Antarctic Science 10 (1): 3 9 4 4 (1998)
The use of oxygen microelectrodes to determine the net
production by an Antarctic sea ice algal community
A. McMINN' and C. ASHWORTHZ
'Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Box 252C Hobart 7001, Tasmania, Australia
Email: [email protected]
2Departmentof Plant Science, University of Tasmania, Box 252C Hobart 7001, Tasmania, Australia
Abstract: Oxygen microelectrodes were used to measure the photosynthetic rates of Antarctic fast ice algal
mats. Using the oxygen flux across the diffusive boundary layer below the fast ice at Davis, a productivity range
of 0-1.78 mg C m-2h-' was measured. This is at the lower end of fast ice productivity estimates and suggests
that conventional I4C techniques may overestimate sea ice algal mat productivity. Photosynthetic capacity
(P,,,) approached 0.05 mg C. (mg chl a)-' h-I. Onset of photosynthesis saturation, Ek,was found at c. 14 pmol
photons m-2s-'. The irradiance of photoinhibition onset, Einh,was c. 20 pmol photons m-2s-' and the irradiance
at the compensation point, Ec, was 4 p o l photons rn-' s-'.
Received 14 August 1997, accepted 10 November 1997
Key words: Antarctic, fast ice, oxygen microelectrodes, photosynthesis, sea ice algae
Introduction
initial development of this technique was undertaken by
Revsbech, Jorgensen and collaborators(Jorgensen & Revsbech
1985, Jorgensen et al. 1983, Revsbech & Jorgensen (1983,
1986), Revsbech et al. (1980, 1983)). They identified two
methods of determining the photosynthetic rates of algal
mats. One measures gross photosynthesis within the algal
mat by measuring the immediate rate of oxygen depletion in
the dark, which is observed after a period of sustained
productionin thelight (Revsbech & Jorgensen 1983,Revsbech
& Jorgensen 1986). The second method, the method used
here, is based on measuring the oxygen flux through the
diffusive boundary layer (DBL) to calculate the local net
oxygen production of the whole mat (Jorgensen & Revsbech
1985). The second method was used in the sea ice because of
the difficulty of inserting the fragile electrodes into the sea
ice. 14C methods of determining productivity measure
something between gross and net productivity. Longer
incubations more closely approximate net productivity while
shorter term incubations more closely approximate gross
productivity. The oxygen microelectrode method described
here measures net community production. Microelectrode
methods have been widely applied to sediments (Jorgensen &
Revsbech 1985)and benthic algal mats (Ellis-Evans& Bayliss
1993, Jorgensen et al. 1983, Vincent et al. 1993) but are
applied here to sea ice algal mats for the first time.
Each year in autumn sea ice expands to cover over 20 million
km2of the Southern Ocean and, while it severely reduces the
amount of light available to phytoplankton, it provides a
transient habitat for sea ice algae. The length of time an area
is covered by sea ice is largely determined by how close it is
to Antarctica; coastal areas may be covered by sea ice for
more than 10 months while those at the extremities of the sea
ice extent may be covered for only a few days. In areas
covered by persistent sea ice primary productivity within the
sea ice may account for up to 50% of the annual total (Knox
1994, Voytek 1989).
In the fast ice close to the Antarctic coast most of the algal
biomass is concentrated in a dense band at the bottom of the
ice. Here, concentrations of up to 309 mg chlam-*(Palmisano
&Sullivan 1983)have been recorded, althoughconcentrations
of 15-120 mg chl a m-2are more typical (McConville et al.
1985,Watanabe & Satoh 1987). Determiningtheproductivity
of sea ice algal communities is far more problematical. Most
studies have used the I4C method (Steeman Nielsen 1952)
which has necessarily involved the melting of the sea ice to
extract the algae (Lizotte & Sullivan 1992, McConville &
Wetherbee 1983, Palmisano & Sullivan 1983). Others
(Grossi et al. 1987, Smith & Herman 1991) have incubated
the algal mat without melting the ice but have often obtained
lower values and have noted the problem of determining the
degree to which the 14Ctracer has infiltrated the ice.
