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Extreme Variations of pC 02 and pH in a Macrophyte
Meadow of the Baltic Sea in Summer: Evidence of the
Effect of Photosynthesis and Local Upwelling
Vincent Saderne1'2*, Peer Fietzek3, Peter Maria Jozef Herman2
1 Benthic Ecology group, GEOMAR: Helmholtz Center for Ocean Research in Kiel, Kiel, Schleswig-Holstein, Germany, 2 Spatial Ecology, NIOZ: Royal Netherlands Institute
for Sea Research, Yerseke, Zeeland, The Netherlands, 3 CONTROS Systems & Solutions GmbH, Kiel, Schleswig-Holstein, Germany
Abstract
The im pact o f ocean acidification on benthic habitats is a m ajor preoccupation o f the scientific com m unity. However, the
natural variability o f pC 02 and pH in those habitats remains understudied, especially in tem perate areas. In this study we
investigated tem poral variations o f the carbonate system in nearshore m acrophyte meadows o f the western Baltic Sea.
These are key benthic ecosystems, providing spawning and nursery areas as w ell as food to numerous com m ercially
im p ortan t species. In situ pC 02, pH (total scale), salinity and PAR irradiance were measured w ith a continuous recording
sensor package dropped in a shallow m acrophyte m eadow (Eckernförde bay, western Baltic Sea) during three different
weeks in July (pC 02 and PAR only), August and Septem ber 2011.The mean ( ± SD) pC 02 in July was 383±117 patm. The
mean ( ± SD) pC 02 and pHtot in August were 2 3 9 ± 2 0 patm and 8.22±0.1, respectively. The mean ( ± SD) pC 02 and pHtot in
September were 1082±711 patm and 7.83±0.40, respectively. Daily variations o f pC 02 due to photosynthesis and
respiration (difference between daily m axim um and m inim um ) were o f the same order o f m agnitude: 281 ± 8 8 patm,
2 1 9 ± 8 9 patm and 1488±574 patm in July, August and Septem ber respectively. The observed variations o f pC 02 were
explained throu gh a statistical model considering w ind direction and speed tog e th e r w ith PAR irradiance. At a tim e scale o f
days to weeks, local upw elling o f elevated pC 02 w ater masses w ith offshore winds drives the variation. W ithin days, prim ary
production is responsible. The results dem onstrate the high variability o f the carbonate system in nearshore m acrophyte
meadows depending on m eteorology and biological activities. We h ig h lig h t the need to incorporate these variations in
future pC 02 scenarios and experim ental designs fo r nearshore habitats.
C i t a t i o n : Saderne V, Fietzek P, Herman PMJ (2013) Extreme Variations of pC02 and pH in a Macrophyte Meadow of the Baltic Sea in Summer: Evidence of the
Effect of Photosynthesis and Local Upwelling. PLoS ONE 8(4): e62689. doi:10.1371/journal.pone.0062689
E d i t o r : Wei-Chun Chin, University of California, Merced, United States of America
R e c e i v e d October 9, 2012; A c c e p t e d March 25, 2013; P u b l i s h e d April 23, 2013
C o p y r i g h t : © 2013 Saderne et al. This is an open-access article distributed under the terms of the Creative CommonsAttribution
License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
F u n d i n g : This work was funded by the European community, Marie Curie ITN CALMARO (PITN-GA-2008-215157). The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
C o m p e t i n g I n t e r e s t s : One of the authors is employed by a commercial company (CONTROS SYSTEMS AND SOLOUTIONS GmbH). This does not alter the
authors' adherence to all the PLOS ONE policies on sharing data and materials.
* E-mail: vsaderne@geomar.de
Introduction
C 0 2(aq) in the surface ocean represents less th a n 1% o f the
dissolved inorganic c arb o n (DIC) w hile H C 0 3_ represents ~ 9 0 %
a n d C 0 3~ ~ 1 0 % . T h e c a rb o n a te system in o p e n oceanic
environm ents is well know n a n d m ost o f the d a ta form ing the basis
for the predictive m odels (see G L O D A P database, [5,6]) are
derived from the open ocean. T hose oceanic actual a n d future
p C 0 2/ p H values are the ones referred to w hen designing ocean
acidification studies [7]. H ow ever, the biogeochem istry o f
nearsh o re ecosystem s features m ore variations a n d differs widely
th a n offshore conditions [8,9], Shallow n earsh o re a n d estilarm e
areas are the h a b ita t o f nu m ero u s b enthic calcifiers. As highlighted
by A ndersson a n d M ackenzie (2012) [10], investigations o n the
effects o f ocean acidification o n calcifiers are neglecting this
na tu ra l variability.
In nearsh o re habitats, the few available investigations w ere
cond u cted on: (1) estuaries, salt m arshes, m angroves a n d m udflats
w here transfers o f carb o n from la n d are occu rrin g (e.g. [11-13])
a n d (2) reefs form ed by corals or calcifying algae because o f the
direct effect o f calcification on the c arb o n a te system (e.g. [14,15]).
T h e c arb o n a te chem istry o f nearshore habitats d o m in a ted by
m acrophytes (kelp forests a n d seagrass a n d /o r seaw eed m eadows)
H u m a n activities since the 19th c entury led to a n increase o f
atm ospheric p C 0 2 from 280 to 392 p a tm [1] a n d the tren d is
rising. Som e scenarios expect a n elevation o f atm ospheric p C 0 2
up to 1000 p a tm d u rin g the 21th century, peaking a ro u n d
1400 p a tm in the y ear 2300 [2,3]. As oceans equilibrate w ith
the atm osphere, dissolution o f C 0 2 in w ater induces a decrease in
p H . G lobal change has alread y led to a n average seaw ater
“ acidification” o f 0. 1 p H units in the w orld ocean [4].
