Post on 01-May-2023
ORIGINAL PAPER
Antarctic coastal microalgal primary productionand photosynthesis
Andrew McMinn • Chris Ashworth •
Ranjeet Bhagooli • Andrew Martin •
Sazlina Salleh • Peter Ralph • Ken Ryan
Received: 19 April 2012 / Accepted: 10 August 2012 / Published online: 28 August 2012
� Springer-Verlag 2012
Abstract Primary production in coastal Antarctica is
primarily contributed from three sources: sea ice algae,
phytoplankton, and microphytobenthos. Compared to other
eastern Antarctic sites, the sea ice microalgal biomass at
Casey Station, in spring 2005 was relatively low, 3.84 ±
1.67 to 21.6 ± 13.3 mg chl-a m-2 but productive,
103–163 mg C m-2 day-1. The photosynthetic parame-
ters, Fv/Fm and rETRmax, imply a community well-
acclimated to the light climate of the benthic, water
column, and sea ice habitats. Phytoplankton biomass was
greatest in late spring (11.1 ± 0.920 lg chl-a l-1), which
probably reflects input from the overlying sea ice. Lower
biomass and depressed Fv/Fm values later in the season were
probably due to nutrient limitation. Benthic microalgal
biomass was consistently between 200 and 400 mg chl-
a m-2 and production increased through into late summer
(204 mg C m-2 day-1). After the sea ice broke out, the
marine environment supported a small phytoplankton bio-
mass and a large benthic microalgal biomass. Compared
with previous studies, Fv/Fm values were relatively low but
there was no evidence of photoinhibition. When sea ice was
present, primary production of benthic microalgae was
either very low or there was a net draw down of oxygen. The
benthic microalgal community made a larger contribution to
total primary production than the phytoplankton or sea ice
algae at water depth less than approximately 5 m.
Introduction
Primary production in Antarctic coastal areas underpins
diverse and productive sympagic, benthic, and pelagic
ecosystems. Sea ice algae, phytoplankton, and benthic
microalgae contribute to most of the primary production,
which occurs over a comparatively short time period and is
highly seasonal. Macroalgae are sometimes important in
some restricted, shallow environments. The maximum
biomass and productivity of each of these three habitat
components are spatially and temporally variable. When
sea ice is present in winter and spring, most of the primary
production is concentrated in the basal layers of the sea ice.
Low light penetration through the ice mostly limits the
development of significant phytoplankton biomass (McM-
inn et al. 2010b). When the ice melts in spring, a large
pulse of sea ice algae is delivered from the ice to the
sediment surface where it is actively grazed by benthic
invertebrates (Dayton et al. 1986; McMinn 1996). The loss
Communicated by K. Yin.
A. McMinn (&) � C. Ashworth � R. Bhagooli � A. Martin �S. Salleh
Institute for Marine and Antarctic Studies, University of
Tasmania, Private Bag 126, Hobart, TAS 7001, Australia
e-mail: andrew.mcminn@utas.edu.au
Present Address:R. Bhagooli
Department of BioSciences, University of Mauritius, Reduit,
Mauritius
Present Address:S. Salleh
Center for Marine and Coastal Studies, Universiti Sains
Malaysia, 11800 Minden, Penang, Malaysia
P. Ralph
Plant Functional Biology and Climate Change Cluster (C3),
University of Technology, Sydney, PO Box 123, Broadway,
NSW 2007, Australia
K. Ryan
School of Biological Sciences, Victoria University of
Wellington, PO Box 600, Wellington, New Zealand
123
Mar Biol (2012) 159:2827–2837
DOI 10.1007/s00227-012-2044-0
of sea ice also increases light penetration into the water
column, which results in strong late spring/early summer
phytoplankton blooms (McMinn and Hodgson 1993;
McMinn et al. 2000b). In areas with persistent sea ice, such
as McMurdo Sound, most phytoplankton may be advected
in from ice-free areas (Dayton 1990). Rapid depletion of
nutrients, however, usually leads to a decline in phyto-
plankton biomass by mid-summer and an increase in ben-
thic microalgal biomass (McMinn et al. 2010b). Although
seaweeds are occasionally locally important, in general
they make only a minor contribution to primary production
in Antarctic coastal ecosystems (Miller and Pearse 1991).
While there have been many studies examining the
contribution of sea ice algae and phytoplankton to coastal
ecosystems in Antarctica (Knox 2006), comparatively few
have investigated the contribution of the benthic microal-
gae, that is, the microphytobenthos (MPB; Dayton et al.
1986; Gilbert 1991; Skowronski et al. 2009). In a previous
study, McMinn et al. (2010b) examined the relative con-
tributions of the MPB to total primary production at an
Antarctic coastal site during early summer. Here, we
extend that study by examining photosynthesis and primary
production into late summer when primary production
shifts from sea ice to benthic microalgal mats.
Materials and methods
Study sites
Field studies were conducted between November 2, 2005
and March 8, 2006 at three sites around Casey Station:
Brown Bay (BB), O’Brien Bay (OB), and Casey Wharf
(CW) (66�280S, 110�520E) in Antarctica (Fig. 1). These
sites are the same as those reported in McMinn et al.
(2010b) and were chosen as they allowed sampling in all
three habitats: sea ice, water column, and benthos (in the
sediment) before and after the annual ice break out. Sea ice
remained present at CW and BB until late December but
persisted into early January at OB. Time of day is pre-
sented as local time (GMT ? 5 h). Snow cover in these
areas was variable but \0.1 m. Ice thickness (when pres-
ent) was approximately 1.5 m over the study sites. The site
is microtidal with a mean tidal range of approximately 1 m.
All sampling locations were sub-tidal at depths between 4
and 14 m (Table 1).
Surface and subsurface irradiance were measured with a
radiometer (Biospherical QSP 200, San Diego, USA) with
2p (sea ice and sediment surface) and 4p (water column)
sensors. Additional irradiance measurements were made
Fig. 1 Location of field sites at
Casey Station, east Antarctica.
Dashed line indicates the 30 m
isobath
2828 Mar Biol (2012) 159:2827–2837
123
with a fiber optic light sensor (after Kuhl et al. 1994) in
conjunction with the oxygen microsensor measurements.
Temperature and salinity were measured at each site with a
conductivity meter (WTW, Weilhelm, Germany). Tem-
perature was also measured with a microelectrode (tip
diameter 0.5 mm) positioned adjacent to the oxygen and
irradiance sensors.
