Variation in phytoplankton standing stock, chemical composition and physiology during sea-ice formation in the southeastern Weddell Sea, Antarctica

J. Exp. Mar. Biol. Ecol., 173 (1993) 211-230 0 1993 Elsevier Science Publishers B.V. All rights reserved

JEMBE

211 0022-0981/93/$06.00

02037

Variation in phytoplankton standing stock, chemical composition and physiology during sea-ice formation in the southeastern Weddell Sea, Antarctica Markus Gleitz and David N. Thomas Alfred- Wegener-Institut fir Polar- und Meeresforschung, Bremerhaven. Germany (Received

8 April 1993; revision

received

22 June 1993; accepted

30 June 1993)

Abstract: Changes in physico-chemical conditions, phytoplankton biomass, biochemical composition and primary productivity were investigated during autumnal sea-ice formation in the southeastern Weddell Sea, Antarctica. During sea-ice growth, brine salinities gradually increased with decreasing temperatures. Nutrient concentrations in the brine of sea ice older than 2 weeks were lower than calculated from initial surface seawater values. The concomittant accumulation of phytoplankton biomass could not be explained solely by physical enrichment. We suggest that several microalgal species retained the capacity to assimilate nutrients and continued to grow in newly formed sea ice. However, nutrient depletions were moderate, and biochemical analyses did not indicate nutrient stress of algal metabolism. Relative abundance of smaller diatom species increased during ice growth, suggesting that pore space available for colonization in conjunction with physiological acclimation capacity were major factors determining successional patterns in recently formed sea ice. Even though ice algal assemblages apparently sustained the capacity to acclimate to reduced irradiances brought about by ice growth and increasing snow cover, maximum primary production was considerably lower than values usually reported from spring and summer ice communities. Therefore, autumnal primary production in newly formed sea ice may not add greatly to total annual production. but may provide an important food source for ice-associated grazers during the winter period, when phytoplankton biomass in the water column is extremely low. Key words: Antarctic;

Ecophysiology;

Ice algae; Phytoplankton;

Primary

production;

Sea-ice formation

INTRODUCTION

The seasonal development and degradation of sea ice is a key factor influencing the ecology of phytoplankton communities in the Southern Ocean (Garrison, 1991; Eicken, 1992; Horner et al., 1992). In late austral summer and autumn, cooling of surface waters induces thermal convection eroding the seasonal pycnocline (Hellmer & Bersch, 1985). Ice crystals begin to form in a several-meter-thick upper layer when the water temperature falls below the freezing point (Weeks & Ackley, 1982). Subsequent meteorological conditions primarily determine growth rate and texture of newly formed sea ice (Eicken & Lange, 1989). Mean wind speeds in the southern Weddell Sea in

Correspondence address: M. Gleitz, Alfred-Wegener-Institut 12 01 61, 27515 Bremerhaven, Germany.

fUr Polar- und Meeresforschung,

Postfach

212

M. GLEITZ AND D.N. THOMAS

March and April are usually high (> 10 m*s-‘), (K&-rig-Langlo, 1992). Thus, windinduced turbulence is commonly observed during initial stages of ice formation, and Langmuir circulation cells transport ice crystals throughout the upper water column (Weeks & Ackley, 1982; Lange et al., 1989). The buoyancy of ice crystal accumulations eventually prevents downward transport, and a “soupy” layer of frazil ice termed “grease ice” forms at the sea surface (Weeks & Ackley, 1982; Eicken & Lange, 1989). Freezing and wave action transforms the viscous “grease ice” to roughly circular, centimeter-sized ice pieces with upturned edges, called “pancake ice” (Weeks & Ackley, 1982). Subsequent growth, ridging and rafting of small “pancakes” into Larger ones (the “pancake ice cycle”) is primarily responsible for the establishment of a closed pack ice cover in most of the Weddell Sea in time scales of weeks (Lange et al., 1989). There is good evidence that physical processes are mainly responsible for the observed enrichment of phytoplankton in sea ice forming under turbulent conditions

Fig. 1. Study area and cruise track of R V Polarsfem expedition ANT X/3. Numbers denote sampling dates (Julian Days). Shaded area denotes approximate location of ice edge. 0 = open water station; 0 = ice station; 0; = ice edge station.

PHYTOPLANKTONR~SPONSESTOSEA-ICEFORMATION

213

(Garrison et al., 1983, 1989; Weissenberger, 1992). Depending upon the strength of water column turbulence during ice formation, microalgal cells are scavenged by ice crystals floating to the sea surface (Clarke & Ackley, 1984; Garrsison et al., 1989). Wave induced pumping of water through “grease ice” layers has also been identified as an important concentration mechanism for phytoplankton-sized particles (Weissenberger, 1992). During the transition from open water to ice, microorganisms are subject to substantial variations of physico-chemic~ parameters, the most prominent being a spatial confinement to the minute brine channel system, a decrease of temperature and an increase of salinity (Horner et al., 1992; Weissenberger et al., 1992). Recently, Gleitz & Thomas (1992) and Grossmann & Gleitz (1993) demonstrated the capacity of several Antarctic diatoms and a natural bacterial population to sustain metabolic activity in controlled laboratory experiments simulating sea-ice formation. Extensive autumnal blooms of algae in newly formed sea ice have been documented by Hoshiai (1977, 1981, 1985) and Watanabe & Satoh (1987) in the Cosmonaut Sea, East Antarctica. However, floristic analyses in conjunction with ecophysiological studies pertinent to sea-ice formation under field conditions have recieved virtually no attention. In the present work, we report on changes in the abiotic environment associated with the tr~sition from the open water to the ice habitat, and the physiolo~cal acclimation strategies that enable incorporated phytoplankton species to colonize and grow in newly formed sea ice. It is shown that proliferation of certain microalgal species does not cease with the seasonal establishment of the pack ice cover, but can be sustained until the advent of the polar night entirely restricts net primary production in sea ice of the high Antarctic.

MATERIAL

AND

METHODS

SAMPLE COLLECTION

Samples were collected during expedition ANT X/3 of R VPoIarstern between 8 April to 6 May 1992 (Julian Days 99 to 128) in a region between 67”30’-‘71”s and 12”~6”E (Fig. l), (Spindler et al., 1993). The advancing ice edge was crossed several times during 7 transects perpendicular to the coastline. This sampling scheme made it possible to collect various stages of newly formed sea ice as well as surface seawater in regions of rapid ice formation. To faciliate comparison, samples were grouped as described in Table I. A total of 8 seawater, 7 “grease ice”, 11 “pancake ice” and 12 samples from closed pack ice were analyzed. However, not all parameters measured during the study were determined for all samples. Surface seawater was collected with Niskin bottles (General Oceanics) attached to a CTD rosette. At several stations, surface water was also collected with a bucket from a zodiac. “Grease ice” was carefully scooped off the sea surface with a “coal scuttle”

214

M. GLEITZ

AND

D.N.

