- Email: [email protected]
Benthic microbial activity in an Antarctic coastal sediment at Signy Island, South Orkney Islands
Estuarine, Coastal and Shelf Science (1989) 28,507-516
Benthic Coastal Orkney
Microbial Sediment Islands
Activity at Signy
in an Antarctic Island, South
D. B. Nedwell Department of Biology, University of Essex, Colchester CO4 3SQ, U.K. Received 21 September 1988 and in revisedform 31 January 1989
Keywords: Antarctic; marine sediments; microbial activity; sulphate reduction; pyrite Microbial activity in a marine sediment in Factory Cove, Signy Island (60”43’S, 45”38’W), South Orkney Islands in the maritime Antarctic was examined during December 1987 and January 1988. The sediment was bioturbated by a dense amphipod population in the surface layer but oxygen penetrated to a depth of only 1.7 mm. The top 1 cm was light coloured and contained negligible concentrations of acid-volatile sulphides. Below 1 cm the sediment was black and contained abundant sulphides. Sulphate reduction rates averaged 6.87 x 10-l gmol sulphate cm-*d-l over the O-15 cm horizon, equivalent to 1.38 pmol organic carbon oxidized cn-*d-l. Of the sulphate reduced, 60% was to tin-reducible products (including pyrite) and 40% to acid-volatile sulphides. Annual sulphate reduction was at least 250 )rmol sulphate cm-%-‘. The sea water temperature varied only between - 18-l “C, but the optimum temperature for sulphate reduction was 21 “C. Oxygen uptake by the benthos averaged 5.33 pm01 oxygen cme2d-l, equivalent to 5.33 umol organic carbon oxidized err-*d-l. Aerobic respiration accounted for 79% of the organic carbon mineralization and sulphate reduction for 21%.
Introduction permanently at low temperature, around 0 “C, the Southern Ocean is one of the most productive marine regions of the world (El Sayed, 1984; Komneier & Sullivan, 1987). The organic matter derived from the primary productivity serves asthe substrates for both grazing and detritus-based food webs, and in a steady-state ecosystem primary production is balanced by mineralization of the organic carbon. In the inshore marine environment the bottom sediments are important sites of deposition of organic detritus from the water column, and in boreal regions microbial activity in the sediments contributes substantially to mineralization of organic carbon (Jorgensen, 1983~). Organic mineralization in these sediments is largely brought about by the activity of aerobic bacteria, together with that of sulphate reducing bacteria in the anaerobic regions of sediment below the surface aerobic layer (Sorensen et QZ., 1979). The proportionate contribution of sulphate reduction to organic mineralization is greatest in coastal Although
0272-7714/89/050507
+ 10 $03.00/0
@ 1989 Academic
Press Limited
508
D. B. Nedwell
sediments where there is commonly only a shallow surface aerobic layer, and declines in deeper water where diminished detrital deposition results in more oxidized sediments (Jorgensen, 1982). Despite the permanently low temperature, Antarctic environments support large active populations of microorganisms, someof which are obligatorily psychrophilic, although the majority are facultative psychrophiles (Stanley & Rose, 1967). Representatives of most of the different physiological groups of bacteria which contribute to organic degradation and nutrient recycling have been isolated from Antarctic or other low temperature sea water and sediments(for example, Herbert & Bell, 1974; Herbert & Bhakoo, 1979; Leduc & Ferroni, 1979; Reichert, 1988). Uptake of organics by bacteria, and active microbial growth occur in Antarctic sea water (Hodson et al., 1981; Delille et al., 1988) but the magnitude of their in situ activity in marine sediments is as yet unknown. Delille and Bouvy (1986) reported active sulphate reduction, indicated by sulphide formation, in fjord sediments from the Kerguelen archipelago while Franzmann et al. (1988) reported slow rates of sulphate reduction in brackish sediment from the antarctic lakesand a fjord. Methane formation and sulphate reduction have been reported in the sediments of fresh water lakes of the maritime Antarctic during summer (Ellis-Evan, 1984, 1985), although sulphate reduction was sulphate-limited. These sediments exhibited strong seasonal changesin redox profiles. The current work wasundertaken during the Antarctic summer 1987-88 to measurethe rates of benthic microbial activities which contribute to organic mineralization in an inshore Antarctic marine sediment. Sampling site The work was carried out during December 1987, and January 1988, at the baseof the British Antarctic Survey in the South Orkney Islands-Signy Island (60”43’S, 45’38’W). A singlesampling site wasselectedalong the permanently marked transect ZM 23 in Factory Cove, opposite the base,approximately 100 m offshore under 6 m water (Figure 1). The bottom sediment is never frozen at this site, and seawater temperatures vary seasonally only between - 1.0-1.0 “C (British Antarctic Survey, unpublished data and seeClarke, 1988). The sediment consistedof glacially eroded quartz-micaschist (Hall, 1987)with 70-90% of particles in the fine sandand very fine sandfractions (0.063-0.25 mm diameter) (British Antarctic Survey, unpublished report N5/1975/H). The sediment was blackened below a light brown surface layer approximately 1 cm thick. In the surface layer the amphipods PontogenearotundifrOns and Tryphosa kergueleni were present at population densities of 2-3 x lo3 individuals m- ’ (British Antarctic Survey, unpublished report N5/1981/H). Vertical cores of sediment were taken by SCUBA divers using perspex core tubes (8 cm internal diameter) and sealedwith silicon rubber bungs. The cores were returned to the laboratory within 10 min and were kept at 0 “C in a water bath. Methods St&hate
reduction
A sediment core was extruded and duplicate subsamplesof sediment taken from known depths using 5 ml plastic hypodermic syringes with the luer end removed. The subsampling was carried out in a constant temperature room at 2 “C and the syringes of
Microbial
activity in antarctic coastal sediment
South 46OW
509
Orkney Islands 45OW
South Orkney
Island
Figure 1. Signy Island, and sampling site. Broken line indicates transect Zh423, and sampling site (A).
sediment were immediately capped with butyl rubber septa to exclude oxygen, and placed in a water bath at 0 “C. Each subsamplewas injected with 20 l.d of %-sulphate (Amersham International, U.K.) in sterile seawater [O-4mCi (4.2 MBq) ml-‘; 1150 Ci (42.6 TBq) umol-‘1 via the butyl rubber septum. The needle was slowly withdrawn along the sediment sample during injection to distribute the radiotracer as evenly as possible. The sampleswere incubated at 0 “C for 24 h, and then frozen at - 80 “C until processed. Each sediment samplewas acidified under oxygen-free nitrogen gas(OFN) and acidvolatile sulphides (AVS) carried over in the OFN stream and trapped in 40 ml zinc acetate solution (1 o/0w/v). (The nitrogen gaswasfirst passedthrough chromous acid to remove any traces of oxygen.) After removal of the AVS the residual sediment was digested with tin and tin chloride at 100 “C to recover the tin-reducible sulphides (TRS) which includes pyrite (Skyring, 1985; Nedwell & Takii, 1988). Again, hydrogen sulphide generated during the digestion was swept by the OFN and trapped in 40 ml zinc acetate solution. Duplicate subsamples(2 ml) from the zinc acetate traps for both AVS and TRS were transferred into Instagel (Packard Instruments Ltd, U.S.A.) and radioactivity measured in a liquid scintillation counter (1209 Rackbeta, LKB Ltd, Sweden). Quenching and self absorption in each samplewas subsequently corrected for by internal standardization by adding 20 ~1of 35Ssulphate solution of known activity to every vial. Concentrations
of sulphide
minerals
The residue from each 40 ml zinc acetate trap was titrated with thiosulphate solution to determine the concentrations of AVS and TRS present in each sediment sample (American Public Health Association, 1975).