Chlorophyll-a analysis
Chlorophyll-a (chl-a) measurements of sea ice were taken
from 4 to 5 replicate ice cores within a 5-m radius at each
site. Because more than 95 % of the chl-a biomass is
typically found in the bottom few centimeters of the sea
ice (McMinn et al. 2000a), only this section of ice core
was sampled for algal biomass. Ice cores were obtained
by drilling a hole to 1.2 m (Jiffy, USA) and then
extracting the bottom 20–30 cm of core by coring man-
ually with an ice coring drill (Kovaks, USA). The bottom
10 cm of the core was removed and trimmed to small
blocks before being melted into an equal volume of
filtered seawater (0.22 lm filter). Melted samples of
100 ml were concentrated onto filters (Whatman GF/F 47
mm diameter) and the pigments were extracted overnight
in 10 ml of methanol at 4 �C. A fluorometer (Turner
Designs 10 AU) was employed to measure chl-a biomass
following the acidification method of Strickland and
Parsons (1972). The fluorometer was calibrated against a
chl-a standard (Sigma Aldrich 1 mg/l Spinach, St Louis).
Water column chl-a analysis was based on the collection
of replicate of water samples (n = 5) from a depth of 5 m
(4 m at Casey Wharf) using a 2-l water sampler (Niskin,
USA). The water was subsequently concentrated onto a
filter (Whatman GF/F 47 mm diameter), extracted and
analyzed in the same way as the ice cores. Sediment
samples for chl-a analysis were collected with a purpose
built, 15 mm diameter gravity corer. The top 1 cm of
sediment from each replicate core (n = 5) was removed
and pigments extracted in the dark in 20 ml of methanol
overnight at 4 �C. The resultant chl-a extract was dec-
anted and measured as described earlier.
Depth integrated water column biomass was calculated
by multiplying the chl-a (Table 1) with the water column
depth (Table 2).
Table 1 Chlorophyll-a biomass and photosynthetic parameters
Site Date Habitat Chla rETRmax Alpha Ek Fv/Fm Inhib
BB 10-Dec Sea ice 21.6 ± 13.3 31.7 ± 13.9 0.227 ± 0.029 140 0.319 ± 0.004 413
OB 11-Dec Sea ice 3.8 ± 1.7 81.0 ± 18.9 0.440 ± 0.236 184 0.338 ± 0.159 289
BB 10-Dec Sediment 367.0 ± 57.9 20.7 ± 2.6 0.163 ± 0.088 48 0.558 ± 0.008 413
BB 10-Jan Sediment 203 ± 40.3 10.8 ± 3.2 0.159 ± 0.146 66 0.423 ± 0.010
BB 7-Feb Sediment 243 ± 8.0 22.7 ± 8.2 0.323 ± 0.097 70 0.343 ± 0.043
BB 8-Mar Sediment 216 ± 15.6 38.0 ± 14.6 0.146 ± 0.100 254 0.593 ± 0.010
OB 2-Feb Sediment 278 ± 34.5 17.1 ± 19.1 0.291 ± 0.060 59 0.253 ± 0.077 413
OB 28-Feb Sediment 253 ± 3.2
CW 8-Mar Sediment 349 ± 34.2
BB 18-Nov Water 11.1 ± 0.9 0.397 ± 0.088
BB 11-Dec Water 0.675 ± 0.034 143.0 ± 18.9 0.581 ± 0.060 247 0.566 ± 0.044 413
BB 7-jan Water 1.58 ± 0.02 10.8 ± 3.2 0.159 ± 0.020 66 0.423 ± 0.250 413
BB 15-Feb Water 1.97 ± 0.56 74.6 ± 16.0 0.422 ± 0.068 177 0.491 ± 0.008 413
BB 28-Feb Water 1.02 ± 0.04 66.9 ± 20.2 0.440 ± 0.081 152 0.611 ± 0.023 517
OB 11-Dec Water 0.568 ± 0.004 144.0 ± 11.8 0.372 ± 0.014 249 0.371 ± 0.012 517
OB 11-Feb Water 2.38 ± 0.47 9.97 ± 6.09 0.289 ± 0.045 34 0.203 ± 0.085 289
OB 15-Feb Water 1.65 ± 0.75 36.8 ± 10.0 0.411 ± 0.045 90 0.485 ± 0.041 413
OB 28-Feb Water 1.61 ± 0.16
CW 7-Jan Water 0.750 ± 0.259
CW 18-Feb Water 0.990 ± 0.585 80.1 ± 9.4 0.352 ± 0.070 227 0.408 ± 0.038 517
CW 8-Mar Water 0.410 ± 0.232 71.4 ± 5.8 0.462 ± 0.064 155 0.620 ± 0.011 517
Chlorophyll-a of the sea ice and benthic samples is measured in mg chl-a m-2. Chlorophyll-a of the water samples is measured in mg chl-a m-3.
rETRmax is the relative maximum electron transfer rate (dimensionless ratio), alpha is the efficiency of light utilization (unit = lmol photons
m-2 s-1)-1), Fv/Fm is the maximum quantum yield of fluorescence (PSII, dimensionless ratio), Ek is the photoacclimation index (lmol photons
m-2 s-1), and Inhib is the lowest value of the RLC to show a decline in rETR (lmol photons m-2 s-1). Water depth of Brown Bay (BB) and
O’Brien Bay (OB) phytoplankton samples was 5 m, while it was 4 m at Casey Wharf (CW). All values are means plus standard deviations
Mar Biol (2012) 159:2827–2837 2829
123
In situ net primary productivity
Sea ice and benthic algal net primary production was
measured using the in situ oxygen flux across the DBL
method (Jorgensen and Revsbech 1985; McMinn et al.
2000a, 2010b). The oxygen microelectrodes (UniSense,
Aarhus) and associated equipment that were deployed to
take the in situ measurements of sea ice and benthic algae
were the same as those used by McMinn et al. (2010b). The
fiber optic light sensor was compared with a 4p PAR sensor
(Biospherical QSP 200), and a linear relationship across a
range of subsurface irradiances was obtained. Light mea-
surements were made by the fiber optic light sensors just
beneath the sea ice and just above the sediment algal mats
for sea ice and benthos measurements, respectively. Light,
temperature, oxygen, and microelectrode positional data
were logged on a PC at the surface approximately every
second. Sea ice primary productivity measurements were
made prior to significant ice melt to ensure the dominant
mode of oxygen transfer was by diffusive rather than
advective processes. As sea ice melts, a layer of fresher
water can develop beneath the ice and similarly, as ice
forms, brine is excluded from the ice which creates a flux
of high salinity water. The development of these salinity
gradients has the potential to significantly influence the
transport of solutes across the ice-water interface (Glud
et al. 2002). However, there was no detectable change in
ice thickness during the experimental period, the temper-
ature remained between -1.7 and -1.8 �C and the salinity
did not vary. This indicates that diffusive rather than
convective molecular transport was responsible for most of
the measured oxygen flux and validates our approach.
