ’ (Fuji, 1979). During winter, sea ice covers almost the entire lagoon. A dense layer of ice algae develops at the bottom of the ice by early spring while phytoplankton in the water column is scarce, Freshwater input, which is mainly supplied by two major rivers, causes a reduction of salinity to less than 32 psu. A siliconrich layer of freshwater from the Hamasaroma River underlies the low salinity-low silicate lenses that form as a result of melting sea ice (Taguchi et al., 1994). Therefore, once the ice algae in Saroma-ko Lagoon are released from the sea ice, they may experience the low salinity-low silicate lenses, then the intermediate salinity but nutrient-rich runoff water, and finally the nutrient-rich and saline bottom water. Little is known about the physiological changes in ice algal cells during passage between these water layers. The purpose of the present study was to test the hypothesis that less saline water decreases the growth rate of ice algae and that the extent of the decrease or possible recovery is a function of the silicate
enrichment. The present experiment was designe examine the effect of less saline water in combination with silicate enrichment during the period of ice melt in Saroma-ko Lagoon, Hokkaido, Japan.
2. Materials and metho On three occasions in the winter of 1992, temperature and salinity under the sea ice were determined with a Sea Bird memory CTD model Seacat 19 at St. E. 2 km from the laboratory (Fig. 1). Die1 variability in temperature and salinity was determined hourly, if possible, from 17;08 on 26 February to 19: 18 on 27 February and from 13: 12 on 23 March to 1257 on 24 March. In addition, spatial variability in temperature and salinity was determined on 11 March to study the effect of freshwater runoff from the Hamasaroma River. The observation stations samSea of Okhotsk
Fig. 1. Map of sampling locations on the ice site in Saroma-ko Lagoon, Hokkaido, Japan. SRC’A is a laboratory of the Saroma Research Center for Aquaculture. The small embayment at the top right is not open to the Sea of Okhotsk.
pled on this occasion
Temperature and sali 0.5 m depth (0.3 m from the bottom ice) to avoid the wate of the sampling hole. for the linear increase m to estimate the slope of pycnocline. Water samples were collected with Niskin bottles at 1, 2.5, 5 and 7.5 m depth through the ice hole at St. E during the period from 19 February to 20 March. Subsamples for silicate an through a membrane filter (type - 20°C until processing. Two ice core samples were collected on ary at St. E with an ice-core sampler ( 1985). The sea ice was 20 cm thick. The 2 to 3 cm were scraped carefully into a dark bottle filled with filtered seawater ( glass fiber filter, collected at 1 m depth) and allowed to melt slowly at - 1.8”C(Garrison and Buck, 1986). The resulting suspension was 10% melted ice and 90% seawater, with a salinity of about 30 psu. Ninety ml of this suspension were diluted to 3000 ml with artificial seawater (Morel et al., 1979) giving a final salinity of about 22 psu. This salinity was close to that at the ice-water interface at the study site (Shirasawa et al., 1997-this issue). These suspensions were enriched with an f/2 medium (Guillard and Ryther, 1962) that lacked silicate. The first bottle did not receive any silicate but had a trace amount from the ice algal suspension. The second and third bottles had 18 and 54 pJ4 of silicate, respectively. Incubation was started with the inoculation of 30 mg 13C labeled sodium bicarbonate. A light-dark cycle (11 h:13 h) with 10 pErnm2 s- ’ of photosynthetically active radiation (PAR) was provided by fluorescence tubes; levels were determined with a Biospherical Instrument Model QSL 100 radiometer. The light-dark cycle and PAR level were chosen based on field measurements (Robineau et al., 1997-this issue). Subsamples were taken on day 1, 2, 6, 12 and 16 of the incubation for silicate, nitrate, nitrite, phosphate, chlorophyll a and pheopigments, and particulate organic carbon and nitrogen. Subsamples were taken on the last three days for 13C analysis.
lated from duplicate samples for all analyses.
3. I. Vertical profiles silicate
of temperature,
salinity and
The slope of the pycnocline at St. Kl was the most pronounced ( - 30.36 psu m- ’) on the transect line (Pig. 2). The effect of surface freshwater runoff was noted to St. K3 while little effect could be seen at St. K4 and K5. Lower salinity water appeared again at St. K6, which was influenced by the fresh-
III STANCE (km) 0
STATI CN Kl i
K2
3
2
1
K3
E
K4
4
KS 1
K6
--_____.32----‘---
Fig. 2. Vertical distribution of salinity almg the line between
the
mouth of Hamasaroma River and Second Channel on 24 1992. E indicates the approximate location of the experimental site. The first sampling depth (0.5 m) corresponded approximately to 0.3 m below the ice-water interface. Shaded bar indicates sea ice.
