GLOBAL BIOGEOCHE•C•
CYCLES. VOL. 13, NO 4, PAGES 827-843. DECEMBER 1999
Controls on the carbon isotopiccompositionof Southern Ocean
phytoplankton
BrianN. Popp,
1TomTroll,2,•FabienKenig,• StuartG. Wakeham,
4 TerriM. Rust,1
Bronte
Tilbrook,
2,5F. BrianGriffiths,
2,5SimonW. Wright,
6 HarveyJ.Marchant,
6
RobertR. Bidigare,
1andEdwardA. Laws1
Abstract. Carbonisotopiccompositions
of suspended
organicmatterandbiomarkercompounds
weredeterminedfor 59 samplesfilteredfrom SouthernOceansurfacewatersin January1994
alongtwo north-southtransects(WOCE SR3 from Tasmaniato Antarctica,and acrossthe Princess
ElizabethTrough(PET) eastof PrydzBay, Antarctica). Along the SR3 line, bulk organicmatter
showgenerally
decreasing
13Ccontents
southward,
whicharewellcorrelated
withincreasing
dissolvedmolecularcarbondioxideconcentrations,
CO2(aq).This relationshipdoesnot holdalong
the PET transect.Using concentrations
andisotopiccompositions
of molecularcompounds,we
evaluate
therelative
rolesof several
factors
affecting
the•513C
of Southern
Oceansuspended
particulateorganicmatter. Along theWOCE SR3 transect,the concentration
of CO2(aq)playsan
importantrole. It is well describedby a supplyversusdemandmodelfor the extentof cellular
CO2 utilizationandits associated
lineardependence
of isotopicfractionation(ep) on the reciprocal
of CO2(aq). An equallyimportantfactorappearsto be changesin algalassemblages
alongthe
SR3 transect,with their contributionto isotopicfractionationalsowell describedby the supply
anddemandmodel,whenformulatedto includethe cell surface/volume
controlof supply.
Changesin microalgalgrowthratesappearto have a minor effect on ep. Along the PET transect,
algal assemblage
changesandpossiblychangesin microalgalgrowthratesappearto strongly
affectthe carbonisotopicvariationsof suspended
organicmatter. Theseresultscanbe usedto
improvethe formulationof modemcarboncyclemodelsthatincludephytoplanktoncarbon
isotopicfractionation.
the PF [Franqois et al., 1997]. The two former explanations
represent"biological" processes,while the latter is principally a
The physical circulation of the Southern Ocean contributes physical phenomenon. Carbon isotopic records of Southern
dramaticallyto global climate controlby directly linking surface Ocean sedimentary organic matter show clear and dramatic
waters with the deep sea in the three major oceanbasinsand by
changesfrom the time of the last glacial maximum to the present
redistributingwaters amongthem via the Antarctic Circumpolar and may contain important information about changesin both
Current. Biological activity in the SouthernOcean may also be biological carbon fixation and oceanic circulation during this
importantto global climate. Enhancedprimary productionrates interval [Fischer et al., 1997] because phytoplankton carbon
in the Southern Ocean have been suggestedas a means of
isotopiccompositions
appearto reflecta balanceof environmental
explaininglow-atmosphericCO2 concentrationsduring the last CO2 supply and biological demand [e.g., Rau et al., 1992;
glacial period [e.g., Knox and McElroy, 1984; Sarrniento and Franqoiset al., 1993; Goerickeet al., 1994]. Before quantitative
Toggweiler, 1984].
Several causal scenarios have been
constraintscan be placedon biologicaland physicalfactorsfrom
hypothesizedand include (1) iron-stimulatedincreasesin export the •513Cof sedimentaryorganicmaterials,fundamental
production in the Subantarcticand Polar Frontal Zones of the
information on the mechanisms controlling the isotopic
Southern Ocean [Martin, 1990], (2) iron-stimulated increasesin
compositionsof phytoplanktonand bulk suspended,sinking,and
exportproductionnorth of the AntarcticPolar Front (PF) [Kumar sedimentedparticulateorganic matter in the SouthernOcean is
et al., 1993], and (3) increasedsurfacewater stratificationsouthof
needed.
1. Introduction
Stable isotopic characterization of marine organic matter
providesimportantinsightsinto the environmentalconditions
2Antarctic
CRC,University
of Tasmania,
Hobart,Tasmania,
Australia. under which carbon fixation occurs. Early on, Sackett et al.
[1965; 1974] found that SouthernOceanplankton and sediments
rNowat Depamnent
of Geological
Sciences,
Universityof Illinoisat
•Schoolof OceanandEarthScienceandTechnology,
Universityof
Hawaii, Honolulu.
havesignificantly
lower13C/12C
ratiosrelativeto thoseat lower
Chicago.
nSkidaway
Institute
of Oceanography,
Savannah,
Georgia.
latitudes. Subsequentstudies of the isotopic composition of
5Alsoat CSIRO, Divisionof Marine Research,Hobart,Tasmania,
marine particulateorganicmatter at high latitudes[Wada et al.,
Australia.
1987; Rauet al., 1989, 1991a, b; Bathmann et al., 1991; Fischer,
6Australian
AntarcticDivision,Kingston,
Tasmania,
Australia.
1991; Dunbar and Leventer, 1992; Rogers and Dunbar, 1993;
Franqois et al., 1993; Goericke and Fry, 1994; Kennedy and
Robertson,1995; Kopczynskaet al., 1995; Dehairs et al., 1997;
Fischer et al., 1997] have confirmedthe extremeisotopicnature
of SouthernOcean organic matter, which some have related to
Copyright1999 by theAmericanGeophysical
Union.
Papernumber1999GB900041
0886-6236/99/1999GB900041
$12.00
827
828
POPP
ETAL.:•13COFSOUTHERN
OCEANPHYTOPLANKTON
SouthernOcean Sections,January1994
communitystructure.We speculateon the implicationsof these
-30
' ' • ß' Au.'s•
'..•
-35
-40
......................................
•...................................
....
2. Materials
........
.
........
,
-55 ...............
Samplesusedfor this studywere collectedfrom the locations
shownin Figure 1 on a cruiseof the R/V Aurora Australis from
Januaryto March 1994, along the WOCE SR3 line (Hobart to
Antarctica) and along a section acrossthe PrincessElizabeth
'
........
.WOCE'
SR3ß
:.....................
-60.... ...... .'•' PriOcess-...... . .... : .... ..........
.....
-65 ß
'....
ß
: •. Eliz.
abeth
'
' -3/•
Trøugh '
60
'
70
[
80
'
: - ß-'..........
Trough(PET), fromtheWestIce Shelfto the KerguelenPlateau.
Samplesof suspended
particulateorganicmatter (SPOM) were
collectedevery-30 nauticalmiles,while the shipwas stopped,
along the transectsfrom the ship's uncontaminatedseawater
;Antarctica
Prydz
Bay
-75
and Methods
'
...
-50ß- ß• Kergueien.
..
sedimentary
organicmaterials.
'. ß
Tasm•/nia
-45
results
for interpreting
the513Cof suspended
particulate
and
....
90
100
110
120
130
140
150
160
Longitude
Figure 1. Map of samplecollectionsites,alongthe World Ocean
Circulation Experiment (WOCE) SR3 (Hobart to Antarctica,
cruisetrack from 45ø55'S, 140øEto 65ø24'S,140øE)and acrossthe
PrincessElizabethTrough (PET), from the West Ice Shelf to the
systemonto precombustedglassfiber filters (143 mm diameters
GelmanA/E) using an in-line filter apparatus. Along the SR3
line, 42 SPOM sampleswere collectedat stationsbetween45øand
65øS; acrossthe PET, 17 sampleswere collectedat stations
between58øand67øS(Table 1). All SPOM samples
werefiltered
from 160-200 L of water, immediatelyfrozen and storedfrozen
until analysis.
Physical oceanographic measurements,carbon analyses
KerguelenPlateau(58ø55'S,82ø01'Eto 65ø19'S,84ø43'E). The ([DIC], fCO:z, alkalinity), biological studies (fluorescence
cruise was carried out in January 1994 onboard Australia's profiles,nutrientanalyses,planktoncounts,andpigmentanalyses)
icebreakerR/V Aurora Australis. Sampleswere collectedwhile
were also performed. Surface waterfCO:z was continuously
stoppedfor CTD work by filtering the ship's clean seawater monitoredfrom the ship'suncontaminated
seawatersystemand
supply.
