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Biogeosciences, 6, 1671–1680, 2009
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Biogeosciences
Calcification of the cold-water coral Lophelia pertusa under
ambient and reduced pH
C. Maier1,2, J. Hegeman1, M. G. Weinbauer2, and J.-P. Gattuso2
1Royal Netherlands Institute for Sea Research (NIOZ), Dept. of Biological Oceanography, BP 59, 1790 AB
Den Burg, The Netherlands
2CNRS-INSU, Laboratoire d’Oc´
eanographie de Villefranche, BP28, 06234 Villefranche-sur-Mer Cedex, France; Universit´
e
Pierre et Marie Curie-Paris6, Laboratoire d’Oc´
eanographie de Villefranche, 06230 Villefranche-sur-Mer, France
Abstract. The cold-water coral Lophelia pertusa is one of
the few species able to build reef-like structures and a 3-
dimensional coral framework in the deep oceans. Further-
more, deep cold-water coral bioherms may be among the
first marine ecosystems to be affected by ocean acidifica-
tion. Colonies of L. pertusa were collected during a cruise
in 2006 to cold-water coral bioherms of the Mingulay reef
complex (Hebrides, North Atlantic). Shortly after sample
collection onboard these corals were labelled with calcium-
45. The same experimental approach was used to assess cal-
cification rates and how those changed due to reduced pH
during a cruise to the Skagerrak (North Sea) in 2007. The
highest calcification rates were found in youngest polyps
with up to 1%d−1new skeletal growth and average rates of
0.11±0.02%d−1(±S.E.). Lowering pH by 0.15 and 0.3 units
relative to the ambient level resulted in calcification being re-
duced by 30 and 56%. Lower pH reduced calcification more
in fast growing, young polyps (59% reduction) than in older
polyps (40% reduction). Thus skeletal growth of young and
fast calcifying corallites suffered more from ocean acidifica-
tion. Nevertheless, L. pertusa exhibited positive net calcifi-
cation (as measured by 45Ca incorporation) even at an arag-
onite saturation state (a)below 1.
1 Introduction
The distribution of cold-water corals is believed to be mostly
controlled by temperature (4 to 12◦C) although other pa-
rameters, such as salinity, current speed and nutrients are
important (Rogers, 1999; Hovland et al., 2002; Roberts et
Correspondence to: C. Maier
(maier@obs-vlfr.fr)
al., 2006). These corals are often also referred to as deep-
water corals as they are usually found below the photic
zone at depths between 30 and 1000m where they can build
large three-dimensional structures (bioherms). Unlike trop-
ical coral reefs that are usually constructed by a great num-
ber of hermatypic (reef-building) corals, the cold-water coral
framework is based on the carbonate accretion of single or
very few species. Cold-water corals lack photosynthetic en-
dosymbiotic algae (zooxanthellae), which stimulate calcifi-
cation in reef-building corals (Gattuso et al., 1999). Hence,
calcification rates are presumably slower in cold-water corals
although no such rate estimates are actually available. That
is, it is more difficult to assess growth and calcification rates
in cold-water than in warm-water scleractinian corals. First,
direct access to the usually deep cold-water corals is logis-
tically challenging and frequent or long-term observations
are limited. Second, cold-water corals lack the annual bands
of high- and low skeletal density that are conveniently pro-
duced by reef-building corals. In the latter, it is easy to
estimate annual linear growth, which, along with measured
skeletal density, allows one to calculate calcification rates
(Knutson et al., 1972). Cold-water corals grow in environ-
ments that mostly lack strong annual seasonality in tempera-
ture and skeletal density banding does not necessarily relate
to annual periodicity (Adkins et al., 2004). Thus it is more
difficult to determine age and growth rates of samples. So
far, the most reliable and direct growth estimates for Lophe-
lia pertusa are derived from specimens that have settled and
grown on artificial substrates, such as oil and gas platforms
in the North Sea. Those cold-water corals have an average
linear skeletal extension rate (LSE) of 26mmyr−1(Bell and
Smith, 1999; Gass and Roberts, 2006). Growth estimates of
specimens maintained in aquaria revealed an annual LSE of
9.4mmyr−1and 15–17mmyr−1for L. pertusa collected in
Published by Copernicus Publications on behalf of the European Geosciences Union.
1672 C. Maier et al.: Cold-water coral calcification
Norwegian Fjords (Mortensen, 2001) and the Mediterranean
Sea (Orejas et al., 2008). There is currently no data avail-
able for rates of calcification (CaCO3precipitation rate) in
cold-water corals.
Human-induced threats such as deep bottom trawling are
known to destroy large areas of cold-water coral bioherms
(Rogers 1999; Foss˚
a et al., 2002; Hall-Spencer et al., 2002).