S. Tquclti et al. / Jourrwl of Marine S_wtemsI I (1997) 45-52
48
water runoff in the surface layer that moved counterclockwise along the east coast from the mouth of Hamasaroma River. One of the typical vertical profiles of temperature and salinity at St. E on 27 February, which corresponded to the beginning of melting season as determined by Hudier et al. (1995), showed salinity > 30 psu with a low temperature of - 1.35”C under the sea ice (Fig. 3A). As the season progressed, the water temperature under the sea ice increased to -0.8”C while the salinity near the ice-water interface was close to 20 psu on 24 March (Fig. 3Bl. This indicated that salinity increased with depth between 0.5 and 1.0 m and that there was uniform salinity (32 psu) below 3.0 m. Under such situations, a low salinity water lens has often been observed under the sea ice (Shirasawa et al., 1997-this issue). Minimum values for salinity were observed around 01 :OOon both occasions when the slope of the pycnocline and salinity at 0.5 m were plotted against the time of day (Fig. 4). This may indicate a die1 variability in the slope of the pycnocline, suggesting that the stability of the low salinity lens would vary with the time of day. However, the pycnocline slopes observed at St. E were less pronounced than those observed at St. Kl near the mouth of Hamasaroma River (Fig. 2) while the slope of the pycnocline in February was less pronounced than that in March. This indicated that the effect of freshwater runoff was limited to the 27 FEBRUARY, 1218 TEMPERATURE (“c) -1.4 -I,2 -1 -0.8.0,6 -0.4 -0.2
24 MARCH, 0957 TEMPERATURE (“c) 0
-1.4-1.2-1 -0.5.0,6-0.4-0.2 0 8
QL, 20
,
,
,
,
,
,
,
22
24
20
25
30
32
34
SALINITY
(psu)
0
SALINITY
(psu)
Fig. 3. Vertical profiles of temperature (@I and salinity (RI ) at St. E on 27 February (A) and on 24 March (B). Shaded bar indicates sea ice.
TIME 17
21
(h) 26-27 FEBRUARY 01
05
09
53
17
21
0
40
4
30
A Ii 33 -10
20
t! s
10
-iii B ; Iz zj v)
cn -20
0
TIME
(h) 23-24 MARCH
el changes in the pycnocline slope (0)
and in the
23-24 March (B) 1992. Arrows on the horizontal axis indicate the time when the profiles shown in Fig. 3 were taken.
top of water column in March while it affected the whole water column in February. The most pronounced slope was observed at 19:18 on 27 February and 1O:OOon 24 March while the least pronounced slopes were observed from 20:00 to 07:OOon 26-27 February and at 13:00 on 23 March. The salinity at 0.5 m ranged from 11.6 1 psu (23:20,26 February) to 30.88 psu (10: 17, 27 February) and from 11.84 psu (01:59, 23 March) to 23.51 psu (09:57, 23 March). Silicate concentration was relatively uniform with depth below 1 m (Fig. 5). However, silicate concentration at 2.5 m increased from < 10 FM on 19 February to a high of > 40 @4 on 9 March. It decreased to < 30 p,M on 13 March and remained at this level until the end of the observation period (20 March). Although these observations were from 1 m and deeper, we assumed that silicate concentrations above 1 m were low near the ice-water interface because of the presence of low salinity water.
able I Size class distribution of cells containing chloropby~~ a (%) with no silica (control) an 54 p&l of silicate during the I6-day experiment 2.5
ay Control
0
1 6 12 16
f8fJ-
54 p
> 10 IO-2 2-0.2
> 10 LO-2 2-0.2
> 10 10-2
2-0.2
52.0 57.0 93.0 90.0 85.0
52.0 56.0 91.0 96.0 97.0
52.0 56.0 92.0 91.0 95.0
8.70 7.30 0.90 0.60 0.70
39.0 8.70 37.0 6.50 6.5 0.45 8.4 8.40 12.0 3.30
39.0 37.0 6.6 3.5 2.2
8.70 6.60 2.10 0.36 0.85
39.0 36.0 7.1 8.4 4.3
Cell size units are pm. 7.5
The initial chlorophyll a come Fig. 5. Temporal variation of silicate (~.LM) under the sea ice Ia~r;nn frnrn 91 G.hn,,xn, tr 25 .Ai,.rd. lQn7 I.. .._. D thn ._._ rner;,-d _...._ -- - . . . _ - - _ ___... 2, ..r.-.i .,I_.
sampling dates and depths. Melting period started on 28 February.
3.2. Conditions during incubation
Nitrate and phosphate concentrations were never below 100 and 26 t.~M, respectively, throughout the incubations. The three initial silicate concentrations were 0, 18 and 54 @W. The silicate concentrations in the latter two treatments gradually decreased during the incubation, but by less than 10% of the initial values.
ments showed a further decrease: the control (no added silicate) decreased steadily to less than 2 mg E a m -3 while the two experimental bottles showed more gradual decreases. The pigment ratios (chlorophyll a:chlorophyll a + pheopigments) were always higher than 0.9 even though they decreased
Table 2 Particulate organic carbon and nitrogen (POC, PON; mg rns3 ) and chlorophyll u (CHL a; mgm - ’) with enrichments of zero (control), 18 pM and 54 f.t,kf of silicate on day 6, 12 and 16 POC
PON
C:N
CHL a
925 510
134 46
6.9 Il.0
37.0 16.0
25 30
Control 6 399 12 360 16 408
30 28 36
13.0 13.C 12.0
7.4 1.6 1.3
54 230 310
18 pm 6 12 16
384 405 483
29 37 50
t-3 11-d 9.7
13.0 8.8 6.0
30 46 80
.% c.Lnz 6 446 12 443 16 482
39 46 58
12.0
12.0 11.0 7.9
36 41 61
Day
0 pfvlSILICATE i8 pM SILICATE
Initial 0
1
C:CHL a
54 @l SILICATE
10 1
OJI
II
0
1
I,
2
3
II
4
5
II
6
7
Ii
8
9
I#rlll 10 11 12 13 14 15 16
DAYS Fig. 6. Temporal variations of chlorophyll a concentration (mgm-‘) in the experimental bottles with enrichments of zero, 18 f.t&j and 54 jk1”I silicate.
