Coexistence of microalgal sedimentation and water column recycling in a seasonally ice-covered ecosystem (Saroma-ko Lagoon, Sea of Okhotsk, Japan)

wine Systems 11 ( 1997) 133- 148

a Dbpartement de bioiogre. Unirersltt? iarai, Q&bec, QuG. CIK 7P4, Canada b Soka Un;L crsity, Laborato~ of biological Oceanography, Department of Bioengineering, Faculty of Engineering, 1-236 Tangi-cho, Tokyo

192, Jupun

Received 9 November 1994; accepted 14 September 1995

Abstract

Seasonal variations in under-ice microal,al sedimentation and plankton dynamics in Saroma-ko, a shallow seasonally ice-covered lagoon (Sea of Okhotsk, Hokkaido, Japan), were followed during a 4-week period at the end of winter. At 3-4 day intenals, sediment traps were deployed at three depths from the undersurface of the ice and water column samples were collected. Sampled variables included chlorophyll a (chl a) and pheopigments, particulate organic carbon and nitrogen (POC, PON), cell identification and enumeration, biogenic silica and dissolved inorganic nutrients. POC/PON, POC/chl a and Si/chl a ratios for suspended biomass as well as cell counts showed the presence of a diversified phytoplankton assemblage with a high mi:roheterotrophic biomass. A major peak in clgal sedimentation occurred at the end of the sampling season (chl u tlux LB. 5 mg m - ’ d- ’ ); the sed’ lmented algae included both ice algae and phytoplankton species. Ice algae did not remain suspended in the plankton biomass, but sedimented rapidly upon release from the ice matrix. Results show that Saroma-ko had a rather special food web structure at the end of winter, when both high microalgal export and water column recycling simultaneously occurred under the ice cover.

Keywords: ice; algae; phytoplankton; sedimentation: recycling

1. Introduction followed by massive sedimentation of intact algal

Spring diatom blooms are characteristic of tem- perate and high latitude marine ecosystems. They generally occur upon stabilization of the nutrient-rich surface mixed Iayer, at th ,.R time of increasing irradi- ante, according to the critical depth model of Riley (1942) and Sverdrup ( 1953). Such blooms are often

cells (Smetacek, 1980, 1985) or sinking of fecal pellets from herbivorous zooplankton (Von Bodun- gen et al., 1988; Laws et al., 1988), which lead to a large export of biogenic carbon from the euphotic zone (Legendre, 1990). In contrast, oceanic systems dominated by small phytoplankton (Li et al., 1983; Platt et al., 1983) are thought to sustain a microbial

* Corresponding author. Phone: 418 656 5917. Fax: 418 656 2339. E-mail: [email protected].

web, where recycling of organic matter is high and from which there is little export (Azam et al., 1983; Michaels and Silver, 1988). However, at high lati-

0924-?963/97/$17.00 Copyright 0 1997 Elsevier Science B.V. Ail rights reserved. Pll SO924-7963(96)00034-6

134 C. Mkhel er al. / Jownai cjkrr’tle Systems I I (1997) 133- 148

tudes, low water temperature might significantly re- duce microbial activity (Pomeroy and Deibei, 1986; Pomeroy and Wiebe, 1988).

In ice-covered regions, dense microalgal assemblages are observed either within the sea ice (e.g., Apoiionio, 1961, 1965; Meguro et al., 1967), at the ice-water interface (e.g., Gosseiin et al., 1985; Trembiay et al., 1989; Johnsen and Hegseth, 1991), or at retreating ice edges (Smith and Nelson, 1985, 1986). These assemblages are generally dominated by diatoms (see Homer, 1985; Homer et al., 1992). In some cases, th!z release of ice algae into the water column is thought to initiate the spring development of phytoplankton (Schandeimeier and Alexander, 1981: Smith and Nelson, 1986; Garrison et al., 1987, 1993). Moreover, ice algae constitute a food source for pelagic copepods, which are capable of grazing near the undersurface of the ice (Runge and Ingram, 1988, 1991; Stretch et al., 19881, so that the downward flux of fecal material can represent an important export pathway for the ice algal biomass (Dunbar, 1984; Von Bodungen et al., 1988; Niithig and Von Bodungen, 1989; Trembiay et al., 1989; Gonzalez et al., 1994). It is thus expected that export of primary production in polar waters would mainly occur through sinking of intact ceils and herbivore fecal pellets. Indeed, the rapid sinking of ice algae during the period of ice melt or at retreating ice edges (Apoiionio, 1965; Alexander, 198U, Leventer and Dunbar, 1987; Bathmann et al,, 1991) can result in a large input of fresh organic material to the benthos (Sasaki and Hoshiai, 1986; Carey, 1987; Fukuchi et al., 1988).