More recently, anthropogenic-induced global changes have
been identified as a major threat to cold-water corals (Orr et
al., 2005; Guinotte et al., 2006). Among factors, elevated
pCO2and temperature are prominent and have been shown
to have detrimental effects on reef-building corals, coralline
algae, and coral communities (Gattuso et al., 1999; Langdon
et al., 2000; Leclercq et al., 2000; Kuffner et al., 2007). Sim-
ilar negative effects have also been shown for other benthic
calcifiers (Gazeau et al., 2007; Hall-Spencer et al., 2008). A
recent study has shown an important resilience of two tem-
perate zooxanthellate corals in response to ocean acidifica-
tion (Fine and Tchernov 2007). Colonies were able to sur-
vive without their calcareous skeleton under extremely low
seawater pH and resumed calcification when pH was brought
back to normal. But even though single species are able to
survive, it does not imply that a coral reef can keep up the
necessary growth under lower pH. A recent study argues that
ocean acidification will trigger a sixth mass extinction of reef
corals within the next couple of centuries (Veron, 2008).
The impact of ocean acidification on cold-water corals has
not been investigated yet even though they appear particu-
larly vulnerable. Cold-water corals are restricted to high lati-
tudes and deeper depths, which exhibit lower saturation state
of calcium carbonate (Guinotte et al., 2006). Additionally,
models project dramatic shallowing in the aragonite satura-
tion horizon (ASH), the depth below which sea water be-
comes undersaturated with respect to aragonite (Orr et al.,
2005). It is anticipated that more than 70% of the cold-water
coral bioherms will be exposed to waters undersaturated with
respect to aragonite by the end of the century (Guinotte et al.,
2006). Therefore, not only might calcification of cold-water
corals be hampered but also their aragonitic framework could
well begin to dissolve posing an additional threat on cold-
water coral associated fauna and a loss in biodiversity.
Here our goals are: (1) to measure short-term rates of cal-
cification of the cold-water coral Lophelia pertusa and (2)
to investigate its response to elevated pCO2(low pH). The
study was carried out at two study sites, at Mingulay (He-
brides, NE Atlantic) and the Skagerrak, where L. pertusa is
the main frame-building species.
2 Methods
Live colonies or colony branches of L. pertusa were sampled
during two cruises in 2006 and 2007 at cold-water coral bio-
herms of the Mingulay reef complex, Hebrides (56.81◦N,
7.43◦W) (Roberts et al., 2005; Maier, 2006) and in the
Skagerrak, southern Norway at Fjellknausene (59.07◦N,
10.74◦E) and Soester (59.08◦N, 10.76◦E) (Maier et al.,
2007), respectively.
During the cruise in 2006 to Mingulay reef, we tested a
simple experimental set-up to assess calcification rates of
L. pertusa by labelling freshly collected corals with 45Ca di-
rectly on board the research vessel Pelagia. Because this ex-
perimental approach provided reasonable data on L. pertusa
calcification, it was used during a second cruise to the Sk-
agerrak in March 2007. During that cruise additional experi-
ments were conducted to test the effect of ocean acidification
on L. pertusa calcification rates.
2.1 Sampling of live Lophelia pertusa
Corals were sampled using a box core sampler (50cm in di-
ameter), which sealed itself off after closing on the bottom.
Thus we collected the benthos substrate together with overly-
ing ambient seawater. After box core was back on deck, sea-
water was siphoned off and live corals were transferred to a
mobile climate-controlled laboratory container and kept at 7–
9◦C in small aquaria with seawater of which ca. 50% was re-
newed every second day. During the first cruise to Mingulay,
a triangular dredge was once used to collect larger samples
for biodiversity determinations. The dredge had a triangular
opening of 1m and a mesh size of 2×2cm and was dredged
over a stretch of ca. 150m during 4 minutes of deployment.
Some of the L. pertusa specimens collected with this trian-
gular dredge were used to test the effect of sampling gear on
calcification rates (4×box core versus 4×dredge samples).
Sampling depths averaged 150m±9m (±S.E., N=10) and
109±3m (±S.E., N=7) at Mingulay and Skagerrak, respec-
tively. Temperature and salinity were determined by a CTD
cast during respective cruises and were 9.9◦C and 34.5‰ at
Mingulay and 7.5◦C and 34.6‰ at Skagerrak at respective
sampling depths.
2.2 45Ca labelling and measurement of calcification rate
Small branches of freshly collected colonies were placed
in 50-ml plastic tubes (Fig. 1a) filled with 30ml of seawa-
ter that was collected at sampling depth and filtered using
0.2µm membranes. Caps were placed on top of tubes to
avoid contamination by spilling of radioisotope-labelled sea-
water, but they were not screwed down to be airtight. The
samples were not stirred, but ship movement was considered
to be adequate to generate enough mixing to avoid stagnant
regions near coral polyps. The 20-ml headspace provided
sufficient oxygen supply for coral respiration, but changes in
the carbonate system took place during incubations, which
have been estimated as described in Sect. 2.5. During the
first labelling experiments at Mingulay reef in 2006, 30µl
of 45Ca (1.53 mCi ml−1)was added to each tube. The ad-
dition of 45Ca (1.88 mCi ml−1)was reduced to 10 µl per
30ml of filtered seawater in the 2007 experiments. During
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C. Maier et al.: Cold-water coral calcification 1673
the second cruise to the Skagerrak (March 2007), two re-
peated experiments were conducted, each with 3 treatments
to assess calcification rates at ambient seawater pH and at pH
lowered by 0.15 and 0.3pH units. The pH of ambient seawa-
ter was measured using a hand-held pH meter calibrated on
the N.B.S. scale. The pH treatments were obtained by ad-
dition of 1N and 0.1NHCl until the required pH value was
reached. In general, each treatment consisted of 8 replicates
(Table 2), except for Mingulay corals where 4 of the repli-
cates were retrieved by box core and the other 4 by triangular
dredge.