The oxygen diffusion flux (J) across the DBL was cal-
culated using the 1-dimensional version of Fick’s first law
of diffusion (Revsbech and Jorgensen 1986):
J ¼ Do � d O2½ �=dxð Þ ð1Þ
where Do = molecular diffusion coefficient (at -1.9 �C =
1.11 9 10-5 cm-2 s-1; Broecker and Peng 1974), d[O2]
= change in oxygen concentration over a depth, dx. To
convert oxygen fluxes into equivalent net productivity values,
the oxygen flux (mmol O2 m-2 h-1) was divided by a pho-
tosynthetic quotient for Antarctic fast ice of 1.03 (Satoh and
Watanabe 1988) and 1.07 for MPB (Longphuirt et al. 2007)
and multiplied by the atomic weight of carbon (12.01). This
value is equivalent to primary production in mg C m-2 h-1.
The daily production rate was estimated by summing the
production each hour over a full 24-h period. The maximum
assimilation number was obtained by dividing the ‘carbon
equivalent’ productivity value by the chlorophyll value to
give units of mg C (mg chl-a)-1 h-1. This change from an
oxygen-based assessment of photosynthesis to a carbon
equivalent maximum assimilation number was made to
enable comparisons with productivity estimates obtained
using the more familiar 14C methods (McMinn et al. 2010b).
Chlorophyll-a fluorescence measurements
Replicate measurements (n = 3) of sea ice algae, phyto-
plankton, and benthic algae were made using a pulse-ampli-
tude-modulated fluorometer (Water-PAM, Walz, Effeltrich,
Germany). The light-acclimated fluorescence (F) was mea-
sured by applying a weak measuring light (\1 lmol photons
m-2 s-1), while a saturating pulse ([3,000 lmol photons
m-2 s-1 for 0.8 s) was applied to determine the light-adapted
maximum fluorescence (Fm0). The ratio of the change in
fluorescence (DF = Fm0 - F) and the maximal fluores-
cence, DF/Fm0, is a measure of the effective quantum yield of
PSII in the illuminated sample. The relative photosynthetic
electron transport rate (rETR) was calculated as the product
of the effective quantum yield of PSII and quantum flux
density of photosynthetically active radiation (PAR; Genty
et al. 1989).
Table 2 Primary production data for Casey 2005/2006
Location Habitat Water depth Date Maximum irradiance Prod/h (O2) Prod/h (C) Prod/d (C) Hours Pmax
Brown Bay Sea ice 8 16 Nov 2005 61 2.14 24.9 163 24 0.64
Brown Bay Sediment 8 26 Nov 2005 20 -0.29 -3.4 -28 0
O’Brien Bay Sea ice 14 7 Dec 2005 42 0.78 9.0 103 24 1.85
O’Brien Bay Sediment 14 8 Dec 2005 11 0.39 4.5 16 14
Casey Wharf Sediment 4 3 Jan 2006 481 2.1 23.9 178 18 0.18
Casey Wharf Sediment 4 12 Jan 2006 382 3.0 34.7 204 18 0.11
Casey Wharf Sediment 4 10 Feb 2006 315 4.5 52.1 38 10 0.29
Casey Wharf Sediment 4 7 Mar 2006 920 3.8 44.2 138 10 0.20
Irradiance refers to maximum midday in situ irradiance (units = lmol photons m-2 s-1), Prod/h (O2) is maximum production measured as mmol
O2 m-2 h-1; Prod/h (C) is the equivalent production in mg C m-2 h-1; Prod/d (C) is the integrated daily production in mg C m-2 day-1; hrs is
the number of hours that there was a net oxygen output; Pmax is the maximum assimilation number derived from the oxygen data and is measured
in mg C (mg chl-a)-1 m-2 h-1; alpha is the photosynthetic efficiency measured as in mg C (mg chl-a)-1 h-1 (lmol photons s-1)-1
2830 Mar Biol (2012) 159:2827–2837
123
All chl-a fluorescence measurements were taken as
close as possible to midday. Care was taken to ensure that
the samples were not exposed to direct sunlight. For sea
ice algae, cells were shaved off the bottom of ice cores
and placed in the measuring cuvette of the Water-PAM
with 1–2 ml of -1.8 �C filtered seawater (McMinn et al.
2005). This method of measurement has the advantage of
not melting the ice and exposing the cells to osmotic and
temperature shocks while making no significant differ-
ence to subsequent fluorescence measurements. Sediment
samples (top 5 mm of each sediment core) were collected
with a small gravity sediment corer, with 15 mm diameter
tubes, and again carried under black plastic into a tent.
Surface sediment was mixed with filtered seawater (col-
lected early in the season when nutrient levels were still
high), shaken, the sediment allowed to settle for 10 s and
the MPB suspension then decanted into a measuring
cuvette. Each sample was exposed to a short burst (5 s) of
far-red light (provided by the WaterPAM unit) to enhance
reoxidation of the QA- pool and obtain a minimal value of
F00 (Krause and Jahns 2003). Seawater for phytoplankton
samples was collected from 5 m under the ice. To per-
form rapid light curves (RLC), samples were light-accli-
mated (to an irradiance as close as possible to ambient,
i.e., approx 10–20 lmol photons m-2 s-1) for 5 min
using the internal actinic light source of the fluorometer.
After 30 s of darkness, rapid light curves were obtained
by illuminating the samples for 10 s before each DF/Fm0
measurement at each of a series of eight incremental
irradiances from 0 to 577 lmol photons m-2 s-1 (White
and Critchley 1999; Ralph and Gademann 2005). Light
was provided by the internal actinic light source, which in
the WaterPAM is centered on 660 nm. The rETR data
generated by the rapid light curves were fitted to the
following equation with a nonlinear least squares regres-
sion (Platt et al. 1980):
rETR ¼ rETRmax½1� expð�aEd=rETRmaxÞ�� expð�bEd=rETRmaxÞ ð2Þ
rETRmax, which is a dimensionless parameter, represents
the maximum potential rETR. a is the initial slope of the
light curve before the onset of saturation and represents
the efficiency of light utilization (unit = (lmol photons
m-2 s-1)-1). Ed (unit = lmol photons m-2 s-1) is the
irradiance (in the general formula 400–700 nm). b is the
parameter characterizing photoinhibition. In the absence of
photoinhibition in the light curves, where b = 0, the
function becomes:
rETR ¼ rETRmax½1� expð�aEd=rETRmax� ð3Þ
The photoacclimation parameter based on fluorescence, Ek,
was calculated by dividing rETRmax by a.