The present study was conducted in Saroma-ko Lagoon, which is the southernmost area having seasonal sea ice in the Northern Hemisphere. It has supported a highly productive farming of scallops and oysters for more than 25 years &rata et al., 1991). Given the high benthic production in Saroma- ko, it may be hypothesized, on the one hand, that ice algae are a significant food source for the benthos at the time of ice melt. 0~ the other hand, Saroma-ko Lagoon exhibits less extreme temperature conditions (period of freezing generally < 3 months; Shira- sawa, 1993) than other ice-covered regions of the Northern Hemisphere, which could make it a favor- able area for the development of an under-ice microbial community.

The study was designed to assess the relative importance of recycling versus export processes under the sea ice of Saroma-ko during the period of ice melt. We concurrently investigated the fate of the ice algal biomass and the structure of the planktonic web at the end of the winter, during the period of growth and decline of the bottom ice-algal community.

2. Material and methods

The suspended and sedimenting alga! biomasses under the first -year ice cover of Saroma-ko Lagoon (Sea of Okhotsk, Hokkaido, Japan; Fig. 1) were

Fig. 1. Location of the sampling station in Saroma-‘ko (Sea of Okhotsk, Japan).

135

the ice at 0.5, 2.5 and 7.5 of the ice. These were

a dense stable layer at the bottom of the trap;

total volume of the trap was gently mixed and transferred to a dark plastic bottle for later analysis in a shore laboratory. The traps were redeploye within 30 min. Transportation of samples between the sampling site and the laboratory, by snowmobile, took about 10 min. Prior to analysis, the trap con- tents were prescreened through a 330 pm mesh to remove large swimmers. This procedure did not appear to remove a significant proportion of algal or fecal material from the samples since there was no significant difference in either chlorophyll a (chl a) or pheopigment concentrations when compared to unscreened samples (paired t-test, p > 0.05). Water samples (Niskin bottles) were taken at 0.5, 2.5, 5.0 and 7.5 m below the undersurface of the ice the day after the traps were retrieved.

Analyses for both suspended and sedimenting biomass included chl a and pheopigments, particulate organic carbon and nitrogen (POC, PON), bio- genie silica. and cell enumeration. Concentrations of dissolved nutrients (NO,, NO,, PO,, SiO,) were determined on watp* -_w. samples filtered through 0.45 brn acetate filters, after rinsing the sample with sampled water (using a sterile disposable syringe equipped with a filter holder). Ammonium concentrations were not determined. Samples were kept frozen at - 20°C until analyses on a Bran and Lubbe model TRACCS 800 autoanalyzer according to the methods provided by Strickland and Parsons (1972).

Chlorophyll a and pheopigments were determined fluorometrically with a Turner Designs fluorometer (Helm-Hansen et al., 1965) on subsamples filtered onto Whatman GF/F glass-fiber filters after extrac- tion in 5 ml DMF (n,n-Dimethylformamide) at 4°C in the dark. In the present paper, pheopigment concentrations are given in chl a equivalents (cf. Conover et al., 1986). Other subsamples were filtered onto pre-combusted (24 h at 450°C) Whatman

ore filters using a plas

tion and enumeration were performed under the inverted microscope (Lun et al., 1958); cell volumes were computed using th f0 for each species t measurements. h total of > 450 cells was measured, i.e., 30 cells per species for the most abundant species and only 10 for the least abundant. For each sampling date, calculation of the total cell volume was based on > 95% of the cell numbers.

3. I. Hydrographic conditions

A general description of Saroma-ko Lagoon is given in Shirasawa (1993) and Shirasawa et al. (1993). The lagoon is shallow ( 14.5 m average depth) and is connected to the Sea of Okhotsk by two channels, the largest one accounting for ca. 90% of the total exchange with the sea. The lagoon is also influenced by freshwater discharge from rivers, which keeps the salinity at < 32. In winter, there is formation of first-year ice, but year to year variability in the duration and the extent of the ice cover is high. In 1992, Saroma-ko Lagoon was completely ice- covered from 5 February through 4 April; ice thick- ness varied between 33 and 39 cm during our sampling period (Shirasawa et al., 1993).

Time-series of water level, current speed and direction, temperature, and salinity at the sampling station during February and March 1992 are given in Shirasawa et al. (1993). A two-week record of water levels shows that the tidal cycle seemed to vary from a typically semi-diurnal cycle to a completely diurnal tide over that period. Current speed was low (Z = 4.2 cm s-r ) with little variability. However, sudden changes in current direction at times of diurnal high tides combined with a slow anticlockwise rotation

136 C. Michel et al. / Jomml qf Marine System I I f 1997) 133- 148

suggest that the general circulation pattern was vari- able during the sampling period (Shirasawa et al., 1993). Under-ice water temperature varied little before mid-March, after which it increased slightly to values > - 1.O”C (Shirasawa et al., 1993).

