ArticlePDF Available

Biogeographic variability in the physiological response of the cold-water coral Lophelia pertusa to ocean acidification

  • Marine Conservation Institute

Abstract and Figures

While ocean acidification is a global issue, the severity of ecosystem effects is likely to vary considerably at regional scales. The lack of understanding of how biogeographically separated populations will respond to acidification hampers our ability to predict the future of vital ecosystems. Cold-water corals are important drivers of biodiversity in ocean basins across the world and are considered one of the most vulnerable ecosystems to ocean acidification. We tested the short-term physiological response of the cold-water coral Lophelia pertusa to three pH treatments (pH = 7.9, 7.75 and 7.6) for Gulf of Mexico (USA) and Tisler Reef (Norway) populations, and found that reductions in seawater pH elicited contrasting responses. Gulf of Mexico corals exhibited reductions in net calcification, respiration and prey capture rates with decreasing pH. In contrast, Tisler Reef corals showed only slight reductions in net calcification rates under decreased pH conditions while significantly elevating respiration and capture rates. These differences are likely the result of environmental differences (depth, pH, food supply) between the two regions, invoking the potential for local adaptation or acclimatization to alter their response to global change. However, it is also possible that variations in the methodology used in the experiments contributed to the observed differences. Regardless, these results provide insights into the resilience of L. pertusa to ocean acidification as well as the potential influence of regional differences on the viability of species in future oceans.
Content may be subject to copyright.
Biogeographic variability in the physiological response of
the cold-water coral Lophelia pertusa to ocean acidification
Samuel E. Georgian
, Sam Dupont
, Melissa Kurman
, Adam Butler
, Susanna M. Str
Ann I. Larsson
& Erik E. Cordes
1 Department of Biology, Temple University, Philadelphia, PA, USA
2 Department of Biological and Environmental Sciences, Sven Lov
en Centre for Marine Sciences Kristineberg, University of Gothenburg,
ackskil, Sweden
3 Department of Marine Sciences Tj
o, University of Gothenburg, Str
omstad, Sweden
Calcification; cold-water coral; deep sea;
energetics; ocean acidification; physiology.
Samuel E. Georgian, Department of Biology,
Temple University, 1900 N. 12th Street,
Philadelphia, PA 19122, USA.
Accepted: 14 March 2016
doi: 10.1111/maec.12373
While ocean acidification is a global issue, the severity of ecosystem effects is
likely to vary considerably at regional scales. The lack of understanding of how
biogeographically separated populations will respond to acidification hampers
our ability to predict the future of vital ecosystems. Cold-water corals are
important drivers of biodiversity in ocean basins across the world and are con-
sidered one of the most vulnerable ecosystems to ocean acidification. We tested
the short-term physiological response of the cold-water coral Lophelia pertusa
to three pH treatments (pH =7.9, 7.75 and 7.6) for Gulf of Mexico (USA)
and Tisler Reef (Norway) populations, and found that reductions in seawater
pH elicited contrasting responses. Gulf of Mexico corals exhibited reductions
in net calcification, respiration and prey capture rates with decreasing pH. In
contrast, Tisler Reef corals showed only slight reductions in net calcification
rates under decreased pH conditions while significantly elevating respiration
and capture rates. These differences are likely the result of environmental dif-
ferences (depth, pH, food supply) between the two regions, invoking the
potential for local adaptation or acclimatization to alter their response to glo-
bal change. However, it is also possible that variations in the methodology used
in the experiments contributed to the observed differences. Regardless, these
results provide insights into the resilience of L. pertusa to ocean acidification as
well as the potential influence of regional differences on the viability of species
in future oceans.
The ability of marine organisms to persist and provide
ecosystem services may be severely reduced in the future
due to ocean acidification, the gradual decrease in pH and
perturbation of the carbonate system of the world’s oceans
as a consequence of increasing atmospheric CO
2013; Wittmann & P
ortner 2013). These changes critically
threaten ecosystem function in a wide variety of biomes
including coral reefs, coastal systems, the open ocean, polar
regions and the deep sea (reviewed in Hofmann et al.
2010). While most published studies have focused on the
physiological effects elicited by exposure to decreased pH
(Riebesell & Gattuso 2015), the potential of local adapta-
tion to modulate the effects of ocean acidification has
received less attention (Sunday et al. 2011). Studies that
have directly compared the responses of multiple popula-
tions to acidification have revealed remarkable plasticity,
suggesting that regional variability may play an important
role in determining the fate of marine organisms in future
oceans (e.g. Langer et al. 2009; Parker et al. 2011; Pistevos
et al. 2011; Sunday et al. 2011; Pancic et al. 2015).