[CO2(aq)]calculatedfromfCO2, temperature,and salinity,after
Weiss[ 1974]. ThefCO 2 measurements
weremadeby circulating
air, which had equilibrated with a shower of water from the
low seasurfacetemperatureandthe consequent
high saturationof
uncontaminatedseawaterline, through a infrared gas analyzer
CO2(aq). It hasbeen assumedthat availability of CO2(aq) is a (LICOR Model 6252) [Metzlet al., 1999]. The air wasdriedprior
major factor controllingcarbonisotopiccompositions
of to analysis,and standardsreferencedto the World Meteorological
phytoplankton[e.g.,Arthur et al., 1985;Hayeset al., 1989;Rau et Organization (WMO) X85 mole fraction scale were used to
al., 1989; Popp et al., 1989; Jasper and Hayes, 1990; Hollander calibratethe analyzer.ThefCO2 datawerecorrectedfor warming
and MacKenzie, 1991]. This has led to the use of stable carbon betweenthe seawaterinlet in the ship'sbow (water depth-5 m)
isotope measurementsfor reconstructingpaleo-pCO2 records andthe equilibrationchamberafter Copin-Montegut[1988, 1989].
[e.g., Jasper et al., 1994]. However, additional factors such as The concentrationsof total dissolved inorganic carbon were
temperature, light intensity, nutrient availability, species determined coulometrically using a Single-Operator Multicomposition,growth rate, and active dissolvedinorganiccarbon Metabolic Analyzer (SOMMA) systemsimilar to that described
(DIC) transporthave also been suggestedto be important in by Johnsonet al. [1993]. Phosphate,silicate, and nitrate plus
determining
the513Cof phytoplankton
[e.g.,Rauet al., 1992; nitrite were measured using the colormetric techniques of
Franf'ois et al, 1993; Goericke et al., 1993; Laws et al., 1995; $trickland and Parsons [1972] on a Alpkem "Flow Solution"
Bidigare et al., 1997a;Laws et al., 1997; Poppet al., 1998].
Autoanalyzercontinuousflow system.Unfortunately,for reasons
In this paper we examine variations in carbon isotopic specificto the autoanalyzersamplesequenceprotocol[Rosenberg
compositionof SouthernOcean suspendedparticulate organic et al., 1995], reliable surface bottle phosphateconcentration
matter,andindividualcompounds,someof which are exclusively determinationswere rare on this voyage, whereas silicate and
derived from phytoplankton(e.g., phytol, steroIs),from surface nitrate plus nitrite were successfullydetermined in nearly all
watersamplescollectedin the SouthernOceansouthof Australia. surfacewater samples.For this reason,in consideringphosphate
We infer the fractionationbehaviorof differentphytoplanktonas utilization, we primarily rely on estimatesfrom surfacebottle
reflectedin the isotopiccomposition
of individualcompounds
and nitrate+nitrite concentrationsassumingRedfield stoichiometry
examinehow it affectsthe carbonisotopiccompositionof bulk (N/P=16 (by atoms),Table 1), an approximationwhich involved
suspendedparticulateorganic matter. We documentisotopic little uncertaintywhen comparedto phosphatedeterminationson
variability in individual compoundsof up to 10%oin a single samplescollecteddeeperin the mixed layer (50-75 m). Salinity
sample and its influence on bulk suspendedorganic matter was determinedusing a YeoKal Mark 4 salinometerstandardized
isotopiccompositions.We discussthe factorswhichcontributeto with IAPSO P-series salinity standards following WOCE
this isotopicvariability,amongthem CO2(aq) concentrations,
the guidelines. Microscopic algal identificationsand countswere
isotopic compositionof CO2, microalgal growth rates, algal done onboard. Chlorophyll a analyseswere done on shoreby
communitystructure,and detailsof the physicaloceanographic high-pressureliquid chromatographyusing particles from 2 L
environment. Our generalhypothesisis that fractionationvaries seawatersamplesfiltered throughglass fiber filters (Whatman
as a function of CO2(aq)concentration,algal growth rates, and GF/F) storedin liquid nitrogen[Wrightand Jeffrey, 1997].
POPPET AL.: fil3c OF SOUTHERNOCEANPHYTOPLANKTON
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POPPET AL.' (•13C
OFSOUTHERN
OCEANPHYTOPLANKTON
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POPPET AL.: fil3c OF SOUTHERN OCEAN PHYTOPLANKTON
831
concentrations
were obtainedby additionof known quantitiesof
Microalgal growth rates were estimatedin two ways from
(1) the temperature,light, and nutrientdependentmodel of Six
an internal standard (5ot(H)-cholestane) to the total neutral
and Maier-Reimer[1996] and (2) shipboard
inc uptake fraction prior to analysis by gas chromatography(GC) and
experiments [Mackey et al., 1995]. The first assumesthe
temperature-growth
relationshipof Eppley [1972], MichaelisMenten nutrient dependence (half-saturation at 0.016 BM
phosphate),and representsphotosyntheticallyactive radiation
(PAR) as the averageover the mixed layer of the exponentially
attenuatedsurface irradiance. Community microalgal growth
rateswere calculatedby combiningmixed layer depth estimates
from shipboardconductivity-temperature-depth
(CTD) temperatureand salinityprofiles,with surfaceirradianceestimatesfor
January 1991 from the model of Bishop and Rossow[1991],
availableat http://www.giss.nasa.gov/data/seawifs/data
(data for
1994 is not yet availableand the 1991 datawere typicalof the 8
yearsprocessed
to date). Mixed layer columngrowthrateswere
computerizedgas chromatography-mass
spectrometry
(GC/MS).
Compound-specificisotopic results reported here were from
duplicate or triplicate analysesby isotope-ratio-monitoring
GC/MS (irmGCMS, Ultra 1, 50 m) performedat the Universityof
Hawaii usingtechniquesdescribedby Hayeset al. [ 1990],Merritt
and Hayes [1994], and Merritt et al. [1995]. Isotopic analyses
reportedin standard
•5-notation
in Table2 havebeencorrected
for
the additionof carbonduringderivatization. Use of compoundspecific isotopic analyses for environmental interpretations
requires knowledge of the relationshipbetween the isotopic
compositionof the compound(s)analyzedand that of the whole
organism[seeHayes, 1993;Summons
et al., 1994].
13
= (• C
- 1)1000
œbiomarker
organism
+1000
estimated
alsofromshipboard
short-term
(1 hour)14Cproduction
• 13
Cbiomarker
+1000
versusirradiance(the so-called,P versusE experiment)carded
out on samplesfrom severaldepths,combinedwith chlorophyllcalibratedfluorescenceprofiles [see Mackey et al., 1995], and, Followingresultsof recentlaboratoryexperiments[Bidigare et
= 7%0 and
like the Six and Maier-Reimer model, with mixed layer depths al., 1997b; Schoutenet al., 1998], we adopt œsterol
estimated
fromCTDprofiles
andirradiances
fromthemodel
of œphytol
= 4%0.Wecalculate
isotopic
fractionation
(œp
[Freeman
Bishop
andRossow
[1991].Tenpercent
respiration
lossanda andHayes,
1992])using
standard
formulation.
Calculations
of•p
carbon/chlorophyll
a ratio
of50(weight/weight)
were
assumed
in based
onsterols
andphytol
include
acorrection
forthedifference
order
tocalculate
netproduction
and
thus
growth
rates.
between
theisotopic
composition
ofthecompound
andthatofthe
No measurements
of theisotopic
composition
of total whole
cellwhich
occurs
during
biosynthesis
ofthecompound,
dissolved
CO2([13C-DIC)
areavailable;
therefore
[13C-DIC
was i.e.,
calculated
using
the
model
ofBroecker
and
Maier-Reimer
[1992].
Thismodelassumes
that•SI3C-DIC
canbe estimated
from
dissolved
phosphate
concentrations
anda constant
difference
œP=( 13
•13Cc02
d-1000
-1)1000
•5Cbiomarke
r+œbiomarker
d-1000
betweenthe isotopiccompositionsof DIC and phytoplankton
(assumed
hereto be20%0).Modeled
variations
in •S13C-DIC
3. ResultsandDiscussion
(Table 1) agreewell with historicalobservations
for the Southern 3.1. OceanographicSetting
Ocean[seeLynch-Stieglitzet al., 1995' Francois et al., 1993].
