Annual Cycles of Phytoplankton ChlorophyllConcentrations in the

GLOBAL BIOGEOCHEMICAL CYCLES, VOL. 7, NO. 1, PAGES 181-193, MARCH 1993
ANNUAL
CYCLES OF PHYTOPLANKTON
CHLOROPHYLL
CONCENTRATIONS
IN THE
GLOBAL OCEAN: A SATELLITE
VIEW
James A. Yoder
GraduateSchoolof Oceanography,
Universityof
RhodeIsland,Narragansett
CharlesR. McClain, Gene C. Feldman,
andWayne E. Esaias
NASA GoddardSpaceHight Center,Greenbelt,
Maryland
Abstract, Conceptual
andmathematical
models
showthatannualcyclesof phytoplankton
biomass
aredifferentwithindifferentregions
of theocean.
The purposeof thismanuscript
is to usecoastalzone
colorscanner
chlorophyllimagery(CZCS-Chl)to
determine
annualcyclesin phytoplankton
chlorophyll
(biomass)
averagedoververylargeareasof the
globalocean.A possible
resultis thatlarge-scale
averaging
of CZCS-Chlwill yieldnointerpretable
signalsbecause
of spatialvariabilityin annualcycles
at scalesmuchsmallerthanouraveraging
scale.
Alternatively,
if ouranalyses
showregularand
persistent
globalpatterns,thenourresultswill
providea basin-scale
overviewof phytoplankton
biomass
seasonality
for comparison
withmodel
resultsor with otherlarge-scale
oceanographic
measurements.
Our resultsshowthatmonthlymean
CZCS-Chlimagery(andusingin situconcentrations
for winterat latitudes
polewardof 40 deg)resolves
important
differences
in annualphytoplankton
chlorophyllcyclesfor differentoceanbasinsand
latitudebelts.As predicted
by simplemodelsof
planktondynamics,ourresultsshow:(1) global
subtropical
watershavecirca2X higherCZCS-Chl
concentrations
in winter thanin summerand(2)
subpolar
watersin thenorthern
hemisphere
(NH)
havemeanmonthlyCZCS-Chlconcentrations
during
May andJunethataremanyfoldhigherthanin
winter,particularlyin theNorthAtlantic. Our results
alsoshow:(1) NorthernIndianOceanis themajor
Copyright1993
bytheAmerican
Geophysical
Union.
Papernumber93GB02358.
0886-6236/93/92GB-02358510.00
subtropical
anomaly,(2) subpolar
watersin theSH
donotshowdifferences
between
springmaximaand
winterminimaaslargeasthosein thesubpolar
NH
and(3) largeroceanareain theSH iscompensated
by highermeanannualCZCS-Chlconcentrations
in
theNH, sothatannualhemispherical
integrals
(mean
annualconcentrations
multipliedby oceanareas)are
verysimilar.Thesimplepatterns
wereportimply
thatmeanannualcyclesin phytoplankton
biomass
averaged
oververylargeareasof theglobaloceanare
largelyexplainable
by verysimplemathematical
modelssuchasthosepresented
severaldecades
ago
by Cushing,Riley, Steele,andothers.
INTRODUCTION
Conceptual
andmathematical
models,suchasthe
oneillustrated
in Figure1 [Cushing,1959],show
thatannualcyclesof phytoplankton
biomass
are
differentwithindifferentregions
of theocean.These
differences
existbecause
processes
affecting
phytoplankton
growth,suchasincidentsolar
irradiance,watercolumnstratification,
nutrient
supply,andgrazingpressure,
varywithlatitudeand
oceanographic
conditions.
Forexample,
Figure1
showsthatat polarandsubpolar
latitudes
theannual
phytoplankton
biomass
cycleis dominated
bythe
springbloom,whichoccursin response
toincreases
in meanirradiance
of themixedlayer.At thesame
latitudes,summerminima and fall maxima are caused
by nutrientlimitationandby theonset,andthen
release,of zooplankton
grazingpressure.
At lower
latitudes
of thesubtropics,
a biomass
peak(much
reduced
in comparison
to high-latitude
spring
blooms)
occurs
duringwinter,whenmixingby
windsandthermalconvection
replenishes
the
182
Yoderetal.: Phytoplankton
Chlorophyll
Concentrations
in response
to individualupwellingevents[Walshet
al., 1978; Yoder, 1985].
Thepurpose
of thismanuscript
is to usecoastal
zonecolorscanner
chlorophyll
imagery(CZCS-Chl)
to determine
annualcyclesin phytoplankton
chlorophyll
(biomass)
averaged
oververylargeareas
of theglobalocean.A possible
result(null
hypothesis)
is thatlarge-scale
averaging
ofCZCSChlwill yieldnointerpretable
signals,
because
of
spatialvariabilityin annualcyclesatscales
much
smaller
thanouraveraging
scale. Alternatively,
if
ouranalyses
showregularandpersistent
global
patterns
similartothoseillustrated
in Figure1,then
CTIC
z
PERATE
ourresultswill providea basin-scale
overviewof
phytoplankton
biomass
seasonality
andmayprove
usefultothoseinterested
in incorporating
the
biological
pumpintoglobalmodelsof carbonfluxin
theocean
andbetween
theocean
andatmosphere
[e.g., Najjar et al., 1992].
TROPICAL
METHODS
ß
J
F
M
A
M
J
J
A
S
O
N
D
MONTH
Fig. 1. Annualcyclesof phytoplankton
biomass
at
different
latitudes
in theNorthern
Hemisphere
as
predicted
froma simplemathematical
modelredrawn
from Cushing[ 1959]. In thetext,we follow the
nomenclature
of Takahashiet. al. [ 1986],sothat
"subtropical"
and"subpolar"
correspond
to "tropical"
and"temperate"
in thisfigure.
euphotic
zonewithplantnutrients.