THOMAS

TABLE I Description

of sample types collected

Sample type

during ANT X/3.

Description

Open Water (OW)

Open water without

Grease

Frazil ice layer accumulating surface

Ice (GR)

Estimated

ice formation at the sea

hours

Young Pancake

Ice (PC I)

Small individual pancakes, < 1 m in diameter, t30 cm thick. No snow cover

days

Older Pancake

Ice (PC II)

Larger pancakes, l-several m in diameter, 30-50 cm thick, often consisting of smaller pancakes frozen together. l-20 cm snow cover

l-2

Closed pack ice sheet 50-120 IO-50 cm snow cover

> 2 weeks

Closed Ice Sheet (US)

age

cm thick.

weeks

that prevented dilution of the ice by the underlying seawater. This material was immediately drained over a coarse sieve to separate slush ice from interstitial water. Young “pancake ice” was sampled in the same manner. Larger “pancake ice” floes (up to 1 m in diameter) were collected using an ice basket operated from the ship with a crane. The device was designed in such a way that the “pancake” floated on the seawater in which it was collected, thus preventing loss of brine from the ice through gravity drainage. Older “pancake ice” with a diameter > 1 m, usually consisting of several smaller “pancakes” frozen together, were sampled by coring (CRREL ice auger, 7.6 cm diameter). Entire cores or core segments were transferred to plastic bags immediately after collection and stored in insulated boxes. In the laboratory, 10 cm core sections were centrifuged at 275 x g for 5 min at -2 ‘C as described by Weissenberger (1992). The collected brine was stored at 0 “C in the dark. Samples from the closed pack ice were obtained after removing short cores (30-40 cm) from the ice sheet. After time spans of several minutes up to about one hour, at least 0.5 1 of brine had accumulated in the “sackhole”, and this material was collected for subsequent analyses (Garrison & Buck, 1986). All samples were obtained from floes consisting predominantly of granular ice (Weissenberger, pers. communication).

PHYSICAL

AND

CHEMICAL

DETERMINATIONS

Subsamples for pH and alkalinity measurements were stored in polypropylene bottles (Nalgene) and allowed to warm to laboratory temperature ( z 20 “C) in the dark. Care was taken to minimize exposure of the sample to the atmosphere. The pH was measured using a microelectrode (Ingold U402-M6-S7/100) connected to a microprocessor pH meter (WTW pH 3000). Prior to the measurement, the electrode was acclimated

PHYTOPLANKTON

RESPONSES

TO SEA-ICE

FORMATION

215

to the respective sample salinity. The pH at the respective in situ temperature was calculated according to Grashoff (1983). Total alkalinity was determined using a potentiometric titration method (Almgren et al., 1983). The inorganic carbon concentration (at -1.5 “C) was calculated using carbonic acid dissociation constants of Goyet & Poisson (1989). Salinity was measured using a microprocessor conductivity salinometer (WTW LF 2000), and in situ temperature was calculated from salinity using the equations given in Assur (1958). Concentrations of nitrate, phosphate, silicate and ammonium were measured shortly after collection using an autoanalyzer (Technicon ASM 2) following standard methods of Technicon modified as described in Spies et al. (1988). Each sample was analyzed at least twice and values averaged. SPECIES

COMPOSITION

Sample volumes of 25-250 ml were fixed with hexamine-buffered formaldehyde (final concentration OS-l%) immediately after collection. In the laboratory at the AlfredWegener-Institut, lo-50 ml were placed in a sedimentation chamber and counted according to UtermiShl(l958). Diatoms were identified according to Priddle & Fryxell (1985) and Medlin & Priddle (1990). Following Round et al. ~1990), we treated Frugi~~rio~~~as a genus (formerly a section of the genus ~~~2~~~~~). Small unicellular C&Xtoeeros species from the Southern Ocean are frequently referred to as being Chaetocem neogrucile. However, this may be misleading and inaccurate (Thomas et al., 1992), and we refer to this species as Chaetoceros cf. neogrucile. CHEMICAL

COMPOSITION

OF PARTICULATE

MATTER

Aliquots of 100-2000 ml were filtered onto GFjC filters (Whatman) for the determination of Chl a, carbohydrate and protein concentrations. Precombusted GF/C filters were used for particulate organic carbon (POC) and nitrogen (PON) measurements. Samples for determination of particulate biogenic silicate were filtered onto cellulose acetate filters (0.4 pm, Sartorius). With the exception of Chl a samples, which were processed on board, all filters were stored at -27 “C until analysis in the laboratory at Bremerhaven. Chl a concentrations were determined fluorometrically after extraction in 90% acetone according to Evans & O’Reilly (1983). For POC and PON measurements, filters were acidified with 0.1 N hydrochloric acid, dried at 60 ‘C and processed using a CHN analyzer (Carlo Erba 1500), calibrated with acetanilide standards. Total carbohydrate was determined after a 30-min extraction in boiling 5 % trichloroacetic acid using the phenol-sulfuric acid method (Kochert, 1978), calibrated with glucose. Protein samples were homogenized and extracted in 0.1 N sodium hydroxide for 3 h at 85 oC, and protein concentrations were subsequently dete~ined photomet~c~ly according to Bradford (1976), using bovine serum albumin as a standard. Particulate biogenic silicate was determined photometrically after a 14-h extraction at 85 ‘C in 0.1

216

M. GLEITZ AND D. N. THOMAS

N sodium hydroxide according to Koroleff (1983), using sodium hexafluorosilicate for calibration. PRIMARY

PRODUCTION

Sample volumes of 50 or 100 ml were inocculated with 0.15-1.48 MBq of 14Clabelled sodium bicarbonate (Amersham Buchler) and incubated in borosilicate glass bottles (Schott) for 5 h at -1.5 “C in a temperature controlled deck incubator at 30, 90 and 160 pmol PAR.m-*as-‘, provided by fluorescent tubes (Philips TL 54). Irradiances were adjusted using neutral density plastic foil, and measured with a spherical light sensor (LI-COR 193 SB). After incubation, samples were filtered onto cellulose nitrate filters (0.45 pm, Sartorius), which were dried at room temperature, exposed briefly to fuming hydrochloric acid, and dissolved in scintillation cocktail (Zinsser). Dark uptake rates determined in triplicate were in all cases subtracted from light uptake measurements. A parallel set of samples (three replicates) for the determination of photosynthetic end products was incubated for 10 h at 90 pmol PAR rn-*+~-~, filtered onto GF/C filters, and stored at -27 “C. The separation of photosynthetic end products was carried out using a differential extraction technique following Li et al. (1980), fully described by Thomas & Gleitz (1993). The procedure yields 4 fractions: lipid, low-molecular-weight metabolites, protein and polysaccharide. All samples were counted in a liquid scintillation counter (Packard), and quench correction was performed by automatic external standardization.