9.6 8.2
1
C:N and C:CHL a indicate mass ratios of carbon to ~~NYI to chlorophyll Q, respectively.
ni@Ggen
and
Table 3 Photosynthetic activity, average concentration of chlorophyll u. and photosynthetic rate with enrichments of zero (control), 18 FM and 54 *UM silicate on day 6. 12 and 16 Photosynthetic Average Photosynthetic Day rate chlorophyll u activity (mg CHL n [mg C (mg (mg C m-3 h-i) CHL a)--‘h-‘j m-“) Control 6 I2 16 18 j.M 6 12 16 54 /.&IV 6 12 16
< 0.01 0 0
12.0 4.5 1.4
< 0.0008 0
increased in the 54 FM treatment (Table 3). Almost no photosynthetic activity was observed in the control sample on any of the three observation days while both samples with silicate enrichment showed photosynthetic activity (Table 3). The increase of the photosynthetic rate with time, which was significantly different from zero ( p < O.OS), suggests that photosynthesis of ice algae was most limited by silicate at day 16.
.
0
4. Discussion 1.20 0.61 0.81
14.0 11.0 1.4
0.083 0.056 0.110
1.40
14.0 12.0 9.4
0.100
1.40
1.60
0.120 0.170
with time. The size distribution of the cells containing the chlorophyll a showed a drastic change with time (Table 1). The size group larger than 10 pm made up 52% of the total chlorophyll a but increased its proportion to as much as 97% with silicate enrichment. The initial concentrations of particulate organic carbon (POC) and nitrogen (PON) were 925 and 134 mgm-‘, respectively, and decreased to 5 10 and 46 mg m’-” within the first day (Table 2). POC and PON generally showed patterns of variation similar to that of chlorophyll a. The carbon:chlorophyll a ratio (C:CHL a) increased from 25 to 30 during the O-1 day period in all three experiments, but showed lower values with increasing concentration of silicate (Table 2). The highest C:CHL a ratio was 3 10 and was observed on day 16 in the control incubation. The carbon: nitrogen ratio (C:N) increased from 6.9 to 11 within the first day then tended to decrease wtth ttme and wtth increasing concentration of silicate (Table 2). The lowest C:N ratio was 8.2 in the sample enriched with 54 @4 of silicate on day 16. 3.3. Photosynthetic activity The photosynthetic activity decreased from day 6 to day 16 in the control and 18 p&Z treatments but
Ice algae developed concentrations greater than 1500 mg CHL crm -3 during our study period in Saroma-ko Lagoon (Robineau et al., 1997-this issue), which corresponds to 75 mg CHL am-’ in the bottom 2 cm of sea ice. Ice began melting on 28 February 1992 (Hudier et al., 1995), producing low salinity water immediately below the ice. Meltwater may have lower levels of silicate since sea ice has lower silicate concentrations than the surface water (Cota et al., 1990; Nelson and Treguer, 1992). In Saroma-ko Lagoon, there was another layer with intermediate salinity (< 20 psu) and high silicate concentration ( > 20 FM) between the meltwater and the bottom water (deeper than 7.5 m). Independent determination of silicate concentration near the bottom (9 m) showed higher concentrations than those at 7.5 m during the melting period (Taguchi et al., 1994). During the melting pertod, the silicate concentration in the bottom water was > 20 pJ4 and salinity was 32 psu (Figs. 2 and 5); this water originated from the Sea of Okhotsk. The intermediate salinity-high silicate water was formed by mixing of meltwater with runoff from the Hamasaroma River. The duration of the low salinity-low silicate lenses formed by meltwater may be controlled by advection of seawater from the water column (Hudier et al., 1995; Shirasawa et al., 1997-this issue). No measurements were made during the present study to determine the stability of these water lenses. However, the bottom surface of ice is not always flat and has irregular structures (Shirasawa et al., 1997-this issue); depression areas are quite often observed underneath the ice that can trap the low salinity-low silicate lenses (Shirasawa et al., 1993). The vertical profile of salinity under the sea ice suggests the
affected by low silicate than those in the > 10 size class (Table I), (3) silicate addition cause increase in the relative abundance of > 10 pm size class of ice algae on day 16 (Table l), and (4) low silicate concentration reduce of ice algae in low salinity wate ever, once the ice algae encounters intermediate salinity but high silicate runoff water outside the low salinity-low silicate lenses, the affected cells could survive, as suggested by the increase of photosynthetic rate with enrichment of 54 I_LMsilicate (Table 3). Microscopic observation of materials collected by sediment traps during the study period revealed a paucity of fecal pellets and degraded ice algal cells (Michel et al., 1997-this issue). These direct observations may argue that transformation of ice algal cells into large, rapidly sinking particles was mainly achieved without the cells passing through animal guts. Nutrient depletion may cause the ice algal cells to become sticky and foml aggregates (Smetacek, if-me\ T ~~~Plarntpc1nnpp V..V_thp _.._ 1703J. 1his pr~css would be ub+tilr.ULVU ice algae are released into the water column and could significantly increase the rate of sedimentation (Riebesell et al., 1991). The low salinity-low silicate lenses produced by melting ice could accelerate the aggregation process. During this process, as observed in the experimental bottles between day 0 and day 6, increases in the C:N and C:CHL a ratios were observed (Table 2). The occurrence of low salinitylow silicate lenses, controlled by water stratification z-A--- _ ~11 I” iempw~i vabi&i;Ly and tidal mix@, rrz; ~rruu~~ in the vertical flux of the aggregates under the sea-ice environment in addition to the spatial variability in species composition caused by the salinity gradient (Poulin et al., 1983) and silicate deticiency, (2) biomass patchiness caused by heterogeneity of the under-ice surface due to physical factors including salinity (Gosselin et al., 1986), and (3) variations in ice algal biomass and growth resulting directly ??
esearch Institute, el, and M. Fortier Hoshino was greatly appreciated. Nutrient analysis was performed by II. Kasai. The analysis of 13C samples was conducted under the guidance of T. Sasaki at the National Institute of Fisheries Science. This is contribution (B-580) from Hokkaido National Fisheries Research Institute.