Relatively
constant
grazingpressure
andlowmixingratesat
subtropical
latitudes
dampen
seasonal
phytoplankton
biomass
maximaandminimain comparison
tohigher
The coastalzonecolorscanner(CZCS) measured
backscatteredradiancesfrom the oceanand
atmosphere
at fourkey wavelengths
(443,520,550
and670nm)fromwhich60,000images(each
coveting
circa970x 1500kmwith4 X 4 kmpixel
resolution)
of surface
oceanchlorophyll
a plus
phaeopigment
(CZCS-Chl) werederivedfor the
globaloceanduringtheperiod1978until1986
[Feldman
et al., 1989].Oneof thedataproducts
produced
by NASA'sGoddard
SpaceFlightCenter
are"climatological
monthly
mean"globalCZCS-Chl
images
derived
bymonthly
compositing
andbinning
the 60,000 individual 4-km resolutionCZCS-Chl
images
(totalof44X 109bytes
ofdata)toafixed,
latitudes.
linearlatitude-longitude
arrayof dimension
1024X
2048[Esaiaset al., 1986;Feldmanet al., 1989].At
theequator,
eachbinrepresents
anareaof 342km2
Themodelandconcepts
summarized
in Figure1
werederivedprimarilyfromstudies
of coastalwaters
of theNorthSeaandNorthAtlantic[Riley,1947;
higherlatitudes[Feldmanet at., 1989]. Forour
studies,
wesubsampled
theoriginal1024X 2048
Sverdrup,
1953; Steele,1959;Cushing,
1959].
Morerecentstudies
showthattheseconcepts
donot
necessarily
applyto all regions
of theglobalocean.
Forexample,
at oceanweather
station
"Papa"
located
in subpolarwatersof the NorthPacific,seasonal
bloomsarevirtuallyabsent[Parsons
andLalli, 1988;
Martinet al., 1989;Miller et al., 1991;Frost,1991].
(18.5 km x 18.5 km) anda somewhatsmallerareaat
images
andworked
witha 512X 512arraythat
couldbeconveniently
displayed
withourPC-Seapak
imageprocessing
hardware
[Firestone
et at.,1989].
Oursubsampling
procedure
yielded
a visually
distorted
globalimage,yetonewhichwecouldstill
easilylocatelatitudeandlongitude
coordinates.
Usingthegeometric
meanasappropriate
forlog-
At Station "S" located near Bermuda in the
normallydistributedCZCS-Chl values,andthe
subtropical
NorthAtlantic,thespring
phytoplankton
bloomis muchlesspronounced
thanin coastal
watersat higherlatitudesandcomesearlierin the
appropriate
formula
forcalculating
variance
[Meyer,
1975],wecalculated
monthlymeanCZCS-Chl
concentrations
(mgm-3)foreach
of13study
zones
year. In subtropicalshelfwatersoff the southeastern
basedonlatituderangesin thedifferentoceanbasins
U.S.coastinfluenced
by Gulf Streamprocesses
and
in thewind-driven
upwellingsystems
associated
withEasternBoundary
Currents
(e.g.,Califomia
Current),seasonal
changes
in phytoplankton
biomass
areoftennogreaterthanthosewhichoccur
(Table 1). We follow the nomenclatureof Takahashi
et at. [1986],sothat"subtropical"
and"subpolar"
correspond
to "tropical"
and"temperate"
asusedby
Cushing[1959]. For thesecalculations,
we
excluded
CZCS-Chl
values
exceeding
10mgm-3,
Yoderet al.: Phytoplankton
Chlorophyll
Concentrations
TABLE
1. Definitions of Latitude Belts and
Stud),ZonesandTheirRespective
Areas
StudyZone
Latitude
Belt
Number
Area.
Name
1012m2
183
notasgoodasfor thoseareashavingmorecloudfree days.
The CZCS samplingstatistic(column2, Table2)
is a relativemeasureof coverageapplicableonly to
thetwelve,monthlyglobalcomposite
imagesusedas
theprimarydatasourcefor thisstudy.Foreach
monthlyimage,thenumberof bins(seeMethods)
havingat least1 measure
of CZCS-Chlfor themonth
Equatorial'
1
Atlantic
14.8
(ION-10S)
2
Indian
13.6
3
Pacific
34.4
were totaled for each of the 13 zones and then
SubtropicsNH
4
Atlantic
23.1
(10N-40N)
5
Indian
6
Pacific
SubtropicsSH
7
Atlantic
20.4
dividedby thetotalareaof therespective
zones
(Table 2). For zones1-9, theCZCS Sampling
Statisticis theaveragefromthe 12monthlyimages.
For zones10-13,only thesevenmonthlyimages
(10S-40S)
8
Indian
30.2
9
Pacific
47.0
10
Atlantic
13.9
SubpolarNH
5.0
42.1
(40N-80N)
11
SubpolarSH
Pacific
47.0
centeredon the month of the summersolstice(see
next section)were usedto derive the mean. Table 2
showsthatthe SubpolarNorth Atlantic(zone10) had
thebestcoverage(mean= 553) of the 13 zonesand
on averagewascoveredmorethantwiceaswell as
(40N-60N)
the Subantarctic(zone 12) which had the worst
12
Subantarctic 31.2
13
Antarctic
coverage(mean= 235). Note thatthissimple
samplingstatisticyieldsno information
asto how
manyindividualCZCS-Chldeterminations
were
usedto derivethemonthlyaveragefor eachbin
(40S-50S)
43.5
(50S-70S)
[Feldman et al., 1989].
Table 2 givestherange,meanandtwo measures
of variabilityof CZCS-Chlwithineachof the 13
zones defined in Table 1. The first measure of
sincethe sensordoesnot accuratelyestimate
chlorophyllconcentration
at thesehigh
concentrations.
We also excluded CZCS-Chl
variability(column5) is thestandard
deviationof the
values
from marginalseassuchasthe MediterraneanSea,
Black Sea,Yellow Sea,Seaof JapanandNorthSea.