RESULTS

PHYSICAL AND CHEMICAL

DETERMINATIONS

From open water to sea ice of increasing age, median pH and salinity values increased to 8.3 and 47 psu, respectively (Fig. 2). Temperatures decreased with increasing salinities, and values as low as -6 “C were calculated for brines collected from PC II (older pancake ice) and CIS (closed ice sheet). Nutrient concentrations in brine (normalized to 34 psu to correct for concentration effects) generally decreased in PC II and CIS samples when compared to OW (open water). Average ammonium concentrations, on the other hand, increased during this period. Maximum ammonium concentrations recorded in CIS were about one order of magnitude higher than values recorded in surface seawater. Cell, POC and Chl a concentrations in brine samples increased progressively with the age of the newly forming sea ice (Fig. 3). Median cell concentrations in CIS samples were about two orders of magnitude higher compared to those measured in OW samples (3 x lo4 vs. 5 x lo6 cells=l-‘). Between OW and CIS, median POC and Chl a concentrations increased from 0.05 to 1.1 mg.l-’ and from 0.14 to 7.15 pg*l-‘,

PHYTOPLANKTON

I

Ssiinity

RESPONSES

35-I

23-l

TO SEA-ICE

Nitrate

Phosphate

I

FORMATION

217

‘87

Ammonium

75-I

Silicate

2.01.5l.O0.5 -

OW

GR

PCI

PC8

Cl-3

OW

OR

PCI

PC8

CIS

OW

GR

PCI

PC11

CIS

Sample Type Fig. 2. Physico-chemical conditions in samples collected during ANT X/3: pH, salinity (psu), nitrate @M), phosphate (PM), ~nmonium (JIM) and silicate (PM), All nutrient concentrations were normalized to 34 psu. 0 = data point; -0= median. Shaded area denotes the observed range. Abbreviations as in Table I.

respectively. Differences were generally highest between GR (grease ice) and PC II, even though slight increases were also observed between OW and GR. SPECIES

COMPOSITION

Diatoms dominated all samples, accounting for about 80% of total phytoplankton cell numbers. A decrease to 60% was observed only at stage PC II, due to an increased abundance of nanoflagellates. At stages OW, GR and PC I, pennate diatoms were more abundant than centric diatoms, accounting for 60-90% of the total diatom cell number. The contribution of centric diatoms increased again at stages PC II and CIS to 27 and 55 %, respectively. A total of 11 pennate species, mostly belonging to the Bacillariaceae, and 10 centric species, mainly of the genera Chaetocevos, Corethron, Eucampia, Dactyliosolen and Rhizosolenia, were identified to the species level (Table II). However, a variety of smaller discoid and pennate species remained unidentified. Dinoflagellates accounted for between 5 and 20% of the total phytoplankton cell density with cell numbers generally between lo’-lo4 cells.l-‘. These were generally small (< 30 pm in diameter) and autotrophic (contained chloroplasts). Nano~ageIlate abundance was highly variable, reaching significant concentrations ( 104-lo6 cells*l-‘), corresponding to about lo-30% of total phytoplankton abundance, only at stages PC I and PC II. Protozoa mainly comprised ciliates, foraminifers and tintinids with cell

218

M. GLEITZ

AND D.N.

OW

OR

THOMAS

PCI PC II

CIS

Sample Type Fig. 3. Cell number (log cells.t-‘), particulate organic carbon (POC, mg.l-‘) and Chl R (jug 1-l) concentrations in samples coliected during ANT X/3. Symbols and abbreviations as in Fig. 2.

numbers generally ( lo3 cells*l-‘. Cell numbers of up to lo4 cells*l-’ were recorded in older ice types (PC I and PC II). Substantial changes in diatom species composition were recorded during ice formation (Fig. 4). In OW and GR samples, several species contributed more or less equally to total diatom abundance. At later stages, relative abundance of Cketoceros cf. neogmcile, Fragi~aria~s~scylindrus and ~itzsch~a lecointei increased subst~tially. At stage CIS, these three species accounted for about 95% of the total diatom ceil concentration. On the other hand, certain species (e.g. Fra~~aria~sisker~e~ensis, Dactylibso/en te~u~anctas~ decreased in abundance in the course of sea-ice formation. Some

PHYTOPLANKTON

RESPONSES

TO SEA-ICE

219

FORMATION

TABLE II

Diatom species identified during ANT X/3. X = present in > 50% of the samples; (X) = present in 10-50:; of the samples; (-) = present in < 10 y0 of the samples; - = absent. For abbreviations see Table 1. Sample type

ow

GR

PC1

PC II

X

X

X X

X

(C) i-f X X X

(X) X X X

CX, (X) X X

(Y) X

(T) X

(X) (-)

(X) t-) X -

CIS

Centrales

Chaetoceros bulbosum (Ehrenberg) Heiden Chaetoceros diehueta Ehrenberg Chu~t(~cer~)spe~ldulun~ Karsten Chuetoceros cf. neogracile Chnetoceros crio~hi~ui~ Castracane Corethron criophilum Castracane Dactyliosolen antarcticus Castracane Dacr$iosolen tenuijunctus (Manguin) Eucumpia antarctica (Castracane) Mangin Rhixsoleniu truncata Karsten Pennales Amphiproru spp. Hasleo sp. Ma0guinea sp. ~~t.~chi~turg~dMlaHustedt Nitzschia pro~o~zgffto~desHasle j~~?zscl~juclo.~~eri~~z(Ehrenberg) W. Smith ~~t~.~ch~~ Iecointei Van Heurck Fr~gjlariopsis rhombica (O’Meara) Hustedt Frugiktriopsis kerguelensis (O’Meara) Hustedt Fragiluriopsis curra (Van Heurck) Hustedt Fragilariopsis cylindncs (Grunow) Krieger

species only attained high concentrations

(-) X X X X (X)

(I, X X X X X

X (S (X)

(X) X

(g) (X) (-) X

(X) (X) (X)

(X)

X

X

(X)

-

X

(-) (-) (X) X X X X X

(E) (X) X X X X X X

X (T) (X) (X) X

in intermediate stages (e.g. Nitzschia closte-

riuw), with relative abundance decreasing again in older ice types.

