Sea ice microbial communities (SIMCO)

P o l a r Biol (1983) 2:171 - 177

© Springer-Verlag 1983

Sea Ice Microbial Communities (SIMCO) 1. Distribution, A b u n d a n c e , and Primary P r o d u c t i o n of Ice Microalgae in M c M u r d o S o u n d , Antarctica in 1980 A. C. Palmisano and C. W. Sullivan Marine Biology Research Section, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089/0371, USA Received 20 May 1983; accepted 12 August 1983

Summary. Algal standing crops for the 1980 McMurdo Sound sea ice microbial communities (SIMCO) averaged 131 ( + 121) mg chl a • m -2 despite strong attenuation of downwelling irradiance by snow and ice cover. Using a C : chl a ratio of 31, annual sea ice production was estimated at 4.1 gC - m -2. S I M C O standing crops in the West Sound, previously considered a biologically depauperate region due to persistent ice cover and local current regimes, were greater than or equal to those of the East Sound when areas of similar ice thickness were compared. Biomass was located almost entirely in the b o t t o m 20 cm of annual ice including over 99O7o of the chlorophyll a and A T P , and 93°7o of the particulate organic carbon. During the ice algal bloom, concentrations of chlorophyll a in the b o t t o m 20 cm of ice averaged 656 mg • m - 3 , 2000 times greater than under ice phytoplankton at 1 m depths. Phaeopigment: chlorophyll a ratios (P : C) were significantly higher in the upper ice column than in the b o t t o m 20 cm. An hypothesis is presented that the ice contains a frozen record of P : C ratios in the surface seawater during ice formation. Photosynthetic rate of ice microalgae measured in the laboratory under simulated in situ conditions ( - 1 . 9 ° C ; 0.3 to 13 ~tE . m - 2 . s -S) ranged f r o m 0.6 to 7.5 mg C fixed • m g chl a -~ • d a - k It was concluded that the b o t t o m type S I M C O contributes a considerable amount of new carbon to McMurdo Sound during the austral spring.

Introduction Polar marine environments are characterized by the extensive coverage of annual sea ice reaching up to 22 x 106 k m 2 in the antarctic (Mackintosh 1972) and 15.6 x 1 0 6 m 2 in the arctic (Nazarov 1963). In McMurdo Sound, Antarctica annual bay-fast sea ice undergoes a yearly cycle of formation and deterioration in which thicknesses of three meters or more may be reached (Paige 1966).

In both the antarctic and the arctic, annual sea ice provides microhabitats for the growth of unique sea ice microbial communities (SIMCO) (Bunt 1968; H o m e r 1976). Diatoms predominate in these communities which bloom in the austral spring; but other microalgae (Ackley et al. 1979), bacteria (Sullivan and Palmisano 1981) and protozoans (Fenchel and Lee 1972; Lipps and Krebs 1974) are also present. Several investigators have coined terms to describe SIMCO such as "epontic" (Bunt and W o o d 1963) meaning "out of the sea" and "sympagic" (Whitaker 1977) meaning "with ice." To avoid ambiguity, however, we have chosen to designate three distinct types of S I M C O based on their location within the ice column (Ackley et al. 1979): 1) surface melt pool and infiltration ice communities (Meguro 1962; Burkholder and Mandelli 1965; and Whitaker 1977); 2) interior communities at intermediate depths within the sea ice (Ackley et al. 1978), and 3) b o t t o m ice communities which may include microorganisms associated with interstitial water in the platelet layer as well as in brine pockets and channels in the congelation ice (Appolonio 1961; Bunt and W o o d 1963; Lewis and Weeks 1970). A dense b o t t o m type SIMCO in the under water ice platelet layer of McMurdo Sound was first described by Bunt and W o o d (1963). This potentially large source of carbon and energy for Antarctic marine ecosystems has received little attention since the pioneering work of Bunt and his coworkers over a decade ago. The objectives of this study on the McMurdo Sound S I M C O in 1980 were twofold: 1) to examine the areal and vertical distribution and abundance of microalgae, and 2) to estimate rates of primary production by the ice microalgal community.