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Guillard, R.R.L. and Ryther, J.H., 1962. Studies of marine planktonic diatoms. I. C~clotefla nana Hustedt and Detondu corn femaceu (Cleve) Gran. Can. J. Microbial., 8: 229-239. Hahn-Hansen, 0.. Lorenzen, C.J., Holmes, R.N. and Strickland, J.D.H., 1965. Fluorescence determination of chlorophyll. J. Cons. Penn. Int. Explor. Mer, 30: 3-15. Hudier, E.J.-J., Ingram, R.G. and Shirasawa, K., 1995. Upward flushing: effects of an upward flux of sea water through first year ice. Atmos.-Ocean, 33: 569-580. Ingram, R.G. and Larouche, P., 1987. Variability of an under-ice river plume in Hudson Bay. J. Geophys. Res., 92: 9541-9547. Lake, R.A. and Lewis, E.L., 1970. Salt rejection by sea ice during growth. J. Geophys. Res., 75: 583-597. Legendre, L., Martineau, M.-J., Therriault, J.-C. and Demers, S., 1992. Chlorophyll a biomass and growth of sea-ice microalgae along a salinity gradient (southeastern Hudson Bay, Canadian Arctic). Polar Biol., 12: 445-453. Lepage, S. and Ingram, R.G., 1991. Variation of upper layer dynamics during breakup of the seasonal ice cover in Hudson Bay. J. Geophys. Res., 96: 12,711-12,724. Michel, C., Legendre, L. and Taguchi, S., 1997. Coexistence of microalgal sedimentation and water column recycling in a seasonally ice-covered ecosystem (Saroma-ko Lagoon, Sea of Okhotsk, Japan). J. Mar. Syst., 11: 133-148. Morel, F.M.M., Rueter, J.G., Anderson, D.M. and Guillard, R.R.L., 1979. Aquile: A chemically defined phytoplankton culture medium for trace metal studies. J. Phycol., 15: 135141. Nelson, D.M. and Treguer, P., 1992. Role of silicon as a limiting nutrient to Antarctic diatoms: evidence from kinetic studies in the Ross Sea ice-edge zone. Mar. Ecol. Prog. Ser., 80: 255264. Poulin, M., Cardinal, A, and Legendre. L., 1983. RBsponse d’une communaut6 de diatomdes de glace B un gradient de salinid (baie d’Hudson1. Mar. Biol., 76: 19 l-202. Rand, J. and Mellor, M., 1985. Ice-coring augers for shallow depth sampling. USA Cold Region Res. Eng. Lab,, CRREL
Rep. 85-21, 22 pp. Riebesell, U., Schloss, L. and Smetacek, VS., 1991. Aggregation of algae released from melting sea ice: implications for seeding and sedimentation. Polar Biol., 11: 239-248. Robineau, B., Legendre, L,, Kishino, M. and Kudoh, S., 1997. Horizontal heterogeneity of microalga! biomass in the first-y@%
sea ice of Saroma-ko Lagoon (Hokkaido, Japan). J. Mar. Syst., 11: 81-91. Runge, J.A. and Ingram, R.G., 1991. Under-ice feeding and die1 migration by the planktonic copepods Culunw gfucifis and fseudoculun~~smirxrtus in relation to the ice algal production cycle in southern Hudson Bay, Canada. Mar. Biol., 108: 217-225. Satoh, H., Yamaguchi, Y., Kokubun, K. and Aruga, Y., 1985. Application of infrared absorption spectrometry for measuring the photosynthetic production of phytoplankton by the stable ‘jC isotope method. La Mer, 23: 171-176. Shirasawa, K., Ikeda, M., Takatsuka, T., Ishikawa, M., Aota, M., Ingram, R.G., Betanger, C., Peltola, P., Takahashi, M., Matsuyama, M., Hudier, E., Fujiyoshi, Y., Kodama, Y. and Ishikawa, N., 1993. Atmospheric and oceanographic data report for Saroma-ko Lagoon of the SARES @aroma-Resolute Studies) Project, 1992. Low Temp. Sci., Ser. A, 52: 69-167. Shirasawa, K., Ingram, R.G. and Hudier, E.J.-J., 1997. Oceanic heat fluxes under thin sea ice in Saroma-ko Lagoon, Hokkaido, Japan. J. Mar. Syst., 11: 9- 19. Smetacek, V.S., 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar. Biol., 84: 239-251. Smith, R.E.H., Harrison, W.G., Harris, L.R. and Herman, A.W., 1990. Vertical line structure of particulate matter and nutrients in sea ice of the High Arctic. Can. J. Fish. Aquat. Sci., 47: 1348-1355. Suzuki, R. and Ishimaru, T., 1990. An improved method for the determination of phytoplankton chlorophyll using N,N-Dimethylformamide. J. Oceanogr. Sot. Jpn., 45: 190-194. Taguchi, S., Hirata, J.A. and Laws, E.A., 1987. Silicate deficiency and lipid synthesis of marine diatoms. J. Phycol., 23: 260-267. Taguchi, S., Demers, S., Fortier, L., Fortier, M., Fujiyoshi, Y., Hattori, H.. Kasai, H., Kishino, M S., Lcgendre, L., .-., Kudoh, _L McGiness, F., Michel, C., Sime-Ngando, T., Robineau, B., Saito, H., Suzuki, Y., Takahashi, M., Therriault, J.-C., Aota, M., Ikeda, M., Ishikawa, M., Takatsuka, T. and Shirasawa, K,, 1994. Biological data report for the Saroma-ko site of the SARES @aroma-Resolute Studies) Project, February-March, 1992. Low Temp. Sci., Ser. A, 53: 67-163. Werner, D., 1970. Productivity studies on diatom cultures. Helgol. Wiss. Meeresunters., 20: 97-103.
