© PLOSI o
OPEN 3 ACCESS Freely available online
-
Predicting the Electron Requirement for Carbon Fixation
in Seas and Oceans
Evelyn Lawrenz1*, Greg Silsbe2, Elisa Capuzzo3, Pasi Ylöstalo4, Rodney M . Forster3, Stefan G. H. Simis4,
O ndrej Prásil1, Jacco C. Krom kam p2, Anna E. Hickm an5, C. M ark M oore5, M arie-Hélèn Forget6,
Richard J. G eider7, David J. Suggett7
1 Laboratory o f Photosynthesis, Institute o f M icrobiology, ASCR (Academy o f Sciences o f th e Czech Republic), Opatovickÿ rnlyn, Treboñ, Czech Republic, 2 Netherlands
Institute o f Ecology, Centre fo r Estuarine and Marine Ecology (NIOO-CEME), Yerseke, The Netherlands, 3 Centre fo r Environment, Fisheries & Aquaculture Science (CEFAS),
Lowestoft, Suffolk, United Kingdom, 4 Finish Environment Institute (SYKE), Helsinki, Finland, 5 Ocean and Earth Science, University o f Southam pton, National
Oceanography Centre, Southampton, Hampshire, United Kingdom, 6 Takuvic Joint International Laboratory, UMI 3376, Université Laval (Canada) CNRS (France),
D epartm ent de Biologie and Québec-Océan, Université Laval, Québec City, Québec, Canada, 7 School o f Biological Sciences, University o f Essex, Colchester, Essex, United
Kingdom
Abstract
Marine ph ytoplankton account for about 50% o f all global net prim ary pro du ctivity (NPP). Active fluorom etry, m ainly Fast
Repetition Rate fluo rom e try (FRRf), has been advocated as means o f providing high resolution estimates o f NPP. Plowever,
not measuring C 02-fixation directly, FRRf instead provides ph otosynthetic qu an tu m efficiency estimates from which
electron transfer rates (ETR) and ultim ately C 02-fixation rates can be derived. Consequently, conversions o f ETRs to C 02fixation requires know ledge o f the electron requirem ent fo r carbon fixation (i>Siû ETR/C02 uptake rate) and its dependence
on environm ental gradients. Such know ledge is critical for large scale im plem entation o f active fluorescence to better
characterise C 0 2-uptake. Flere we examine the variability o f experim entally determ ined
values in relation to key
environm ental variables w ith the aim o f developing new w orking algorithm s fo r the calculation o f @eC from environm ental
variables. C oincident FRRf and 14C-uptake and environm ental data from 14 studies covering 12 marine regions were
analysed via a meta-analytical, non-parametric, m ultivariate approach. C om bining all studies, @eC varied between 1.15 and
54.2 mol e - (mol C)-1 w ith a mean o f 10.9±6.91 mol e- mol C)- 1 . A ltho ug h variability o f
was related to environm ental
gradients at global scales, region-specific analyses provided far Im proved predictive capability. Plowever, use o f regional
0>e_c algorithm s requires objective means o f defining regions o f Interest, w hich remains challenging. Considering Individual
studies and specific small-scale regions, tem perature, nutrient and light availability were correlated w ith 0>eC albeit to
varying degrees and depending on the study/region and the com position o f the extant ph ytoplankton com m unity. At the
level o f large blogeographlc regions and distinct w ater masses, 0>eC was related to nu trien t availability, chlorophyll, as well
as tem perature a n d/or salinity In m ost regions, w hile light availability was also Im portant In Baltic Sea and shelf waters. The
novel 0>e_c algorithm s provide a m ajor step forward fo r widespread fluorom etry-based NPP estimates and h ig h lig h t the
need for furthe r studying the natural variability o f
to verify and develop algorithm s w ith Im proved accuracy.
C itation : Lawrenz E, Silsbe G, Capuzzo E, Ylöstalo P, Forster RM, et al. (2013) Predicting the Electron Requirement fo r Carbon Fixation in Seas and Oceans. PLoS
ONE 8(3): e58137. doi:10.1371/journal.pone.0058137
Editor: Lucas J. Stal, Royal Netherlands Institute o f Sea Research (NIOZ), The Netherlands
Received October 13, 2012; A ccepted January 30, 2013; Published March 13, 2013
C opyrigh t: © 2013 Lawrenz et al. This is an open-access article distributed under th e terms o f the Creative Commons A ttrib u tio n License, w hich permits
unrestricted use, distribution, and reproduction in any medium, provided th e original a uthor and source are credited.
Funding: This w ork and some o f th e cruises have been made possible via fu nding through th e EU FP7 project PROTOOL FP7 (grant num ber 226880). The funders
had no role in study design, data collection and analysis, decision to publish, or preparation o f th e manuscript.
C om peting Interests: The authors have declared th a t no com peting interests exist.
* E-mail: [email protected]
uptake rate after subtracting o u t any C 0
Introduction
2
lost to o x id a tio n o f
organic carbon over a d ie l cycle [ 1 ],
A ccu ra te ly evaluating the im p a ct o f local e n viro n m e n ta l and
O f all global NPP, m a rin e ecosystems account fo r ca. 50% [2],
global clim ate change u pon tro p h ic dynam ics a nd biogeochem ical
an a m o u n t equivalent to ca. 51 • 1
n u trie n t cyclin g is fu n d a m e n ta lly tied to
[2,3]; alm ost a ll o f this p ro d u c tiv ity is fro m
how
w e ll p rim a ry
p ro d u c tiv ity , defined here as carbon ( C 0 2) fixa tio n , is charac­
terised. F o llo w in g the in c o rp o ra tio n o f in o rg a n ic rad io-labelled
0 15
g o f fixe d carbon p e r year
p h y top la n kto n .
H ow ever, m arin e ecosystem-scale p ro d u c tiv ity estimates co n tain a
C 0 2 in to algal cells has becom e a standard m ethod for
q u a n tify in g p rim a ry p ro d u c tiv ity . H ow ever, to this day, there still
h ig h degree o f un ce rta in ty, since th e y are u ltim a te ly derived by
e xtra p o la tio n fro m discrete measurements o f N P P o r G PP [4,5]
w ith lim ite d spatial and te m p o ra l resolution. R em ote sensing
exists considerable u n ce rta in ty as to w h e th er 1 4 C 0 2 uptake
measures gross p rim a ry p ro d u c tiv ity (GPP) o r net p rim a ry
p ro d u c tiv ity (NPP). F o llo w in g the tra d itio n a l view , G PP refers to
(ocean colour) p ro d u c tiv ity a lg o rith m s are the m ost w id e ly used
to o l fo r m aking these extrapolations in o rd e r to b e tter characterise
carbon fix a tio n w ith o u t a cco u ntin g fo r any carbon losses due to
H ow ever, these p ro d u c tiv ity algorithm s are e x p lic itly dependent
resp ira tio n a n d /o r excretion, w h ile N P P represents the carbon
o n relative ly few discrete, surface “ tr u th ” 14C p rim a ry p ro d u c tiv ity
PLOS ONE I www.plosone.org
the nature and extent o f v a ria b ility in N P P in m arin e ecosystems.
1
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
T a b le 1. Studies included in the meta-analysis.
S tud y/C ruise ID
G eog raph ical area
AMT6
Atlantic
AMT 11
Atlantic
AMT15
Tropical Atlantic
D246
D ate
<rpsnspec
npsn
ETR/14C
N
References
14 May-12 Jun 98
0.002
In situ1/PE;
40
[24,25]
15 Sep-09 Oct 00
0.003/0.002
In situ1/PE;
66
[24,25]
17 Sep-29 Oct 04
0.003
In sltuVPE"
[26]
Celtic Sea
17-28 May 00
0.002
In situVPE5, SIS
[27,28]
JR98
Celtic & Irish Sea
31 Jul-11 Aug 03
measured
On deck1/PE;
Time series
Gulf o f Finland
11 A pr-15 Nov 00
0.002
In situVin situ'
Time series
Massachusetts Bay
27 Feb-29 Nov 00
1.75
Time series
Ariake Bay, Japan
26 Jun-04 Oct 06
1.75
SYNTAX
Baltic Sea
21 - 30 Jul 2010
CEND0811
North Sea
08-12 May 11
D366 UK-OA
UK & European shelf
06 Jun-12 Jul 11
Time series
Bedford Basin, Canada
23 Feb-18 Apr 07
+
measured
On deck2/PE5
20
BIOSOPE2
Pacific Ocean
12 Sep-21 Nov 04
1.5
0.003
On deck3/PE5
25
d
SUPREM011
Gulf o f Finland
11-15 Apr 11
+
0.002
On deck2’7/PE5
42
e
28
[29]
In situ1/PE;
37
On deck2/FAST
24
[30]
0.002
[31]
0.003
On deck2/FAST
c
Data were collected during cruises undertaken as part o f the Atlantic Meridional Transect (AMT) Program, Individual cruises to the Celtic Sea, Baltic Sea, North Sea, other
UK and European shelf waters and the Pacific, as well as part o f tim e series studies In the Gulf o f Finland, Massachusetts Bay (USA), Ariake Bay (Japan) and Bedford Basin
(Canada). M ethodological differences existed In the way data were corrected for spectral discrepancies between the fluorom eter and 14C-lncubator light source
(ftpstopec), in the estimates o f the number o f photosystem II (nPS!!), and In the approach used to compare electron transport rates (ETR) and 14C fixation.
+ spectral corrections applied according to Moore et al. [11 ]. In some samples, a spectral correction factor o f 1.75 was used w hile a spectral correction was n.a. denotes
not applicable because primary productivity was measured on samples Incubated In the cuvette holder o f a FASTact Fluorometer.
ripsH was assumed to be constant (0.0033 or 0.0020 mol RCII (mol chia) ') or calculated either according to it) nPSu = 500 (FyFm)/0.65 or (f) Oxborough et al.[7]. ETRs
were either measured in situ or on discrete samples using a 1FASTtrecka, or 2FASTact FRR fluorom eter, a 3FIRe benchtop fluorom eter or a 4FRRFDlvin9 Flash. Superscript 5
denotes photosynthesis Irradiance curves measured on samples Incubated for 1-4 hours using a photosynthetron [32] or equivalent Incubator, 6 denotes 2 hour in situ
b ottle Incubations, w hile 7 Indicates rapid lig h t curves carried o u t In on-deck laboratories under tem perature controlled conditions. SIS stands for 24 hour on deck
'simulated in situ' Incubations, and N Is the num ber o f observations fo r each study, a) Silsbe and Ylöstalo unpublished, b) Lawrenz, Capuzzo, Forster, Suggett
unpublished, c) Suggett and Forget unpublished, d) Prásll, Gorbunov, Babin, Huot unpublished, e) Ylöstalo et al. unpublished.
dol:10.1371 /journal.pone.0058137.t001
measurements. M a n y researchers have, therefore, tu rn e d to high
resolution bio-optical-based approaches in o rd e r to m eet this
p ro vid e accurate estimates o f the rate o f gross
0
2
evo lu tio n fro m
P S II [16,17] and, hence, GPP. E h ifo rtun a te ly, m an y applications
(e.g. clim ate m odels, fisheries assessments) req u ire th a t p rim a ry
challenge.
Pulse A m p litu d e M o d u la te d (P A M ; [ 6 ]) and Fast R e p e titio n
Rate (FR R ; [7,8]) flu o ro m e try p ro vid e the p o te n tia l to d ra m a t­
p ro d u c tiv ity be expressed n o t as E T R o f 0
ic a lly increase the n u m b e r o f estimates o f N P P in m arin e
ecosystems [ 8 ] , As w ith o th er b io -o p tica l sensors, active flu o ro m ­
C 0 2, th a t is, NPP. As such, a p p lic a b ility o f broad-scale active
fluorescence-based measurements o f E T R are p o te n tia lly lim ite d i f
E T R s cannot be easily converted to G PP a nd eventually NPP.
2
e vo lu tio n b u t ra th e r
in the p hotosynthetic cu rre n cy (sensu Suggett et al. [18]) o f fixed
e try can be utilised in situ and thus, measurements o f p ro d u c tiv ity
Such conversion requires knowledge o f the E T R to C 0
can be lin k e d d ire c tly to measurements o f p h ysica l/ch e m ica l
variables at the tim e o f sam pling [9 -1 1 ]. In a d d itio n , data can be
collected at h ig h te m p o ra l (seconds) and spatial resolution a n d /o r
2
fix a tio n
ra tio , i.e. the electron req u ire m e n t fo r carbon fix a tio n (0 >fjc) w ith
units m o l e (m ol C) . W ith E T R and short-term (hours) C O "
fix a tio n incubations representing G PP ra th e r th a n N P P [19,20],
over large scales [12]. I f direct, in situ measurements o f N P P using
active fluorescence co u ld be achieved, the advantages o f this
0 r c also captures gross ra th e r th a n a net efficiency.
approach w o u ld represent a step change in ope ra tio n a l capacity,
Since the in tro d u c tio n o f active fluorescence to m a rin e research,
a n u m b e r o f studies have attem pted to com pare measurements o f
in terms o f accuracy and resolution, com pared to ‘co n ve ntio n a l’
1 4 C-based approaches, w h ich are lim ite d b y the need to incubate
E T R w ith (quasi-)simultaneous measurements o f C 0
2
uptake, the
relative ly large w a te r samples, often fo r lo n g durations [13], w ith
la tte r representing GPP, N P P o r som ething in between depending
attendant p o te n tia l problem s due to ‘bo ttle effects’ [14,15]. Thus,
on in cu b a tio n tim es (1 h o u r to a fu ll diel cycle) [1 0 ,21 -2 3 ]
(Table 1, references therein). In itia lly , these exercises aim ed to
the w idespread im p le m e n ta tio n o f active fluorom eters on broadscale te m p o ra l o r spatial sam pling platform s, such as ships o f
evaluate w h e th er E T R s p ro vid e d a robust q u a n tifica tio n o f G PP
o p p o rtu n ity and m oorings w o u ld represent a m a jo r advance in
[3 2 -3 5 ]. M o re recent studies have sought to understand the extent
and nature o f va ria tio n between the E T R and G PP a n d /o r N PP
evaluating the v a ria b ility o f p rim a ry p ro d u c tiv ity in seas and
oceans.
[10,11,18,36], N um erous b io ch e m ica l processes o ther th a n C 0 2
fix a tio n can act to consume electrons, A T P a n d /o r reductant; fo r
A c tiv e fluorescence can be used to estimate the rate at w h ich
electrons flo w fro m w a te r th ro u g h photosystem I I to N A D P H (the
exam ple,
oxygenase
a c tiv ity
o f rib ulose-l,5-bisphosphate
M e h le r Ascorbate Peroxidase (M A P ) a c tiv ity [32] and n u trie n t
assim ilation [35,37]. A ll these processes are expected to e x h ib it
b o th taxon-specific a nd e n viro n m e n ta l dependencies w ith corre­
p ro d u c tio n o f energy (ATP) and reductant (N A D P H ) used to fix
C 0 2. T hus, measurements o f E T R b y active fluorescence, at best,
PLOS ONE I www.plosone.org
the
carboxylase/oxygenase (Rubisco) v ia p h o to re sp ira tio n [32], ch lo ro re sp ira tio n via a p lastid te rm in a l oxidase (P T O X ) [33,34],
so-called lin e a r photosynthetic electron transfer rate, E T R ), and
o th e r electron acceptors. E T R is m ost closely related to the rate o f
gross 0 2 evolution, and p o te n tia lly less d ire ctly to the subsequent
2
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
w ith the la tte r be in g used as a p ro x y fo r p h yto p la n kto n biomass.
sponding v a ria b ility o f 4>ec [11,18]; indeed, a recent co m p ila tio n
o f published F R R -based <Fe>c data sets suggested the existence o f
W e fu lly acknowledge th a t oth er e n viro n m e n ta l variables, such as
the silicate o r iro n are often also key in d e te rm in in g p h y to p la n k to n
some general ta xo no m ic patterns in the v a ria b ility o f <Fec [38].