We also wanted to estimate the total amount of
CZCS-Chl in eachof the 13 zones.To integrateover
area,we multipliedthemonthlymeanCZCS-Chl
concentration
(mgm-3)foreachstudy
zonebyits
area(Table 1), andthento a depthof 1 m, to yield
totalCZCS-Chl (mg) in theupper1 m acrossthe
entirezone. The 1-m integrationdepthwaschosen
arbitrarily(to be discussed).
annual mean CZCS-Chl (column 4) for each zone.
The secondmeasuresof variability(columns7-9) are
the minimum,maximum,andaveragecoefficientof
variation(standard
deviationdividedby themean)
basedon the statistics
derivedby summingCZCSChl for all of the bins within each zone for each
monthlyimage. In otherwords,thesecond
measures
of variabilityarean approximate
measure
of spatialvariabilitywithineachzoneandfor each
month.
The results in column 9 show that the
coefficientof variationtypicallyexceeds1.0
indicatingthatthestandard
deviationis generallyof
RESULTS
the same order as the mean. The results in columns
Coveraee and Data Characteristics
4 and5 showthatmeanannualCZCS-Chl for many
of the zonesarestatistically
different(e.g.,with 95%
confidence), whereasresultsin columns 6-8 indicate
CZCS operatedfrom October1978untilJune
1986,but CZCS dataacquisitionis biasedin both
time andspacefor two reasons.First,CZCS shared
powerwith otherscientificinstruments
onthe
Nimbus7 spacecraft
andthusdid notoperate
continuously.On a daily basis,theinstrument
was
switchedon approximatelytwiceasoftenduringthe
first 3 yearsof operationthanduringthelastfour
[McClainet al., 1990]. Targetswerenotrandomly
selected,and,for example,areassuchasthewestern
NorthAtlanticwerecoveredmuchbetterthanmany
otherpartsof theglobalocean[McClainet al.,
1990]. Second,CZCS could not view the ocean
throughclouds,andthuscoverageoverpersistently
cloudyregions(e.g., North PacificandSouthern
Ocean;seeBishopandRossow,1991)wasgenerally
thattheannualcycleswithinat leastsomeof the
zones(e.g., zone 3) are not robust. During the
remainderof thismanuscript,we focuson zones
havingannualcycleswith at leasta twofold
difference between maximum and minimum values
andwith systematicincreases
(or decreases)
for
several months between nodes.
Corrections to the CZCS Results
On thebasisof aninitialscreening
of ourresults,
we suspected
thatCZCS overestimated
Chl i!
concentrations
at highlatitudes
fromlatefall to early
spring. In addition,theCZCS wasincapableof
determining
Chl it concentrations
duringsomewinter
monthsat latitudeshigherthancirca60 degrees
184
Yoderet al.: Phytoplankton
Chlorophyll
Concentrations
TABLE 2. CZCSSampling
Statistic
(CZCSSS)andOtherSununm'y
Statistics for the Zones Described i n Table 1
CZCS-ChL
Concentration
Coefficient of Determination
mgm-3
Zone CZCSSS Ran•e
Mean
Standard
n MinimumMaximumAverale
1
248
0.08-0.19
0.14
0.04
12
0.9
2.1
1.4
2
279
0.06-0.15
0.10
0.03
12
0.7
1.3
0.9
3
291
0.08-0.11
0.09
0.01
12
0.8
1.0
0.9
4
375
0.07-0.16
0.11
0.03
12
1.0
1.5
1.3
5
343
0.11-0.79
0.30
0.18
12
1.2
3.8
1.9
6
349
0.06-0.11
0.08
0.02
12
0.8
1.4
1.2
7
273
0.07-0.14
0.10
0.02
12
1.1
1.4
1.2
8
298
0.07-0.14
0.09
0.02
12
0.9
1.1
1.0
9
228
0.06-0.13
0.08
0.02
12
0.8
1.3
1.0
10
553
0.39-0.89
0.68
0.17
7
1.1
1.8
1.5
11
381
0.39-0.66
0.50
0.10
7
1.1
1.8
1.5
12
235
0.17-0.23
0.21
0.02
7
1.0
!.4
1.1
13
292
0.16-0.28
0.21
0.04
7
1.1
1.7
1.4
Seetextfor definitions
andinterpretations.
because
of low incidentirradiance.To partially
validatethespringandfall CZCS-Chlestimates
at
highlatitudesandto derivewinterconcentrations
for
veryhighlatitudes,we compared
climatological
monthlyCZCS-Chlestimates
withclimatological
monthlyin situChl a measurements
for thethree
openoceanstationswheresuchdataareavailable
(Figure2): oceanweatherstation"Papa"(N. Pacific
at 50ON, 145ow), oceanweatherstation"India"
(N. Atlantic at 59ON, 19ow), and station"S" near
Bermuda
(N. Atlanticat 32ON,65ow). Although
themeanseasonal
patterns
illustrated
in Figure2
representmultiyearaveragesof CZCS-Chlandin
situresults
overdifferent
years,theresults
clearly
indicate
thatCZCS-Chloverestimated
monthly
mean
Chla concentration
at "Papa"
for September,
October,andNovember.Comparisons
wereless
conclusive
at "India,"in partbecause
in situdata
were not available for November and December. At
"S,"CZCS-Chlconcentrations
agreedwellwiththe
lowerrangeobserved
byMenzelandRyther[ 1961]
from 1958 to 1959 and with the more recentresults
(1988 to 1989) from the U.S. JointGlobal Ocean
FluxStudytimeseries[Knapet al., 1991].High
concentrations
reported
by MenzelandRyther(1961)
to correctsatelliteobservations
for latitudeshigher
than40 degasdescribedbelow. For latitudes
higherthan40ONin boththeNorthAtlanticand
North Pacific, we made no correctionsto the CZCS-
Chl datafor the7 months(March-September)
centeredon the month of the summersolstice(June).