Standard RLCs only generate 8 estimates of DF/Fm0 in
their P versus E function, unlike traditional 14C-based
P versus E functions, which typically have 20 or more data
points (Lewis and Smith 1983). This low number of data
points makes the correct estimation of both a and b unre-
liable. Therefore, because none of the communities in this
study were inhibited at their maximum ambient irradiance,
we removed any ‘inhibited’ data points (rarely more than
one per RLC) from the nonlinear least squares regressions.
In this way, we achieved a more robust estimate of
rETRmax and a. Photosynthetic parameters from the dif-
ferent sites and sampling periods were compared using a
series of targeted 1-way ANOVAs that was necessary
because of the unbalanced experimental design with SPSS
software. Significance was determined at P \ 0.05. Gain
settings on the PAM were consistently between 5 and 10
for the MPB and sea ice algae but were between 15 and 18
for the phytoplankton.
Results
Chlorophyll-a
Chl-a from the sea ice, water column, and benthos was
measured intermittently over a period of approximately
4 months (Table 1). Sea ice algal biomass was relatively
low, 21.6 ± 13.3 mg chl-a m-2 at Brown Bay and only
3.8 ± 1.7 mg chl-a m-2 at O’Brien Bay. In contrast, the
benthic microalgal biomass was consistently high at both
sites. At Brown Bay, it was consistently above 200 mg
chl-a m-2 and reached 367.0 ± 57.9 mg chl-a m-2 in
November 2005, while at O’Brien Bay, it varied between
253.0 ± 3.2 mg chl-a m-2 and 278.0 ± 34.3 mg chl-
a m-2. Benthic microalgal biomass at Casey Wharf was
349.0 ± 34.2 mg chl-a m-2. The sediment at all sites was
mostly comprised of sandy mud (Stark 2000) and the
oxygenated zone extended to 4.5 mm below the surface.
Phytoplankton biomass fluctuated between a minimum of
0.410 ± 0.232 lg chl-a l-1 and a maximum of 11.1 ±
0.9 lg chl-a l-1. While a single high value was recorded
during the period of spring sea ice melt (18 Nov at BB,
11.1 ± 0.9 lg chl-a l-1), the concentration of chl-a at all
three sites was generally between 0.5 and 2.5 lg chl-a l-1
(December to March). Species composition of the
November phytoplankton sample was overwhelmingly
comprised of sea ice taxa such as Entomoneis kjellmannii,
indicating a likely origin from the overlying sea ice. Depth-
integrated biomass levels (assuming a well mixed water
column) were between a minimum of 1.6 mg chl-a m-2
(Casey Wharf, March 8, 2006) and a maximum of 88.8 mg
chl-a m-2 (Brown Bay, 18 November 2005).
Mar Biol (2012) 159:2827–2837 2831
123
Primary production
Sea ice
Primary production by sea ice algae was measured at each
site, although 24-h data were only collected from Brown
Bay and O’Brien Bay (Table 2, Fig. 2). Net primary pro-
duction occurred continuously over the 24-h period at both
sites. Maximum production was 2.14 mmol O2 m-2 h-1 at
Brown Bay and 0.77 mmol O2 m-2 h-1 at O’Brien Bay.
Daily net primary production was equivalent to 163 mg
C m-2 day-1 at Brown Bay and 103 mg C m-2 day-1 at
O’Brien Bay (Fig. 2). Maximum photosynthetic rates were
0.64 mg C (mg chl-a)-1 m-2 h-1 at Brown Bay and
1.85 mg C (mg chl-a)-1 m-2 h-1 at O’Brien Bay. Because
net oxygen production was always positive, it was not
possible to determine compensation points.
Benthos
When sea ice was present, net primary production by the
MPB was either very low or negative. At Brown Bay in
November 2005 there was a net draw down of oxygen with
minimum oxygen consumption equivalent to 0.29 mmol
O2 m-2 h-1 and daily net consumption equivalent to
28 mg C m-2 day-1. At O’Brien Bay during December
2005, the maximum net production was equivalent to
0.39 mmol O2 m-2 h-1 and daily production was equiva-
lent to 16 mg C m-2 day-1 (Table 2).
Net benthic primary production was measured at Casey
Wharf in January, February, and March 2006 (Table 2,
Fig. 3). Net oxygen export occurred during this period and
daily maxima varied between a minimum of 2.1 mmol O2
m-2 day-1 on January 3, 2006 and a maximum of 4.5
mmol O2 m-2 day-1 on February 10, 2006. Daily pro-
duction rates varied between a carbon equivalent of
38 mg C m-2 day-1 on February 10, 2006 to 204 mg
C m-2 day-1 on January 12, 2006. In early January, there
was net oxygen export for 18 h of the day but this
decreased to 10 h in February and March (Fig. 3).
Maximum photosynthetic rates (*Pmax) at Casey Wharf
remained between 0.109 and 0.292 mg C (mg chl-a)-1
m-2 h-1 during January, February, and March and com-
pensation points varied between 5 and 15 lmol photons
m-2 s-1 (Table 2). The thickness of the oxygenated zone
within the sediments did not vary significantly between
sampling periods but did vary between day and night
(P \ 0.05). During the day, it extended up to 4.5 ± 0.4
mm into the sediment, while at night, it contracted to
approximately 2.5 ± 0.2 mm (Fig. 4).
Photosynthesis (PAM fluorometry)
Rapid Light Curves (RLC) were successfully obtained
from microalgae in the sea ice, benthos, and water column.
Sea ice RLCs were only collected in December, when the
sea ice was still present. RLCs from the sediments were
collected between December and March and from the
water column between November and March.
Sea ice
There was no significant difference in maximum dark-adapted
Fv/Fm values between sites, 0.319 ± 0.004 at Brown Bay and
0.338 ± 0.159 at O’Brien Bay (n = 3, P [ 0.05, Table 1).
Although the efficiency of light utilization values (a) were
more variable than the Fv/Fm values, Brown Bay 0.227 ±
0.029 and O’Brien Bay 0.440 ± 0.236, they were not sig-
nificantly different (n = 3, P [ 0.05). However, maximum
electron transport rates (rETRmax) at the two sites were sig-
nificantly different with a rate of 31.7 ± 13.9 in Brown Bay
Fig. 2 Diurnal sea ice primary production in Brown Bay (16–17
Nov) and O’Brien Bay (6–7 Dec). Maximum midday irradiances
relevant to these primary production profiles are given in Table 1.