b 9
’ Hokkaido National Fisheries Research Institute. Kushiro, Hokkaido 085, Japan ’ Biology Department, Uniljersity qf Waterloo, Waterloo, Ont. N2L 361, Canada ’ Sea Ice Research Laboratoq, Hokkaido Vvirersity, Monbetsu, Hokkaidc 094. Japan
Received 18 September 1994; accepted 11October 1995
Abstract
The response of ice algae to low salinity was determined at three levels of silicate enrichment during the winter of 1992 in Saroma-ko Lagoon, Hokkaido, Japan. Regardless of the silicate concentration, the chlorophyll a content decreased by 50% of its initial value within the first day of exposure to low salinity water (22 psu) and continued to decrease gradually thereafter. The degree of decrease after the first day was a function of silicate concentration. The size distribution of the ice algae at the beginning of the incubation was 52% in the size class > 10 p,rn, 39% in 10-2 pm and 9% in 2-0.2 pm. Within two weeks of silicate enrichment, the 2-0.2 pm fraction decreased to less thti 1% while the > 10 pm fraction increased to more than 90%. Low salinity and low silicate concentrations reduced the chlorophyll a biomass and photosynthetic activity. Silicate enrichmecrts, ewn st th e !ow s&&y, e&nsced phottijynthctic rrctivity cgd the relative abundance of the > 10 pm cells. Our results suggest that ice algae may not survive if trapped in the low salinity lens that is present immediately below the ice during melting because of possible osmotic damage associated with silicate deficiency.
However, ice algal cells may recover from the damage when they sink into the high salinity and silicate-rich underlying water in Saroma-ko Lagoon. The ecological role of low salinity water is discussed in relation to vertical flux of ice algae. Keywords: salinity; silicate; deficiency; cell size; less saline lenses; photosynthesis
1. Introduction Growth of ice algae is vigorous in brine pockets even at salinities as high as 50 psu (Arrigo and Sullivan, 1992). As the ice melts, it produces a low salinity lens immediately below the sea ice. Ice algae
* Corresponding author. Present address: Lab. of Biological Oceanography, Dep. of Rioengineering, Soka University Hachioji, Tokyo 192, Japan. Phone/fax: $1 426 91 8002. E-mail: [email protected].
that are flushed into this layer during melting may go through a drastic change in their physiological condition, particularly in the vicinity of freshwater runoff, where the ice algae are even more likely to encounter a wide range of salinities (Ingram and Larouche, 1987; Lepage and Ingram, 1991; Runge and Ingram, 1991). The presence of ~~~~~entsin brine pockets 0 sea ice is essential for ice algal growth. Unfortunately, it is difficult to dire&y determine nutrient concentrations in brine pockets due to their small size (less than 1 mm diameter; Lake and Lewis,
0924-7963/97/$17.00 Copyright 0 1997 Elsevier Science B.V. All rights reserved. PII SO924-7963(96)00026-7
46
S. Tqpchi et al. / Jowxnl of Mmhe Systems 11 f 1997145-52
1970). However, Smith et al. (1990) observed a close correspondence of dissolved inorganic nutrients (except for silicate) to the approximately exponential vertical increase in the chlorophyll a concentration in fine sections of bottom sea ice in the High Arctic. Nutrient contents of sea ice in Saroma-ko Lagoon were not as low as those reported for the Canadian Arctic (Taguchi et al., 1994), but regardless of the varying amounts of nutrients in sea ice (Smith et al., 1990), the nutrient concentrations in the low salinity lenses are low compared to those in the underlying water column (Cota et al., 1990). The duration of this low salinity and silicatelimited water layer may be a function of the advection of seawater from the water column. When a stable condition lasts longer than one day, low salinity and silicate deficiency are expected to affect the physiology of ice algae at the ice-water interface since silicate deficiency may occur within 24 h (Badour, 1968; Werner, 1970; Taguchi et al., 1987) and may subsequently play a significant role in competition between species (Egge and Aksnes, 1992). Saroma-ko Lagoon is located at the northeast coast of Hokkaido, Japan. It is highly eutrophic with the annual gross primary production by phytoplankton estimated to be 780 g Cm“ yr- ’ (Fuji, 1979). During winter, sea ice covers almost the entire lagoon. A dense layer of ice algae develops at the bottom of the ice by early spring while phytoplankton in the water column is scarce, Freshwater input, which is mainly supplied by two major rivers, causes a reduction of salinity to less than 32 psu. A siliconrich layer of freshwater from the Hamasaroma River underlies the low salinity-low silicate lenses that form as a result of melting sea ice (Taguchi et al., 1994). Therefore, once the ice algae in Saroma-ko Lagoon are released from the sea ice, they may experience the low salinity-low silicate lenses, then the intermediate salinity but nutrient-rich runoff water, and finally the nutrient-rich and saline bottom water. Little is known about the physiological changes in ice algal cells during passage between these water layers. The purpose of the present study was to test the hypothesis that less saline water decreases the growth rate of ice algae and that the extent of the decrease or possible recovery is a function of the silicate
enrichment. The present experiment was designe examine the effect of less saline water in combination with silicate enrichment during the period of ice melt in Saroma-ko Lagoon, Hokkaido, Japan.