For the3 months(November-January)
centeredon
the month of the winter solstice(December),we
assumedthatthe in situresultsfrom "Papa"and
"India"betterrepresented
meanwinterconditions
at
highlatitudes
in theNorthPacificandNorthAtlantic,
respectively,
thandidtheCZCS-Chlimagery.Thus
we usedclimatological
monthlyin situconcentrations
for these3 monthsfor theanalyses
reported
in the
restof thismanuscript.
Fortheremaining
2 months
of theyear(OctoberandFebruary),
we interpolated
betweentheCZCS-Chlestimates
for September
(and
March) and the winter values basedon the in situ
data. Time seriescomparisons
betweenthe
climatological
monthlyin situresultsandthe
corrected CZCS-Chl
estimates are illustrated in
Figure 3.
A correction
procedure
for highlatitudes
in the
southern ocean similar to that described for the North
AtlanticandPacificis notpossible,
because
long
at "S" are unusual and are not considered
time seriesof in situ Chl it concentrations
are not
representative
of thisstation(Deuseret al., 1990).
On thebasisof thecomparisons
illustrated
in
Figure2, we madenochanges
to theCZCS-Chl
available.Nevertheless,
we anticipate
similar
problems
with theCZCS-Chldataduringwinter
monthsat high latitudesin thesouthernocean.Thus
measurementsbetween 40ON and 40os butdecided
we chose a winter concentration for latitudes south of
185
Yoderet al.: Phytoplankton
Chlorophyll
Concentrations
3.0
(September-March)
centeredon themonthof the
-
OWSP
-
2.0
/
C
summer solstice(December).
To summarize the effects of our correction
procedure,theanalysesreportedin theremainderof
thismanuscriptarebasedsolelyon CZCS-Chl
resultsfor latitudesbetween40ON and 40os, and
solelyon CZCS-Chl resultsfor latitudespolewardof
40 degfor the7 monthsof theyearcenteredon the
summersolsticeof eachhemisphere.In situand/or
1.0
modified CZCS-Chl
I
I
I
I
I
I
I
I
I
I
3.0
ows!
A
_
2.0
measurements were used for
latitudespolewardof 40 degfor the5 months
centeredon thewintersolsticeof eachhemisphere.
Therearepotentialflaws in ourcorrectionprocedure,
particularlyin the southernhemisphere
(SH), butour
resultsfor highlatitudesareprobablymuchmore
realisticthanff we wereto haveusedonlysatellite
data(e.g., comparethe trendsin Figures2 and3).
Fromthispointhence,we will usetheterm "CZCS-
I
czcs-ch/
•
Chl" to refer to both corrected and uncorrected
results.
1.0
Seasonal Trends in Mean Monthly CZCS-Chl
Concentrations
In situ
•X
-
I
I
I
I
I
I
I
I
I
I
I
Figures4 and5 showmonthlymeanCZCS-Chl
Z
concentrations within each of the ocean basins and
within each of the five belts defined in Table 1.
- OWSP
1.5
[ Stn."S"
•CZCS-Chl
O JGOFS
3.0
1.0
?
0.5
2.0
•
E 1.0
0
8 ' o
2
4
6
8
10
12
•
"r'
MONTH
Fig.2. Annualcyclesin mixedlayerchlorophyll
il
U
concentrations
at oceanweatherstations"Papa"
U30
1'14
'
(OWSP)in theNorthPacificand"India"(OWSI) in
the North Atlantic and at station"S" (Stn "S") off
Bermuda. For OWSP and OWSI, solid lines are
monthly
meanCZCS-Chlconcentrations
overthesite
0
I
I
I
_
I
I
I
I
I
I
I
I
I
owsI
Z
2.0
anddashedlinesaremeanmonthlyin sirevalues
[fromParsons
andLalli, 1988]. ForStn"S,"solid
linesshowtherangeof in situvaluesreportedby
MenzelandRyther[ 1961],opencirclesarein sire
......
A
_
czcs-chy
•
!.0
values
reported
byKnapet al. [1991],andthesolid
circlesaremeanmonthlyCZCS-Chlconcentrations.
I
40osbasedontheclimatological
monthlym'mimum
CZCS-Chl
concentration
(0.12mgm-3)forthe
Subantarctic
andAntarcticzones(Table1) duringthe
3 months centered on the month of the winter solstice
(June).As for thenorthernhemisphere
(NH), we
did not correct CZCS-Chl estimates for the 7 months
I
2
MONTHS
I
4
I
I
6
I
I
8
PAST WINTER
I
I
I
10
I
12
SOLSTICE
Fig.3. Annualcycles
inmixedlayerchlorophyll
il
concentrationsafter CZCS valueswere corrected
according
to theprocedure
described
in thetext.
Symbols
andlinesasforFigure2.
186
Yoderetal.' Phytoplankton
Chlorophyll
Concentrations
0.3
1. MeanmonthlyCZCS-Chlconcentrations
duringsummer
in theSubpolar
SHBeltareonly
approximately
doublethoseof thewinter(Figure4).
2. In theAtlanticandIndianOcean
Equatorial
belts,CZCS-Chlvariesannually
overa twofold
0.2
0.1
_
•//••'-•
/•
0
I
I
I
I
rctic
range.Lowest
concentrations
(<0.1mgm-3)occur
duringAprilin bothbasins,
whereas
highest
concentrations
arefoundduringDecember
and
January
fortheAtlanticandSeptember
fortheIndian
Ocean(Figure4). CZCS-Chlconcentrations
in the
Equatorial
Pacificarerelativelyconstant
compared
to
theEquatorial
AtlanticandIndianOcean(Figure4).
3. MeanmonthlyCZCS-Chlconcentrations
duringwinterin all threestudyzonesof the
Subtropical
SH Beltareapproximately
1.5times
Sub Antarctic
I
I
I
I
I
I
I
EQUATORIAL
those of the summer with little interbasin difference
(Figure4).