Marine Ecology ª2016 Blackwell Verlag GmbH 1
Marine Ecology. ISSN 0173-9565
The deep sea alone stores 25% of anthropogenic car-
bon (Canadell et al. 2007; Sabine & Feely 2007), provid-
ing a crucial buffering capacity that may mitigate the
immediate effects of climate change in surface waters but
ultimately places all deep-sea ecosystems at risk. The
same adaptations that allow organisms to be successful in
the cold and generally food-limited deep-sea environment
(for example, slower metabolism, slower growth, lower
protein content and lower enzyme levels; Drazen & Seibel
2007; Seibel & Drazen 2007) may partially impair their
ability to physiologically compensate for rapid changes in
pH (Seibel & Walsh 2003; Melzner et al. 2009). Among
the most vulnerable groups in the deep sea are cold-water
corals, organisms that already survive and calcify at low
pH and saturation states (Davies & Guinotte 2011;
Thresher et al. 2011; Lunden et al. 2013; Georgian et al.
2016). Cold-water corals support high levels of biodiver-
sity by creating complex three-dimensional habitat and
providing essential ecosystem services such as carbon
sequestration and nutrient cycling (Wild et al. 2004; van
Oevelen et al. 2009). As benthic waters become increas-
ingly acidified, cold-water coral communities could be
lost in the coming decades, in many cases before they
have been discovered.
There is evidence to suggest that the physiological
mechanisms underlying the calcification pathway in cold-
water corals may provide some resilience to ocean acidifi-
cation. Cold-water corals actively elevate the pH of their
internal calcifying fluid by as much as 1.0 pH unit higher
than external seawater, approximately double the increase
observed in shallow-water corals (McCulloch et al. 2012).
This plausibly represents an evolutionary strategy to
counter the chronically low carbonate saturation state in
deep-sea environments, and may serve as an indication
that cold-water corals could be resilient to future acidifi-
cation (McCulloch et al. 2012). However, there are only a
few isolated observations of cold-water corals at or near
the saturation horizon in situ, and most of these are of
solitary corals, suggesting that undersaturated, low pH
conditions are not suitable for framework formation.
Therefore, it is imperative to experimentally quantify
both calcification and the metabolic response of cold-
water corals to low pH and saturation states in order to
evaluate their future in an increasingly acidified ocean.
Only a small number of ocean acidification experimental
studies have been conducted on cold-water corals to date,
and the results have been both highly variable and contrast-
ing. Most notably, a 6-month study found that net calcifi-
cation rates in the cold-water coral Lophelia pertusa linearly
increased with elevated CO
partial pressure (pCO
) values
as high as 982 microatmospheres (latm) (corresponding to
a pH of 7.75), although calcification occurred at extremely
low levels in all treatments (Form & Riebesell 2012). There
was no change in calcification rates between ambient
(445 latm) and projected (867 latm) pCO
treatments in
short-term shipboard experiments on Madrepora oculata
(Maier et al. 2012). Similarly, Hennige et al. (2014) found
no change in calcification in L. pertusa growth in acidified
conditions as high as 750 ppm (pH of approximately 7.77),
but documented a significant decline in respiration over a
21-day period. In contrast, a recent 3-month study on both
L. pertusa and M. oculata found no significant change in
either respiration or calcification rates even with CO
centrations as high as 1000 ppm (pH of approximately
7.73; Maier et al. 2013a,b). Calcification, skeletal density
and energy reserves in Dendrophyllia cornigera did not
change significantly during a 314-day acidification experi-
ment with pH values as low as 7.81; however, in the same
study, Desmophyllim dianthus exhibited a significant, 70%
reduction in calcification (Movilla et al. 2014). Finally, two
short-term experiments demonstrated that L. pertusa had
considerably reduced calcification under reduced pH values
of 7.75 (Maier et al. 2009) and 7.6 (Lunden et al. 2014a).
Therefore, while individual studies have provided impor-
tant insights into the possible response of cold-water corals,
the large variability among and within studies renders the
potential resilience of cold-water corals to expected levels
of acidification uncertain at best.
It is possible that discrepancies in the observed
response of cold-water corals to acidification have been
caused in part by natural variation among the studied
populations. Cold-water corals are found in a variety of
habitats in every ocean basin (Guinotte et al. 2006;
Davies et al. 2008), with limited gene flow among regions
(Le Goff-Vitry et al. 2004; Morrison et al. 2011; Lunden
et al. 2014a). Therefore, biogeographically separated pop-
ulations may exhibit highly variable responses to acidifi-
cation due to local adaptation or acclimation to different
pH regimes. In the present study, we tested how near-
future levels of ocean acidification affected the net calcifi-
cation, respiration and capture rates of biogeographically
and genetically distinct L. pertusa populations from the
Gulf of Mexico and the Tisler Reef (Norwegian Skager-
rak). Ultimately, these data are an important first step in
understanding natural variation at the regional scale, and
highlight the importance of considering the role of bio-
geography when assessing the effects of global change on
wide-ranging species.