CHEMICAL

COMPOSITION

OF PARTICULATE

MATTER

C:N ratios were similar in samples from the different ice formation stages, the median ranging from 6.6 to 9.1 (Fig. 5). Median POC:Chl a and protein:carbohydrate ratios ranged from 200 to 650 and 0.3 to 0.7, respectively. Slightly lower POC:Chl a ratios were observed in samples from PC II and CIS. However, given the large variation within the data set, no clear patterns could be confidently resolved. On the other hand, the estimated median particulate biogenic silicate content per diatom cell decreased significantly from 2.4 (OW) to 0.4 ng pSi.cellli (CIS). PRIMARY

PRODUCTION

Mean photos~thetic carbon assimilation normalized to Chl a biomass decreased with age of newly formed sea ice (Fig. 6). Mean uptake rates at the three quantum

M. GLEITZ AND D. N. THOMAS

220

mean diatom cell number I -’

(X104,

remaining diatom species Chaetoceroa

dichaeta

Chaetocercw cf. IWOgracile ~~l~~oien

te~u~u~~~s

Nt~sch~a ctos~~u~ Fragitarlopssis cylindrus Fragitertopsis kerguelensis Nltzschla lecointei

ow

GR

PCI

PC II

CIS

Sample Type

Fig. 4. Relative abundance (% of mean cell number) of diatom species in samples collected during ANT X/3. Abbreviations as in Table I.

irradiances ranged from 0.25 to 0.52 mg C*mg Chl a-‘-h-’ in OW and GR samples, increasing with increasing light levels. However, uptake rates recorded for sample type CIS did not exceed 0.2 mg Cemg Chl a-‘*h-*, and was similar at all 3 irradiances. Average cell-specific carbon uptake rates ranged from 2.5 to 4 in OW samples, and decreased in the course of sea-ice formation to 0.3 pg C=cell-‘ah-’ (CIS). Similar to Chl a-specific photosynthesis, no increase in cell-specific photosynthetic carbon assimilation was observed with increasing irradiance in sample type CIS. However, the increase in cell concentration (Fig. 3) overcompensated for the decrease in photosynthetic capacity. Thus, mean primary production based on sample volume increased from 0.05 to 1.5 mg C*m-3*h-’ between sample types OW and CIS. Relative allocation of radiolabelled carbon into the cellular pools of smafl metabolites, polysaccharide, protein and lipid amounted to about 60,20, 10 and lo%, respectively, and did not vary significantly between different sample types (Fig. 7).

DISCUSSION

Changes in physico-chemical parameters (Fig. 2) demonstrated that phytoplankton incorporation into forming sea ice was associated with substantial alterations in the abiotic environment. Within days, microalgae may be exposed to temperatures as low as -6 “C and a ~o~esponding increase in salinity to values P 90 psu. As essentially no salt ions are incorporated into ice crystals, nutrient salts become concentrated in the brine as a function of salinity (Weeks & Ackley, 1982). In samples from ice stages

PHYTOPLANKTON

,6

RESPONSES

C:N

TO SEA-ICE

1500,

FORMATION

221

POC : Chl a

14121086-

2.0

8 _ psi cell“

Prot : Carb

7

0.0 f

I

OW

GR

I

PC1 PCII

1

CIS

OW

GR

PC

I PC11 CIS

Sample Type Fig. 5. Biochemical composition of samples collected during ANT X/3: C:N (w:w), particulate organic carbon (POC):Chl a (w:w), protein:carbohydrate (w:w) and particulate biogenic silicate (ng.cell-I, only diatom cell concentrations were considered). Symbols and abbreviations as in Fig. 2.

PC II and CIS, average nitrate and silicate concentrations normalized to 34 psu were ail below expected concentrations, indicating substantial nutrient utilization, whereas ammonium concentrations often exceeded predicted values. Evidently, incorporated phytoplankton retained the capacity to assimilate nutrients under the transient environmental conditions associated with sea-ice formation. Also, high ~monium levels indicated that nitrogen remineralization by heterotrophic activity exceeded photosynthetic ammonium consumption in many samples collected from older ice stages. In accordance with data presented here, Clarke & Ackley (1984) and Dieckmann et al. (1991) measured nitrate and silicate depletions in Weddell Sea pack ice older than 2 months, which the authors related to algal nutrient uptake. Strong chemical gradients between surface seawater and brine show that fluxes of dissolved matter may be restricted between the brine solution of older new ice and the water column. However, salinity and nutrient values similar to those of surface water were in some cases also recorded in older ice types. Since all CIS samples were collected from sackholes drilled to similar depths (30-40 cm) into floes of various thicknesses, brines with higher salinities were presumably collecteded in the upper, more isolated part of the ice column (thicker floes), whereas values closer to seawater may

222

M. GLEITZ AND D. N. THOMAS

i

0.8 ‘; (D 5 0.6 E” 0.4 0 g 8.2 0.0

4.0 c c c? E 0 in E

3.2 2.4 1.6 0.8 0.0 OW

GR

PCI

PCII

CIS

Sample Type Fig. 6. Photosynthetic carbon assimilation of samples collected during ANT X/3. (A) normalized to Chl a biomass, (B) normalized to total phytoplankton concentration and (C) normalized to sample volume. Columns denote arithmetic mean, bars denote 95% confidence limits. m = 30, a = 90, •I = 160 pmol Par ’ m-2*s-‘. Abbre~ations as in Table I.

characterize brines collected near the ice-water interface. However, inflow of seawater due to hydrostatic pressure equilibration may have also altered the original brine composition, since sackholes sometimes were filled rapidly to sea level. The slight initial increases in cell density, Chl a and POC from OW to GR (Fig. 3) are most likely due to physical concentrations processes, as phytoplankton growth rates at water temperatures close to the freezing point are too slow to account for this increase (Eppley, 1972; Bartsch, 1989). Enrichment factors estimated from cell concentrations at three ice-edge stations where OW and GR were sampled simultaneously (Julian Days 117 to 119, Fig. 1) range from 1.5 to 2.5. Similar values have been reported

PHYTOPLANKTON

RESPONSES TO SEA-ICE FORMATION

223

Low-moleculatweight metabolites Polyssccharide

ow

GR

PCI

PC II

EI

Protein

0

Lipid

CIS

SampleType

Fig. 7. Relative allocation (% of total uptake) of radiolabelled carbon into recent photosynthate of samples collected during ANT X/3. Columns denote arithmetic mean, bars denote 959: confidence limits. Abbreviations as in Table I.

by Grossman & Gleitz (1993) for Antarctic diatom species in a laboratory experiment simulating new ice formation, and by Garrison et al. (1989) in field investigations. The increase from GR to CIS, however, can only be explained by growth of those species capable of acclimating to variations in environmental conditions. Obviously, the change in abiotic conditions from the open water to the ice environment preferentially selects for certain diatoms such as Chaetoceros cf. neogracile, Fragilariopsis cylindrus and Nitzschia lecointei (Table II, Fig. 4). Physiological acclimation capacity resulting in differential growth rates may be one factor responsible for compositional changes. Many species observed in the open water were also present at low relative abundances in older ice, indicating cessation of growth (Table II). Ecophysiological aspects of sea ice algal assemblages have been studied extensively during the past years, but it is difficult to evaluate the behavior of single species from results obtained with mixed and diverse field samples (Rivkin, 1985; Thomas & Gleitz, 1993). The responses of individual polar diatoms to abiotic variations relevant to a summer to winter transition have been studied by Palmisano & Sullivan (1982), Bartsch (1989), Aletsee & Jahnke (1992), Gleitz & Thomas (1992) and Grossmann & Gleitz (1993). All species investigated (Amphiprora kufirathii, Fragilariapsis cylindrus, Fragilariopsis curta, Nitzschiafrigida, Thalassiosira antarctica, Thalassiosira sp., Chaetoceros cf. neogracile) continued to divide up to salinities of 100 psu with corresponding temperatures as low as -6 ’ C, even though metabolic rates had clearly

slowed down. The capacity to photoacclimate to an increase in irradiance, which is suggested to occur when ph~opl~kton cells are initially inco~orated into sea ice, was demonstrated in an experiment simulating new ice formation for ~haetoceros cf. neogracife by Gleitz & Thomas (1992). However, most of the species investigated are