510
D. B. Nedwell
Sulphate After digestion each sediment sample was filtered through a glass fibre filter paper (GF/C, Whatman), washed three times with distilled water and filtered, and the filtrates bulked together and made up to 100 ml. The sulphate concentration in the filtrate was determined by a barium sulphate turbidimetric technique (American Public Health Association, 1975). Optimum temperature for sulphate reduction Slurries of sediment (50% v/v) in deoxygenated seawater were prepared with sediment from the l-4 cm horizon of a vertical core. This was the horizon within which sulphate reduction was greatest (see Results). Hungate technique was used to exclude oxygen from the slurry, all transfers and manipulations being carried out under a stream of OFN. Aliquots (16 ml) of the slurry were dispensed into 30 ml screw-capped universals, which were placed along an ahuninium temperature-gradient block incubator and allowed to equilibrate to temperature for 1 h. Sodium lactate solution (100 ~1 to give 25 PM final concentration) was injected into each universal, followed immediately by 20 ~1 of 35Ssulphate solution. The lactate was added to provide a supply of electron donor for sulphate reducers. Otherwise, in an electron-donor limited environment, the rates of sulphate reduction measured might be substrate-limited rather than temperature-limited, and so influence the observed optimum temperature for sulphate reduction. The universals were shaken thoroughly and placed back in the gradient block for 15 h. At the end of the incubation period 5 ml zinc acetate solution (5% w/v) was added to each universal to stop further activity and to ‘ fix ’ sulphide until further treatment. Each sample was subsequently acidified, and the radioactivity in the AVS determined as described previously. The aluminium block incubator was heated at one end and cooled at the other by thermocirculators to maintain the temperature gradient. The temperature at each point along the gradient was checked by using a thermometer immersed in water in universals along the gradient, and the gradient was always linear. Two experiments were carried out over temperature ranges between 0.7-25 “C and 17-37 “C. With 14 positions along the gradient, this gave an approximately 1.5 “C temperature difference between adjacent universals. Benthic oxygen uptake Vertical cores of sediment (approximately 20 cm length) were taken from the study site in Factory Cove, and the bottom bung of each core was pushed up until the sediment surface had 11 of seawater above it in the core tube. The cores were then placed in a water bath at 0 “C for 24 h to re-equilibrate after the disturbance of coring. Air was continuously bubbled through the seawater to maintain air-saturated dissolved oxygen (DO) concentrations in the water column. The apparatus was always covered with a double thickness of black polythene sheet to exclude light. After 24 h the core tubes were closed with an airtight perspex cap through which protruded a Clark-type oxygen electrode [Radiometer (UK) Ltd, U.K.] into the water column. A magnetic follower was suspended below the cap in the water column to maintain mixing after the air steam was stopped. The air stream was then cut off and the decrease in DO concentration with time was followed for 4 h. During this time the decrease of DO was sufficient to accurately determine a rate, but the DO was not depleted to the extent that it started to limit the rate of DO transfer across the sediment-water
Microbial
activity in antarctic coastal sediment
Sulphlde -4 I
(log mmol Sq-‘sedlmentl -2 0 ’
-3 . . .
511
’
0.m
-I ‘I-
,.rm
,-
. .
CD
m
.
0
..‘a0
,-
a.
,-
Figure 2. Distribution of sulphides, and oxygen in the sediment (0, acid-volatile sulphide; 0, tin-reducible sulphide; and n , dissolved oxygen). Broken line indicates depth of surface oxidized layer. interface (Jones, 1976). The DO during the experiment did not fall below 80% of the airsaturated value. The percentage saturation of DO was read at 15 min intervals with an oxygen meter (Strathkelvin Instruments, U.K.) and converted to equivalent DO concentration. The air-saturated concentration of oxygen in seawaterat 0 “C was determined as 0.3708 mM (SD 0.0035) by Winklers titration method (Strickland & Parsons, 1972). Three separate cores of sediment were used to measuredecreaseof DO, with duplicate DO uptake measurementson eachcore. Preliminary measurementof oxygen uptake by 11 of seawaterin the absenceof sediment showed no significant decrease,and decreaseof DO from the water column in the presenceof sediment was therefore attributed solely to the respiratory activity of the benthic biota.
Oxygen concentrationprofile in the sediment The oxygen profiles in cores from the sampling site were measured by Dr Ian Hawes (British Antarctic Survey) with a microelectrode (Microsense, Israel) of the design of Revsbech et al. (1980). The oxygen concentrations were determined at 0.1 mm intervals using a micromanipulator to insert the electrode. Specificgravity: water content of the sediment Cores of sediment were taken and frozen at - 20 “C. They were then extruded while still frozen and sectioned with a fine saw. The wet weight of each depth slice wasdetermined, and then each section was dried to constant weight over 3 d at 80 “C to determine the water content. Results The distributions of AVS and TRS with depth in the sediment from Factory Cove are shown in Figure 2. Sulphare reduction rates, including reduction to both AVS and TRS,
512
D. B. Nedwell
log SO,
Reduction
-3 0;
rate
(pmol
S 4-l
-2
sediment
d-l) 0
-1
1 .
. .
. . . .
5-
. .
.
W.
”
.
.
“.
IO -
. . .
.
.
.
.
15 -
20
-
.
. .
.
J Figure
3. Rates of sulphate
Figure
4. Optimum
reduction
Temperature
temperature
in the sediment.
(“Cl
for sulphate
reduction:
(0,
Run 1; and 0, Run 2).
were between 0.1-0.2 umol sulphate g-’ sediment d- ’ in the top O-3 cm, but decreasedby an order of magnitude between 3-5 cm (Figure 3). Below 5 cm the rates of sulphate reduction were uniformly low. Overall, 60% of the sulphate wasreduced to TRS and 40% to AVS, with no obvious trends with depth in the proportions of these end products. Both of the experiments to investigate the optimum temperature for sulphate reduction showed a maximum at about 21 “C (Figure 4).