Chlorophyll-a values are given in Table 1
2832 Mar Biol (2012) 159:2827–2837
123
and 81.0 ± 18.9 at O’Brien Bay (n = 3, P [ 0.05). Pho-
toinhibition was only evident at actinic light levels above
413 lmol photons m-2 s-1 in Brown Bay and above
289 lmol photons m-2 s-1in O’Brien Bay.
Benthos
In the sediments, there were significant differences among
the Fv/Fm values at the benthic sampling sites (Table 1).
The highest mean value of 0.593 ± 0.010 obtained on
March 8, 2006 from Brown Bay was significantly higher
than other Brown Bay and O’Brien Bay values (n = 3,
P [ 0.05). Other benthic Fv/Fm values varied between
*0.25 and 0.56. Photoinhibition was only evident at
actinic light levels above 413 lmol photons m-2 s-1 in
both Brown Bay and O’Brien Bay.
The efficiency of light utilization values (a), which were
between 0.146 ± 0.100 and 0.323 ± 0.097, and maximum
electron transport rates (rETRmax), which were between
17.1 ± 19.1 and 38.0 ± 14.6, did not vary significantly
among sites (n = 3, P [ 0.05).
Water column
Phytoplankton samples showed more variability between
sampling periods than the benthic algae. Fv/Fm varied
between a minimum of 0.203 ± 0.085 and a maximum of
0.620 ± 0.011 and while most samples were significantly
different from each other (n = 5, P [ 0.05), there was no
sequential pattern in these differences (Table 1).
The efficiency of light utilization (a) mostly varied
within a narrow range, *0.35–0.46, with only one being
above this range (Brown Bay 11 Dec, 0.581) and one
below (Brown Bay 7 Jan, 0.159). These exceptions were
significantly different from remaining samples but no other
samples were significantly different (Table 1).
Maximum photosynthetic rates (rETRmax) of phyto-
plankton samples varied over a wide range from 10.0 ± 6.1
Fig. 3 Diurnal primary production of MPB at Casey Wharf; top left 2–3 Jan, bottom left 11–12 Jan, top right 9–10 Feb, bottom right 7–8 Mar.
Maximum midday irradiances relevant to these primary production profiles are given in Table 2. Chlorophyll-a values are given in Table 1
Mar Biol (2012) 159:2827–2837 2833
123
(O’Brien Bay, 11 Feb) to 144.0 ± 11.8 (O’Brien Bay11
Dec). Most samples from the same location were signifi-
cantly different from each other but it was not possible to
identify a seasonal pattern in the change. Photoinhibition
was only evident at actinic light levels above 413 lmol
photons m-2 s-1 in Brown Bay, between 289 lmol photons
m-2 s-1 and 517 lmol photons m-2 s-1 in O’Brien Bay
and above 517 lmol photons m-2 s-1 at Casey Wharf
(Table 1).
Discussion
Species succession and temporal biomass patterns in
coastal East Antarctica are reasonably well known with
respect to sea ice algae and phytoplankton and are quite
consistent between years. The sea ice algal biomass con-
tinues to grow throughout spring until warming by under
ice seawater causes the bottom algal community to drop
out (McMinn and Ashworth 1998). The fast ice usually
breaks up and drifts away by December or early January
(McMinn et al. 2004) allowing an early diatom bloom,
which consumes much of the available nutrients, followed
by blooms of dinoflagellates, phytoflagellates, and/or
Phaeocystis (Davidson and Marchant 1992; McMinn and
Hodgson 1993; McMinn et al. 2000b). This pattern con-
trasts with locations such as McMurdo Sound that have
more persistent ice cover and where much of the phyto-
plankton biomass is advected in from ice-free areas
(Dayton and Oliver 1977). Phytoplankton biomass usually
peaks in spring and declines in late summer (Rivkin 1991;
Robinson et al. 1999). Sea ice algal biomass at Casey in
2005 was relatively low (\25 mg chl-a m-2) and signifi-
cantly lower than previously measured values from eastern
Antarctica, which typically exceed 100 mg chl-a m-2 in
spring (McConville et al. 1985; McMinn and Ashworth
1998) and can exceed 300 mg chla m-2 in other parts of
Antarctica (Palmisano and Sullivan 1983; Trenerry et al.
2002). However, similarly low values were reported from
the Casey region in the previous year (McMinn et al.
2010b) and probably relate to the timing of sampling as
much of the sea ice algae had probably fallen into the
underlying water column, as evidenced by the much
increased phytoplankton biomass, which was dominated by
sea ice taxa. Primary production within the sea ice was
moderate and comparable to estimates from the same
location in 2004 (0.73 mmol O2 m-2 h-1, McMinn et al.
2010b) and in 1983 (1.58–32.92 mg C m-2 h-1, McCon-
ville et al. 1985).
The photosynthetic parameters from the sea ice algae of
both Brown Bay and O’Brien Bay are similar and indicate
a community mostly well-acclimated to the light, temper-
ature, and nutrient conditions. Fv/Fm values were both
*0.32, which while low compared to most phytoplankton
and MPB measurements, are consistent with the values
regularly obtained with sea ice samples (Ralph et al. 2005,
2007; McMinn et al. 2010a). They were considerably lower
than from the same location a year earlier (McMinn et al.
2010b), which were between 0.485 and 0.668; the reason
for this difference and the unusually high values in 2004 is
not currently known. There was no evidence of photoin-
hibition at ambient environmental irradiances (i.e.,
\100 lmol photons m-2 s-1), and it is likely that an
active xanthophyll cycle was providing effective photo-
protection (Griffith et al. 2009).