The development of oxygen microelectrodes for measuring
photosynthesis in minimally disturbed benthic algal
communities has provided a method that does not require the
use of I4Ctracers. The electrodes, which have tip diameters
as small as 5 pm, can be inserted into algal mats with
minimum disturbance to the local environment. Much of the
Materials and methods
Three replicate sea ice algal mat samples were collected
regularly from a site 8 km north of Davis (68"35'S, 77"59'E)
between 26 October and 2 December 1995 (Fig. 1). Samples
for productivity analysis were collected between 17 and 25
November 1995. The ice at this site was 1.05 m thick and
39
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40
A. McMlNN & C. ASHWORTH
Fig. 1. Fast ice algal mats from Davis. The mats were sampled
from a site 8 km offshore from Davis on 17 November 1995.
a. Bottom of a fast ice core from Davis, Antarctica, showing
algal mat development in the bottom few centimetres. Ice core
is 13 cm in diameter; the coloured algal layer is only 1 cm
thick.
b. The underside of the fast ice at Davis showing microscale
heterogeneity. This core is submerged within the experimental
apparatus and is being artificiafly illuminated from underneath.
Ice core diameter is 13 cm.
covered with 10 cm of snow. A Jiffey drill was used to auger
to within 20 cm of the bottom of the ice. The lowest 20 cm
of ice only was taken with a 13 cm diameter SIPRE corer,
immediately placed in a black plastic bag and returned to the
laboratory. Previous work had shown that >95% of the algal
biomass in fast ice was concentrated in the bottom 20 cm
(Palmisano & Sullivan 1983, McConville & Wetherbee
1983, Grossi et al. 1987, Watanabe & Satoh 1987, McMinn
1996). All experiments were conducted in a darkroom to
eliminate stray light from the surroundings.
A 20 cm diameter glass-bottomed tank was connected to a
refrigerated recirculating water bath (Lauda) filled with
filtered sea water from the sample site, and with a temperature
maintained at -1 .O"C. The ice cores were inverted so that the
algal mat faced upwards and placed into the tank, which was
illuminated from below with either a halogen or daylight
fluorescent light source. Light intensity was controlled by the
use of neutral density filters, Oxygen microelectrodes,
temperature minisensors and fibre optic light microprobes
were inserted into the algal mat vertically from above and
ambient water temperature was maintained.
The Clarke-type oxygen microelectrodes with guard
cathodes (Aquamatic Pty L t d , Denmark) and tips
approximately 60-120 pm in diameter, exhibited 90%
response times of approximately 5-10 seconds. The stirring
sensitivity of the micro oxygen electrodes was measured in
the recirculating water bath and was found to be <1%
(Jorgensen & Des Marais 1990).
The probes were mounted on a slide track which allowed
them to be inserted vertically in 50 pm steps into the DBL
while the data were logged directly onto a PC. Probe
movement was controlled by a motorised micromanipulator
also under PC control. Vertical movement of the electrodes
was in 50 pm increments. The oxygen microelectrode
preamp signal was measured and logged in ADC units. This
signal was converted to oxygen concentration by linear
calibration with Winkler titrations of water deoxygenated by
20 min of N, bubbling, air saturated water and an intermediate
oxygen concentration all at - 1.O"C. Calibration was performed
prior to use of microelectrodes in the algal mat.
An Aquamatic temperature minisensor with a tip diameter
of 0.5 mm and offset from the oxygen and light electrodes by
I cm was used to collect the temperature data. The ambient
temperature of the darkroom was maintained at 10°C to
minimise warming of the experimental tank. At the end of
experimentation a small temperature gradient had developed
at the water surface but as this was minimal, ie less than 1"C,
and well outside the DBL it was unlikely to have effected the
estimation of oxygen diffusion.
Fibre optic light microprobes were constructed to measure
scalar irradiance (Kuhl et al. 1994). They had tip diameters
of c. 0.2 mm and were calibrated with reference to
measurements by a Biospherical Instruments QSP-170 47c
quantum radiometer. PAR scalar irradiances within the tank
werc measured at the ice-water interface within 1 mm of the
oxygen microelectrode. Ambient light levels beneath the sea
ice at the field site were measured with the same radiometer
to determine appropriate light levels to be used in the
laboratory study.
Algal mats were illuminated for a minimum of 30 min
before oxygen profiles were measured to ensure that a steady
state oxygen distribution had been achieved within the DBL.
Circulation from the water bath to the tank was suspended
during this process.
The measured 0, gradients over the DBL were used to
calculate the net oxygen production in light. The oxygen
diffusion flux (J) across the DBL is equivalent to the net
productivity of the algal mat and was calculated using the
one-dimensional version of Fick's first law of diffusion
(Revsbech & Jorgensen 1986):
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MEASURING PRODUCTIVITY OF ICE ALGAE
J=DoK
ax
120,
I
41
I
I I
I
I
I
I
where Do= molecular diffusion coefficient (at -1 .O"C =l. 14
x lo-' cm2 s-I (Broecker & Peng 1974))
dX =effective DBL thickness (Jsrgensen & Revsbech 1985)
or 90% level (Jsrgensen & Des Marais 1990)
aC = change in oxygen concentration across the DBL.
