Vol. 54: 121-136, 1989
MARINE ECOLOGY PROGRESS SERIES
Mar. Ecol. Prog. Ser.
P ublished Ju n e 8
Blue-green light effects on light-limited rates of
photosynthesis: relationship to pigmentation and
productivity estimates for Synechococcus
populations from the Sargasso Sea
B. B. Prézelin1*, H. E. G lover2, B. Ver H oven1, D. Steinberg1, H. A. M atlick1,
O. Schofield1, N. N elson 1, M. Wyman3, L. Campbell4
1 D epartm ent oí B iological S cien ces and M arine S cien ce Institute, U n iversity oí C aliiornia, Santa Barbara, C aliiorn ia 93106,
USA
2 B ig elo w Laboratory ior O cean S cien ces, W est B oothb ay H arbor, M ain e 04575, USA
3 D epartm ent oí B io lo g ica l S cien ces, U niversity oí W arwick, C oventry CV4 7AZ, U nited K ingdom
4 D epartm ent oí O ceanograph y, U niversity oí H aw aii, H on olu lu , H aw aii 96822, USA
ABSTRACT: T h e im p a c t of b lu e - g r e e n light in cu b a tio n on short-term diurnal, daily, a n d in te g ra t e d
w a t e r colu m n e stim a te s of w ho le w a t e r (> 0.2 pm) a n d Syne c h oco c cus-spe cific p h o to sy n th e s is w as
a sse ss e d th ro u g h o u t th e e u p h o tic z one at 2 stations in th e S a rg a sso Sea. Replicate sa m p le s w e r e
in c u b a t e d u n d e r both tu n g s t e n w hite light a n d b ro a d b a n d b l u e - g r e e n light, w h e r e th e latter sim u la ted
light quality w ithin th e u p p e r w a t e r colum n of th e o p e n sea. D iurn a l variations in size-fraction ed
(0.2-0.6 pm, 0.6-1 pm, a n d 1-5 pm) b lu e - g r e e n vs w hite light p h o to sy n th e s is -ir r a d ia n c e (P-I) curves,
chlorophyll (Chi) a n d ph y c o ery th rin (PE) c oncentratio ns, a n d cell a b u n d a n c e of PE-rich c y an o b a cte ria l
S y n e c h o c o c c u s spp. a n d C hl-flu orescin g alg ae, w e r e m e a s u r e d within sa m p le s from th e surface, PE
m axim um , Chi m ax im u m , a n d th e b a s e of th e e u p h o tic zone. S y n e c h o c o c c u s spp. d o m in a t e d u l tr a ­
p h y to p la n k to n co m m u n itie s do w n to the light d e p th s of the PE m a x im u m (3 to 7 % su rface illumination,
10), with m ax im a in cell a b u n d a n c e routinely loca ted at light d e p th s > 5 0 % I0. B l u e -g r e e n a n d white
light in cu b a tio n conditions g e n e ra lly did not affect lig h t - s a t u r a t e d ra te s of p h o to sy n th e s is (Plndx) but
b lu e - g r e e n light routin ely did p ro v id e m u c h h ig h e r e stim a te s of lig ht-lim ite d ra te s of p h o to sy n th e s is
(alpha). For size-fractioned su b p o p u la tio n s d o m in a t e d b y S y n e c h o c o c c u s spp., b l u e - g r e e n light v a lu e s
of a lp h a w e re > 5-fold g r e a te r th a n w hite light e stim ate s. C o m p a r e d to w hite lig ht estim ates, blueg r e e n light e stim a te s of total (> 0.2 pm) daily in te g r a t e d w a t e r c o lum n p rim a ry p roductivity w e r e 6 to
13 % higher, while the con trib utio n of S y n e c h o c o c c u s spp. to overall p rim a ry p r o d u c tio n rose from
b e tw e e n 57 a n d 61 % to b e t w e e n 73 a n d 84 %. From the surfa ce d o w n to a b o u t 5 % I0, the PE c o n te n t of
S y n e c h o c o c c u s cells i n c r e a s e d with d e c r e a s in g light a n d / o r in c re a s in g in o rg a n i c n itr o g e n availability.
I n c re a se s in S y n e c h o c o c c u s PE/cell o c cu rre d in direct pro p o rtio n to b l u e - g r e e n ligh t m e a s u r e m e n t s of
p h o to sy n th e tic q u a n t u m efficiency, fu r th e r in d ic a tin g th a t t h e s e c y a n o b a c te r ia a re physiologically well
su ited to h a rv e s t p h o to sy n th etiea lly utilizeable light th ro u g h o u t a l a r g e p ortio n of th e e u p h o ti c zone.
• A d d r e s s e e for c o rre s p o n d e n c e
et al. 1987). As a result, the primary productivity of
oceanic central gyres now appears to be based largely
on the photosynthetic activity of ultraphytoplankton
communities (Glover 1985, Fogg 1986, Joint 1986, Li
1986, Shapiro & Guillard 1986, W aterbury et al. 1986, Li
& Platt 1987). Ultraphytoplankton are more ab u nd an t
than net-phytoplankton in these oligotrophic environ­
ments (Murphy & H au g e n 1985, Glover et al. 1988a, b,
Iturriaga & Marra 1988), perhaps in part because
photosynthetic activity of smaller phytoplankters is
favored by w arm er tem peratures found in tropical
© I n ter-R e se arc h /P rin te d in F. R. G e r m a n y
0 1 7 1 -86 30/8 9/0 054 /012 1/$ 03.00
IN T R O D U C T IO N
Estimates of primary production in oceanic water
masses have been revised upw ard as knowledge of the
abundance and activity of very small (< 3 pm) ultra­
phytoplankton has advanced during the last decade
and field approaches to measuring photosynthetic rates
have improved (Glover 1985, Joint 1986, Li 1986,
Waterbury et al. 1986, Marra & H einem ann 1987, Smith
122
Mar. Ecol. Prog. Ser. 54: 121-136, 1989
w ater masses (Malone 1980), they have neglible sink­
ing rates (Malone 1980, Takahashi & Bienfang 1983)
and surface communities may be sustained by n a n o ­
molar levels of nitrate (Glover et al. 1988a). Further­
more, oceanic ultraphytoplankton can have near m axi­
mal rates of in situ growth (Campbell & Carpenter
1986, Prezelin et al. 1987c, Iturriaga & Marra 1988),
which could lead to vertical stratification and accum u­
lation of distinct ultraphytoplankton communities at
different euphotic zone depths of relatively stable
w ater columns.
There are both prokaryotic and eukaryotic photo­
autotrophs within ultraphytoplankton communities
sam pled from oceanic w ater masses (Murphy &
H au g e n 1985). The prokaryotic component is domi­
n ated by phycoerythrin-rich (PE) cyanobacterial
Synechococcus spp. (Glover 1985, 1988a, b, M urphy &
H a u g e n 1985, Fogg 1986, Joint 1986, Li 1986, Shapiro
& Guillard 1986, W aterbury et al. 1986, Li & Platt 1987)
and Chi b-containing free-living relatives of Prochloron
(Chisholm et al. 1988). The eukaryotic ultraphyto­
plankton are often represented by a variety of
prasinophytes, prymnesiophytes, chrysophytes and
cryptophytes (Thomsen 1986). At present, it appears
that Synechococcus populations are responsible for the
majority of w ater column productivity in the open sea
(Glover 1985, Fogg 1986, Joint 1986, Shapiro & Guil­
lard 1986, W aterbury et al. 1986, Li & Platt 1987) and
that the vertical distribution of these cyanobacterial
populations differs distinctly from that of other photo­
synthetic ultraphytoplankton populations within the
same w ater column (Murphy & H au gen 1985, Olsen et
al. 1985, Glover et al. 1986, 1988b; Chisholm et al. 1988,
Li & Wood 1988).
During summer, communities of Prochloron-like and
eukaryotic ultraphytoplankton are generally more
a b u n d a n t at and below the deep chlorophyll maximum
(Chi max) (Glover 1985, Murphy & H aug en 1985,
Glover et al. 1986, Chisholm et al. 1988, Glover et al.
1988b), w here they are thought to be p ho toadapted to
low intensity blue-violet light (Wood 1985, Glover et al.