H ow ever, as yet, no single (global) systematic evaluation attem pted
to consider h o w e n viro n m e n ta l gradients regulate
co m m u n ity co m p o sitio n and physiological responses and, hence,
influence <Fe>c- H ow ever, these data were either n o t collected as
p a rt o f the studies in clu d e d here o r n o t available. M eth o d o lo g ica l
C learly, active flu o ro m e try co u ld become a m u ch m ore
p o w e rfu l to o l fo r e stim ating GPP (or even NPP) in carbon
u pon ro u tin e ly m easured variables can be established. Therefore,
we constructed a database o f FR R -based measures o f <Fec and
variables in clu d e d differences in F R R protocols and 14C in cuba­
tio n techniques (see below). Locations o f samples were character­
ized b y la titu d e a nd lon g itu de , w h ile seasonal differences were
characterized b y co n ve rtin g sam pling dates to J u lia n day. A ll the
associated e n viro n m e n ta l variables k n o w n to regulate p rim a ry
e n viro n m e n ta l data were e ith e r k in d ly p ro vid e d b y the authors o f
p ro d u c tiv ity , (e.g. tem perature, n utrients and lig h t) fro m b o th
the published w o rk, the B ritish O ceanographic D a ta C entre
(B O D C , w w w .bodc.ac.uk) o r were taken fro m the o rig in a l
cu rre n cy i f generic relationships describing the dependency o f <Fe>c
previously published and unpublished data sets a nd used a m etaanalytical approach to determ ine the p re d ic ta b ility o f <Fec fro m
e n viro n m e n ta l variables. Specifically, we addressed the fo llo w in g
p u b lica tio ns and d ig itize d (Plot D ig itiz e r 2.5.0, Free Software
Foundation) fro m relevant figures.
three questions: (1) T o w h a t extent does <Fe>c va ry w ith in and
Values o f K d (in units o f m
*) were derived fro m ve rtica l
between oceanic areas and w a te r masses? (2) C an a ‘g lo b a l’ <Fec
ever be a pplied o r should region-specific values always be used
instead? (3) H o w is the v a ria b ility o f <Fe>c related to th a t o f
F in la n d [29], the U K -O c e a n A c id ific a tio n cruise (D366) and the
e n viro n m e n ta l factors o r com binations th e re o f (lig h t attenuation,
P acific Ocean (B IO S O P E 2) dataset.
irra d ia n ce profiles fo r the A M T cruises, B e d fo rd Basin, the C eltic
Sea (JR98), B a ltic Sea (S Y N T A X 2 0 1 0 ), A ria ke Bay, the G u lf o f
nutrients, tem perature, salinity, etc.)? O u r analysis dem onstrated
th a t v a ria b ility in <Fec was strongly correlated w ith the a va ila b ility
F o r the re m a in in g studies, M O D IS 4 km satellite products o f
euphoric zone depth (zeu), here defined as 1% o f surface P A R ,
pro d u ce d b y the G io v a n n i o n lin e data system (N A S A G o d d a rd
E a rth Science D a ta and In fo rm a tio n Services Center) averaged
o f lig h t and nutrients, as w e ll as tem perature a n d /o r salinity, albeit
to v a ry in g degrees a nd depending on h o w data are organized in to
region-specific subsets. Predictive algorithm s based on these
relationships are presented. T re a tm e n t o f data at the regional
scale p ro v id e d m uch im p ro ve d pre d ictive ca p a b ility o f these
over
8
days were used to calculate K d b y solving
E 1% = E 0 x e - ZeuKd
algorithm s relative to large scale o r global algorithm s. A lth o u g h
m an y o f the algorithm s still need fu rth e r ve rifica tio n a nd revision,
(1)
this approach demonstrates strong relationships between <Fe c and
e n viro n m e n ta l gradients in m an y areas o f the ocean.
fo r K d w ith E 0 set to 100%. M u ltip ly in g K d b y the actual sam pling
depth then gives C (dimensionless), w ith C < 4.6 corresponding to
irra d ia n ce levels > 1 % [39]. F o r data collected p rio r to 2002
M aterials and Methods
(Massachusetts Bay), SeaW IFS 9 k m zeu products were used fo r
ca lcu la tin g K d a nd subsequently
Data com pilation
FRRF measurements
A com prehensive assessment o f the v a ria b ility in <Fec fro m
F R R fluorescence transients were e ith e r measured in situ o r on
discrete samples o n -b o a rd using F A S T tracka I o r F A S T tracka I I
published lite ra tu re and previously unpublished data was p e r­
form ed. W e b o f Science and J S T O R search engines were used to
retrieve published data on coin cid e n t F R R fluorescence-based
fluorom eters w ith F A S T act systems (Chelsea T echnologies G rou p ,
L td ., W est M olesey, U K ), F IR e benchtop instrum ents (Satlantic,
LP, H a lifa x , Canada) o r a F R R Dlvmg Flash flu o ro m e te r (K im o to
E T R s and carbon fix a tio n rates fro m m arin e habitats, yie ld in g 17
studies. H ow ever, o n ly 7 o f these studies rep o rte d key e n viro n ­
m ental variables in a d d itio n to
c o r both E T R s and C 0 2-fixa tio n
E le ctric C o., L T d ., Osaka, Japan) (see T a b le 1). F R R fluorom eters
rates (resem bling e ith e r N P P o r G PP depending on the in cu b a tio n
were ro u tin e ly p ro g ra m m e d to generate a standard p ro to c o l w ith
lengths a nd g ro w th conditions), fro m w h ich <FeC co u ld be
calculated. Previously unpublished data corresponding to p a rallel
E T R and C 0 2 fix a tio n measurements fro m an a d d itio n a l 7 fie ld
5 0 -1 0 0 single tu rn o ve r (ST) saturation flashlets o f 1.1 -3 .3 ps
d u ra tio n a t 1 -3 .6 ps intervals [18,40]. Each in d u c tio n curve was
separated b y ~ 1 0 ms. T o increase signal to noise, betw een 5 and
160 sequential in d u c tio n curves were averaged p e r acquisition.
cam paigns in 20 0 4-2 0 1 1 , some o f w h ich were undertaken as p a rt
o f P R O T O O L (h ttp ://w w w .p ro to o l-p ro je c t.e u /), were also in ­
T h e biophysical m odel o f K o lb e r et al. [41] was fitte d to all
fluorescence transients to derive the in itia l fluorescence (F¿¡ and
m a xim a l fluorescence (Fm) yields measured in the dark, the
cluded (Table 1). T og e th e r, these data sets in clu d e d ten research
cruises and fo u r tim e series studies covering a range o f d iffe re n t
geographical areas (Fig. 1), in c lu d in g the tem perate, tro p ica l and
m in im a l (Fo’), steady state (F’) and m a xim a l (Fm’) fluorescence
subtropical A tla n tic O cean ( A M T 6 , A M T 11, A M T 15), Massa­
chusetts Bay (USA), B e d fo rd Basin (Canada), A ria ke Bay (Japan),
yie ld measured u n d er a m b ie n t irradiance, as w e ll as the fu n ction a l
absorption cross section o f photosystem I I (PSII) in the d a rk (ffpsu)
the C e ltic and Iris h Sea (D246, JR 9 8 ), the N o rth Sea
(C E N D 0 8 11/P R O T O O L , G u lf o f F in la n d (in clu ding S U P R E ­
M O 11/P R O T O O L ) , the B a ltic Sea ( S Y N T A X 2 0 1 0 /P R O ­
T O O L ) , U K and European shelf waters ( D 3 6 6 /P R O T O O L )
and lig h t (opsii ) (in units o f A 2 q u a n ta - 1 ). F or m ost studies, the
p hotosynthetic electron transfer rate th ro u g h P S II (units o f m o l e(mg chia)-
h - ) [42,43] was calculated as:
and the Pacific O cean (B IO S O P E ).
E T R = E x G psn
A com prehensive data m a trix w ith 333 d iffe re n t samples and
th e ir corresponding physico-chem ical and m eth odological v a ri­
F '
x n P S ii X - T 7 X
<S>R C
X
2.43
x
IO “
5
(2)
ables was created. Physico-chem ical variables in clu d e d salinity,
w here E is lig h t intensity, npsn the ra tio o f fu n ctio n a l P S II reaction
tem perature, n u trie n t concentrations ( N 0 3- and P 0 43 - ), the
diffuse v e rtica l a tte nu a tio n coefficient (Kd) o f p h o to syn th e tica lly
centres to ch lo ro p h y ll (in units o f m o l R C II (m ol chia)"1), @pc aa
assumed constant o f 1 electron yielded fro m each reaction centre
I I (R C II) charge separation and 2.43 • IO " 5 is the fa cto r th a t
active ra d ia tio n (PAR), o p tica l depth (Q and ch lo ro p h y ll a (chia),
PLOS ONE I www.plosone.org
3
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
♦
Bedford Basin
O
AM T 6
I
@
A M T 11
*
•
AM T 15
^
60°N
I
I
30°N
□
Pacific B10S0PE 2
o
Ariake Bay
♦
Massachusetts Bay
0
G ulf o f Finland
A
I
A
I
A
V
.
V
Baltic Sea SYNTAX2010
UK-OA D366
North Sea CEND0811
Celtic Sea D246
Celtic Sea JR98
9 0 °W
9 0 °E
Figure 1. D ata sets used in th e m eta-analysis. G u lf o f F in la n d in c lu d e s b o th th e S U PREM O 2011 a n d th e R aateoja e t al. [29] s tu d y (See T a b le 1 fo r
d e ta ils).
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 5 8 1 3 7 .g 0 0 1
made fo llo w in g b rie f d a rk exposure. C onsequently, u n d er
circumstances w here ra p id reversal o f certain com ponents o f
N P Q occurs d u rin g the d a rk m easurements, F q /F - f m ay be
overestim ated p o te n tia lly causing overestimates o f E T R evaluated
using Eqn. (2) b y up to 30% in p h yto p la n kto n cultures [ 8 ].
A p a rt fro m the b la n k co rre ctio n o f the absolute fluorescence
yields (see above and [45]), the accuracy o f the E T R also depends
on h o w variable some assumed ‘constants’ are and h o w w ell
certain corrections are applied; specifically, (1) nPsn [46], (2) the
spectral co rre ctio n o f o PSn, and (3) differences between ET R -based
and C 0 2-based values o f lig h t harvesting efficiency (a) and
m a x im u m photosynthesis rates (Pmax). F irstly, nPsn is k n o w n to
v a ry between taxa and e n viro n m e n ta l conditions b y up to a fa cto r
o f 5 [ 8 ] b u t is ra re ly m easured in the context o f FRR-based
p ro d u c tiv ity studies. In fact, o f the studies used here o n ly M o o re et
al. [11] and Suggett & Forget (unpubl.) used d irect measurements
accounts fo r the conversion o f Á 2 q u a n tu m " 1 to m 2 (m ol R C II) ’ 1,
m o l chi« to m g chi«, seconds to hours and p m o l quanta to m o l
quanta [13,29]. M easurem ents o f <Jpsn account fo r transient n o n ­
p h o to ch e m ica l quenching in the antenna bed as a result o f
exposure to transient lig h t [44], and thus, values o f o PSI/ were
ty p ic a lly taken fro m the F R R f d a rk cham ber to increase signal to
noise.
T h e P S II efficiency factor, te rm e d F q’/ F / (was calculated as
(Em’- F ) / ( E m’- F 0) either fro m fluorescence emissions measured
sequentially on d a rk acclim ated samples and then u n d e r actinic
lig h t, o r estimated as the difference in the apparent
p h o to ch e m ica l efficiency between the F R R lig h t and
P S II
dark
cham ber quasi-sim ultaneously, as in Suggett et al. [25]. In this
case, no b la n k co rre ctio n to the fluorescence yields is req u ire d
because any c o n trib u tio n o f b ackground fluorescence (to F \ F q o r
F m)
effectively
cancels
between
lig h t
and
d a rk
ch a m b e rs/
o f npsn- T h e m a jo rity o f the o th e r studies assumed values o f 0.002
and 0.003 m o l R C II (m ol chia) 1 fo r populations do m in a te d by
eukaryotes and prokaryotes, respectively [47], o r calculated nPsn
using a new ly developed a lg o rith m , w h ic h w ill also have associated
caveats [7]. In evaluating the use o f this assumed constant nPsn in
some o f o u r data sets, we com pared @ec derived w ith constant
rtpsu to <7C/, based on measured nPs n {see discussion). W e re tu rn to
the issue o f spectral corrections in the section “ m a tch in g E T R s
w ith C -uptake” .
A lth o u g h the F R R f approach provides a general estimate o f a
conditions [25,44], F o r tw o studies [25,28], the electron tran sp o rt
rate was evaluated using the equivalent equation:
E T R = E x o p s ii x t ip s ii x
F '
—^-7
i m
x
F
-E
-
x %
x 2.43 x 10
5
(3)
i y
w here values o f F v/ F m and (Jpsn are measured in the d a rk o r
assumed d a rk values based on measurements fro m deeper in the
w a te r colum n, th a t is, fro m depths w here E < E K and w here n o n ­
and Pmax, the lig h t saturation p o in t (EK) fo r the E T R m ay be lo w e r
th a n th a t fro m 14C uptake because of, fo r exam ple, electron
consum ing processes [4 8 -5 0 ]. T h e la tte r can cause the tu rn o v e r
tim e fo r Q A to decouple fro m th a t o f the w hole chain P S II
tu rn o ve r, so th a t the E K fo r the E T R m ay n o t be w h o lly in d icative
o f w here lig h t is lim itin g o r saturating fo r C 0 2 uptake.
p h o to ch e m ica l q uenching can be assumed to be negligible [25]. In
the la tte r case, the influence o f b o th p h o to ch e m ica l and n o n ­
p h o to ch e m ica l quenching are a ll accounted fo r b y changes in F q /
F m\ T h is slightly alternative approach was em ployed to enable
E T R s to be estim ated in the absence o f a ’d a rk ch a m b e r’ , and
consequently, corresponding lig h t and d a rk acclim ated samples
fro m all m easurem ent depths, w h ic h w o u ld be req u ire d in o rd e r to
14C 02 fixation rates
apply Eq. 2. B o th , Eqns. la n d 2, appear to re tu rn consistent
C 0 2 fix a tio n was m easured by e ith e r in situ incubations [29],
sim ulated in situ incubations [27,28,30,31] o r photosynthesis versus
irra d ia n ce (PE) relationships [11,25,26] in a ‘p h o to syn th e tro n ’
estimates fo r quenching [ 8 ], and hence, E T R . I t should fu rth e r be
noted th a t d e riv a tio n o f F q’/ F / requires a m easurem ent to be
PLOS ONE I www.plosone.org
4
March 2013 I Volume 8 I Issue 3 I e58137
Electron Requirement for Carbon Fixation
instantaneous lig h t was standardised b y n o rm a liz in g E relative to
the saturating lig h t intensity, E k , as d eterm ined fro m 1 4 C-specific
PE curves, i.e. E :E K (dimensionless). In this way, E can be
a ccording to Lewis and S m ith [51] o r an eq u iva le nt th e re o f (see
T a b le 1 fo r details). C 0 2 fix a tio n in A ria ke Bay (Japan) was
measured using the stable isotope 1 3 C -labelled N a H 1 3 C 0 3 [31].
In c u b a tio n lengths va ried between the d iffe re n t studies, w ith the
considered relative to the lig h t h isto ry to w h ich cells are acclim ated
h a n d lin g [8,18]. M o re o ve r, the m ethods used to determ ine C 0 2
fix a tio n d iffered considerably between studies (Table 1). Some o f
[52] p ro v id in g in fo rm a tio n as to w h e th er the values o f <&ec
correspond to lig h t lim ite d photosynthesis (E:EK < 1 ) o r lig h t
saturated photosynthesis (E:EK > 1 ). N ote, however, th a t E comes
fro m in situ P A R measurements, w h ile E k was usually based on
measurements m ade in the la b o ra to ry. In this case, the spectral
q u a lity o f E and E k m ay d iffe r and values o f E / E k ratios fro m
d iffe re n t studies m ust be treated w ith caution.
A ll C 0 2 fix a tio n rates (in m g C L 1 h *) were norm alised to the
corresponding ch i a c o n ce ntra tio n to yie ld C 0 2 uptake rates as m ol
the m ost recent studies in the B a ltic Sea (S Y N T A X 2 0 1 0 ) and
C0
2
N o rth Sea (C E N D 0 8 1 1 ) fo llo w e d recom m endations o f Suggett et
al. [ 8 ] and measured 14C uptake b y p la cin g the radioactive sample
d ire c tly in the cuvette h o ld e r o f the F A S T a c t flu o ro m e ter. T h is
C0
2
vast m a jo rity in c u b a tin g fo r a few ( 1 M ) hours and thus ca p tu rin g
p ro d u c tiv ity somewhere between G PP and N P P [19,20].
Matching ETRs w ith C-uptake
Id e ally, measurements o f p hotosynthetic carbon fix a tio n and
E T R should be m ade sim ultaneously on the exact same sample to
reduce errors arising fro m differences in sample trea tm e nt and
(mg chia)
1
h
*; thus values o f the <&e c (in m o l electrons m ol
’ ) were d e term ined as
<$eC = E T R /C 0 2 u p ta k e r a te
(4)
simultaneous in c u b a tio n technique avoided discrepancies in the
in te n sity and spectral q u a lity o f the a ctin ic lig h t sources. In this
way, E T R a nd G PP were m easured fo r 1 h on the same sample at
in situ tem peratures and a t a lig h t in te n sity corresponding to either
G ive n the large a rra y o f data sets a nd the various differences in
approach fo r d e te rm in in g b o th 14C uptake and F R R fluorescence
E T R s [8,18], we recognise th a t a m a jo r assum ption in h e re n t to
o u r analysis is th a t e n viro n m e n ta l influences o u tw eigh m eth o d o ­
lo g ica l influences on <£eC, b o th, w ith in and between studies.
h a lf o r tw ice the value o f E k (as d e term ined fro m F R R f ra p id lig h t
curves); these lig h t intensities relative to E K were chosen to yie ld a
measure o f <&ec corresponding to an irra d ia n ce fo r lig h t-lim ite d
and lig h t saturated photosynthesis.