2. Materials and metho On three occasions in the winter of 1992, temperature and salinity under the sea ice were determined with a Sea Bird memory CTD model Seacat 19 at St. E. 2 km from the laboratory (Fig. 1). Die1 variability in temperature and salinity was determined hourly, if possible, from 17;08 on 26 February to 19: 18 on 27 February and from 13: 12 on 23 March to 1257 on 24 March. In addition, spatial variability in temperature and salinity was determined on 11 March to study the effect of freshwater runoff from the Hamasaroma River. The observation stations samSea of Okhotsk
Fig. 1. Map of sampling locations on the ice site in Saroma-ko Lagoon, Hokkaido, Japan. SRC’A is a laboratory of the Saroma Research Center for Aquaculture. The small embayment at the top right is not open to the Sea of Okhotsk.
pled on this occasion
Temperature and sali 0.5 m depth (0.3 m from the bottom ice) to avoid the wate of the sampling hole. for the linear increase m to estimate the slope of pycnocline. Water samples were collected with Niskin bottles at 1, 2.5, 5 and 7.5 m depth through the ice hole at St. E during the period from 19 February to 20 March. Subsamples for silicate an through a membrane filter (type - 20°C until processing. Two ice core samples were collected on ary at St. E with an ice-core sampler ( 1985). The sea ice was 20 cm thick. The 2 to 3 cm were scraped carefully into a dark bottle filled with filtered seawater ( glass fiber filter, collected at 1 m depth) and allowed to melt slowly at - 1.8”C(Garrison and Buck, 1986). The resulting suspension was 10% melted ice and 90% seawater, with a salinity of about 30 psu. Ninety ml of this suspension were diluted to 3000 ml with artificial seawater (Morel et al., 1979) giving a final salinity of about 22 psu. This salinity was close to that at the ice-water interface at the study site (Shirasawa et al., 1997-this issue). These suspensions were enriched with an f/2 medium (Guillard and Ryther, 1962) that lacked silicate. The first bottle did not receive any silicate but had a trace amount from the ice algal suspension. The second and third bottles had 18 and 54 pJ4 of silicate, respectively. Incubation was started with the inoculation of 30 mg 13C labeled sodium bicarbonate. A light-dark cycle (11 h:13 h) with 10 pErnm2 s- ’ of photosynthetically active radiation (PAR) was provided by fluorescence tubes; levels were determined with a Biospherical Instrument Model QSL 100 radiometer. The light-dark cycle and PAR level were chosen based on field measurements (Robineau et al., 1997-this issue). Subsamples were taken on day 1, 2, 6, 12 and 16 of the incubation for silicate, nitrate, nitrite, phosphate, chlorophyll a and pheopigments, and particulate organic carbon and nitrogen. Subsamples were taken on the last three days for 13C analysis.
lated from duplicate samples for all analyses.
3. I. Vertical profiles silicate
of temperature,
salinity and
The slope of the pycnocline at St. Kl was the most pronounced ( - 30.36 psu m- ’) on the transect line (Pig. 2). The effect of surface freshwater runoff was noted to St. K3 while little effect could be seen at St. K4 and K5. Lower salinity water appeared again at St. K6, which was influenced by the fresh-
III STANCE (km) 0
STATI CN Kl i
K2
3
2
1
K3
E
K4
4
KS 1
K6
--_____.32----‘---
Fig. 2. Vertical distribution of salinity almg the line between
the
mouth of Hamasaroma River and Second Channel on 24 1992. E indicates the approximate location of the experimental site. The first sampling depth (0.5 m) corresponded approximately to 0.3 m below the ice-water interface. Shaded bar indicates sea ice.
S. Tquclti et al. / Jourrwl of Marine S_wtemsI I (1997) 45-52
48
water runoff in the surface layer that moved counterclockwise along the east coast from the mouth of Hamasaroma River. One of the typical vertical profiles of temperature and salinity at St. E on 27 February, which corresponded to the beginning of melting season as determined by Hudier et al. (1995), showed salinity > 30 psu with a low temperature of - 1.35”C under the sea ice (Fig. 3A). As the season progressed, the water temperature under the sea ice increased to -0.8”C while the salinity near the ice-water interface was close to 20 psu on 24 March (Fig. 3Bl. This indicated that salinity increased with depth between 0.5 and 1.0 m and that there was uniform salinity (32 psu) below 3.0 m. Under such situations, a low salinity water lens has often been observed under the sea ice (Shirasawa et al., 1997-this issue). Minimum values for salinity were observed around 01 :OOon both occasions when the slope of the pycnocline and salinity at 0.5 m were plotted against the time of day (Fig. 4). This may indicate a die1 variability in the slope of the pycnocline, suggesting that the stability of the low salinity lens would vary with the time of day. However, the pycnocline slopes observed at St. E were less pronounced than those observed at St. Kl near the mouth of Hamasaroma River (Fig. 2) while the slope of the pycnocline in February was less pronounced than that in March. This indicated that the effect of freshwater runoff was limited to the 27 FEBRUARY, 1218 TEMPERATURE (“c) -1.4 -I,2 -1 -0.8.0,6 -0.4 -0.2
24 MARCH, 0957 TEMPERATURE (“c) 0
-1.4-1.2-1 -0.5.0,6-0.4-0.2 0 8
QL, 20
,
,
,
,
,
,
,
22
24
20
25
30
32
34
SALINITY
(psu)
0
SALINITY
(psu)
Fig. 3. Vertical profiles of temperature (@I and salinity (RI ) at St. E on 27 February (A) and on 24 March (B). Shaded bar indicates sea ice.