1987) and/or exploiting the u pw ard advection of
nutrients across the thermocline (Glover 1985). From
the Chi max down, a decline in both cell abundance
and cellular rates of photosynthesis by Synechococcus
spp. generally are observed (Glover et al. 1986, 1988b,
Prézelin et al. 1986). The decline may be linked to the
very low photosynthetic quantum efficiency these
cyanobacteria have for absorbed light at w avebands in
the blue-violet portion of the visible spectrum, where
their cell absorption is dominated by nonphotosyn­
thetic carotenoids (Lewis et al. 1986, Boucher et al.
unpubl.). In contrast, Synechococcus spp. are often are
order of m agnitude more a b u n d an t in the u pp e r eu p h o ­
tic layer of the mid-Atlantic than all size categories of
Chl-fluorescing cells combined (Murphy & H augen
1985, Glover et al. 1986, 1988a, b, Li & Wood 1988).
Possible explanations for the predominance of
Synechococcus over eukaryotic algae in the upper part
of the euphotic zone include lower selective grazing
pressure on the cyanobacteria, a higher efficiency in
utilizing nanomolar levels of inorganic nitrate (Glover
et al. 1988a), and/or higher efficiency in utilizing the
blue-green spectral bands (500 to 550 nm) dominating
the underw ater light field of the upper mixed layer
(Wood 1985, Lewis et al. 1986, Glover et al. 1987,
Campbell & Iturriaga 1988, Li & Wood 1988, Boucher et
al. unpubl.).
Further improvements in predicting ocean primary
production will come, in part, from a better un derstan d­
ing of the bio-optical interactions that influence the
temporal/spatial distribution and activities of the major
photosynthetic components within the ultraphyto­
plankton communities. Given that mixed community
assemblages are routinely sampled in the field, ship­
board determinations of metabolic rates for specific
phytoplankton subpopulations can be very difficult.
However, methodological advances have enabled us to
combine selective size fractionation, epifluorescence
microscopy, Chi and PE quantification, and small vol­
ume radiolabelling techniques in the present study, in
order to detail the photophysiological characteristics
and photosynthetic activities of Synechococcus sub­
populations in a m anner usually restricted to laboratory
studies of clonal isolates. As part of a larger effort to
determine the environmental variables that influence
the natural distribution of Synechococcus, the present
field study was carried out to assess the impact bluegreen light incubation conditions can have on short­
term diurnal, daily, and integrated water column
estimates of whole water (> 0.2 pm) and on
Synechococcus- specific primary productivity. Bluegreen light conditions simulated light fields in the
upper euphotic zone and included the absorption
w aveband of phycoerythrin (PE), which has been
shown in carbon action spectra measurem ents to drive
a major fraction of photosynthetic activity in
Synechococcus spp. (Lewis et al. 1986, Boucher et al.
unpubl.). For temporal and spatial replication, m eas­
urem ents of photophysiological variables were re p e a t­
ed at 3 intervals betw een daw n and dusk throughout
the euphotic zone at 2 stations in the Sargasso Sea. By
epifluorescence microscopic enumerations of Chi- and
PE-fluorescing components within size-fractioned
samples, we were able to compare the effect that bluegreen and white light incubations have on estimates of
w ater column primary productivity and the increased
contribution that Synechococcus spp. m ake to that pro­
duction. Furthermore, it was possible to relate the rela­
tive blue-green photosynthetic light quantum effi­
Prézelin et al.: B lu e-g re en light effects on p h o to sy n th es is
ciency of Synechococcus spp. to cellular concentrations
of phycoerythrin in field populations sampled through­
out the euphotic zone of the Sargasso Sea.
METHODS
The study was conducted at 2 stations in the Sar­
gasso Sea during summer 1986, working from the RV
Endeavor'. Stn 1 was occupied betw een 21 and 28 July
and was located 140 km east of Bermuda. Stn 2 was
occupied betw een 2 and 9 August and was located
165 km north-northwest of Bermuda (Table 1). An
180 m submersible pum ping system was constructed to
collect discrete water samples and to simultaneously
profile the vertical distribution of temperature, in vivo
chlorophyll (Chi) fluorescence and in situ scalar
irradiance (Biospherical Design). Intake hose diameter
was 2" (5 cm) (ID), minimizing shear effects on phyto­
plankton communities and giving radiolabel uptake
rates equivalent to those m easured w hen replicate
samples were collected from GoFlo bottles (Prézelin &
Glover unpubl.). Pump flow rate approximated 30 gal
(1131) m in-1 , with a hose transit time of about 3 mm
from intake to outlet into a darkened container (10 gal
[381], turnover time of 20 s) on deck where samples
were debubbled. A portion of the debubbled pump
effluent was directed via a sumbersible pump (Little
Giant 2E-38N) through a secondary debubbler (11) and
into an adapted Turner designs fluorometer to measure
123
in vivo Chi fluorescence. Analog data from the
fluorometer, in situ light, tem perature and depth
probes, as well as from a surface quantum irradiance
sensor (Biospherical Design) were recorded on strip
charts.
Just prior to passage through the fluorometer, 125 ml
unfiltered samples were collected from a linetap
directly into prew ashed 125 ml polyethylene bottles
and frozen for subsequent onshore analyses of inor­
ganic nutrient concentrations. Nitrate concentrations
in the upper 60 m were m easured using a chemiluminescence technique with a precision of ± 2 n M
(Garside 1982). At d ee p e r depths, nitrate, nitrite and
ammonia concentrations were determined by standard
colorimetric methods with precisions of ± 0.08, 0.01
and 0.02 y M respectively (Strickland & Parsons 1972).
Larger-volume samples w ere collected directly from
debubbled pump effluent in the darken ed deck con­
tainer and placed in darken ed 201 polyethylene car­
boys that were immediately transported inside to the
laboratory for analyses. Shipboard enumeration of PEfluorescing Synechococcus spp. and Chl-fluorescing
algae were carried out by direct count epifluorescence
microscopy, following procedures identical to those
detailed by Glover et al. (1986).
For determination of Chi a concentration, duplicate
water samples w ere filtered, with the chosen volume
(50 ml to 11) d ep end in g upon the in vivo Chi fluores­
cence signal from the pum p profile and on the filter
pore size. Replicate samples were filtered through
T able 1 Physical a n d c h em ical characteri stics of sa m p lin g d e p th s at 2 stations in th e S a rg a sso S e a in s u m m e r 1986. Data a re
p r ovid ed for sa m p le s u s e d for m e a s u ri n g p hoto sy n th etic characteristics. PE max: d e p t h of m a x i m u m u n c o u p le d in vivo
ph y c oery thrin fluo resce n ce intensity p e r m J ; Chi max: d e p th of m a x im u m in vivo chlorophyll a flu o res ce n ce intensity p e r m 3
Sam p ling
de p th
Date
Stn 1
Surface
21 Jul
PE m ax
25 Jul
Chi max
23 Jul
Base of
eu p h o tic zone
24 Jul
Stn 2
Surface
3 A ug
PE m ax
5 Aug
Chi m ax
3 A ug
Base of
e uph otic zone
5 Aug
ND: no d a ta
Location
%
/0 Ilo
Tem p
(°C)
2
90
25.5
20
80
3
21.6
105
310
10
95
1
21.2
615
670
190
130
0.3
20.9
1675
1050
120
2
90
25.6
9
ND
ND
85
7
21.5
130
290
60
115
2
20.9
565
390
145
148
0.5
20.6
1080
230
160
D ep th
(m)
32°
63°
32"
68°
32°
63°
32°
65°
44.3'
06.9'
45.4'
08.7'
42.8'
00.4'
42.1'
59.7'
N
W
N
W
N
W
N
W
33°
65°
33°
65"
33°
65°
33°
65°
44.4'
20.0'
42.3'
19.9'
44.4'
20.0'
42.3'
19.9'
N
W
N
W
N
W
N
W
no3
(nJVf)
NH„
(n M)
no2
|n M )
ND
ND
M a r Ecol. Prog. Ser. 54: 121-136, 1989
124
Nuclepore filters of 5, 1, 0.6 and 0.2 (im pore sizes.
M ethods of filtration and extraction were previously
described (Glover et al. 1986). Chi concentrations were
determ ined directly for > 5, > 1, > 0.2 pm communities,
and by m athematical subtraction for 0.2-0.6 pm, 0.6-1
pm, and 1-5 pm fractions. Standard errors for
chlorophylls were routinely less than 10 % of the mean.