The top of the DBL was estimated by determining the level
at which the oxygen concentration had increased by 10% of
the difference between the maximum and minimum
concentrations (i.e. the oxygen export equivalent of the 90%
of 'free-flow concentration' (Jsrgensen & Des Marais 1990)).
Detection of the end point of the DBL, ie when the electrodes
had reached the ice surface, was based on observation with a
dissecting microscope and repeated unchanging 0, readings.
If the electrodes came into direct contact with the ice both the
temperature and 0, readings dropped sharply.
After oxygen flux measurements were completed the
samples were melted into filtered sea water for chlorophyll
analysis (Strickland & Parsons 1972), using a GBC UV/VIS
9 16 spectrophotometer.
The photosynthetic parameters Pmax,i.e. the maximum
photosynthetic rate (mg C (mg chl a)-' h-I), E,, i.e. the
irradiance of the onset of saturation (pmol photons m-2s-') a,
the photosynthetic efficiency (mg C (mg chl a)-' h-' (pmol
photons rn-, s-l)-l)and Einh,the irradiance of the onset of
photoinhibition (pmol photons m-2s-I) were estimated from
the composite P-E scatter plot.
Results
Algal mats begin to develop on the underside of the fast ice at
Davis in late September each year. Biomass reaches a
maximum, usually around 90-120 mg chl a m-,, in late
November and then declines rapidly. Much of this decline
occurs as a result of small increases in the underlying water
temperatures and slow melting of the ice from above. The
algal biomass is overwhelmingly concentrated in the lower
5 cm (McMinn 1996), most of it as an encrusting layer on the
hard ice underside (Fig. 1). In 1995 the algal mat community
was dominated by Entomeneis kjellmannii (80-96%) with
lesser contributions from Nitzschia stellata (1-9%) and
Navicula glaciei (0-5%).
Light reaching the bottom algal mat at Davis was severely
reduced by c. 10 cm of snow cover. Midday under ice
irradiances in late October and November were between 1.5
and 4.0 pmol photons m-zs-I,which represents less than 0.5%
of the incident surface irradiance. During this time, the
biomass of the algal mat was increasing indicating that net
primary production was occurring despite the low ambient
irradiances. By the time the samples for productivity analysis
were taken (17-25 November), increases in the chl a biomass
had plateaued and begun to decline (Fig. 2 ) . The biomass of
Fig. 2. Growth of fast ice algal mat at a site 8 km north of Davis.
Chlorophyll a biomass estimates are the mean for triplicates (*
standard deviation).
the sea ice algal mats during this time was between 34.1 and
153.1 mg chl a m-,. In the laboratory the algal mats were
illuminated at scalar irradiances between 0.1 and 33.1 pmol
photons m-' s-l. The oxygen flux across the DBL was between
0 and 0.00423 nmol 0, cm-' s-'. Using a photosynthetic
quotient (ie O,/CO,) of 1.03 (Satoh & Watanabe 1988), this
is equivalent to a productivity range of 0-1.78 mg C rn-, h-I.
A detectable oxygen flux was only realised at irradiances
above 4 pmol photons m-' s-'; this represents the
compensation irradiance, Ec. The photosynthetic capacity
(Pmax)was approximately 0.05 mg C (mg chl a)-' h-I. An
example of oxygen measurements across the DBL of one of
the mats is presented in Fig. 3.
Discussion
Productivity estimates of Antarctic fast ice algal mats are
highly variable, extending from almost zero to over 240 mg
C m-2d-' (Grossi et al. 1987). Most of this variability is due
to differences in biomass and in situ irradiance, which
themselves are mostly due to differences in seasonality, ice
thickness, snow thickness and ice transparency (Kirst &
Wiencke 1995, Trodahl & Buckley 1989). Some of the
variation is, however, also almost certainly due to differences
in the method of measurement used. These differences have
oftenmade comparison ofresults difficult. Most studies have
used the I4Cmethod (the exception being Satoh & Watanabe
(1988) who used an oxygen exchange method) but some used
incubation times of 4-5 h (McConville et al. 1985, Satoh &
Watanabe 1988), some 12 h (Palmisano et al. 1985a) and
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A. McMlNN & C. ASHWORTH
42
-
0
F 5
A
I
I
I
I
0
E
Y
s
8
0
10
water column
pmol
o2r'
Fig. 3. A depth vs. oxygen recording across the DBL of a fast
ice algal mat. The starting point of the depth scale is arbitrary
and depends on where the first oxygen reading was made.
some 24 h (Palmisano & Sullivan 1983, Grossi et al. 1987).