Nutrient concentrations were quite high, so nutrients probably did not limit phytoplankton growth during the spring of 1992 (Fig. 2). Nitrate and nitrite did not decrease to concentrations < 5.0 and 0.15 PM, respectively (Fig. 2a, b), while concentrations of phosphate and silicic acid were consistently > ca. 0.5 and 10 p&f, respectively (Fig. 2c, d). Nutrient concentrations were generally lower during February than March. (Fig. 2). All nutrients increased from surface to bottom in Febmary; the pattern ir;as -re--

0

2.5

5.0

7.5

0

2.5

5.0

g 7.5 6

80 2.5

5.0

7.5

0

2.5

5.0

7.5 19 24 29 5 10 15 20

February March

Fig. 2. Seasonal changes in nutrient concentrations in the water column.

0

2.5

5.0

7.5

0

2.5

5.0

7.5

0

E 2.5 5 8 5.0 0

7.5

0

2.5

5.0

7.5

0

2.5

5.0

7.5

a chi 8 (mg m”>

b Pheopigmmts (mg m9)

d PON (mg ni3)

e Biogenic silica (mg ti’)

19

Fig. 3. Seasonal Gal.

24 29 5 10 15 20

February March

changes in suspended particulate organic mate-

versed in March except for PO,, which showed a roughly uniform vertical distribution (Fig. 2).

3.2. Suspended bibmass

The suspended algal biomass exhibited two dis- tinct peaks in the upper 2.5 m, with surface chl a concentrations up to 10 mg mW3 on 26 February and 6 March (Fig. 3a). These events were followed, after

February and increased significant hitney rank sum test, p

6

6 -- -

4

2

0-T

00 19 24 29 5 10 15 20

February arch Fig. 4. Seasonal changes in composition rataos of the suspended - . biomass. Dashed lines: critical values (c) 6.6 (Redtield et ai., 1963) and (e) 0.12 (Nelson and Gordon, 1982).

Fig. 5. Seasonal changes in the composition of the phytoplankton assemblage: (a) relative numbers and (b) relative volumes. Arith- metic means of all sampling depths. Pennate diatoms: I = Nmiculu spp.; 2 = Fragilaria spp.; 3 = Achnanthes spp.; 4 = other pennate. Centric diatoms: I = Thalussiosira spp.; 2 = Leptocylindrus spp.; 3 = other centric.

< 0.01). Concentrations of POC, PON and biogenic silica exhibited changes parallel to those in chl a (Fig. 3c-e). Rank correlations (Kendall’s T) between these variables and chl a, over all sampled depths a;.d dates, were all significantly different from zero ( p < 0.01).

Fig. 4 shows different ratios, which provide a means for characterizing the suspended particles. Values of POC/chl a and PON/chl a (by weight; Fig. 4a, b) range from ca. 25 to 215 and from 5 to 53, respectively. They do not show any clear seasonal trend but, before the second week of March, the POC/chl a ratio was significantly lower at 0.5 m compared to other depths (Fig. 4a, rank test, p < 0.05). The POC/POY ratio, with an average value of 5.2, was general :y lower (rank test, p < 0.01) than the Redfield ratio of 6.6 (Redfield et al., 1963) (Fig. 4c); the ratio did not show any signifi- a~-* -rndq+;nn -rith ~ith~r time 0~ &+h (Friedman’s *_=a&; f a$=&‘-li_*ig ** ii*, ____=_ _____ _ two-way analysis of variance by ranks, p > 0.05).

138 C. Micltel et al. / Jmtrnal of Amine Systems I I (I 997) 133-148

spp. and Achnanthes spp., accounted for ca. 20 to 30% of cell numbers and showed highest proportions on 6 and 17 March. Naked flagellates (mostly < 20 pm) and dinoflagellates together comprised ca. 25% (median 23%; range 1 l-29%) of cell numbers (Fig. 5a). On a volume basis, the distribution pattern of

February March

Fig. 6. Seasonal changes in particulate organic matter flux in sediment traps at 0.5, 2.5 and 7.5 m: (a) absolute (histograms) and percent (chl u/total pigments) fluxes of chl n and (b) flux of particulate organic carbon (POC). No data at 0.5 m from 16 to 19 March.

The biogenic silica/chl a ratio ranged between ca. 5 and 50 and increased with depth, indicating loss of pigments relative to silica over the water column (Fig. 4d; Friedman’s, p < 0.05). Biogenic silica/POC values were often lower than 0.12 (Fig. 4e), which is a typical value for diatom assemblages (Nelson and Gordon, 1982). The ratio was slightly higher at 7.5 m than at all other depths (Fig. 4e), but the difference was not statistically significant (Fried- man’s, p > 0.05).