Cell-specific Chi concentrations in pure 0.6-1 pm
S ynechococcus populations (95 to 100% of all autofluorescent cells), w ere used in conjunction with cell
num bers in the 1-5 and 0.2-0.6 pm fractions, to esti­
mate Synechococcus Chi in these other size ranges.
The quantity of other algal Chi in 1-5 and 0.2-0.6 pm
fractions could then be calculated by substraction of
the am ount of Synechococcus Chi from the total con­
centration in each size category. It was only at the Chi
max and the 0.5 % light dep th that the 0.6-1 pm frac­
tion could not be considered a pure population of
Synechococcus, since they represented < 50 % of autofluorescing cells in this size range. At these depths, we
could only estimate cellular Chi concentrations of
Synechococcus spp. by proportion, using relative n u m ­
bers of Synechococcus: algal cells within the 0.6-1 pm
fraction. Synechococcus Chi may therefore have been
overestimated at the base of the euphotic zone, since
algae in this size range are believed to contain more
Chi per cell than Synechococcus spp. (Glover et al.
1987).
Phycoerythrin (PE) concentrations were determined
using a modification of procedures outlined by Wyman
et aí. (1985). Synechococcus cells were collected on
0.6 pm Nuclepore filters and resusp en ded in 4 to 5 ml
of 50 % glycerol, which uncouples energy transfer
be tw een phycoerythrin and phycocyanin. Cell n u m ­
bers in resuspensions were determ ined by shipboard
epifluorescence microscopy as previously described
(Glover et al. 1986). PE w as excited at 520 nm and the
PUB
■Chi a
125
PEB
A c cesso ry
■— c h l s — «
A c cesso ry
— c h ls —
acn
CL>
C
in vivo fluorescence emission of the pycoerythrobilin
(PEB) chromophores detected at 577 nm (half b a n d ­
width of 4 nm) in a Turner 111 fluorometer equipped
with en hancer gates to increase sensitivity. The
fluorescence intensity of the uncoupled PE in the
natural communities was calibrated at sea against
similarly treated whole cells of oceanic Synechococcus
clone WH7803 of known PE content and against iso­
lated phycobilisomes and purified phycoerythrin from
the same organism. The purpose of using phyco­
bilisomes and PE is to check for the amount of
quenching resulting from 'package' effects in whole
cells. Since the effective concentration of PE localized
in cells is high, there will always be a loss of emission
intensity owing to quenching and reabsorption. In vivo
fluorescence intensity in suspensions of uncoupled
cells was linear over the range 0 to 550 ng PE m P 1.
Diurnal m easurements of photosynthesis-irradiance
(P-I) relationships were conducted at 4 depths at both
stations. Following vertical profiling of the w ater col­
umn, samples were collected at dawn, midday and
dusk from the surface, the depth of the uncoupled PE
m -3 fluorescence maximum, the depth of the in vivo
Chi fluorescence maximum and the base of the e u ­
photic zone (0.3 to 0.5 % I0) (Table 1). Unfiltered whole
w ater samples were inoculated with sodium 14C-bicarbonate (3 to 5 g.C ml-1 final activity) and 15 to 17 ml
aliquots dispensed into acid-washed glass scintillation
vials, following procedures detailed in Prezelin et al.
(1986, 1987b). Each P-I curve represented 14 light
samples (measured at irradiances up to 550 pE m -2 s -1
in white light; up to 200 pE m -2 s _1 in blue-green light),
duplicate darks and duplicate time zero controls. Iden­
tical samples were incubated over 'white' and 'bluegreen' light, provided by a fan-cooled 500 W quartzhalogen lamp (GTE Sylvania 500T3Q/CL-120V) with
or without a Lee polyester # 1 1 8 blue-green light filter
I** X a n th o p h y lls
00
75
<L>
>
25
400
450
500
550
Wavelength (nm)
6 00
650
700
Fig. 1. S p e c tra l o u tp u t of a t u n g s te n lam p c o n ­
figu red in a p h o to sy n th e tr o n (see text) in the a b ­
s e n c e (solid line) a n d p r e s e n c e ( d a sh e d line) of a
Lee p o lyester # 1 1 8 blue lig ht filter. The
w a v e l e n g th r a n g e s for light a b sorp tion by major
p ig m e n ts p r e s e n t in o c ea n ic p h y to p la n k t o n are
in d ic a te d by horizontal bars a n d include
Chlorophyll (Chi) a, accessory Chi b a n d c, x a n t h ­
ophylls a n d ph y c o ery th rin (PE). A bsorption p e a k s
for p h y c ouro bilin (PUB) a n d phy coery thro bilin
(PEB) c h ro m o p h o re s w ithin PE are ind ic a te d by
a rrows
Pré zelin et al.: B lu e-g re en light effects on p ho to sy n th es is
screen (Fig. 1). The spectral output of the transmitted
light was m easured at 5 nm intervals over the visible
spectrum, using a Jarrel-Ash model 82-440 Ebert
monochromator configured to reduce scattering to
0.0001 %. The monochromator was placed 10 cm from
the light source, the path length through the m ono­
chromator was 50 cm, and a Li-cor collector was placed
at the monochromator exit slit. Emerging light from the
monochromator completely covered the irradiance col­
lector, and measurements are reported as percent of
maximum spectral output. Data were corrected for the
spectral sensitivity of the Li-cor sensor.
Following incubation (2 to 3 h) in one of 4 white or
blue-green light 'photosynthetrons' (Lewis & Smith
1983) water-cooled to in situ temperature (± 2C°),
both blue-green and white light samples were filtered
onto 25 mm Nuclepore filters of 0.2, 0.6, 1,0 and 5.0
pm pore size. Methods of filtration, washing and addi­
tion of scintillation cocktail were based on methods
described in Prézelin et al. (1986, 1987b). While at sea,
isotope incorporation was determined on a portable
LKB 1217 scintillation counter which was interfaced
with an Apple II microcomputer for data storage and
manipulation.
Photosynthetic
parameters
were
derived from P-I curves, using procedures detailed in
Prézelin et al. (1987b). This approach does not allow
an independent assessment of the standard deviation
of individual parameters. However, independent
determinations of the m ean Pmaxi from averages of
data points on the light-saturated portion of the P-I
curve, indicated that one standard deviation of Pmax
was routinely less than 15 %, and often less than 10 %,
of the m ean (n = 4 to 10). The lower limit of detection
for Ik (the minimum irradiance required to light-satu­
rate photosynthesis) was 3 pE m -2 s-1. Alpha was
usually determined as the slope of the light-limited
region of the P-I curve. On occasions w here Ik values
were very low (< 3 pE m -2 s-1) and insufficient data
points were available in the light-limited region of a PI curve, maximum alpha values were estimated as the
quotient Pmax/Ik. Rates of photosynthesis were d eter­
mined directly for > 0.2, > 0.6, > 1.0, and > 5.0 pm
fraction and by mathematical deduction for the
0.2-0.6, 0.6-1.0 and 1-5 pm fractions.
Estimates of water column productivity rates were
derived from calculations of in situ photosynthetic p e r­
formance, P¡, given the relation
Pt = Pmax tanh
(I /I k )
(1)
which requires knowledge of both the diurnal (dawnto-dusk) variations in underw ater irradiance (I) and the
diurnal patterns in size-fractioned P-I parameters as a
function of depth in the water-column (Smith et al.
1987). By combining these estimates of in situ diurnal
productivity patterns for each size fraction with m e a ­
125
surements of midday vertical profiles of in situ Chi and
primary productivity (Prézelin unpubl.), as well as with
data on Synechococcus chlorophyll distribution within
different size classes as a function of depth and time of
day, it was then possible to sum Synechococcus prim ­
ary production for all size categories and determine the
relative contribution that Synechococcus m akes to total
primary productivity throughout the day at any depth.
RESULTS
The physical and chemical characteristics of critical
depths at the time of sampling in the present study are
summarized in Table 1. Details of the temporal variability
in water column characteristics during 5 d at each of the 2
stations are presented elsew here (Glover et al. 1988a, b).
Most notable was the difference in nitrate concentrations
in surface waters at the 2 stations. At Stn 1 there was a
transient increase m nanomolar (nM] levels of nitrate (to
betw een 21 and 27 n M N 0 3 in the u pp e r 25 m) which
selectively stimulated a unispecific bloom of S y n ec h o ­
coccus spp. (Glover et al. 1988a); at Stn 2 there was
neglible temporal variation in phytoplankton biomass
and in the surface isothermal layer the nitrate concen­
trations were less than 10 n M (Glover et al. 1988b).