A cidification is e n h an cin g the corrosiveness o f seaw ater to calcite
a n d aragonite, the two isoform s o f calcium carbonates com posing
the shells a n d skeletons o f m arin e organism s. Corrosiveness is
expressed by the satu ratio n states f í arat! a n d H caic. A saturation
state below 1 indicates a tendency tow ards dissolution o f the
crystal. A ragonitic structures (e.g. scleratinian corals, n acre o f
bivalve shells) are m o re soluble th a n calcific (e.g. o u ter shell o f
oyster) [4-5].
O n c e dissolved, C 0 2 becom es p a rt o f the c arb o n a te system,
alm ost entirely com posed o f b ica rb o n ate ( H C 0 3_ ) a n d carb o n ate
ions ( C 0 3~ ). U n d e r actual atm ospheric concentratio ns o f C 0 2,
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C arbonate Chem istry in M acrophyte M eadow s
is alm ost unknow n, even th o u g h they rep resen t ~ 5 % o f the
p rim a ry p ro d u c tio n in the ocean a n d % o f the vegetal biom ass
[16,17]. In these habitats, the c arb o n a te system is driven b y the
photosynthetic physiology o f the m acrophytes, taking u p carb o n
d u rin g the day a n d releasing it by respiration d u rin g the night
[18,19]. Since C 0 2 is a m in o r co m p o n e n t o f D IC a n d its diffusion
ra te in seaw ater is 10,000 tim es low er th a n in air [20], m ost
m acrophytes are relying on H C 0 3- for photosynthesis [21-24],
M acrophyte m eadow s a re highly productive a n d n e t auto tro p h ic
(carbon sink) [25,26] e xporting their excess p ro d u c tio n to the
n e ighboring ecosystem s u n d e r the form o f litter o r dissolved
organic c arb o n [27]. M icrobial d eg rad atio n o f exp o rted organic
c arb o n leads to elevated p C 0 2 a n d hypoxia o f d eeper offshore
w aters [28]. T his p h e n o m e n o n is particularly im p o rta n t in
eu tro p h ied ecosystem s like the Baltic Sea [29]. In the in n er bays
o f the w estern Baltic, local upw elling o f h y percapnie w ater masses
is regularly observed, increasing the surface p C 0 2 u p to
2500 p atm . T his typically h appens a t the e n d o f sum m er w hen
offshore w inds are upw elling deep w aters after long periods o f
stratification [30-32].
T h e aim o f this study, cond u cted in the w estern Baltic Sea over
th ree weeks o f sum m er 2011, was to m easure (1) the d a y /n ig h t
variations o f p C 0 2 due to photosynthesis a n d respiration o f a
m acro p h y te bed, (2) the evolution o f the baseline p C 0 2 over
sum m er a n d (3) the effect o f local upwellings o n the c arb o n a te
system a n d its diel variations. T h e variations o f D IC , m easu red in
the m acrophyte m eadow , w ere m odeled w ith a statistical m odel
considering w ind direction a n d speed to g eth er w ith photosynthetically active rad iatio n (PAR).
m easures the C 0 2 m ole fraction in a h eadspace b e h in d a
m em b ran e equ ilib rato r w ith a tw o-w avelength non-dispersive
infra-red detector (ND IR). T h e equ ilib rato r is com posed o f a flat
silicone com posite m em b ran e, the N D IR u n it a n d additional
sensors for pressure, te m p e ra tu re a n d relative hum idity used to
c o rrect the N D IR signal a n d calculate the p a rtial pressure. A small
internal p u m p insures the continuous circulation o f air in the
equilibrator. T o co rrect the drifting o f the in stru m en t w ith tim e,
regular zeroings are autom atically p erfo rm ed b y scrubbing the
C 0 2 from the internal gas stream . T h e zeroings are acco u n ted
d u rin g post processing o f the d a ta . A first description o f the
in stru m e n t can b e found in [36] a n d deploym ents o n various
platform s are presen ted in [37]. T h e in stru m e n t was calibrated by
the m an u fa ctu re r p rio r to every d eploym ent in the ran g e o f 100—
1000 p a tm a t 17°C, 18°C a n d 18°C for the first, second a n d th ird
deploym ent respectively. A n overall accuracy o f b e tte r th a n ± 1 %
o f the u p p e r range value is assum ed for post processed d ata. In
o rd e r to achieve a co n stan t a n d sufficiently short response tim e o f
the instrum ent, the H y d ro C ™ is eq u ip p ed w ith a w ater p u m p
(Sea-Bird E lectronics, USA) th a t provides a continuous w ater flow
o f approx. 35 m l sec- to the m em b ran e, leading to a response
tim e T 63% o f 3 m in a n d a Tgg% o f a pproxim ately 15 m in. T hese
response tim es are sufficiently fast to resolve the observed signal
changes w ith o u t the n eed for signal deconvolution. T o co rrect the
p C 0 2 series for the in stru m e n t drift, the zerooing signals w ere
re g ard e d as nodes a n d linearly interp o lated in tim e to result in a
sm ooth signal drift correction th ro u g h o u t the deploym ent tim e.
