Sea ice algae Major contributors to primary production and algal biomass in the Chukchi and

40 Pages·2008·0.76 MB·English

by  Rolf Gradinger

Author’s Accepted Manuscript
Sea ice algae: Major contributors to primary
production and algal biomass in the Chukchi and
BeaufortseaduringMay/June2002
RolfGradinger
PII: S0967-0645(08)00346-9
DOI: doi:10.1016/j.dsr2.2008.10.016
Reference: DSRII2455
www.elsevier.com/locate/dsr2
Toappearin: Deep–SeaResearchII
Accepteddate: 27October2008
Citethisarticleas:RolfGradinger,Seaicealgae:Majorcontributorstoprimaryproduction
and algal biomass in the Chukchi and Beaufort sea during May/June 2002, Deep–Sea
ResearchII(2008),doi:10.1016/j.dsr2.2008.10.016
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Title

Sea ice algae: major contributors to primary production and algal biomass in the

Chukchi and Beaufort Sea during May/June 2002

Rolf Gradinger
University of Alaska Fairbanks

Fairbanks, AK 99775-7220 t
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[email protected]
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Abstract
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Sea ice and water samples were collected at 14 stations on the shelves and slope regions
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of the Chukchi and Beaufort Seas during the spring 2002 expedition as part of the Shelf
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Basin Interaction Studies. Algal pigment content, particulate organic carbon and nitrogen
and primary productivity were estimated f or both habitats based on ice cores, brine
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collection and water samples from 5m depth. The pigment content (0.2 - 304.3 mg
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pigments m-2) and primary produtctivity (0.1 to 23.0 mg C m-3 h-1) of the sea ice algae
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significantly exceeded water column parameters (0.2 and 1.0 mg pigments m-3; <0.1 to
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0.4 mg C m-3 h-1), making sea ice the habitat with the highest food availability for
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herbivores in earlyc spring in the Chukchi and Beaufort Seas. Stable isotope signatures for
ice and water sAamples did not differ significantly for δ15N, but for δ13C (ice: -25.1 to -
14.2‰; water: -26.1 to -22.4‰). The analysis of nutrient concentrations and the pulse
amplitude modulated fluorescence signal of ice algae and phytoplankton indicate that

nutrients were the prime limiting factor for sea ice algal productivity. The estimated

spring primary production of about 1-2 g C m-2 of sea ice algae on the shelves requires
the use of substantial nutrient reservoirs from the water column.

Keywords: Arctic, Beaufort Sea, Chukchi Sea, primary production, sea ice,
phytoplankton, PAM, nutrients, ice algae
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Introduction
Arctic shelves comprise roughly 50% of the Arctic Ocean and are the regions where sea

ice conditions have changed most dramatically over the last decades (ACIA 2004). The

most drastic changes occurred within the Chukchi and Beaufort Seas where the seasonal
and spatial properties of biological processes are strongly dependent on exchange

processes with the Bering Sea and the adjacent deep Arctic Ocean (Codispoti et al. 2005).
The Chukchi and in particular the Beaufort Sea exhibited substantial interannual
variability in summer minimum ice extent with record low concentrations in 1997/1998

(McPhee et al. 1998, Jeffers et al. 2001), 2002/2003 and 2005 (Stroeve et al. 20t07),
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leaving the Beaufort and Chukchi Seas ice-free well above 75˚N latitude. In contrast, the
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early and mid-1980s were characterized by heavy ice years in the same area, with almost
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the entire US Beaufort Sea sector ice-covered throughout the summers of 1980, 1983 and
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1985 (Gloersen et al. 1992). u
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Sea ice is a major regulating component in controlling pelagic and benthic production
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through modulating water column stratification and light fields (e.g. Hunt et al. 2002, Hill
et al. 2005, Bluhm and Gradinger in press) . In addition, sea ice algae contribute between
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4 and 26 % to total primary production in seasonally ice-covered waters (Legendre et al.
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1992), and this fraction may excteed 50 % in perennially ice covered waters due to the
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year-round reduction in shortwave radiation penetrating the water column (Gosselin et al.
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1997). While it is generally acknowledged that sea ice primary production does
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contribute significantly to the biogeochemical cycles in Arctic waters (e.g. Gosselin et al.
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1997, Søreide Aet al. 2006), a thorough evaluation of the impacts of proposed and
observed changes in the sea ice regime on the sea ice biology and its linkages to its
environment is still in its early stages.