The suspended phytoplankton biomass was a mixed assemblage of pennate and centric diatoms together with naked flagellates and dinoflagellates. Cells < 10 pm in diameter accounted for ca. 70% of total cell numbers. Apart from flagellates < 5 pm, which made up a large proportion of cell numbers (ca. 40%, Fig. 5a) but represented negligible cell volumes (ca. l%, Fig. 5b), the assemblage was dominated by ikptocylindrus spp., a centric diatom that made up ca. 25% of the cell numbers before the second week of March (Fig. 5a). Other centric diatoms were almost absent before the second week of March, after which Thalassiosira spp. made up a smali fraction of ceil numbers (< IO%, Fig. 5a). Pennate diatoms, mostly Naoicula spp., Fragilaria

0 ; I I ‘I I I I

60

40

20

0 E 0.5 g 0.4- e

g 0.3- g OS- 8 O.l-* k in 0 I I I I I

19 24 29 5 10 15 20 February March

Fig. 7. Seasonal changes in composition ratios of the sedimented biomass. Dashed lines: critical values (c) 6.6 (Redfield et al., i863) and (e) 0.12 (Nelson and Gordon, 1982). No data at 0.5 m from 16 to 19 March.

ichel et al. /.hunlal qf wirte SyUerns I I f 1997) IS..?- 148 139

The contribution

the end of lLlarch (Fig. 5b).

3.3 Sedimer- fed biomass

A major change in sedimentation occurred after 16 March, when the chl a flux increased fro mgme2 d-’ to a m aximum value of ca. 5 mg m- 2 d- ’ (Fig. 6a). Concomitantly, the proportion of chl a in total pigments (chl u + pheopigments) increased from an average value of 67% (C.V. = 13%; three depths, six sampli;lg dates) to 86% (C.V. = 11%; three depths, two samp!ing dates) (Fig. 6a). The contribution of chl a to trapped pigments increased at all depths, but it was significantly lower in the 7.5 m trap than at other depths during the entire sampling period (Fig. 6a; Friedman’s, p < 0.01; multiple comparison test: 7.5 m < 2.5 m; 7.5 m < 0.5 m).

The increased flux of chl c1 was accompanied by an increase in the flux of POC, from ca. 45 mgm-’ d-’ to a maximum value of 120 mgm-’ d-’ (Fig. 6b). However, the increase in POC sedimentation (ca. three-fold) was small compared to that of

with depth (Friedman’s, p > 0.05). The POC/PON ratio did not show any significant change with either time or depth (Friedman’s, p > 0.05), and it was equivalent to the Redfield value of 6.6 (X = 6.6, C.V. = 8.5%) (Fig. 7~). Ratios of biocenic Si/chl a and biogenic Si,/POC were higher 8; X5 m than at

er depths (Fig. 7d, e), which is similar to what was observed for the same ratios in the suspended biomass (Fig. 4d, e). The difference was statistically significant for only the Si/POC ratio (Friedman’s, p < 0.05).

Table 1 shows the relative export of suspended chl a, POC and PON as well as their sinking rates. On a day-to-day basis, the biomass collected in sediment traps always represented < 8% of the SUS-

pended material. The percentoqe of suspended POC that sank out of the water column was always higher

Table 1 ’ Areal suspended biomass, proportion lost through sinking, and sedimentation rates. The sampling period is for each sediment trap mooring, the suspended biomass was sampled within each mooring period

Sampling period Area1 biomass, from 0 to 7.5 m Daily proportion of areal biomass Sedimentation rate at 7.5 m (mgm-*) a intrapsat7.5m(%d-‘)b (md-‘)’

Chl a POC PON Chl a POC PON Chl a POC PON

21-25 Feb. 25 Feb.-2 March 2-5 March S-9 March 9- 12 March ‘I 2- 16 March II 6-?O March 20-.I3 March

17.90 22.38 16.59 28.58

8.44 15.08 13.84

2.80 0.21 707.4 160.3 2.15 5.25 3.96 0.16 0.39 0.30 204.0 290.4 4.00 3.74 2.54 0.30 0.28 0.19 709.4 382.3 2.25 3.05 2.71 0.17 0.23 0.20 737.5 201.9 7.91 6.21 4.34 0.59 0.47 0.32 058.4 241.8 3.13 3.37 2.72 0.23 0.25 0.20 907.2 185.1 7.71 5.43 4.30 0.58 0.41 0.32

39.05 1551.4 357.9 4.28 4.57 3.65 0.32 0.34 0.27

a Trapezoidal integration from 0 to 7.5 m. b (Flux T.5 =/area1 biomass,_7.f; ,) X 100. c Flux 7.s &area1 biomass,_,,, J7.5 m).