Fortu n ate ly, a ll studies em ployed sim ila r F R R f protocols (above).
Even so, in fo rm a tio n on core variables associated w ith the E T R
determ inations were in itia lly in clu d e d in o u r database and
F o r m ost studies, 1 4 C-specific PE experim ents were p e rfo rm e d
on discrete w a te r samples w h ilst F R R data (and hence E T R s) were
d e term ined fro m in situ casts o r on deck (Table 1). In cu b a tio n
exam ined alongside the e n viro n m e n ta l variables to ve rify any role
lengths va ried between the d iffe re n t studies, w ith the vast m a jo rity
in c u b a tin g fo r a few (1-4) hours and thus ca p tu rin g p ro d u c tiv ity
rates somewhere between G PP and N P P [19,20]. F o r this same
o f m ethod u pon a p parent v a ria b ility in Û>e c (see “ statistical
ap p ro a ch ” section). N o te th a t the ‘m eth o d o lo g ica l’ data across
reason, a d h erin g to strict d e finitions o f N P P and G PP th ro u g h o u t
co rre ctio n o f Gpsn a pplied o r n o t applied); therefore, the available
in fo rm a tio n was converted in to a Boolean code w ith num bers one
studies
the m an u scrip t is n o t always possible. W e have therefore specified
N P P o r G PP w here possible b u t otherwise use the term s C 0 2
fix a tio n o r p rim a ry p ro d u c tiv ity . In situ F R R data were com pared
is
categorical
ra th e r
th a n
continuous,
(e.g.
spectral
and zero representing use a nd non-use o f a p a rtic u la r m ethod,
respectively. In total, 3 m eth odological variables were u ltim a te ly
to the PE data fro m the same depth as the discrete w a te r sample.
F o r on-deck based E T R measurements d u rin g S U P R E M O ll,
in clu d e d in the in itia l data set: nPSi i assumed o r measured, spectral
co rre ctio n o f (Jpsii assumed o r measured, and E :E K > 1 o r
a ctin ic lig h t was p ro vid e d b y an external p ro g ra m m a b le lig h t
source. T h e lig h t in te n sity m easured d u rin g the F R R data
acquisition (used to calculate the E T R ) was then a pplied to the
1 4 C -PE e q uation to y ie ld a measure o f the instantaneous
14C
E :E k < 1 .
A t this p o in t it should also be noted th a t a p a rt fro m
e n viro n m e n ta l factors, differences in p h yto p la n kto n c o m m u n ity
uptake fo r m a tch in g w ith the E T R . F o r some studies, sim ulated in
situ 14C data were collected (corrected using 1 4 C -P E to yie ld ‘gross’
com position m ay also influence & t c- U n fo rtu n a te ly, ta xonom ic
data was n o t consistently available fo r the m a jo rity o f studies.
H ow ever, we assume th a t p h yto p la n kto n co m m u n ity com position
14C uptake [27,28] (Table 1). H ere, we adopted a sim ilar
approach b u t fu rth e r norm alised d a ily 14C uptake rates to h o u rly
w ill p a rtia lly refle ct e n viro n m e n ta l characteristics a nd some
influence o f c o m m u n ity co m p o sitio n on & ec w ill lik e ly be
rates based on knowledge o f the lig h t regim e.
im p lic itly accounted fo r
e n viro n m e n ta l variables.
D ire c t com parison o f the E T R s and
C uptake requires th a t
the spectral q u a lity o f the a ctin ic lig h t o f the F R R f and 14C
in c u b a to r is e ith e r equivalent o r corrected for. T h e spectral values
in
our
analyses
p u re ly
based
on
Statistical approach
o f gpsn (measured w ith a blue L E D ) also needed to be scaled to the
lig h t q u a lity o f the a ctin ic source used fo r the 14C incubations [40].
In m ost cases, in situ F R R values o f ffpsu and the 14C a ctin ic lig h t
source were b o th spectrally corrected to m atch the spectral q u a lity
M a n y o f the fo llo w in g analyses were ca rrie d o u t on b o th the
entire dataset o r on in d iv id u a l subsets thereof, w h ich , fo r exam ple,
represent d iffe re n t oceanic regions. A lth o u g h the m a jo rity o f o u r
samples were collected in the A tla n tic O cean and adjacent shelf
corresponding to the sample depth [40]. In cases w here b o th
F R R - and 1 4 C - PE curves were m easured on discrete samples,
data were spectrally corrected fo llo w in g M o o re et al. [11]. F o r the
waters w h ile o th er regions (e.g. Pacific, In d ia n O cean, and
M e d ite rra n e a n Sea) are u n d e rre p re se n te d /n o t represented at all,
we still use the te rm ’glo b a l’ fo r analyses ca rrie d o u t on the dataset
studies th a t d id n o t e m ploy a spectral co rre ctio n (Table 1) we
as a whole.
Spearm an R a n k O rd e r C o rre la tio n analysis on the in d iv id u a l
assumed a constant fa cto r o f dpSn/ \ J b [11,31] and GPsn/ 1.5
(Prásil et al. unpubl.) based on a p p ro xim a te values fro m the o ther
studies fo r the w a te r types in question.
data sets (i.e. samples grouped b y study) were used to id e n tify key
variables th a t m ay be associated w ith <J>e c. C orrelations, evaluated
T a k in g in to account the lig h t h isto ry o f samples fro m d iffe re n t
in SPSS 15.0 (SPSS In c., C hicago, IL , U S A ) were considered
studies was the greatest challenge in c o m p ilin g the database due to
considerable inconsistencies in the a v a ila b ility and q u a lity o f lig h t
data. T hus, irradiances were expressed as o p tica l depths, and
significant w h e n j&<0.05. These correlations were ca rrie d o u t i) on
the in d iv id u a l data sets (i.e. samples grouped b y study), ii) on the
global dataset, iii) on studies pooled a ccording to regions (e.g.
PLOS ONE I www.plosone.org
5
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
N o rth Sea, B a ltic Sea, A tla n tic O cean etc.) and iv) a cco rd in g to
shelf/oceanic waters, thus p ro v id in g an overview o f w h ich
Thus, once a no n -sig n ifica n t test result was o b tained (fi>0.005),
samples below th a t s im ila rity level were no longer p a rtitio n e d in to
variables m ay be im p o rta n t. A ll data were then com bined in to
one large database to ca rry o u t a ll o ther statistical analyses using
clusters and co u ld be regarded as homogeneous [53].
6
A ll data were then re-grouped a ccording to the results o f the
cluster analysis and S IM P R O F test. T h e P R IM E R -B E S T m atch
[53], unless noted
p e rm u ta tio n test was then used to id e n tify variables a nd variable
n o n -p a ram e tric m u ltiva ria te techniques in P R IM E R -E version
(P R IM E R -E , L td . Ivyb rid g e , D evon, U K )
otherwise.
com binations th a t best “ e xp la in ” the v a ria b ility in
c [53]. T h a t
In te r-c o rre la te d a nd right-skew ed physico-chem ical variables
(e.g. salinity, tem perature, chirr, N 0 3 —, and P 0 4 3 ) were
is, the a lg o rith m ra n d o m ly perm utes a resemblance m a trix
generated fro m & ec (based on all possible pair-w ise sample
id e n tifie d using D ra ftsm a n plots and then square-root transform ed
to stabilise the variance and ensure th a t Euclidean distance could
be used as an a p p ro p ria te s im ila rity measure (see below). T o
account fo r differences in scales and units between d iffe re n t
com binations) relative to a resemblance m a trix generated fro m
subsets o f the e n viro n m e n ta l data m a trix searching fo r h ig h ran k
correlations
between
the
tw o
and
generating
a
co rre la tio n
coefficient (p). Repeated (99) p erm utations o f ra n d o m ly ordered
e n viro n m e n ta l data fo llo w to test the significance o f the results at a
variables, the la tte r were n o rm a lize d b y subtracting the m ean fro m
each e n try o f a single variable and d iv id in g it b y the va riab le ’ s
standard deviation.
level o f j&CO.Ol [53],
N o n -m e tric M u ltid im e n s io n a l Scaling (nM D S ) was used as a
O n e o f the m a in goals o f this meta-analysis was to generate
algorithm s to p re d ic t
c fro m e n viro n m e n ta l variables fo r
means to m ap e n viro n m e n ta l characteristics o f samples in a lo w ­
dim ensional space based on a tria n g u la r resemblance m a trix th a t
specific regions. T he re fore , m athem atical relationships between
the e n viro n m e n ta l data and & e>c were pro d u ce d fo r each cluster
was created b y ca lcu la tin g E u clidean distances between every
th a t contained
possible p a ir o f samples. H ence, E u clidean distances between
samples represented the dissim ilarities in the suite o f th e ir physico­
chem ical properties. P rin cip a l C o m p o n e n t Analysis (PCA) was
regression (M L R ). O n ly those variables and variable com binations
c a cco rd in g to the
th a t were significandy correlated w ith
at least 5 data points
using m u ltip le
lin e a r
P R IM E R -B E S T -te s t were entered in to the M L R in SPPS.
then used to id e n tify variables a ccounting fo r the differences
between samples. V ariables in itia lly in clu d e d in the P C A were
salinity, ch i a, N 0 3 , P 0 4 3 , tem perature, K¿, and C, as w e ll as a
B o o le a n -m a trix o f m ethodological differences w ith regard to nPsn,
Spatial and tem poral variability in < P e C
ap sii and E :E K (as described above, T a b le 1).
In clu sio n o f the m eth odological and lo ca tio n variables (latitude,
M e a n values fo r & ec in all b u t fo u r studies were < 1 0 m o l e
(m ol C) *, resulting in a global m ean ( ± standard deviation) o f
lo n g itu de (absolute values) and J u lia n day) usually increased
dissim ilarities, i.e. Euclidean distances, between samples o f
d iffe re n t studies com pared to analyses fro m w h ich m ethodological
theoretical ra tio o f 5 m o l e
(m ol C) 1 (see discussion) were
observed in the G u lf o f F in la n d 2000 and in p a rt o f the A M T 15
Results
10.9± 6.91 m o l e-
(m ol C )- 1 . Values o f 0 eC less th a n the
and lo ca tio n variables h ad been excluded. Because the ‘m eth o d ­
ological choices’, in p a rticu la r, ca n n ot be effectively in co rp o ra ted
in to p re d ictive algorithm s fo r <&e c, the results we show in the m ain
data. V a r ia b ility o f í>e>c w ith in a nd between in d iv id u a l studies was
te xt here are based on PCAs w ith o u t m ethodological and lo ca tio n
variables. Nevertheless, the results o f the P C A in c lu d in g these
m eth odological and lo ca tio n variables have been in clu d e d in
A p p e n d ix S I (Fig. S I). O n ly those variables w ith the highest
largest in
considerable, w ith a to ta l range o f 1.15-54.2 m o l e- (m ol C ) - 1 fo r
a ll studies co m b in e d (Fig. 2). W ith in -s tu d y va ria tio n o f & e>c was
the
Pacific
O cean
(7.9-54.2 m o l e
(m ol
C)
*),
Massachusetts Bay (8.5-50.1 m o l e- (m ol C )- 1 ), a nd the A M T
15 data (1.1-28.2 m o l e
(m ol C) *); in contrast, least w ith in -
study variance was ty p ica lly observed fo r tim e series’ at a single
eigenvectors were in clu d e d in any fu rth e r analysis to assess the
v a ria b ility in & t cB o th n M D S and P C A generate lo w dim ensional ordinations.
lo ca tio n (Ariake Bay: 5 .1 -5 .7 m o l e (m ol C) , B e d fo rd Basin:
3 .6 -1 0 .3 m o l e (m ol C) *, and the G u lf o f F in la n d 2000: 2.0—
9.4 m o l e- (m ol C )- 1 ). As there were no d istin ct differences in the
H e re we o n ly show the n M D S plots, w h ic h m atched the P C A plots
well, because n M D S better preserves the distances between
samples w h e n m ap p in g them onto a 2D o r 3D space [53]. In
n u m b e r a nd types o f ffpsiispec and nPSn corrections between the
tim e series studies and the o th er cruises, it w o u ld appear th a t
v a ria b ility o f <&ec is generally greater spatially th a n te m p o ra lly
a d d itio n n M D S provides a measure, the stress value, o f h o w w ell
w ith in the in clu d e d locations. T h e tim e series studies in clu d e d here
the lo w dim ensional ord in a tio n s represent the distances between
samples. I n all cases the stress value o f the n M D S was considerably
lo w e r in the 3D o rd in a tio n relative to the 2D o rd in a tio n . T hus, the
were
3D-im ages are presented here w here the in d iv id u a l planes (x-y, x-
short
d u ra tio n
(1.5-7
months),
how ever,
Spearm an R a n k O d e r C o rre la tio n s co u ld be fo u n d between
<&e c an d every e n viro n m e n ta l variable in clu d e d in the study, albeit
to va ry in g degrees and depending on h o w data were grouped. O n
z, y-z) are separate panels.
Because e n viro n m e n ta l factors showed considerable spatial and
te m p o ra l v a ria tio n , w h ich , in tu rn , influence physiological
a global scale, i.e. co m b in in g the entire data set, <&e c exh ib ite d
responses o f p h yto p la n kto n and subsequendy í>e>c to va ryin g
significant positive correlations w ith J u lia n day (i.e. tim e/season)
degrees, hie ra rch ica l agglom erative cluster analysis and a sim ila r­
ity p ro file (S IM P R O F ) test were used to fin d and define groups o f
samples w ith sim ila r physico-chem ical properties [53]. S IM P R O F
and salinity, w h ile significant negative correlations existed w ith
la titu d e, lo ngitude, c h k concentrations K d and Ç (Table 2). These
correlations explained at least 12% o f the variance in a ll cases. T o
tests w ere used as a stopping rule o f the cluster analysis, so th a t
successive p a rtitio n s along the branches o f the den dro g ra m are
consider i f the global data p o o l m ay obscure regional-scale trends,
correlations were also ca rrie d o u t (i) on the in d iv id u a l studies and
o n ly p e rm itte d i f the n u ll hypothesis o f ‘no structure between
samples’ was rejected. T o reduce the n u m b e r o f clusters to a
(ii) b y p o o lin g studies representative o f p a rtic u la r regions, such as,
the B a ltic Sea (in clu ding the G u lf o f Finland), the A d a n tic Ocean
manageable size a nd to ensure th a t a sufficient n u m b e r o f samples
large enough fo r a lg o rith m developm ent were in clu d e d in each
(all A M T cruises com bined) and b y co m b in in g data fro m shelf and
oceanic waters, respectively.
cluster, the j6 -value fo r the S IM P E R O F test was reduced to 0.005.
PLOS ONE I www.plosone.org
o f relative ly
te m p o ra l v a ria b ility m ay fu rth e r increase i f lo n g -te rm studies
(m u ltip le years) are included.
6
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
corresponded to a surface w a te r lens in the H N L C and H u m b o ld t
u p w e llin g region o f the Pacific Ocean. F o r the o th e r A tla n tic
studies, A M T
6
and 11, i f ^ also declined w ith increasing N 0
3
a n d /o r P 0 43 - , b u t as the depth o f the surface m ixe d layer a n d /o r
O
Ö
n itra clin e va ried between stations, the relatio n sh ip between depth
and i f c was n o t linear.
40
E
N egative correlations between i f c and 'Ç fo r A M T 1 5 , the C eltic
o
E
Sea (JR98), the Pacific O cean a nd the G u lf o f F in la n d in dicated
th a t i f ,c often increased towards depths o f greater lig h t a v a ila b ility
in surface waters o r w ith d e clin in g K¿ values fro m coastal to
S
were also fo u n d b u t o n ly in B a ltic Sea a nd shelf waters.
offshore regions. N egative correlations o f & ec w ith depth, A /a n d Ç
Regional differences in environmental conditions
The
in itia l
correlative
exercise
fo r
each
separate
study
dem onstrated th a t the relationships between i f c a n d e n viro n m e n t
are dependent u p o n ho w data w ith in and between data sets are
grouped; therefore ‘choice’ o f g ro u p in g w ill in e vita b ly influence
the outcom e o f e m p irica l algorithm s generated to p re d ic t $>e c
fro m physico-chem ical variables. A m a jo r objective o f this study
(S)
was to id e n tify e n viro n m e n ta l predictors o f i f
therefore P C A in
co m b in a tio n w ith cluster analysis was subsequently used to
Figure 2. V a ria b ility in the electron req uirem ent o f carbon
fixation ( 0 eci d erived fro m corresponding FRRf-ETR and 14Cprim ary p ro du ctivity m easurem ents. Boxes re p re s e n t th e m e d ia n ,
id e n tify
the p rin c ip a l differences in
1
)
e n viro n m e n ta l c o n d itio n
between sites regardless o f the study to w h ich they belonged and
2 ) to fo rm clusters o f sites w ith sim ilar e n viro n m e n ta l conditions,
0.25 a n d 0.75 q u a rtile , w h is k e rs are th e 1.5 in te rq u a rtile ra n g e . O u tlie rs
are in d ic a te d b y o p e n circles. T h e d a sh e d g re y lin e is th e th e o re tic a l
re fe re n c e ra tio o f 4 m o l e ~ [m o l C U 1. A M T = A tla n tic M e rid io n a l
w h ich co u ld then be analysed fu rth e r w ith
respect to th e ir
T ra n sects, CS = C e ltic Sea, NS = N o rth Sea, GoF = G u lf o f F in la n d 2 000
(tim e s e rie s ), U K -O A = UK O ce a n A c id ific a tio n c ru is e , M A =
M a ssa ch u se tts Bay (tim e series). SYN TAX2010 is a B a ltic Sea cruise,
association w ith i f c.The first three p rin c ip a l com ponents o f the
G o F 2 0 1 1 is th e SUPREM O 2011 s tu d y a n d th e P acific O cean s tu d y is th e
BIOSOPE- c ru ise to th e S o u th e a s t P acific (see T a b le 1, F ig u re 1 fo r
d e ta ils).