Microbial
activity in antarctic coastal sediment
513
Linear regressionanalysis of the oxygen uptake data, which conformed to straight lines (P < O-05),showed that in all casesthere were significant decreasesof DO over a 4 h period. Analysis of variance revealed significant differences in the rate measured both between cores and between repeat measurementson the samecore. However, overall the rate of DO change had a mean value of -0.011 (standard error 0.002) umol oxygen h-l, corresponding to an oxygen transfer rate from water into sediment of 5.23 ( f O-95) umol oxygen cme2 d-l. The profiles of oxygen concentration down the sediment showed that oxygen penetrated to a depth of only 15-1.7 mm (seeFigure 2). Discussion Oxygen penetrated only 1.5-1.7 mm into the sediment despite the active bioturbation of the sediment by the amphipod community. Although tin-reducible sulphides (pyrite) were present in the top 1 cm layer there was negligible acid-volatile sulphide, and the top 1 cm of sediment was light brown in colour. Jorgensen (1983b, 1988) has previously pointed out that in temperate coastalmarine sedimentstheremay be only a shallow surface aerobic layer containing oxygen, although below this the sediment may still be chemically oxidized. This oxidized but anoxic layer hasbeen termed the ’ sub-oxic ’ or ‘ Fe-Mn ’ zone (Sorensen & Jorgensen, 1987). Any hydrogen sulphide diffusing upwards from the deeper, reduced anoxic layers may not reach the aerobic layer before it is oxidized at the baseof the sub-oxic layer. This seemsto be the casein this antarctic coastalsediment. The rates of sulphate reduction determined in the cores from the Factory Cove site were first converted from rates on a sediment weight basisto equivalent rates per ml sediment by multiplying by the measuredspecific gravity of the sediment at each depth. These rates were then integrated with depth over the O-15 cm depth by summation of adjacent 1 cm deep slices,and by using linear interpolation and a simple trapezium method to determine integrated sulphate reduction rates between measured horizons. This gave values of 5.507 x 10-l and 8-227 x 10-l umol sulphate cm -2 d-l for each core respectively (average 6.87 x 10-l) over the &15 cm horizon which encompassedthe surface zone of greatest activity. These data contrast with the only other data available for sulphate reduction rates in an Antarctic sediment of 4 x 10m3pmol sulphate cm-‘d-l, in Ellis Fjord, Vestfold Hills, Antarctic (Franzmann et al., 1988), determined by a method identical to that used in the present work. These much slower rates, compared to those at Signy Island, cannot immediately be explained although primary production rates in the waters at Signy appear to be considerably greater than in other Antarctic waters (Horne et al., 1969; Whitaker, 1982; Clarke et al., 1988). This hasbeen attributed to the relatively high light intensities and dissolved nutrient concentrations in thesewaters. Much of the available data for sulphate reduction in other ecosystemsreports average rates per litre of sediment in the O-10 cm horizon (seeNedwell, 1982). In the present casethe rates integrated over the &lo cm horizon were equivalent to 0.05 1 and 0.081 umol sulphate 1-l d-’ for this Antarctic sediment. This is lower than the summer rates reported for temperate coastal and intertidal sediments, although greater than winter rates reported for those environments (see Skyring, 1987). The rates were also greater than those reported for deep ocean sedimentswhere the temperature regime is similar to Antarctic seawater,but where organic input to the sediment from the water column is much less.Nedwell and Abram (1978) reported that in temperate salt marsh sediment temperature variation had the greatest effect on sulphate reduction rates, followed by the availability of electron
514
D. B. Nedwell
donors. In the present case, where seawater temperature remains virtually constant throughout the year, the availability of electron donors derived from organic matter deposited onto the sediment is likely to play a controlling part in any seasonalchangesof sulphate reduction rates in the sediment. The presenceof the large amphipod populations, which visibly bioturbate the surface layer of sediment, will alsotend to enhancethe rate at which deposited organics become incorporated into the sediment, and hence available to the sulphate reducers in the anaerobic layers below the surface aerobic zone. The measurementsreported here were carried out during the Antarctic spring, before the spring algal bloom had started to settle onto the bottom (N. Gilbert, personal communication). They are, therefore, likely to be minimum values for sulphate reduction rates in this environment, and may increase later in the seasonafter deposition of organic detritus to the sediment stimulates sulphate reduction. Bearing in mind, therefore, that these are likely to be minimal estimates,and that the virtually constant seawatertemperature will have little seasonaleffect upon the rates, the depth-integrated daily rates yield annual values of 201 and 300 umol sulphate cm- 2y -l. This compares with estimates of annual sulphate reduction (to AVS only) in temperate salt marsh sediments of between 66-410 umol sulphate crnm2y-’ (Senior et al., 1982) although these estimateshave to be increased substantially if TRS is included (Nedwell & Takii, 1988). Thus, notwithstanding the uniformly low environmental temperature, sulphate reduction in these Antarctic sediments at Signy Island was still significant in magnitude even when compared to sedimentswhich exhibit much higher summer temperatures, but where sulphate reduction is greatly inhibited by low temperatures during winter. In this context it is interesting to note that, although the sulphate-reducing bacteria seem well adapted to their low temperature environment, the optimum temperature for sulphate reduction (21 “C) was nevertheless greatly above the temperature of the environment. Morita (1975) hasdefined obligate psychrophiles as ‘ having an optimal temperature for growth at about 15 “C or lower, a maximal temperature for growth at about 20 “C, and a minimal temperature for growth at 0 “C or lower ‘, and the present data therefore gives little evidence of obligately psychrophilic adaptation by the sulphate reducing bacteria in theseAntarctic sediments. Ellis-Evans (pers. corn.) hasalso found that sulphate-reduction in Signy Island lakeshad an optimum of 26 “C, while Antarctic methanogenic bacteria show little physiological adaptation to low temperature and the optimum for methanogenesis was >30 “C (Ellis-Evans, 1984). The rate of oxygen uptake by the benthic biota was 5.33 umol oxygen cme2 d-r. The amount of organic carbon oxidized can be calculated stoichiometrically from the equation CH,O + O,+ CO, + H,O and was equivalent to 533 umol organic-C cme2 d-l. This represents the organotrophic activity of the total benthic community including both micro- and meio-benthos. It may also include a component resulting from aerobic reoxidation of products of anaerobic metabolism, such as sulphide, although it is not possible to differentiate this within the overall oxygen consumption rate. By comparison, the sulphate-reducing bacteria are the major anaerobic organotrophs in anaerobic marine sedimentsand oxidize organic matter according to the overall equation 2 (CH,O) + SOd2- + 2H+ -+2CO,+H,S
+2H,O
The rates of sulphate reduction for each core, integrated over the &15 cm horizon where sulphate reduction isgreatest, were equivalent to 1.10and 1.65 (mean l-38) umol organic-C
Microbial
activity in antarctic coastal sediment
515
ctn2 d-‘. Assuming that sulphide reoxidation did not significantly contribute to oxygen uptake, the total organic oxidation rate was 5.33+ 1.38=6.71 umol organic-C cmp2 d-‘, of which sulphate-reduction contributed 21%. If sulphide was completely reoxidized within the surface layer, thus contributing to the benthic oxygen uptake, the proportionate contribution of sulphate reduction to total organic carbon mineralization would increase to 26%. This proportion is smaller than the 50% or organic-C oxidation by sulphate reduction reported for a temperate coastal marine sediment in the Limfjord, Denmark (Jorgensen, 1977) particularly when it is considered that Jorgensen’sdata were for sulphate reduction only to AVS, and did not include pyrite. However, the contribution by sulphate reduction to overall organic degradation in a sediment is regulated by the depth of the surface oxidized layer within which sulphate reduction cannot occur (Jorgensen, 1982), and a deeper oxidized layer in the Antarctic sediment may explain the smaller proportion of organic mineralization by sulphate reducers. A few estimates of primary production in the waters off Signy Island are available. Horn et al. (1969) estimated an annual primary production rate during 1966-67 of 130g C mm2y - ’ in the seawaterat a station in Borge Bay, just outside Factory Cove, and suggested that this was a conservative estimate. Whitaker (1982) measured 86 and 289 g C me2 y-’ in 1972-73 and 1973-74, respectively, in Borge Bay. In comparison, the daily mineralization rate of 6.71 umol organic-C ctn2 d-’ measured in Factory Cove extrapolates to 294 g C rnv2 y-l. Clearly, these annual estimates are extrapolated from very limited data and Clark et al. (1988) have emphasisedthat the size of the summer bloom varies greatly from year to year. However, it at least indicates similar orders of magnitude for sedimentary organic detrital degradation compared to primary production in the overlying water column. Further work is required to obtain more precise estimates of theseimportant ecological processesin theseunique Antarctic environments. Acknowledgements I wish to thank The Royal Society and the Natural Environment ResearchCouncil (Grant GR3/6482) for grants which permitted this research to be carried out. The collaboration of Drs C. Ellis-Evans and I. Hawes, Mr Peter Rotheray, and the men at the Signy Island baseisacknowledged, and in particular I wish to thank Steve Bancroft for retrieving cores. References American Public Health Association 1975 Standard methods for the examination of water and waste water. Washington. Clarke, A. 1988 Seasonality in the Antarctic marine environment. Comparative Biochemistry and Physiology 9OB, 461473. Clarke, A., Holmes, L. J. & White, M. G. 1988 The annual cycle of temperature, chlorophyll and major nutrients at Signy Island, South Orkney Islands, 1969-82. British Anrarctic Survey Bulletin 80,65-86. Delille, D. & Bouvy, M. 1986 Microflores sulfato reductrices en milieu subantarctique. In: Deuxienre Colloque Inrernarional de Bacteriologii Marine Brest: CNRS, pp. 265-272. Delille, D., Bouvy, M. & Cahet, G. 1988 Short term variations of bacteria-plankton in Antarctic zone: Terre Adelie area. Microbial Ecology l&293-309. Ellis-Evans, J. C. 1984 Methane in maritime Antarctic freshwater lakes. Polar Biology 3,6>71. Ellis-Evans, J. C. 1985 Decomposition processes in maritime Antarctic lakes. In: Antarctic Nutrient Cycles and Food Webs, (Siegfried, W. R., Condy, P. R. & Laws, R. M., eds) Berlin: Springer-Verlag, pp. 253-260. El-Sayed, S. 2. 1984 Productivity of the Antarctic waters-a reappraisal. In: Marine Phyroplankton and Productivity, (Holm-Hansen, O., Bolis, L. & Gilles, R., eds) Berlin: Springer-Verlag.