TIME 17
21
(h) 26-27 FEBRUARY 01
05
09
53
17
21
0
40
4
30
A Ii 33 -10
20
t! s
10
-iii B ; Iz zj v)
cn -20
0
TIME
(h) 23-24 MARCH
el changes in the pycnocline slope (0)
and in the
23-24 March (B) 1992. Arrows on the horizontal axis indicate the time when the profiles shown in Fig. 3 were taken.
top of water column in March while it affected the whole water column in February. The most pronounced slope was observed at 19:18 on 27 February and 1O:OOon 24 March while the least pronounced slopes were observed from 20:00 to 07:OOon 26-27 February and at 13:00 on 23 March. The salinity at 0.5 m ranged from 11.6 1 psu (23:20,26 February) to 30.88 psu (10: 17, 27 February) and from 11.84 psu (01:59, 23 March) to 23.51 psu (09:57, 23 March). Silicate concentration was relatively uniform with depth below 1 m (Fig. 5). However, silicate concentration at 2.5 m increased from < 10 FM on 19 February to a high of > 40 @4 on 9 March. It decreased to < 30 p,M on 13 March and remained at this level until the end of the observation period (20 March). Although these observations were from 1 m and deeper, we assumed that silicate concentrations above 1 m were low near the ice-water interface because of the presence of low salinity water.
able I Size class distribution of cells containing chloropby~~ a (%) with no silica (control) an 54 p&l of silicate during the I6-day experiment 2.5
ay Control
0
1 6 12 16
f8fJ-
54 p
> 10 IO-2 2-0.2
> 10 LO-2 2-0.2
> 10 10-2
2-0.2
52.0 57.0 93.0 90.0 85.0
52.0 56.0 91.0 96.0 97.0
52.0 56.0 92.0 91.0 95.0
8.70 7.30 0.90 0.60 0.70
39.0 8.70 37.0 6.50 6.5 0.45 8.4 8.40 12.0 3.30
39.0 37.0 6.6 3.5 2.2
8.70 6.60 2.10 0.36 0.85
39.0 36.0 7.1 8.4 4.3
Cell size units are pm. 7.5
The initial chlorophyll a come Fig. 5. Temporal variation of silicate (~.LM) under the sea ice Ia~r;nn frnrn 91 G.hn,,xn, tr 25 .Ai,.rd. lQn7 I.. .._. D thn ._._ rner;,-d _...._ -- - . . . _ - - _ ___... 2, ..r.-.i .,I_.
sampling dates and depths. Melting period started on 28 February.
3.2. Conditions during incubation
Nitrate and phosphate concentrations were never below 100 and 26 t.~M, respectively, throughout the incubations. The three initial silicate concentrations were 0, 18 and 54 @W. The silicate concentrations in the latter two treatments gradually decreased during the incubation, but by less than 10% of the initial values.
ments showed a further decrease: the control (no added silicate) decreased steadily to less than 2 mg E a m -3 while the two experimental bottles showed more gradual decreases. The pigment ratios (chlorophyll a:chlorophyll a + pheopigments) were always higher than 0.9 even though they decreased
Table 2 Particulate organic carbon and nitrogen (POC, PON; mg rns3 ) and chlorophyll u (CHL a; mgm - ’) with enrichments of zero (control), 18 pM and 54 f.t,kf of silicate on day 6, 12 and 16 POC
PON
C:N
CHL a
925 510
134 46
6.9 Il.0
37.0 16.0
25 30
Control 6 399 12 360 16 408
30 28 36
13.0 13.C 12.0
7.4 1.6 1.3
54 230 310
18 pm 6 12 16
384 405 483
29 37 50
t-3 11-d 9.7
13.0 8.8 6.0
30 46 80
.% c.Lnz 6 446 12 443 16 482
39 46 58
12.0
12.0 11.0 7.9
36 41 61
Day
0 pfvlSILICATE i8 pM SILICATE
Initial 0
1
C:CHL a
54 @l SILICATE
10 1
OJI
II
0
1
I,
2
3
II
4
5
II
6
7
Ii
8
9
I#rlll 10 11 12 13 14 15 16
DAYS Fig. 6. Temporal variations of chlorophyll a concentration (mgm-‘) in the experimental bottles with enrichments of zero, 18 f.t&j and 54 jk1”I silicate.
9.6 8.2
1
C:N and C:CHL a indicate mass ratios of carbon to ~~NYI to chlorophyll Q, respectively.
ni@Ggen
and
Table 3 Photosynthetic activity, average concentration of chlorophyll u. and photosynthetic rate with enrichments of zero (control), 18 FM and 54 *UM silicate on day 6. 12 and 16 Photosynthetic Average Photosynthetic Day rate chlorophyll u activity (mg CHL n [mg C (mg (mg C m-3 h-i) CHL a)--‘h-‘j m-“) Control 6 I2 16 18 j.M 6 12 16 54 /.&IV 6 12 16
< 0.01 0 0
12.0 4.5 1.4
< 0.0008 0
increased in the 54 FM treatment (Table 3). Almost no photosynthetic activity was observed in the control sample on any of the three observation days while both samples with silicate enrichment showed photosynthetic activity (Table 3). The increase of the photosynthetic rate with time, which was significantly different from zero ( p < O.OS), suggests that photosynthesis of ice algae was most limited by silicate at day 16.