Salinity (psu), voltage (analogue signal from the p H m easure­
m ent) a n d tem p e ra tu re (°C) w ere re co rd e d autom atically every
45 m in w ith a p H -m e te r/c o n d u c tim e te r M ettler-T oledo S G 7 /8
(M ettler T oledo, Sw itzerland). F o r the m ea su re m e n t o f p H on
total scale, seaw ater T R IS p H buffers for 15 psu w ere m ade
a ccording to the S O P 6a o f D ickson et al. (2007) [38]. A com bined
electrode w ith a solid polym er electrolyte reference, e quipped w ith
a n N T C (negative tem p e ra tu re coefficient) therm istor was used
(Inlab e x p ert p ro , M ettler T oledo, Sw itzerland). T h e calibration o f
a new electrode was m ade 24 h before each deploym ent. T o do so,
the T R IS buffer was im m ersed in a therm ostatic b a th a n d the
voltage o f the p H electrode was m easu red w ith a n accuracy o f
± 0 .1 m V . T h e tem p e ra tu re o f the buffer was varied by 1.5°C
a ro u n d seaw ater tem p eratu re. T h e tem p e ra tu re corresponding to
every m V change was re co rd e d w ith accuracy b e tte r th a n 0 .0 U C
w ith a Fluke 5658 reference th erm o m eter d o ted o f a 5608
p latin u m resistance sensor (Fluke, USA). T his process was
re p ea te d b y increasing a n d decreasing the te m p e ra tu re to get an
average voltage (mV) versus T (°C) reference curve for the electrode
in the buffer. T h e N T C sensor o f the p H sensor, o f resolution
0.1 °C, was calibrated against a reference th erm o m eter a n d the
resulting regression was achieved w ith a R 2 > 0 .9 9 . T h e resulting
equatio n was used to co rrect the sam pled tem p eratu re. T h e
sam pled voltage a n d c o rrected te m p e ra tu re w ere c onverted to
p H tot by m aking use o f the initial T R IS buffer calibration o f the
electrode a n d by using the equations given in the S O P 6a. In the
lab, w ork c o n d u cted o n C ertified R eference M aterial (CRM )
(A ndrew D ickson, Scripps Institution o f O ceanography) together
w ith 35 psu buffers d e m o n stra ted a n accuracy o f 0.003 to 0.005
p H units a n d a precision b e tte r th a n 0.001 p H unit. H ow ever, this
accuracy was n o t re ac h ed in the field a n d therefore the p H series
w ere n o t used to derive the c arb o n a te system b u t instead the
alkalinity from discrete sam ples (see 2.3 for m eth o d a n d 4.4 for
discussion on the m ethod).
Salinity was m easu red w ithin 0.01 psu by a M ettler T oledo
Inlab 738 conductivity p ro b e after calibration a t 25°C w ith KC1
0.1 m ol L -1 (Fischer Scientific, USA). T h e P A R irrad ian ce (400 to
Materials and M ethods
2.1 Study site
Physico-chem ical p a ram ete rs o f seaw ater w ere reco rd ed in a
m acro p h y te m eadow (3 m depth) in E ckernförde Bay (western
Baltic Sea, G erm any, 5 4°27' N , 9°54' E, see Fig. 1), du rin g
3 weeks o f sum m er 2011: July: 2 9 .0 6 -0 8 .0 7 , August: 2 9 .0 7 -0 5 .0 8
a n d Septem ber: 0 9 .0 9 -1 6 .0 9 . In Ju ly , only p C 0 2 a n d PA R
irrad ian ce w ere re co rd e d by two in d ep e n d en t sensors. F or the
A ugust a n d S eptem ber deploym ents, a m ultim eter reco rd in g p H ,
salinity a n d te m p e ra tu re was a d d ed to the C 0 2 a n d P A R sensor.
W in d speed (m s ’) a n d direction (rad) w ith a resolution o f 10 m in
w ere p rovided b y the m eteorological station o f A schau in
E ckernförde Bay (54°27'40 N , 9 °5 5 '3 0 E) belonging to the
division o f m arin e technology a n d research o f the G e rm an N avy.
T h e nearsh o re h a b ita t o f E ckernförde is a m ixed b o tto m type
d o m in a ted b y m acrophyte vegetation. T h e m acrophyte vegetation
covers a pproxim ately 75% o f the surface. D o m in an t species are
the b ro w n algae Fucus serratus (40-60% o f the m acrophytes),
grow ing o n stones a n d rocks a n d the seagrass postera marina (< 1 0 %
o f the m acrophytes) grow ing on sandy b ottom s [33]. T h e inner
basin reaches a m ax im u m d e p th o f 28 m in gende slope. T h e
w ater colum n is stratified in sum m er, w ith a pycnocline a ro u n d
1 5 m d e p th [34]. S eptem ber is the p e rio d o f m axim al stratification
a n d hypoxia in the deep w ater. H ence, 0 2 reaches m inim al
concentrations o f a b o u t 30 p M , associated w ith peaks o f p C 0 2 up
to 2500 p a tm a n d accum ulation o f dissolved m eth a n e [29,35]. N o
specific perm its w ere req u ire d for the study, the location is not
privately-ow ned o r p ro tec te d in a n y w ay a n d the study did not
involve en d an g e red or p ro tec te d species.
2.2 The autonom ous measuring system
T h e p C 0 2 was m easured w ith a H y d ro C ™ u n d erw ater sensor
(C O N T R O S Systems & Solutions, G erm any). T h e in stru m en t
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C arbonate Chem istry in M acrophyte M eadow s
E9°50‘
52'
54'
56'
N54°
29'
28'
leteo station
Aschau
E c k e rn fö rd e
Sampling site
27'
Baltic ^
»_S e a %
Schnellm ark
wood
Figure 1. Stu dy site. M ap of th e inner Eckernförde Bay indicating th e locations of th e survey site an d th e m eteorological station, urban area
(brown) an d fo rests area (green).
doi:10.1371/jo u rn al.pone.0062689.g001
700 nm ) was re co rd e d every 5 m in using a L I-192 q u a n tu m sensor
con n ected to a L I- 1400 d a ta logger (Li-Cor Biosciences, LTSA). All
series w ere exten d ed to one m inute interval series by linear
interpolation.
w ind speed w eighted b y w ind direction (WWt).