516
D. B. Nedwell
Franzmann, P. D., Skyring, G. W., Burton, H. R. & Deprez, P. P. 1988 Sulfate reduction rates and some aspects of the limnology of four lakes and a fiord in the Vestfold Hills, Antarctica. Hydrobiologia 165, 25-33. Hall, K. 1987 The physical properties of quartz-micaschist and their applications to freeze-thaw weathering studies in the maritime Antarctic. Earth Surjace Processes and Landjorms 12,137-149. Herbert, R. A. & Bell, C. R. 1974 Nutrient cycling in the Antarctic marine environment. British Antarctic Survey Bulletin 39,7-l 1. Herbert, R. A. & Bhakoo, M. 1979 Microbial growth at low temperatures. In: Growth in Cold Environments (Russell, A. D., ed.) London: Society for Applied Bacteriology (13) pp. 1-16. Hodson, R. E., Azam, R., Carlucci, A. F., Fuhrman, J. A., Karl, D. M. & Holm-Hansen, 0. 1981 Microbial uptake of dissolved organic matter in McMurdo Sound, Antarctica, Marine Biology 61,89-94. Home, A. J., Fogg, G. E. &Eagle, D. J. 1969 Studies in situ of the primary production of an area of inshore Antarctic sea. 3ournar of the Marine Biology Associarion of the U.K. 49,393-405. Jones, J. G. 1976 The microbiology and decomposition of seston in open water and experimental enclosures in a productive lake. 3ournal of Ecology 64,241-278. Jorgensen, B. B. 1977 The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnology and Oceanography 22,814-832. Jorgensen, B. B. 1982 Mineralisation or organic matter in the sea bed-the role of sulphate reduction. Nature 296,643-645. Jorgensen, B. B. 1983a Processes at the sediment-water interface. In: SCOPE 21, The Major Biogeochemical Cycles and Their Interactions (Bolin, B. & Cook, R., eds), Chichester: John Wiley, pp. 477-509. Jorgensen, B. B. 19836 The microbial sulfur cycle. In: Microbial Geochemistry (Krumbein, W. E., ed.), Blackwell: Oxford, pp. 91-124. Jorgensen, B. B. 1988 Ecology of the sulphur cycle: oxidative pathways in sediments. In: The Nitrogen and Sulphur Cycles (Cole, J. A. & Ferguson, S. J., eds), Cambridge: Cambridge University Press, pp. 31-63. Kottmeier, S. T. & Sullivan, C. W. 1987 Late winter primary production and bacterial production in sea ice and seawater west of the Antarctic peninsular. Marine Ecology Progress Series 36,287-298. Leduc, L. G. & Ferroni, G. D. 1979 Quantitative ecology of psychrophilic bacteria in an aquatic environment and characterization of heterotrophic bacteria from permanently cold sediments. Canadian Jounral of Microbiology 25,1433-1442. Morita, R. Y. 1975 Psychrophilic bacteria. Bacteriological Reviews 39,14P167. Nedwell, D. B. 1982 The cycling of sulphur in marine and freshwater sediments. In: Sediment Microbiology (Nedwell, D. B. &Brown, C. M., eds), London: Academic Press, pp. 73-106. Nedwell, D. B. &Abram, J. W. 1978 Bacterial sulphate reduction in relation to sulphur geochemistry in two contrasting areas of saltmarsh sediment. Estuarine Coastal Murine Science 6,341-35 1. Nedwell, D. B. & Takii, 1988 S. Bacterial sulphate reduction in sediments of a European salt marsh: acidvolatile and tin-reducible products. Estuarine, Coastal and Shelf Science 26,599-606. Reichert, W. 1988 Impact of the Antarctic benthic fauna on the enrichment of biopolymer degrading psychrophilic bacteria. Microbial Ecology IS,31 1-321. Revsbech, N. P., Sorensen, J., Blackbum, T. H. & Lomholt, J. P. 1980 Distribution of oxygen in marine sediments measured with microelectrodes. Limnology and Oceanography 25,4OHll. Senior, E., Lindstrom, E. B., Banat, I. M. & Nedwell, D. B. 1982 Sulfate reduction and methanogenesis in the sediment of a saltmarsh on the East Coast of the United Kingdom. Applied and Environmental Microbiology 43,987-996. Skyring, G. W. 1985 Anaerobic microbial processes in coral reef sediments. Proceedings of the Fifth International Coral Reef Congress, Tahiti, 3,421-425. Skyring, G. W. 1987 Sulfate reduction in coastal ecosystems. GeomicrobiologyJournal5,295-374. Sorensen, J., Jorgensen, B. B. & Revsbech, N. P. 1979 A comparison of oxygen, nitrate and sulphate respiration in coastal marine sediment. Microbial Ecology 5,105-l 15. Sorensen, J. & Jorgensen, B. B. 1987 Early diagenesis in sediments from Danish coastal waters: microbial activity and Mn-Fe-S geochemistry. Geochimica et Cosmockimica Acta 51,1583-1590. Stanley, S. 0. & Rose, A. H. 1967 Bacteria and yeasts from lakes on Deception Island. Proceedings of the Royal Society London 252B, 19%207. Strickland, D. J. & Parsons, T. R. 1972 A Pructicul Handbook of Sea Water Analysis. Fisheries Research Board of Canada, Ottawa. Whitaker, T. M. 1982 Primary production of phytoplankton off Signy Island, South Orkneys, the Antarctic. Proceedings of the Royal Society of London, Series B 214,169-189.