Tem p e ra tu re, chia and K j had the highest coefficients fo r the
lin e a r co m b in a tio n o f variables co m p risin g P C I, i.e. they were
d o i:1 0 .1 3 7 1 /jo u r n a l.p o n e .0 0 5 8 1 3 7 .g 0 0 2
associated w ith the separation o f samples along P C I (Table 3).
P C A co m bined accounted fo r 8 6 % o f the cu m u la tive v a ria tio n in
e n viro n m e n ta l variables (P C I 47% , PC2 24% and PC3 15%).
S alinity, N 0 3_ a nd P 0 43 - diffe re n tia te d samples along PC2,
w h ile a single variable, Ç, had the highest Eigenvectors o f PC3.
C luster analysis in co m b in a tio n w ith a S IM P R O F test
A t the level o f the in d iv id u a l study, d iffe re n t en viro n m e n ta l
variables showed v a ryin g degrees o f co rre la tio n depending on the
generated 15 sig n ifica n tly d iffe re n t clusters (ƒ><().005) labelled
region. M u ltip le notable trends were evident between <PfC,
sam pling depth, L j, 'Ç and n u trie n t a va ila b ility, in clu d in g : 1 )
changes o f <Pf C w ith depth, w h ich were observed d u rin g A M T 1 5 ,
alp h abetically fro m a-o (/><().005) across a range o f Euclidean
distances (representing dissim ilarities between samples) fro m 0 —
in the C e ltic Sea, the N o rth Sea (N S -C E N D 0 8 1 1) and the G u lf o f
4.4; these clusters often overlapped in the n M D S o rd in a tio n o f the
F in la n d /B a ltic Sea; 2) a decline in & r c w ith increasing K j d u rin g
A M T 6 and in the B altic Sea, and w ith increasing ç d u rin g
Euclidean distance m a trix derived fro m the enviro n m e n ta l
variables, in d ic a tin g th a t there existed sim ilarities in some o f the
A M T 15, in the C e ltic Sea, Pacific O cean and in the G u lf o f
F in la n d /B a ltic Sea; and 3) a change in & r c w ith n u trie n t
concentrations, d u rin g the A M T cruises, one o f the C eltic Sea
e n viro n m e n ta l conditions between samples fro m d iffe re n t studies
(Table 4, Fig. 4).
cruises (JR98) a nd in the G u lf o f F in la n d /B a ltic Sea. In the B altic
Sea (S Y N T A X 2 0 1 0 ) a nd B e d fo rd Basin significant correlations
biogeographic regions a n d /o r seasonal (i.e. tem perature depen­
existed between & ec a nd tem perature and salinity, respectively.
N o c o rre la tio n o f i f , c w ith co m m o n e n viro n m e n ta l variables were
fo u n d in Massachusetts Bay o r d u rin g the U K - O A cruise. N ote
masses (Table 4). A ll the samples collected in the B altic Sea and
G u lf o f F in la n d fe ll in to b io g eographically distin ct clusters (b, c, f, g
Some
of
the
resulting
clusters
corresponded
to
obvious
dent) groupings, w h ile others represent m ore o r less d istin ct w ater
also, th a t depth-dependent trends in <X>r c co u ld o n ly be assessed
and h) characterised b y lo w salinities (Fig. 5). T h e fo u r G u lf o f
F in la n d clusters (b, c, g, h) clearly represented te m p o ra l changes in
w here m u ltip le depths h ad been sampled at each station across
e n viro n m e n ta l
large p ro p o rtio n s o f the cruise tra n s e c t/tim e series, such as in the
open ocean studies w here data were available up to a depth o f
~ 2 0 0 m (e.g. A M T cruises, Pacific O cean, C eltic SeaJR98) o r the
characterised b y extrem ely lo w tem peratures d u rin g late w in te r
(SETPREM O 11 cruise) coupled w ith h ig h n u trie n t a va ila b ility.
G u lf o f F in la n d ( S U P R E M O ll) studies w here up to fo u r depths
spring cluster c w ith still relative ly lo w te m p e ra tu re s(< 5 UC) and
clusters g and h, w h ic h co n tain all the sum m er and a u tum n
conditions
w ith
samples
in
cluster
b
being
L o w tem perature and h ig h n utrients set this cluster a part fro m
were sampled across the euphotic zone at each station. T hus, a
lack o f relationship between i f , c and depth m ay sim ply reflect
samples characterized b y w a rm tem peratures ( ~ 15 UC), lo w N 0
3
lim ite d sam pling depths o r, in shallow waters w ith ra p id ve rtica l
a va ila b ility and h ig h Kd and t values. Samples fro m the B altic Sea
m ix in g , a cclim a tion to an average w a te r co lu m n irradiance.
A notable feature fo r the Pacific and A tla n tic transects as w e ll as
p ro p e r (cluster f) were characterised b y alm ost undetectable
n u trie n t concentrations. O th e r clusters w ith samples representative
the C eltic Sea (JR 98, data n o t shown) was a p ro n o u n ce d increase
o f d istin ct regions include the N o rth Sea cluster i and cluster k
o f i f c surface waters w ith lo w N 0 3 a n d /o r P 0 4 3 a va ila b ility
(Fig. 3, T a b le 2). In fact, the highest i f c values across a ll studies
c o n ta in in g C eltic Sea samples a nd samples fro m the European
PLOS ONE I www.plosone.org
shelf edge collected d u rin g A M T 6 . L ike in the B a ltic Sea, deplete
7
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
T a b le 2 . Spearman Rank Order Correlation Coefficients for correlations between <PeC and environm ental variables.
Lat
Lon
JD
D ep th
Tem p
Sal
N03
P 0 43
Chia
Kd
Ç
All Studies
-0 .2 7 2
-0 .4 5 0
0.297
-
-
0.226
-
-
-0 .1 3 0
-0 .2 4 4
-0 .1 2 3
Shelf
-0.431
-0 .5 4 6
0.214
0.149
0.376
0.229
0.186
- 0 .1 36a
-0.511
-0 .1 5 5
Oceanic
-0 .3 2 4
-0 .3 2 0
- 0.201
-
-
-
-0 .2 4 3
- 0 .1 67a
-
-
-
0.250
0.276
-0.361
-0 .4 1 7
-0 .1 75a
Baltic co m b in e d f
'
0-347
0.530
-0 .3 3 7
0.271
-0 .4 3 8
0.276
0.269
0.320
-0 .5 6 2
-0 .5 6 9
AMT 6
0.322
-
0.322
-
0.520
-
-0 .3 7 4
-0 .4 0 6
-0 .5 7 7
-0 .4 1 5
-
AMT 11
-0 .3 4 4
-0.431
0.344
-
-
0.329
-
-0 .3 3 8
-
-
-
AMT 15
-
-
-
-0 .7 0 9
-
-
-0 .7 6 5
-
-0.681
-
-0 .7 5 6
CS-D246
.
.
.
.
.
.
.
CS-JR98
-
-
-
-0 .5 6 4
-
-
-0.391
-
-
-
-0 .4 8 2
CS-DS46+JR98
-
-
0.377
-0 .6 1 4
0.423
-
-
-
-0 .3 7 4
-
-0 .4 1 6
NS-CEND0811
-
-
-
0.616
-
-
-
-
-
-
-
UK-OA D366
.
.
.
.
.
.
.
-
0.568
-
-
-
-
-
-
-0 .6 5 3
Studies combined
AMT combined
- 0.212
.
.
PO-BIOSOPE
-0 .4 8 2
.
.
SYNTAX2010
-
G0 F2OOO
n.a.
n.a.
SUPREM011
-
-
-
-0 .6 4 5
-
-
-0 .4 9 4
-
-
-
GoF +SUPREM011
0.352
0.752
-0 .7 3 7
—0.310a
-0 .6 8 3
0.668
0.582
0.586
-0 .4 5 2
-0 .7 0 5
-0 .6 8 4
Bedford Basin
n.a.
n.a.
-
n.a.
-
0.582
-
-
-
-
-
MA Bay
.
_
_
_
_
_
_
-
.
n.a.
.
Values in bold or normal fo n t indicate significant correlations where p<0.01 and p<0.05, respectively.
JD is Julian Day. f denotes Baltic proper and the Gulf o f Finland com bined. - non-significant correlations (p>0.06). b denotes correlations w ith 0.05>p>0.06.
doi:10.1371 /journal.pone.0058137.t002
n u trie n t concentrations in cluster k sets this cluster a part fro m
cluster i.
w e ll as extrem ely lo w ch lo ro p h y ll a nd n u trie n t concentrations fell
in to clusters m and o. W h ile cluster m contained samples fro m
Samples fro m B e d fo rd Basin fe ll in to tw o clusters: cluster d
in term ediate depths collected d u rin g A M T 6 and A M T 11 and
c o n ta in in g samples collected fro m m id -M a rc h to m id -M a y w hen
fro m the surface o f the South Pacific G yre (SPG) and H N L C
c h lo ro p h y ll concentrations increased and n u trie n t concentrations
region in the Pacific, cluster o was com prised o f surface samples
fro m the open ocean (all A M T cruises), central N o rth Sea and
and w a te r c la rity dro p p e d fro m previous levels th a t characterized
samples fro m cluster e, w h ich were collected in late w in te r
(February to m id -M a rc h ). Interestingly, cluster e also contained
alm ost all o f the Massachusetts B ay samples, some N o rth Sea
samples fro m fro n ta l regions as w e ll as A M T
6
and Pacific Ocean
C eltic Sea JR 9 8 ).
C learly, tem perature, salinity, ch lo ro p h yll, n u trie n t concentra­
tions and lig h t a v a ila b ility were the m ain e n viro n m e n ta l factors
responsible fo r the d istin ct g ro u p in g o f samples in to clusters. G iven
samples fro m the H u m b o ld t and Benguela u p w e llin g areas,
respectively. T h is represents sim ilarities in physico-chem ical
th a t cluster analysis in strongly stratified, off-shore waters resulted
properties o f these d iffe re n t w a te r masses ra th e r th a n biogeo-
and surface samples and due to the pron o u n ce d effects o f w ater
graphical regions. D u rin g late w in te r, salinity in the ice covered
B e d fo rd Basin was sim ila r to th a t in o ff shore waters, w h ile
p lo tte d the m ean <£f C, grouped a ccording to samples fro m the
c h lo ro p h y ll and n u trie n t concentrations as w e ll as o p tica l
properties m atched those o f u p w e llin g /fro n ta l regions; hence,
th e ir g ro u p in g together.
T h e re m a in in g clusters (j, 1, m , n, o) also co ntained samples fro m
a v a rie ty o f d iffe re n t cruises/regions. Samples collected fro m the
deep c h lo ro p h y ll m a x im u m (D C M ) in o ff shore regions d u rin g the
A M T cruises, the Pacific O cean cruise and the C eltic Sea (JR98)
fell
in to
one
cluster
0
, w h ich
was
characterized
by
high
tem peratures as w e ll as h ig h e r n u trie n t a va ila b ility and 'Ç relative
to the o ther offshore samples. C luster 1 contained samples fro m
in term ediate depths in tem perate waters on the European shelf
and the shelf edge, w h ich h ad relative ly lo w tem peratures. W h a t
set cluster 1 a part fro m cluster n, w h ich also co ntained samples
fro m the European shelf, was its overall greater o p tica l depth.
in d istin ct groupings corresponding to D C M , in te rm e d ia te depth
co lu m n stratifica tio n on lig h t and n u trie n t a va ila b ility, we also
surface m ixe d layer (S M L) a nd D C M against depth and N 0
3
fo r
each biogeographic pro vin ce sampled d u rin g the Pacific and A M T
cruises (Fig. 6 ). As such, distin ct differences in & eC existed between
the S M L and D C M samples fro m the Pacific and A M T 15 cruise,
w here 0 r c was m u ch h ig h e r in the S M L th a n at the D C M and the
increase in & r c coincided w ith a d ro p in n u trie n t a v a ila b ility o r
even d epletion o f n utrients in surface waters. D u rin g the A M T 6
and A M T 11 cruises, on the o th er hand, no such pron o u n ce d
differences in & eC and n u trie n t concentrations between S M L and
D C M was observed fo r the sampled locations in m ost o f the
biogeographic provinces.
In sum m ary, there existed distin ct groupings fo r m an y o f the
cruises
and
regions
based
on
differences
in
enviro n m e n ta l
gradients w ith in and between regions and w a te r masses. T h is also
O p e n ocean samples w ith h ig h w a te r c la rity a nd tem peratures, as
PLOS ONE I www.plosone.org
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
30
30
25
20
S-
100
150
NAG
EM
200
40
30
H
a- lo o
—
150
CZ
8
-
NAG
SAG
EM
100
150
200
EQ
EQ
Figure 3. Changes in th e electron re q uirem ent o f carbon fixation (<Pe,à and N 0 3 across 4 cruise transects. (A) and (E) Pacific Ocean
(BIOSOPE), (B) and (F) AMT 6, (C) and (G) AMT 11, and (D) and (Fl) AMT 15. Units o f <PeC (left panels) are in mol e~ (mol C F 1), N 03~ concentrations
(right-hand panels) are in pmol L_1. Dashed lines denote transitions between different biogeographical provinces, where SPG is the South Pacific
Gyre, FINLC FHigh Nutrient Low Chlorophyll areas, UPW denotes upwelling regions, AB is the Angola Basin, SAG South Atlantic, NAG the North Atlantic
Gyre, EM the Eastern Margin o ff Western Europe, and CZ is the Suptropical Convergence zone. Note, difference in scales on both axes and the colour
contours.
doi:10.1371/journal.pone.0058137.g003
confirm s th a t user specific differences in m eth o d o lo g y d id not
appear to have a systematic influence.
T a b le 3. Eigenvectors o f Principal C om ponent Analysis (PCA).
Relationships between environmental conditions and
PC3
®e,c
C lu ste ring all available data based on the in h e re n t e n v iro n ­
0.111
-0 .1 8 4
m en ta l characteristics dem onstrated th a t the dependence o f & e c
-0 .5 0 9
0.054
0.337
0.541
-0 .0 8 7
on e n viro n m e n ta l gradients cannot be resolved at the level o f the
in d iv id u a l studies. C luster analysis therefore enabled us to
p o 43~
0.399
0.491
- 0.020
Chia
0.464
0.232
0.020
Kd
0.424
0.373
-0.091
v a ria b ility o f & ec- P e rm u ta tio n tests conducted on the in d iv id u a l
clusters (i.e. clusters a -q , T ab le 4) indeed showed th a t often
Ç
0.001
0.023
-0 .9 7 3
m u ltip le variables co m bined were sig n ifica n tly correlated w ith & e c
V a ria b le
PC I
PC2
Temperature
-0 .4 7 6
Salinity
—0.325
NOF
objectively id e n tify h o w to p o o l data across the m ultidim e n sio n a l
e n viro n m e n ta l variable
(Table 4) to fu rth e r examine
(BES T, p < 0.05 o r ƒ><().01), and th a t d iffe re n t variable co m b in a ­
tions were d riv in g
c in d iffe re n t clusters and regions (Table 5).
Values in bold represent variables w ith the highest coefficients fo r each PC. Kd is
the vertical attenuation coefficient o f photosynthetically available radiation and
£ is optical depth.
doi:10.1371 /journal.pone.0058137.t003
PLOS ONE I www.plosone.org
m a trix
These ‘best’ variable com binations were entered in to m u ltip le
lin e a r regression to derive algorithm s fo r the p re d ic tio n o f ib .c ,
9
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
T a b le 4 . Samples grouped according to similarities in environm ental conditions as determ ined by cluster analysis and SIMPROF.