Theisotopic
composition
ofCO2(aq)
wasdetermined
from•513C
-
Thesamples
cover
thecomplete
range
ofopenSouthern
Ocean
DIC andtherelativeabundances
of carbonate
species.Thelatter environments
(Figures2 and3). The Southern
Oceancanbe
wasdetermined
fromconcentrations
of DIC, phosphate,
silicate, dividedintoseveralbroadregionsseparated
by majoroceanic
andfCO2 following
Millero[1995].Thedissociation
constantsfronts[Rintoul
et al., 1997].Fromthenorthto thesouth,
these
for carbonicand boric acidsusedin this calculationwere from includethe Subantarctic
Zone (SAZ) from --40ø-50øS
boundedto
Dickson[1990a,b] andRoyet al. [1993]andcorrected
for the thenorthbytheSubtropical
Convergence
(STC)andto thesouth
effectsof pressure
usingMillero[1979]. Thepotential
error bytheSubantarctic
Front(SAF). TheSAFmarksthenorthern
involved
inusing
modeled
fiI3C-DIC
values
isdifficult
toassess;
edgeof theeastward
flowingAntarctic
Circumpolar
Current
although,
it islikelytobesmall
relative
tovariation
intheisotopic(ACC),usually
centered
around
50ø-51øS
between
140øand152øE
composition
oforganic
materials.
A subsample
ofeachfilterwas andis characterized
by rapidtemperature
andsalinity
changes
prepared
forbulk•513C
analyses
using
methods
ofWedeking
etal. (--8ø-5øC
and-34.5tolessthan34.2,respectively)
overabout
30[1983]afteracidfuming
(HC150%vol/vol
for12hours).
50nautical
miles.Summer
warming
canoftenmask
thechange
in
Filterscontaining
SPOMwereprocessed
for compoundtemperature
across
theSAFin surface
waters.ThePolarFrontal
identification
andcompound-specific
isotopic
analysis
at the Zone(PFZ)extends
south
fromtheSAFtothePF,a subsurface
Skidaway
Institute
of Oceanography
using
procedures
described
feature
marked
by thenorthern-most
extentof coldsubsurface
by Wakeham
andCanuel[1988].Approximately
halfof the waters
(<2øC
atabout
200m),typically
found
atabout
54øS
south
samples
collected
alongtheWOCESR3section
andall of the ofAustralia.
ThePolarZone(PZ)extends
onsouthward
tothe
PETsamples
wereprocessed.
Briefly,thefilterswereSoxhletAntarctic
Divergence,
which
marks
thetransition
fromprevailing
extracted
withmethylene
chloride:methanol
(2:1,vol/vol),and westerlies
tocoastal
Antarctic
easterlies,
aswellasthelocation
of
extractable
lipidswerepartitioned
intomethylene
chloride
after upwelling
of circumpolar
deepwater.South
of theAntarctic
addition
of the5%NaC1solution.
Neutralandacidiclipidswere Divergence,
theinfluence
of sea-ice
is large,andwereferto this
separated
by saponification
usingaqueous
0.5 N potassium
region
astheSeasonal
Sea-Ice
Zone(SSIZ).South
ofAustralia,
hydroxide
in methanol
followed
byserial
extraction
frombasic thePZcanbefurther
divided
intonorth
andsouth
zones
bythe
solution
(pH> 13)andacidic
solution
(pH< 2). Thetotalneutral presence
of a southern
branch
of thePolarFront(PF-S).The
fractionwasderivatized
to trimethylsilyl-ethers
with N,O- southern
branchis lessclearlydefinedthanthenorthern
but
bis(Trimethylsilyl)trifiuoroacetamide
andanalyzed
directly
bygas generally
occurs
between
57øand60øS.Indicators
ofthesouthern
chromatography.
Distributions
ofindividual
compounds
andtheir PFinclude
theregion
where
there
isarapidchange
indepth
ofthe
832
POPPET AL.' (•13COF SOUTHERNOCEANPHYTOPLANKTON
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POPP ET AL.- •513COF SOUTHERN OCEAN PHYTOPLANKTON
Tasmania
83 3
WOCESR3 Section, Jan.94
Antarctica
E25 10/J Subantarctic
I':/ I]IIFronal/i/f•
Polar
/' 4•'•'•-'•••••.
.0• :,J•
Zone I:/
',..!- '"
i /") ,,.---.---"-,,./•
Zone
2 :
1
/• •. 9
• :/t)/"",,
•//
75 [ ' /) •
PolarZon•
2///•: //fPol:rZone
•
::•JSeasonal
/•11/ i t] f I
north /
i / south
6
_/.•Sea-Ice
F:
•
50
75
100
lOO
46
48
50
52
54
56
58
60
62
64
Latitude, øS
Figure2. Distributions
of temperature,
salinity,
andchlorophyll
a alongtheSR3transect
in thetop 100m.
Locations
of oceanographic
zones
andthemajorfronts
thatdividethemareshown,
following
Rintoul
etal. [1997]
andasdescribed
in thetext. Temperature
isquiteuniformwithintheSubantarctic
Zone(SAZ)anddecreases
across
theSubantarctic
Front(SAF),although
seasonal
surface
warming
broadens
thethermal
expression
of theSAFin
comparison
to its north-south
salinitychange.The2ø isotherm
marksthetopof thesubsurface
temperature
minimum
layer,aswellasdefining
theposition
ofthePolarFrontbytheposition
ofitsnorthward
extent.Salinity
generally
decreases
fromnorthto south.ThePolarZone(PZ)wasextremely
homogeneous
in salinity;
fresher
waters
formed
frommelting
sea-ice
inputs
occurred
neartheserface
in theSeasonal
SeaIceZone(SSIZ).Upward
intrusion
of warmsaltyCircumpolar
DeepWateroccurred
at theAntarctic
Divergence
(AD) (shading
indicates
salinities
> 34.4).Therelatively
lowsalinity
water(< 34.4)in themiddleoftheotherwise
saltySAZwastheresult
of a largeeddywhichalsobrought
cooler
waterintotheregion.TheSAZ,SSIZ,andnorthPZ all contained
relatively
abundant
chlorophyll
a (shading
indicates
> 0.6ug/L),withthePZalgae
concentrated
subsurface
nearthe
topof thecolder
waters.ThePolarFrontal
Zoneandwaters
neartheAntarctic
Divergence
contained
verylittle
chlorophylla.
temperature
minimumlayer,or wherethereis a steepgradient
in
salinityin the 150-300m depthrangebetweenwaterwith a
salinityof 34.0-34.2to 34.6, whichis characteristic
of upper
layer (Figure3). The differentSouthernOceanenvironments
exhibitbothoverlapanddifferences
in typicalalgalcommunities.
For example,northof the SAF, coccolithophores
are relatively
CircumpolarDeep Water.
All of the zones defined above can be characterizedas high-
commonbut aremuchlesssosouthof the SAF andparticularlyin
the diatom-dominated Polar and Seasonal Sea-Ice Zones. These
by changesin nutrient
nutrient, low-chlorophyll (HNLC) oceanic environments, biologicalvariationsare accompanied
element
abundances.
Of
particular
note
is that while nutrient
although
therearesignificant
differences
amongthemin termsof
biological,physical, and chemicalattributes. Levels of levels generallyincreasesouthward,nitrate levels increase
chlorophyll
a generally
decrease
southward
across
theSAZto the stronglyacrossthe SAF, but silicatelevelsremainlow much
branchof thePF is reached(Table
AntarcticDivergenceand then increaseagain southof the farthersouth,untilthesouthern
1).
Zonal
homogeneity
is
of
course
onlya first approximation
to
Divergence(Figure2). Algal distributions
within the water
Southern Ocean environments,and there are also significant
columnalsovary. Notethe subsurface
chlorophyll
maximumin
thenorthPolarZonealongthe SR3 section(Figure2) andin the differences between the SR3 and PET sections. These include
compositions,
deep
offshore
portionof thePET section
at thetopof thewinterwater differencesin watermasstemperature-salinity
834
POPP
ETAL.:•13COFSOUTHERN
OCEANPHYTOPLANKTON
Princess Elizabeth Trough, Jan.94
100 -,
' '
.....