W W j = w ind sp e e d \m s ~ 1] •eos ( w in d direction [rod] + W up ),
W ith W up bein g a p a ra m e te r b etw een 0 a n d 2tt, corresponding to
the w ind direction for w hich w ind-induced upw elling is m axim al.
As exam ples, if W up = 0 o r 2tt, m axim al weights are given to
n o rth e rn winds, if W up = Jt m axim al weights are given to
S o u th ern w inds. A “ left-sided” ru n n in g integration was p erform ed
o n the w eighted w ind tim e series over a p e rio d kw:
2.3 Calculation o f the carbonate system
Sam ples for alkalinity w ere taken a t the beginning, m iddle a n d
e n d o f the m easu rem en t periods o f A ugust (the 29.07, 02.08 a n d
05.08, no replication) a n d S eptem ber (the 09.09, 13.03 a n d 16.09,
one replicate). Alkalinity was m easured w ith a n accuracy o f
± 5 pinoi kg 1 using a n open cell poten tio m etric titra to r as
described in the S O P 3b o f [38] (T itrando 888, M eth ro m ,
Sw itzerland). A regression was calculated b etw een the total
alkalinity a n d salinity o f the sam ples from A ugust a n d S eptem ber
pooled together. T h e regression was highly significant (F-statistic:
pC O .001, R 2 = 0 .8 3 , n = 9): Alkalinity = 9 0 5 .1 7 * Salinity +59.
83, w ith b o th slope a n d intercept significant at pCO.OOl a n d
p < 0 .0 1 (t-test, n = 9). T herefore, the alkalinity for the entire
p erio d was estim ated from the salinity series. T h e D IC , f í arat! a n d
fecale w ere derived from calculated alkalinity a n d the m easured
pC O o acco rd in g to the equations described in [39] w ith the R
package Seacarb [40] using first a n d second c arb o n a te system
dissociation constants for estilarm e systems from [41] a n d the
dissociations constants o f H F a n d H S 0 4 - o f [42,43].
Cmy = /i,,, + ctw Jrr=
W h ere C w t is the 24 h running-average series o f D IC a t tim e t,
W W , is the w eighted w ind speed a t tim e t, p w a n d
are
regression p a ram ete rs a n d kw is d e term in ed as the integration
p e rio d yielding the best fit. P aram eters in the regression w ere
chosen to m inim ize residual variance. In the regression betw een
tim e series, form al hypothesis tests, F-statistics a n d regression
coefficients w ere n o t considered as th ey w ould be biased due to
auto-correlation.
T h e w ithin-day variations o f D IC , Cid w ere m odeled by
exponentially w eighted ru n n in g integration o f the P A R series
over a p erio d o f 12 hours w ith a n exponential decay rate X
(m in- 1 ):
2.4 Statistical m odeling
T h e calculated D IC series o f A ugust a n d S eptem ber was
explained th ro u g h a statistical m odel. It considered th a t (1) the
weekly tren d o f the D IC series is caused b y the upw elling o f DICIrich b o tto m w ater, (2) the diel variatio n o f the D IC series is caused
by p rim a ry p ro d u c tio n a n d respiration o f the m eadow . T h e weekly
trends o f D IC (Cw) w ere separated from the diel oscillations (Cid)
by a central ru n n in g average w ith a tim e fram e o f 24 h. LTpwelling
was assum ed to be driven b y w ind. C w was fit by a function o f
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hv W W {x)dx,
fX = t
Cd, = fid + ad
P A R { x )-e ( - X(,- l))dx
x = t-1 2 h
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C arbonate Chem istry in M acrophyte M eadow s
T h e night peaks (m ean ± SD) o f p C 0 2 w ere 2 3 9 7 ± 4 2 5 patm ,
w ith drops o f p H to (m ean ± SD) 7 .2 6 ± 0 .0 7 . D u rin g daytim e,
m in im u m p C 0 2 levels w ere still m u ch h igher th a n atm ospheric
concentrations w ith m in im a o f (m eans ± SD) 681 ± 211 p a tm a n d
corresponding m ax im a o f p H o f 7.77 ± 0 .1 8 .
In a final step, the irrad ian ce a n d w ind sub-m odels w ere
sum m ed to o b tain the final m odel. T h e sta n d ard deviation o f the
residuals betw een m odel a n d D IC observation w ere considered for
the p a ram ete riz atio n o f W up, kw a n d X.
Results
3.2 Carbonate system
3.1 Measures
In August, m eans ± SD o f the w eek a n d d a y /n ig h t variations o f
D IC w ere 1609± 37 pm ol kg-1 a n d 131 ± 4 5 pm ol k g -1
respectively (Fig. 4 central left panel). T h e seaw ater was always
sup ersatu rated w ith respect to b o th a ragonite a n d calcite w ith diel
m eans ± SD o f 2 .2 ± 0.2 a n d 3 .7 ± 0 .3 a n d m eans ± SD d a y /n ig h t
variations o f 1 .4 ± 0 .6 a n d 2 .4 ± 0 .9 respectively (see Fig. 4, top left
panels).
In S eptem ber the daily m ea n ± SD D IC concentrations
preced in g a n d du rin g the upw elling event w ere 1 8 2 9 ± 4 5 a n d
2 1 5 8 ± 27 pm ol kg *, respectively (Fig. 4 central right panel). T h e
diel variations o f D IC w ere h igher before th a n d u rin g the
upw elling, w ith m ea n ± SD o f 2 5 9 ± 10 pm ol kg 1 against
2 0 5 ± 9 1 pm ol kg *, respectively.