140 C. Niche1 et al. /Journal of Marine Systems 11 (1997) 133- I48

21 25 2 5 9 12 16 19 February March

Fig. 8. Seasonal changes in the composition of the sedimented algal assemblage: (a) relative numbers and (b) relative volumes. Arithmetic means of all sampling depths. Pennate diatoms: I = Navicula spp.; 2 = Fragilaria spp.; 3 = Achnanthes spp,; 4 = other pennate. Centric diatoms: I = Detonula spp,; 2 = Leptocylindrus spp.; 3 = other centric.

than that of PON (Wilcoxon signed rank test, p < 0.05), but the two proportions did not show any seasonal trend. However, the export of chl 611 was lower before the first week of March than after. Sedimentation rates exhibited patterns similar to those of percent loss by sinking (Table 1).

Algal composition in the traps consisted of a mixed assemblage of pennate and centric diatoms, flagellates, and dinoflagellates (Fig. 81, as was the case for the suspended biomass (Fig. 5). However, compared to the suspended biomass, the contribution of pennate diatoms was higher in the traps and that of centric diatoms lower, whereas flagellates > 5 p,rn and dinoflagellates contributed about the same proportions in the traps as in the water column (Figs. 5 and 8). The major difference between the suspended and sedimented assemblages was the presence of Detonula spp. in the traps but not in the water column. Detonuka spp. were largely dominant in the ice algal assemblage (Kudoh, pers. commun.).

Table 2 gives the relative contributions of the major diatom genera at 0.5 m under the ice ,in both the water column and the traps. Besides the different contributions of LeptocyZindrus spp. and Detonula spp. to each assemblage, Table 2 shows some interesting seasonal changes that can be used to charac- terize the three peaks in chl a observed at 0.5 m

Tsb!e 2 Percent cell numbers in the two major groups of diatoms and the :nain genera within these groups for suspended and sedimented (in parentheses) algal assembiages at 0.5 m under the ice cover

Diatom taxa February March1

z-251 &*I ?k2) :2-5) (65_9, tso_lu ::2-16) 17 (16-19) E-*3)

Pennate diatoms 25.5 28.5 20.3 17.8 46.2 10.4 12 48.5 23.5

Achnanthes spp.

Navicula spp.

Fragilaria spp.

Centric diatoms

Leptocylindrus spp.

Detonula spp,

Thalassiosira spp.

03.0) (22.2) (22.2) (27.4) (35.6) (36.6) (19.5) (32.9) (37.0) (:::, 23.5 15.6 10.0 21.7

(5.0) (:::I (Y

(8.0) c2:::,

(8.1) (23.7) (2%

$, (1::S UT::, &::I 25.6

(22.9) (1::) z.3, (:::I E,

(i.31 (L 5011

zi5 (1:::) (G, (i.2) &I 11.4 (0.4) (7.4)

26 45.7 53.8 30.3 8.19 16.8 19.0 30.5 (1.8) (20.7) (20.7) (8.5) (15.0) (5.75) (11.0) (11.7) (15.3) 25.3 49.0 45.5 52.7 26.3 16.8 14.6 25.5 (1.6) (4.2) (4.2) (4.2) (5.9) G2 (7.8) (1.4) (12.0)

&I &I &) $1 (::$ & &I (1% (i.2) 0.5 0 0 0 0 0 0 4.7

(0) (0.2) (0.51 (0) (cj (91 (0) (2.9) _r_

sponded to a large increase i

Instead, high proportions of Nakula spp. and Detonulu spp. were found in the trapped assemblage. Tine second peak, on 6 Marcl,, ~~~~n-z--+~n~ +q h;k LuI kGz3ptiilubu rb 111gjll

proportions of Navicula spp. in both the water column and trapped assemblages. Finally, the increase in suspended chl a observed after mid-March dif- fered from the previous ones, with significant contributions of Fragilaria and Thalassiosira species. trapped assemblage at 0.5 m was dominated by Achnanthes spp., with Leptocylindrus, Detonula and Thalassiosira also present (Table 2).

iscussion

4.1z Water column

Maximum nutrient concentrations in the under-ice water column (Fig. 2) were similar to those reported by Tada et al. (1993) for March 1987, i.e., lo- 12 @4 for NO, + NO, and 1.3 p M for PO,. Accord- ing to these authors, their values were similar to those recorded earlier (Kikuchi, 1979). Maximum chl a concentrations (ca. 10 mg m-“; Fig. 3a) are consistent with those reported in Saroma-ko just after ice melt (in April), i.e., 6.7 and 19.1 mg m -’ in 1987 and 1988, respectively (Tada et al., 1993). During the ice-covered period (in 1987) low suspended chl a concentrations ( < 1 mg mV3), reported by Fukuchi et al. (1989) and Satoh et al. (1989), were followed by a bloom-like increase with concentrations reaching 3-5 mgmV3 (Fukuchi et al., 1989). These last values are similar to those we measured in 1992 at the end of March (up to ca. 6 mgms3; Fig. 3a). At that time, the steady increase in chl a concentrations over the water column likely reflected the onset of a phytoplankton bloom under the ice cover because of the relatively high occurrence cf Thalassiosiru (Fig. 5), which has been reported to dominate the water column assemblage in Saroma-ko (Satoh et al., 1983).