E50
IO0
59
60
61
62
63
64
65
66
Latitude, øS
Figure 3. Distributionsof temperature,
salinity,andchlorophylla alongthe PET transectin the top 100 m. Surface
waters varied from nearly 2øC in the north to the freezing point in the SSIZ. Remnantsubzerowinter water
(shaded)underliesthe entire sectionat -50 m depth,effectivelyisolatingsurfacewaters. In the SSIZ, melting seaice observedduringthe cruiseproducedsalinitiesbelow 33.6 (shaded).As in the SR3 section,relativelywarm salty
water intrudesupward into the mixed layer at the Antarctic Divergence(dotted line). Chlorophylla levels were
elevated(shadingindicates>2.5 ug/L) in boththe northerlyshallowrelativelywarm surfacewatersand nearthe ice
edge,with muchlower levelsat the AD. North of the AD, the algaewere concentratedsubsurface
at the top of the
remnant winter water.
as well as surface water nutrient concentrations, local circulation
Southern Ocean phytoplankton[e.g., Rau et al., 1991a, b;
patternsincluding sea-icedrift, and mixed layer depths. Full
details of these variations are beyond the scopeof this paper;
thosepertinentto carbonisotopicvariationsare discussed
further
Bathmann et al., 1991; Fischer, 1991; Dunbar and Leventer,
in section 3.2. Recent discussionsinclude Rintoul et aL [1997],
1992; Rogers and Dunbar, 1993; Francois et al., 1993;
Kopczynskaet al., 1995; Dehairs et al., 1997; Fischer et al.,
1997]. Althoughcollectedwithin 20 days of each other on the
Wonget al. [1998], andWorbyet al. [1998].
Concentrations
of CO2(aq)in surfacewatersalongthe SR3 line
differentlyin thetwo sections
(Figure4). Alongthe SR3 transect,
varyfrom13.1to 23.5gmolkg-1,arenearequilibrium
withthe
atmosphere,and vary mainly as a function of temperature
(Figure4) except near the retreatingice edge where enhanced
phytoplankton
production
likely causeda drawdownof CO2(aq),
consistentwith lower phosphateconcentration.The [CO2(aq)]
samevoyage,813C-SPOMwasrelatedto [CO2(aq)]quite
8•3C-SPOMis negatively
correlated
withCO2(aq)concentrations
(•13C=-0.89[CO2(aq)]- 9.29, r2 = 0.91, Figure4). Similar
correlationsbetween the isotopic compositionof SPOM and
[CO2(aq)
] havebeenfoundby Rauet al. [199lb], Francoiset al.
[1993], and Dehairs et al. [1997] from the SouthernOcean. In
despite
similarranges
of CO2(aq)and813Cvalues,
a
alongthePETtransect
varyfrom14.6to22.0gmolkg-1andare contrast,
generallybelow that expectedfor equilibriumwith atmospheric
CO2 (Figure4). Unlikethemajorityof SR3results,[CO2(aq)]is
poorly correlated with sea surface temperaturesuggesting
biologicalactivitystronglyinfluenced[CO2(aq)]alongthe PET
transect.Severalauthorshavesuggested
thatthe concentration
of
CO2(aq) mainly controlsthe carbonisotopic compositionof
poor correlation between SPOM isotopic compositionand
CO2(aq)
concentration
wasfoundalongthePETline(•13C=
-0.71[CO2(aq)]
- 13.40,r2 = 0.52, Figure4). Becausethe
relationship
between
[CO2(aq)]
and8•3C-SPOM
is sodifferent
in
each of these oceanicregions,we discussthe SR3 and PET
transectsseparatelybeforecomparingthem.
POPP ET AL.: •13C OF SOUTHERN OCEAN PHYTOPLANKTON
SAF
PF
PFS
835
AD
12.5
a
15.o
-17.5
- 20.0
- 22.5
-32!
'
25.0
-2O
-25 Q.
• -30o
ø"'ø'
-35-
,
.•....,0•
'o----•......-oh,
-•, •!
j3 -..-ø •'.-'
•"".... i-....
iI ",
! ..-•1•:':'"':'•1....
'• ...............
','¾•"
'"...•,
d.i........
o .....
-o' '', ,-••-'
!
i
(,o -40-
i
-45
5'0
45
'
i
',..i ,'
,'
"•;:"•---o'
,
....o .........•.,.;.......
!.....................
o
:
'o"• ....
i
6'0
5'5
6'5
Latitude, øS
03 -20
12.5
c
Q. -22--
SPOM
=
phytol
.... • ....
sterol I
jCO2(aq),1•
• -24-
17.5
0 -26 -
- 20.0
(_3 -28-
- 22.5
j & CSPOM
-30
.... [] ....
15.o
sterol II
-2O
Equi•bdum
CO
2 .....
i
i
60
65
di;
!
25.0
.
........
o ........ sterol III
03 -25
---o---
sterol IV
-- n- -
sterol V
Q.
• -30
- -3,5
(,0 -40-
-45
O"
ø'"'ø'"nl o.<:•.o
i
=
'-•O.o.O.'o
i
60
6'5
Latitude, øS
Figure
4. Distributions
ofsurface
aqueous
CO2,
•513C-SPOM,
andtheisotopic
compositions
ofphytol
and
thefive
major
steroIs.
Front
locations
arethesame
asinFigure
2. CO2levels
were
generally
close
toatmospheric
equilibrium
values
(dashed
line)along
SR3butdeviated
from
equilibrium
inthefarsouth
and
north
of$R3andin
all of thePET. Individual
sterol
isotopic
compositions,
whilegenerally
decreasing
southward,
exhibit
greater
variations
thanthose
ofbulk$POMorphytol.
Sterol
I, cholesta-5,22E-dien-315-ol;
sterol
II, cholest-5-en-315-ol;
sterol
III, 24-methylcholesta-5,22E-dien-315-ol;
sterol
IV, 24-methylcholesta-5,24(28)-dien-315-ol;
sterol
V, 24ethyl-5ot-cholest-7-en-315-ol.
3.2. WOCE
SR3 Transect
Rau et al., 1996, 1997]andlaboratoryexperiments
[Lawset al.,
1995;1997;Bidigareetal., 1997a;?oppetal., 1998]suggest
that
Although
the [CO2(aq)]canexplaina largeamountof the
microalgal
growth
rateandcellsizeandshape
alsocontribute
to
variationin ;513C
of SPOMalongtheSR3transect,
variabilityin
thecarbonisotopic
composition
of individual
compounds
along
thesetransects
(Figure4) indicatethatotherfactorsaffectthe
•S13C-SPOM.
Recentresultsof modeling[Goerickeet al., 1994;
thecarbonisotopic
composition
of phytoplankton,
essentially
asa
balanceof CO2 supplyand demand. Contributionsfrom
heterotrophic
carbonsources
canalsoplaya role [Fry, 1988;
Hayes,1993;KenigetaL,1994].We nowexamine
thesefactors
836
1.0
POPP
ETAL.:•13COFSOUTHERN
OCEAN
PHYTOPLANKTON
lO
Oceandiatomsby variousinvestigatorsduringthe australsummer
Production-Irradiance
•'"'.........
... Six
and
Maier-Reimer
Model
(Table3),aswellastheshipboard
14Cresults
discussed
next.
-
8
In contrastto the Six and Maier-Reimer [ 1996] model, mixed
0.8-
layer columngrowthratesestimatedfrom shipboard14C
measurements
arelower,averaging
0.48+ 0.17d-l, andexhibitno
systematicchange with latitude (Figure 5). Both variations in
,
photosynthetic
response
(asestimated
fromthe14CP versusE
experiments)and changesin the vertical distributionsof the algae
in the water column(determinedfrom the fluorescenceprofiles)
contributeto the variationsin column growth rates. For example,
0.2-
2
maximum
14Cuptake
ratesat saturating
irradiances
(Pmax
values
"Prnax
at 10 m) were quite constantfrom 45ø to 60øS, and the lower
columngrowthratesfrom 49ø to 52øSare primarily the resultof
the deepermixed layersand algal distributionsat the SAF and in
Latitude, øS
the PFZ. In contrast,southof the Antarctic Divergence(-64øS),
the small diatomdominatedalgal communityexhibitedrelatively
Figure 5. Comparison along the SR3 section of community
phytoplankton
mixedlayergrowthratesfromshipboard
InC-based low Pmaxvalues,but their near surfacelocationleadsto column
productionversusirradianceexperimentswith those predicted growthratesthat are similarto the restof the transect.
from temperature,light, and major nutrientdistributionsusingthe
These observationshighlight some of the issuesinvolved in
o.o
io
io
model of Six and Maier-Reimer
[1996].
o
Also shown are
productionratesat saturatingirradiance(Pmax
values)from the 10
m depthshipboardsamples.
estimating
growth
ratesappropriate
to assessing
13Cfractionation
from 14CP versus
E experiments.
Usingmixedlayercolumn
growthratesassumesthat the observedvertical algal distributions,
P versusE parameters,and climatologicalirradiancesare typical
of the periodoverwhichthe 13C compositions
have been
from measurements
of algal growth rates, community structure,
andbiomarkercompoundabundances
andisotopiccompositions.
3.2.1.
Growth
rates.