Ice algal parameters vary on various temporal and spatial scales. On a local scale, the
biological patchiness of algal parameters in sea ice is relatively low (frequently < 15%)
compared to >50% between locations (regional scale) driven by the physico-chemical
settings (Gosselin et al. 1997, Gradinger 1999, Haecky and Andersson 1999, Steffens et
al. 2006). Regional data on ice algal activity and biomass are still very sparse and greatly
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limited in time and space due to difficulties in accessing sea ice habitats at different times
of year and substantial challenges posed to adapting standard methodologies to the ice

environment (Gosselin et al. 1997, Gradinger 1999, Mock and Gradinger 1999). Due to

these constraints, the overall data set on Arctic ice algal biomass and productivity is
approximately two orders of magnitude smaller than that assembled for the pelagic realm.

Temporal variation of sea ice biological characteristics is high with factors of about 10
for algal and bacterial biomass, and over 50 for primary and bacterial production reported
in the very few time series data sets (Horner 1980, Smith et al. 1988, Gradinger et al.

1991, Haecky and Anderson 1999). A significant fraction of this spatial and temtporal
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variability is directly linked to environmental variables, in particular light availability and
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nutrient supply, as modulated by the snow cover, ice morphology and microstructure
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(Sullivan et al. 1985, Gosselin et al. 1986, Gradinger et al. 1991, Legendre et al. 1991). In
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Arctic summer, such inherent variability is amplified in multui year sea ice by the local
production and redistribution of meltwater (Eicken 1994n).
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The NSF funded Shelf-Basin Interaction (SBI) studies project (Grebmeier and
Harvey 2005) aimed at providing a thorou gh understanding of the current status of the
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Chukchi/Beaufort ecosystems with a regional focus on the outer shelves and slopes. We
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used the opportunity during the StBI 2002 spring expedition to the Chukchi/Beaufort Sea
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shelf and slope regions to address the following hypotheses in this regional context:
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(1) Sea ice contributes significantly to algal biomass and production during periods of
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ice cover.
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(2) The stable Aisotope composition of the ice-produced material derives from pelagic data
and can be used to assess the cryo-pelagic-benthic coupling.
(3) The final concentration of ice algal biomass is mainly regulated by the available

nutrient reservoir in the water column.

and
(4) The accumulation of algal biomass within the sea ice can alter the primary production
of phytoplankton by substantial reduction of available light in the euphotic zone.

Material and methods
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Water and ice samples were collected in the Chukchi and Beaufort shelves and slope
regions (Fig. 1) during the spring 2002 SBI expedition onboard the USCGC Healy

between May 10 and June 8, 2002. Stations are labeled by providing the complete date

(YYMMDD, e.g. 020510). The general sea ice conditions in this area during the
expedition and detailed information on sea ice sediment load are described in Eicken et

al. (2005).

For the purpose of this paper, we present sea ice parameters both as integrated and

weighted mean concentrations of chemical and biological properties. I calculatetd
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weighted means, i.e. integrating over the entire ice thickness and then dividing by the ice
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thickness following Gosselin et al. (1997). This approach allows a direct evaluation of the
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contribution of the release of organic material from the sea ice (assuming complete ice
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melt) on the water column properties in the study area. u
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Ice and water sampling
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Ice floes were selected as being representative for the snow and ice thickness in the given
area based on hourly ice observations cond ucted during the cruise (for details see Eicken
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et al. 2005). Snow depth was measured at 10 locations in a 5 m radius around the coring
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site. Ice cores were collected witth a 9 cm diameter ice corer with a fiberglass barrel and
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were immediately sectioned in 1 to 20 cm long segments after retrieval. Segments were
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stored in coolers in the dark for transport back to the ship’s laboratory, where they were
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processed separately.
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Brine was collected with a bilge pump from sack holes that had been drilled down to
within 5 cm of the bottom of the ice floes and was also stored in the dark in a cooler. A

Kemmerer water sampler was deployed through one core hole and water from 5 m depth

was collected for comparison with the ice physical, chemical and biological properties at
each station.

Light
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Light measurements in the PAR range (400-700 nm) were made simultaneously with a
LICOR 2pi (surface) and 4pi (underwater) PAR sensor connected to a LICOR 1800 data

recorder. Pairs of readings were taken starting at 0 m depth (4pi sensor fully submerged

in ice core hole) to a maximum of 9 m water depth. Correct depth reading was ensured by
fixing the sensor on a straight, calibrated fiberglass rod. Although the holes in the sea ice

were covered with snow prior to the light measurements, we did not use light intensities
measured within the ice floes from the surface to the ice water interface for any further
analysis as they were likely impacted by handling artifacts (extraction of ice core,