Mid- to late summer nutrient concentrations at near
shore coastal Antarctic sites are usually drawn down to
very low levels (Rivkin 1991; McMinn et al. 1995, 2000b)
and together with grazing pressure may have contributed to
the decline in phytoplankton biomass seen throughout
summer at Casey (Rivkin 1991; Davidson and Marchant
1992; Robinson et al. 1999). In this study, phytoplankton
biomass peaked in November with subsequent levels of
biomass being considerably lower but comparable to other
sites in eastern Antarctica, such as at Davis Station
(McMinn et al. 2000b; Pearce et al. 2008), and Terra
Adelie to the Mertz Glacier (Beans et al. 2008). Photo-
synthetic parameters were variable but depressed Fv/Fm
values mostly indicated a community under moderate
levels of stress. With the exception of the data from the end
of the season (28 February and 8 March; average Fv/
Fm = 0.616, Table 1), the average Fv/Fm values were only
0.46. Even though nutrient concentrations were not mea-
sured, data from the same location and similar locations in
Fig. 4 Example of diurnal change in oxygen concentration within the
sediment at Casey Wharf at three different times, 1:47 AM, 3:07 PM
and 5:45 PM on the same day (6 March 2006). The depth is given as
mm above the sediment. Irradiances at the sediment surface were
\0.5 lmol photons m-2 s-1 at 1:47 AM, 576 lmol photons m-2 s-1
at 3:07 PM and 368 lmol photons m-2 s-1 at 5:45 PM. Chlorophyll-
a concentration was 349 ± 34.2 mg chl-a m-2
2834 Mar Biol (2012) 159:2827–2837
123
previous years at this time of year indicate low concen-
trations of both phosphate and nitrate ? nitrite with the
latter probably reaching limiting concentrations (McCon-
ville et al. 1985; Perrin et al. 1987). It is probable that these
are contributing to the reduced maximum quantum yield of
PSII values.
Benthic microalgal mats have a notoriously patchy dis-
tribution, and attempts to quantify this biomass have always
been beset with a large degree of uncertainty (Glud et al.
2009). Benthic biomass levels, which were here between
200 and 400 mg chl-a m-2, are consistent with previous
estimates from this area, that is, *70–200 mg chl-a m-2
(McMinn et al. 2010b) and *200 mg chl-a m-2 (McMinn
et al. 2004) and also with many Arctic studies (Glud et al.
2009). Interestingly, Blanchard et al. (2000), in a modeling
study of MPB biomass of intertidal areas of France, dem-
onstrated that biomass converged toward a maximum of
*300 mg chl-a m-2 but diurnal tides, which caused sedi-
ment re-suspension and introduced grazing, reduced the
biomass to an equilibrium level of *160 mg chl-a m-2.
Although from a different environment, these biomass
levels are quite similar to those found in the Casey area. The
relatively stable benthic biomass levels throughout the
summer at Casey in 2005/2006 also imply that even though
primary production was significant, grazing pressure was
approximately equal to production.
The relatively low Ek and rETRmax values of the MPB,
which were generally lower than those of the phytoplank-
ton, suggest some level of shade adaption. Blanchard et al.
(2004) suggested that at high biomass levels, that is,
[200 mg chl-a m-2, the self-shading is likely to be
extreme. They also found that MPB cells can often with-
stand short exposure to high irradiance and only become
photo-inhibited at the same irradiance after exposure of
approximately 90 min. The 10 s exposures used in the
RLCs at Casey therefore does not reliably determine the
irradiance levels at which cells become photo-inhibited and
the real values are likely to be lower than those presented
in Table 1.
The micro-oxygen electrode system of measuring MPB
primary productivity produced a dataset with a systematic
diurnal response and a close relationship with irradiance that
is consistent with the fluorescence-based measurements
using PAM fluorometry. Daily production rates were
between 38 and 178 mg C m-2 day-1. This compares with
daily production levels of 70.8 mg C m-2 day-1 in 2004
(McMinn et al. 2010b). Glud et al. (2009) recently reviewed
microalgal production in the Arctic and reported a large
range of values, obtained by using several different methods,
with values up to 1,370 mg C m-2 day-1, although most
were in a range of 100–500 mg C m-2 day-1, which is
consistent with those reported here from the Antarctic.
Measurements of oxygen production by the MPB at night
in the dark, when there was a net uptake of oxygen,
approximate net community respiration. When the sea ice
was present, there was no net export of oxygen and the
oxygen uptake throughout the day and night represents net
community respiration (equivalent to an average of
*0.17 mmol O2 m-2 h-1). Uptake in the dark (i.e., at night)
was maximal in February 2006 when it reached the equiva-
lent of *1.5 mmol O2 m-2 h-1, which is approximately
34 % of the maximum output in the light and this remained
consistent through to March (33 %). It should be noted that
Casey Station is located at 66.28�S (north of the Antarctic
Circle) and so never experiences true 24 h daylight or
darkness. These export/uptake proportions are consistent
with those measured in shallow marine benthic communities
worldwide (Sundback and Jonsson 1988). Although the
MPB had lower rETRs at ambient environmental irradiances
than the phytoplankton (Table 1), their much greater bio-
mass (Table 1) would have ensured they made an equal if not
greater contribution to primary production than the phyto-
plankton during the ice-free period at the Casey Wharf site.
With the exception of the single, very high depth-integrated
phytoplankton biomass level on 18 November (89 mg chl-
a m-2), water column biomass levels were less than 10.0 mg
chl-a m-2, which compares with biomass levels consistently
greater than 200 mg chl-a m-2 in the MPB. McMinn et al.
(2010b), using a method based on PAM-measured rETRs,
estimated the contribution of the MPB to total daily primary
production at the same location and at this time of year to be
approximately 90 %. This assessment, however, is consid-
ered indicative only as the inherent assumptions are some-
times difficult to verify (Glud et al. 2009).
Whether the benthos at Casey is a net importer or
exporter of organic carbon (Urabe et al. 2004) can be
assessed by integrating the net respiration losses under the
ice measured in November (equivalent to 2.4 mmol O2
m-2 day-1) over the length of the ice-covered period,
generally considered to be May to December (576 mmol
O2 m-2), and comparing it with the average net oxygen
daily production measured between January and March
(11.9 mmol O2 m-2 day-1) and integrating this over the
ice-free period from January to April (1,428 mmol O2
m-2 day-1). This simple calculation strongly implies that
the MPB is a net exporter of carbon into the local marine
ecosystem and is thus a source of food for higher trophic
levels. Unfortunately, it is not possible to make a calcula-
tion for the whole ecosystem as, although productivity
measurements were made for the sea ice, they were not
made for the water column.
Macroalgae are generally thought to make only a rela-
tively minor contribution to most Antarctic coastal eco-
systems but they can be locally abundant. In the Casey area
Mar Biol (2012) 159:2827–2837 2835
123
for instance, the large kelp, Himantothalus sp., has been
found on some rocky substrates down to 50 m (Stark
2000), although none were present in the areas investigated
here. As no attempt has ever been made to quantify their
abundance, distribution or productivity, it is not possible to
determine their broader contribution to local primary
production.