The model
of Six and Maier-Reimer
determined. It also assumesthat the surface SPOM samples
obtainedfrom 10 m depthhave experiencedthe columnweighted
meangrowthrate, i.e. that the surfacelayer has indeedbeen well
[1996]predicts
growthratesrangingfrom0.5 to 0.9 d-1,which
mixed
decreaseto the southand are controlledmainly by temperature
(Figure 5). Mixed layer depth variations(of typically 40-125 m)
play a secondaryrole, followed by cloud cover driven irradiance
variations. High surfacewater phosphateconcentrations
(Table 1)
precludephosphategrowth limitation in the model despite the
relatively high half-saturationconstant. The model growth rates
are generally higher than growth rates estimatedfor Southern
provide two ways to evaluate these assumptions. First of all,
dividing column chlorophyll inventories by production rates
suggestsresidencetimes (i.e. the biomassreplacemente folding
time) of 1-3 days, so that more than 95% of biomasswill have
accumulatedin the past 3-9 days. This suggeststhat storm
timescaleeventswhich deepenmixed layers and changecloud
levels couldbe important. Comparisonof clear sky i•adiances
over the residence
time
of the cells.
The observations
Table 3. Growthratesof AntarcticDiatomsEstimatedby VariousInvestigators
DuringtheAustralSummer
Reference
Sakahaugand HolmHansen [1986]
GrowthRates,d-1
mean = 0.24
range= 0.1-0.34
Spies[ 1987]
mean= 0.52
range= 0.26-0.92
Tilzer and Dubinsky
[ 1987]
mean = 0.14
range= 0.04-0.19
Comments
Growthratesbasedon chlorophyllmeasurements
in batch
cultures.Scotia/Weddell
Seas.Temperature
= -1 to 4øC.
Culturesdominatedby diatoms--Chaetoceros
tortissimusGran,Nitzschia,Fragilariopsisspp.and
Thalassiosirasp.
Growth ratesdeterminedby successive
cell countson
naturalpopulationsincubatedin polycarbonate
bottles.
WeddellSea. Temperature
=-IøC Thalassiosira,
Eucampia,Chaetoceros,
Rhizosoleina,
Nitzschia,
Thalassiothrix, Coscinodiscus and others.
Wilson et al. [1986]
surface rates = 0.26-0.36
integratedrates= 0.10-0.15.
Growth rates based on C-14 incubations and assumed C:chl
ratio of 50. SouthernDrake Passage.Temperature= -2
to +8øC. Net planktondominatedby diatomsCorethron
criophilum,Chaetoceros
spp.,Thalassiosira
sp.and
Rhizosoleniaalata. 76% of chlorophyllin cellswhich
passthrougha 20 gm filter.
Growthratesdeterminedfrom autoradiography
andcarbon
estimatesbasedon cell volume. Recedingice edgein
WesternRossSea. Mainly Nitzschiacurta with some
Nitzschia closterium.
POPPET AL.:•13COFSOUTHERN
OCEANPHYTOPLANKTON
SAF
PF
PFS
Diatoms> 20 •m
carbon/chlorophyllratios changedsystematicallywith latitude,
althoughwe haveneitherany reasonto expectthis nor any datato
rule it out. We useda shipboardestimateof carbon/chlorophyll
which is slightly lower than the average from the literature
[Sakshaugand Hobn-Hansen,1986; Figueiras et al., 1994; Smith
et al., 1996; DiTullio and Smith, 1996], but the uncertainty is
[]
Diatoms< 20 •
ratherlarge(> 30%). Because
the ]4C basedgrowthrates
[]
Coccolithophores
•
Flagellates
AD
75-
I
25
50
55
60
837
65
Latitude, 'S
correspondto estimatesof SouthernOcean diatoms (Table 3)
better than thosepredictedfrom the Eppley [1972] temperature
dependenceof the Six and Maier-Reimer [1996] model, the
simplestconclusionremainsthat growth rates were reasonably
independent
of latitude,temperature,and CO2(aq)concentrations
alongthe SR-3 transectin January1994 (althoughthis may not be
true in other seasons).This interpretationimplies that variations
in microalgal growth rates contributed only variance to the
observed
correlation
of •5•3C-SPOM
with CO2(aq),ratherthan
influencing its average nature. In fact, latitude by latitude
comparison
of the sparse•4C-basedgrowthrateswith the
variability
of the•5•3C-SPOM
correlation
withCO2(aq)
reveals
no
60-
o
40
ß
sterol I
[]
sterol II
[]
sterolIII
•'• sterotIV
[71 sterolv
2O
consistenteffect of growth rate at all; for example, regions in
whichthe•4Cdatasuggest
relativelylowgrowthrates(e.g.near
50øand62øS)do notexhibitrelativelylow •5]3C-SPOM
values
given their CO2(aq) concentrations.Furthermore,lower than
maximumgrowthratesare consistent
with recentdatasuggesting
that micronutrients,in particular bioavailable iron, may exert
strongcontrolson SouthernOceanphytoplanktongrowth rates
[Martin et al., 1990; Banse, 1996; $edwick and DiTullio, 1997].
50
55
60
65
Latitude, øS
Figure 6. Distributionof cell countsand biomarkercompound
abundances
along the SR3 section. The legendsfor cell counts
and sterolabundances
list the componentsin order from mostto
least abundant.While individual speciesabundanceswere not
quantified, Nitshia,
Coretheron, Chaetocerosis, and
Fragillariopsiswere important constituents. Individual sterol
abundances
generallyvary little with latitude comparedto the
large variation in their isotopiccomposition(see Figure 4).
It appearsthat factorsother than algal growth rates are more
important in controlling the carbon isotopic compositionof
SPOM.
3.2.2. Community Structure. Effects of communitystructure
on •513C-SPOM
wereevaluated
by comparing
distributions
of
flora (microscopiccell counts)with the concentrationand isotopic
composition
of algalbiomarkers.
Importantly,
•5•3C-phytol
and
•SI3c-SPOM
values
arewellcorrelated
([13Cphyto
I = 1.15*
•j13CsPoM
- 0.86,ta = 0.91)witha meandifference
of 4.7_+1.2%o
(Tables 1 and 2), a result expected since all oxygenic
photoautotrophs
producechlorophylla, the majorsourceof phytol
SterolI, cholesta-S,22E-dien-3[•-ol;
sterolII, cholest-S-en-3•-ol; and SPOM. The mean difference is slightly higher than that
sterol III, 24-methylcholesta-S,22E-dien-3•-ol;sterol IV,
obtained from phytoplankton cultures (-4%o [Hayes, 1993;
24-methylcholesta-S,24(28)-dien-3[•-ol;
sterol V, 24-ethyl-Sct- Bidigare et aL, 1997b; Shoutenet al., 1998]), but is consistent
cholest-7-en-3[•-ol.
withminimal
heterotrophic
contributions
to $13C-SPOM
[seeFry
with cloud-covered
valuessuggestsirradiancechangeswould not
exceeda factorof 2 [Bishopand Rossow,1991]. For typicallight
attenuationlengthsof-40 m, storm-drivendeepeningof an
initially very shallow mixed layer from 20 to 100 m would
decrease
meanlightlevelstwo-fold,with similarmisestimation
of
and Sherr, 1984]. However, phytoplanktoncommunitychanges
do play an importantrole in controllingep.
Diatoms dominate the flora along most of t•e SR-3 transect
(Figure6). Largediatoms(>20 !.tm)makeup -30% of the counted
cells throughoutthe transect. Small diatoms(<20 gm) increase
steadilysouthwardfrom very low levels(-5%) nolth of the SAF
to 10% in the PFZ, 25% in the PZ and reach 80-90% south of the
growthrate. Second,because
growthratesestimated
fromthe 10
m bottlesamples
alone(notshown)arevery similarto thecolumn
growth rate, and because profiles of algal community
compositions
show little variationwith depth (H. Marchant,
unpublished
observations,
1994), the assumptionthat the 7 m
depth underway SPOM sampling obtained algae which
experienced
thecolumnweightedmeangrowthrateappears
well
AntarcticDivergencein the SSIZ. Coccolithophores
also exhibit
very low levels north of the SAF and increase southward,
reachingrelative abundancesof-20% in the PFZ and PZ before
disappearingfurther south. Flagellates exhibit a maximum of
-20% in the PFZ, contribute-15% in the PZ, but are presentin
very low abundancesin both the far north (SAZ) and far south
justified.