Benthic Coastal Orkney
Microbial Sediment Islands
Activity at Signy
in an Antarctic Island, South
D. B. Nedwell Department of Biology, University of Essex, Colchester CO4 3SQ, U.K. Received 21 September 1988 and in revisedform 31 January 1989
Keywords: Antarctic; marine sediments; microbial activity; sulphate reduction; pyrite Microbial activity in a marine sediment in Factory Cove, Signy Island (60”43’S, 45”38’W), South Orkney Islands in the maritime Antarctic was examined during December 1987 and January 1988. The sediment was bioturbated by a dense amphipod population in the surface layer but oxygen penetrated to a depth of only 1.7 mm. The top 1 cm was light coloured and contained negligible concentrations of acid-volatile sulphides. Below 1 cm the sediment was black and contained abundant sulphides. Sulphate reduction rates averaged 6.87 x 10-l gmol sulphate cm-*d-l over the O-15 cm horizon, equivalent to 1.38 pmol organic carbon oxidized cn-*d-l. Of the sulphate reduced, 60% was to tin-reducible products (including pyrite) and 40% to acid-volatile sulphides. Annual sulphate reduction was at least 250 )rmol sulphate cm-%-‘. The sea water temperature varied only between - 18-l “C, but the optimum temperature for sulphate reduction was 21 “C. Oxygen uptake by the benthos averaged 5.33 pm01 oxygen cme2d-l, equivalent to 5.33 umol organic carbon oxidized err-*d-l. Aerobic respiration accounted for 79% of the organic carbon mineralization and sulphate reduction for 21%.
Introduction permanently at low temperature, around 0 “C, the Southern Ocean is one of the most productive marine regions of the world (El Sayed, 1984; Komneier & Sullivan, 1987). The organic matter derived from the primary productivity serves asthe substrates for both grazing and detritus-based food webs, and in a steady-state ecosystem primary production is balanced by mineralization of the organic carbon. In the inshore marine environment the bottom sediments are important sites of deposition of organic detritus from the water column, and in boreal regions microbial activity in the sediments contributes substantially to mineralization of organic carbon (Jorgensen, 1983~). Organic mineralization in these sediments is largely brought about by the activity of aerobic bacteria, together with that of sulphate reducing bacteria in the anaerobic regions of sediment below the surface aerobic layer (Sorensen et QZ., 1979). The proportionate contribution of sulphate reduction to organic mineralization is greatest in coastal Although
0272-7714/89/050507
+ 10 $03.00/0
@ 1989 Academic
Press Limited
508
D. B. Nedwell
sediments where there is commonly only a shallow surface aerobic layer, and declines in deeper water where diminished detrital deposition results in more oxidized sediments (Jorgensen, 1982). Despite the permanently low temperature, Antarctic environments support large active populations of microorganisms, someof which are obligatorily psychrophilic, although the majority are facultative psychrophiles (Stanley & Rose, 1967). Representatives of most of the different physiological groups of bacteria which contribute to organic degradation and nutrient recycling have been isolated from Antarctic or other low temperature sea water and sediments(for example, Herbert & Bell, 1974; Herbert & Bhakoo, 1979; Leduc & Ferroni, 1979; Reichert, 1988). Uptake of organics by bacteria, and active microbial growth occur in Antarctic sea water (Hodson et al., 1981; Delille et al., 1988) but the magnitude of their in situ activity in marine sediments is as yet unknown. Delille and Bouvy (1986) reported active sulphate reduction, indicated by sulphide formation, in fjord sediments from the Kerguelen archipelago while Franzmann et al. (1988) reported slow rates of sulphate reduction in brackish sediment from the antarctic lakesand a fjord. Methane formation and sulphate reduction have been reported in the sediments of fresh water lakes of the maritime Antarctic during summer (Ellis-Evan, 1984, 1985), although sulphate reduction was sulphate-limited. These sediments exhibited strong seasonal changesin redox profiles. The current work wasundertaken during the Antarctic summer 1987-88 to measurethe rates of benthic microbial activities which contribute to organic mineralization in an inshore Antarctic marine sediment. Sampling site The work was carried out during December 1987, and January 1988, at the baseof the British Antarctic Survey in the South Orkney Islands-Signy Island (60”43’S, 45’38’W). A singlesampling site wasselectedalong the permanently marked transect ZM 23 in Factory Cove, opposite the base,approximately 100 m offshore under 6 m water (Figure 1). The bottom sediment is never frozen at this site, and seawater temperatures vary seasonally only between - 1.0-1.0 “C (British Antarctic Survey, unpublished data and seeClarke, 1988). The sediment consistedof glacially eroded quartz-micaschist (Hall, 1987)with 70-90% of particles in the fine sandand very fine sandfractions (0.063-0.25 mm diameter) (British Antarctic Survey, unpublished report N5/1975/H). The sediment was blackened below a light brown surface layer approximately 1 cm thick. In the surface layer the amphipods PontogenearotundifrOns and Tryphosa kergueleni were present at population densities of 2-3 x lo3 individuals m- ’ (British Antarctic Survey, unpublished report N5/1981/H). Vertical cores of sediment were taken by SCUBA divers using perspex core tubes (8 cm internal diameter) and sealedwith silicon rubber bungs. The cores were returned to the laboratory within 10 min and were kept at 0 “C in a water bath. Methods St&hate
reduction
A sediment core was extruded and duplicate subsamplesof sediment taken from known depths using 5 ml plastic hypodermic syringes with the luer end removed. The subsampling was carried out in a constant temperature room at 2 “C and the syringes of
Microbial
activity in antarctic coastal sediment
South 46OW
509
Orkney Islands 45OW
South Orkney
Island
Figure 1. Signy Island, and sampling site. Broken line indicates transect Zh423, and sampling site (A).
sediment were immediately capped with butyl rubber septa to exclude oxygen, and placed in a water bath at 0 “C. Each subsamplewas injected with 20 l.d of %-sulphate (Amersham International, U.K.) in sterile seawater [O-4mCi (4.2 MBq) ml-‘; 1150 Ci (42.6 TBq) umol-‘1 via the butyl rubber septum. The needle was slowly withdrawn along the sediment sample during injection to distribute the radiotracer as evenly as possible. The sampleswere incubated at 0 “C for 24 h, and then frozen at - 80 “C until processed. Each sediment samplewas acidified under oxygen-free nitrogen gas(OFN) and acidvolatile sulphides (AVS) carried over in the OFN stream and trapped in 40 ml zinc acetate solution (1 o/0w/v). (The nitrogen gaswasfirst passedthrough chromous acid to remove any traces of oxygen.) After removal of the AVS the residual sediment was digested with tin and tin chloride at 100 “C to recover the tin-reducible sulphides (TRS) which includes pyrite (Skyring, 1985; Nedwell & Takii, 1988). Again, hydrogen sulphide generated during the digestion was swept by the OFN and trapped in 40 ml zinc acetate solution. Duplicate subsamples(2 ml) from the zinc acetate traps for both AVS and TRS were transferred into Instagel (Packard Instruments Ltd, U.S.A.) and radioactivity measured in a liquid scintillation counter (1209 Rackbeta, LKB Ltd, Sweden). Quenching and self absorption in each samplewas subsequently corrected for by internal standardization by adding 20 ~1of 35Ssulphate solution of known activity to every vial. Concentrations
of sulphide
minerals
The residue from each 40 ml zinc acetate trap was titrated with thiosulphate solution to determine the concentrations of AVS and TRS present in each sediment sample (American Public Health Association, 1975).