Material and Methods
Gulf of Mexico
Site description and sample collections
Corals were collected in June 2013 onboard the E/V Nau-
tilus using the remotely operated vehicle (ROV) Hercules at
2Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
the Viosca Knoll 826 (VK826) lease block in the Northern
Gulf of Mexico (Fig. 1a, b). The VK826 site contains the
largest continuous cold-water coral habitat yet discovered
in the Gulf of Mexico (Schroeder 2002; Cordes et al. 2008).
The site is characterized by a large carbonate mound
approximately 500 m in diameter (Davies et al. 2010) as
well as a series of smaller mounds on the order of tens of
meters across (Georgian et al. 2014), both containing a
high density of living Lophelia pertusa thickets. A diverse
fauna of octocorals, black corals, fish and associated inver-
tebrate species utilize the L. pertusa reef structure as habitat
at the site (Cordes et al. 2008; Lessard-Pilon et al. 2010).
Water samples collected by ROV directly over the reef
revealed that pH on the total scale (pH
) ranged from
7.898.03, salinity-normalized total alkalinity ranged from
2288.72334.7 lmolkg
and the aragonite saturation
state (Ω
) ranged from 1.331.69 (Table 1; Lunden et al.
2013). Water temperature varies considerably throughout
the year, with values as low as 6.5 °C in winter months,
and as high as 11.6 °C in the summer (Mienis et al. 2012).
Dissolved oxygen concentrations at the site are extremely
low compared to other L. pertusa habitats, ranging between
2.63.2 mll
, but are consistent with values for other
Gulf of Mexico benthic habitats (Schroeder 2002; Davies
et al. 2008). The site experiences relatively strong current
flows averaging 8 cms
, with peak currents as high as
38 cms
(Mienis et al. 2012).
Corals were sampled within a depth range of 450
500 m from visually distinct colonies separated by at least
2030 m to avoid sampling identical genotypes (sensu
Lunden et al. 2014a) and returned to the surface in a
temperature-insulated ‘biobox’. After collection, corals
were transferred to Temple University (Philadelphia, PA,
USA) and housed in a 550-l maintenance aquarium sys-
tem as described in Lunden et al. (2014b) for approxi-
mately 7 months prior to experimentation.
Experimental design
One experimental tank (60 l) was established for each of
the following target treatments: in situ (pH
7.9), slightly
acidified (pH
7.75) and highly acidified (pH
Actual pH
and Ω
closely matched target conditions
(Table 1), and were significantly different among treat-
ments [analysis of variance (ANOVA) with HolmSidak
post-hoc tests, P <0.001]. Treatments were randomly
assigned to a tank, and corals were then randomly
assigned to treatments. Temperature (average of
8.1 0.2 °C), salinity (average of 35.1 0.04 psu), dis-
solved oxygen (average of 6.4 0.1 mll
) and total
alkalinity (average of 2328 23 lmolkg
) did not dif-
fer significantly across treatments (Table 1; KruskalWal-
lis ANOVA, P >0.05). Temperature was measured once
every 5 min using Hobo temperature loggers (Onset UA-
001-64), salinity was measured daily using a handheld
refractometer and dissolved oxygen was measured twice
weekly using a Strathkelvin 782 dual oxygen meter and
SI130 microcathode electrode. Corals were fed Marine
three times per week (0.25 ml Marine Snowl
) but were starved for 24 h prior to the mea-
surement of physiological rates. Total alkalinity was
adjusted to approximately 2300 lmolkg
to match
in situ conditions by addition of 12 N HCl to seawater
made using the Instant Ocean
salt mix. Total alkalinity
was measured three times per week by acid titration on a
(a) (b)
(c) (d)
Fig. 1. Map of study sites and sample
collections. (a): Location of the VK826 site
within the Gulf of Mexico. (b): Multibeam
bathymetry of the VK826 site with sampling
locations indicated by black circles. (c):
Location of Tisler Reef in the Skagerrak,
Norway. (d): Multibeam bathymetry of Tisler
Reef (Lavaleye et al. 2009) with sampling
locations indicated by black circles.
LA, Louisiana; NO, Norway; SE, Sweden.
Marine Ecology ª2016 Blackwell Verlag GmbH 3
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
Mettler-Toledo DL15 autotitrator and checked against
certified reference material (Batch 134, Dickson Lab, La
Jolla, CA, USA). pH
was adjusted using American Mar-
ine Pinpoint pH Controllers, which automatically bubble
either gaseous CO
or ambient air to lower or raise pH,
respectively. Each pH system was calibrated weekly on
the total scale with standard Tris-HCl and 2-aminopyri-
dine/HCl (AMP-HCl) buffers. The aragonite saturation
state was calculated from pH
, total alkalinity, tempera-
ture and salinity using CO2SYS software (Pierrot et al.