Five major sterols,four known to occur in diatoms [e.g.,
Volkman,1986], comprise-60% of the sterolsalong the SR-3
transect. One of the five, 24-methylcholesta-5,22E-dien-3[•-ol
(sterolIII), exhibitsa small increasein the SSIZ in the far south
where small diatomsdominate(Figure 6), and a less abundant
Overallthe ]4C-basedgrowthratesappearappropriate
for
assessing
growth
ratecontributions
to 13Cfractionation,
although
the methodologyis not without uncertainties(see review by
Sakshaug
et aL [1997]). For example,thepossibilityexiststhat
(SSIZ).
838
POPP
ETAL.:fi13C
OFSOUTHERN
OCEANPHYTOPLANKTON
30
.
y= 24.83-150x •-=0.71
25
1a....
'.
(phytolonly)
[]
o 20-
co 15-
10-
ß
SPOM
phytol
5
I
I
0.00
I
0.04
0.02
0.06
I
0.08
0.10
,,
significantly than their relative concentrations,and in different
ways than those of either SPOM or phytol. The isotopic
compositionof sterol III exhibits a trend toward progressive
depletion
in 13Crelativeto phytoltowardthesouth,
despite
its
p/(CO2*SAV
), pmolkg'1
relatively invariant fractional abundance(Figures 3 and 6).
30
_b
sterol,24-ethyl-5•x-cholest-7-en-313-ol
(sterolV), showsdoubled
relativeconcentrations
in the PZ wherecocolithophores
increase
similarly,althoughthereare no reportsof thislattercompound
in
Emilianiahuxleyi,thedominantcocolithophore
in thisregion[see
Sikes et al., 1997]. In general, the sterol relative abundance
exhibits much less variation with latitude than the organism
counts(Figure 6). This suggeststhat severalof the organism
classes(at leastthe small and large diatomscertainly)contribute
to the productionof the major steroIsand with similar relative
sterolabundances
in eachorganismclass. In contrast,individual
sterol isotopic compositions change with latitude more
y= 27.74-171x •=0.95
Comparison
tothecellcounts
suggests
thesimplest
interpretation
,
is that it is producedby both the large and small diatomsand that
25-
the smaller diatoms, which increase in relative abundance to the
south, are the dominant source of this molecule in the south.
o
o
o
Toevaluate
theroleof community
structure
incontrolling/513C
o 20-
o
compositions,
• was calculatedfor SPOM, individualsterols,and
phytol, and the relationshipsbetween•, It, and [CO2(aq)] were
then comparedwith results of recent laboratory experiments
[Lawset al., 1995, 1997; Bidigare et al., 1997a;Poppet al., 1998]
which found that a supplyversusdemandmodel for CO2 uptake
and associatedisotopicfractionationcould describea wide range
co15-
10.,
ß
o
of algal speciesisotopiccompositionsif cell size and shape
ß
sterol III
,,,
5
0.00
I
0.02
I
I
0.04
0.06
I
0.08
0.10
/(CO2*SAV), mol kg.1
30
y = -403x+ 24.95 •- = 0.65
methylcholesta-2,24(28)-dien-313-ol
(IV)and 24-ethyl-5a-cholest7-en-315-ol
(V) are poorly correlatedwith It/CO2 implyingthat
o 20-
thesebiomarkersare derived from a variety of organismsacross
the section(datanot shown). However, œpfor SPOM, phytol,and
the remaining steroIsare well correlatedwith g/CO2; however,
the slopeand interceptof the lines describingthesedata are quite
co 15-
different.
10-
0.00
I
I
0.02
0.04
•
•,
sterol I
EG
Sterol II
I
I
0.06
0.08
Severalauthorshave recognizedthat the supplyof CO2 to a
microalgalcell is affectedby [CO2(aq)] and cell size [Franfoiset
al., 1993; Goericke et al., 1993' Laws et al., 1995; Rau et al.,
0.10
/CO 2, gmolkg'1
Figure 7. Assessmentof the role of community structure
variationsalong the SR3 transect. Solid lines show regression
analysisfor œpversusg/(CO 2*SAV), whereasdottedlines show
regressionanalysisfor Ep versusIt/CO2. Considerationof the
mean diatom surface area/volume ratio change with latitude
(SAV) for phytol,SPOM, andsterolIII decreases
the slopeof the
regressionand yields an interceptsconsistentwith results of
laboratory experiments suggesting changes in community
structureinfluencefractionationof phytol, SPOM, and sterolIII.
Regression
of œpontog/CO 2 for sterolsI andII yieldsan intercept
consistentwith results of laboratory experiments suggesting
changes in community structure do not affect the isotopic
composition
of thesesterols.The œpvaluesfor steroIsIV andV
are poorlycorrelatedwith It/CO2 implyingthat thesebiomarkers
are derivedfrom a variety of organismsacrossthe section(data
not shown).
byphytoplankton
growthrate(It = 0.48d]). Asnotedpreviously
[Franfois et al., 1993], isotopic variationsin DIC accountfor a
small fraction of the variation in œp. The œp values for 24-
25-
5
variations were taken into account. For this comparisonwe
assumedEbiomarke
r values of +4%0 for phytol and +7%0 for the
steroIs; the modeled isotopic compositions of DIC and that
demandfor CO2(aq) by the cell was constantand is represented
1996], andrecently,Popp et al. [1998] showedthat the slopesof
the linesdescribingrelationshipsbetweenœpand g/[CO2(aq)] for
eukaryoticalgal speciesare a direct functionof differencesin the
surface area and volume of microalgal cells. In addition, for
eukaryoticalgae,Poœpet al. [1998] showedin the limit asg/CO2
--> 0 that œpshouldapproach
•, the maximumfractionation
associatedwith the flux-weighted averageof all carbon-fixing
reactions in the cells.
Maximum
fractionations
of 25-28%0 have
beensuggested
by Ravenand Johnson[ 1991] andby Goerickeet
al. [1994]. To determineif cell surfaceareaandvolumechanges
contributedto the relationshipbetweenœpand g/CO2 acrossthe
SR3, we consideredchangesin the meancell size of the dominant
diatom flora as a function of latitude as determinedby light
microscopy. It was assumedbased on distributionsof diatom
species(H. Marchant, unpublishedobservations,1994), that the
counted small (<20 Itm) and large diatoms (>20 Itm) had
equivalent spherical diameters of 2 and 16 Itm, respectively.
POPPET AL.: fil3c OF SOUTHERNOCEANPHYTOPLANKTON
These choices represent well the surface area and volume
characteristicsof the mix of distinctly nonsphericalcells in the
observeddiatom fractions(e.g., many pennate>20 gm diatoms
have lengthsof 40-50 gm but widths of <10 gm). Using this
approach,meansphericaldiatomcell diameterchangedfrom 13
gm in the north to 5 gm in the southindicatingan increasein
mean diatom cell surface area/volume ratio.
Changes in cell size and shapeswith latitude affect the
relationship between ep and g/CO 2 for phytol sterol III
significantly(Figure7). Specifically,for phytolandsterolIII, the
slopeof the ep versusg/CO2*SAV (whereSAV is the surface
area to volume ratio of the diatom) decreasesthree-fold and the y
interceptof a linearfit to thedataconverges
on theexpectedvalue
of 25-28%o. Without considerationof changesin cell size and
shape,regression
analysispredictsunreasonably
high valuesfor
$39
constantgrowth,this approximationmay well not be applicable,
particularlygiven the strongchangesin environmentalconditions
and vertical algal distributionsalongthe PET transect. In the PZ,
there was a strongsubsurfacechlorophyllmaximum within the
strongdensitygradientbetweensummer-warmedsurfacewaters
and the cold winter water layer (Figure 3). This densitygradient
was absent in the vicinity of the Antarctic Divergence, and
although chlorophyll again exhibited a subsurfacemaximum,
abundances
were muchlower. Southof the AntarcticDivergence
melting sea-icewaspresentduringthe transect,with an associated
cold and fresh, shallow stratified layer, within which algal
abundances
rosedramatically(Figure 3). Thus, while we have no
data on growth rates,there are good reasonsto expect variations.