At both stations, the seasonal thermocline occurred
at 25 to 30 m (24 to 25 °C) and the depths of the PE
maxima, the Chi maxima and the base of the euphotic
zones occurred on similar isotherms. PE maxima were
located at 80 to 85 m, at 3 to 7 % I0 and on the 21.5 °C
isotherm. While PE maxima were within the upper
region of the nitracline, ammonium was the major form
of inorganic nitrogen assayed at these depths (Table 1).
Broad Chi maxima occurred 15 to 30 m below the PE
maxima and across the 1 to 3 % isotherm at both sta­
tions. The depth of the Chi maximum was shallower at
Stn 1, w here the downwelling attenuation coefficient
(Kpar) was 54 % higher than at Stn 2 (0.056 and 0.037
respectively). Both Chi maxima were located near the
21 °C isotherm at nitrate concentrations around 600
nM , although there was twice as much ammonia m e a ­
sured at Stn 1 in comparison to Stn 2. The base of the
euphotic zone at the 0.3 to 0.5 % I0 light depths w ere at
n ear identical tem peratures and w ere enriched to pM
levels of nitrate at both stations. Ammonia levels con­
tinued to increase with depth at Stn 1 but decreased at
Stn 2, resulting in relative proportions of N H 4: N 0 3: N 0 2
of 1.6:1.0:0.07 and 0.2:1.0:0.14 at the base of the
euphotic zone at Stns 1 and 2 respectively.
More than 88 % of the integrated standing crop of
Chi a at both stations occurred in the < 5 pm fraction
(Glover et al. 1988b), indicating ultraphytoplankton
dominated the photosynthetic communities. Within the
ultraphytoplankton, the depth distribution of PE-
Mar. Ecol. Prog. Ser. 54: 121-136, 1989
126
Station
I0
fluorescing Synechococcus spp. and Chl-fluorescing
algae differed distinctly (Fig. 2). At both stations, m ax­
imum Synechococcus cell abu ndance maxima were at
light depths > 50% I01 w here these cyanobacteria
numerically dominated the ultraphytoplankton (note
difference in scales used in Fig. 2). Given that
Synechococcus cell ab undance maxima in surface
waters were not coincident with depths of the
cyanobacteria-specific PE maxima found deep er in the
euphotic zone, it was apparent that the deeper popula­
tions of Synechococcus were comparatively dilute in
num ber but were enriched in cellular light-harvesting
phycoerythrin (for greater detail, see Glover et al.
1988b). Conversely, abundances of Chl-fluorescing
ultraplankton were low in surface waters but increased
within the nitracline w here both the PE and Chi m ax­
ima occurred. Near and below the 2 % I0 depth, a b u n ­
dances of ultraplankton algae and Synechococcus cells
are approximately equal within the same community.
A comparison of blue-green versus white light effects
was m ade for Chl-specific rates of photosynthesis in
whole water communities (>0.2 pm) un der light-saturat­
ing (Pmax) and light-limiting (alpha) conditions. The
values of these parameters as well as the related variable
Ik (PmaX:alpha) are displayed in Fig. 3 to 5. Diurnal
Station 2
1
(cells I '1 IO6 )
( c e l l s I' 1 I d 6
)
1s
too
Algae
10
Chi MAX
0. 1
Fig. 2. Profiles of vertical a b u n d a n c e s of PE-fluorescing
S y n e c h o c o c c u s spp. (heav y solid line) a n d < 5 um Chl-fluore scin g a lg a e p lo tte d as a function of light d e p t h at Stns 1 a n d
2 in th e S a rg a sso Sea. N o te th e a b u n d a n c e scale for
S y n e c h o c o c c u s is 5 tim es g r e a t e r t h e n th a t of u ltr a p la n k to n
algae. D e p t h of s e a s o n a l th e rm o c lin e is i n d ic a te d by a h o ri­
zo nta l d a s h e d line, w hile d e p th s of PE a n d Chi m a x im a are
i n d ic a te d by arrow s
S ta tio n
S ta tio n
1
2m
4
b) 2m
4
2
2
o L_
oL
1200
4 00
2000
400
1200
2000
1200
2000
2
2
c)
0. I
o a
d)
PE max
PE max
1
1
a
2
o>
r e
r-t O
oL
o L_
1200
400
200 0
400
2
a)
f)
C hi max
C hi max
1
oL
400
1200
2000
2000
2
h)
.SK Io
1
o L_
400
1200
L o c a l S ta n d a r d Tim a
2000
th ra )
2 000
1200
L o c a l S ta n d a r d Tim a
(h ro )
Fig. 3. C o m p a r iso n of blueg r e e n (♦) a n d w h ite (O)
t u n g s t e n light m e a s u r e ­
m e n ts of Chl-specific rates
of l ig h t- s a tu r a te d p h o t o ­
syn thesis (PmdX) of w ho le
w a t e r p h y t o p la n k t o n c o m ­
m u n ities (> 0.2 ,um) s a m ­
p le d over th e d a y from (a,
b) th e surfa ce (2 m); (c, d)
th e PE m ax; (e, f) th e Chi
max; a n d (g, h) the b a se of
th e e u p h o tic zo n e (< 0.5 %
I0) at 2 station s in the S a r­
g a sso Sea. V ertical b a rs i n ­
d icate 1 s t a n d a r d deviation
of th e m e a n
127
Prézelin et al.: B lue-green light effects on photosynthesis
S t a t io n
1
S ta tio n
.0 4
.0 4
.02
.02
2
o L_
1200
400
c)
200 0
400
1200
2000
1200
2000
1200
2000
1200
2000
6
PE max
6
m
4
.02
Ü r-.
2
S
o l_
a
1200
400
sa
2000
400
.0 4
.0 4
71
C hi max
71 C hi max
.02
.02
0L
400
2000
1200
400
8
2
4
1
0 I—
oL
400
1200
L o c a l S ta n d a r d Tim e
2 000
th ra )
400
L o c a l S ta n d a r d Tim a
(h ra )
Fig. 4. C o m p ariso n of b lu e - g r e e n (♦) a n d white (O) t u n g s t e n light m e a s u r e s of Chl-specific r a te s of light-lim ite d ph o to sy n th es is
(alpha) of w ho le w a t e r p h y to p la n k t o n c o m m un itie s (> 0.2 pm) s a m p le d over the d a y from (a, b) the surface (2 m); (c, d) the
p h yc oerythrin m a x i m u m (PE max); (e, f) the C hlorophyll m a x im u m (Chi max); a n d (g, h) th e b a s e of the e u p h o tic z o n e (< 0.5 % I0)
at 2 stations in th e S argasso Sea. Only a lp h a s w ith r e g re s s e d linearities > 0.65 (n > 4) w e r e plotted, a lt h o u g h m ost a lp h a s plo tted
h a d r v a l u e s > 0.85 a n d n = 7 to 13
patterns of daytime changes in Pmax and alpha were
generally the same w hen m easured under blue-green or
white light incubation conditions (an exception being the
alpha values for PE max at Stn 2, Fig. 4 d). Midday maxima
in photosynthetic rates were not routinely observed, the
highest rates of light-saturated and light-limited photo­
synthesis being m easured during early morning hours.
The magnitude of daytime changes in Chl-specific Pmax
dam ped with depth, being greatest in surface waters
(about 3-fold) where assimilation rates were also highest
(Fig. 3). The magnitude of daytime changes in Chlspecific alpha were as high as 8-fold but did not show a
de p th-dependent relationship (Fig. 4). Highest alpha
values were observed at the base of the euphotic zone
and within the PE max at Stn 2. Since changes in Pmax and
alpha did not covary, diurnal patterns in Ik were evident
and were distinctly different at individual depths at the 2
stations (Fig. 5). With the exception of the base of the
euphotic zone, highest Ik values at all other sampling
depths were observed at midday and were up to 7-fold
higher than either daw n or dusk measurements. Diurnal
variations in Ik d a m pened with depth and m ean daily Ik
values declined with depth.
For most samples, b lue-green and white light incub a­
tion conditions did not influence the m easured rates of
Chl-specific Pmax- O ne exception was evident during
morning within the PE max at Stn 1 (Fig. 3c), w hen bluegreen light m easurem ents of Pmax (Pmaxblue) were twice
at great as white light m easurem ents of Pmax (Pmaxw hite).