4. Mean monthlyCZCS-Chlconcentrations
duringMay andJunein theSubpolar
NH Beltare
manyfoldhigherthanduringwinter(December
and
January)with the maximumwinterto summer
difference
(10-fold)occurring
in theN. Atlantic
(Figure5). Resultsfrom boththeN. Atlanticand
Pacificshowa slightfall peakfollowinga relative
0.2
ß.'"..... """-.,Incl.
0.]
ß
*e, e .....
0
0.3
I
I
**ø*
I
I
I"a C.
I
I
I
I
I
I
I
summer minima.
5. Mean monthlyCZCS-Chlconcentrations
in
theAtlanticandPacificbasins
of theSubtropical
SUBTROPICS
N.H. Belt show identical trends with winter
S.H.
1.0
0.2
-
SUBARCTIC
0.8
.Incl.
eeee
,
.
0.6
I
I
2
I
I
4
MONTHS
I
6
PAST
I
I
8
WINTER
I
I
I
10
I
0.2
12
SOLSTICE
i
Fig. 4. Annualcyclesin meanmonthlyCZCS-Chl
concentrations
for eachstudyzonewithinthe (upper)
SubpolarSH, (middle)Equatorial,and(lower)
SubtropicalSH belts. SeeTable 1 for definitionsof
studyzonesandbelts. We arbitrarilyreferenced
the
EquatorialBelt to theNH wintersolstice.
•
1.O-
u
0.8-
i
SUBTROPICS-
I
I
I
I
I
I
I
I
I
N.H.
z
<:t 0.6
Figure4 illustratestheresultsfrom the threebelts
(Subpolar
SH,Subtropical
SHandEquatorial)
having
relatively
low(<0.3mgm-3)maximum
monthly
CZCS-Chlconcentrations,
andFigure5
illustrates
theresults
fromthetwobelts(Subpolar
NHandSubtro•pical
NH)having
relatively
high
(circa1 mgm-a) maximum
monthly
CZCS-Chl
concentrations
averaged
across
entireoceanbasins.
Annualcycles
asresolved
bymonthly
meanCZCSChlimagery
areevident
in allbelts(Figures
4 and5)
as summarized below:
•: 0.4
0.2
0
MONTH
Fig. 5. Annualcyclesin meanmonthlyCZCS-Chl
concentrations
for eachstudyzonewithinthe(upper)
SubpolarNH and(lower)Subtropical
NH belts.See
Table 1 for definitionsof studyzonesandbelts.
Yoderet al.: Phytoplankton
ChlorophyllConcentrations
187
1.0
0.8
-
Subpolar
N.H
0.6
0.4
0.2
_
-1- 0.20
u
I
d
t,u
0.15
0.10
0.05
2
4
MONTHS
6
PAST
8
WINTER
10
12
SOLSTICE
Fig. 6. Annualcyclesin meanmonthlyCZCS-Chl
concentrations
for eachof thefive belts. Subpolar
NH andSH areillustratedin theupperpaneland
Equatorial, SubtropicalSH andNH areillustratedin
thelowerpanel.We arbitrarilyreferenced
the
EquatorialBelt to theNH wintersolstice.SeeTable
(DecemberandJanuary)concentrations
Inteeration
approximately
1.5timesthosein summer(July).
The N. IndianOceanis a majoranomalyof the
Subtropical
Belt. CZCS-Chlconcentrations
during
Augustareapproximately
8-foldhigherthanwinter
concentrations,
(Figure5).
Mean monthlyCZCS-Chlconcentrations
for each
of the five belts(i.e. averagedoverall basins)are
illustratedin Figure6. For theEquatorialBelt (lower
panel),theslightincreasein CZCS-Chlduringthe
lattermonthsof theyearreflecttheinfluenceof the
AtlanticandIndianOceanequatorialbelts,notthe
Pacific(seeFigure4). Patternsaresimilarin NH
andSH Subtropical
Beltsduringwinterandspringin
therespective
hemispheres,
butmeanCZCS-Chlis
higherin theN.H. duringsummerandfall owingin
partto theeffectsof themonsoonin thenorthern
Indian Ocean(seeFigure5). Figure6 alsoillustrates
an importantasymmetry
betweenthesubpolar
belts
of theNH and SH in thatspringandsummerpeak
CZCS-Chlconcentrations
aremuchhigherin theNH
than the SH.
1 for definitions of belts.
Over Area
Figure7 showsmeanmonthly,spatially
integrated(x,y dimensions)
CZCS-Chlwithinthe
subpolarandsubtropical
beltswithineach
hemisphere.To calculatethetotalamountof
phytoplankton
chlorophyllin theglobalocean,one
shouldalsointegratein the thirddimension,i.e.,
overthedepthof themixedlayeror euphoticzone.
As will be discussed,
we did not integrateoverdepth
of themixedlayeror euphoticzone,butarbitrarily
integratedto a depthof 1 m.
Resultsin Figure7 showthatseasonaltrendsin
subpolarandsubtropicalwatersareout of phasein
eachhemisphere,thusdampeningseasonality
of
hemispherical
integrals.Thereis virtuallyno
seasonalityin the SH, andspringandsummervalues
in the northernhemisphere
arelessthan2X higher
thanwinter,(Theequatorial
beltfrom10øNto 10os
wasleft out of Figure7, sinceit doesnot
significantly
affectthemonthlypatterns
withineach
hemisphere.)
188
Yoderet al.' Phytoplankton
Chlorophyll
Concentrations
30
20
10
0
30
,I
I
I
I
I
I
-
Total
S.H.