Nonetheless, while keeping in mind these caveats, it is
informativeto examinecommunitystructurecontributionsto the
rangeof sterol;513C
compositions.
ef. Theseresultsare consistent
with the laboratory-derivedlarge
Both cell counts and sterol biomarker abundances
relationship between ep, g, [CO2(aq)], and cell surface
area/volumeof Poppet al. [1998] and imply that changesin cell
size had a significantinfluence on the isotopiccompositionof
sterolIII, phytol, and SPOM alongthe SR3 transect. The steep
slopeof ep versusg/CO2 uncorrectedfor SAV for cholest-5-en315-ol(sterolII) andcholesta-5,22E-dien-31S-ol
(sterolI), and an
intercept of-25%o are consistent with derivation of these
compounds
from largecellswith no significant
changein the
mean surface/volume. The fact that the slope of the line
describing the ep - B/CO2*SAV relationship for phytol is
intermediatebetween that of sterol UII and sterol III (Figure 7)
indicatesthat both large and small cells contributedto phytol. In
comparisonto the sterolIII correlation,the lower coherenceof the
cholesteroland phytol ep versusg/CO2 correlations(Figure 7)
probably arises from contributions from a wider range of
organismsincluding surface/volumechanges,speciesspecific
growth rate variations, and possibly heterotrophic effects,
althoughrecentstudiessuggestvery little isotopicfractionationof
sterolsduring their incorporationby zooplankton[Grice et al.,
1998]. The relationshipsshownin Figure7 exemplifythe added
value of isotopicinformationto biomarkerapproaches
generally
and specificallyconstrainthe way by which communitystructure
contributions
to the phytoland •S13C-SPOM
valuescan be
assessed.
In summary,althoughthe size and shapesof individual algal
species along the SR3 were not determined, estimates of
communitycell size changesfrom the phytoplanktonsize class
countssuggests
both surfacem'ea/volume
and [CO2(aq)]changed
illustrate
significant algalassemblage changes across the PET section
(Figure 8). Smatl diatoms dominate the waters close to the
Antarctic Divergence (AD) but give way dramatically to large
diatoms both to the north in the PZ and to the south in the SSIZ.
The sterol distributions
also show a difference
between
the AD
waters, where methyl-cholesterolsare fairly abundant(sterolsIII
and IV, Figure 8) and elsewhere where they are in low
concentration. In addition, the sterols discriminate strongly
between the PZ where sterol V is the most abundant sterol and the
SSIZ whereit is virtually absent. Notably sterolV was relatively
rare alongSR3 (Figure 6).
As in theSR3transect,
;S13C-phytol
and•S13C-SPOM
reflecta
mix of contributionsfrom severalsourceswhich is illustratedby
their latitudinal relations to sterol isotopic compositions
(Figure4).
Phytol •5•3Cagaingenerallylies betweenthe
relatively heavy nonmethylatedsterols and the lighter methyl
sterols.However,
in thePZ,•S13C-phytol
is muchmoredepleted,
approachingmethyl sterolvalues,in association
with the abundant
presenceof the extraordinarily isotopically light 24-ethyl-5ot-
cholest-7-en-31S-ol
(sterolV, •13C approximately-43%•).
The
overall rangeof sterolisotopiccompositionsin the PZ is extreme,
exceeding 10%• in a single sample, and if a constant offset
betweensteroland phytoplanktoncarbonisotopiccompositionis
assumed(gsterol
=7%•, seeabove),it impliesthat algaewith a wide
rangeof cellsizesand/orgrowth
ratescontribute
to •S13C-SPOM.
Although notably, there is no suggestionof a contributionfrom
sea-icehostedalgaeeven in the SSIZ, which are known to exhibit
roughly by a factor of 2 acrossthe SR3 transect and thus that
heavy•513C,up to -10%•,in response
to strongdepletionof
changesin [CO2(aq)] and communitystructurewere equally
important in controlling the isotopic composition of
1999].
phytoplankton
and•S13C-SPOM
alongSR3. Thisresultmustof
inorganiccarbon[e.g., Dunbar and Leventer,1992; Gibsonet al.,
The sourceorganismproducingthe extraordinarilyisotopically
course
betempered
bythefactthatit assul•es
thatthecommunitylight A7-sterols(sterolV) in thesesamplesis unknown.
A7-sterols
generallyhavenot beenpreviously
growth rate estimatesare representativeof all the organism Furthermore,
classes.
reportedin any SouthernOcean organisms. Several diatomsand
green algae from non-Southern Ocean locations contain low
3.3.
abundances
of A7- andAs,7-sterols
[Volkman,
1986;Patterson,
PET Transect
Clearlythe [CO2(aq)]explainsa muchsmalleramountof the
1992; Volkman et al., 1993; Barrett et al., 1995] as does a
variationin the •513Cof SPOM alongthe PET transectin
dinoflagellate,Scrippsiellatrochoidea [Harvey et al, 1988]. The
comparisonto the SR3 results (Figure 4), particularly in the
offshorePZ portion where low CO2(aq) is not accompaniedby
A7-sterols
are relativelyabundant
in sponges
[Voogt, 1976;
probablyplayeda largerrole thanalongSR3. Unfortunately,no
is presentthe isotopiccompositionof phytolis affectedindicates
Ballantine et al., 1979a, b], tunicates [Ballantine et al., 1977] and
13C-enriched
SPOM. Thusgrowthrateandecosystem
changes holothurians[Ballantine et al., 1981]. The fact that when sterolV
14C-based
growthratesweredetermined
duringthePETtransect. that the organismproducingthis compoundis a photoautotroph.
While surfacetemperaturesvaried minimally (Figure 3) so that
the Six and Maier-Reirner [1996] model predicts relatively
Large diatomsappearto dominatethe flora in the region in the
PET wherethisA7-sterol
is abundant
suggesting
thata large
840
POPP
ETAL.-813C
OFSOUTHERN
OCEAN
PHYTOPLANKTON
and when chlorophyll a concentrationswere high, strongly
AD
lOO
suggesting
thatthe A7-sterol
wasnotderivedfromsmall,slow
75
Diatoms> 20 •m
Diatoms< 20 •m
.o 50
Flagellates
growing microalgae. Recently, Laws et al. [1997] showedthat
largefractionationscan resultfrom activetransportof CO2(aq) by
diatoms. Although we have no data to show that any plankton
alongthe PET were acquiringCO2 by meansotherthandiffusion,
the simplestconclusionmost consistentwith our observationsare
that large diatoms grew while actively transportinginorganic
carbonand synthesizedsterol V. Alternatively, differencesin the
isotope
effectassociated
withbiosynthesis
of theA7 sterol([e.g.,
25
60
62
64
Schouten et al., 1998] could affect the calculation of Ko and
possibly invalidate the interpretation that these cells actively
transportedinorganiccarbon. Of particularnote is that whatever
the source of sterol V, when this organism is abundant, it can
stronglyaffectthe isotopiccomposition
of SPOM indicatingthata
single fractionation-[CO2(aq)] global relationship [e.g., Rau,
1994] may not adequatelydescribeisotopicvariationsin Southern
Oceanphytoplankton.
Why does the PET transectdisplay a much strongereffect of
algal assemblagevariationsthan occurredalong SR3? First, the
extentof nutrientutilization and biologicaldrawdownof CO2(aq)
concentrationis much greateralongPET. This resultsfrom both
the "bloom" conditions and the strong stratification present
inshorein responseto melting sea-iceinputs and offshoreabove
an intensewinter water layer. The greater"evolution"of the PET
systemmay have led to a greater diversity of growth rates and
nutrientconcentrationsboth spatiallyand temporally,so that the
conditionsmeasuredat the time of samplingmay not representas
66
Latitude, øS
80
I
60
(D 40
D.
sterol I
[]
sterolii
[]
sterolIII
•
sterot!V
[]
sterolV
20
60
62
64
66
Latitude, øS
well those that contributed to biomass formation.
Figure 8. Distributionof cell countsand biomarkercompound
abundancesalong the PET transect. The legendsfor cell counts
and sterol abundanceslist the componentsin order from most to
least abundant.
The sterol distributions
also show a difference
between the AD waters, where methyl-cholesterolsare fairly
abundant(sterol III and IV) and elsewherewhere they are lower.
In addition, the sterols discriminate strongly between the PZ
where sterol V is the most abundant
sterol and the SSIZ
where it
is virtually absent(sterol V was relatively rare along SR3, see
Figure6). SterolI, cholesta-5,22E-dien-315-ol;
sterolII, cholest-5-
en-3•-ol; sterolIII, 24-methylcholesta-5,22E-dien-3•-ol;
sterol
IV, 24-methylcholesta-5,24(28)-dien-3[5-ol;
sterolV, 24-ethyl-5c•cholest-7-en-3•-ol.
Second, the
PET transect is more strongly affected by coastal Antarctic
oceanographic
processesthan the SR3 transect. Sea-iceexhibits
strongoffshore movement in the PET region, in contrastto the
long-shorewesterly drift dominantthroughoutEast Antarctica
[Worby et al., 1998]. Just to the west, Prydz Bay exhibits a
clockwisegyre circulation [Wong, 1998]. In combinationthese
lead to an East Antarctic maximum in the seasonalityof sea-ice
extent in the PET region [Worby et al., 1998], and a
correspondinglarge coastal contribution to algal production
processes.In contrast,circulationandsea-icedrift are dominantly
zonalat the longitudeof the SR3 section,confiningcoastaleffects
to a narrow band.