.
0
4. Discussion 1.20 0.61 0.81
14.0 11.0 1.4
0.083 0.056 0.110
1.40
14.0 12.0 9.4
0.100
1.40
1.60
0.120 0.170
with time. The size distribution of the cells containing the chlorophyll a showed a drastic change with time (Table 1). The size group larger than 10 pm made up 52% of the total chlorophyll a but increased its proportion to as much as 97% with silicate enrichment. The initial concentrations of particulate organic carbon (POC) and nitrogen (PON) were 925 and 134 mgm-‘, respectively, and decreased to 5 10 and 46 mg m’-” within the first day (Table 2). POC and PON generally showed patterns of variation similar to that of chlorophyll a. The carbon:chlorophyll a ratio (C:CHL a) increased from 25 to 30 during the O-1 day period in all three experiments, but showed lower values with increasing concentration of silicate (Table 2). The highest C:CHL a ratio was 3 10 and was observed on day 16 in the control incubation. The carbon: nitrogen ratio (C:N) increased from 6.9 to 11 within the first day then tended to decrease wtth ttme and wtth increasing concentration of silicate (Table 2). The lowest C:N ratio was 8.2 in the sample enriched with 54 @4 of silicate on day 16. 3.3. Photosynthetic activity The photosynthetic activity decreased from day 6 to day 16 in the control and 18 p&Z treatments but
Ice algae developed concentrations greater than 1500 mg CHL crm -3 during our study period in Saroma-ko Lagoon (Robineau et al., 1997-this issue), which corresponds to 75 mg CHL am-’ in the bottom 2 cm of sea ice. Ice began melting on 28 February 1992 (Hudier et al., 1995), producing low salinity water immediately below the ice. Meltwater may have lower levels of silicate since sea ice has lower silicate concentrations than the surface water (Cota et al., 1990; Nelson and Treguer, 1992). In Saroma-ko Lagoon, there was another layer with intermediate salinity (< 20 psu) and high silicate concentration ( > 20 FM) between the meltwater and the bottom water (deeper than 7.5 m). Independent determination of silicate concentration near the bottom (9 m) showed higher concentrations than those at 7.5 m during the melting period (Taguchi et al., 1994). During the melting pertod, the silicate concentration in the bottom water was > 20 pJ4 and salinity was 32 psu (Figs. 2 and 5); this water originated from the Sea of Okhotsk. The intermediate salinity-high silicate water was formed by mixing of meltwater with runoff from the Hamasaroma River. The duration of the low salinity-low silicate lenses formed by meltwater may be controlled by advection of seawater from the water column (Hudier et al., 1995; Shirasawa et al., 1997-this issue). No measurements were made during the present study to determine the stability of these water lenses. However, the bottom surface of ice is not always flat and has irregular structures (Shirasawa et al., 1997-this issue); depression areas are quite often observed underneath the ice that can trap the low salinity-low silicate lenses (Shirasawa et al., 1993). The vertical profile of salinity under the sea ice suggests the
affected by low silicate than those in the > 10 size class (Table I), (3) silicate addition cause increase in the relative abundance of > 10 pm size class of ice algae on day 16 (Table l), and (4) low silicate concentration reduce of ice algae in low salinity wate ever, once the ice algae encounters intermediate salinity but high silicate runoff water outside the low salinity-low silicate lenses, the affected cells could survive, as suggested by the increase of photosynthetic rate with enrichment of 54 I_LMsilicate (Table 3). Microscopic observation of materials collected by sediment traps during the study period revealed a paucity of fecal pellets and degraded ice algal cells (Michel et al., 1997-this issue). These direct observations may argue that transformation of ice algal cells into large, rapidly sinking particles was mainly achieved without the cells passing through animal guts. Nutrient depletion may cause the ice algal cells to become sticky and foml aggregates (Smetacek, if-me\ T ~~~Plarntpc1nnpp V..V_thp _.._ 1703J. 1his pr~css would be ub+tilr.ULVU ice algae are released into the water column and could significantly increase the rate of sedimentation (Riebesell et al., 1991). The low salinity-low silicate lenses produced by melting ice could accelerate the aggregation process. During this process, as observed in the experimental bottles between day 0 and day 6, increases in the C:N and C:CHL a ratios were observed (Table 2). The occurrence of low salinitylow silicate lenses, controlled by water stratification z-A--- _ ~11 I” iempw~i vabi&i;Ly and tidal mix@, rrz; ~rruu~~ in the vertical flux of the aggregates under the sea-ice environment in addition to the spatial variability in species composition caused by the salinity gradient (Poulin et al., 1983) and silicate deticiency, (2) biomass patchiness caused by heterogeneity of the under-ice surface due to physical factors including salinity (Gosselin et al., 1986), and (3) variations in ice algal biomass and growth resulting directly ??
esearch Institute, el, and M. Fortier Hoshino was greatly appreciated. Nutrient analysis was performed by II. Kasai. The analysis of 13C samples was conducted under the guidance of T. Sasaki at the National Institute of Fisheries Science. This is contribution (B-580) from Hokkaido National Fisheries Research Institute.
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