Methods Field studies were conducted on annual sea ice in McMurdo Sound, Antarctica at six sites shown in Fig. 1. Ice and seawater samples were collected between 10 Nov 1980 and 16 Dec 1980 during the austral spring sea ice algal bloom.

172 0 e

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170"

168"

166"

164" 163°W

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To measure particulate organic carbon (POC), aliquots of ice melt water were filtered onto GF/C filters, placed in ampules, and frozen. Both filters and vials were precombusted at 500°C for 24 h. Frozen samples were returned to the University of Southern California for analysis with an infrared gas analyzer (Oceanography International Corp., College Station, Texas) by the wet oxidation methods of Menzel and Vaccaro (1964). Adenosine triphosphate (ATP) was extracted and analyzed in triplicate by the methods of Karl and Holm-Hansen (1978). Aliquots of ice melt were filtered onto GF/C filters, rapidly immersed in 5 ml boiling 20 mM Tris buffer (pI-t 7.8), and boiled for 5 min. ATP determination was performed on a Labline ATP photometer (SAI, San Diego, CA) using luciferin-luciferase extract (SAI) in EDTA-MgSO 4 buffer on peak height mode (6 s). Samples preserved in 2% glutaraldehyde were returned to the University of Southern California where they were prepared for scanning electron microscopy on 0.2 ~tm pore size Nuclepore filters by the methods of Paerl and Shimp (1973) except that ethanol was substituted for acetone in the dehydration step. The dehydrated sample was critical point dried, sputter-coated with gold-paladium, and examined in a Cambridge scanning electron microscope or a Hitachi model scanning transmission electron microscope at Scripps Institution of Oceanography. Under ice irradiance was measured by SCUBA divers with a QSI140 underwater radiometer (Biospherical Instruments, La Jolla, CA). An environmental chamber was constructed in which irradiance was calibrated to match under ice measurements (Palmisano and Sullivan 1982). Light was provided by cool-white fluorescent bulbs equipped with blue-green (450-550 nm) filters to mimic the under ice light spectrum (Maykut and Grenfell 1975). The chamber was maintained at - 1.8 °C -+ 0.2 °C (ambient water temperature in McMurdo Sound) by a Frigomix-Thermomix unit (Braun), with an ethylene-glycol/water bath. To measure photosynthetic rate, samples of ice microalgae at the ice-seawater interface were collected by divers at Cape Armitage. Sterile, opaque black jars of 500 ml volume were pushed into the algal layer, covered with lids, and returned to the surface. Samples were kept in an insulated light-proof container en route to the Eklund Biological Laboratory. The uptake of HI4CO3 was determined by the methods of Strickland and Parsons (1972). Sixty ml samples were incubated in light or dark bottles with 5 gCi H14CO3 (New England Nuclear, Boston, MA) for 1 8 - 2 4 h in the environmental chamber. Aliquots of 10 ml were then filtered onto 1.0 ~tm porosity membrane filters (Nuclepore), dried, and assayed in toluene-based scintillation fluid in a Beckman LSC-100 liquid scintillation counter. Counts were corrected by the external standard ratio methods. Data were analyzed by the statistical methods described by Duncan et al. (1977).