Cluster
Description
n
a
Ariake Bay + Massachusetts Bay
2
b
Gulf o f Finland (SUPREM011)
22
c
Gulf o f Finland 2000 (m id-Apr to mid-May)
5
d
Bedford Basin (mid-Mar to end o f Apr)
9
e
Bedford Basin (Feb to mid-Mar), MA Bay, North Sea CEND0811, AMT6 UPW and Pacific Ocean UPW
67
f
Baltic proper (SYNTAX2010)
22
g
Gulf o f Finland 2000 mid May, mid and late Jul, early Aug
5
h
Gulf o f Finland late May to early Jul, Aug to Oct
10
i
North Sea CEND0811 (Pen Field, South Pen Field, D366 (Falmouth, Southern North Sea, Flelgoland)
5
j
Offshore DCM o f AMT6, 11, 15 & Pacific Ocean, Celtic Sea JR98 DCM
49
k
Celtic Sea D246, AMT 6 European shelf edge surface
9
I
AMT6, 11 European shelf edge intermediate depths, Celtic Sea JR98 DCM, CEFAS0811 (North Dogger), D366 (Central North Sea)
17
m
AMT6 open ocean, surface & intermediate depths, AMT 11 open ocean intermediate depths, Pacific Ocean SPG surface, FINLC surface
54
n
Celtic Sea JR98 (Irish Sea), North Sea (D366 Falmouth, St George Straight, Mingulay, Bay o f Biscay
12
o
AMT6, 11.15 open ocean surface, D366 Central North Sea, Celtic Sea (JR98) surface
45
SPG South Pacific Gyre, FINLC High N utrient Low Chlorophyll region, DCM Deep Chlorophyll Maximum; n is the num ber o f samples per cluster.
doi:10.1371/journal.pone.0058137.t004
3-D S tress: 0.06
Studies
▼ AMT 6
▼ AMT11
▼' V AMT15
• CS-D246
V
o CS-JR98
Pacific
+ North Sea
X UK-OA
▲ Baltic Sea
▲ GoF 2000
A GoF 2011
MA Bay
♦
•
Bedford B
*
Ariake B.
►♦
/K» T oV
< *>
D
B
Clusters
•
•
o
•
o
•
o
o
•
•
AA
ih
o
•
•
0
o
a
b
c
d
e
f
g
h
i
j
k
I
m
n
0
Figure 4. Three-dim ensional non-m etric M ultidim ensional Scaling (nM DS) o rd in atio n o f th e environ m en tal conditions o f all field
campaigns. Panels (A), (B) and (C) are the x-y, x-z and y-z plane o f the nMDS 3D ordination, respectively. (D) is the x-y plane where the symbols
denote the various clusters as determined by cluster analysis in combination w ith similarity profile (SIMPER) tests. Clusters were significantly different
from another (SIMPROF, p<0.005). For an overview of sample groupings according to these clusters see details in text and Table 4.
doi: 10.1371/journal.pone.0058137.g004
PLOS ONE I www.plosone.org
10
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
Temperature
Salinity
HI
r
-<I
abcdefghi jklmno
a b c d e f g h i j kImno
~r-,
< V
r h r lm
.^1
abcdefghi jklmno
Figure 5. V a riab ility in the electron requirem ent fo r carbon fixa tio n ( 0 e,c) and environ m en tal conditions w ith in d iffe re n t clusters of
samples. Clusters were generated by cluster analysis combined with a SIMPROF test. For samples contained in each cluster see also Table 4. Values
are means and error bars are standard deviations (with n of 2-67, see Table 4) of <Pe C (mol e~ mol CT1), temperature ( C), salinity, chlorophyll a (Chi a,
mg nrT3), nitrate and phosphate (pmol L_1), the vertical attenuation coefficient of photosynthetically available radiation (Kd, nrT1), optical depth £,
(dimensionless) and sampling depth (z, in meters).
doi:10.1371/journal, pone.0058137.g005
w h ich , in m an y cases, resulted in significant relationships w ith <&e¡c
significant M L R existed between <Pe c and e n viro n m e n ta l variables
(M L R , p < 0.05) (Table 5). S ig n ifica n t relationships (R2 < 0 .0 5 )
in any o f these regions (clusters e—i, k, 1).
between <&e¡c and e n viro n m e n ta l variables existed in the G u lf o f
T o develop region-specific algorithm s, we also grouped the
F in la n d (cluster b), B edford Basin (cluster d), European shelf
clusters according to m ea n in g fu l w ater masses and biogeographic
waters (cluster n) and offshore samples fro m in te rm e d ia te depths
(cluster m), surface waters (cluster n) and the deep ch lo ro p h yll
regions resulting in 11 significant algorithm s covering the G u lf o f
m a x im u m (D C M ) (cluster j). S urprisingly, P O 4 0 , ra th e r than
F inland), European shelf waters (in clu ding the N ortheast A tla n tic),
NO3
N o rth w e st A tla n tic shelf waters, the e q u ato ria l A tla n tic and the
F in la n d , the B a ltic Sea as a w hole (i.e. in c lu d in g the G u lf o f
a va ila b ility, was often p a rt o f the va riable com binations
showing the strongest association w ith 0 e c, usually in a d d itio n to
South A tla n tic O cean. A lth o u g h some o f these region-specific
tem perature a n d /o r salinity. T h e strong relationships between
relationships exh ib ite d a lo w I t . they were h ig h ly significant. T h e
and P O 4 0
and lack th e re o f w ith N O 3
m a y be due to N O 3
relationships between <t>^c and e n viro n m e n ta l variables were
concentrations being close to o r below the detection lim it in open
strongest in the G u lf o f F in la n d and the Pacific O cean (i? "< 0 .0 5 ),
ocean waters and, d u rin g the sum m er m onths, often also in shelf
fo llo w e d b y the N o rth w e st A tla n tic shelf samples (i.e. M assachu­
waters, w h ic h comprom ises the detection o f relationships w ith
setts Bay + B e d fo rd Basin). Relationships fo r the A tla n tic were
<Zh,c.
an
im p o rta n t
m uch
d e term in a nt o f & e c in these waters, b u t w ith PC) 1 ’
being the
(/><0.01). O nce again, P O 4 0
T hus,
NO3
a v a ila b ility
m ay
still
be
less pron o u n ce d
(R2 < 0 .2 2 ),
albeit h ig h ly
ra th e r th a n N O 3
significant
a v a ila b ility
o n ly m a c ro n u trie n t le ft in o u r analysis, o n ly the la tte r was p u lle d
appeared to p la y a greater role in these M L R s . O n a global scale,
out. D espite the d istin ct clustering o f samples fro m the fro n ta l and
M L R yielded an R 2 o f 0.038, b u t w ith b o th N O 3
u p w e llin g regions, the B a ltic Sea and E uropean shelf edge, no
c o n trib u tin g to the v a ria b ility in <//,/,.
PLOS ONE I www.plosone.org
11
and P O 1 ’
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
60
• SM LSPG
O DCM SPG
A SM LH NLC
zl DCM HNLC
♦ SML UPW
O DCM UPW
50
.
^
40
'
.
30
Í
I
20
10
0
50
30
B
100
150
SML AB
DCM AB
SML Eq
DCM Eq
25
200
10
0
15
20
25
SML NAG
DCM NAG
SML EM
DCM EM
20
15
+
10
5
0
20
40
60
80
100
120
7
14
21
28
30
•
SM LSTCZ
O
▼
V
■
o DCM STCZ
25
A SM LSAG
¿I DCM SAG
♦ SML Eq
20
DCM Eq
SM LNAG
DCM NAG
SM LEM
15
10
5
_ l__________ I__________ I__________ I__________ I__________ I_
0
20
30
40
60
80
D
100
120
140
8
■ SM LSTCZ
Ö DCM STCZ
• SM LSAG
o DCM SAG
♦ SML Eq
o DCM Eq
25
20
15
10
5
i
0
50
100
Depth [m]
150
200
2
3
NO ' [pmol L'
0
4
5
6. I aan electron req uirem ent fo r carbon fixation (<Pe,à across d iffe re n t biogeographical provinces fo r fou r cruises. AeC
left panels) and N 03~ (right panels) are shown for the Pacific Ocean (A and E), AMT 6 (B and F), AMT 11 (C and G) and AMT 15 (D and H),
standard deviations w ith n = 3 to 14. SML denotes surface mixed layer, DCM the deep chlorophyll maximum, SPG is the South Pacific
gh Nutrient Low Chlorophyll areas, UPW upwelling regions, SA South Africa, AB Angola Basin, Eq equator, NAG North Atlantic Gyre, EM
n in the North East Atlantic, and STCS the Subtropical Convergence Zone. Note change in x- and y-axis scale.
iurnal.pone.0058137.g006
vww.plosone.org
12
March 2013 I Volume 8 I Issue 3 I e58137
Electron Requirement for Carbon Fixation
T a b le 5 . M ultivariate correlations and regressions between environm ental variables and <&eiC for different clusters and regions.
BEST
Cluster
P
a
-
MLR
Variables
P
M od el
R2
P
-
-
-
b GoF
0.238
>0.05
T, S, Kc, Ç
—3.82T+2.80S+3.01Kd- 1 .12Ç
0.735
< 0.01
c GoF
0.538
>0.05
S
n.s.
0.701
>0.05
d Bedford Basin
0.303
>0.05
T
—1.31 T+11.78
0.710
<0.05
e Fronts and UPW
0.234
< 0.01
S
n.s.
0.085
>0.05
f Baltic proper
0.135
>0.05
T
n.s.
0.103
>0.05
9 Go F
0.430
>0.05
N, P, Kd
n.s.
0.676
>0.05
h GoF
0.195
>0.05
S, PO43-
n.s.
0.369
>0.05
i North Sea
0.539
>0.05
s, P0 43- ,
n.s.
0.965
>0.05
j DCM offshore
0.402
< 0.01
T, S
—8.05T+8.89S —3.23
0.251
< 0.01
k Celtic Sea, EUR shelf edge
-0 .0 5
>0.05
N O T , Chia
n.s.
0.150
>0.05
I EUR shelf edge
0.254
>0.05
%
n.s.
0.012
>0.05
m Inter m. depths offshore
0.201
<0.05
S, N, P, Chia
—50.85S+4.25NO3_+0.675PO43_ -11.81 Chla+322.8
0.315
< 0.01
n EUR shelf, North Sea
0.468
>0.05
T
6.40T -1 3 .4 6
0.434
<0.05
o Surface offshore
0.190
>0.05
S, N o T , Chia
—4.09S —5.83N03_+12.09Chla+32.59
0.269
< 0.01
GoF (b c g h)
0.447
< 0.01
T, S, N O fi, Kd
-0.741 T+14.8S+0.206N03" -2 .6 9 K d -2 6 .1 4
0.561
< 0.01
Baltic + GoF (b c g h e)
0.236
< 0.01
S, N O T , Chia, Kd, Ç
1.30S -5 .2 1 N 0 3" -0 .6 1 Chia -2 .5 3 K d+0.77Ç+5.75
0.266
< 0.01
Shelf (i k I n)
0.245
< 0.01
T, N O T , P043b Chia, Ç
3.39T+1.44N03" -2.20PO 43_ -1.42C hla -0.57Ç-0.25
0.273
<0.05
Offshore SML (m o)
0.173
<0.05
N 0 3- , P O y T Chia
—5.97NO3~+9.62PO43_+0.33Chla +11.35
0.083
< 0.01
Offshore SML+DCM (j m o)
0.296
< 0.01
T
—5.45T+37.51
0.090
< 0.01
EUR Shelf/NE Atlantic
0.142
<0.05
T, P043T Chia
0.04T -1 1 .5 3 P 0 43_ - 1 .09Chla+10.99
0.207
< 0.01
NW Atlantic Shelf
0.329
< 0.01
T, S, N O T , P043~
—0.57T+0.25S+1.36N03_ -5 .6 6 P043 - +22.58
0.322
< 0.01
Equatorial Atlantic
0.205
<0.05
S
0.47S -0 .7 2 3
0.090
<0.05
South Atlantic
0.395
< 0.01
N O T , P043b Chia
0.32NO3" - 1 3.07P043_+0.78Chla+6.20
0.213
<0.05
Pacific SPG +HNLC
0.233
>0.05
S, P O y T Chia
—25.27S -94.29PO43_+29.29Chla+920
0.589
< 0.01
Pacific SPG + HNLC + UPW
0.183
>0.05
S, P O y T Chia
17.53S+33.11P043 -+14.6 Chla+1397
0.554
< 0.01
Global
0.114
< 0.01
T, N O T , P043~
0.31 T -0 .4 9 N 0 3"+6.34P043_+4.05
0.038
< 0.01
ç
Biogeographic regions
Results o f the BEST test are the variable com binations resulting in the highest correlation coefficient (p) between th e resemblance matrices o f th e environm ental data
and 0 eC. Abbreviations: GoF G ulf o f Finland, UPW U pwelling region, SML surface mixed layer, DCM deep chlorophyll maximum, EUR European SPG South Pacific Gyre,
HNLC High nutrient low chlorophyll area,. Cluster a was excluded from th e BEST test and MLR due to its small sample size (n = 2).
doi:10.1371 /journal.pone.0058137.t005
te rm 14co2uptake rates, so th a t m ost <Pec values available to this
day w o u ld p ro vid e a conversion fro m E T R to G PP o r to
Discussion
Reconciling electron transfer and carbon fixation
som ething between N P P a nd GPP. ETnder m ost conditions, N PP
W h ile e m p irica l evidence demonstrates th a t fluorescence-based
measures o f the P S II ph o to ch e m ica l efficiency, and hence E T R s,
are lin e a rly related to net o r gross carbon fix a tio n rates under
m an y conditions [16,47,54], there are still considerable u n ce rta in ­
differs fro m G PP b y a fa cto r o f 2 to 2.5 [55,19,20], fo r w h ic h the
ties about w h a t drives & e C as w e ll as differences between N P P and
GPP. G ro w th rate dependent d iffe re n tia l a llo ca tio n o f fixed
fu rth e r investigation and is the focus o f ong oing w o rk.
carbon and v a ry in g lifetim es o f in te rm e d ia te products m ay cause
large discrepancies between N P P and GPP, w h ich short te rm
1 4 C 0 2 uptake measurements m ay n o t capture [19,20], W h ile it is
fo r electron sinks associated w ith n u trie n t red u ctio n , the slope o f
generally accepted th a t sh o rt-te rm
cu rre n t $>r c values cannot account. Conversion o f E T R to N PP
and assessments o f the p o te n tia l e rro r in & ec a nd subsequently
N P P due to e m p lo yin g short te rm 14C incubations w ill require
ETnder ‘o p tim a l’ g ro w th (where N P P ~ GPP), and a ccounting
the lin e a r relatio n sh ip between E T R a nd N P P should y ie ld values
fo r <Pe c o f 4—6 m o l e- (m ol C ) _ 1 [1 6 -1 8 ], T o date, m ost F R R f-
14C in cu b a tio n techniques
based studies use an electron req u ire m e n t fo r carbon fix a tio n o f
ap p ro xim a te GPP, H alsey et al. [19,20] dem onstrated th a t this is
o n ly the case in fast g row ing, n u trie n t-re p le te p h yto p la n kto n . In
n u trie n t
lim ite d
cells,
on
the
o th er
hand,
sh o rt-te rm
5 m ol e
14C
req u ire d p e r 0
incubations equate N P P o r p rim a ry p ro d u c tiv ity rates somewhere
1
to convert E T R s to carbon fix a tio n rates,
2
m olecule pro d u ce d and (ii) th a t 1-1 .5 m o l o f 0
2
is produced fo r each m o l C 0 2 fixed, i.e. the photosynthetic
q u o tie n t takes values o f 1 -1.5 m o l 0 2 (m ol C 0 2) 1 [56], Indeed,
between N P P and GPP. F ailure to accurately q u a n tify GPP w ill
in e v ita b ly affect
M o st data published in the past and also
some studies here co n firm e d $>ec equal (or close to) 4—6 m o l e-
those used in o u r meta-analysis com pared E T R to relative ly short­
PLOS ONE I www.plosone.org
(m ol C)
assuming (i) th a t at least 4 e_ transported th ro u g h P S II are
13
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
(m ol C) *). H ow ever, the vast m a jo rity o f estimates fo r <t>ec are
considerably higher, sometimes reaching extremes o f > 5 0 m o l e
based a lg o rith m [7] (C E N D 0 8 1 1 , U K - O A D 366). These co m ­
parisons showed th a t a constant h r h j m ay lead to an underestim ate
(m ol C)
o f <Pe>c b y 2 8 -4 7 % (Fig. S2, T a b le S I in A p p e n d ix S I), w h ich
co u ld thus, at least in p a rt, exp la in the lo w
in the G u lf o f
1
(e.g. B IO S O P E Pacific O cean Cruise) o r a lte rn a tive ly
&e,c o f < 5 m o l e (m ol C) 1 G u lf o f F in la n d 2000 and A M T 15.
T hus, fo r m an y cases, a p p lica tio n o f an assumed value o f 4 -6 m ol
F in la n d data. T h e npsn values estimated fo r the N o rth
e- (m ol C ) - 1 to F R R data w o u ld yie ld erroneous estimates o f Cuptake (w ith in the lim ita tio n s o f the 1 4 C -uptake itse lf fo r
q u a n tify in g C -uptake).