20
Subpolar
10
•
,,
Subtropical
I
I
I
I
I
I
2
4
6
8
10
12
MONTHS
PAST WINTER
Fig.7. Annualcyclesin meanmonthlyCZCS-Chl
spatialintegrals(meanmonthlyCZCS-Chl
concentration
multipliedby thezonalareasandthen
summedby belt)for subtropical
andsubpolar
waters
of the (upper)northernand(lower)southern
Theareaunderthe"total"curvesin Figure7 are
measures of the total mean annual CZCS-Chl in the
SOLSTICE
hemispheres.
Solidlinesshowthesumof subpolar
andsubtropical
monthly
integrals.
Notethatthe
unitsonthey axisindicate
thatthemonthly
values
reflect
integration
overareabutnotdepth
(seetextfor
explanation).
theSH. Thus,forthesubtropics
andparticularly
for
upperonemeterof eachhemisphere.
Meanannual
subpolar
waters,largerareain theSH is
compensated
by highermeanannualconcentrations
CZCS-Chlin theupper1 m of thetwohemispheres
areremarkably
similaranddifferby only9 percent
in theNH, sothattheirrespective
integrals
arevery
(242X 109g fortheNHversus
263fortheSH).
The differenceis within1 percent(162 versus163),
whenwe only useresultsfrom the7 monthsof the
yearbasedsolelyonCZCSdata. Why arethetwo
hemispheres
sosimilar?Table 1 showsthattheSH
Subtropics
have 1.39X moreareathantheNH
Subtropics.However,meanCZCS-Chl
concentration
oftheNHSubtropics
(0.11mgm-3)is
1.22Xhigherthanfor theSH Subtropics.
Differences
in hemispherical
areaandmeanCZCSChl for Subpolarwatersarefar moredramatic.
Subpolarwaterscover2.7X moreareain the SH
than the NH (Table 1). However, meanCZCS-Chl
concentration
intheNH(0.45mgm-3)is2.5X
greater
thanthemean
concentration
(0.18mgm-3)in
similar.
Are the differencesbetweenthe meanCZCS-Chl
concentration
of subpolarwatersof theNH andSH
caused
byhighermeanconcentrations
in openwaters
or by highermeanCZCS-Chlconcentrations
within
largeroceanmarginareasof thesubpolar
NH?
Figure8 showsmonthlymeanCZCS-Chl
concentrations
(forthe7 months
based
solelyon
satellitedata) for the North and SouthAtlantic and
North and South Pacific. The data were extracted
from10degX 10degstudyareascentered
between
latitudes
of40ONto50ONinthecentral
partofthe
respectivebasins.The resultsshowthatmean
CZCS-Chlconcentrations
in openocean
waters
are
significantly
higher
in theNH versus
SH,averaging
0.3(sd= 0.1)versus
0.07(sd= 0.02)mgm-3,for
Yoderet al.' Phytoplankton
ChlorophyllConcentrations
189
1.0 -
0.8
0.6
0.2
0
I
I
I
I
I
I
1.0-
0.8 N. Pacific
0.6
0.4
0.2
S. Pacific
I
4
MONTHS
6
PAST
8
WINTER
,,
10
SOLSTICE
Fig. 8. Annualcycles(7 monthsof satellitedata
only)in meanmonthlyCZCS-Chlconcent_rations
for openwatersbetween40 and50 deglatitudein the
NorthandSouthAtlantic(upper)andNorthandSouth
Pacific(lower). Largeerrorbars(standard
deviations)
arenotshownin theupperplate,because
of significant
overlapbetweenupperandlowercurves.
theNorthandSouthPacific,respectively
and0.4 (sd
detect
chlorophyll
below
oneattenuation
length
(K-1,
= 0.1)versus
0.2(sd= 0.1)mgm-3,fortheNorth
andSouthAtlantic,respectively.The second
question
of oceanmargininfluence
cannotbe
addressed
directlywith thelow spatialresolution
imageryusedin ourstudy.Specifically,
ocean
marginstudies
requireeither1 x 1 kin, or possibly
4
x 4 km, resolutionimagery. However,continental
coastline(exclusiveof the ice-coveredAntarctic
continent)
at subpolar
latitudes
is approximately
2.9X longerin theNH thantheSH indicating
that
themargininfluencemayalsocontribute
to
hemispheric
differences
in meanCZCS-Chlat
subpolarlatitudes.
whereK is theexponential
decayconstant
describing
the verticalattenuationof solarirradiance).This is
themainreason
wechosenottointegrate
chlorophyll
overdepth,sincewe donotyethavea reliable
procedure
for doingsoona globalscaleatmonthly
resolution.Integrating
CZCS-Chlwithdepthis
complicated
for tworeasons.First,theintegration
depthcouldeitherbethedepthof themixedlayeror
thedepthof theeuphoticzone. The latteris
appropriate
whentheeuphotic
zoneis deeperthanthe
baseof themixedlayer. Second,subsurface
chlorophyllmaximumlayersarecommonwhenthe
euphoticzoneis deeperthanthemixedlayer[e.g.,
HerblandandVoituriez, 1979;Venxicket al., 1987]
andaregenerallydeeperthancanbe observed
with a
satellite sensor. Sufficient data exist to model the
DISCUSSION
CZCS-Chlimageryhaswellknownlimitations
thatshouldbeconsidered
wheninterpreting
the
resultspresented
here. One of themostserious
limitationsis theinabilityof satellitecolorscanners
to
seasonality
of theverticalchlorophyll
prof'fie
and
thusdepth-integrated
chlorophyll
formostof the
Atlanticbasin[Plattet al., 1991],butnotglobally.
To the extent that the effects of these two CZCS
limitationsdiffer betweenoceanbasins,latitudebelts
andthetwo hemispheres,
ourresultsarea biased
Yoder et al.: Phytoplankton
ChlorophyllConcentrations
190
viewof annualphytoplankton
biomass
cycles.Our
resultsarealsoinfluencedby thenonrandom
coverage
of theglobalocean
caused
bothbycloud
conditions
andby themannerin whichCZCSwas
operated.Forexample,
moreCZCSdatawere
collectedin the NH than the SH, and thusthe SH
results
areprobably
lessreliablethanthose
obtained
in the NH.