Fig. 1. Map of McMurdo Sound, Antarctica showing sampling sites. CR Cape Royds; TR Turtle Rock; CA Cape Armitage; IS Ice Shelf; N H New Harbor

To study the distribution and abundance of microalgae in sea ice, ice samples were collected at five sites with a SIPRE ice auger with a 7.5 cm barrel diameter. Three cores were taken per site within a one meter radius. The bottom 20 cm of the ice, which visual inspection showed to contain the golden-brown microalgal layer, was removed with a stainless steel band saw. The remainder of the core was sectioned bottom to top in 50 cm lengths. Ice samples were placed in plastic bags in Freezesafe styrofoam containers to protect them from high light and temperatures less than - 2 ° C and transported to the Eklund Biological Laboratory at McMurdo Station. Ice sections were allowed to melt at 0 - 5 °C prior to analysis for biomass. All operations were conducted in low light conditions. At each site, seawater samples were collected at 1 m depths below ice with a Kemmerer PVC water sampler. Samples for chlorophyll a and phaeopigment analysis were collected on glass fiber filters (GF/C, Whatman) and extracted in 90% acetone for 17 h. Concentrations of chlorophyll a and phaeopigments were determined in duplicate with a Turner 111 fluorometer equipped with a high-sensitivity door and a red-sensitive photomultiplier (Holm-Hansen et al. 1965).

Results

A n n u a l s e a ice in M c M u r d o S o u n d f o r m e d in A p r i l 1980 f o l l o w i n g a m a j o r b r e a k o u t t h a t e l i m i n a t e d all a n n u a l a n d s o m e m u l t i y e a r s e a ice i n t h e s o u n d ( G o w et al. 1981). B y N o v e m b e r , ice t h i c k n e s s r a n g e d f r o m 133 c m a t t h e ice e d g e a t C a p e R o y d s ( T a b l e 1) t o 2 5 5 c m a t t h e e d g e o f t h e R o s s Ice S h e l f . T h e ice w a s p r i m a r i l y o f t h e congelation type; however, a sub-ice platelet layer of up t o s e v e r a l t e n s o f c e n t i m e t e r s in t h i c k n e s s w a s p r e s e n t i n s o m e a r e a s o f t h e S o u n d ( G o w et al. 1981). S n o w a n d ice depths on the East and West Sound were not significantly d i f f e r e n t ( p o o l e d t-test). T h e r e was n o significant d i f f e r e n c e ( p o o l e d t-test) in t h e t o t a l a m o u n t o f c h l o r o p h y l l a • m - 2 a n n u a l ice i n t h e

173 Chlorophyll o (mg.m-3)

Table 1. Annual sea ice and snow thickness in McMurdo Sound, 1980 lO-] I

10-2 Site

Date

Snow (cm)

ice surface

Ice (cm)

10 o I

I01 I

102 I

104

I0 3 I

0-?-0 cm SITOW

I

>170

5o] Cfll

East Sound Cape Royds Turtle Rock Ice Shelf Edge

11-24-80 12-1-80 12-4-80

1.5 0 2.0

133 205 255

120-170

I

I cm I. . . .

70-]20

West Sound New Harbor I New H a r b o r II

I

11-28-80 11-28-80

1.5 0

220 205

50 em L. . . .

20-70

,50 l em

0-20

Table 2. Chlorophyll a and Particulate Organic Carbon (POC) in East

under ice seawater

and West Sound A n n u a l Sea Ice. Value are Y~ _+ SD of three cores sampled in a 1 m radius at each site Site

Date

Chlorophyll a mg. m 2

11-24-80 12-1-80 12-4-80

202 25.1 52.1 93.1

' 1

I

I

20

i

cm

i

Fig. 2. Vertical profiles of chlorophyll a in ice cores from McMurdo Sound. Means and ranges for five vertical sections of 15 ice cores and for under ice seawater are shown

POC mg • m -2

East Sound Cape Royds Turtle Rock Ice Shelf Edge East Sound £ _+ SD

_+ 199 _+ 9.1 _+ 5.3 _+ 95.3

3027 3020 1585 2543

_+ 794 _+ 596 _+ 47 _+ 832

Phoeopigrnents (mg.m-3)

lO-Z ice surface

West Sound New Harbor I New H a r b o r II West Sound f~ SD

i00 I

10" I I

10 2 I

i01 I

10 3

I04

I

I

0-?__0cm SnOW =,~