Corals were incubated for 24 h, after which they were
washed three times for 1 h with unlabelled seawater to al-
low the efflux of unbound 45Ca from the coelenteron, NaOH-
soluble compartment (tissue), and skeleton (Tambutt´
e et al.,
1996). Coral branches were then frozen and stored at −20◦C
pending analyses.
Back in the laboratory, whole coral branches were dried at
60◦C. Single corallites were broken off according to polyp
rank (Fig. 1b) and the dry weight was determined. The tis-
sue was removed in 6 N NaOH at 90◦C for several hours and
subsequently rinsed with MilliQ water. This procedure was
repeated until all tissue was removed. The remaining skele-
ton was dried at 60◦C and the skeletal dry weight of each
sub-sample was determined. Tissue dry weight was deter-
mined by subtracting skeletal dry weight after removal of tis-
sue from dry weight before tissue was removed. The remain-
ing skeleton was dissolved in 1N HCl and neutralized with
1N NaOH. Eight ml of InstaGel Plus (PerkinElmer) scin-
tillation liquid was added to sub-samples and counts were
measured on a Wallace 1211Rack Beta Scintillation counter
with an external standard and corrected against a quenching
curve.
2.3 Normalization of calcification rate
The rate of calcification (G) was normalized to the initial
skeletal weight and calculated from newly produced calcium
carbonate (Cn)and skeletal dry weight at end of experiment
(Pn)with Ggiven in percent of initial skeletal weight using
the formula:
G[%d−1] = (Cn/(Pn−Cn)))/n ×100 (1)
with n=duration of experiment (here:n=1 day).
For comparison with other published studies that have
used different units, our units for G used in this study [%
d−1] can easily be translated into mg CaCO3g−1skeleton
d−1or mmol CaCO3(or Ca2+)mol−1skeleton d−1using
the average initial skeletal weight given in Table 2.
Fig. 1. (a) Experimental approach: branch of Lophelia pertusa is
incubated for 24 h with the radioisotope label 45Ca in a Greiner
tube containing 30ml of seawater and a headspace of 20ml air.
(b) Branches are sub-sampled according to polyp rank (PR) with
youngest polyps corresponding to a PR of 1 and subsequent num-
bering along the longest branch axis.
2.4 Initial parameters of the carbonate system of
experiments
2.4.1 Dissolved inorganic carbon (DIC) and total
alkalinity (TA)
To characterise the seawater carbonate chemistry of study
sites, data for dissolved inorganic carbon (DIC) and total
alkalinity (TA) were used from sites close to sampling ar-
eas. For the Mingulay area data were derived from the GLO-
DAP (Global Data Analysis Project) database (Key et al.,
2004), cruise A24 of the World Ocean Circulation Experi-
ment (WOCE) June, 1997 at 9.334◦W; 57.75◦N from 151m
water depth. For the Skagerrak site, data were provided by
H. Thomas and A. Borges for 58.50◦N; 9.50◦E sampled in
February 2001 at a sampling depth of 100m (Bozec et al.,
2006 and Thomas et al., 2009). The DIC and TA of the GLO-
DAP data are believed to be consistent to 4 and 6 µmolkg−1,
respectively (Key et al., 2004).
2.4.2 Other parameters of the carbonate system
The Seacarb package (Gattuso and Lavigne, 2009) was used
to characterize parameters of the carbonate system of seawa-
ter used for 45Ca labelling experiments (Table 1). Dissolved
inorganic carbon and TA were used to calculate other pa-
rameters (pH, pCO2and a). The hydrostatic pressure was
set to zero, because experiments were conducted on board
and not at sampling depths. Salinity and temperature were
those of ambient seawater at sampling depths (and incuba-
tions). For an assumed consistency of the GLODAP DIC
and TA of 4 and 6 µmol kg−1(Key et al., 2004), the range
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1674 C. Maier et al.: Cold-water coral calcification
Table 1. Parameters of the carbonate chemistry at the beginning of the incubations.