Before the upw elling, the seaw ater was alm ost always supersat­
u ra te d for aragonite a n d calcite (see Fig. 4 top right panel, 09.09 to
13.09). H ow ever a t the hours o f m axim al p C 0 2 (6:00), aragonite
saturation d ro p p e d below 1: m ea n ß arat!: 0 .8 ± 0 .3 (± SD).
O ppositely, seaw ater reach ed m axim a for ß arat! a n d ß caic a ro u n d
18:00. T h e resulting diel oscillations w ere o f 4 .3 ± 0 .3 a n d 2 .6 ± 0 .2
for calcite a n d aragonite, respectively.
D u rin g the upw elling event the seaw ater was constantly
u n d e rsatu ra te d w ith m ea n ± SD ß caic a n d ß araa o f 1 ± 0 .5 a n d
0 .6 ± 0 .3 , exception m ade o f the hours a ro u n d 18 h, w ere m odest
m ax im a (m ean ± SD) o f 1 .9 ± 0 .6 a n d 1.1 ± 0 .4 w ere reach ed (see
Fig. 4 top right panel, 13.09 to 16.09).
T h e th ree weeks revealed im p o rta n t d a y /n ig h t oscillations o f
p H a n d p C 0 2. T h e p C 0 2 increased d u rin g the night a n d
decreased d u rin g the day re ac h in g m in im a a n d m ax im a at 18:00
a n d 6:00 respectively. T h e p H inversely m irro re d these p C 0 2
variations.
In Ju ly , only p C 0 2 a n d light was recorded. T h e m ea n p C 0 2 o f
the w eek was 390 p a tm (m ean ± SD), corresponding to the
atm ospheric C 0 2. H ow ever, diel oscillations o f 281 ± 8 8 p a tm
(m ean ± SD) w ere recorded, w ith a phase shift o f ~ 6 h betw een
light a n d p C 0 2 cycles. T his shift, co m m o n to all three
m easu rem en t periods is illustrated for Ju ly in Fig. 2.
In August, seaw ater was u n d e rsatu ra te d for C 0 2 c o m p a red to
the atm osphere w ith a w eek m ea n o f 239 p a tm only. H ow ever, the
diel variations rem a in e d com p arab le to those o f Ju ly w ith a m ean
o f 2 1 9 ± 2 4 p a tm (± SD) (Fig. 3, top left panel). T h e m ean ± SD
daily m axim al a n d m inim al p C 0 2 values w ere 3 7 4 ± 6 7 a n d
155 ± 3 2 , respectively. T h e m axim al am plitude was 416 patm . T h e
p H variations m irro re d fluctuations in p C 0 2 w ith a weekly m ean
o f 8.21, m ea n diel am plitude o f 0 .3 4 ± 0 .1 5 (± SD) a n d m ea n daily
m in im u m a n d m ax im u m o f 8 .0 3 ± 0 .0 7 a n d 8 .3 7 ± 0 .0 8 (± SD).
T h e average salinity a n d tem p e ra tu re d u rin g the w eek w ere
1 4 .5 ± 0 .3 psu a n d 1 9 .1 ± 0 .7 °C , respectively (Fig. 3, low er left
panel).
T h e recordings o f S eptem ber exhibit a strong difference
betw een the b eginning (09.09 to 13.09) a n d the e n d o f the w eek
(13.09 to 16.09). T h e m ea n ± SD salinity a n d tem p e ra tu re du rin g
the first th ree days w ere 17.8± 0.6 psu a n d 1 5 .9 ± 0 .6 "C while
d u rin g the three last days they increased a n d decreased to
2 0 .7 ± 0 .5 psu a n d 1 2 .4 ± 0 .4 "C respectively (Fig. 3, low er right
panel). T his sudden decrease in seaw ater density is revealing an
upw elling occu rrin g in the m iddle o f the week. C onsequently, we
observed a large discrepancy o f the p C 0 2/ p H b etw een those two
periods w ith m eans o f 426 p a tm /8 .1 4 a n d 1593 p a tm /7 .4 6
respectively (Fig. 2, top right panel). In th a t second p a rt o f the
week, oscillations o f p C 0 2 becam e extrem e. T h e m axim al daily
am plitudes reco rd ed w ere 2184 p a tm p C 0 2 a n d 1.15 p H units.
3.3 Model
T h e D IC calculated from p C 0 2 a n d alkalinity a n d the D IC
p red icted b y the statistical m odel for A ugust a n d S eptem ber are
presen ted in Fig. 4 central panels. T h e differences b etw een b o th
are p re sen te d in Fig. 4. low er panels (residuals). In A ugust, the
m odel pred icted a diel D IC m ean (± SD) o f 1610 ± 16 pinoi k g -1
a n d diel am plitudes o f D IC o f 8 6 ± 1 4 pinoi kg 1 (m ean ± SD).
T h e differences b etw een m odeled a n d calculated D IC is 1 pinoi
k g -1 for the diel average a n d 44 pinoi k g -1 for the diel am plitude.
In Septem ber, the m odel p red icted a diel D IC m ea n (± SD) o f
1852 ± 83 pm ol k g -1 before the upw elling a n d 2143 ± 4 7 pinoi
kg 1 d u rin g the upw elling. T h e differences w ith the calculated
D IC are 23 pinoi kg 1 a n d 15 pinoi kg *, respectively. Before
a n d du rin g upw elling, the diel am plitudes o f D IC p red icted by the
m o d e la re 141 ± 6 1 pinoi kg 1 a n d 15 0 ± 107 pinoi kg 1 (m ean ±
SD), respectively. T h e difference from the calculated D IC is
117 pinoi kg 1 a n d 55 pinoi kg ’.