2006). Partial water changes (4 l) were performed weekly.
Experiments for the Gulf of Mexico population began
in February 2014. Nine colonies consisting of between
five and 15 live polyps (average of 10.8 3.2 polyps)
were used per treatment. After the colonies were moved
to the experimental tanks, pH
was slowly decreased to
the target level for each treatment over a period of 48 h.
Prior to experimental measurements, corals were accli-
mated to treatment conditions for 1 week. After the accli-
mation period, respiration, feeding and buoyant weight
were measured as described below at the start and end of
a 2-week experimental period.
Physiological measurements
Net calcification was assessed using the buoyant weighing
technique (Jokiel et al. 1978; Davies 1989), which has
been successfully used in numerous growth studies for
both shallow- (Anthony et al. 2008; Dove et al. 2013)
and deep-water (Orejas et al. 2011; Form & Riebesell
2012; Larsson et al. 2013; Lunden et al. 2014a) corals.
The buoyant weight of each colony was obtained at the
start and end of the 2-week experimental period by
weighing fragments submerged in seawater and attached
by a hook to an analytical balance (Denver Instrument,
precision of 0.1 mg). Buoyant weights were converted to
dry weights in air using the density of the skeleton and of
the seawater. A correction for the contribution of tissue
to buoyant weights (following Davies 1989) was applied
to obtain the dry weight of the skeleton alone. Net
calcification was then calculated as the change in skeletal
dry weight over the 2-week experimental period,
expressed as % starting weightday
The respiration rate of each colony was measured as
oxygen consumption in an 800-ml closed acrylic chamber
during hour-long incubations. Dissolved oxygen concen-
trations were measured in lmoll
using a Strathkelvin
782 dual oxygen meter and SI130 microcathode electrode.
The electrode was calibrated at the experimental tempera-
ture with a dual point calibration using 100% air-satu-
rated water and a deoxygenated sodium sulfite solution.
Temperature was controlled by submerging the chamber
in a water bath, and a Hobo temperature logger (Onset
UA-001-64) was mounted inside the chamber to monitor
for temperature changes during incubations, which never
exceeded 0.2 °C. Incubations were conducted with sea-
water from experimental aquaria so that the starting pH
matched treatment conditions. Circulation within the
chamber was obtained using a magnetic stir plate set at a
stir speed of approximately 80 rpm. This generated suffi-
cient flow to prevent oxygen depletion at the electrode
tip, and also appeared to elicit a more natural polyp
behavior. Microbial respiration (0.6 0.08 lmol
,n=12) was accounted for by measuring
empty chambers and was subtracted from live coral mea-
surements. Corals were allowed to acclimate to conditions
in the chamber for half an hour prior to measurements,
and oxygen saturation never fell below 90% during incu-
bations. At the end of the experiment, each colony was
dried at 60 °C until reaching a constant mass (4896 h),
placed in a muffler furnace at 450 °C for 4 h to combust
all organic matter, and reweighed to calculate the ash-free
dry mass of each colony.
The feeding rate of each colony was measured as the
capture rate of adult Artemia salina during a 1-h period
in 0.8 l incubation chambers containing a starting prey
density of 125 A. salinal
.A. salina stocks were fed
cultured algae after hatching until reaching maturity (36
weeks) and had an average length of 3.54 0.9 mm
Table 1. Seawater carbonate parameters measured near collection sites and in experimental aquaria. Experimental measurements are given as
the 14-day experimental average ( SD), with pH measured daily on the total scale (pH
) and total alkalinity (TA, lmolkg
) measured twice
weekly. Aragonite saturation state (Ω
) and CO
partial pressure (pCo
) (microatmospheres, latm) values were calculated in CO2SYS. Gulf of
Mexico in situ measurements are averages for the VK826 site (Lunden et al. 2013). Tisler Reef in situ measurements are from a neighboring
Lophelia pertusa reef in the Skagerrak, Norway (Maier et al. 2009).
treatment target pH
Gulf of Mexico Tisler Reef
in situ 7.93 2313 1.43 505 8.06 2313 1.89 383
control 7.90 7.92 (0.03) 2333 (16) 1.51 (0.10) 552 (42) 7.91 (0.03) 2312 (21) 1.38 (0.08) 579 (41)
low pH 7.75 7.76 (0.03) 2334 (17) 1.07 (0.07) 831 (54) 7.76 (0.03) 2312 (29) 1.00 (0.05) 845 (61)
very low pH 7.60 7.62 (0.03) 2331 (15) 0.80 (0.05) 1165 (76) 7.60 (0.04) 2309 (26) 0.74 (0.07) 1208 (132)
4Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
during both experiments. Circulation was provided using
a magnetic stir plate (stir speed of approximately
80 rpm). This provided sufficient flow to provide a con-
stant flow of prey items past each Lophelia pertusa polyp
(visual observation). Incubations were conducted with
seawater from experimental aquaria so that the starting
pH matched treatment conditions. Coral colonies were
allowed to acclimate to the incubation chamber for
30 min prior to the addition of prey items. Capture rate
was standardized to polyp number and reported as A.