V alues o f 0 e c > 5 m o l e-
(m ol C ) - 1
Sea
spanned a range o f 0.0018 to 0.0056 m o l R C (m ol chia) \ w h ich
is com parable w ith the range observed fo r eukaryotic and
p ro ka ryo tic p h yto p la n kto n [46,47,58], b u t higher, b y ca. a factor
o f 2, th a n npsn d ire ctly m easured b y M o o re et al. [11] in European
shelf waters a t a sim ilar tim e o f year. C le a rly fu rth e r d irect
have been observed
previously and p o te n tia lly reflect processes th a t act to decouple
E T R s fro m C -fix a tio n , such as p h o to re sp ira tio n [32], ch lo ro respiration v ia a plastid te rm in a l oxidase (P T O X ) [33,34] and
m easurements o f npsn and va lid a tio n o f algorithm s proposed fo r
e stim ating the value o f this va riab le [7] are re q u ire d before a m ore
M e h le r reaction [32]. W e re tu rn to this issue in the fo llo w in g
robust assessment o f the
sections. In contrast, values o f 0 „ c < 5 m o l e (m ol C) 1 are m ore
d iffic u lt to reconcile w ith biophysical and physiological processes,
p o te n tia lly in d ic a tin g the m agnitude o f re m a in in g m ethodological
associated w ith npsn cun be achieved. Such measurements are
the focus o f ong oing w ork.
e rro r
in
calculated
w h ic h
is
such as in co rre ct assumptions
O th e r sources o f discrepancies between electron transfer and
carbon fix a tio n m ay stem fro m differences am ong protocols fo r
co ncerning the value o r v a ria b ility o f nPSn (see below), inadequate
spectral c o rre ctio n o r re m a in in g non-system atic errors in b o th
E T R -lig h t response curves (rapid lig h t curves vs. steady state lig h t
curves) [61], deviations in the timescales o f in situ E T R and
carbon fix a tio n and fluorescence estimates. T h e re were tw o studies
w ith a h ig h p ro p o rtio n o f <&ec values < 5 m o l e (m ol C) *: the
la b o ra to ry 1 4 C-photoynthesis measurements [43,61], discrepancies
in the E k values d e rived fro m E T R and C 0 2 uptake [5 2 -5 4 ], o r
discrepancies in d e rivin g
the effects o f w a te r co lu m n structure and subsequent changes in
A M T 15 cruise (H ickm a n et al. unpublished) and the G u lf o f
F in la n d 2000 study. U n lik e d u rin g the A M T 15 cruise w here
< 5 m o l e- (m ol C )-
lig h t a va ila b ility on the ‘shape’ o f E T R lig h t response curves [ 8 ].
F o r the data in clu d e d in the present study and the associated
differences in m ethodology w ith regard to E T R calculations (ffpsn,
o ccurred o n ly in samples fro m the D C M ,
we co u ld n o t id e n tify any consistency in the occurrence o f such
npsn) and 14C in cu b a tio n techniques, we estimated that, in w orst
lo w values th a t co u ld be related to sample h a n d lin g and processing
in the G u lf o f F in la n d 2000 data. T hus, the h ig h p ro p o rtio n o f lo w
<&ec values in the G u lf o f F in la n d m ig h t p o in t to systematic errors
in the E T R calculations, i.e. in the com ponent values fo r ffpsn,
npsn a n d /o r E, values th a t are often assumed (or n o t w ell
case scenarios,
m ay be over- o r underestim ated b y as m uch as
53% (data n o t shown). A detailed assessment o f these m eth o d o ­
lo g ica l differences between techniques and studies is b eyond the
scope o f this study, a nd we refer the reader to a previous
com prehensive reviews o f these issues [8,38]. H o w e ve r, we note
measured). W h ils t values o f ffpsn m easured b y F R R f have been
shown to m atch independent b io -o p tica l measurements w e ll [46],
th a t v a ria b ility in estimated values o f (t>ec was lo w e r th a n th a t
observed across a ll studies (Fig. 2) fo r the tw o new studies in clu d e d
we have to assume th a t the b io -o p tica l in stru m e n ta tio n used to
here, w h ic h were p e rfo rm e d u n d er the m ost co n tro lle d conditions
q u a n tify b o th E and ffpsn have been a p p ro p ria te ly calibrated. In
the G u lf o f F in la n d [29], values o f ffpsn ty p ica lly range fro m ca.
150-300 A 2 q u a n tu m - 1 , w h ich is on the lo w e r end o f the range o f
(S Y N T A X 2 0 1 0 and N o rth Sea C E N D 0 81 1 ), i.e. were E T R and
C 0 2 fix a tio n were sim ultaneously measured on the same sample.
T hus, the extent to w h ich the extrem e values a n d /o r v a ria b ility in
values expected fo r assemblages d o m in a te d b y diatom s, d in o fla gellates, cryptophytes a nd cyanobacteria (data n o t shown), b u t still
w ith in the range co m m o n ly observed fo r such species [38].
Absolute underestim ations o f ffpsn as a result o f erroneous
w h ich is observed in some o ther studies, represents re m a in in g
errors in e ith e r carbon fix a tio n o r E T R estimates rem ains unclear.
in s tru m e n t calibrations are therefore u n like ly a significandy
c o n trib u tin g factor. H ow ever, in cases w h e n cyanobacteria
Environmental regulation o f < P e C
D a ta presented in this study focused alm ost exclusively on the
apparent effect o f rea d ily measurable e n viro n m e n ta l variables on
In fo rm a tio n on p h yto p la n kto n co m m u n ity com position
dom inate, E T R s m ay be underestim ated due to the saturating
lig h t blue L E D pulse be in g in e fficie n t at d riv in g reaction centre
closure, resulting in lo w
values. F urth e rm o re , assum ption o f a
co u ld n o t be ro u tin e ly in clu d e d and we assumed th a t any change
in ta xo no m y was in h e re n tly accounted fo r in the enviro n m e n ta l
constant npsn w ill in tro d u ce errors due to ta xo n o m ic v a ria b ility in
physiological traits [46]. M o re o ve r, p h yto p la n kto n cells tend to
descriptors. Indeed, e n viro n m e n t often leads to d istin ct structural
differences o f the pho to syn th e tic apparatus and acclim a tion
responses am ongst p h yto p la n kto n fro m d iffe re n t biogeographic
change the size o f th e ir p hotosynthetic units in response to lig h t
and n u trie n t a v a ila b ility [5 7 -5 9 ] and ve rtica l m ix in g [60]. Hence
npsn can v a ry am ong species b y m ore th a n a fa cto r o f fo u r, fro m
0.0010 to 0.0042 m o l R C (m ol C hia ) - 1 [46]. R aateoja et al. [29]
regions [3 4 ,6 2 -6 7 ] and, towards unique, often consistent fluores­
cence "signatures" o f P S II [1 0 ,11 ,3 8 ,6 8-7 0 ]. F uture assessments o f
the in te r- a nd intraspecific v a ria b ility in & ec w ill, o f course, be
assumed a constant npsn o í 0.002 m o l R C (m ol C h ia )- 1 , w h ic h is
representative o f the eukaryote p h yto p la n kto n co m m u n ity ob ­
served
in
th e ir
study
(m ostly
diatom s,
dinoflagellates
necessary to fu lly resolve the mechanisms responsible fo r changes
and
in 0 e c and the derived algorithm s (Table 5), w h ich are p u re ly
based on statistical m odels and should therefore n o t be in te rp re ted
fro m a m echanistic perspective. F ro m the relative ly few available
cryptophytes; b u t n o t ty p ica lly w h e n cyanobacteria dom inate.
Consequently, increasing assumed values o f nPSn in the study o f
Rateeoja et al. [29] to account fo r the presence o f cyanobacteria
[8,46] w o u ld increase E T R s and hence p o te n tia lly $>eC to values
studies on p h yto p la n kto n cultures g ro w n u n d er various conditions
to date, (fre e usually does n o t exceed values o f ~ 2 5 m o l e (mol
C) 1 as opposed to estimates o f up to 54 m o l e m o l C 1 fro m
> 5 m o l e- (m ol C )- 1 .
W e assessed the p o ten tia l e rro r in $>e C due to the use o f a
constant nPSn in some o f the data sets presented in this study by
co m p a rin g
<£eC based on a constant nPS_n w ith
n a tu ra l com m unities (reviewed in
c values
calculated fro m E T R w here npsn was eith e r measured v ia oxygen
flash yields (Bedford Basin data) o r calculated using a fluorescence
PLOS ONE I www.plosone.org
Suggett et al.
[ 8 ]). L o w e r
m a xim a l values fo r p h yto p la n kto n cultures co u ld indicate a less
extrem e range o f g ro w th environm ents tested in the la b o ra to ry as
com pared to n a tu ra l conditions, such as, the h ig h -lig h t, low n u trie n t conditions o f the surface open ocean th a t are d iffic u lt to
14
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
M a n y samples fro m Massachusetts B ay and o ther open ocean
reproduce in the la b o ra to ry. F urth e rm o re , la b o ra to ry studies often
exam ine cells th a t are in ‘steady state’ g ro w th whereas na tura l
com m unities m ay persist u n d er (rapidly) changing en viro n m e n ta l
areas fell in to one cluster w ith the B e d fo rd Basin data (Table 4,
Fig. 5). T h e B e d fo rd Basin spring cluster (d) was characterized by
h ig h ch lo ro p h y ll concentrations, whereas samples in the late
conditions. I n the la tte r case, non-steady state conditions could
lead to a strong and transient u n co u p lin g o f electron transfer and
w in te r
carbon fix a tio n [10,71,72], w h ich w o u ld suggest th a t the p rim a ry
source o f v a ria tio n in & ec is the e n viro n m e n t ra th e r than
ta xo n o m ic v a ria b ility . T h e effect o f g ro w th rate on o u r a b ility to
measure G PP b y short-term 14C incubations u n d er n a tu ra l
cluster
(e)
had
lo w
ch lo ro p h y ll
concentrations
and
tem peratures m ore sim ilar to those in fro n ta l and u p w e llin g
regions o f the N o rth Sea, and the A tla n tic and Pacific Oceans.
T h e w ide range o f e n viro n m e n ta l gradients observed in these
clusters m ay be the reason w h y M L R d id n o t re tu rn any
significant relationships between
c and e n viro n m e n ta l variables.
conditions m ay fu rth e r co n trib u te to the w id e r range o f <l>e>c
values fro m fie ld observations relative to culture-based 0 , r
[19,20],
F urth e rm o re , such relationships m ay n o t necessarily be lin e a r [81]
and o th e r models w ill have to be tested in the future.
M o s t o f the
C onsiderable v a ria b ility o f <l>e>c existed n o t o n ly spatially b u t
also te m p o ra lly. G iven the large range o f <&ec fo r the entire data
biogeographic
o th er
studies,
provinces
(sensu
also extended
L o n g h u rst
across m u ltip le
[82])
or
d istin ct
environm ents w a te r masses ( S M L /D C M ) , and a lth o ug h there
seemed to be consistent overlaps between n u trie n t deplete regions
and areas o f h ig h & ec (Fig. 3), the absolute n u trie n t concentration
set, it is notable th a t m ean & ec in all b u t one o f the tim e series
studies (Massachusetts Bay) never exceeded 10 m o l e (m ol C) ’ .
T h e greater variance in the Massachusetts Bay tim e series study
could, on the one hand, have been related to its longer d u ra tio n (9
m onth) relative to the o th er tim e series (1.5 -6 m onth) and, on the
o th e r hand, to its topography; w h ile the G u lf o f F inlan d , B edford
Basin and A ria k e Bay, are a ll surrounded b y la n d fo rm in g at least
was often n o t correlated w ith & e c (Table 2). Im p o rta n t examples
are the open ocean regions, h ig h lig h tin g h o w enviro n m e n ta l
fo rcin g can con fou n d establishm ent o f strong relationships
between & ec and measurable e n viro n m e n ta l variables a t the
basin scale: & e>c often declined w ith increasing depth and towards
p a rtia lly land-enclosed basins, Massachusetts Bay is relative ly
exposed and m ore strongly influenced b y exchange o f w a te r w ith
the n u trid m e ; even so, <&ec was often n o t sig n ifica n tly correlated
w ith m easured n u trie n t co n ce ntra tio n m ost lik e ly reflecting
differences in n u trie n t a v a ila b ility between the gyres, H N L C
areas and coastal u p w e llin g regions. A d d itio n a lly , n u trie n t stocks
are n o t necessarily a good in d e x o f the level o f n u trie n t stress
w ith in a p o p u la tio n , w h ich w ill depend ra th e r on the overall
the A tla n tic Ocean. Nevertheless, seasonal changes appear to
influence the v a ria b ility in
c a lthough m an y areas are still
under-sam pled.
In the G u lf o f F inlan d , fo r example, ve rtica l m ix in g and the
depth o f the surface m ixe d layer change across d iffe re n t seasons
[7 3 -7 5 ] and w ith it the o p tica l and physicochem ical properties o f
(re-)supply rates o f the n u trie n t relative to the demands o f the
the w a te r co lu m n , th a t is, lig h t and n u trie n t a v a ila b ility o f the
exta nt p h yto p la n k to n c o m m u n ity [29]. T h e clustering o f the G u lf
o f F in la n d samples - in to a late w in te r (b), spring (c), sum m er (g)
and s u m m e r/e a rly a u tu m n (h) m irro rs these physicochem ical
e xta nt co m m u n ity. In the iro n a nd n itro g e n deplete SPG [12] and
the lo w -iro n H N L C region o f the Pacific O cean [83], <&ec
declined w hen N 0 3_ concentrations were above the detection
lim it (usually at the deep ch lo ro p h y ll m axim u m ). A p a rt fro m the
changes. H ow ever, the h ig h ly dyn a m ic nature o f this system makes
the developm ent o f p re d ictive algorithm s fo r the entire B a ltic Sea
(in clu ding the G u lf o f F inland) challenging. T h e best predictors o f
extrem e o u tlie r o f <&e¿ > 50 m o l e (m ol C) *, highest <&ec values
were observed in the u p w e llin g region and the gyre corresponding
to samples fro m a lo w - N 0 3_ surface w ater lens w ith high
0 „ c fo r the w hole region were tem perature, sa lin ity and P 0 4 3 ,
irradiances. Beneath this surface w a te r lens, N 0
resulting in a relative ly weak (R 2 = 0.266) alb e it h ig h ly significant
relationship. F or the G u lf o f F in la n d on its ow n, however, the
relationships were m uch stronger (R2 = 0.561, ƒ><().01), in d ic a tin g
lig h t levels dro p p e d and i>e>c declined.
3
increased w h ile
Ir o n and n itro g e n lim ita tio n m ay be expected to influence the
p hotosynthetic apparatus in d iffe re n t ways, w ith iro n deficiency
causing a pre fe re ntia l decline in iro n rich -ce llu la r com ponents (e.g.
th a t the G u lf o f F in la n d should perhaps be treated as its ow n
region.
PS I, P S II a nd cytochrom e b 6 f) [5 6 ,8 4 -8 6 ]. T hus, d iffe re n t form s
o f n u trie n t lim ita tio n can induce differences in the fluorescence
D is tin c t te m p o ra l changes in e n viro n m e n ta l gradients also
existed in B e d fo rd Basin, w here in itia l correlations (Table 2)
signatures o f the resident p h yto p la n kto n co m m u n ity [67,72] and
subsequently in <£e C. Iro n lim ite d p h yto p la n kto n in H N L C
regions, fo r instance, m y express the c h lo ro p h y ll-b in d in g p ro te in
showed significant relationships o f <&e c w ith salinity, w h ic h m ay
have b o th in d ire c t (via alterations o f density and w a te r co lu m n
stratification) and d ire c t (osmotic) effects on
c. T h e co m b in a tio n
o f lo w nutrients coupled w ith sudden h ig h lig h t a va ila b ility due to
IsiA , w h ich reduces the a p parent P S II p h o to synthetic efficiency
and p rim a ry p ro d u c tiv ity rates n o rm a lize d to ch lo ro p h y ll [87,88].
T h e la tte r w o u ld cause <&ec to increase. N u trie n t lim ita tio n in
elevated freshw ater discharge after snow m e lt and ice breakup
co u ld cause an u p -re g u la tion o f electron, A T P a n d /o r red u cta n t­
co m b in a tio n w ith h ig h -lig h t stress in surface waters m ay hence
have been responsible fo r the highest
c o b tained in these
regions, suggesting a h ig h degree o f u n co u p lin g between electron
consum ing pathways (e.g. p h o to re sp ira tio n and M e h le r reaction).
C onceivably, sim ila r changes in salinity co u ld also d ire ctly affect
<&ec b y causing osm otic stress o r an increase in resp ira tio n o f the
transfer and ca rb o n fixa tio n . S im ila rly, variations in nitro g e n
exta nt p h yto p la n k to n co m m u n ity [76]. B e d fo rd Basin p h yto p la n k­
to n c o m m u n ity com position often shifts fro m diatom s and
assim ilation and n itro g e n fix a tio n req u ire large am ounts o f A T P
also leading to an u n c o u p lin g o f electron tran sp o rt fro m carbon
dinoflagellates to chlorophytes after the snow m e lt (Suggett &
Forget unpublished) [77], m a tch in g the increase o f í>e>c■ T hus, in
fix a tio n [67,89,90].