224

M. GLEITZ AND D.N. THOMAS

abundant constituents of sea ice algal communities, and the observed tolerance to thermohaline stress is not very surprising. In general, polar diatom species are able to acclimate to a wide range of different light, salinity and temperature conditions (Horner, 1985; Palmisano & Sullivan, 1985a; Horner et al., 1992). Thus, physiological parameters alone do not explain the differential success of certain diatom species in sea ice. Pore space in sea ice is in thermodynamic equilibrium with the ice temperature, decreasing with decreasing temperatures (Maykut, 1985). A mean diameter of 200 pm was measured for brine channels of Weddell Sea pack ice, and channel n~ro~ng to diameters of 5 to 100 pm is frequently observed in photo~aphs of brine channel casts (Weissenberger et al., 1992). Therefore, during ice formation, phytoplankton cells experience a dramatic decrease in space availabie for colonization. Ceil dimensions of diatom species identified in this study are given in Table III, and it may be noted that the three diatom species dominating CIS samples belong to the smallest diatoms found in this study (the larger species of Nitzschia Iecointei were only found in early ice stages). It seems that spatial confinement severly inhibits the growth of species exceeding 40 pm in any dimension. Also, mechanical destruction of large or long spined species

TABLE III Cell dimensions of diatom species identified in samples collected during ANT X/3. Apical axis (pm)

Transapical axis (pm)

Pervalvar axis (timI

Valve diameter (pm)

10-40 8-15 8-12 z-10 20-30 40-200 100-200 30-55

20-40 10-25 9-18 2-10 20-30 10-20 20 7-12 30-70 10-20

Centrales Chaetoceros bulbosum (Ehrenberg) Heiden Chaetoceros dichaeta Ehrenberg Chaetoceros pendulum Karsten Chaetoceros cf. neogracile Chaetoceros crio~hi~umCastracane Corethron c~o~hi~urnCastracane ~a~~~l~~~ole~ a~larct~~~ Castracane ~a~t~iioso~entenu@mctus (Man~in) Eucampia antarctica (Castracane) Mangin Rhizosolenia truncata Karsten

70-200

Pennales Amphiprora spp. Haslea sp. Manguinea sp. Nitschia turgidula Hustedt Nitzschia prolongatoides Hasle Nitzschia closterium (Ehrenberg) W. Smith Nitzschia tecointei Van Heurck Fragiiatiopsis rhombica (O’Meara) Hustedt Fragila~opsis ke~e~ens~ (omega) Hustedt Fra~~a~opsis curta (Van Heurck) Hustedt Fragilariopsis cylinders (Grunow) Krieger

40 150

50-100 30-80 20-70 120 25-160 20-25 40 1O-40 5-30

20 50 15-20 2-4 l-3 10 3-20 5-15 10 4-6 1-6

PHYTOPLANKTON

during ice formation 1989). In a laboratory

may preclude experiment

225

RESPONSES TO SEA-ICE FORMATION

colonization simulating

of the ice by these species (Bartsch,

new ice formation

with Antarctic

of a large Thalassiosira tumida and Fragilariopsis curta, Grossmann

& Gleitz

clones (1993)

estimated that > 50% of the T. tumida cells were destroyed during ice incorporation. F. curta had a mean of > 50 cells per chain prior to ice formation. Following ice incorporation, chains consisted of only three cells, and individual cells were regularly observed. From the data summarized here, we conclude that spatial confinement in the course of ice formation must have a significant influence on species distribution within the sea ice channel system, resulting in preferential accumulation of smaller species. Different overwintering strategies may also play a role in determining variations in species abundance. Garrison & Buck (1985) suggested that sea ice and open water may be a closely coupled system, with some species utilizing the ice as a habitat, while others may form resting stages and only use it as a means to overwinter. Fryxell (1989) observed auxospore and resting cell formation of Corethron criophilum, Eucampia antarctica and Chaetoceros criophilum in the open waters of the northwestern Weddell Sea during autumn, indicating that some species might not grow when incorporated into ice. Additionally, protozooplankton grazing may also influence species composition. Selective feeding by grazers on Fragilariopsis cylindrus within ice has been suggested by .Fryxell (1989). Larger, presumably heterotrophic dinoflagellates, ciliates and tintinids as well as faecal pellets were frequently observed in our samples, indicative of protozooplankton grazing. However, observations made during this study are inadequate to comment on possible zooplankton feeding strategies. No distinct changes in C:N and protein:carbohydrate ratios were observed in samples collected during sea-ice formation (Fig. 5). High C:N (> lo), low protein:carbohydrate ratios (< 0.3) and an enhanced carbon flow into storage compounds has been interpreted as an indication for nitrate deprived metabolism of sea-ice microalgae (McConville et al., 1985; Palmisano & Sullivan 1985b; Cota & Sullivan 1990; Gosselin et al., 1990; Lizotte & Sullivan, 1992). In the present study, C:N ratios generally ranged between 5 and 9, indicating that algal metabolism was not severly nitrogen limited. This conclusion is supported by protein:carbohydrate ratios (mostly > 0.3) and carbon allocation patterns (Fig. 7) which remained essentially constant between the different ice types. Carbon incorporation into carbohydrate or lipid pools was generally low (lo25% of total uptake) and did not increase during ice formation. Nutrient determinations support the conclusion drawn above, since only few samples showed severe nitrate depletions (< 3 PM, Fig. 2). Also, in these samples, enhanced ammonium concentrations (3-8 PM) may have partly compensated for the low nitrate content. Ratios of POC:Chl a are higher than values typically reported for sea ice algal assemblages (Lizotte & Sullivan, 1992; Gosselin et al., 1990) suggesting that non-algal and detrital carbon contributed significantly to POC (Daly, 1990). The decrease in cellular particulate biogenic silicate is consistent with the observed dominance of smaller diatom species in older new ice samples (Fig. 4). Ice algal photosynthetic capacity normalized to Chl a biomass and to cell density