Site pH treatment T (◦C) S DIC (µmolkg−1) TA (µmol kg−1) pHTpCO2(ppm) arag
Mingulay ambient 9.9 34.5 2126 2231 8.1 352 2.25
Skagerrak ambient 7.5 34.6 2143 2231 8.1 386 1.89
Skagerrak −0.15 pH 7.5 34.6 2143 2255 7.91 544 1.38
Skagerrak −0.3 pH 7.5 34.6 2143 2203 7.76 791 0.97
*Values in italics were calculated using the variables in bold and the Rpackage seacarb (Gattuso and Lavigne, 2009). Data for DIC and TA
were derived from the GLODAP database, WOCE, cruise A24 at 9.334◦W; 57.75◦N (Key et al., 2004) and from Thomas and Borges for
the Skagerrak at 58.50◦N; 9.50◦E (Bozec et al., 2006 and Thomas et al., 2009).
of uncertainty of other parameters of the seawater carbonate
system was estimated and values between minima and max-
ima ranged by 0.05 units for 1pHT, 45ppm for 1pCO2and
0.2 units for 1a. These uncertainties are likely underesti-
mates because the TA and DIC data were, despite their prox-
imity to the sampling site, not taken from exactly the same
location and at the same time as coral samples.
For treatments that were reduced by 0.15 and 0.3pH units
by the addition of HCl, the ppH function of the seacarb pack-
age was used under a closed system approach to estimate the
resulting changes in the seawater carbonate chemistry.
2.5 Changes in the carbonate chemistry during time of
incubation
Coral respiration, calcification and nutrient release into sea-
water cause changes in the carbonate system. To estimate the
changes that took place during the 24 h incubations, we used
a closed-system approach with step-wise (hourly) equilibra-
tion due to gas exchange between seawater and headspace
pCO2taking into account the following changes in DIC and
TA in seawater caused by respiration, calcification and excre-
tion. Calcification (G) decreases TA (1TA=2×G) and DIC
(1DIC=G); respiration (R) does not significantly change
TA, but increases DIC (1DIC=R); and ammonium excretion
increases TA (1TA=14/16×E) (Gattuso et al., 1999).
Hourly coral calcification was calculated using average G
and weight of branches incubated during this study. Respira-
tion was estimated using the data on L. pertusa metabolism
from Dodds et al. (2007), while data on ammonium release
by L. pertusa were derived from Duyl et al. (2005).
An initial pCO2of 400ppm was assumed in the
headspace. A stepwise method was used: every hour the TA
and DIC were calculated as follows:
TAt+1=TAt−2G+0.875E(2)
DICt+i=DICt+R−G(3)
with G,Rand Ein µmolkg−1seawater h−1.
At each time step, pCO2was equilibrated between seawa-
ter and the headspace using the following relationship:
pCO2(eq t+1)=(pCO2(air t )/a+pCO2(t +1)/b)/(a+b)×ab (4)
where pCO2(eq t+1)is the pCO2equilibrated between
headspace and seawater after each hourly time increment,
pCO2(air t) is the pCO2of the headspace before hourly equi-
libration with seawater pCO2, and pCO2(t+1)is the pCO2
of seawater after hourly change in seawater chemistry, but
before equilibration with air. For equilibration of pCO2be-
tween seawater and air, constants (a and b) were used taking
into account partial pressure and molecular weight of CO2
in gas and seawater and the respective volumes of 20ml and
30 ml of headspace and seawater, respectively. The constants
represent the slopes of correlation curves derived by plotting
corresponding concentrations of CO2and pCO2values and
multiplication by the respective volume of air or seawater
taking into account seawater temperature and density of CO2
in gas. In this study, a=55586 and b=34847.
The TA and DIC after air-sea equilibration were used to
calculate the new pCO2(i.e. pCO2(t+1)of Eq. 4), aand
pH using Seacarb of consecutive hourly time steps of 24 h.
The average TA, DIC, pH, pCO2and aduring incubations
were calculated using the data of the 24 hourly time steps
(Table 3).
2.6 Statistical analyses
Statistical analyses were conducted using the software pack-
age Statistica 7.0. The error is reported as one standard error
of mean (S.E.). To test the effects of sampling method, polyp
rank, and pH, we used a t-test or a 1-way or 2-way ANOVA
depending on the comparisons. Posthoc tests were conducted
using the Tukey honest significance test (HSD) for equal or
unequal N. One outlier was removed prior to statistical com-
parisons for Skagerrak experiment 1 at ambient pH and polyp
rank 1. This reduced the S.E. from 0.08 to a value of 0.02,
with the S.E. after removal of extreme being consistent with
S.E. of other treatments (Table 2).
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C. Maier et al.: Cold-water coral calcification 1675
Table 2. Overview of incubation experiments for different sites and pH treatments. Average number of polyps per branch, tissue dry weight
(DW), skeletal weight, and calcification rates normalized to initial skeletal weight of branches.
Date PH Polyps Tissue DW Skeleton G
Site labelling treatment N branch−1±S.E. (mg) ±S.E. (mg) ±S.E. (% d−1)±S.E.