510
D. B. Nedwell
Sulphate After digestion each sediment sample was filtered through a glass fibre filter paper (GF/C, Whatman), washed three times with distilled water and filtered, and the filtrates bulked together and made up to 100 ml. The sulphate concentration in the filtrate was determined by a barium sulphate turbidimetric technique (American Public Health Association, 1975). Optimum temperature for sulphate reduction Slurries of sediment (50% v/v) in deoxygenated seawater were prepared with sediment from the l-4 cm horizon of a vertical core. This was the horizon within which sulphate reduction was greatest (see Results). Hungate technique was used to exclude oxygen from the slurry, all transfers and manipulations being carried out under a stream of OFN. Aliquots (16 ml) of the slurry were dispensed into 30 ml screw-capped universals, which were placed along an ahuninium temperature-gradient block incubator and allowed to equilibrate to temperature for 1 h. Sodium lactate solution (100 ~1 to give 25 PM final concentration) was injected into each universal, followed immediately by 20 ~1 of 35Ssulphate solution. The lactate was added to provide a supply of electron donor for sulphate reducers. Otherwise, in an electron-donor limited environment, the rates of sulphate reduction measured might be substrate-limited rather than temperature-limited, and so influence the observed optimum temperature for sulphate reduction. The universals were shaken thoroughly and placed back in the gradient block for 15 h. At the end of the incubation period 5 ml zinc acetate solution (5% w/v) was added to each universal to stop further activity and to ‘ fix ’ sulphide until further treatment. Each sample was subsequently acidified, and the radioactivity in the AVS determined as described previously. The aluminium block incubator was heated at one end and cooled at the other by thermocirculators to maintain the temperature gradient. The temperature at each point along the gradient was checked by using a thermometer immersed in water in universals along the gradient, and the gradient was always linear. Two experiments were carried out over temperature ranges between 0.7-25 “C and 17-37 “C. With 14 positions along the gradient, this gave an approximately 1.5 “C temperature difference between adjacent universals. Benthic oxygen uptake Vertical cores of sediment (approximately 20 cm length) were taken from the study site in Factory Cove, and the bottom bung of each core was pushed up until the sediment surface had 11 of seawater above it in the core tube. The cores were then placed in a water bath at 0 “C for 24 h to re-equilibrate after the disturbance of coring. Air was continuously bubbled through the seawater to maintain air-saturated dissolved oxygen (DO) concentrations in the water column. The apparatus was always covered with a double thickness of black polythene sheet to exclude light. After 24 h the core tubes were closed with an airtight perspex cap through which protruded a Clark-type oxygen electrode [Radiometer (UK) Ltd, U.K.] into the water column. A magnetic follower was suspended below the cap in the water column to maintain mixing after the air steam was stopped. The air stream was then cut off and the decrease in DO concentration with time was followed for 4 h. During this time the decrease of DO was sufficient to accurately determine a rate, but the DO was not depleted to the extent that it started to limit the rate of DO transfer across the sediment-water
Microbial
activity in antarctic coastal sediment
Sulphlde -4 I
(log mmol Sq-‘sedlmentl -2 0 ’
-3 . . .
511
’
0.m
-I ‘I-
,.rm
,-
. .
CD
m
.
0
..‘a0
,-
a.
,-
Figure 2. Distribution of sulphides, and oxygen in the sediment (0, acid-volatile sulphide; 0, tin-reducible sulphide; and n , dissolved oxygen). Broken line indicates depth of surface oxidized layer. interface (Jones, 1976). The DO during the experiment did not fall below 80% of the airsaturated value. The percentage saturation of DO was read at 15 min intervals with an oxygen meter (Strathkelvin Instruments, U.K.) and converted to equivalent DO concentration. The air-saturated concentration of oxygen in seawaterat 0 “C was determined as 0.3708 mM (SD 0.0035) by Winklers titration method (Strickland & Parsons, 1972). Three separate cores of sediment were used to measuredecreaseof DO, with duplicate DO uptake measurementson eachcore. Preliminary measurementof oxygen uptake by 11 of seawaterin the absenceof sediment showed no significant decrease,and decreaseof DO from the water column in the presenceof sediment was therefore attributed solely to the respiratory activity of the benthic biota.
Oxygen concentrationprofile in the sediment The oxygen profiles in cores from the sampling site were measured by Dr Ian Hawes (British Antarctic Survey) with a microelectrode (Microsense, Israel) of the design of Revsbech et al. (1980). The oxygen concentrations were determined at 0.1 mm intervals using a micromanipulator to insert the electrode. Specificgravity: water content of the sediment Cores of sediment were taken and frozen at - 20 “C. They were then extruded while still frozen and sectioned with a fine saw. The wet weight of each depth slice wasdetermined, and then each section was dried to constant weight over 3 d at 80 “C to determine the water content. Results The distributions of AVS and TRS with depth in the sediment from Factory Cove are shown in Figure 2. Sulphare reduction rates, including reduction to both AVS and TRS,
512
D. B. Nedwell
log SO,
Reduction
-3 0;
rate
(pmol
S 4-l
-2
sediment
d-l) 0
-1
1 .
. .
. . . .
5-
. .
.
W.
”
.
.
“.
IO -
. . .
.
.
.
.
15 -
20
-
.
. .
.
J Figure
3. Rates of sulphate
Figure
4. Optimum
reduction
Temperature
temperature
in the sediment.
(“Cl
for sulphate
reduction:
(0,
Run 1; and 0, Run 2).
were between 0.1-0.2 umol sulphate g-’ sediment d- ’ in the top O-3 cm, but decreasedby an order of magnitude between 3-5 cm (Figure 3). Below 5 cm the rates of sulphate reduction were uniformly low. Overall, 60% of the sulphate wasreduced to TRS and 40% to AVS, with no obvious trends with depth in the proportions of these end products. Both of the experiments to investigate the optimum temperature for sulphate reduction showed a maximum at about 21 “C (Figure 4).