B e d fo rd Basin m u ltip le e n viro n m e n ta l factors (salinity, tem pera­
ture, stratification) were lik e ly at play, p o te n tia lly e xe rtin g lig h t
Conclusions
and osm otic stress on the extant, b u t changing, p h yto p la n kto n
rates o f N P P depend on o u r a b ility to accurately p re d ic t <l>e>c fo r
given e n viro n m e n ta l co n d itio n . T h is present study shows, fo r the
Conversions o f FR R f-based E T R estimates to carbon-specific
c o m m u n ity [7 7 -8 0 ]. R esolving the u n d e rlyin g mechanisms
responsible fo r seasonal changes in
c in rem ains a challenge
and w ill req u ire teasing a p a rt d a ylig h t h o u r effects fro m
tem perature effects and oth er physicochem ical variables.
PLOS ONE I www.plosone.org
first tim e, the extent o f v a ria b ility o f
<j, a lb e it w ith in the past
m eth odological constraints o f accurate q u a n tifica tio n o f b o th
E T R s and NPP. M o s t data on & ec available to this day are based
15
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
on sh o rt-te rm 14C incubations w h ich , depending on algal g ro w th
(TIF )
rates, m ay capture G PP ra th e r th a n NPP. F u rth e r studies are
needed to fu lly resolve the discrepancies between
derived
Figure S2 Com parison o f
(in m ol e
(mol C) ’)
calculated with an »t/>s// = 0.0020 m ol RC (mol chia)-1
and where n Psu w as m easured w ith oxygen flash yields
(Bedford Basin) or by FRR fluorom etry according to
Oxborough et al. [11] (UK-OA D366 and North Sea
CEND0811). B o ld lin e represents the regression equation fo r all
fro m G PP o r N P P in b o th cultures a nd n a tu ra l com m unities.
Nevertheless, o u r w o rk shows th a t some o f the v a ria b ility in
c
can be lin k e d to e n viro n m e n ta l variables th a t are ro u tin e ly
measured. G ive n the observed va ria b ility , it is h ig h ly u n like ly th a t
a global approach o r a lg o rith m can be pro d u ce d w h ic h captures a
h ig h p ro p o rtio n o f the variance in
three
c- H ow ever, w ith the present
studies
com bined:
i>e>c
constant
nPsn = 0.617 x
{ f i e,c
measured nPSII)+2.165 (R2 = 0.807, n = 1 1 0 , p < 0 .0 5 ). Regression
coefficients are shown in T a b le S I in A p p e n d ix S I.
study we p ro vid e firm evidence th a t such algorithm s can in fact be
generated fo r biogeographic regions and d istin ct w a te r masses,
b rin g in g us closer th a n ever to p re d ic tin g carbon uptake fro m
(TIF )
E T R s. Indep e n d e n t va lid a tio n o f these algorithm s is still required,
Appendix SI Results o f PCA including m ethodological
and location variables and assessm ent o f the effect o f
variable nPSII on Phie,C.
and, we m ay expect they w ill be refined as m ore data accum ulate.
Im p o rta n d y , o u r study provides m eth o d o lo g y fo r fu tu re data
co lle ctio n and in te g ra tio n to im p ro ve <&e c algorithm s. C learly,
developing standardized protocols w o u ld greatly facilitate in te r­
(D O C X )
comparisons o f studies and reduce some o f the p o te n tia l e rro r due
to m ethodological differences. Assessing the role o f p h yto p la n kto n
Acknowledgments
taxonom y, developm ent o f n o n -lin e a r models and testing o f the
present alg o rith m s on novel, independent data represent necessary
W e are extremely grateful to Sarat C. T ripathy and Prof. Jo ji Ishizaka
(HyARC N agoya University), C hristopher Melrose (NOAA N ortheast
Fisheries Science Center, (Mika R aateoja (Finnish E nvironm ent Institute)
and T im Smyth (Plymouth M arine Laboratory) who very graciously
provided additional environm ental data from their previously published
work, as well as R ob T hom as a t the British O ceanographic D ata C entre
for supporting the retrieval o f the A M T and JR 9 8 data and W endy Lea at
the M assachusetts W ater Resources A uthority for providing the M assa­
chusetts Bay data. W e also acknowledge the mission scientists an d principal
investigators of M O D IS and SeaW IFS who provided data via the
Giovanni online data system, developed and m aintained by NASA GES
D ISC. W e are also grateful for the comm ents provided by AJ Milligan and
an anonym ous reviewer.
fu tu re steps to im p ro ve the level o f accuracy.
O n e o f the m a jo r re m a in in g challenges in u tilis in g these
algorithm s is d e fin in g the (biogeographic) regions, w h ile keeping in
m in d th a t th e ir boundaries m ig h t a ctu ally shift in space a nd tim e.
Hence ca u tio n is still req u ire d in widespread a p p lica tio n o f the
c u rre n t algorithm s. Even so, the appearance o f clear patterns and
p ro o f o f p re d ictive p o w e r o f e n viro n m e n ta l variables in the present
article provides strong support and m uch im p ro ve d confidence for
successful conversion o f E T R s to carbon fix a tio n rates at a m uch
greater spatial and te m p o ra l resolution th a n c u rre n t 14C fixa tio n
approaches.
Author Contributions
Supporting Inform ation
Advice with statistical analysis: R JG . Conceived and designed
experiments: EL J K DJS GS R M F. Perform ed the experiments: EL
GS PY M -H F SS EC O P A E H C M M DJS RM F. Analyzed the data:
DJS. C ontributed reagents/m aterials/analysis tools: RM F. W rote
paper: EL DJS.
Figure SI Principal com ponent analysis including the
environm ental data, location data and m ethodological
inform ation (A) and w ith the m ethodological differences
excluded from the analysis (B).
the
JK
EL
the
References
1.
11.
L in d e m a n R L (1 9 42 ) T h e tro p h ic d y n am ic aspect o f ecology. E cology 2 3 :3 9 9 —
2.
F ie ld
CB,
B e h ren feld
M J,
R an d e rso n J T ,
Falkow ski
PG
(1 9 98 )
P rim a ry
m e n ta l gradients in a shelf sea. L im n o l. O ce a n o g r. 5: 9 3 6 —949.
p ro d u c tio n o f the biosphere: In te g ra tin g te rrestrial a n d oceanic com ponents.
12.
Science 281: 2 3 7 -2 4 0 .
3.
C a r r M - E , Friedrichs A M , S chm eltz M , A k a M N , A n to in e D , e t al. (2 0 06 ) A
13.
Elsevier A c ad em ic Press, N e w Y o rk . pp. 2 8 7 —236.
Lon g h u rs t A , S ath ye n d ra n ath S, P la tt T , C a v e rh ill C (1 9 95 ) A n estim ate o f
14.
global p rim a ry p ro d u c tio n in the ocean fro m satellite ra d io m e te r data. J P la nk ton
E co l 26: 5 5 - 7 6 .
B eh ren feld M J , Boss E , Siegel D A , Shea D M . (2 0 05 ) C a rb o n -b a s ed ocean
15.
p ro d u c tiv ity a n d p h y to p la n k to n physiology fro m space. G lo b a l Biogeochem
Schreiber U , N e u b a u e r C , Schuw a U
(1 9 93 ) P A M
16.
flu o ro m e te r based on
17.
O x b o ro u g h K , M o o r e M G , Suggett D , Law son T , C h a n H G , et al. (2 0 12 ) D ire c t
18.
flu o ro m e try (F R R f) data. L im n o l O ce a n o g r M e th 10: 1 4 2 -1 5 4 .
relationship betw ee n the
tra n s p o rt
and
q u e n c h in g
of
E dw ards G E , B aker N R
(1 9 93 ) C a n C O
2
assim ilation in m a ize leaves be
Suggett D J, M a c In ty r e H L , K a n a T M , G e id e r R J (2 0 09 ) C o m p a rin g electron
photosynthetic currencies fo r eukaryo tic ph y to p la n kto n . A q u a tic M ic r o b ia l E col
56: 1 4 7 -1 6 2 .
editors. C h lo ro p h y ll a fluorescence in a quatic sciences: m ethods a n d a pplica­
19.
tions. S prin ger D o rd re c h t, p p . 103—127.
H a lse y K H ,
M illig a n
AJ- B eh ren feld M J (2 0 10 ) Physiological o p tim iza tio n
underlies g ro w th ra te-d ep en d e n t chlorophyll-specific gross a n d n e t p rim a ry
Falkow ski P G , K o lb e r Z S (1 9 9 5 ) V a ria tio n s in C h lo ro p h y ll Fluorescence Yields
pro d u c tio n . Photosynth Res 103: 1 2 5 -1 3 7 .
in P h yto p lan k to n in the W o r ld O ceans. A u s tr J P la n t Physiol 22: 3 4 1 -3 5 5 .
20.
M o o r e M G , Suggett D J , H o llig a n P M , Sharpies J , A b ra h a m s E R (2 0 03 ) Physical
H a lse y K H , M illig a n AJ- B eh ren feld M J (2 0 11 ) L in k in g tim e -d e p en d e n t carbonfix a tio n efficiencies in D u n a lie lla
controls on p h y to p la n kto n physiology a t a shelf fro n t: a fast rep etitio n -rate
tertiolecta (C hlorop hyceae) to u n d e rlyin g
m e tab olic pathw ays. J P hycol 47: 6 6 —76.
flu o ro m e te r based fie ld study. M a r E co l P rog Ser 259: 29M -5.
PLOS ONE I www.plosone.org
(1 9 89 ) T h e
e le c tro n
transport w ith gas exchange: pa ram e te ris ing exchange rates betw ee n alternative
Suggett D J , M o o r e M , G e id e r R J (2 0 1 1 ) E s tim a tin g a quatic p ro d u c tiv ity fro m
active fluorescence m easurem ents. In : Suggett D J , Prásil O , B o ro w itzk a M A ,
10.
B aker N R
o f p h o to s y n th e tic
8 9 -1 0 2 .
flu x o n a v o lu m e basis: a n e w appro ac h to the analysis o f Fast R e p e titio n R a te
9.
y ie ld
p re d ic te d a ccurately fro m chlo ro p h yll fluorescence analysis? Photosynth Res 37:
estim ation o f fu n c tio n a l P S II reaction centre c o ncentration a n d P S II electron
.
B, B riantais J - M ,
c hlo ro p h yll fluorescence. B io c h im Biophys A c ta 9 90 : 8 7 —92
in basic a n d a p p lie d photosynthesis research. Photosynth Res 3 6:65 —72.
8
G e n ty
q u a n tu m
m e d iu m -fre q u en c y pulsed X e -fla s h m easuring light: A hig h ly sensitive n e w tool
7.
Fogg G E , C a lv a r io -M a r tin e z O (1 9 89 ) Effects o f bo td e size in de te rm ina tions o f
p rim a ry p ro d u c tiv ity b y ph y to p la n kto n . H y d ro b io lo g ia 173: 8 9 —94
Cycles 19: G B 1 0 0 6 , d o i:1 0 .1 0 2 9 /2 0 0 4 G B 0 0 2 2 9 9
.
V e n r ic k E L , Beers, J R , H e in b o k e lJ F (1 9 77 ) Possible consequences o f co n ta in in g
m ic ro p la n k to n fo r physiological rate m easurem ents. I E x p e rim e n ta l M a r B iol
Res 17: 1 2 4 5 -1 2 7 1 .
6
M a c In ty r e H L , C u lle n JJ (2 0 05 ) U s in g cultures to investigate the physiological
ecology o f m icroalgae. In : A ndersen R A , e ditor. A lg a l c u ltu rin g techniques.
D e e p Sea Res I I 5 3 3 , 7 4 1 7 7 0 , d o i:1 0 .1 0 1 6 /j.d s r2 .2 0 0 6 .0 1 .0 2 8 .
5.
B eh ren feld M J , K o lb e r Z S (1 9 99 ) W id e s p re a d iro n lim ita tio n o f p h y to p la n kto n
in the S outh P acific O c e a n . Science 283: 8 4 0 —8 43 .
com parison o f global estimates o f m a rin e p rim a ry p ro d u c tio n fro m ocean color.
4.
M o o r e M C , S uggett D J, H ic k m a n A E , K i m Y - N , T w e d d le J F , e t al. (2006)
P h yto p lan k to n p h o to ac clim a tio n a n d p h o to ad a p ta tio n in response to e n viro n ­
4 18 .
16
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
21.
B oy d
P W , A ik e n J ,
fluo re sc e n ce
based
K o lb e r
{p u m p
ZS
(1 9 97 ) Com parisons
and
p ro b e )
o f ra d io c a rb o n
m eas u rem e n ts
and
48.
49.
p hotosynthetic characteristics in the N o rth e a s t A d a n tic O c e a n . M a r E co l P rog
C o rn o
G , L e te lie r R M , A b b o tt M R ,
K a rl D A
T e c h n o l 18: 1 9 2 4 -3 4 .
(2 0 06 ) Assessing p rim a ry
50.
p ro d u c tio n v a ria b ility in the n o rth Pacific subtropical gyre: a com parison o f fast
T halassiosira weissflogii. M a r E co l P rog Ser 448 : 6 7 —78.
K r o m k a m p J C , D ijk m a n N A , Peene J , Sim is S G H , Gons H J (2 0 08 ) E stim ating
51.
p h y to p la n k to n p rim a ry p ro d u c tio n in L a ke Ijsselm eer {T h e N e the rlands ) using
v a ria b le fluorescence { P A M -F R R F ) a n d
14C -u p ta k e
25.
26.
27.
E co l P rog Ser 13: 9 9 - 1 0 2 .
52.
Suggett D J {2000) V a r ia b ility o f p h y to p la n k to n p ro d u c tiv ity rates in the A d a n tic
photosynthesis
S o u th a m p to n , U n ite d K in g d o m , D o c to ra l Thesis, 184 pp.
m icroalgae a n d cyanobacteria. J P hycol 38: 17—38.
53.
Suggett D J, M o o r e M C , M a r a ñ ó n E , O m a c h i C , V a r e la R A , e t al. {2006)
54.
H ic k m a n {2007) T h e photophysiology a n d p rim a ry p ro d u c tiv ity o f p h y to p la n k ­
S m yth T J , P e m b e rto n K L , A ik e n J , G e id e r R J {2004) A
56.
R a a te o ja N ,
Seppälä J , K u o s a H
57.
{2004) B io -o p d ca l m o d e llin g o f p rim a ry
58.
T r ip a th y
S C , Ish iza ka J , F u jik i T ,
59.
uptake by
la b o ra to ry study s im ula ting v e rtic a l m ixin g . J G e n e ra l M ic ro b io l 139: 2 2 7 7 —
2 284.
61.
63.
64.
65.
u n d e r transient
A c a d Sei U S A 105: 7 8 8 1 -7 8 8 6 .
Estévez-Blanco P, C e rm e ñ o P , E spiñe ira M , F e rn án d e z E {2006) P h ytoplank ton
66.
67.
Baixas, N W o f Spain). J P la nk ton Res 28: 1 1 5 3 -1 1 6 5 .
G rossm an A R , M a c k e y K R M , B ailey S {2010) A perspective on photosynthesis
flow . J P hycol 46: 6 2 9 -6 3 4
68.
4 0 :4 -2 5 .
B eh ren feld M J , W o rth in g to n K , S herrell R M , C h a v e z FP , S tru tto n P, e t al.
{2006) C o n tro ls on tro p ic al Pacific O c e a n p ro d u c tiv ity revealed th ro u g h n u trie n t
Suggett D J , M o o r e M C , H ic k m a n A E , G e id e r R J {2009) In te rp re ta tio n o f fast
stress diagnostics. N a tu r e 4 42 : 1 0 2 5 -1 0 2 8 .
re p etitio n ra te {F R R ) fluorescence: signatures o f p h y to p la n k to n c o m m u n ity
69.
structure versus physiological state. M a r E co l P ro g Ser 376: 1—19.
K ir k J T O
{2010) L ig h t a n d photosynthesis in a quatic ecosystems, 3r
edition.
L o n d B 363: 2 6 8 7 -2 7 0 3 .
70.
Suggett D J, K r a a y ,G , H o llig a n P, D a v e y M , A ik e n J , e t al. {2001) Assessment o f
71.
K o lb e r Z S , Prásil O , Falkow ski P G {1998) M easurem ents o f v aria b le c hlo ro phyll
72.
Suggett D J , O x b o ro u g h K , B a ke r N R , M a c In ty r e H L , K a n a T M , e t al. {2003)
73.
m easurem ents fo r assessment o f photosynthedc electron transport in m a rin e
use
o f v a r ia b le
fluorescence
74.
tu rn o v e r protocols a n d suggested term inolo gy. E u r J P hycol 38: 103—112.
spring p h y to p la n k to n
b lo o m .