T h e set o f p a ram ete rs p ro d u c in g the best fitting m odels are W up
= 3 tt/2 , corresp o n d in g to w esterly w ind, a p e rio d o f integration kw
o f 55 h a n d X o f 0.0025 m in _1a n d 0.001 m in -1 for A ugust a n d
S eptem ber respectively. T h e sta n d ard deviation o f the residuals
betw een m odeled a n d calculated D IC are 25 pm ol kg 1 a n d
49 pm ol k g - 1 , corresp o n d in g to percentages o f unexplained
variatio n o f 1.6% a n d 2.5% for A ugust a n d S eptem ber
respectively (Fig. 3 low er panels). Fig. 5 presents, for S eptem ber
only, the evolution o f the m odel residuals as function o f the w ind
direction (Wup) a n d the integration p erio d (kw). E asterly w inds as
m axim al w eights pro d u ce the w orst fitting m odels while westerly
w inds the best fitting ones, southerly a n d no rth erly w inds are
in term ediate. T h e p a ra m e te r X h a d less influence o n the outcom e
o f the m odel (Fig. 6), increasing its accuracy b y a m axim um o f 2 to
800
n
600 -
*
400 ■
0
U
200-
1500
ID 1 0 0 0
3.
%
%
D a te (U T C )
Figure 2. C om parison b e tw e en Light and p C 0 2 series in July.
Dark bands: period of darkness. Dashed lines: estim ated cen ter o f th e
daylight distribution.
doi:10.1371/jo u rn al.pone.0062689.g002
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C arbonate Chem istry in M acrophyte M eadow s
9.0 -,
5
3000
'E' 2500 8.5 ■
% 2000 3 1500
8.0
«
7.5
O* 1000
£
I
500-
0J
o- 7.0 J
0
u
20
i
^ 231
- g
-3
-i
-£
E 18
3 16
E
ai 14
1
S
12
-
21
19
17
15
™ 13
10-1
-
11 J
T i m e (U TC)
Figure 3. In situ m easu rem en ts for A u gu st and S ep tem b er. p C 0 2 (cyan), pH (red) Salinity (black) and tem p e ra tu re (dark blue) recorded in
A ugust (left) an d S ep tem b er (right). The recording frequency w as o n e m inute for p C 0 2 an d 45 m inutes for th e 3 o th er p aram eters. Sym bols in th e
p lots m ark th e recording events; linkage b etw e e n th e m easu rem en ts every 45 min w as achieved by linear interpolation. Secondary vertical gridlines
unit: 6 h.
doi:10.1371/jo u rn al.pone.0062689.g003
4 pm ol kg- 1. D espite its p o o r effect on the m odel, the presence o f
this p a ra m e te r is justified by the consideration o f the decrease o f
the day length b etw een A ugust a n d S eptem ber (the p e rio d o f
integration o f the irrad ian ce is fixed to 12 h in both).
4.1 Inter-weekly dynamics
T h e p C 0 2 o f o u r m easu rem en t site exhibited very different
weekly trends over the sum m er. In A ugust, w e observed an
im p o rta n t a n d stable p C 0 2 u n d ersatu ratio n . T his reflects the
conditions o f the w hole Baltic a t this period, g e n era te d b y the
succession o f bloom s o f phytop lan k to n a n d c yanobacteria [44,45].
In S eptem ber this stable condition is in te rru p ted by the
strengthening o f the westerly w inds, leading to the upw elling o f
the w ater masses isolated until th en below the pycnocline. T h e
chem istry o f the deep w aters o f E ckernförde b a y are m o n ito red
since 1957 a n d p C 0 2 o f ab o u t 2500 p atm , linked to h eterotrophic
processes, are yearly observed in sum m er (Boknis Eck tim e series:
Discussion
In o u r study, w e show ed the im p o rtan ce o f the diel variations o f
p C 0 2 a n d p H due to photosynthesis a n d the im p o rtan ce o f the
variations o f the c arb o n a te chem istry baseline over sum m er. W e
d e m o n stra ted the interactive effects o f upw elling a n d algal
m etabolism o n the c arb o n a te chem istry w ith a sim ple statistical
m odel.
7
6
3
5 4 3 2 -
1 0 J
2400 -,
b
2150 -
Ö
1900 -
X
3
1650 1400 -
Ijl
0
g
-1 0 0
-
®
-200
-
A
A
A
A
A
A
A
A
Figure 4. C alculated and m o d e led c arb on ate chem istry. Top panels: S aturation sta te s for calcite (light brown) and aragonite (dark brow n) for
A ugust (left) and S ep tem b er (right). Dashed line: S aturation threshold. Central panels: O bserved (cyan) an d m odeled (red) DIC for A ugust (left) and
S ep tem b er (right). The residuals b etw een m odel and observations are p resen ted in b o tto m left and right for A ugust and S ep tem b er respectively.
S econdary vertical gridlines unit: 6 h.