Microbial
activity in antarctic coastal sediment
513
Linear regressionanalysis of the oxygen uptake data, which conformed to straight lines (P < O-05),showed that in all casesthere were significant decreasesof DO over a 4 h period. Analysis of variance revealed significant differences in the rate measured both between cores and between repeat measurementson the samecore. However, overall the rate of DO change had a mean value of -0.011 (standard error 0.002) umol oxygen h-l, corresponding to an oxygen transfer rate from water into sediment of 5.23 ( f O-95) umol oxygen cme2 d-l. The profiles of oxygen concentration down the sediment showed that oxygen penetrated to a depth of only 15-1.7 mm (seeFigure 2). Discussion Oxygen penetrated only 1.5-1.7 mm into the sediment despite the active bioturbation of the sediment by the amphipod community. Although tin-reducible sulphides (pyrite) were present in the top 1 cm layer there was negligible acid-volatile sulphide, and the top 1 cm of sediment was light brown in colour. Jorgensen (1983b, 1988) has previously pointed out that in temperate coastalmarine sedimentstheremay be only a shallow surface aerobic layer containing oxygen, although below this the sediment may still be chemically oxidized. This oxidized but anoxic layer hasbeen termed the ’ sub-oxic ’ or ‘ Fe-Mn ’ zone (Sorensen & Jorgensen, 1987). Any hydrogen sulphide diffusing upwards from the deeper, reduced anoxic layers may not reach the aerobic layer before it is oxidized at the baseof the sub-oxic layer. This seemsto be the casein this antarctic coastalsediment. The rates of sulphate reduction determined in the cores from the Factory Cove site were first converted from rates on a sediment weight basisto equivalent rates per ml sediment by multiplying by the measuredspecific gravity of the sediment at each depth. These rates were then integrated with depth over the O-15 cm depth by summation of adjacent 1 cm deep slices,and by using linear interpolation and a simple trapezium method to determine integrated sulphate reduction rates between measured horizons. This gave values of 5.507 x 10-l and 8-227 x 10-l umol sulphate cm -2 d-l for each core respectively (average 6.87 x 10-l) over the &15 cm horizon which encompassedthe surface zone of greatest activity. These data contrast with the only other data available for sulphate reduction rates in an Antarctic sediment of 4 x 10m3pmol sulphate cm-‘d-l, in Ellis Fjord, Vestfold Hills, Antarctic (Franzmann et al., 1988), determined by a method identical to that used in the present work. These much slower rates, compared to those at Signy Island, cannot immediately be explained although primary production rates in the waters at Signy appear to be considerably greater than in other Antarctic waters (Horne et al., 1969; Whitaker, 1982; Clarke et al., 1988). This hasbeen attributed to the relatively high light intensities and dissolved nutrient concentrations in thesewaters. Much of the available data for sulphate reduction in other ecosystemsreports average rates per litre of sediment in the O-10 cm horizon (seeNedwell, 1982). In the present casethe rates integrated over the &lo cm horizon were equivalent to 0.05 1 and 0.081 umol sulphate 1-l d-’ for this Antarctic sediment. This is lower than the summer rates reported for temperate coastal and intertidal sediments, although greater than winter rates reported for those environments (see Skyring, 1987). The rates were also greater than those reported for deep ocean sedimentswhere the temperature regime is similar to Antarctic seawater,but where organic input to the sediment from the water column is much less.Nedwell and Abram (1978) reported that in temperate salt marsh sediment temperature variation had the greatest effect on sulphate reduction rates, followed by the availability of electron
514
D. B. Nedwell
donors. In the present case, where seawater temperature remains virtually constant throughout the year, the availability of electron donors derived from organic matter deposited onto the sediment is likely to play a controlling part in any seasonalchangesof sulphate reduction rates in the sediment. The presenceof the large amphipod populations, which visibly bioturbate the surface layer of sediment, will alsotend to enhancethe rate at which deposited organics become incorporated into the sediment, and hence available to the sulphate reducers in the anaerobic layers below the surface aerobic zone. The measurementsreported here were carried out during the Antarctic spring, before the spring algal bloom had started to settle onto the bottom (N. Gilbert, personal communication). They are, therefore, likely to be minimum values for sulphate reduction rates in this environment, and may increase later in the seasonafter deposition of organic detritus to the sediment stimulates sulphate reduction. Bearing in mind, therefore, that these are likely to be minimal estimates,and that the virtually constant seawatertemperature will have little seasonaleffect upon the rates, the depth-integrated daily rates yield annual values of 201 and 300 umol sulphate cm- 2y -l. This compares with estimates of annual sulphate reduction (to AVS only) in temperate salt marsh sediments of between 66-410 umol sulphate crnm2y-’ (Senior et al., 1982) although these estimateshave to be increased substantially if TRS is included (Nedwell & Takii, 1988). Thus, notwithstanding the uniformly low environmental temperature, sulphate reduction in these Antarctic sediments at Signy Island was still significant in magnitude even when compared to sedimentswhich exhibit much higher summer temperatures, but where sulphate reduction is greatly inhibited by low temperatures during winter. In this context it is interesting to note that, although the sulphate-reducing bacteria seem well adapted to their low temperature environment, the optimum temperature for sulphate reduction (21 “C) was nevertheless greatly above the temperature of the environment. Morita (1975) hasdefined obligate psychrophiles as ‘ having an optimal temperature for growth at about 15 “C or lower, a maximal temperature for growth at about 20 “C, and a minimal temperature for growth at 0 “C or lower ‘, and the present data therefore gives little evidence of obligately psychrophilic adaptation by the sulphate reducing bacteria in theseAntarctic sediments. Ellis-Evans (pers. corn.) hasalso found that sulphate-reduction in Signy Island lakeshad an optimum of 26 “C, while Antarctic methanogenic bacteria show little physiological adaptation to low temperature and the optimum for methanogenesis was >30 “C (Ellis-Evans, 1984). The rate of oxygen uptake by the benthic biota was 5.33 umol oxygen cme2 d-r. The amount of organic carbon oxidized can be calculated stoichiometrically from the equation CH,O + O,+ CO, + H,O and was equivalent to 533 umol organic-C cme2 d-l. This represents the organotrophic activity of the total benthic community including both micro- and meio-benthos. It may also include a component resulting from aerobic reoxidation of products of anaerobic metabolism, such as sulphide, although it is not possible to differentiate this within the overall oxygen consumption rate. By comparison, the sulphate-reducing bacteria are the major anaerobic organotrophs in anaerobic marine sedimentsand oxidize organic matter according to the overall equation 2 (CH,O) + SOd2- + 2H+ -+2CO,+H,S
+2H,O
The rates of sulphate reduction for each core, integrated over the &15 cm horizon where sulphate reduction isgreatest, were equivalent to 1.10and 1.65 (mean l-38) umol organic-C
Microbial
activity in antarctic coastal sediment
515
ctn2 d-‘. Assuming that sulphide reoxidation did not significantly contribute to oxygen uptake, the total organic oxidation rate was 5.33+ 1.38=6.71 umol organic-C cmp2 d-‘, of which sulphate-reduction contributed 21%. If sulphide was completely reoxidized within the surface layer, thus contributing to the benthic oxygen uptake, the proportionate contribution of sulphate reduction to total organic carbon mineralization would increase to 26%. This proportion is smaller than the 50% or organic-C oxidation by sulphate reduction reported for a temperate coastal marine sediment in the Limfjord, Denmark (Jorgensen, 1977) particularly when it is considered that Jorgensen’sdata were for sulphate reduction only to AVS, and did not include pyrite. However, the contribution by sulphate reduction to overall organic degradation in a sediment is regulated by the depth of the surface oxidized layer within which sulphate reduction cannot occur (Jorgensen, 1982), and a deeper oxidized layer in the Antarctic sediment may explain the smaller proportion of organic mineralization by sulphate reducers. A few estimates of primary production in the waters off Signy Island are available. Horn et al. (1969) estimated an annual primary production rate during 1966-67 of 130g C mm2y - ’ in the seawaterat a station in Borge Bay, just outside Factory Cove, and suggested that this was a conservative estimate. Whitaker (1982) measured 86 and 289 g C me2 y-’ in 1972-73 and 1973-74, respectively, in Borge Bay. In comparison, the daily mineralization rate of 6.71 umol organic-C ctn2 d-’ measured in Factory Cove extrapolates to 294 g C rnv2 y-l. Clearly, these annual estimates are extrapolated from very limited data and Clark et al. (1988) have emphasisedthat the size of the summer bloom varies greatly from year to year. However, it at least indicates similar orders of magnitude for sedimentary organic detrital degradation compared to primary production in the overlying water column. Further work is required to obtain more precise estimates of theseimportant ecological processesin theseunique Antarctic environments. Acknowledgements I wish to thank The Royal Society and the Natural Environment ResearchCouncil (Grant GR3/6482) for grants which permitted this research to be carried out. The collaboration of Drs C. Ellis-Evans and I. Hawes, Mr Peter Rotheray, and the men at the Signy Island baseisacknowledged, and in particular I wish to thank Steve Bancroft for retrieving cores. References American Public Health Association 1975 Standard methods for the examination of water and waste water. Washington. Clarke, A. 1988 Seasonality in the Antarctic marine environment. Comparative Biochemistry and Physiology 9OB, 461473. Clarke, A., Holmes, L. J. & White, M. G. 1988 The annual cycle of temperature, chlorophyll and major nutrients at Signy Island, South Orkney Islands, 1969-82. British Anrarctic Survey Bulletin 80,65-86. Delille, D. & Bouvy, M. 1986 Microflores sulfato reductrices en milieu subantarctique. In: Deuxienre Colloque Inrernarional de Bacteriologii Marine Brest: CNRS, pp. 265-272. Delille, D., Bouvy, M. & Cahet, G. 1988 Short term variations of bacteria-plankton in Antarctic zone: Terre Adelie area. Microbial Ecology l&293-309. Ellis-Evans, J. C. 1984 Methane in maritime Antarctic freshwater lakes. Polar Biology 3,6>71. Ellis-Evans, J. C. 1985 Decomposition processes in maritime Antarctic lakes. In: Antarctic Nutrient Cycles and Food Webs, (Siegfried, W. R., Condy, P. R. & Laws, R. M., eds) Berlin: Springer-Verlag, pp. 253-260. El-Sayed, S. 2. 1984 Productivity of the Antarctic waters-a reappraisal. In: Marine Phyroplankton and Productivity, (Holm-Hansen, O., Bolis, L. & Gilles, R., eds) Berlin: Springer-Verlag.