disturbance of snow cover). We included only measurements starting at 2 m watter depth
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for the purpose of the following analysis.
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Exponential attenuation Lambert-Beer type models are typically used to estimate the
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photon flux density as a function of ice thickness, snow deptuh and ice algal pigment
content. I applied such an exponential model (modified anfter Smith et al. 1988) to
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estimate the light intensity at a given water depth z in relation to the incoming photon
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flux density (Io, μΕ m-2 s-1), snow depth (zs, m), ice thickness (zi, m), water depth (zd, m)
with and without including ice algal pigme nts (zp, sum of chlorophyll a plus
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phaeopigments, mg pigments/m2) using equations (1) and (2):
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t
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(1) Iz (4pi)=A*Io (2pi)*exp(-a*zi)*exp(-b*zs)*exp(-c*zd)*exp(-d*zp) (with pigments)
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and
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(2) Iz (4pi)=A*Io c(2pi)*exp(-a*zi)*exp(-b*zs)*exp(-c*zd) (without pigments).
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The constant A (which combines the effects of albedo and the ratio between 2pi and 4pi
sensor readings) and the attenuation parameters a to c (m-1) and d (mg pigments m-2)-1

(with asymptotic standard error values) were estimated using the Gauss-Newton least

squares interpolation approach in SYSTAT (version 11). The potential impacts of melt
ponds and sediment layers were not included in this light model as we did not observe
these features at our sampling locations although sea ice sediment occurred in parts of the
study area (Eicken et al. 2005).
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Algal pigment and stable isotope ratio determination
The collected ice samples were melted directly (without addition of filtered sea

water) in the dark in a cold room (2-4 º C). Immediately after complete melt, 5 to 250 ml

sub-samples were filtered onto Whatman GF/F filters and subsequently frozen (-80 °C)
for ice algal pigment analysis (Chlorophyll a; Chl a and phaeophytin) to estimate

biomass. Another set of 5 to 250 ml sub-samples was filtered onto pre-combusted GF/F
filters, and frozen for later determination of stable isotope composition (δ13C, δ15N) and
amount of particulate organic carbon and nitrogen (POC, PON). For the determination of

algal pigments, POC, PON and stable isotope composition (δ13C, δ15N) of the wtater
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samples, 0.2 - 0.5 l each were filtered onto GF/F filters and treated like the ice samples.
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Algal pigments were extracted from filters with 7 ml of 90 % acetone for 24 hours
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(Gradinger et al. 2005). Pigment concentrations (Chlorophyll a and phaeophytin) were
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determined fluorometrically with a Turner Designs fluorometer (Arar & Collins 1992).
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Filters for stable isotope analysis were dried in a drying oven at 65 °C for 1–2 days
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and then HCl-fumed (to remove carbonates) in a vacuum chamber for 24 hours. The

filters were analyzed at the University ofd Alaska Fairbanks (UAF) Stable Isotope Facility
where they were run on ThermoFinneigan Delta mass spectrometers for their δ13C and
δ15N values and particulate organtic carbon (POC) and nitrogen (PON) masses. Sample
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isotopic ratios are expressed in the conventional notation as parts per thousand (‰)
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according to the followcing equation:
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(3) δX = [(RA /R ) – 1] • 1000
sample standard

where X is 13C or 15N of the sample and R is the corresponding ratio 13C/12C or

15N/14N. Terminology being used when presenting isotope data is: enriched=heavier

(means containing more of the heavy isotope) and depleted=lighter (means containing
less of the heavy isotope).
Nutrient analysis
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A total of 80 melted ice segments plus water samples from all stations were analyzed
for the concentration of nitrate, silicate and phosphate according to WOCE standards by

the SBI nutrient team (Codispoti et al. 2005). Sea ice samples originated from the directly

melted ice core segments and water samples from the Kemmerer bottle samples. The
water and melted ice core samples were stored in the dark at 4 ºC prior to analysis (within

12 hours). Weighted mean values for the sea ice cores and actual concentrations from 5 m
depth are presented in this paper.
Primary production measurement

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Uptake rates of isotopically labeled precursors (13C: NaH13CO3; Cambripdge Isotope
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La b. Inc.) were used to determine the ice algal and phytoplankton carbon assimilation
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under simulated in situ conditions in a refrigerated incubator (-1 ºC, cPAR=14 μΕ m-2 s-1).
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Standardized light conditions and temperature conditions were used to allow for direct
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comparison of sea ice and water column data for all stations, eliminating the variable
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temperature, light and ice conditions at each of these sites. In addition, restricted station
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time and problems with temperature control of smimulated in situ incubators (see Hill et al.
2005 for details) did not allow for in situ incubations or for deck simulated in situ

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incubations during this expedition. At each site, 500 ml of brine (collected in sack holes
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representing ice algal populations) and surface water (5 m depth) were incubated for 4 to
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6 hours with 13C tracer additiopns of 4 to 6% of the natural concentrations in duplicate
treatments. We report the eaverage of these treatments because the variability between the
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production estimates of the two samples was <15% of the average in all samples. Total
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DIC (dissolved inorganic carbon) concentrations were determined by titration with 0.01 n
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HCl during the expedition (Anderson et al. 1999). At the end of the incubations, samples
were filtered onto pre-combusted Whatman GF/F filters, rinsed with filtered sea water

and immediately frozen for mass spectrometric analysis in Fairbanks (see above).