Within the constraints discussedabove, our
results
area uniqueviewof themeanannual
cycle
(monthlyresolution)of phytoplankton
chlorophyllin
the surfacewatersof theglobalocean.Of particular
interest are the differences and similarities between
seasonalCZCS-Chl concentrations
in subpolar
watersof theNorthPacificandAtlantic,subtropical
watersin bothhemispheres,
subpolarwatersin the
NH andSH andthe similarityof seasonally'
integratedchlorophyllcontentin thesurfacewaters
of the two hemispheres.
Two previousstudiesshowedthateithermean
chlorophyllconcentrations
or primaryproduction
weregenerallyhigherin theNorthPacificthanthe
North Atlantic[Lewiset al., 1988;Hinga, 1985].
Our maximummonthlymeanCZCS-Chl
concentration
for the subpolarwatersof theNorth
Atlantic
basin
(0.9mgm-3)isslightly
higher
than
the meanmaximumchlorophyllconcentration
(0.7
mgm-3)forthesame
general
region
inferred
from
the globalsecchidiskarchive[Lewiset al., 1988],
whereasour maximummonthlymeanCZCS-Chl
concentration
fortheNorth
Pacific
(0.6mgm-3)is
considerably
lower thanthatinferredfrom the secchi
diskarchive
(1.4mgm-3).Wedonotknow
the
masonsfor thisapparentdiscrepancy
betweenthe
two chlorophyllestimatesin theNorthPacific,but
bothCZCS andsecchi-based
chlorophyllestimates
haveprobableerrorsbetweenplus/minus
40 to 100
percent[Lewiset al., 1988;Gordonet al., 1983].
Relativetrendsin theannualCZCS-Chlcyclesof
subpolar
watersin theNorthAtlanticandPacificare
generallyconsistent
withprevious
descriptions
[ParsonsandLalli, 1988] in thattheNorth Atlantic
exhibitsgreaterrangebetweenwinterminimaand
spring/summer
maximathantheNorthPacific.As
quantified
in earlymodelsof plankton
dynamics
[e.g.,Cushing,1959],the springincreasein
phytoplankton
biomass
(i.e., springbloom)in
subpolar
NorthAtlanticwatersis caused
by seasonal
increases
in incidentsolarirradianceandby seasonal
stratification(whichdecreases
thedepthof the
surfacemixedlayer). In response
to theresultant
increase in mean levels of solar irradiance in the
mixedlayer,phytoplankton
growthrateincreases
andexceedszooplankton
grazingrateandother
lossesleadingto a gradualbuildupof phytoplankton
biomass.By late springor summer,phytoplankton
lossesexceedgrowth,haltingandthenreversing
the
springincrease
in phytoplankton
biomass.In situ
studiesat Station"Papa"in thenortheastern
subpolar
Pacificshowthatseasonal
uncouplingbetween
phytoplankton
growthandzooplankton
grazingdoes
not occur there to the extent observed in the North
Atlantic [ParsonsandLalli, 1988;Frost,1991]. Our
CZCS-Chl resultsfrom station"Papa"(e.g.,Figure
3) shownonseasonality
similarto thein situstudies,
butthe annualpatternfor all subpolarwatersof the
North Pacificis not too dissimilarfrom subpolar
watersof the North Atlantic(e.g.,Figure5).
Seasonalcyclesin CZCS-Chl concentrations
in
subtropical
watersin theAtlanticandPacificare
identicalandbotharesimilarto therelativepattern
sketchedby Cushing(seeFigure1). WinterCZCSChl concentrations
areapproximately
doublethosein
summer.This subtropical
patternis generally
attributedto two factors:Higherplantnutrientflux
to the surfacemixedlayerin winter(coincidingwith
the breakdown of the seasonalthermocline)than
summerandrelativelyhighincidentsolarirradiance
duringwintercomparedto conditions
at higher
latitudes.With respectto seasonal
CZCS-Chl
cycles,the majorsubtropical
anomalyis theNorthern
Indianocean. Upwellingof nutrient-richwaters
duringthe summermonsoon[Banse,1987; Brock
andMcClain, 1992]resultsin meanmonthlyCZCSChl concentrations in the Northern Indian Ocean
duringsummerthatareashighasthosefoundduring
the springbloomin theNorthAtlantic. The
NorthernIndianOceanrepresents
only about3
percentof thetotalareaof globalsubtropical
waters,
andthusthemeanseasonal
cyclein CZCS-Chlin
subtropical
watersgloballyis minimallyaffectedby
thehighsummerCZCS-Chlconcentrations
in the
Northern Indian Ocean.
AnnualCZCS-Chlpatternswithinthethree
equatorialzonesareall different.The Pacificis
nonseasonal,
theIndianhasan August/September
maximum,andtheAtlantichasa maximumduring
December.The August/September
maximumin the
EquatorialZoneof theIndianOceanmayberelated
to the Monsooncycleasobserved
in subtropical
watersof thatbasin.The EquatorialAtlanticwasnot
coveredwell by CZCS, andthusthe annualcycle
presented
in Figure4 maynotberepresentative
of
the meanannualcycleof itsregion(F. MullerKarger,personalcommunication,
1992).
CZCS-Chl resultsshowthatspringandsummer
phytoplankton
biomasspeaksarenotobservedin
subpolarwatersof the SH to theextenttheyare
observed in the North Atlantic and Pacific.
This is a
majorasymmetrybetweenthetwo hemispheres
and
cannotbe explainedsolelyby hemispherical
differencesin thetotalareaof productiveocean
marginwaters. Instead,meanCZCS-Chl
concentrations
in openwatersat subpolarlatitudes
aresignificantlylowerin theSH comparedto
comparable
latitudesin theNH. Many explanations
arepossible,includinghemispheric•d
differences
in
ironavailability[Duceet al., 1991;Martinet. al.