516
D. B. Nedwell
Franzmann, P. D., Skyring, G. W., Burton, H. R. & Deprez, P. P. 1988 Sulfate reduction rates and some aspects of the limnology of four lakes and a fiord in the Vestfold Hills, Antarctica. Hydrobiologia 165, 25-33. Hall, K. 1987 The physical properties of quartz-micaschist and their applications to freeze-thaw weathering studies in the maritime Antarctic. Earth Surjace Processes and Landjorms 12,137-149. Herbert, R. A. & Bell, C. R. 1974 Nutrient cycling in the Antarctic marine environment. British Antarctic Survey Bulletin 39,7-l 1. Herbert, R. A. & Bhakoo, M. 1979 Microbial growth at low temperatures. In: Growth in Cold Environments (Russell, A. D., ed.) London: Society for Applied Bacteriology (13) pp. 1-16. Hodson, R. E., Azam, R., Carlucci, A. F., Fuhrman, J. A., Karl, D. M. & Holm-Hansen, 0. 1981 Microbial uptake of dissolved organic matter in McMurdo Sound, Antarctica, Marine Biology 61,89-94. Home, A. J., Fogg, G. E. &Eagle, D. J. 1969 Studies in situ of the primary production of an area of inshore Antarctic sea. 3ournar of the Marine Biology Associarion of the U.K. 49,393-405. Jones, J. G. 1976 The microbiology and decomposition of seston in open water and experimental enclosures in a productive lake. 3ournal of Ecology 64,241-278. Jorgensen, B. B. 1977 The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnology and Oceanography 22,814-832. Jorgensen, B. B. 1982 Mineralisation or organic matter in the sea bed-the role of sulphate reduction. Nature 296,643-645. Jorgensen, B. B. 1983a Processes at the sediment-water interface. In: SCOPE 21, The Major Biogeochemical Cycles and Their Interactions (Bolin, B. & Cook, R., eds), Chichester: John Wiley, pp. 477-509. Jorgensen, B. B. 19836 The microbial sulfur cycle. In: Microbial Geochemistry (Krumbein, W. E., ed.), Blackwell: Oxford, pp. 91-124. Jorgensen, B. B. 1988 Ecology of the sulphur cycle: oxidative pathways in sediments. In: The Nitrogen and Sulphur Cycles (Cole, J. A. & Ferguson, S. J., eds), Cambridge: Cambridge University Press, pp. 31-63. Kottmeier, S. T. & Sullivan, C. W. 1987 Late winter primary production and bacterial production in sea ice and seawater west of the Antarctic peninsular. Marine Ecology Progress Series 36,287-298. Leduc, L. G. & Ferroni, G. D. 1979 Quantitative ecology of psychrophilic bacteria in an aquatic environment and characterization of heterotrophic bacteria from permanently cold sediments. Canadian Jounral of Microbiology 25,1433-1442. Morita, R. Y. 1975 Psychrophilic bacteria. Bacteriological Reviews 39,14P167. Nedwell, D. B. 1982 The cycling of sulphur in marine and freshwater sediments. In: Sediment Microbiology (Nedwell, D. B. &Brown, C. M., eds), London: Academic Press, pp. 73-106. Nedwell, D. B. &Abram, J. W. 1978 Bacterial sulphate reduction in relation to sulphur geochemistry in two contrasting areas of saltmarsh sediment. Estuarine Coastal Murine Science 6,341-35 1. Nedwell, D. B. & Takii, 1988 S. Bacterial sulphate reduction in sediments of a European salt marsh: acidvolatile and tin-reducible products. Estuarine, Coastal and Shelf Science 26,599-606. Reichert, W. 1988 Impact of the Antarctic benthic fauna on the enrichment of biopolymer degrading psychrophilic bacteria. Microbial Ecology IS,31 1-321. Revsbech, N. P., Sorensen, J., Blackbum, T. H. & Lomholt, J. P. 1980 Distribution of oxygen in marine sediments measured with microelectrodes. Limnology and Oceanography 25,4OHll. Senior, E., Lindstrom, E. B., Banat, I. M. & Nedwell, D. B. 1982 Sulfate reduction and methanogenesis in the sediment of a saltmarsh on the East Coast of the United Kingdom. Applied and Environmental Microbiology 43,987-996. Skyring, G. W. 1985 Anaerobic microbial processes in coral reef sediments. Proceedings of the Fifth International Coral Reef Congress, Tahiti, 3,421-425. Skyring, G. W. 1987 Sulfate reduction in coastal ecosystems. GeomicrobiologyJournal5,295-374. Sorensen, J., Jorgensen, B. B. & Revsbech, N. P. 1979 A comparison of oxygen, nitrate and sulphate respiration in coastal marine sediment. Microbial Ecology 5,105-l 15. Sorensen, J. & Jorgensen, B. B. 1987 Early diagenesis in sediments from Danish coastal waters: microbial activity and Mn-Fe-S geochemistry. Geochimica et Cosmockimica Acta 51,1583-1590. Stanley, S. 0. & Rose, A. H. 1967 Bacteria and yeasts from lakes on Deception Island. Proceedings of the Royal Society London 252B, 19%207. Strickland, D. J. & Parsons, T. R. 1972 A Pructicul Handbook of Sea Water Analysis. Fisheries Research Board of Canada, Ottawa. Whitaker, T. M. 1982 Primary production of phytoplankton off Signy Island, South Orkneys, the Antarctic. Proceedings of the Royal Society of London, Series B 214,169-189.