Mingulay 20-Jul-06 ambient 8 6.63 ±0.65 104.91 ±15.53 1597.6 ±221.9 0.067 ±0.019
Skagerrak 15-Mar-07 ambient 8 5.25 ±0.37 112.47 ±6.50 1926.0 ±170.7 0.046 ±0.010
Skagerrak 15-Mar-07 −0.15 pH 8 5.00 ±0.78 152.69 ±39.07 1896.2 ±362.0 0.033 ±0.004
Skagerrak 15-Mar-07 −0.30 pH 8 7.75 ±0.67 321.75 ±26.81 3145.4 ±329.8 0.02 ±0.003
Skagerrak 17-Mar-07 ambient 8 6.63 ±0.96 176.95 ±25.05 1992.4 ±358.5 0.021 ±0.004
Skagerrak 17-Mar-07 -0.15 pH 8 6.63 ±0.98 136.23 ±21.72 4717.3 ±843.2 0.015 ±0.003
Skagerrak 17-Mar-07 -0.30 pH 8 8.00 ±0.93 319.64 ±45.27 4712.3 ±663.4 0.010 ±0.002
Table 3. Estimated average parameters of the carbonate chemistry changing as result of coral metabolism during experiments. Ammonium
excretion (E) as well as rates of calcification (G) and respiration (R) were normalized to kg−1seawater and h−1and used to estimate hourly
changes in TA and DIC over the 24 h incubations according to sampling sites and treatments as described in Sect. 2.5.
Site pH G R E DIC TA pHTpCO2arag
treatment (µmol kg−1h−1)(µmol kg−1)(ppm)
Mingulay ambient 11.86 3.82 7.87 2007 2041 7.62 1097 0.82
Skagerrak ambient 8.40 4.70 7.13 2075 2197 7.93 518 1.47
Skagerrak −0.15 pH 7.85 7.93 7.13 2117 2152 7.66 1054 0.85
Skagerrak −0.3 pH 7.72 9.43 9.71 2137 2143 7.53 1389 0.63
3 Results
3.1 Carbonate system of seawater
3.1.1 Initial conditions of seawater chemistry
The calculations of initial conditions of seawater chemistry
(Table 1) were based on DIC and TA of seawater taken at
similar depths approximately 100km away from study sites
(Key et al., 2004 and Thomas et al., 2009). Calculated am-
bient pHTwas 8.10 at Mingulay and 8.06 at Skagerrak. The
calculated pCO2and afor ambient pH treatments were
352ppm and 2.25 for Mingulay and 386ppm and 1.89 for
the Skagerrak treatments. For the Skagerrak experiments, a
decrease of pH by 0.15 and 0.3 units would consequently
cause a decrease of afrom 2.25 to 1.38 and an increase in
pCO2from 352 to 544; a pH decrease of 0.3 would cause
ato drop further to 0.97 and pCO2would rise further to
791ppm.
3.1.2 Changes in seawater chemistry during incubation
Changes in the carbonate chemistry as consequence of res-
piration and calcification rates were estimated for the differ-
ent treatments and the resulting average values for param-
eters of the carbonate chemistry during incubation and are
summarized in Table 3. As a result of changes in DIC by
−55µmolkg−1and TA −117 µmol kg−1, the pHTwas 0.27
units lower than the initial pH, while pCO2increased by
496 ppm and a dropped by 0.68 units on average (Table 4).
This resulted in values for pHTbetween 7.53 and 7.93; pCO2
between 518 and 1389ppm; and abetween 0.63 and 1.47
(Table 3).
3.2 Calcification rates
3.2.1 Bulk calcification of L. pertusa and response to
lower pH
Lophelia pertusa branches had on average 6.55±0.32 polyps
branch−1and the skeletal and tissue dry weights averaged
2855±241 and 189±15mgbranch−1, respectively (Table 2).
The average rate of calcification was 0.067±0.019%d−1
(N=8) for Mingulay corals but calcification rates spanned
2 orders of magnitude, between 0.0027 and 0.1923% d−1.
Calcification at ambient conditions was higher in corals col-
lected at Mingulay than those collected in the Skagerrak.
Pooling the Skagerrak data for ambient conditions leads to
a mean Gof 0.033±0.024% (N=16), which is significantly
different from that of Mingulay corals (t-test, t(1,22)=2.126,
p=0.045). A one-way ANOVA reveals a significant effect of
pH on bulk calcification rates of L. pertusa collected in the
Skagerrak (F(2,45)=7.03, p<0.001). Post-hoc comparisons
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1676 C. Maier et al.: Cold-water coral calcification
Fig. 2. Calcification rates (G) of Mingulay corals collected by box
core or dredge as a function of polyp rank. Box and whiskers are
±S.E. and S.D., respectively.
revealed that Gwas significantly different between ambient
seawater and the treatment where pH was lowered by 0.3
units (HSD, p<0.01). Whereas, for treatments that were dif-
ferent by 0.15 pH units no significant differences with respect
to Gcould be observed (HSD, p=0.22 and p=0.31 between
ambient and −0.15 pH and between −0.15pH and −0.30 pH
units, respectively).
3.3 Effect of polyp rank and sampling method on
calcification rates
Calcification rates were evaluated according to polyp rank
and sampling method (Fig. 2). Variation between samples
was very high, ranging from 0.005%d−1and 1.027%d−1.