At all times during the sampling period. the phytoplankton area1 standing stock (integrated values

coverage in Saroma-ko was 61 days 100 days in 1987 (Shirasawa et al., and constant proportions of Lep

equent decrease (Fig. 5), suggest that this species actively growing prior to the start of sampling,

during a period when Saroma-ko was still not completely ice covered. In ad ition, the steady presence of dinoflagellates (Fig. 5) which were shown to be abundant after ice melt in Saroma-ko (Watanabe et al., 1993), suggests that a phytoplankton assemblage did persist during the 1992 winter due to the short ice-covered period and consequent increased under- water irradiance.

POC/chl a ratios (range: 25-214 by weight; Pig. 4a) are within the range of published values for phytoplankton assemblages in the Weddell Sea (31- 5 13; Nelson et al., 1989; Leynaert et al., 1991; Smetacek et al., 1992) and in the Ross Sea (138; Smith and Nelson, 1985) as well as for ice algae in the Canadian Arctic (30- 180; Gosselin et al., 1990). High POC/chl a ratios have been reported for phytoplankton cultures under nutrient limitation (Caperon and Meyer, 1972; Harrison et al., 1977), yet the abundance of nutrients in Saroma-ko rules out nutrient limitation. The observed high POC/chl a ratios may reflect the presence of heterotrophic contributors to the suspended biomass. Indeed, cell counts showed the presence of significant numbers of choanoflagellates (5 = 1.4 X lo4 ind. l- ‘) and ciliates (E = 1.9 X lo3 ind. l- ‘) in the water column. The observed concentrations of choanoflagellates fall within the range of values found in the ice edge zone of the Weddell Sea, i.e., 1000 to 2 X lo6 ind. 1-l (Silver et al., 1980; Buck and Garrison. 1983, 1988). Numbers of ciliates similar to those in Saroma-ko have been reported in the Antarctic, i.e., 1 X IO3 to 9 x IO3 ind. l- ’ (Buck and Garrison, 1983; Leaky et al., 1994). It thus appears that an active microbial rood web coexisted witll phytopiankton in the water

142 C. Michel et at. / Jownai of Marine Systems I I f 1997) 133- 148

column during the sampling period. This agrees with previous findings of Takahashi ( 198 11, who observed a rich autottophic and heterotrophic community under the ice of Saroma-ko. The relatively low POC/PON for suspended biomass (Fig. 4c) is also consistent with the presence of high heterotrophic biomass. Indeed, in the absence of nutrient limitation, dinoflagellates have been shown to exhibit lower POC/PON ratios than phytoplankton (Cullen and Horrigan, 1981). Bacteria are also known to have low POC/PON ratios (ca. 4; Lee and Fuhrman, 1987) and, in a culture of bacterivorous flagellates with bacteria, Borsheim and Bratbak (1987) measured POC/PON of ca. 5. For different tintinnid species, Verity and Langdon (1984) measured POC/PON ratios ranging from 4.6 to 5.5, and Klep- pel et al. (1991) reported that ciliates contain more proteins and lipids than phytoplankton. Finally, the slightly lower Si/POC ratio (Fig. 4e) compared to that of diatom-dominated assemblages (0.12; Nelson and Gordon, 1982) also reflects a diversified suspended biomass, with some contributors lacking siliceous structures.

4.2, Sedimentation

A typical feature of springtime sedimentation in ice-covered marine waters is a transient increase in the flux of pigments. This has been reported for both the Antarctic (Von Bodungen et al., 1986; Sasaki and Hoshiai, 1986; Matsuda et al., 1987; Fukuchi et al., 1988; Bathmann et al., 1991) and the Arctic (Tremblay et al., 1989; Wassmann et al., 1991 and references therein). The spring cycle of sedimentation in Saroma-ko also exhibited an increase in the flux of pigments and POC (Fig. 6). In 1992, the flux of POC was within the range of previous estimates for Saroma-ko (Sasaki and Fukuchi, 1993), and the fluxes of both POC and chl a were comparable to those reported for some other ice-covered regions (Fukuchi and Sasaki, 198 1; Sasaki and Hoshiai, 1986; Fukuchi et al., 1~88). The proportionally stronger increase in the flux of chl a compared to that of POC implies that algae contributed most of the exported biomass during the period of high sedimentation, as previously observed in the Antarctic (Matsuda et al,, 1987). Using a POC/Chl a ratio of 20, which was the average value for ice algae and