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C arbonate Chem istry in M acrophyte M eadow s
80
70
60
O)
50
0
0.002
0.004
0.006
0.008
0.01
A (m irr1)
South
North
West
Figure 6. S en sitivity o f th e m od el to 4. Evolution of th e stan d ard
deviation o f th e residuals b etw e e n m odel and observation in pm ol k g -1
DIC in A ugust (red) and S ep tem b er (black) as a function o f X (m in-1 ),
th e in stan tan e o u s rate o f increase used for th e exponentially w eig h ted
running integration of th e irradiance series.
doi:10.1371/journal.pone.0062689.g006
North
2t t
W up (R a d ia n )
stronger d u rin g the upw elling th a n before b u t we observe the
opposite for D IC (m ean ± SD D IC : 258.6 ± 10.5 pm ol k g -1
against 205.1 ± 9 0 .7 pm ol kg '), possibly revealing a reduction o f
photosynthesis d u rin g the upw elling. T his could b e explained by
an osm otic stress en g en d ered by a ra p id increase o f salinity [51,52]
ra th e r th a n b y the elevated p C 0 2. Indeed, a n y increase in D IC
a n d p C 0 2 is p re su m ed to be beneficial to m arin e m acrophytes
[53], even if this have never b e en form ally p ro v e n [54],
Figure 5. Sen sitivity o f th e m od el to th e integration period le,
and w ind direction Wup. C ontour plot o f th e sta n d ard deviation of
th e residuals b etw een m odel an d observation in pm ol kg-1 DIC (color
palette) for th e S ep tem b er series as a function of Wup, th e azim uth of
reference used as maximal w eight, and th e kw, th e period o f th e
running in teg ratio n of th e w eighted wind series.
doi:10.1371/jo u rn al.pone.0062689.g005
[46]). O u r study shows th a t the nearshore b io ta in shallow w ater is
exposed to these high concentrations d u rin g upw elling events. T h e
deep-w ater p C 0 2 is p re su m ed to increase in the future by the
co njunction o f h igh er atm ospheric p C 0 2 a n d red u ced salinity a n d
alkalinity o f the Baltic Sea [32]. M elzner et al. (2012) [29] are
expecting this deep w ater body to reach p C 0 2 o f 4000 to
5000 p a tm a n d the h ypercapnie events o f S eptem ber to increase
in m agnitude. Besides, the frequency a n d d u ra tio n o f those
upw elling events could also increase as a reinforcem ent o f the
w esterly w inds in th e Baltic region is expected w ith global w a rm ing
4.3 Model
W e w ere able to explain the D IC variations o f A ugust a n d
S eptem ber to a n accuracy o f± 5 0 pm ol kgw ith a simple
statistical m odel (three p a ram ete rs only), based o n w ind a n d PA R .
T h e w eighing p ro c ed u re o f the w ind speed, although sim ple in its
geom etric a p p ro ach , a p p ea red to w ork very well as a n explanation
o f the m ulti-day trends.
O u r m odel designates w esterly w inds as responsible for
upw elling. T his result is slightly different from previous observa­
tions a n d sim ulations in o th er regions o f the Baltic Sea identifying
southw esterly w inds as bein g the m ost effective [30], T his small
discrepancy is certainly due to the east-west orien tatio n o f
E ckernförde bay c o m p a red to the general n o rth -east/so u th -w est
o rien tatio n o f the Baltic Sea. T h e use o f exponentially w eighted
integration o f irrad ian ce as a proxy for p rim a ry p ro d u c tio n was
less effective th a n the sim ilar a p p ro ac h used for the upwelling.
Indeed, w hile the daily D IC m eans are quite accurately p red icted
(< 2 0 pinoi kg '), the diel am plitude is system atically underesti­
m ate d b y 40 to 70 pinoi kg- 1 D IC . T his variation, u nexplained by
the m odel, could b e due to h e terotrophic respiration, air-sea
exchange o f C 0 2 [17] or diel v a riation o f alkalinity as discussed in
4.1. H ow ever, despite the simplistic n a tu re o f o u r m odel, it is a first
step in the u n d erstan d in g a n d prediction, in a context o f global
change, o f the c arb o n a te system dynam ics in the Baltic n earshore
areas.
[47].
4.2 Daily oscillations
D iel oscillations, related to photosynthesis a n d respiration, are
superim posed to the w eek scale dynam ics. In no rm al sum m er
conditions (without upwelling), the m ea n (± SD) am plitudes o f the
diel variations w ere 2 4 3 ± 9 5 p a tm C 0 2 (July, August) a n d
0 .3 4 ± 0 .1 5 p H units (August only). Such diel variations have
already b e en observed in m acro p h y te stands w orldw ide: in
seagrass beds o f A ustralia [16], M e d ite rran e a n [48] a n d Z an zib ar
[19], in tidal rocky-shores o f the n o rth ea stern Pacific [49] a n d in
algal m eadow s o f the D an ish islands [18], A m ong nearshore
ecosystem s, the highest diel variations are o ccurring in m acrophyte
d o m in a ted ecosystem s, upw elling areas a n d estuaries [50], O u r
study site cum ulates those three characteristics: brackish, weakly
buffered a n d eu tro p h ied ecosystem d o m in a ted b y m acrophytes
a n d subm itted to upw elling. W e re co rd e d diel oscillations o f
1 6 0 4 .9 ± 7 9 5 .7 p a tm (m ean ± SD) d u rin g the upw elling event o f
S eptem ber. T o o u r know ledge only near-shore m angroves exhibit
w ider diel variations w ith 3500 p atm reco rd ed in the B erm uda
4.4 Measurement reliability
T h e accuracy o f the post-processed p C 0 2 d a ta is expected to be
< ± 1 0 p a tm for values w ithin the calib rated m easuring range o f
1 0 0-1000 p atm . A n ad ditional e rro r can be expected w h en the
p C 0 2 exceeds the m easuring range as in this case the calibration
polynom ial o f the instrum ent is extrapolated. W e expect this e rro r
to b e ± 1 5 0 p a tm a t m ax im u m for the highest p C 0 2 reco rd ed in
S eptem ber at a ro u n d 2600 patm .