Ranks of higher or equal to 4 were grouped together in or-
der to reach sample sizes large enough for statistical com-
parison. The sampling method had no significant effect on
the calcification rates (2-way ANOVA, F(1,44)=1.16, p=0.29)
whereas polyp rank did (F(3,44)=7.71, p<0.01). The interac-
tion between the sampling method and polyp rank was not
statistically significant (F(3,44)=1.24, p=0.31). The calcifi-
cation rate was highest in the youngest polyps (polyp rank 1)
with 0.279±0.055% (N=20) and decreased in older polyps
with 0.064 ±0.008% (N=13). Out of the older polyps, those
with polyp ranks 2 to 4 had an average calcification rate of
0.034±0.006%, those with ranks greater than 4 had an av-
erage calcification rate of 0.019±0.002%. Posthoc compar-
ison on effect of polyp rank revealed, that calcification rates
of polyp rank 1 were significantly different from polyp ranks
2 to 4 (Tukey HSD test for unequal N, p<0.01). No sig-
nificant differences in calcification rates were found between
polyp ranks 2 to 4 (HSD for unequal N, p>0.89).
3.3.1 Effect of lower pH on calcification according to
polyp rank
Both experiments carried out on Skagerrak corals showed a
decrease of G with decreasing pH for bulk analyses of incu-
bated branches (Table 2). These results were less clear in ex-
periment 2 when calcification rates were analysed according
to polyp rank (Fig. 3). Overall, similar results were obtained
on colonies collected in the Skagerrak and Mingulay. The
rates of calcification decreased with increasing polyp rank.
This was found in all pH treatments and for both experi-
ments. The first experiment showed a clear trend of decreas-
ing calcification rates with decreasing pH for all polyp ranks.
Changes were more pronounced for young polyps where pH
was lowered by 0.3 units relative to ambient seawater for
which calcification decreased to 41% for polyp rank 1 and
46% for polyp rank 2. For polyp rank 3, the decrease was
less pronounced and calcification at a pH of 0.3 units be-
low ambient was 62% of that found in ambient seawater; for
polyp ranks above 3, the decline was similar, 60%.
The results of the second experiment are less clear
(Fig. 3b). There was no substantial decrease in calcification
rates between ambient seawater and treatments with lower
pH. Only for polyp ranks 1 and 3 were the calcification rates
slightly lower for L. pertusa in the treatment with −0.3pH
units relative to ambient seawater. Between treatments of -
0.15 and -0.3 pH units, calcification rates were lower at the
lower pH level, confirming results from experiment 1.
4 Discussion
4.1 Methodological constraints
To the best of our knowledge, no physiological experiment
has been carried out in situ on deep-sea corals and very few
studies have been conducted in the laboratory. Here, colonies
were incubated on board ship, using freshly collected speci-
mens and ambient seawater. Although this is as close as the
community has come to achieving in situ conditions, exper-
iments at sea do entail several limitations of lab space, time
and working with radioactive material. In this section, we
examine the methodological constraints experienced and the
uncertainties that they generate.
The radioisotope labelling technique is a very sensitive
method to determine coral calcification and is thus, well
suited for short-term incubations and to measure calcifica-
tion according to polyp age. For tropical corals it was sug-
gested to grow nubbins completely covered by tissue to avoid
non-biologically 45Ca adsorption by the skeleton (Tambutt´
e
et al., 1995). In our experiments, the oldest corallite (of high-
est polyp rank) was the part that contained the broken off
area and had bare skeleton exposed to 45Ca-labelled seawa-
ter. These samples generally exhibited very low calcification
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C. Maier et al.: Cold-water coral calcification 1677
Fig. 3. Calcification rates (G) of Skagerrak corals according to polyp rank and as function of pH for experiments 1 (a) and 2 (b).
rates (<1% of the bulk) demonstrating that non-biologically
bound 45Ca was negligible, despite the bare skeleton.
Due to the small volume used (30ml) we were unable to
determine TA and DIC, respiration, and nutrient excretion in
the incubations. TA and DIC data were obtained from sea-
water sampled during other cruises at similar depths in the
area of the study sites. A closed system approach was used
to model changes in seawater carbonate chemistry assuming
that air-exchange between the vials and ambient air was neg-
ligible. A small amount of exchange would overestimate the
changes in seawater carbonate chemistry. Among the data
used to model changes in the seawater chemistry during in-
cubations (Table 3) the respiration and excretion data were
taken from the literature (Dodds et al., 2005; van Duyl et al.,
2005). A sensitivity analysis was carried out to estimate the
uncertainty associated with lower and higher respiration and
excretion rates (Table 4).
There are several methods to experimentally change the
carbonate chemistry and decrease the pH (Gattuso and Lavi-
gne 2009). For practical reasons, we lowered the pH of ambi-
ent seawater adding HCl until the desired reduction (0.15 or
0.3pH unit) was reached. This is a straight forward method
to reach target pH values, but also it generates a decline in to-
tal alkalinity that is not expected in the present century. Nor
does this approach mimic the projected increase in DIC. In
our experiments, the computed deviation from changes ex-
pected by the pCO2approach were 58µmolkg−1for both
DIC and TA at a pH reduced by 0.15 units and 108 and
110µmolkg−1for DIC and TA at a pH reduced by 0.3 units.