Conversely, a second exception was detected in surface
waters at Stn 2 w here the value of Pmaxblue m easured
throughout the day were only about half of those m e a ­
sured for Pmax white (Fig. 3b). Blue-green light m e a su re­
ments of alpha (alphabiue) were routinely equal or higher
than white light alpha (alphawh¡ie) (Fig- 4). There was
one exception at the base of the euphotic zone, w here
estimates of alpha w ere particularly difficult to m ake
owing to the very low biological activity of the samples.
The m agnitude of alp hablue:alphawhite varied with time
of day and was greated at Stn 2 in PE max populations
Mar. Ecol. Prog. Ser. 54: 121-136, 1989
128
S ta tio n
1
S ta tio n
400
2
400
b)
O
200
2d
200
400
a)
1200
2000
1200
2 000
C h i max
4 00
1200
2000
2 000
f)
C h i max
2000
0 . 3X Io
2 000
h)
1200
L o c a l S ta n d a r d T in a
2000
th ra )
0 .5 X
Io
1200
L o c a l S ta n d a r d T I d s
2000
thr8>
Fig. 5. C o m p a r iso n of b l u e - g r e e n (♦) a n d w h ite (o) tu n g s t e n light m e a s u r e s of Ik (= Pmax : alpha) for w ho le w a t e r p h y to p la n k to n
c o m m u n itie s (> 0.2 ,um) s a m p le d over the d a y from (a, b) th e surface (2 m); (c, d) the PE max; (e, f) th e Chi max; a n d (g, h) the base
of the e u p h o tic z o n e (< 0.5 % I0) at 2 stations in the S a rga sso Sea
dom inated by PE-enriched Synechococcus populations
(Pig. 3). The resultant combined effect of blue-green
light incubation conditions on estimates of both Pmax and
alpha was that whole w ater samples required much
lower irradiances of blue-green light than white light to
saturate in situ rates of community photosynthesis.
These observations are evident in the much lower Ik
values m easured und er blue-green light (Ikblue) than
white light (Ikwhite) for all samples except the PE max at
Stn 1 (Fig. 5)..
In situ photosynthetic performance (P¡) was esti­
m ated from combined knowledge of P-I parameters
and the underw ater light field. A comparison of P¡
estimates derived from white light P-I param eters and
blue-green light P-I param eters for whole water (> 0.2
pm) communities and the 0.6-1 pm size fraction is
given in Table 2. Note that in some instances the
differences betw een blue-green and white light
estimates were in d epend ent of time of day, while in
other instances blue-green vs white light P¡ estimates
were much greater at one time of day than another. For
samples taken from below surface waters, blue-green
light incubations generally gave rise to higher
estimates of in situ productivity. The difference
betw een white and blue-green light estimates of P,
showed an increasing trend with depth for whole water
communities. In surface waters, blue-green light
estimates w ere similar to or were significantly less than
white light estimates of photosynthetic performance.
Interestingly, the m agnitude of the blue-green vs white
light increases were similar for whole water com­
munities sampled at similar light depths at the 2 sta­
tions. For the 0.6-1 pm size fraction, blue-green light
incubation led to 3-fold higher estimates of photo­
synthetic performance at Stn 1 and 3-fold lower
estimates of photosynthetic performance at Stn 2.
Within the PE max at both stations, blue-green light
estimates were about 40 % higher than white light
estimates. Within the Chi max at both stations, bluegreen light estimates for the 0.6-1 pm fraction were 2 to
3-fold higher than white light estimates.
To further define the differential effect blue-green
light incubations might have on Synechococcus and
algal subpopulations of ultraphytoplankton within the
Prézelin et al.: B lu e-g re en light effects on ph o to sy n th es is
T ab le 2. B lu e -g re e n :w h ite ratio of e stim a te s of in situ rates of
photo syn thetic p e rfo r m a n c e (P,) in su b s u rfac e w hole w a te r
( > 0 .2 pm) a n d 0.6-1.0 pm size-fractioned c o m m un itie s from 2
stations in the S argasso S e a in J u l y - A u g u s t 1986. S a m p le s
w e r e collected at different tim es of the d a y a n d replicates
in c u b a t e d u n d e r e q u a l flu enc es of b l u e g r e e n or w hite light.
E stim ate s of P, w e re de riv e d from k n o w l e d g e of P-I p a r a m e ­
ters a n d the u n d e r w a t e r light field. PE m ax a n d Chi m ax as in
T able 1
Sa m p le d e p th
N o on
D usk
X ± SD
1.04
0.32
1.03
0.54
0.72
0.64
0.93 ± 0.18
0.50 ± 0.14
PE m ax
Stn 1
Stn 2
0.67
2.75
1.37
0.87
0.70
1.90
0.91 ± 0.40
1.89 ± 0.94
Chi m ax
Stn 1
Stn 2
1.35
1.76
1.98
0.99
1.88
0.89
1.73 ± 0.33
1.21 ± 0.47
Base of
e u p h o tic zone
Stn 1
Stn 2
1.00
5.90
3.88
1.03
2.98
0.32
2.62 ± 1.47
2.42 ± 3.03
0.6-1.0 pm
Surface (2 m)
Stn 1
Stn 2
0.33
4.95
0.34
1.11
-
3.03 ± 2.72
0.34 ± 0.01
PE m ax
Stn 1
Stn 2
2.44
1.96
0.93
0.79
0.80
1.45
1.39 ± 0.91
1.40 ± 0.59
Chi m ax
Stn 1
Stn 2
1.02
-
3.18
3.55
2.94
2.68
2.38 ± 1.18
3.12 ± 0.62
-
-
-
Base of
eu p h o tic zone
Stn 1
Stn 2
1
S ta tio n
% S yn e ch o c o c c u s C h i
0
20
40
[S u rla c e
60
80
2
% S ynechococcus
100
0
20
40
60
Chi
80
1 00
[Su fiaoel
B lu e - g re e n P,:White P¡
Dawn
> 0.2 pm
Surface (2m)
Stn 1
Stn 2
S tatio n
129
> 6 .0 0
-
Insufficient da ta to c o m p le te calculations
size-fractioned communities at both stations, the dis­
tribution of Chi biomass betw een the 2 components was
first calculated within different size fractions betw een
0.2 and 5 pm in size. Fig. 6 displays the percentage of
total Chi biomass attributable only to Synechococcus
spp. within different size fractions sampled at similar
light depths at both stations. Synechococcus Chi bio­
mass accounted for virtually all ultraphytoplankton Chi
in < 5 pm size fractions sampled from surface waters and
more than 80 % of Chi biomass in < 1 pm size fractions
sampled from the PE max at both stations. Contribution
to the 1-5 pm fraction with the PE max was dominated
by algae at Stn 1 and by Synechococcus at Stn 2. Below
the PE max at Stn 1, Synechococcus biomass accounted
Fig. 6. C o m p ariso n of p e r c e n t a g e of total Chi bio m a ss a tt r i b u t ­
ab le to S y n e c h o c o c c u s spp. w ithin different size fractions
s a m p le d at the surface, within the PE m a x a n d Chi max, a n d
the b a s e of the eu p h o tic zone (< 0.5 % I0) at 2 stations in the
S a rg a sso Sea
for the majority of Chi within the 0.6-1 pm size fraction
only, with eukaryotic algae accounting for the majority
of Chi biomass in the 0.2-0.6 and 1.5 pm fractions at the
Chi max and the base of the euphotic zone. At Stn 2, the
Chi distribution below the PE max was dominated by
algae in all size fractions with the Synechocuccus con­
tribution declining with increasing size fraction in com­
munities sampled from the Chi max and the base of the
euphotic zone.
Fig. 7 and 8 display the ratios of blue-green vs white
estimates of Chl-specific Pmax an d alpha within different
phytoplankton size fractions as a function of depth at the
2 stations. Surface values were sorted by time of day,
while values for other depths represent the m eans of
daily averages. For Stn 1, whole community (> 0.2 pm)
measures of Pmaxblue: Pmax white approxim ated 1:1 and
most subfractions within the same sample reflected
whole community values. Notable exceptions w ere at
midday within surface 0.6-1 and 1-5 pm fractions,
exclusively comprised of Synechococcus Chi biomass,
w here blue-green light m easures of Pmax w ere > 4 times
greater than white light m easures of Pmax. Similar bluegreen light enrichment of Pmax values was observed at
various times of day for Synechococcus-dominated
population within the PE max, but were less evident in
size fractions where mixed populations of cyanobacteria
and eukaryotic algae were found. At Stn 2, whole
communities sampled from surface waters over the day
Mar. Ecol. Prog. Ser. 54: 121-136, 1989
130
and incubated u n de r blue-green light actually showed
only half the photosynthetic potential of white light
samples. With increasing depth, whole w ater values for
Pnuixblue:Pmaxwhite steadily increased toward a value of
1.5 at the base of the euphotic zone. Size fractions within
whole w ater communities showed similar Pmaxblue:Pmaxwhite values, with the one exception of the 0.6-1 ¡um
mixed community of the Chi maximum.