Corrections for isotope dilution effects were not applied because of the short incubation
time (<6 h, Dugdale and Wilkerson 1986). Primary production rates were calculated
following the equations provided in Legendre and Gosselin (1996). The carbon specific
production values of the brine samples were multiplied with the sea ice bottom POC
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values to estimate the primary production of the ice algae in the bottom 10cm of the ice
floes which contained the highest POC concentrations at all stations (data not shown).

Pulse amplitude fluorescence (PAM)
For further comparison of phytoplankton and ice algal properties, the photosynthetic

yield and its relation to PAR was measured with a Waltz Water-PAM (focuses on
photosystem PS II) for the water column (5m) and sea ice (brine) samples. Samples were
measured immediately after collection within one hour after return to the ship. Prior to

m easurements samples were stored at -1º C and a light intensity of 14 μΕ m-2 s-t1. Rapid
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response light curves (RLC) were assessed using nine different actinic light intensities
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(I=0 to 1000 μΕ m-2 s-1) and saturation pulse settings of 1 sec pulse length and 15 s pulse
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interval. We used an exponential curve fit, relating photosynthetsic yield Y and photon
flux density I with: u
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(4) Y=Ymax*exp(-k/100*I).
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The relative electron transport rate (rETR) was calculated with
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(5) rETR = Y*I*0.5*0.84

according to Walz (2000). The additional factors reflect estimates of the relative fraction
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of PSII (0.5) as well as the functional chlorophyll cross section (0.84). As these factors
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are only estimated, calculated rEtTR values are considered only as relative measures.
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Based on the RLCs, the photosynthetic parameters alpha (initial slope of the ETR vs I
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curve), rETRmax c(maximum rETR value), and Ek (photosynthetic index:
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rETRmax/alpha) were calculated according to Harrison and Platt (1986) with
(6) rETR = rETRmax*(1-exp(-alpha*I/rETRmax).
I provide k in addition to the derived parameter of alpha, ETRmax and Ek of the relative

electron transport rate (rETR) vs light (I) curve (e.g. McMinn et al. 2005), as rETR is a

derived parameter based on the estimation of the photosynthetic yield Y. The nonlinear
relations (4) and (6) were estimated using the Gauss-Newton least squares interpolation
approach in SYSTAT (version 11).

Statistical tests
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Average values for sea ice and water properties were compared using the two sample t-
test providing Bonferroni adjusted p-values using SYSTAT (version 11).

Results
Ice thickness and snow depth

The measured ice thickness at the 14 occupied stations varied between 0.5 and 2.0 m with
a median value of 1.2 m (Fig. 2a). Snow depth ranged from 0.4 to 13 cm with a median
of 6.2 cm. Snow depth of less than 5 cm was only encountered on sea ice of thicknesses

>1.5 m. t
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Inorganic nutrients
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The concentrations of nutrients in the surface water beneath the ice floes showed a clear
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southwest to northeast gradient (Fig. 1c, d). High nitrate andu silicate values (>10 µM
NO , >30µM SiO ) were restricted to the four stations onn the Chukchi Sea shelf (stations
3 4
a
020510 to 020517, Fig. 1), while the deepest stations were characterized by oligotrophic
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conditions with NO < 0.2 µM and SiO <4 µM.
3 4

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The highest weighted mean silicate concentrations per core (Fig. 3a, b; range: 1.1 - 26.2
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uM) were encountered in the norttheastern study area and exceeded the water column
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concentrations. For silicate at most other locations and nitrate and phosphate in general,
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the concentrations in the sea ice floes were below surface water concentrations with
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phosphate values between 0.1 and 1.5 µM and nitrate between 0 and 1.8 µM.
c
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The ratio between the weighted mean sea ice versus water column concentrations were
below 0.5 for the four Chukchi shelf stations that exhibited high algal biomass, while

values exceeding 0.5 were observed in the northeastern part of the study area (Fig. 3c).

This implies that complete sea ice melt would dilute surface water nutrient concentrations
at stations with ratios <1, specifically on the Chukchi shelf.

Ice algal pigments