[ 10].
H ow ever, the im p o rtan ce o f these variations is relative, as the
fraction o f D IC presen t as C 0 2(aq) in high p C 0 2/lo w p H seaw ater
is h igher th a n in low p C 0 2/h ig h p H seaw ater (see B jerrum plot in
e.g. [39]). T hus, in Septem ber, the diel variations o f C 0 2 are
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D espite o u r efforts, w e did n o t achieve in the field the p H
accuracy necessary to use it as in p u t p a ra m e te r for the derivation
o f the c arb o n a te system, as we a re able to in laboratory. W e
estim ate the e rro r in p H o f the o rd e r o f 0.01 due to u n correctable
drift du rin g the m ea su re m e n t periods. In the conditions o f
te m p e ra tu re a n d salinity o f the w estern Baltic, such inaccuracy
in p H produces anom alies in derived alkalinity o f the o rd e r o f 10—
100 pm ol kg 1 a t p H / p C 0 2 inferior to 7 .8 /8 0 0 p a tm a n d up to
1000 a t h igher p H /lo w e r p C 0 2. F or future field studies, D urafets
sensors [55] o r spectrophotom etric sensors [56] rep resen t p ro m ­
ising alternatives to glass electrodes, b o th capable o f reach in g
accuracies o f 0.001 to 0.0001 p H units. W e h a d to perform
alkalinity titrations a n d rely o n a salinity to alkalinity relationship
to achieve the calculations. T h is m eth o d is relevant [57,58] a n d we
estim ate the e rro r on the derived D IC to b e < 1 5 pm ol k g -1 D IC .
H ow ever, it ignores a n y changes o f alkalinity a t co n stan t salinity.
T his p h e n o m e n o n is very im p o rta n t in coral a n d shellfish reefs due
to the uptake or release o f C a 2+ b y calcification o r dissolution
[59,60]. H ow ever, in m acrophyte ecosystem s, we expect very
m arginal diel variations o f alkalinity due to photosynthesis a n d
respiration [61].
m ain tain ed a t sim ilar p C 0 2 are re d u ce d by 56% a n d 41%
respectively [63]. Besides, the grow th o f the Baltic brackish
b arn ac le Amphibalanus improvisus, com petitor o f Mytilus for space,
rem ains unaffected a t b o th larval a n d a d u lt stage a t p C 0 2
> 3 0 0 0 p a tm [64], M acro p h y te m eadow s are also tran sien t
habitats, sheltering early life stages o f nu m ero u s anim al species.
T hose m ight exhibit m ore tolerance to ocean acidification as well.
As exam ple, the spawns o f Baltic herrings Clupea harengus, deposited
o n m acrophyte beds [65], are n o t affected in their em bryonic
developm ent by high p C 0 2/lo w p H [66]. T h e volatility o f the
c arb o n a te system a n d the extrem e acidic events we observed could
have ex erted a selective pressure o n Baltic populations, explaining
the resistance o f the local fauna to acidification stress in laboratory.
N evertheless, all the studies qu o ted previously w ere cond u cted
u n d e r stable elevated p C 0 2. N o n e coupled elevated p C 0 2
baseline a n d the diel variations we observed.
Conclusion
O u r study represents one o f the first attem pts o f high resolution
continuous m ea su re m e n t o f the c arb o n a te system in the highly
variable e n v iro n m en t th a t is the Baltic S ea’s n earshore. T h e three
weeks show ed quite different results related to the dynam ics o f the
w hole Baltic c arb o n a te system, to the m eteorological condition
a n d to very local processes o f photosynthesis a n d respiration. T his
study highlights the im p o rtan ce o f the n a tu ra l variations o f p C 0 2
a n d p H a n d em phasizes the consideration o f these in ocean
acidification studies o n nearsh o re organism s.
4.5 Effect on fauna
T h e daily oscillations o f p C 0 2 gen erated by photosynthesis
could be o f prim e im p o rtan ce for calcifiers, creating a t daytim e
periods o f high saturation states favourable to C a C 0 3 precip ita­
tion. Such coupling b etw een photosynthesis a n d calcification has
already b e en observed in a H aw aiian coral re e f by D ru p p et al.
(2011) [59] a n d S h am b erg er et al. (2011) [60] w here calcification is
m axim al a t m idday w hen the p C 0 2 is m inim al due to planktonic
photosynthesis. In th a t reef, the intensity o f the photosynthesis is
m o d u lated b y w ind driven inputs o f n utrients from the flum e o f a
n e ighboring estuary.
In general, studies cond u cted o n w estern Baltic populations o f
anim als, calcifying or not, ten d to dem onstrate th eir tolerance to
acidic conditions [62]. Also, the Baltic pop u latio n o f the mussels
Mytilus edulis experiences red u ced grow th a n d dissolution o f the
shell only w h en Í2arag < 0 .1 5 corresponding to a p C 0 2 o f ~
4000 p a tm [31]. D espite this w eakening o f th eir shells, the
p re d atio n by sea stars Asterias rubens a n d crabs Carcinus maenas
Acknowledgm ents
W e thank M . Fischer, C. H iebenthal, C. Howe, B. H uan g X uan, C.
Lieberum , K. Maczassek and C. Pansch, Y. Sawall an d the crew o f the F.
B. Polarfuchs for their field assistance.
Author Contributions
M anuscript im provem ent: PF PMJFi. Conceived an d designed the
experiments: VS. Perform ed the experiments: VS. Analyzed the data:
VS PF PM JH . C ontributed reagents/m aterials/analysis tools: VS PF
PM JH . W rote the paper: VS.
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