phytoplankton in Saroma-ko for 1992 (Kudoh, 1993) algae would comprise ca. 60% of the sinking POC after mid-March (30% before that period; see Fig. 6) However, at the same time, chl a represented ca. 90% of the total pigments in the traps (Fig. 6a), so pheopigments (ca. 10% of the trapped pigments, presumably from copepod feces) can hardly explain the remaining 40% of sinking POC. Downs and Lorenzen (1985) reported that POC/pheopigment ratios of copepod fecal pellets range from 1 l- 18 for herbivorous animals to 25-29 for omnivores or car- nivores. Using a POC/pheopigment conversion factor of 30 (fecal pellets of copepods with a broad diet; Downs and Lorenzen, 1985) to convert pheopigments into sinking POC results in only ca. 25% of non-algal POC being explained by sinking fecal pellets during the whole sampling period (23 and 27% during periods of high and low fluxes, respectively). This represents a minimum estimate, since the calculation accounts neither for the loss of pigments during digestion (Conover et al., 1986; Lopez et al., 1988; Head, 1992) nor for the formation of colorless residues (Kiorboe and Tiselius, 1987), both of which could have occurred during copepod feeding. In addition, the presence of dinoflagellates and flagellates in both the water column and sediment traps (Fig. 5 and Fig. 8) suggests that they contributed to the exported organic matter by direct sinking and fecal pellet production. Heterotrophic flagellates and dinoflagellates can degrade chl a into various types and proportions of pigments (Goldman and Caron, 1985; Strom, 1993) and also into colorless residues (Klein et al., 1986; Barlow et al,, 1988) which could make up as much as 95% of the in- gested pigments (Klein et al., 1986). Given the significant numbers of microheterotrophs, their feces could account for part of the unexplained sinking POC. Flagellates and dinoflagellates were not sys- tematically identified, but the dominant dinoflagellates were Gymnodinium spp., which are known to have a broad diet and produce feces (Btick et al., 1990). Finally, the higher POC/PON ratios in sediment traps (Fig. 7c) compared to the water column (Fig. 4c) are indicative of accumulation of feces in the sinking material, since these ratios are often reported to be higher in feces than in the food source as a consequence of preferential nitrogen assimila- tion by animals (Morales, 1987).

tion is the incre

vide the season into three perio

half of March (ca. 0.7 mgm-* d- ‘), and was high at the end of March (ca. 3 mg m-* d- I). During the sampling period, the ice algal assemblage was dominated by Detonula spp. and Navicula F pers. commun.), so these two taxa can tracers for ice algae released from the ice. Similarly, Achnanthes spp. and Leptocylindrus spp. can be used to trace phytoplankton, since they were scarce or absent in the ice algal assemblage (Kudoh, pers. commun.). It is interesting to note that, during the whole season, ice algal taxa (mainly Detonula and Navicula) contributed to the trapped material (Table 2; Fig. 8) but did not make up a significant part of the suspended assemblage, except on one occasion as a transient contribution of Navicula (on 6 March; Table 2). This contribution of ice algae (Navicula) to the suspended biomass corresponds to a transient increase in chl a close to the undersurface of the ice (Fig. 3a). The reverse did not occur for phytoplankton, i.e., genera Achnanthes and Leptocylindrus were commonly found in sediment traps in various proportions; however, during the first part of the sampling season, their abundances in the trapped assemblage were quite low compared to those in the water column irable 2). At the end of the season, during the period of increased flux, both phytoplankton and ice algal taxa were abundant in sediment traps.

The above observations concerning sedimenting algae lead to two conclusions. First, except on one occasion, ice algae did not contribute to the phytoplankton assemblage in Saroma-ko. This may be due to the shallowness of Saroma-ko Lagoon, which would prevent sinking algae from staying in the water column as part of the suspended biomass. The algal biomass still present in the ice at the beginning of ice melt thus rapidly reaches the bottom, where it provides a large quantity of food for the benthos. The rapid transit from the ice to the lagoon floor favors a supply of “high quality” food, as there is

phytoplankton durin ally so low that its

pellets from herbivorous zooplankton often make up a large part of the downward flux in ice-covered

1986; Carey, 1987; 1199 1) and, on the short term,

massive sinking of ice algae may occur Hoshiai, 1986). Saroma-ko is the southe sonally ice-covered area in the Northern so the ice is not very t!Cck (ca. 30 cm). This, combined with the fact that the ice-covered period was short in 1992, allowed relatively high phytoplankton production under the ice cover. As a consequence, the area1 suspended biomass (chl a ranging from 8 to 39 mgm -* ; Table 1) was of the same order as the biomass of ice algae (from 5 to 38 mgm-*; Robineau, pers. commun.). It follows that phytoplankton significantly contributed to the pigment flux, as shown by species composition in the trapped material (Table 2).