Tisler Reef corals
Site description and sample collections
Lophelia pertusa colonies were collected in January 2014
from the Tisler Reef in the Norwegian Skagerrak (Fig. 1c,
d). The Tisler Reef is a relatively shallow (70155 m)
cold-water coral reef composed of living L. pertusa colo-
nies as well as extensive dead skeletal structures (Lavaleye
et al. 2009). It covers an area of approximately 240 km
making it one of the largest inshore cold-water coral
reefs. Following the discovery of the reef in 2002 and the
documentation of extensive pre-existing damage from
bottom trawling, the reef was protected in 2003 by Nor-
wegian fishery regulations (Lund
alv & Jonsson 2003;
a & Skjoldal 2010). The reef experiences strong cur-
rents up to 50 cms
, with tidally influenced down-
welling providing the bulk of nutrition to the reef
(Wagner et al. 2011). Water temperature typically fluctu-
ates between 6 and 9 °C (Lavaleye et al. 2009). While the
carbonate chemistry directly above the reef has not been
measured, a neighboring L. pertusa reef at the same depth
within the Norwegian Skagerrak had a pH
of 8.06, total
alkalinity of 2313 lmolkg
and a Ω
of 1.89 (Table 1;
Maier et al. 2009).
All required permits were obtained from the Norwe-
gian Fisheries Directorate prior to collection. Corals of
the white color morph were collected from discrete
colonies at a depth of approximately 100 m using the
R/V Nereus and ROV Sperre SUB-Fighter 7500, and
transported to the Sven Lov
en Centre for Marine
Sciences (University of Gothenburg) at Tj
o. Corals
were maintained in flow-through aquaria with sand-fil-
tered water (3235 psu and 8 °C) with water intake
from 45 m depth. In June 2014, corals were moved to
the Sven Lov
en Centre facility at Kristineberg and main-
tained in a 40 l flow-through aquarium (3235 psu and
8°C) with water intake from 32 m. Corals were allowed
to acclimate to the conditions at the Kristineberg facility
for 1 month prior to the start of the experiment. The
experiment for the Tisler Reef population began in
August 2014.
Experimental design
While we attempted to minimize methodological differ-
ences between the Gulf of Mexico and Tisler Reef experi-
ments, some modifications (described below) were
necessary due to the available facilities and equipment, as
well as differences in the Lophelia pertusa colonies them-
selves. Corals were randomly assigned to 20-l experimental
flow-through aquaria at the Kristineberg facility with an
average flow rate of 1.5 0.2 lmin
. Two replicate aqua-
ria were established for each treatment, each containing
four coral colonies (n =8 per treatment). pH was con-
trolled to within 0.05 in each experimental aquarium
using the AquaMedic pH computer (Bissendorf, Germany)
via the direct injection of gaseous CO
. pH was measured
daily on the total scale on filtered water samples (0.45
micron acetate syringe filter) using a Metrohm (827 pH
lab) electrode calibrated using standard Tris-HCl and
AMP-HCl buffers (Unite d’Oceanographie Chimique,
ege, Belgium). Total alkalinity was mea-
sured twice weekly on filtered water samples (0.45 micron
acetate syringe filter) by acid titration on a Titroline Alpha
Plus titrator (SI Analytics). pH
and Ω
were statistically
indistinguishable between replicate tanks (KruskalWallis
ANOVA, P >0.05) but statistically distinct among all
treatments (KruskalWallis ANOVA with Student–
Newman–Keuls post-hoc,P<0.001). Temperature aver-
aged 7.9 0.07 °C across all treatments, and was not sta-
tistically different in any treatment (KruskalWallis
ANOVA, P >0.9). It was not possible to control salinity
(average of 33.3 0.4 psu), which was slightly lower than
in the Gulf of Mexico experiment, but was statistically iden-
tical across treatments (KruskalWallis ANOVA, P >0.9).
Dissolved oxygen was also slightly lower than in the Gulf of
Mexico experiment, averaging 5.71 0.3 mll
, but was
identical across treatments (KruskalWallis ANOVA,
P>0.9). Total alkalinity averaged 2310 24 lmolkg
and was not statistically different across treatments
(KruskalWallis ANOVA, P =0.813). Because total alka-
linity was within the normal range for L. pertusa at this site,
it was not altered in the experimental aquaria.