4. Conclusions
diatom could be the sourceorganismeven thoughthe occurrence
of sterol V in SouthernOcean diatomshas not been previously
noted [e.g., Nichols et al., 1986, 1990, 1991, 1993' Skerratt et al.,
1995]. Sterol V occurredin low concentrations
in samplesfrom
the WOCE SR-3 sectionbetween52ø-60øSwhere large diatoms
are alsoabundant. In that regionthe carbonisotopiccomposition
Usingthe sterolbiomarkerapproachwe havebeenable to sort
out the relative roles of severalfactorscontributingto the carbon
of sterolV wasalsoextraordinarily
depleted
in 13C(Figure6). It
isotopiccompositionof SouthernOcean suspendedparticulate
organic matter. Across the open Southern Ocean along the
WOCE SR3 transect in early summer, the [CO2(aq)] plays a
strongrole, which is well describedby a supplyversusdemand
model for the extent of cellular CO2 utilization and its associated
linear dependence
of isotopicfractionation(œp)on the reciprocal
is possiblethat our microscopicobservationsoverlookedsome
of CO2(aq)•
concentration.
Changes
in algalassemblages
arealso
verysmallcellswhichproduced
thisA7 sterol.However,given
theunusually
highabundance
of thisA7-sterol,
it is difficultto
understandhow the sourceorganismcouldhavebeenmissedeven
if it was very small.
It is unclear
whysterolV is sodepleted
in 13Crelative
to the
other compoundsanalyzed. Large fractionationis expectedin
small, slow growing phytoplankton[e.g., Francois et al., 1993'
Goericke et al., 1994; Laws et al., 1995; Popp et al., 1998].
However,
this is inconsistent
with
observations:
Sterol
V
concentrationsare high when large diatomsdominatedthe flora
importantto carbonisotopiccompositional
changesalongthe SR3
transect. Their contributionis also well describedby the supply
and demand
model,
when
formulated
to
include
cell
surface/volumeratio control of supply. These conclusionsrely
partly on the determinationof essentiallyconstantgrowth rates
alongtheSR3transect
obtained
fromshipboard
community
•4C
primary productionstudies,and thereforepossiblegrowth rate
variationsamongdifferentalgal classescouldhavecontributedto
a portionof the carbonisotopiccompositional
changespresently
attributedto algal assemblagechanges.
POPPET AL.' •13C OF SOUTHERN OCEAN PHYTOPLANKTON
Along the PET transect, contributions from growth rate
variations are likely given the wide range of mixed layer
conditionsand possibleinputs of bioavailable iron from the
841
samplesand the Australian Antarctic Divsion and ANARE for logistical
support. This work was partially supported by National Science
FoundationgrantsOCE-9301204, 9633091 (BNP, RRB, EAL, and SGW),
and OCE-9521332 (BNP and EAL), and by Environment Australia,
Australia's National GreenhouseResearchProgram, the CSIRO Climate
Change Research Program (including grants to J. Parslow and B.
Tilbrook). The massspectrometers
usedin this studywere purchasedwith
supportfrom NSF (EAR 91-17610 and OCE 91-16195 BNP; OCE 9102642 BNP and D. M. Karl). An AustralianDIST travel grant (T. Trull
94/670) providedfor important exchangevisits betweenAustralian and
U.S. investigators.
This paperis SOEST contributionnumber4877.
melting ice [e.g., Sedwick and DiTullio, 1997]. However, the
phytoplanktonclasscounts,and presenceof unusualbiomarkers
with extremeisotopiccompositions
nonetheless
point to changes
in algal assemblage
asan importantcontrol.
These resultsshouldbe usedto improve the formulation of
modern carbon cycle models. To date many models have
approximatedphytoplanktoncarbon isotopic fractionation as
either constant[e.g., Maier-Reirner, 1993; Lynch-Stieglitzet al.,
1995] or as directly dependenton CO2(aq) concentration[e.g., References
Bacastowet al., 1996]. Clearlya formulationexpressing
ep asthe Arthur,M. A., W. E. Dean, and G. E. Claypool,Anomalous13C
enrichmentin modernmarine organiccarbon,Nature, 315, 216-218,
reciprocalof CO2(aq)hasnow emergedasthe bestapproach[e.g.,
1985.
Francoiset al., 1993' Rau et at, 1997: Bidigare et at, 1997a;this Bacastow, R. B., C. D. Keeling, T. J. Lueker, M. Wahlen, and W. G.
work], and growthrate and cell size/shapeeffectsshouldalsobe
Mook, The 13C Suesseffect in the world surfaceoceansand its
included[Laws et al., 1995;Rau et al., i997' Popp et al., 1998;
implicationsfor oceanicuptakeof CO2: Analysisof observations
at
this work].
Bermuda,Global Biogeochem.Cycles,10, 335-346, 1996.
The resultsare alsousefulto guidethe studyandinterpretation Ballantine, J. A., A. Lavis, J. C. Roberts, and R. J. Morris, Marine steroIs,
V, SteroIsof sometunicata:The occurrence
of saturatedring steroIsin
of SouthernOcean sedimentaryrecords.The inversedependence
thesefilter-feedingorganisms,J. Exp. Mar. Biol. Ecol., 30, 29-44,
of fractionationon CO2(aq)concentrations
meansthat cold waters
1977.
with high-dissolvedcarbondioxidelevels will exhibit relatively Ballantine, J. A., A. Lavis, and R. J. Morris, SteroIs of the
low sensitivityof phytoplankton
13Ccompositions
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Biochem.Biophysiol.,18, 1459-1466, 1979a.
changes (as noted previously by Francois et al. [1993]), and
thereforegrowth rate and size/shapeeffectswill need to be very Ballantine, J. A., A. Lavis, and R. J. Morris, Marine steroIs, VII, The
sterolcompositions
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Occurrence
of newC 26and
carefullyconsideredin interpretations
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C30 stanolsin an oceanicsponge,Comp. Biochem.Biophysiol.63B,
Biomarkerisotopicmeasurements
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119-123, 1979b.
assessalgal communitychangesgenerallyand more specifically Ballantine,J. A., A. Lavis, and R. J. Morris, Marine steroIs,XV, Sterols
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the possible presence of the organism responsible for the
extremely
13C-depleted
4-ethyl-5{x-cholest-7-en-315-ol
observed
in
thePET section
whichaffected
õ•3C-SPOMsostrongly.The
biomarkerapproachusinglong chainalkenoneswhich are derived
almost exclusively from a few speciesof haptophytealgae has
been very successfulin warm waters [e.g., Jasper and Hayes,
1990; Bidigare et al., 1997a], and there is a need to expand their
use to the Southern Ocean. Because of the specificity of
alkenonesto selecthaptophytes
[e.g., Volkrnanet-al., 1991],
variations in surface area-to-volume ratio should be relatively
small. Bidigare et aL [1997a] also showed that the carbon
isotopic fractionation of alkenone-producingalgae in natural
marine environmentsvaried systematicallywith the concentration
of dissolvedphosphate.Theseauthorssuggested
that whereboth
Cd/Ca and the isotopiccompositionof C37 alkadienonescan be
determined,it may be possibleto userelationshipsbetween[PO4]
and Cd/Ca ratios in shells of planktonic foraminifera
[e.g.,Mashiottaet al., 1997] to constraingrowth rate variations
and accuratelyestimate paleo-[CO2(aq)], although the exgct
relationshipbetween PO4 and fractionation of the alkenonecontaininghaptophytesmay be unique in the SouthernOcean.
Sincemuchof the algal assemblage
derivedvariability in the ep
versus1/CO2(aq)relationshipfor SouthernOceanphytoplankton
occurs in the SSIZ [this work; Dehairs et al., 1997] and in the
vicinity of majorfronts[thiswork; Francoiset al., 1993, Dehairs
et al.' 1997], the openPZ appearsto be the mostpromisingarea
for applicationof this approachfor reconstructions
of pastsurface
SouthernOcean CO2(aq) concentrations.
However,evenwithin
thisregion,furtherstudiesof modemcarbonisotopicfractionation
are needed to addressseasonalchangesand the relationships
betweensuspended
phytoplanktonand sedimentedorganicmatter
carbonisotopiccompositions.
Acknowledgments. We wish to thank Mark Pretty and the captain
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(ReceivedAugust17, 1998;revisedJune25, 1999;
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