D a v is
RF
L im n o l
The
b la n k
c an
m a ke
a
b ig
diffe re n ce
in
77.
o f active fluorescence
to
estim ate
dyn am ic s
in
th e
F la m e lin g IA , K ro m k a m p J {1984) Responses o f respiration a n d photosynthesis
L i W K W , H a rris o n W G , H e a d E J H {2006). C o h e re n t assembly o f p h y to p la n k ­
to n c om m unities in diverse tem p e ra te ocean ecosystems. P roc R o y a l Soc B B iol
ph y to p la n k to n photosynthesis in situ. L im n o l O c e a n g r 38: 1646—1665.
PLOS ONE I www.plosone.org
n u tr ie n t
Res 16: 1 7 8 1 -1 7 9 1 .
L im n o l O ce a n o g r M e th 2: 3 1 6 -3 3 2 .
U se
and
o f Scenedesm us protuberans Fritsch to g ra d u al a n d steep salinity increases. J P la nk ton
optical d e term inations o f lig h t absorption b y photosystem I I in p h y topla nkton.
{1993)
p ro to z o o p la n k to n
Basin {Baltic Sea) in 2 0 0 2 —2 00 3 d u rin g the G e rm a n G L O B E G
P roject., I n t J E a rth Sei 98: 2 5 1 -2 6 0 .
76.
Suggett D J , M a c In ty r e H L , G e id e r R J {2004) E v a lu a tio n o f biophysical and
Falkow ski P G
P h y to p la n k to n ,
B o rn h o lm
{2 0 0 3 )
{2007) M o d e llin g nitro g e n a n d phosphorus
v a n Beusekom JJE , M e n g e d o h t D , A ugusting C B , S chilling M , Boersm a M
{2 0 0 9 )
o ceanographic m easurem ents. L im n o l O c e a n g r B u ll 12:29—35.
ZS,
Lessin G , Lips I , R audsepp U
O ce a n o lo g ía 49: 2 5 9 -2 7 6 .
75.
O c e a n o g r 51: 2064—2 076.
C u lle n JJ,
T a m m in e n T , A ndersen T {2007) Seasonal p h y to p la n k to n n u trie n t lim ita tio n
lim ita tio n on p h y to p la n k to n g ro w th in N a r v a B ay, south-eastern G u lf o f Fin lan d .
Suggett D J , M a b e r ly S C , G e id e r R J {2006) Gross photosynthesis a n d lake
the
W a g n e r H , J ak o b T , W ilh e lm C {2 00 6) B alancing the energy flo w fro m captured
e utrophic ation. M a r E co l P rog Ser 340: 1 2 1 -1 3 8 .
The
m easurem ents in a quatic ecosystems: differences b etw een m u ltip le a n d single
d u rin g
{2001) Photosystem I I
patterns as revealed b y bioassays over B altic Sea gradients o f salinity and
ph y to p la n kto n . E u r J P hycol 38: 3 7 1 -3 8 4 .
m etab o lis m
M a s o jid e k J , G ro b b e la a r J U , P echar L , K o b liz e k M
lig h t to biom ass u n d e r flu c tu a tin g lig h t conditions. N e w P h yto l 169: 9 5 —108.
Fast re p etitio n ra te a n d pulse a m p litu d e m o d u la tio n c h lo ro p h yll a fluorescence
c o m m u n ity
{2012) D iffe re n t responses o f photosynthesis a n d flo w
cyanobacteria d u rin g a diel cycle. J P la n k to n Res 23: 5 7 —6 6.
e xp e rim en tal protocols. B io c h im Biophys A c ta 1367: 8 8 —106.
{2 0 0 3 )
Q iu
electron tra ns port a n d oxygen p ro d u c tio n in n a tu ra l w aterbloom s o f freshw ater
fluorescence using fast re p etitio n rate techniques: defin in g m e thodology and
RM
S -W , B-S
Synechococcus strains {C yanophyceae). M a r B iol 159 :5 19 —5 32 .
flu o ro m e te r. L im n o l O c e a n o g r 46: 8 0 2 —8 10 .
F o rs te r
L iu
c ytom etric signals to iro n lim ita tio n a n d nitro g e n source in coastal a n d oceanic
photosynthesis in a spring cyanobacteria! b lo o m b y use o f a fast re p etitio n rate
K ro m k a m p J C ,
B eh ren feld M J , H a lse y K H , M illig a n AJ {200 8) E vo lv ed physiological responses
o f p h y to p la n kto n to th e ir inte g rated g ro w th enviro n m e n t. P h il T ra n s R Soc
C a m b rid g e : C a m b rid g e U n iv ers ity Press. 6 6 2 p.
K o lb e r
{2009) Biogeograp hy o f photosynthetic lig h t-
in the oligotrophic oeans: hypotheses c oncerning a ltern a te routes o f electron
B eh ren feld M J , Prásil O , B a b in M , B ru y a n t F {2004). I n search o f a p hysiological
basis fo r covariations in lig h t-lim ite d a n d ligh t-s a tu rated photosynthesis. J Phycol
4 7.
B ib b y T S , Z h a n g Y , C h e n M
h arvesting genes in m a rin e ph y to p la n kto n . PloS O N E 4: e46 01 .
re p etitio n ra te flu o ro m e try a t coastal em baym ents affected b y upw e llin g {Rias
4 6.
C a rd o l P , B a ille ui B, R a p p a p o rt F , D e re lle E , B eal D , e t al. {2 00 8) A n original
a d a p tatio n o f photosynthesis in the m a rin e green alga Ostreococcus. P roc N a tl
photosynthedc efficiency a n d p rim a ry p ro d u c tio n rates estim ated fro m fast
45.
S trzepek R F , H a rris o n PJ {2 00 4) Photosynthetic archite c tu re differs in coastal
a n d oceanic diatom s. N a tu r e 431 : 6 8 9 —6 9 2 .
conditions. P la n t Physiol 9 1 :3 3 1 —337.
4 4.
S canlan D J {2003) Physiological diversity a n d niche a d a p tatio n in m a rin e
Synechococcus. A d v M ic r o b Physiol 47: 1—64.
H o lm e s JJ, W e g e r H G , T u r p in D H {1989) C h lo ro p h y ll a fluorescence predicts
2
Sunda W G , H u n ts m a n S A {1995) Photosynthetic a rchitecture differs in oceanic
a n d coastal ph y to p la n kto n . M a r C h e m 50: 1 8 9 -2 0 6 .
53: 9 0 0 -9 1 3 .
/N O
{2006) M ic ro p h yto b e n th o s v ertical
Res 90: 2 9 ^ 3 .
62.
M a c k e y K R M , P ay ta n A , G rossm an A R , Bailey S {200 8) A photosynthetic
3
S erôdio J , V ie ir a S, C r u z S, C o e lh o H
m ig ra to ry photoresponse as c h aracterized b y lig h t response curces. Photosynth
B ailey S, M e h lis A , M a c k e y K R M , C a rd o l P , F in a zi G , e t al. {2008) A lte rn a tiv e
or N O
K r o m k a m p J , L im b e e k M {1993) E ffe c t o f s h o rt-term v a ria tio n in irrad ia n ce on
light-ha rv es ting a n d photosynthesis o f the m a rin e d ia to m Skeletonema costatum : a
strategy fo r c oping in a h igh-light, lo w -n u trie n t en viro n m e n t. L im n o l O ce a n o g r
43.
Berges J A , G harlebois D O , M a u z e r a ll D C , Falkow ski P G {1996) D iffe re n tia l
in m icroalge. P la n t Physiol 110: 6 8 9 -6 9 6
60.
B adger M R , v o n C a e m m e re r S, R uuska S, N a k a n o H {2000) E le c tro n flo w to
2
D u b in s ky Z , Falkow ski P G , W y m a n K {1986) L ig h t harvesting a n d u tiliza tio n by
effects o f nitro g e n lim ita tio n o n photosynthetic efficiency o f photosystem I a n d I I
S hibata T , O k a m u r a K , e t al. {2010)
to tal phytosynthetic electron flo w to C O
Falkow ski P G , O w en s T G {1980) Light-shade adap tio n - tw o strategies in m a rin e
ph y to p la n kto n . P la n t C e ll Physiol 27: 1 3 3 5 -1 3 4 9 .
M e lro se D C , O v ia tt C A , O ’R e illy J E , B e rm a n M S {2006) Com parisons o f fast
A c ta 1777: 2 6 9 -2 7 6 .
4 2.
Law s E A {1991) Photosynthetic quotients, n e w p ro d u c tio n a n d n e t c o m m u n ity
ph y to p la n kto n . P la n t 66: 5 9 2 -5 9 5 .
Finnish coastal zone, B altic Sea: fast re p ed d o n rate
p hotosynthetic electron flo w to oxygen in m a rin e Synechococcus. B io c h im Biophys
4 1.
W illia m s PJ le B , R obinson C , S onderg aard M , Jespersen A - M , B entley T L , et
p ro d u c tio n in the o pen ocean. D e e p Sea Res 30: 143—167.
1446.
4 0.
of
w ith the d ia to m Skeletonema costatum. J P la nk ton Res 18: 1 961—1974.
{M e h le r reaction) a n d rubisco oxygenase. P h il T ra n s R Soc L o n d D 355: 1 43 3 —
39.
{2004) C h lo ro p h y ll fluorescence as a pro b e
al. {1996) A lg a l 1 4 C a n d to tal c arbon m etabolism . 2. E x p e rim e n ta l observations
m ethodology to
oxygen in hig h e r plants a n d algae: rates a n d co n tro l o f d irec t photored u c tio n
38.
K
a n d b io ta -e n v iro n m e n t
85.
55.
B ay, southwestern J a p a n . E stuarine C oastal S h e lf Sc 87: 163—173.
37.
O x b o ro u g h
s im ilarity profiles
p h y ll fluorescence: a signature o f photosynthesis. S prin ger, D o rd re c h t, pp. 6 5 —
Assessment o f c arb o n - a n d fluorescence-based p rim a ry p ro d u c tiv ity in A ria k e
36.
analyses:
o f O c e a n a n d E a rth Sciences, D o c to ra l Thesis, 237pp.
P e m b e rto n K L , C la rk e R , J o in t I {2006) Q u a n tify in g uncertainties associated
re p ed d o n ra te fluorescence estim ated p rim a ry p ro d u c tio n a n d 14C
35.
B a ke r N R ,
c o m m u n ity
photosynthetic prod u c tiv ity. In : P apageorgiou G C , G o vin d je e, editors. C h lo ro ­
p h y to p la n kto n . M a r E co l P rog Ser 311: 37—46.
34.
in
to n w ith in the deep c h lo ro p h yll m a x im u m . U n iv ers ity o f S o u th a m p to n , School
flu o ro m e try in Case 2 w aters. M a r E co l P rog Ser 267: 9 —26.
33.
a n d photosynthetic pigm ents
C la rk e K R , S om erfie ld I J , G o rle y R N {2008) Testin g o f n u ll hypotheses in
linkage. J E x p M a r B io l E co l 3 6 6 :5 6 -6 9 .
p ro d u c tio n in the S W
32.
curves
D e e p Sea Res I I 5 3 :1 5 7 3 -1 5 9 2 .
1350.
31.
response
e xp lo ra to ry
fro m fast re p ed d o n ra te flu o ro m e try . J o u rn a l o f P la nk ton R esearch 26: 1 33 7 —
30.
irrad ia n ce
Photosynthedc electron tu rn o v e r in the tro p ic al a n d subtropical A d a n tic O ce a n .
d e te rm in e p rim a ry p ro d u c tio n a n d p h y to p la n kto n photosynthedc param eters
29.
M a c ln tr y e H L , K a n a T M , A n n in g T , G e id e r R J {2002) P hoto a cc lim atio n o f
O ceans observed using the Fast R e p e d d o n R a te fluo ro m e te r. U n iv e rs ity o f
w ith the m eas u rem e n t o f p rim a ry pro d u c tio n . M a r E co l P rog Ser 322: 5 1 —59.
28.
Lew is M R , S m ith J G {1983) A S m all V o lu m e , S h o rt-In c u b a tio n -T im e M e th o d
fo r M e a s u re m e n t o f Photosynthesis As A F u n c tio n o f In c id e n t Irra d ia n c e . M a r
techniques. E u r J P hyc ol 43:
3 2 7 -3 4 4 .
24.
M illig a n AJ, A p a ric io U A , B eh ren feld M J {2011) Fluorescence a n d n o n p h o to ­
c hem ical q ue nch ing responses to sim ulate v ertic al m ix in g in the m a rin e d iato m
re p etitio n rate flu o ro m e try a n d 14C m easurem ents. J P hyc ol 4 2 :5 1 —6 0.
23.
L a n e y S R , L e te lie r R M , D esiderio R A , A b b o tt M R , K ie fe r D A , e t al. {2001)
M e a s u rin g the n a tu ra l fluorescence o f p h y to p la n k to n cultures. J A tm o s O c e a n
Ser 149: 2 1 5 -2 2 6 .
22.
T in g C S , O w en s G {1994) T h e effects o f excess irrad ia n ce on photosynthesis in
the m a rin e d ia to m Phaeodactylum tricornutum. P la n t Physiol 106: 763 —770.
o f p h y to p la n k to n
Sei 2 7 3 {15 9 6) 1 9 5 3 -1 9 6 0 .
17
March 2013 | Volume 8 | Issue 3 | e58137
Electron Requirement for Carbon Fixation
78.
79.
W u Y , Peterson I K , T a n g C C L , P la tt T , S ath ye n d ra n ath S, et al. (2 0 07 ) T h e
86
.
n itra te , phosphate, o r iro n starvadon. J P hycol 29: 7 5 5 —766.
W u Y , P la tt T , T a n g C C L , S athye n d ra n ath S (2 0 08 ) R e g io n a l differences in the
87.
Z h a i L , P la tt T , T a n g C , S ath ye n d ra n ath S, W a lls R H (2 0 11 ) P h ytoplank ton
68
8 3.
88
M illig a n
o f P haeodactylum
AJ,
B ehren feld
MJ
tricornutum
(2011).
(B acillariop hyceae)
Surplus
to
photosynthedc
.
6
: e l8 7 5 3 .
R y a n -K e o g h T J , M a c e y A I , G ackshutt A M , M o o r e M G , B ib b y T S (2 0 12 ) T h e
N a p o lé o n C , C la q u in P (2 0 12 ) M u lti-p a r a m e tr ic relationships betw ee n P A M
cyanobacteria! c h lo ro p h yll-b in d in g -p ro te in Is iA Acts to increase the in vivo
m easurem ents a n d c arbon in c o rp o ratio n , an in situ a pproach. P LoS O N E 7:
effective absorption cross section o f P S I u n d e r iro n lim ita tio n . J P hycol 48: 145—
154.
Lon g h u rs t A R (1 9 98 ) E cological geograph y o f the sea. A c ad em ic Press, 3 98 p.
89.
B o n n e t S, G u ieu C , B ru y a n t F , Prasil O , V a n W a m b e k e F e t al. (2 0 08 ) N u tr ie n t
G ree n e R M , G e id e r RJ, Falkow ski P G
L e v ita n O , Rosenberg G , Sedik I , Sedokova E , G r ig e lJ , e t al. (2 0 07 ) E levated
CO
2
enhances n itrogen fix a tio n a n d grow th in the m a rin e c ya nobacterium
Trichodesm ium . G lo b a l C h a n g e B io l 13: 5 3 1 —538.
Biogeosciences 5: 2 1 5 -2 2 5 .
90.
(1 9 91 ) E ffe c t o f iro n lim ita d o n on
L e v ita n O , K r a n z S A , S pungin D , Prásil O , R o s t B , e t al. (2 0 10 ) C o m b in e d
effects o f C O
photosynthesis in a m a rin e d iato m . L im n o l O ce a n o g r 36: 1 77 2 —1782.
8 5.
PS,
P LoS O N E
: 7 8 1 -7 9 1 .
lim ita tio n o f p rim a ry p ro d u c tiv ity in the S outheast Pacific { B IO S O P E cruise).
8 4.
S chrader
apparatus
a n tennae com plexes unde rlie diagnostics o f iro n lim ita d o n in a cyanobacterium .
e 40 28 4 .
8 2.
(1 9 93 ) Response o f the
L a b ra d o r Shelves. J P la n k to n Res 29: 5 0 9 -5 1 4 .
ph enology on the Scotian Shelf. IC E S J M a r Sei
8 1.
G reene R M , O la iz o la M
photosynthetic
tim in g o f the spring b lo o m in the L a b ra d o r Sea. M a r E co l P rog Ser 355: 9—20.
8 0.
G e id e r RJ, L a R o c h e J ,
im p a c t o f sea ice on the in itia tio n o f the spring b lo o m on the N e w fo u n d la n d and
2
a n d lig h t on the N 2 -fix in g cya n o b a cteriu m T ric h o d e s m iu m
IM S 1 0 1 : A m echanistic view . P la n t Physiol 154: 3 4 6 -3 5 6 .
G ree n e R M , G e id e r R J, K o lb e r Z , Falkow ski P G (1 9 9 2 ) Iro n -in d u c e d changes
in lig h t harvesdng a n d photo ch e m ica l energy conversion processes in eukaryodc
m a rin e algae. P la n t Physiol 100: 5 6 5 -5 7 5 .
PLOS ONE I www.plosone.org
18
March 2013 | Volume 8 | Issue 3 | e58137