Blue-green light enrichment of m easured rates of
light-limited photosynthesis was common at all depths
at both stations, with greatest alph abiue:alphawh¡te ratios
associated with size fractions in which Synechococcus
Chi biomass dominated phytoplankton samples (Figs. 6
and 8). Greater than 5-fold increases in Chl-specific
alpha w ere evident w h e n alph ablue:alphawh¡ie ratios
were compared for surface 0.2-0.6 an d 0.6-1 pm frac­
tions at Stn 1 (95 % Synechococcus Chi) and 0.2-0.6 pm
fraction at Stn 2 (72% Synechococcus Chi); and Chi
max 0.6-1 pm fraction at Stn 1 (60% Synechococcus
Chi). Working with only surface and PE max 0.6-1 pm
size fractions, in which Synechococcus spp. accounted
for > 95 % of Chi biomass (Fig. 6), it was evident that
Chl-specific b lue-green light alpha values increased in
direct proportion (r = 0.94) to the PE concentration
within these cyanobacteria (Fig. 9).
Photosynthetic param eters derived from white light
m easurem ents of P-I relations were used to estimate in
situ rates of photosynthetic performance (P¡) for whole
w ater (> 0.2 pm) communities and Synechococcus su b­
components and these were com pared to estimates
based upon blue-green light incubations. At Stn 1, the
impact of blue-green light incubations was to increase
total water column production estimates by less than 6 %
(from 360 to 380 mg C m “ 2 d _ *) but to increase estimates of
Synechococcus contribution to that production from 57 to
73 % (Fig. 10). Similarly at Stn 2, the use of blue-green
light incubation had much less effect on estimates of
whole community production (which increased 13 %
under blue-green light conditions) than on estimates of
Synechococcus spp. contribution to water column pro­
ductivity (Fig. 11). Due primarily to increases in alpha
estimates under b lue-green light conditions for PE max
populations of Synechococcus, estimates of Synechococ­
cus spp. contribution to total w ater column productivity
rose from 61% under white light conditions to 84%
und er blue-green light conditions at Stn 2 (Fig. 11).
D ISCU SSIO N
The determination of photosynthesis-irradiance (P-I)
param eters in phytoplankton communities is important
because they can be used to discern temporal/spatial
patterns of in situ productivity, quan tu m yield, photo­
synthetic potential and/or susceptibility to photoinhibi-
Pmax
S tatio n
1
0 2-0.6
2
0 . 6-1 0
1 . 0 -5 . 0
E
0.6-1 o l
O
1 .0-5.01
<D
0 .2-0.8 I
TO
N
U)
C
w h ite
S tatio n
0
______
.5
1
2
ir
2
3
>4
Surface
n
0
S
0 . 8 -1 .
s
i
—
o
—
c
0 .2-0.6 I
03
0 .6 -
Q.
O
-C
Q.
Pmax
1
3
and
dusk
'
0.2-0.6J
blu e
h
—
~ -~ Z—
Pn
B
■
—1
1
PE
Max
Chi
M ax
H
0 .2 -0. 6
0 . 6-1
B
•
0 3 -0 .5 %
lo
1
Fig. 7. C o m p ariso n of ratio of b lu e - g r e e n vs w h ite t u n g s te n
light m e a s u re s of Pmax in different size fractions of p h y t o p l a n k ­
ton s a m p le d over the day from the surfa ce (2 m), PE max, Chi
m ax a n d the b a se of the e u p h o tic zone (< 0.5 % I0) at 2
stations in the S argasso Sea. Ratios of Pmaxblue : Pmaxwhite for
w hole w a t e r c om m un ities (> 0.2 pm) are s h o w n as b lac k bars;
ratios for size-fractioned (0.2-0.6, 0.6-1, 1-5, > 1 , > 5 pm)
c o m m u nitie s a re s h o w n as h a tc h e d bars. In surface sa m ples,
n o o n tim e d a ta w a s sorted out a n d c o m p a re d to the m e a n of
rep lica te m e a s u r e m e n t s m a d e at d a w n a n d /o r dusk. At PE
max, Chi m ax a n d b a se of eu p h o tic zone, the m e a n of all
d a y tim e m e a s u r e m e n t s (n = 1 to 3) of b lu e - g r e e n : white Pmax
ratio is p re se n te d . Vertical bars ind icate 1 s t a n d a r d d eviatio n
of m e a n s
tion, from which bio-optical models of oceanic produc­
tivity can be tested (Bidigare et al. 1987, Prézelin et al.
1987a, Smith et al. unpubl.). In order to measure P-I
relationships of phytoplankton up to light levels equal to
midday sun at the ocean surface, shipboard incubators
are routinely used with short-term exposure to a range
of irradiances generated by high intensity tungsten
lamps. However, the spectral output from this white'
light source is known to be enriched in red wavebands
that favor light absorption by Chi a found in all photo­
synthetic cells and by accessory Chls (Chi b and Chi c)
found in chlorophytes, prochlorophytes and chromophytic algae (Fig. 1) (Prézelin & Boczar 1986). While
such spectral biasing of incubation illumination might
be expected to lead to errors in productivity estimates
(Kiefer & Strickland 1970), the actual use of white light
P-I parameters to predict independently derived
estimates of in situ productivity patterns for mixed
diatom and prymnesiophyta communities has recently
proved quite satisfactory (Prézelin et al. 1987a, Smith et
al. unpubl.). These coastal communities have several
Prézelin et al.: B lu e-g re en light effects on p h o to sy n th es is
A lp h a
S tatio n
: Alpha
w h ite
S ta tio n
1
d a wn
D. 2 - 0 6
D.6-1
2
S urface
dusk
0-5.0
C
b lu e
D .2-0.6
o
0 . 6 - 1.0
0 .2 -0. 6
0 . 6 -1 .0
C/5
c
ro
0 .2 - 0.6
0 . 6 - 1. 0
Q.
o
>*
.c
0 .2-0.6 '
CL
0.3 -0 .5 %
nd
lo
0 . 6 -1 . 0
Fig. 8. C o m p ariso n of ratio of b lu e - g r e e n vs w hite tu n g ste n
Light m e a s u r e s of chl-specific a lp h a in different size fractions
of p h y to p la n k to n s a m p le d over the d a y from th e surface (2 m),
PH max, Chi m ax a n d th e b a se of the e u p h o tic z one (< 0.5 %
I0) at 2 stations in th e S argasso Sea. Ratios of
a lp h a blue : a lp h a white for w h ole w a t e r c om m un itie s (> 0.2 pm)
are sh o w n as b lac k bars; ratios for size-fractioned (0.2—0.6,
0.6-1, 1-5, > 1, > 5 pm) com m u n itie s are s h o w n as h a tc h e d
bars. In surface sam ple s, n o o n tim e da ta w a s sorted out a nd
c o m p a r e d to the m e a n of replicate m e a s u r e m e n t s m a d e at
d a w n a n d /o r dusk. At PE max, Chi m ax a n d b a s e of e up hotic
zone, the m e a n of all d a y tim e m e a s u r e m e n t s (n = 1 to 3) of
blu e: white a lp h a ratio is p re se n te d . Vertical bars indicate 1
s ta n d a rd deviation of m e a n values
0.14
c
o
0.10
0.08
E
n.
o
c
0.06
0.04
0.02
Surta i
0.00
fg P E S y n e c h o c o c c u s c e ll" 1
Fig. 9. Variatio ns in b lu e - g r e e n light m e a s u r e s of Chl-specific
a lp h a as a function of variations in cellular PH co n ce n tra tio n s
in S y n e c h o c o c c u s po p u latio n s s a m p le d from th e su rface
(stars) a n d within the PE m a x (circles) at 2 stations in the
S argasso Sea. T h e correlation coefficient for the linear r e g re s ­
sion of the d a ta w a s 0.94
131
features that may reduce their susceptibility to spectral
bias by the tungsten incubation lamp source. First, the
high ab und an ce and species diversity within coastal
assemblages may result in a spectral averaging of light
absorption by the whole community that overcomes the
spectral bias of the light field. Second, photosynthetic
absorption and action spectra suggest that red and blueviolet light are functionally equivalent in light-harvest­
ing capabilities by the accessory Chls that drive much of
the photosynthetic activity of chromophytic and Chi tocontaining organisms that dominate coastal waters (Pré­
zelin & Boczar 1986). Lastly, there is less spectral d e p e n ­
dency in the distribution of absorbed photosynthetic
excitation energy betw een photosystems I and II in Chi
c- and Chi b-containing algae than in the phycobilinnch systems of cyanobacteria (Prézelin & Boczar 1986),
which represent only a small fraction of the phytoplank­
ton biomass in coastal regions.