Physiological measurements
Net calcification was measured using the total alkalinity
anomaly (Smith & Key 1975; Ohde & Hossain 2004)
rather than buoyant weighing, because in preliminary tri-
als, small colonies (such as those available from the Tisler
Reef) were prone to considerably more error using the
buoyant weighing method (data not shown). Corals were
individually placed in closed glass chambers (220 ml) in
a water bath that maintained temperature to 0.2 °C
during all trials. To avoid hypoxia or the severe reduc-
tions of pH during incubations, ambient air was continu-
ously bubbled into the side of the chambers at a slow
Marine Ecology ª2016 Blackwell Verlag GmbH 5
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
rate (12 bubbless
). This also provided adequate circu-
lation within the chamber. A 60-ml water sample was
collected by syringe before and after the 12-h incubation
period, and measured for total alkalinity in duplicate as
described above. In addition, three seawater-only cham-
bers were measured along with each treatment group to
account for microbial activity. Changes in alkalinity
within the control chambers were subtracted from the
results from the chambers with corals. Net calcification
was then calculated as lmol CaCO
using the
following formula:
calcification = 0:5V½ðDTAFÞðDTACÞ=TTW;
where V is the volume of seawater in liters, DTA
is the
average change in total alkalinity during the incubation of
each fragment, DTA
is the average change in total alka-
linity during the control incubations, T is the incubation
time in hours and TW is the final tissue weight of each
fragment in grams. To allow for comparison to other
studies, we then calculated net calcification as % starting
. While the excretion of nutrients can intro-
duce error into this method, we did not account for this
here because previous studies have described the influence
as negligible (Maier et al. 2012; Hennige et al. 2014).
Respiration trials were conducted for each coral colony
as described above; however, due to the smaller size of
the colonies (average size of 5.5 1.5 polyps compared
to an average of 10.8 3.2 polyps in the Gulf of Mexico
experiment), a smaller chamber (400 ml) was used for
incubations. Microbial respiration was accounted for by
measuring oxygen consumption in an empty chamber,
but was consistently negligible at 0.98 0.18 (SD) lmol
(n =16). Measurements of the dried tissue
weight and capture rate of A. salina adults were con-
ducted for each coral colony as described above.
Statistical analysis
The water chemistry parameters of experimental aquaria
were compared separately for the Tisler Reef and Gulf of
Mexico experiments using a one-way ANOVA with
HolmSidak post-hoc tests if the data were normally dis-
tributed with equal variances. Otherwise, we used a
KruskalWallis ANOVA with StudentNewmanKeuls
post-hoc tests. Following a model selection process using
the Akaike information criterion to select the best model
type, linear regressions were used to assess the relation-
ship between each physiological rate and pH. Analyses of
covariance (ANCOVAs) were then used to compare the
response of Tisler Reef and Gulf of Mexico corals to
reduced pH. Statistical analyses were conducted in JMP
version 12.1.0 (ANOVAs and linear regressions, SAS
Institute Inc., Cary, NC, USA) and R version 3.1.2
(ANCOVAs, R Development Core Team 2008) using an
alpha level of 0.05. All data are presented as aver-
ages SD unless otherwise stated.
Tissue and behavior
There was no observed tissue or polyp mortality in any
treatment in either the Gulf of Mexico or Tisler Reef
experiments. Qualitatively, Gulf of Mexico corals exhib-
ited greater signs of visual stress in acidified treatments,
including frequently retracted polyps, extended mesentery
filaments (acontia) and increased mucus production. In
contrast, Tisler Reef corals exhibited no obvious visual
indications of stress; polyps in all treatments were gener-
ally extended and active, especially in the presence of
food. Corals from both sites maintained a full coverage
of coenosarc tissue layer in all treatments, preventing the
direct exposure of skeleton to seawater.
Net calcification
Within the Gulf of Mexico experiment, net calcification
under in situ conditions (pH
=7.9) was variable,
ranging from 0.0260.048%day
with an average of
0.036 0.007%day
. Net calcification was linearly
dependent on pH, with a decrease of 0.1485%day
(linear regression, r
=0.84, P <0.001) (Table 2,
Fig. 2). Corals in the pH
=7.75 treatment had a reduced
but positive net calcification rate of 0.0176 0.012%
, while corals in the 7.6 treatment exhibited net
dissolution of skeletal material at an average rate of
0.009 0.003%day
, although it was not possible to
determine whether gross calcification occurred but at a
lower rate than dissolution.
Tisler Reef corals exhibited higher and more variable net
calcification in the control treatment, with rates ranging
from 0.0470.085%day
and an average rate of
0.067 0.016%day
. Net calcification in the low pH
treatment (pH
=7.75) averaged 0.056 0.015%
, and all colonies exhibited positive net calcification
in the undersaturated treatment (pH
=7.6) with an aver-
age of 0.048 0.011%day
. While net calcification in
Tisler Reef corals decreased (0.0593%day
pH unit
significantly under reduced pH conditions (Table 2; linear
regression, r
=0.25, P =0.013), all colonies exhibited pos-
itive net calcification even in undersaturated conditions.