1990, 1991], incidentsolarirradiance[Bishopand
Yoderet al.: Phytoplankton
Chlorophyll
Concentrations
Rossow,1991; Mitchell et al., 1991], verticalmixing
[Nelsonand Smith, 1991], andzooplanktongrazing
[Frost, 1991].
CZCS-Chlcontent(area-integrated)
of the
surfacewatersof thetwo hemispheres
aresimilaron
anannualbasisimplyingthatoceanprimary
productivity
of thetwo hemispheres
mayalsobe
similar. The lattermustbe cautiously
interpreted
for
severalreasons.First,integrationwith depthcould
changeestimates
of therelativeamountof euphotic
zonechlorophyllcontentof thetwo hemispheres.
Second,environmentalconditionsaffect the rate of
photosynthesis
perunitchlorophyll,
andtheremay
be hemispherical
differences
in suchconditions.For
example,recentstudiessuggest
thatsubpolar
waters
of the SH receivelesssolarirradianceduringthekey
growthseasons
thanat comparable
latitudes
and
seasonsin the NH [BishopandRossow,1991].
Primaryproduction
modelsbasedon bio-opfical
provincesfor all basins,similarto thosenow
availablefor the Atlantic [Plattet al., 1991], will be
requiredto resolvedifferences
betweentheannual
meanandseasonality
of hemispherical
primary
production.
Recentmeasurements
showthatthe springbloom
in subpolar
watersof theNorthAtlanticsignificantly
reduces dissolved carbon dioxide in surface waters
[Watsonet al., 1991]. This carbondioxide
drawdownis partof a complicated
sequence
of
biologicalandphysicalprocesses
whichcauses
the
NorthAtlanticto be animportantsinkfor
atmospheric
carbondioxide.Is therea relation
betweentheshapeof thecurvedescribing
themean
annualcyclein phytoplankton
biomass
andtheCO2
sourceor sink characteristics
for variousregionsof
theglobalocean?In otherwords,aretheimbalances
betweenphytoplankton
biomass
accumulation
and
lossanimportantcharacteristic
affectingthefateof
CO2 in surfacewaters?Becausemanyfactorsother
thanprimaryproductivity
(suchasheatflux,
remineralizafion,
oceancirculationandgasexchange)
affectsurfaceoceanCO2 a simplerelationship
probablydoesnotexist;at leastoverthetime
(monthly)andspace(basin)scaleswe consider.For
example,the subpolarwatersof theNorthPacific
(zone 11, Table 1) are a sourceof CO2 for the
atmosphere,
whereastheNorthAtlantic(zone10,
Table 1) is a sink [Takahashiet al., 1986]. Both
showsimilarbasin-averaged
annualcyclesin CZCSChl. The annualCZCS-Chl cyclein subtropical
waters of the North and SouthAtlantic (zones4 and
7, Table 1) arevirtuallyidentical,yet theNorth
Atlanticis a significant
sinkandtheSouthAtlanticis
a weak sourceof CO2 [Takahashi,1986)]. To the
extentthatinterbasinor interhemispheric
differences
in thebiologicalpumpaffecttheair/seaexchange
rate
of CO2, our resultssuggest(notsurprisingly)
that
satellite ocean color data alone will not resolve the
important
biologicalprocesses
contributing
to such
differences.
191
With minorexceptions,our analysesof global
CZCS-Chl imageryshowseasonal
pattemsin
subtropical
andsubpolarwatersthataresimilar
identicalto the simplesketches
originallypresented
by Cushing[ 1959]manydecadesago(seeFigure1).
The sketches
werebasedon a verysimplepredator
andpreymodelwith someimplicitassumptions
concerning
phytoplankton
growth-limiting
effectsof
nutrients and solar irradiance.
The obvious
implicationof theexcellentagreement
betweenour
resultsandthosefrom theCushingmodelis thatthe
grossaspectsof phytoplankton
dynamicsin the
surfacewatersof theglobaloceanareverysimple
whenall of themesoscale
variabilityhasbeen
averagedout. This wasan unexpected
findingin that
a very likely alternativewasthatourlargescale
averagingwouldsmearall signalsyieldingeithera
straightline on graphsshowingmeanCZCS-Chl
versusmonthor randomnoise. Are thesimple
patternsthatwe describefortuitousor is thema
masonfor theapparentagreement
with theCushing
model?Assumingthelatter,onepossibleexplanation
is an analogywith resultsobtainedby thosewho
infer changesin oceanproductivityovertime scales
of thousands
to millionsof yearsby measuring
changesin percentageof organicmatterdownthe
lengthof deep-seasedimentcores.Subsamples
drawnandanalyzedfrom deep-sea
coresgenerally
yield a mixtureof materialthataccumulated
over
manyhundredsto thousands
of years,andthusyearto-year,decade-to-decade,
etc.time scalefluctuations
areaveragedout. Longerperiod(thousands
to
millionsof years)fluctuations
in percentsediment
organiccarbon,representing
shiftsin ocean
productivityoccurringovermanythousands
to
millionsof years,showrelativelysmoothpattems
thatare coherentover oceanbasins[e.g.,Stein,
1991]. Averagingpixelsfrom a monthlymean
globalCZCS-Chl image,whichin tum is a
compositeof manysingleimagescollectedduring
hundredsto thousands
of orbits,mayin someways
be analogous
to determiningmeancarboncontentof
a coresubsample,
but in the spatial,ratherthanthe
temporal,domain.
Acknowledements.
We thank scientists and
technicians
at theGoddardSpaceFlightCenterand
theUniversityof Miami for thehugetaskof
processing
theCZCS imageryandgenerating
the
dataproductsusedin our study. JohnRyan
providedtechnicalassistance
at URI. The work was
supported
by theEcosystemDynamicsand
Biogeochemical
Processes
Branchof NASA
Headquarters
andby theEOS Interdisciplinary
ScienceProgram.
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