4.3. Tropitic pathways

Both water column and sediment trap data indi- cate that the under-ice alga! cnsmt~nity in Saroma-ko _-__ __ --- probably supported an active microbial food web at the end of winter in 1992. Numbers of microheterotrophs in the water column were higher than in the ice (Sime-Ngando et al., 1997-this issue) and some recycling of algal material seemed to occur in the water column. This is shown by the increasing Si/chl a and Si/POC ratios with d water column and sediment traps 7d,e), and by the lower contribution of chl a to the total pigments in the 7.5 m sediment trap (Fig. 6a). Table 1 indicates that the daily proportion of ex- pofied algal binmass through sinking did not exceed

ca. 8% of the suspended biomass. The same table shows that the relative expoq of PON was consistently lower than that of POC, which led to lower sinking rates for PON than for POC. Again, this agrees with the view that some utilization and recycling of organic matter took place in the water column, since relatively more PON than POC re- mained suspended. The higher POC/PON ratio in sediment traps compared to that of suspended matter could reflect recycling of PON and/or the presence of fecal matter in the traps (see Section 4.2). The fact that this ratio did not change with depth (Fig. 7c) indicates that the material reaching the floor of the lagoon was still of high nutritional value (Findlay, 1982).

Sedimentation rates computed from water column and trap data were low (Table 1) and fall within the range of non-nutrient limited cells (e.g., Bienfang et al., 1982) actively growing cells (Eppley et al., 1967) and/or small cells (Smayda, 1970, 197 1). This is consistent with the facts that phytoplankton did not seem to experience nutrient limitation and that ca. 70% of the suspended algae (by numbers) were in the < 10 p,rn size class. Considering that algae released from the ice probably had higher sinking rates than phytoplankton (i.e., the former did not remain long in suspension), sedimentation rates derived from trap and water column data would represent maximum rates for phytoplankton algae. Saroma-ko would thus be a mixed environment, with high suspended biomass of small cells and, simultaneously, high export of larger ice algae. This leads to both an active microbial web in the water column and a large export towards the bottom. In the Wed- dell Sea ice edge zone, Lancelot et al. (1993) ob- sef\lPd 0 84nminanfia nf nnnnnhxrtnnlnnlfltdx- -nil- A-t v -- Y YVLI~L~~UL~VV v* ukau~pa~ bupauunbuafi bbub LLICLC

they attributed to the presence of overwintering krill, whose grazing reduced diatom seeding in the water column. In Saroma-ko, the presence of overwintering zooplankton could also have reduced the abundance of large cells in the suspended assemblage. However, it appears that zooplankton grazing pressure was low during the sampling period (Saito and Hattori, 1997- this issue). It is thus suggested that the main factor preventing the establishment of large cells in the suspended assemblage was their rapid sedimentation to the bottom. Because of the shallowness of the lagoon, fast-sinking cells rapidly reach the bottom,

where strong grazing pressure by the cultured scallops removes them from the prinary production compartment. The role of benthos in shallow Saroma-ko would thus be similar to that of krill in the ice-edge zone, where the grazing pressure of krill on ice algae, especially at the time of ice melt, may control the initiation and magnitude of phytoplankton blooms dominated by diatoms (Marschall, 1988; Smetacek et al., 1990) and favor the development of nanophytoplankton (Lancelot et al., 1993). In Saroma-ko, the short herbivorous web (from ice algae to benthos), which results from rapid sinking of ice-algal cells, leaves way for a microbial web in the water column. Contrary to the idea that microbial activity may be very low in low-temperature waters (Pomeroy and Deibel, 1986; Pomeroy and Wiebe, 1988) data from Saroma-ko are consistent with the view that the microbial compartment may be an important component of some high-latitude ecosystems (Garrison and Buck, 1989; Azam et al., 1991; Garrison et al., 1993).

Saroma-ko showed coexistence of water column microheterotrophic production and rapid export of ice algae to the benthos during the period of ice melt. In the continuum of trophic pathways ranging from the microbial loop to the herbivorous web, proposed by Legendre and Rassoulzadegan (1995) Saroma-ko would represent the special case of a system where a pelagic microbial food web superimposes itself on a herbivorous web, leading to simultaneous high export form the ice to the bottom and high recycling in the under-ice water column. The particular conditions favoring the transient co-occurrence of the two trophic pathways at the time of ice melt suggest that coupling between the water column and the benthos

^____ _^ -

Acknowledgements

The main source of funding for Canadian partici- pation in the SARES project was a grant from the Japan Science and Technology Fund (Department of External Affairs and Trade of Canada). C.M. received a post-graduate scholarship from the Natural Sciences and Engineering Council of Canada (NSERC). A research grant to L.L. from NSERC and a team grant from the Fonds FCAR of Quebec

thanks are due to t

ockanqr+ +i@es dl4 gg&?fbec grants from NSERC and the

and C. Manger and P. Peltola for their help in the field. This paper is a contribution to the programme of GIROQ and to the Hokkaido National Fisheries Institute.

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Documents

Coexistence of microalgal sedimentation and water column recycling in a seasonally ice-covered ecosystem (Saroma-ko Lagoon, Sea of Okhotsk, Japan)