226

M. GLEITZ AND D.N. THOMAS

decreased during sea-ice formation (Fig. 6). Changes observed in abiotic parameters (e.g. increase of salinity, decrease of temperature; Fig. 2) may have impaired photosynthetic capacity in samples collected from advanced new ice stages. A decrease in photosynthetic capacity as a response to an increase of salinity (and/or decrease of temperature) has frequently been observed in studies with natural ice algal communities (Palmisano et al., 1987a; Kottmeier & Sullivan, 1988; Arrigo & Sullivan, 1992). However, vacations were more pronounced than would be expected from the photosynthesis vs. salinity vs. temperature experiments cited above, and additional aspects may have to be considered. We hypothesize that a decrease in light availability also influenced photosynthetic performance, and the decrease in Chl a specific photosynthesis may indicate changes in the photophysiological status of the assemblages. The thickening of the ice sheet in conjunction with increasing snow accumulations on the ice surface during sea-ice formation and the progression of the season obviously results in a reduced light supply to interior algal assemblages (Table I), (Palmisano et al., 1987b; Watanabe & Satoh, 1987). Microalgal cells, including ice algae, generally respond to such a change by increasing cellular pigment concentrations, thereby increasing the number or size of photosynthetic units (Barlow et al., 1988; Falkowski & LaRoche, 1991). POC:Chl a ratios were generally lower in samples collected from ice types PC II and CIS (Fig. S), which may denote an increase in Chl a concentration of the algae. A decrease in the light level required for and of the magnitude of light saturated photosynthesis (normalized to Chl a) is frequently observed during shade acclimation in pack ice microalgae (Gleitz & Kirst, 1991; Lizotte & Sullivan, 1991), and changes in the photosynthetic performance recorded during ice formation apparently follow this trend: Lowest uptake rates were measured for samples taken from a consolidated, closed pack ice sheet (CIS), where photosynthesis appeared to be saturated at the lowest light intensity employed, in contrast to photosynthetic uptake rates measured in OW or GR samples (Fig. 6). We suggest that photoacclimation potential apparently is a key factor in determining rates of primary production of pack ice assemblages during autumn. In samples from ice stages PC II and CIS, Chl a concentrations on an area1 basis ranged from 1 to 30 mgem-‘, with most values falling below 5 mg.me2 (J. Weissenberger, unpubl. results). Thus, for an average production of 0.2 mg C*mg Chl a-‘*h-i at an irradiance of 30 pmol PAR*m-2*s-’ (Fig. 6), primary production in newly formed sea ice is estimated to usually not exceed 1 mg C*m-2*h-‘. This estimate is similar to values reported by Garrison & Buck (1991) for ice assemblages during spring, other production estimates for spring and summer communities, however, are usually higher by 1-2 orders of magnitude (Burkholder & Mandelli, 1965; McConville et al., 1985; Grossi et al., 1987). We conclude that the contribution of ice-based late season primary production to annual production may be rather insignificant. This study has clearly shown that certain diatom species are able to acclimate to the new ice en~ronment and continue to grow despite large variations in prevailing abiotic conditions. The microalgal community in newly formed sea ice may be important

227

PHYTOPLANKTONRESPONSESTOSEA-ICEFORMATION

for ice associated heterotrophs during the winter period, when phytoplankton biomass in the water column is extremely low (Bartsch, 1989). Ice algae located at the ice - water interface provide a concentrated food source for Antarctic krill Euphausia superba (Marschall, 1988; Stretch et al., 1988). Daly & Macaulay (1988) observed larval and juvenile krill feeding on the underside of ice floes during autumn in the marginal ice zone of the western Weddell Sea. Larval krili continued to grow during the winter season, ingesting an estimated 10% of body carbon per day, of which ice diatoms con~ibuted a si~ifi~~t fraction. Seasonal pack ice serves as a rich nursery ground and provides refuge from predators for young krill during winter (Daly, 1990).

ACKNOWLEDGEMENTS

Thanks are due to G. Dieckmann, D. Garrison, R. Gradinger, S. Grossmann and J. Weissenberger for their assistance in the field. We are greatful to U. Klauke and M. St&ken-Rodewald for nutrient determinations, and to S. Kratzer and E.-M. Nothig for doing the cell counts and species identification. The help from the Captain and crew of R V P~~~rs~~~~ is kindly acknowledged. We thank G. Dieckmann and K. Lochte for helpful comments on the m~uscript. Publication 65 I of the Alfred-Wegener-Institut fur Polar- und Meeresforschung.

REFERENCES Aletsee, L. & J. Jahnke, antarctica Comber

1992. Growth

T., D. Dyrssen

& S. Fonseiius,

1983. Determination

ads qfseawater analysis, edited by K. Grasshoff, second Arrigo,

physiological

characteristics

of alkalinity

M. Ehrhardt

of Sciences,

National

of salinity

sea ice microalgae.

of sea ice and its tensile strength.

Research

R.C., M. Gosselin,

1988. Photoadaptive

1992. The influence of Antarctic

Assur, A., 1958. Composition

Bartsch,

Thcdassiosira

marine diatoms

at temperatures

below the freezing point

and total carbonate.

In, Mech-

& K. Kremling,

Verlag Chemie, Weinheim,

and temperature

covariation

edition, pp. 99-123.

K.R. & C.W. Sullivan,

Barlow,

of the psychrophilic

in batch cultures

pp. 643-647.

of sea water. Polar Biol., Vol.11, Almgren,

and productivity

and Nitzschiafrigidu Grunow

Council,

L. Legendre,

strategies

Washington

on the photo-

pp. 746-756.

In, Arctic sea ice, U.S. National

D.C., publication

J.-C. Therriault,

in sea-ice microalgae.

J. Phycol.. Vol.28,

S. Demers,

Academy

598, pp. 106-138.

R.F.C.

Mantoura

& C.A. Llewellyn,

Mar. Ecol. Prog. Ser., Vol. 45, pp. 145-152.

A., 1989. Die Eisalgenflora des Weddellmeeres (Antarktis): Artenzusammensetzung und Biomasse sowie

dkophysiologie ausgewiihlter Arten. (German Bradford,

utilizing the principle Burkholder,

with English

Rep. Polar Res., Vol. 63, 110 pp.

abstract).

M.M., 1976. A rapid and sensitive method for the quantification of protein-dye

P.R. & E.F. Mandelli,

binding.

of microgram

quantities

of protein

Analyt. Biochem., Vol. 72, pp. 248-254.

1965. Productivity

pp. 872-874. Clarke, D.B. & SF. Ackley, 1984. Sea-ice structure

of microalgae

and biological

in Antarctic

sea ice. Science, Vol. 149,

activity in the Antarctic

marginal

ice zone.

J. Geopkys. Res., Vol. 89, No. C2, pp. 2087-2095. Cota,

G.F.

Antarctic.

& C.W.