An ANCOVA demonstrated significant differences in
the slopes (ANCOVA, F
=12.96, P <0.001) and
6Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
intercepts (ANCOVA, F
=157.69, P <0.0001) of the
Gulf of Mexico and Tisler Reef linear regressions, indicat-
ing that reduced seawater pH caused larger reductions in
net calcification in the Gulf of Mexico population
(Table 3). The combined net calcification rates (%day
of both Tisler Reef and Gulf of Mexico corals in the con-
trol treatment (pH
=7.9) were negatively correlated with
their starting dry weight, indicating that smaller corals
from both sites calcified at a proportionally higher rate
than large colonies (linear regression, r
=0.27, P <0.05).
Gulf of Mexico and Tisler Reef corals exhibited contrast-
ing metabolic responses to acidification (Fig. 3). In the
Table 2. Results of the linear regression
models assessing the relationship between pH
and physiological rates for Gulf of Mexico
and Tisler Reef corals.
site rate r
equation FP
Gulf of Mexico calcification 0.84 y=0.1485x1.1385 134.68 <0.0001
respiration 0.68 y=14.25x106.07 54.10 <0.0001
feeding 0.16 y=2.9105x20.913 4.60 0.042
Tisler Reef calcification 0.25 y=0.0593x0.4024 7.39 0.013
respiration 0.52 y=11.054x+92.955 23.33 <0.0001
feeding 0.32 y=11.106x+96.437 10.21 0.00418
Fig. 2. Net calcification (%day
) of coral colonies after 14 days in
each pH treatment [pH on the total scale (pH
)=7.9, 7.75, 7.6].
Tisler Reef experimental data shown as blue triangles. Gulf of Mexico
experimental data shown as red circles. Vertical error bars indicate
the SD for net calcification measurements; horizontal error bars
indicate the SD of pH measured over the experimental period.
Dashed lines indicate linear regressions for the Gulf of Mexico
(red; r
=0.84, P <0.001) and Tisler Reef (blue; r
=0.25, P =0.01)
data. The slope [analysis of covariance (ANCOVA), F
P<0.001] and intercept (ANCOVA, F
=157.69, P <0.0001) of
the site regressions are significantly different. pCO
pressure; atm, microatmospheres.
Table 3. Results of the analyses of covariance testing whether the
relationship between pH and physiological rates differed significantly
between Gulf of Mexico and Tisler Reef corals. See Table 2 for results
of the individual linear regression models.
rate effect residual df SS FP
calcification slope 47 0.0016 13.0 <0.001
intercept 48 0.0242 157.7 <0.0001
respiration slope 47 128.07 72.1 <0.0001
intercept 48 89.47 20.3 <0.0001
feeding slope 47 39.3 15.0 <0.001
intercept 48 932.1 275.5 <0.0001
df =degrees of freedom; SS =sum of squares.
Fig. 3. Respiration rate [lmol O
g tissue weight (TW)
coral colonies after 14 days in each pH treatment [pH on the total
scale (pH
)=7.9, 7.75, 7.6]. Tisler Reef experimental data shown as
blue triangles. Gulf of Mexico experimental data shown as red circles.
Vertical error bars indicate the SD for respiration rate measurements;
horizontal error bars indicate the SD of pH measured over the
experimental period. Dashed lines indicate linear regressions for the
Gulf of Mexico (red; r
=0.68, P <0.0001) and Tisler Reef (blue;
=0.52, P <0.0001) data. The slope [analysis of covariance
(ANCOVA), slope, F
=72.1, P <0.0001] and intercept (ANCOVA,
intercept, F
=20.3, P <0.0001) of the site regressions are
significantly different. pCO
partial pressure; atm,
Marine Ecology ª2016 Blackwell Verlag GmbH 7
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
control treatments (pH
=7.9), Gulf of Mexico corals
respired at an average rate of 6.9 1.8 lmol
, with a range of 4.89.5 lmol O
. Across all treatments, respiration in Gulf of
Mexico corals was highly variable (2.19.5 lmol
), with an average rate of 4.4 1.1 lmol
in the low pH treatment (pH
and 2.6 0.5 lmol O
in the very low pH
treatment (pH
=7.6). Respiration was significantly
dependent on pH, with reduced respiration observed
under lower pH conditions (Table 2; linear regression,
=0.68, P <0.0001).
Tisler Reef corals respired at an average rate of
5.5 1.8 lmol O
in the control treatment
=7.9), 7.4 1.6 lmol O
in the low
pH treatment (pH
=7.75) and 8.9 1.7 lmol
in the very low pH treatment (pH
Respiration was significantly dependent on pH, with con-
siderably elevated rates observed under reduced-pH condi-
tions (Table 2, Fig. 3; linear regression, r
P<0.0001). The Tisler Reef and Gulf of Mexico popula-
tions exhibited significantly different respiration responses
to pH (ANCOVA, slope, F
=72.1, P <0.0001;
ANCOVA, intercept, F
=20.3, P <0.0001; Table 3),
with Tisler Reef corals respiring at a higher rate under
reduced seawater pH and Gulf of Mexico corals respiring
at a lower rate.