The present study was prom pted by questioning
w hether the spectral bias of white' light might be
inappropriate for estimating oceanic primary p roduc­
tivity and in defining the photophysiological charac­
teristics of cyanobacterial populations of PE-rich
Synechcococcus spp. One reason for concern arose
from the knowledge that these cyanobacteria routinely
dominate phytoplankton species a b u nd an ce above the
Chi max in the open ocean (Glover et al. 1988a, b) and
blue-green light absorbed by PE alone can account for
a large majority of the photosynthetically fixed carbon
in the cell (Lewis et al. 1987, Boucher et al. unpubl.).
The use of conventional tungsten 'white' light sources
in photosynthetrons would therefore minimize the
light-harvesting capabilities of PE and lower its con­
tribution to photosynthetic carbon fixation. Some of the
spectral bias in 'white' light sources can be overcome
by placing colored filters over the tungsten lamps, such
that the spectral output of the incubation illumination
both simulates the spectral quality of light fields within
the u pper water-column of the open sea (Jerlov 1976)
and overlaps the broad 485 to 565 nm maximum in
spectral quantum yield for PE-driven photosynthesis
that is characteristic of PE-rich cyanobacteria (Lewis et
al. 1986, Boucher et al. unpubl.). The aim of the present
study was to assess the impact of blue-green versus
'white' light incubation on primary productivity
estimates of Sargasso Sea communities dom inated by
Synechococcus and to determ ine if any observed differ­
ences could be linked to other photophysiological
characteristics of these cyanobacterial populations.
B lu e-green versu s 'w hite' lig h t effects on P -I
param eters
Diurnal (daytime) periodicity of Pmax and alpha have
b e e n docum ented for ultraphytoplankton communities
Mar. Ecol. Prog. Ser. 54: 121-135, 1989
132
STATION 1
Dai l y
integrated
rates
of pr i m ar y p r o d u c t i o n
n
0
B
W H I T E LIGH T
mg
2
C
m "3
4
d a y '1
6
BLUE U G HT
mg
B
10
0
2
C
m " 3 d a y -1
4
6
8
5
15
25
S e a s o n a l th erm o clin e
3 5
45
55
65
75
P E MAX
B5
1 % lo
95
CH L MAX
05
115
25
27%
4 3%
57%
73%
To t a l a c t i v i t y =
360 m g C m “ 2 d a y - 1
Total activity =
383 m g C m ' 2 d a y - 1
Fig. 10. D e p th profiles of daily i n t e g r a t e d rates of in situ p rim a ry pro d u c tio n at Stn 1 in the S argasso Sea, c o m p a r in g estim ates
d e r iv e d from (A) w h ite light m e a s u r e s a n d (B) b l u e - g r e e n light m e a s u r e s of diurnal c ar b o n fixation. S u m m a tio n of w a te r-c o lu m n
daily i n te g r a t e d r a te s of p r o d u c tio n a re s h o w n as a p ie - d i a g r a m b e n e a t h e a c h d e p th profile. Fractional c ontribution by
S y n e c h o c o c c u s spp. su b p o p u l a ti o n s to w h o le c o m m u n itie s p r o d u c tio n (> 0.2 pm, le n g th of bars) is s h o w n by th e b lac k ba rs on the
d e p t h profile a n d th e b la c k portion of th e p ie - d ia g ra m s
dominated by PE-rich Synechococcus (Putt & Prézelin
1985, Prézelin et al. 1986, 1987b, c). These studies
dem onstrated d e p th -d e p e n d en t and w ater massd e p en d e n t changes in the timing and amplitude of
daytime variations in photosynthesis, which were in de­
p e n d e n t of Chi concentrations and dark rates of carbon
fixation. Generally, the timing of p e a k photosynthetic
potential occurred b etw een d a w n and midday and
w ere or were not coincident with diurnal variations in
alpha. The amplitude of diurnal variations in Pmax and
alpha tended to d am pen with depth. Laboratory exper­
iments have shown that diel periodicity in S ynechococ­
cus photosynthesis is not driven by a biological clock
(Sweeney & Borgese 1988), but is linked to changes in
cell cycle photobiology (Boucher et al. unpubl.). In the
present study, diurnal patterns of Pmax and alpha in
whole water samples at both stations were charac­
terized by low amplitudes and w hen evident at all,
peak activities occurred at times other than midday.
While the possible mechanisms to account for
w av elength-dependence of Pmax and alpha are
described below, it can be concluded that time of day
can influence the degree of spectral dependency evi­
dent in the photosynthetic activity of an oceanic phyto­
plankton community.
The present study generally demonstrated Pmax to be
a w avelength-independent param eter for oceanic
ultraphytoplankton (< 5 pm) communities (Fig. 7).
However, there were 2 clear exceptions, both involving
surface ultraphytoplankton that were almost exclu­
sively comprised of Synechococcus cells. First, at Stn 1
there were 2 surface subpopulations of Synechococcus
in 0.6-1 and 1-5 ,um fractions, which showed a greater
than 4-fold increase in Pmax w hen incubated under
blue-green instead of white light at midday (Fig. 7).
Concurrent m easurements determined that there was
Prézelin et al.: B lue-green light effects on photosynthesis
133
STATION 2
Daily
of
integrated
primary
B
W HITE LIGHT
mg
0
C
m“ 3
2
1
rates
production
3
B L U E LIGHT
mg
day
4
5
O
i
C
m“ 3
d a y -1
4
3
2
5
5
15
2 5
S e a s o n a l th e rm o c lin e
35
45
55
65
75
P E MAX
85
95
105
C H L M,
115
1 % lo
1 25
1 35
145
16%
39%
61%
(
84%
J
Total activity =
180 m g C m " 2 day" 1
Total
activity
=
203 mg C m " 2 day" 1
Fig. 11. D e p th profiles of daily in te g ra t e d rates of in situ prim ary pro d u c tio n at Stn 2 in th e S a rg a sso Sea, c o m p a r in g e stim a te s
d e riv e d from (A) w hite light m e a s u r e s a n d (B) b lu e - g r e e n light m e a s u r e s of d iu rn al c arb o n fixation. S u m m a tio n of w a te r - c o lu m n
daily i n te g r a t e d rates of pro duction are sh o w n as a p ie -d ia g r a m b e n e a t h e a c h d e p th profile. Fractional c o n tribu tion by
S y n e c h o c o c c u s spp. s u b p o p u la tio n s to w h ole co m m u n itie s prod uction (> 0.2 um, le n g th of bars) is s h o w n by the b la c k b a r s on the
d e p th profile a n d th e blac k portion of the p i e - d i a g r a m s
no discernable change in the PE/Chl ratio within these
size fractions at this time (unpubl.). This Pmax
biue-green : Pmax white increase was not evident at all in
independent whole water estimates, which combined
ultraphytoplankton communities with the > 5 pm frac­
tion (Fig. 3). One explanation for the blue-green light
increases in Synechococcus Pmax might be a midday
'white' light-driven photoinhibition, whereby the
unrealistic biasing in incubation illumination away
from blue-green to red wave bands could have altered
the cellular balance betw een the various deexcitation
mechanisms which normally protect the photosynthetic
components from photoinhibitory effects (cf. Powles
1984).
The second example of spectral effects on estimates
of Pmax occurred in surface waters at Stn 2, where
throughout the day all size fractions of ultraphyto­
plankton communities consistently gave blue-green
light Pmax estimates that w ere only half of those m e a ­
sured und er 'white' light (Fig. 7). Like Stn 1,
Synechococcus populations accounted for > 90 % of all
ultraphytoplankton Chi in surface waters (Fig. 6). It is
not clear w hether these results indicate a blue-green
light induced decrease or 'white' light induced increase
in Pmax. but it was app arent that the difference occurred
independently of cyanobacterial size or time of day.