Consequently, the pCO2was only 24 and 36ppm below tar-
get values, and awas 0.02 and 0.05 higher, which is negli-
gible relative to the adecreases of 0.49 and 0.87 when the
pH was lowered by 0.15 and 0.3 units, respectively.
Table 4. Estimates of the carbonate chemistry with half and double
(bold) the assumed values of Rand Eas given in Table 3 (the 1st
row of each treatment in italics contains the values of Tables 2 and
3).
Site pH G R E DIC TA pHTpCO2a
treatment (µmol kg−1h−1] (mol kg−1)(ppm)
Mingulay ambient 11.86 3.82 7.78 2.01×10−32.04×10−37.62 1097 0.82
11.86 7.64 3.94 2.03×10−32.00×10−37.4 2047 0.57
11.86 1.91 3.94 1.98×10−32.00×10−37.55 1303 0.73
11.86 7.64 15.74 2.06×10−32.14×10-3 7.75 798 1.08
11.86 1.91 17.74 1.92×10−32.14×10-3 7.88 569 1.41
Skagerrak ambient 8.40 4.70 7.13 2.08×10−32.20×10−37.93 518 1.47
8.40 9.40 3.57 2.12×10−32.15×10−37.66 1174 0.94
8.40 2.35 3.57 2.05×10−32.15×10−37.65 593 1.32
8.40 9.40 14.26 2.14×10−32.28×10−37.98 477 1.66
8.40 2.35 14.26 2.09×10−32.28×10−38.1 344 2.12
Skagerak –0.15 7.85 7.93 7.13 2.12×10−32.152E+00 7.66 1054 0.85
7.85 15.86 3.57 2.17×10−32.15×10−37.49 1935 0.74
7.85 3.97 3.57 2.07×10−32.15×10−37.83 692 1.21
7.85 15.86 14.26 2.20×10−32.28×10−37.79 817 1.21
7.85 3.97 14.26 2.10×10−32.28×10−38.08 365 2.02
Skagerak –0.3 7.72 9.43 9.71 2.14×10−32.14×10−37.53 1389 0.63
7.72 18.86 4.86 2.20×10−32.17×10−37.45 2159 0.7
7.72 4.72 4.86 2.08×10−32.17×10−37.84 661 1.25
7.72 18.86 19.42 2.24×10−32.34×10−37.86 685 1.38
7.72 4.72 19.42 2.13×10−32.34×10−38.13 324 2.33
4.2 Calcification of Lophelia pertusa incubated at
ambient pH
We show here that calcification rates of Lophelia pertusa can
be relatively high but also reveal an enormous range depen-
dent on corallite age and size. The youngest polyps had a
maximum calcification rate of up to 1%d−1. This rate falls
within the range found for tropical, zooxanthellate corals
(Erez, 1978; Marubini and Atkinson, 1999; Marubini and
Thake, 1999; Reynaud et al., 2003). However, the bulk cal-
cification rate of whole branches was low and in the range of
dark calcification of tropical corals (Erez, 1978). Bulk calci-
fication rates average out the extremely fast and slow growth
www.biogeosciences.net/6/1671/2009/ Biogeosciences, 6, 1671–1680, 2009
1678 C. Maier et al.: Cold-water coral calcification
rates of young and old corallites, respectively. Bulk calcifi-
cation is thus an intermediate value and greatly depends on
the proportion of older and younger corallites in a branch.
This needs to be taken into account when determining cal-
cification rates of bulk samples and not of single corallites
(e.g. buoyant weight or total alkalinity anomaly techniques).
Our extremely low growth rates for older corallites agree
with aquarium observations where cold-water coral polyps
with a diameter larger than 7mm do not exhibit any lin-
ear extension (Mortensen 2001). Mortensen also observed
that skeletal extension occurred as episodic, rapid-growth
events, which may explain the large range of calcification
rates observed in the youngest polyps (polyp rank 1). Our
finding that the young polyps can calcify extremely quickly,
suggests that new corallite production (budding) is impor-
tant for the growth and maintenance of the 3-dimensional
structure of cold-water coral bioherms. Thus high abun-
dance of new coral buds may consequently be a good indica-
tor for the potential of a cold-water coral bioherm to main-
tain rapid growth and its 3-dimensional structure, which sus-
tains the high biodiversity associated with these ecosystems.
A coral branch can produce several new corallites per year
(Mortensen, 2001; Orejas et al., 2008), but it is not known
which factors trigger budding in L. pertusa. It could be in-
trinsic (genetically controlled) as well as environmentally in-
duced. Food and nutrient availability are suggested to be
important factors providing the necessary energy for calci-
fication and reproduction (Spiro et al., 2000), but changes in
abiotic environmental parameters such as temperature, cur-
rent regimes and carbonate chemistry might further influence
new corallite formation. Also, fragmentation and other dis-
turbances may eventually trigger higher budding rates: It has
been shown that L. pertusa has a high recovery potential and
injuries to calyx tissue may result in new polyp formation
(Maier, 2008). Also, sponge bioerosion can induce addi-
tional aragonite secretion at younger growth stages of coral-
lites (Beuck et al. 2007), and growth morphologies with
densely spaced new corallites and high budding rates have
been observed in dying L. pertusa colonies (Freiwald et al.,
1997).