In most studies the sea ice samples were melted into filtered
sea water prior to incubation, but Grossi et al. (1987) used
unmelted ice samples. In situ measurements using I4Cwere
made by Palmisano et al. (1985a), McConville et al. (1985),
Grossi et al. (1987) and Satoh & Watanabe (1988). Hourly
productivity estimates include 7.64 mg C m-' h-' at 9 niol
photons m-2s-l and 45.1 mg chl a
under 5 cm of snow at
Syowa in October (Satoh & Watanabe 1988) and
1.58-32.92 mg C m-2h-I at 12-38 mol photons m-' s-I and
2.72-1 5.6 mg chl a m-zbetweenNovember andDecember at
Casey (McConville et al. 1985).
Our chlorophyll specific production rates (at an ambient
scalar irradiance of 4-6 pmol photons m-zs-I) measured by
oxygen microelectrodes in the Davis mats, ie 0.001-0.042
mg C. (mg chl a)-' hl, are lower than previous Antarctic fast
ice productivity estimates. These include 0.052-0.346 mg C
(mg chl a)-' h-' (Palmisano et al. 1985b), 0.16-3.2 mg C (mg
chl a)-' h-' (McConviHe et al. 1985), 0.03-2.96 mg C (mg
chl a)-' h-' (Grossi et al. 1987) and 0.19 mg C (mg chl a)-' h-'
(Satoh & Watanabe 1988). The closest values, ie 0.03 mg C
(mg chl a)-I h-' at an irradiance of 6 pmol photons m-2s-I, are
from the study of Grossi et al. (1987), which was the only
other study to use unmelted ice samples. Smith & Herman
(1991) reported nearly an order of magnitude difference
between the measurements of sea ice productivity in situ
(with unmelted ice samples) and in an incubator in Arctic sea
ice algal mats. They attributed much of this difference to
problems with tracer diffusion into the ice in the in situ
estimate but also considered small differences in spectral
composition, handling procedures and temperature to be
contributory. However, if these results are compared with
those from the Antarctic (ie here and Grossi et al. 1987) it
would appear that extracting the algal cells from their natural
ice environment and irradiating them suspended in either
environmental chambers or bottles leads to an overestimation
of in situ photosynthetic rates. In addition to the reasons
suggested by Smith & Herman (199 l), it is likely that cells in
the upper portion of the mat are nutrient limited and make
little contribution to net photosynthesis but still contribute to
the biomass. Also, the mats naturally receive a gradient of
light intensity, a changing spectral composition and self
shading and so it is unrealistic to separate the cells from the
mat and expose each cell to a similar light intensity as
happens in conventional I4C incubations.
A simple calculation shows that the biomass accumulation
between 25 October and 12 November, the period of mat
growth, can be reasonably explained by the measured
assimilation numbers (Fig. 2). The net growth rate over the
18 day period is 0.021 d-' (increase from 76.8 to 112.5 mg
chl a m-z). The average assimilation number for irradiances
between4 and 6 pmolphotons m-zs-I, equivalent to maximum
midday under ice irradiances, is 0.012 mg C (mg chl a)-' h'.
If a carbon to chlorophyll ratio of 50:l is assumed then it
would only take an average of 5 h a day of under ice
irradiances between 4 and 6 pmol photons m-2s-l, to achieve
the net growth rate.
With the photosynthesiskalar irradiance data collected
from the Davis sea ice algal mat it is possible to compile a
composite P-E diagram (Fig. 4). This diagram is based on
data taken from several different mats, collected on different
days and with differing biomasses but it is still possible to
broadly determine the important photosynthetic parameters.
Pmax(ie maximum chlorophyll specific production rate) is
c. 0.05 mg C (mg chl a)-' h-'; E, (ie onset of saturation) is
c. 14 pmol photons m 2s.', Ei,,h(ie irradiance ofphotoinhibition
onset) is c. 20 pmol photons m-*s-'. The absence of data
points below 4 pmol photons m-z s-', the compensation
irradiance Ec, does not allow a determination of a, the
photosynthetic efficiency. The closest Antarctic P-E values
0.050
7-
0.045
L
C
7
4
0.040
A
3
P
Y
-g
:.