One possible explanation is that nitrogen limitation in
the Stn 2 Synechococcus population could be linked to
a general mobilization of PE protein reserves to such an
extent that the light-harvesting phycobilins w ere effec­
tively decoupled from photosynthesis. Nitrate concen­
trations in surface waters at Stn 2 were less than half of
134
Mar. Ecol. Prog. Ser. 54: 121-136, 1989
those m easured at Stn 1, w here a recent input
ap p e a re d to have induced a S ynechococcus bloom that
was characterized by cells with a high PE content
(Glover et al. 1988a, b). In contrast, surface S y n e ­
chococcus cells at Stn 2 had only half the PE content as
those at Stn 1, but contained the same am ount of Chi.
These observations are consistent with laboratory
studies, which have shown nutrient deficient cya­
nobacterial cells contain normal Chi levels, while phycobilins are d e grad ed and has led to the conclusion that
light-harvesting phycobilins such as PE can also func­
tion as a nitrogen reserve (Boubissa & Richmond 1980,
Wyman et al. 1985, Carr & Wyman 1986). Furthermore,
the spectral quantum yield for photosynthesis, which is
driven by PE light absorption, is markedly reduced m
nu trient-depleted Synechococcus cells, while that of
Chi remains about the same (Lewis et al. 1986, Boucher
et al. unpubl.). If nutrient stress resulted in a decoupl­
ing of PE from the Chl-containing phototraps of
Synechococcus, then photosynthesis could have been
driven primarily by blue and red light absorption of
cyanobacterial Chi. This explanation would account for
the lack of spectral depend en cy on Chl-specific alphas
in these surface samples (Fig. 8), w hereby blue-green
light absorbed by the blue Soret region of S ynechococ­
cus Chi is about as effective in driving carbon fixation
as the tungsten 'white' light absorbed by the red Soret
region of Synechococcus Chi (Boucher et al. unpubl.).
Under such conditions, a spectral depen dency m Pmax
could result from an imbalance in the partitioning of
absorbed light energy to Chls within photosytem I and
II.
Synechococcus
spp.
numerically
dominated
ultraphytoplankton communities down to b e tw een 3
and 7 % Ior with maxima in cell ab u n dance routinely
located at > 50 % I0 (Fig. 2). It was within these p o p u ­
lations that blue-green light routinely provided much
higher (> 5-fold) estimates of light-limited rates of
photosynthesis (alpha) than white light (Fig. 8). C o n­
current with these observations, the PE content of
S ynechococcus cells increased with decreasing light
and/or increasing nitrogen availability (Glover et al.
1988b), cells had a high ratio of phycourobilin to
phycoerythrobilin chromophores (Campbell & Iturriaga
1989) and cellular rates of Synechococcus photosynthe­
tic perform ance w ere equally high from surface waters
down to the maximum in PE concentrations (3 to 7 % I0)
(Prézelin & Glover unpubl.). These observations su g ­
gest that photoadaptive increases in the content of
blue-green light obsorbing PE was central to the
m ain tenan ce of high photosynthetic rates by
Synechococcus populations throughout a large portion
of the euphotic zone. The present study also documents
that the observed increases in PE/cell occurred in direct
proportion to blue-green light m easurem ents of photo­
synthetic quantum efficiency (Fig. 9), further indicating
that these cyanobacteria are well suited to harvest the
available light throughout a large portion of the e u ­
photic zone. Hence, the color of the incubation light
may be an important consideration in future studies
aimed at determining the physiological bases of photo­
synthetic regulation in natural Synechococcus popula­
tions.
Spectral effects on photosynth etic perform ance and
contribution to prim ary productivity
The present study emphasizes the comparison of
photosynthic rates m easured in size-fractions of com­
munities incubated under tungsten 'white' or bluegreen spectral bands. However, we recognize that the
base of the euphotic layer is dominated by blue-violet
light (400 to 465 nm), which enhances light absorption
and photosynthetic quantum efficiency in a variety of
ultraplankton algae (Prézelin & Boczar 1986, Lewis et
al. 1986, Glover et al. 1987). As a consequence, the
present study may underestimate the productivity of
eukaryotic algal communities and prokaryotic Prochlorophytes (Chisholm et al. 1987, 1988, Olson et al.
1988). Thus we are emphasizing Synechococcus spp.,
which dominated ultraphytoplankton communities
from the surface down to depths just above the deep
Chi maximum.
If the argum ent regarding the distinct nature of bluegreen light photophysiology of Synechococcus is
accepted, then blue-green light or in situ estimates of
primary productivity may be more accurate than
white' light estimates and the former may provide a
better basis to determine their contribution to total
primary productivity in the open ocean. Since bluegreen light m easurements tended to raise alpha and
lower Ik values, one impact on primary production
estimates would probably come at depths where
’w hite’ light m easurements suggested light-limitation
or photoinhibition. We observed that blue-green light
incubations had the greatest impact on in situ produc­
tivity estimates just below the seasonal thermocline to
the depth of the PE maximum (Figs. 10 and 11).
Wavelength d epend ent effects on photosynthetic p a ­
rameters were less evident within ultraphytoplankton
communities at and below the Chi max, where
phycobilin-nch organisms did not dominate and little
difference m w a velength-dependent calculations of
primary productivity were therefore found.
Since the blue-green light effects on individual size
fractions tended to be greater than those expressed by
the whole water sample, the percent contribution to
total primary production by any fraction was also
affected by the spectral quality of the incubation. A
Prézelin et al.: B lu e-g re en light effects on p h o tosy nthesis
comparison of the estimated contribution of the 0.6-1
pm Synechococcus dominated fraction to whole water
rates of in situ photosynthetic performance is su m ­
marized in Table 2. With increasing depth, there is a
clear trend toward increased estimates of total primary'
production w hen blue-green rather than 'white' light
conditions were used.
In conclusion, the color of the incubation light did not
alter the timing of daytime variations in Pmaxr although
there were occasions w hen color of the incubation light
did affect the magnitude of Pmax measured throughout
the day. In contrast, alpha was often wavelengthde p en den t and the ratio of blue-green vs 'white' light
alpha measurements could depend on the time of day
that the m easurem ent was made. In general, small
daytime variations in Pmax combined with larger no n ­
coincident changes in alpha gave rise to distinct di­
urnal patterns in Ik. The spectral dependency in Ik
estimates were clearly evident, with greatest changes
in amplitude occurring in surface waters. It was the
spectral dependency on alpha and Ik that had the
greatest impact on b lue-green vs 'white' light estimates
of in situ productivity, especially for Synechococcusdominated size fraction. However, the difference
betw een blue-green and white light estimates of daily
integrated rates of primary productivity were small
since Synechococcus populations were localized in the
upper part of the euphotic zone w here photosynthesis
was light-saturated throughout most of the day. While
spectral dependency of Synechococcus photosynthesis
did not impact greatly on the estimates of water column
productivity, it was an important photophysiological
consideration that linked the relative quantum effi­
ciency of photosynthesis to the cellular concentrations
of PE in natural populations of Synechococcus. The
results showed that increases in the cellular content of
PE in Synechococcus populations were central to m ain­
taining high photosynthetic rates throughout most of
the euphotic zone.
A c k n o w le d g e m e n ts . W e a c k n o w l e d g e helpful discussions with
R. Bidigare a n d R. Iturriaga a n d access to their d a ta sets prior to
publication. We th a n k W. C o n n e ly , A. Langeley, A. E. Smith a n d
c rew of the RV E n d e a v o r ' for a ssista nce with m e a s u re m e n t s . R.
Smith lent th e sp e c tro r a d io m e te r a n d C. G a rsid e m a d e in o r­
g a n ic n u trie n t m e a s u r e m e n t s . This re s e a rc h w a s s u p p o r te d by
N S F g ra n ts O C E 8 5 2 1 1 7 0 a n d O C E 8 5 1 5 7 3 8 a w a r d e d jointly to
B. B. Prezelin a n d H. E. Glover.
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T h is article w as s u b m itte d to th e e d ito r
M a n u sc rip t first re c eive d : O cto b er 26, 1988
A c c e p te d : F ebruary 20, 1989