Calcification rates of Mingulay L. pertusa were signifi-
cantly higher than those for Skagerrak corals. It is not clear
what causes this difference and whether this constitutes a
site-specific characteristic or if differences are due to dif-
ferent sampling depths, seasonality, or seawater carbonate
chemistry. The higher calcification rates of Mingulay corals
may reflect a higher initial aat this site. On the other
hand, many of the branches of L. pertusa sampled from Sk-
agerrak showed encrustations or overgrowth by the sponge
Hymedesmia coriacea (van Soest et al., 2005; Maier et al.,
2007). Such sponge overgrowth can constitute an additional
stress factor. Energy spent for chemical or mechanical de-
fence would consequently be not available for calcification
and might have caused reduced calcification of Skagerrak
corals.
4.3 Sampling gear
For Mingulay corals, the effect of sampling L. pertusa with
different gear (box core or dredge) was tested, because
dredging inflicts more damage on benthic organisms than
does box coring. In this study, the range of calcification rates
was lower for dredged corals than for those retrieved by box
coring (Fig. 2), but mean values were not significantly dif-
ferent. Thus our specimens of L. pertusa branches used were
either not more stressed than the box cored corals or they
recovered quickly from additional stress induced by dredg-
ing. The latter would be supported by aquarium observations
showing a high recovery potential of L. pertusa to skeletal
fragmentation (Maier, 2008).
4.4 Calcification rates in response to reduced pH
The rate of calcification decreased when pH was lowered by
0.15 and 0.3 units relative to ambient seawater. The arago-
nite saturation state (a)was approximately 1.9 for ambient
seawater, whereas it declined to 1.4 and 1.0 at the lower pH
levels (Table 1). These declines of 25 and 46% resulted in
corresponding declines in calcification by 29 and 55%. Yet
L. pertusa exhibited positive net calcification even when a
reached values close to 1. Moreover, if biologically-induced
changes in seawater chemistry during incubations were taken
into account, the positive net calcification would even corre-
spond to an abelow 1 (Table 3). In contrast, the average
responses of warm-water reef building corals and coral com-
munities exhibit no net calcification at aclose to 1 (Gat-
tuso et al., 1998; Langdon and Atkinson, 2005; Schneider
and Erez, 2006). That L. pertusa still shows positive net cal-
cification rates supports the idea that L. pertusa is already
adapted to lower alevels, where they live, i.e., in the deeper
ocean and higher latitudes. Nevertheless, a decrease of more
than 50% in calcification rates of L. pertusa as response to a
decline of 0.3pH units as anticipated for the end of the cen-
tury constitutes a drastic decline with respect to coral growth.
Nothing is as yet known on the growth rate necessary to build
and maintain the 3-dimensional coral framework and this
might also be highly dependent on other site-specific factors.
There will definitely be regional constraints where higher
sedimentation rates require faster calcification to avoid being
buried by the sediment load. Other regions might be more
affected by additional rise in temperature where cold-water
coral distribution is already at an upper temperature limit,
as assumed for cold-water corals in the Mediterranean Sea.
Specifically, if additional stressors are added to those of cli-
mate change, a 50% decrease in calcification rate may well
be detrimental to cold-water coral bioherms.
Biogeosciences, 6, 1671–1680, 2009 www.biogeosciences.net/6/1671/2009/
C. Maier et al.: Cold-water coral calcification 1679
5 Conclusions
This study provides the first measurements of calcification
rates in a deep-sea coral. Despite the methodological con-
straints due to the simple experimental set up used during
the onboard experiments, L. pertusa showed clear patterns of
calcification with youngest polyps calcifying most rapidly,
at rates comparable to those of slow growing, reef-building
corals. Dramatically reduced calcification rates at lower pH
treatments are a clear response to increased pCO2and lower
pH. It is now crucial to optimise experiments for calcifica-
tion studies and extend work to other species of cold-water
corals as well as broaden studies to wider geographical and
depth ranges. It is also a priority to carry out longer-term ex-
periments designed to evaluate possible acclimation mecha-
nisms of cold-water corals and to test how cold-water corals
will react to the combined effects of ocean acidification and
elevated temperature.
Acknowledgements. The Dutch Science Foundation (NWO) pro-
vided ship time and funding via the project biology and ecosystem
functioning of deep-water corals (BIOSYS, project no 835.20.024
and 814.01.005). We thank captain and crew of R/V Pelagia
and help provided by NIOZ-MRF. We also thank H. Thomas
and A. Borges who provided DIC and TA data at Skagerrak.
Additional support was provided by the European Commission
through a Marie-Curie Fellowship (MECCA, project no 220299 )
and the European Project on Ocean Acidification (EPOCA; grant
agreement no 211384). The critical comments of the anonymous
referees and J. Orr greatly improved this paper.
Edited by: J. Orr
The publication of this article is financed by CNRS-INSU.
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