The melting sea ice in spring exports a large pulse of
biomass to the benthos within a short period of time, and in
some areas, this equates to a large proportion of the annual
nutrition to the benthic invertebrate community (Dayton
et al. 1986). It is inevitable that both the timing and
magnitude of this pulse will be influenced by climate
change (Arrigo and Thomas 2004), and although sea ice
algae do not have a higher nutritional value than phyto-
plankton (or probably MPB), they do provide a pulse of
production to the sea floor in spring that would be
unavailable from phytoplankton (Leu et al. 2010). Many
Antarctic benthic invertebrates exhibit a high degree of
omnivory, however, relying on multiple food sources
(Dayton 1990), that includes both settling sea ice algae and
benthic algae (Gillies et al. 2012). While a change in the
timing of primary production might affect invertebrate
reproduction success (Pearse et al. 1991), the annual
availability is likely to remain relatively unaffected.
There has been an expansion of Antarctic sea ice in
recent decades (Turner et al. 2009); however, a significant
decrease is expected by the end of the century. This will
inexorably lead to a decline in annual sea ice algae pro-
duction (Arrigo and Thomas 2004), as there is less time for
the algal biomass to accumulate. Whether this will lead to
greater annual phytoplankton production, however, is
unclear. In the Chukchi Sea and western Beaufort Sea, an
area traditionally considered nutrient limited for much of
the year, it was thought that a loss of sea ice would not
necessarily lead to a significant net increase in annual
primary productivity (Walsh et al. 2005). However, unex-
pected large phytoplankton blooms have indeed followed
the recent unprecedented summer ice retreat (Arrigo et al.
2008), which suggests that predictions based on our current
understanding of these systems may be unreliable.
Acknowledgments Andrew McMinn and Peter Ralph acknowledge
support from an Australian Research Council (ARC) Discovery
Grant. Logistic support was provided by the Australian Antarctic
Division.
References
Arrigo KR, Thomas DN (2004) Large scale importance of sea ice
biology in the Southern Ocean. Antarct Sci 16:471–486
Arrigo KR, Van Dijken G, Pabi S (2008) The impact of a shrinking
Arctic ice cover on marine primary production. Geophys Res
Lett 35:L19603. doi:10.1029/2008GL035028
Beans C, Hecq JH, Koubbi P, Vallet C, Wright S, Goffart A (2008) A
study of the diatom-dominated microplankton summer assem-
blages in coastal waters from Terre Adelie to the Mertz Glacier,
East Antarctica (139�E–145�E). Polar Biol 31:1011–1117
Blanchard GF, Guarini J-M, Orvain F, Sauriau P-G (2000) Dynamic
behaviour of benthic microalgal biomass in intertidal mudflats.
J Expt Mar Biol Ecol 264:85–100
Blanchard GF, Guarini J-M, Dang C, Richard P (2004) Characterizing
and quantifying photoinhibition in intertidal microphytobenthos.
J Phycol 40:692–696
Broecker WS, Peng TH (1974) Gas exchange rates between air and
sea. Tellus 26:21–35
Davidson AT, Marchant HJ (1992) Protist abundance and carbon
concentration during a Phaeocystis-dominated bloom at an
Antarctic coastal site. Polar Biol 12:387–395
Dayton PK (1990) Polar benthos. In: Smith WO (ed) Polar
oceanography, part B: chemistry, biology, and geology. Aca-
demic Press, London, pp 631–685
Dayton PK, Oliver JS (1977) Antarctic soft-bottom benthos in
oligotrophic and eutrophic environments. Science 197:55–58
Dayton PK, Watson D, Palmisano A, Barry JP, Oliver JS, Rivera D
(1986) Distributional patterns of benthic microalgal standing
stock at McMurdo Sound, Antarctic. Polar Biol 6:207–213
Genty B, Briantias JM, Baker NR (1989) The relationship between
the quantum yield of photosynthetic electron transport and
quenching of chlorophyll fluorescence. Biochem Biophys Acta
990:87–92
Gilbert NS (1991) Primary production by benthic microalage in near
shore marine sediments of Signey Island, Antarctica. Polar Biol
11:339–346
Gillies CL, Stark JS, Johnstone GJ, Smith SDA (2012) Carbon flow
and trophic structure of an Antarctic coastal benthic community
as determined by delta C-13 and delta N-15. Estuar Coast Shelf
Sci 97:44–57
Glud RN, Kuhl M, Wenzhofer F, Rysgaard S (2002) Benthic
microphytes of a high arctic fjord: importance for ecosystem
primary production. Mar Ecol Prog Ser 238:15–29
Glud RN, Woelfel J, Karsten U, Kuhl M, Rysgaard S (2009) Benthic
microalgal production in the Arctic: applied methods and status
of the current database. Bot Mar 52:559–571
Griffith GP, Vennell R, Lamare MD (2009) Diadinoxanthin cycle of
the bottom ice algal community during spring in McMurdo
Sound, Antarctica. Polar Biol 32:623–663
Jorgensen BB, Revsbech NP (1985) Diffusive boundary layers and
the oxygen uptake of sediments and detritus. Limnol Oceanog
30:111–122
Knox GA (2006) Biology of the Southern Ocean, 2nd edn. CRC
Press, Christchurch
Krause GH, Jahns P (2003) Pulse amplitude modulated chlorophyll
flourometry and its applications in plant science. In: Green BR,
Parson WW (eds) Light-harvesting antennas in photosynthesis;
advances in photosynthesis and respiration. Kluwer, Dordrecht,
pp 373–399
Kuhl M, Lassen C, Jorgensen BB (1994) Light penetration and light
intensity in sandy marine sediments measured with irradiance
and scalar irradiance fibre-optic microprobes. Mar Ecol Prog Ser
105:139–145
Leu E, Wiktor J, Soreide JE, Berge J, Falk-Petersen S (2010)
Increased irradiance reduces food quality of sea ice algae. Mar
Ecol Prog Ser 411:49–60
Lewis MR, Smith JC (1983) A small volume short incubation time
method for the measurement of photosynthesis as a function of
incident irradiance. Mar Ecol Prog Ser 13:99–102
Longphuirt SN, Clavier J, Grall J, Chauvaud L, Le Loch F, Le Berre F,
Flye-Sainte-Marie L, Richard J, Leynaert A (2007) Primary
production and spatial distribution of subtidal microphytobenthos
2836 Mar Biol (2012) 159:2827–2837
123
in a temperate coastal system, the Bay of Brest, France. Estuar
Coast Shelf Sci 74:367–380
McConville MJ, Mitchell C, Wetherbee R (1985) Patterns of carbon
assimilation in a microalgal community from annual sea ice in
eastern Antarctica. Polar Biol 4:135–142
McMinn A (1996) Preliminary investigation of the contribution of
fast ice algae to the spring phytoplankton bloom in Ellis Fjord,
eastern Antarctica. Polar Biol 16:301–307
McMinn A, Ashworth C (1998) The use of oxygen microelectrodes to
determine the net production by an Antarctic sea ice algal
community. Antarct Sci 10:30–35
McMinn A, Hodgson D (1993) Seasonal phytoplankton succession in
Ellis Fjord, eastern Antarctica. J Plankton Res 15:925–938
McMinn A, Gibson J, Hodgson D, Aschman J (1995) Nutrient
limitation in Ellis Fjord, Antarctica. Polar Biol 15:269–276
McMinn A, Ashworth C, Ryan KG (2000a) In situ net primary
productivity of an Antarctic fast ice bottom algal community.
