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

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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

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(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.

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