Sullivan,

1990. Photoadaptation,

J. Phycof., Vol. 26, pp. 399-41 I.

growth

and production

of bottom

ice algae in the

228

M. GLEIT’Z AND D. N. THOMAS

Daly, K.L., 1990. Overwintering development, growth, and feeding of larval Euphausia superba in the Antarctic marginal ice zone. Limnol. Oceanogr., Vol. 35, pp. 1564-1576. Daly, K.L. & M.C. Macaulay, 1988. Abundance and distribution of krill in the ice edge zone of the Weddell Sea, austral spring 1983. Deep-Sea Res., Vol. 35, pp. 21-41. Dieckmann, G.S., M.A. Lange, S.F. Ackley & J.C. Jennings, Jr., 1991. The nutrient status in sea ice of the Weddell Sea during winter: effects of sea ice texture and algae. Polar Biol., Vol. 11, pp. 449-456. Eicken, H., 1992. The role of sea ice in structuring Antarctic ecosystems. Polar Biol., Vol. 12, pp. 3-13. Eicken, H. & M.A. Lange, 1989. Development and properties of sea ice in the coastal regime of the Southeastern Weddell Sea. J. Geophys. Res., Vol. 94, pp. 8193-8206. Eppley, R.W., 1972. Temperature and phytoplankton growth in the sea. Fish. Bull., Vol. 70, pp. 10631084. Evans, C.A. & J.E. O’ReilIy, 1983. A Handbook for zhe Measurement of Chlorophyll a in Netplankton and Nannoplankton. SCAR/SCOR/IABO/ACMRR Group of Specialists on Living Resources of the Southem Ocean, BIOMASS Handbook No. 9,44 pp. Falkowski, P.G. St J. LaRoche, 1991. Acclimation to spectral irradiance in algae. J. Phycol., Vol. 27, pp. 8-14. Fryxell, G.A., 1989. Marine phytoplankton at the Weddell Sea ice edge: Seasonal changes at the specific level. Polar Biol., Vol. 10, pp. l-18. Garrison, D.L., 1991. Antarctic sea-ice biota. Am. Zool., Vol. 31, pp. 17-33. Garrison, D.L. & K.R. Buck, 1985. Sea-ice communities in the Weddell Sea: Species composition in ice and plankton assemblages. In, Marine biology ofpolar regions and e&=ctsofstress on marine organisms, edited by J.S. Gray & M.E. Ch~sti~sen, Wiley & Sons, New York, pp. 103-122. Garrison, D.L. & K.R. Buck, 1986. Organism losses during ice melting: a serious bias in sea ice community studies. Polar Biol., Vol. 6, pp. 237-239. Garrison, D.L. & K.R. Buck, 1991. Surface-layer sea ice assemblages in Antarctic pack ice during the austrd spring: environmental conditions, primary production and community structure. Mar. Ecol. Prog. Ser., Vol. 75, pp. 161-172. Garrison, D.L., S.F. Ackley & K.R. Buck, 1983. A physical mechanism for establishing algal populations in frazil ice. Nature, Vol. 306, pp. 363-365. Garrison, D.L., A.R. Close & E. Reimnitz, 1989. Algae concentrated by frazil ice: evidence from laboratory experiments and field measurements. Ant. Sci., Vol. 1, pp, 313-316. Gleitz, M. & G.O. Kirst, 1991. Photosynthesis-irradiance relationships and carbon metabolism of different ice algal assemblages collected from Weddell Sea pack ice during austral spring (EPOS 1). Polar Bill., Vol. 11, pp. 385-392. Gleitz, M. & D.N. Thomas, 1992. Physiological responses of a small Antarctic diatom (Ch~t~eros sp.) to simulated environmental contraints associated with sea-ice formation. Mar. Ecol. Prog. Ser., Vol. 88, pp. 211-278. Gosselin, M., L. Legendre, J.-C. Therriault & S. Demers, 1990. Light and nutrient limitation of sea-ice microalgae (Hudson Bay, Canadian Arctic). J. Phycol.. Vol. 26, pp. 220-232. Goyet, C. & A. Poisson, 1989. New determination of carbonic acid dissociation constants in seawater as a function of temperature and salinity. Deep-Sea Res., Vol. 36, pp. 1635-1654. Grasshoff, K., 1983. Determination of pH. In, Methods of seawater analysis, edited by K. Grasshoff, M. Ehrhardt & K. Kremling, Verlag Chemie, Weinheim, second edition, pp. 85-97. Grossi, S.M., S.T. Kottmeier, R.L. Moe, G.T. Taylor & C.W. Sullivan, 1987. Sea ice microbial communities. VI. Growth and primary production in bottom ice under graded snow cover. Mar. Ecoi. Prog. Ser., Vol. 35, pp. 153-164. Grossmann, S. & M. Gleitz, 1993. Microbial responses to experimental sea-ice formation: implications for the establishment of Antarctic sea-ice communities. J. Exp. Mar. Biol. Ecol., this issue, pp. 273-289. Hellmer, H.H. & M. Bersch, 1985. The Southern Ocean. A survey of oceanographic and marine meteorological research work. Rep. Polar Res., Vol. 26, 115 pp.

PHYTOPLANKTON Homer,

R.A.,

1985. Ecology

Boca Raton, Homer,

Florida,

R.A., SF.

Reeburgh,

229

FORMATION

In, Sea ice biotu, edited by R.A. Homer,

of sea ice microalgae.

Ackley, G.S. Dieckmann,

B. Gulliksen,

& C.W. Sullivan,

CRC Press,

T. Hoshiai,

1992. Ecology

L. Legendre,

of sea ice biota.

LA. Melnikov,

1. Habitat,

terminology,

W.S. and

Polar Biol., Vol. 12, pp. 417-427.

T., 1977. Seasonal

change

of ice communities

Polar oceans, edited by M.J. Dunbar, versity, Montreal, Hoshiai,

TO SEA-ICE

pp. 83-104.

M. Spindler

methodology. Hoshiai,

RESPONSES

Proceedings

in the sea ice near Syowa

of the Polar Oceans

Station

Conference

Antarctica.

held at McGill

In, Uni-

May 1974, pp. 307-3 17.

T., 1981. Proliferation

of ice algae in the Syowa

Res., Series E, Biology and Medical

Station

Science No. 34, National

area, Antarctica.

Institute

iwem.

Nat. Inst. Polar

of Polar Research,

Tokyo, Japan,

pp. t-12. Hoshiai,

T., 1985. Autumnal

proliferation

food webs, edited by W.R.

of ice-algae

Siegfried,

sea-ice. In, Antarctic nutrient cycles and

in Antarctic

P.R. Condy

& R.M.Laws,

Springer

Verlag,

Berlin,

Heidelberg,

pp. 89-92. Kochert,

G., 1978. Carbohydrate

determination

by the phenol-sulfuric

In, Handbook of phy-

acid method.

cological methods. Physiological and biochemical methods, edited by J.A. Hellebust bridge University Konig-Langlo,

Press, Cambridge,

& J.S. Craigie,

Cam-

pp. 95-97.