Aquat Microb Ecol 21:177–185
McMinn A, Bleakley N, Steinburner K, Roberts D, Trenerry L (2000b)
Effect of permanent sea ice cover and different nutrient regimes
on the phytoplankton succession of fjords of the Vestfold Hills
Oasis, eastern Antarctica. J Plankton Res 22:287–303
McMinn A, Runcie J, Riddle M (2004) The effect of seasonal sea ice
break-out on the photosynthesis of benthic diatom mats at Casey,
Antarctica. J Phycol 40:62–69
McMinn A, Hirawake T, Hamaoka T, Hattori H, Fukuchi M (2005)
Contribution of benthic microalgae to ice covered coastal
ecosystems in northern Hokkaido, Japan. J Mar Biol Assoc
UK 85:283–289
McMinn A, Martin A, Ryan K (2010a) Phytoplankton and sea ice
biomass and physiology during the transition between winter and
spring (McMurdo Sound, Antarctica). Polar Biol 33:1547–1556
McMinn A, Pankowski A, Ashworth C, Bhagooli R, Ralph P, Ryan K
(2010b) In situ net primary productivity and photosynthesis of
Antarctic sea ice algal, phytoplankton and benthic algal
communities. Mar Biol 157:1345–1356
Miller KA, Pearse JS (1991) Ecological studies of seaweeds in
McMurdo sound, Antarctica. Am Zool 31:35–48
Palmisano AC, Sullivan CW (1983) Sea ice microbial communities
(SIMCO) I. Distribution, abundance and primary production of
microalgae in McMurdo Sound, Antarctica. J Phycol 18:489–498
Pearce I, Davidson AT, Wright S, Van Den Enden R (2008) Seasonal
changes in phytoplankton growth and microzooplankton grazing
at an Antarctic coastal site. Aquat Microb Biol 50:157–167
Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic
benthic marine invertebrates: tempos, modes, and timing. Am
Zool 31:65–80
Perrin RA, Lu P, Marchant HJ (1987) Seasonal variation in marine
phytoplankton and ice algae at a shallow coastal site. Hydrobi-
olgia 146:33–46
Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of
photosynthesis in natural assemblages of marine phytoplankton.
J Mar Res 38:687–701
Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to
assess photosynthetic activity. Aquat Bot 82:222–237
Ralph PJ, McMinn A, Ryan K, Ashworth C (2005) Short-term effect
of temperature on the photokinetics of microalgae from the
surface layers of Antarctic pack ice. J Phycol 41:763–769
Ralph PJ, Ryan KG, Martin A, Fenton G (2007) Melting-out of sea-
ice algae causes greater photosynthetic stress than freezing-in.
J Phycol 43:948–956
Revsbech NP, Jorgensen BB (1986) Microelectrodes: their use in
microbial ecology. In: Marshall KC (ed) Advances in microbial
ecology. Plenum Press, NY, pp 293–352
Rivkin RB (1991) Seasonal patterns of planktonic production in
McMurdo Sound, Antarctica. Am Zool 31:5–16
Robinson C, Archer S, Williams PJ (1999) Microbial dynamics in
coastal waters of East Antarctica: plankton production and
respiration. Mar Ecol Prog Ser 180:23–36
Satoh H, Watanabe K (1988) Primary productivity in the fast ice area
near Syowa Station, Antarctica, during spring and summer
1983/1984. J Oceanogr Soc Jpn 44:287–292
Skowronski RSP, Gheller PF, Bromberg S, David CJ, Petti MAV,
Corbisier TN (2009) Distribution of microphytobenthic biomass
in Martel Inlet, King George Island (Antarctica). Polar Biol
32:839–851
Stark JS (2000) The distribution and abundance of soft-sediment
macrobenthos around Casey Station, East Antarctica. Polar Biol
23:840–850
Strickland JDH, Parsons TR (1972) A practical handbook of seawater
analysis, 2nd ed. Bull Fish Res Board Canada, vol 167, pp 1–311
Sundback K, Jonsson B (1988) Microphytobenthic productivity and
biomass in sublittoral sediments of a stratified bay, southeastern
Kattegat. J Expt Mar Biol Ecol 122:63–81
Trenerry LJ, McMinn A, Ryan KG (2002) In situ oxygen microelec-
trode measurements of bottom-ice algal production in McMurdo
Sound, Antarctica. Polar Biol 25:72–80
Turner J, Comiso JC, Marshall GJ, Lachlan-Cope TA, Bracegirdle T,
Maksym T, Meredith MP, Wang Z, Orr A (2009) Non-annular
atmospheric circulation change induced by stratospheric ozone
depletion and its role in the recent increase of Antarctic sea ice
extent. Geophys Res Lett. doi:10.1029/2009GL037524
Urabe J, Takehito Y, Gurung TB, Sekino T, Tsugeki N, Nozaki K,
Maruo M, Nakayama E, Nakanishi M (2004) The production-to-
respiration ratio and its implication in Lake Biwa, Japan. Ecol
Res 20:367–375
Walsh JJ, Dieterle DA, Maslowski W, Grebmeier JM, Whitledge TE,
Flint M, Sukhanova IN, Bates N, Cota GF, Stockwell D, Moran
SB, Hansell DA, McRoy CP (2005) A numerical model of
seasonal primary production within the Chukchi/Beaufort Seas.
Deep Sea Res II Topical Stud Oceanog 52:3541–3576
White AJ, Critchley C (1999) Rapid light curves: a new fluorescence
method to assess the state of photosynthetic apparatus. Photo-
synth Res 59:63–72
Mar Biol (2012) 159:2827–2837 2837
123