2
E
B
as
0.035
4
4
0.030
0.025
4
0.020
4
4
4
0.015
0.010
4
4
4
4
0.005
LL
0.000
0.0
4
4
10.0
4
4
20.0
30.0
Scalar Inadlance (wnol photon8 m-'a-')
Fig. 4. Photosynthesis vs. scalar irradiance curve. Each point
represents a different oxygen-depth profile across a DBL.
Sample for this profile were taken from within a few metres
of each other at the same site.
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40.0
MEASURING PRODUCTIVITY OF ICE ALGAE
to those reported here are those from fast ice covered with
5 cm of snow at McMurdo Sound (Palmisano et al. 1985a,
Palmisano & Sullivan 1985). There, P,, was 0.079 mg C (mg
chl a)-'h-I, E, was approximately 5 pmol photons m-zs-' and
I;, was approximately 25 pmol photons m-2s-'.
Although micro oxygen electrodes have provided some
interesting results, there are a number of problems and
limitations associated with the technique that effect the
accuracy of the productivity and photosynthetic rate
measurements. A significant problem with the interpretation
of our photosynthesis-scalar irradiancemeasurements derived
here arises from the non-homogenous distribution of biomass
withinthe algalmats (Fig. 1). The oxygen fluxmeasurements
are essentially based on point readings whereas the biomass
is based on 13 cm diameter ice cores. As the biomass is
unevenly distributed, it is not possible to determine whether
single measurements are truly representative of the biomass.
Further, each incubationmeasures the photosyntheticresponse
of a different community, each of which has a different degree
of shelf shading, nutrient limitation etc. It is thought that
these factors account for most of the scatter on the P-E
diagram (Fig. 4). In future work this problem will be partly
offset by replicate oxygen measurements on the same mat.
The action of inserting the microelectrodes themselves into
the DBL can alter the thickness of the DBL by disturbing the
flow velocity around the sensor tip. This results in a thinning
of the DBL by 2 5 4 5 % and a consequent modification to the
oxygen flux (Glud etal. 1994). In samples where the oxygen
gradient is small, such as at the ice-water interface, this
modification is likely to be small (Glud et al. 1994). It is also
likely to be further reduced where there is no flow velocity
aroundthe sensortip, althoughthis has not yet been adequately
tested. Given the various errors associated with making these
oxygen flux measurements, i.e. measurement of DBL
thickness, oxygen electrode sensitivity and calibration,
elevation of the oxygen flux by depression of the DBL and
stirring sensitivity, there is a net error associated with the
method of at least f 20%.
Further, not all ice environments are suitable for
measurement. In much of the McMurdo Sound region, for
instance, ice platelets attach to the undersurface of the ice
creating a highly irregular ice-water interface where it would
not be possible to measure a DBL. This method is also
inappropriate for use in most surface and interior ice algal
communities of the pack ice because of the difficulty of
penetrating the ice matrix with the fragile electrodes. In the
Davis algal mats discussed here, most of the biomass was
concentrated in the lowest 2 cm of the ice (Fig. 1) and so the
diffusion paths were relatively short. In sea ice with less
concentrated bottom algal mats the diffusion paths will be
longer resulting in a longer time necessary to establish
equilibrium. There is also an apparent lower limit to the
biomass for which the oxygen flux can be measured. Algal
mats with a biomass of less than c. 20 mg chl a m-*evolved too
43
little oxygen for the electrodes to produce significant results
and so, for instance, it would be difficult to obtain productivity
estimates of algal mats in early stages of development in
spring by this method.
There are a number of practical difficulties as well. It is not
easy to maintain an ice core in a water tank without either the
ice core melting or the water freezing for lengthy periods of
time and yet this is essential as it was taking between 20 min
and 1 h for the DBL to reach equilibrium. In practice this
results in rarely achieving more than one set of readings at a
single irradiancefromany one ice core. The oxygen electrodes
are also very fragile and yet in this method they are being
driven into hard ice and this inevitably leads to many
breakages.
Taking into account the problems associated with the
oxygen microelectrode method, the inherent advantages,
which include the speed with which the measurements can be
taken and the minimum disturbance to the immediate ice
environment of the algal mat, should still ensure it becomes
an alternative method for investigating sea ice algal ecology
in some circumstances.
Acknowledgements
Financial and logistical support for this project was provided
by Australian National Antarctic Research Expeditions
(ANARE) and ASAC GrantNo 854. We thankprofwarwick
Vincent and Dr Ralph Smith for reviewing the manuscript
and Andrew Davidson and Clive Crossley for making helpful
comments on an earlier draft.
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