G., 1992. The meteorological

data of the Georg-von-Neumayer-Station

(Antarctica)

for 1988,

1989, 1990 and 1991. Rep. Polur Res., Vol. 116, 70 pp. Koroleff,

F., 1983. Determination

Ehrhardt

& K. Kremhng,

Kottmeier,

ST. & C.W. Sullivan,

linity on rates of meta~lism Lange,

M.A.,

H.E. Glover

& 1. Morris,

pack ice: evidence

G.S.

by K. Grasshoff,

M.

pp. 174-183.

communities.

9. Effects of temperature

and sa-

Polur Biol., Vol. 8, pp. 293-304.

and heterotrophs.

Dieckmann

1980. Physiology

& H. Eicken, of carbon

1991. Photosynthesis-irradiance for in situ activity.

M.P. & C.W. Sullivan,

microalgae

1988. Sea ice microbial

edition,

1989. Development

of sea ice in

by Oscillatoriu thiebautii in

assimilation

Sea. Limnol. Oceanogr., Vol. 25, pp. 447-456.

Lizotte, M.P. & C.W. Sullivan, Lizotte,

of seawateranalysis, edited

second

Sea. Ann. Glacial., Vol. 12, pp. 92-96.

the Caribbean Antarctic

Weinheim,

and growth of autotrophs

S.F. Ackley, P. Wadhams,

the Weddell Li, W.K.W.,

In, Methods

of silicon.

Verlag Chemie,

of McMurdo

1992. Biochemical

Sound, Antarctica:

relationships

in microalgae

associated

with

Mar. Ecol. Prog. Ser., Vol. 71, pp. 175-184. composition

and photosynthate

evidence for nutrient

distribution

in sea ice

stress during the spring bloom. Ant. Sci.,

Vol. 4, pp. 23-30. Marschali,

H.-P.,

1988. The overwintering

strategy

of Antarctic

krill under the pack-ice

of the Weddell

Sea.

Polar Biol., Vol. 9, pp. 129-135. Maykut,

G.A., 1985. The ice environment.

Florida,

pp. 21-82.

McConville,

M.J.,

community

C. Mitchell

from annual

In, Sea ice biotu, edited by R.A. Homer,

& R. Wetherbee,

sea ice, East Antartica.

1985. Patterns

of carbon

CRC Press, Boca Raton,

assimilation

in a microalgal

Polar Biol., Vol. 4, pp. 135-141.

Medlin, L.K. & J. Priddle, 1990. Polar marine d&urns. British Antarctic Survey, Cambridge, 214 pp. Palmisano, A.C. & C.W. Sullivan, 1982. Physiology of sea ice diatoms. I. Response of three polar diatoms to a simulated Palmisano,

summer-winter

transition.

A.C. & C.W. Sullivan,

J. Phycol., Vol. 18, pp. 489-498.

1985a. Growth,

Sea ice biora, edited by R.A. Horner,

metabolism,

and dark survival in sea ice microalgae.

CRC Press, Boca Raton,

A.C. & C.W. Sullivan,

croalgae Palmisano,

from McMurdo Sound, Antarctica. Limnol. Oceanogr., Vol. 30. pp. 674-678. A.C., J.B. SooHoo & C.W. Sullivan, 1987a. Effects of four environmental

Palmisano, Changes

relationships

in Antarctic

of photosynthetic

sea-ice microalgae.

A.C., J.B. SooHoo,

R.L. Moe & C.W. Sutlivan,

in under-ice

irradiance

spectral

nities. Mar. Ecol. Prtrc. Ser., Vol. 35, pp. 165-173.

carbon

assimilation

in sea-ice mivariables

on

Mar. Biol., Vol. 94, pp. 299-306.

1987b. Sea ice microbial

during the development

In,

pp. 131-146.

Palmisano,

photosynthesis-irradi~ce

1985b. Pathways

Florida,

of Antarctic

comm~ities.

sea ice microalgal

VII: commu-

230

M. GLEITZ

AND

D.N.

THOMAS

Priddle, J. & G. Fryxell, 1985. Handbook of the common plankton diatoms of the southern ocean: centrales except the genus Thalassiosira. British Antarctic Rivkin, R.B., 1985. Carbon-14

Survey,

labelling patterns

Cambridge,

159 pp.

of individual

marine phytoplankton

from natural

popula-

tions. Mar. Biol., Vol. 89, pp. 135-142. Round,

F.E.,

Cambridge

R.M.

Crawford

University

Spies, A., U.H. Brockmann land Sea in summer. Spindler,

& D.G.

1990. The diatoms. Biology and morphology of the genera.

Mann,

Press, Cambridge,

747 pp.

& G. Kattner,

1988. Nutrient

regimes in the marginal

ice zone of the Green-

Mar. Ecol. Prog. Ser., Vol. 47, pp. 195-204.

M., G. Dieckmann

& D.N. Thomas,

1993. The expedition

ANTARKTIS

X/3 of RV “Polarstern”

1992. Rep. Polar Res., Vol. 121, 122 pp. Stretch, J.J., P.P. Hamner, of antarctic Thomas,

W.M. Hamner,

W.C. Michel, J. Cook & C.W. Sullivan,

krill Euphausia superba on sea ice microalgae.

D.N. & M. Gleitz,

tions: Variation

1993. Allocation

between two diatom

1988. Foraging

behavior

Mar. Ecol. Prog. Ser., Vol. 44, pp. 131-139.

of photoassimilated

carbon

into major algal metabolite

species isolated from the Weddell Sea (Antarctica).

frac-

Polar Biol., Vol.

13, pp. 281-286. Thomas,

D.N., M.E.M.

Baumann

tion in a small unicellular ture and irradiance. Utermdhl,

& M. Gleitz,

1992. Efficiency

of carbon

Chaetoceros species from the Weddell

assimilation

Sea (Antarctica):

and photoacclimainfluence

of tempera-

J. Exp. Mar. Biol. Ecol., Vol. 157, pp. 195-209.

H., 1958. Zur Vervollkommnung

der quantitativen

Phytoplankton-Methodik.

Int. Ver. Theor.

Angew. Limnol. Mittlg., Vol. 9, pp. l-38. Watanabe,

K. & H. Satoh,

Antarctica,

1987. Seasonal

variations

Weeks, W.F. & S.F. Ackley, 1982. The growth, Cold Reg. Res. and Eng. Lab., Hanover, Weissenberger,

crop near Syowa

Station,

East

structure,

brine pockets

of sea ice. CRREL Monograph 82-1,

in den Solekanalchen

des antarktischen

Meereises.

(Ger-

Rep. Polar Res., Vol. 111, 159 pp.

J., G. Dieckmann,

ine and analyze

and properties

N.H., 130pp.

J., 1992. Die Lebensbedingungen

man with English abstract). Weissenberger,

of ice algal standing

in 1983184. Bull. Plankton Sot. Jpn. Vol. 34, pp. 143-164.

R. Gradinger and channel

& M. Spindler,

structure.

1992. Sea ice: A cast technique

Limnol. Oceanogr., Vol. 37, pp. 179-183.

to exam-