Capture rate
The capture rate of Gulf of Mexico corals was relatively
low across all pH treatments (Fig. 4), averaging 2.1 1.2
in the control treatment (pH
1.7 0.5 preypolyp
in the low pH treatment
=7.75) and 1.3 0.9 preypolyp
in the very
low pH treatment (pH
=7.6). Reductions in seawater
pH were correlated with a small but significant reduction
in capture rate (linear regression, r
=0.16, P =0.04;
Table 2), although the removal of a single outlier in the
control treatment rendered this relationship insignificant
(linear regression, r
=0.07, P =0.11).
The Tisler Reef population exhibited a markedly differ-
ent feeding response to reduced seawater pH (Fig. 4).
Corals in the control treatment (pH
=7.9) fed at a rela-
tively variable rate ranging from 6.710.3 prey
, with an average capture rate of 8.6 1.5
. Reduced pH conditions were signifi-
cantly correlated with elevated capture rates (linear
regressions, r
=0.32, P <0.01), with the highest capture
rates observed in the low pH treatment (pH
average of 10.4 2.1 preypolyp
) and the very low
pH treatment (pH
=7.6; average of 12.0 2.9 prey
). An ANCOVA test revealed that the slopes
=15.0, P <0.001) and intercepts
(Table 3; ANCOVA, F
=275.5, P <0.0001) of the
Gulf of Mexico and Tisler Reef regression models were
significantly different, indicating that the two populations
had contrasting feeding responses to reduced pH.
Recent experimental work has revealed considerable vari-
ation in the physiological response of cold-water corals to
ocean acidification (Maier et al. 2009, 2012, 2013a,b;
Form & Riebesell 2012; Hennige et al. 2014; Lunden et al.
2014a), rendering the future of cold-water coral ecosys-
tems unclear. In the present study, we demonstrated that
contrasting responses to identical pH changes can be
observed between two populations of the cold-water coral
Lophelia pertusa. Gulf of Mexico corals exhibited reduced
physiological performance in all tested parameters, a
commonly observed stress-response in marine inverte-
brates (e.g. Kaniewska et al. 2012). In contrast, Tisler Reef
corals were able to maintain net calcification by elevating
respiration and capture rates, a strategy that may confer
some resilience to acidification if it can be maintained
over extended time periods (e.g. Stumpp et al. 2011).
Fig. 4. Capture rate (preypolyp
) of coral colonies after
14 days in each pH treatment [pH on the total scale (pH
7.75, 7.6]. Tisler Reef experimental data shown as blue triangles. Gulf
of Mexico experimental data shown as red circles. Vertical error bars
indicate the SD for capture rate measurements; horizontal error bars
indicate the SD of pH measured over the experimental period.
Dashed lines indicate linear regressions for the Gulf of Mexico (red;
=0.16, P =0.04) and Tisler Reef (blue; r
=0.32, P <0.01) data.
The slope [analysis of covariance (ANCOVA), slope, F
P<0.001] and intercept (ANCOVA, intercept, F
P<0.0001) of the site regressions are significantly different. pCO
partial pressure, atm, microatmospheres.
8Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
Differences in experimental methodology may explain
some of the large variability observed among L. pertusa
populations, both in this and in previous studies. One of
the major experimental differences in the present study
was the use of a flow-through system in the Tisler Reef
experiment and recirculating aquaria in the Gulf of Mex-
ico experiment. Previous cold-water coral physiology
studies have utilized both systems, perhaps accounting
for some of the variability among studies. Despite evi-
dence that recirculating systems are adequate for housing
shallow-water (Barron et al. 2010) and deep-sea (Lunden
et al. 2014a,b) corals, it is plausible that this difference
partially accounted for the lower physiological perfor-
mance observed in the Gulf of Mexico corals, as previous
studies have found reduced physiological rates in recircu-
lating systems (e.g. Otoshi et al. 2003; but see Tomoda
et al. 2005). However, we did not observe any detectable
buildup of waste products (nitrate, nitrite or ammonia;
data not shown) during the course of the present study.
In addition, the Instant Ocean
artificial seawater used in
the current study matches the chemical composition of
seawater better than other artificial mixes (Atkinson &
Bingman 1998), and has been successfully used in a large
number of physiology experiments (Marchant et al. 2010;
Castillo et al. 2014; Lunden et al. 2014a). Regardless, it is
possible that the recirculating system was sub-optimal
and could partially explain the lower absolute net calcifi-
cation measurements recorded for the Gulf of Mexico
Another experimental difference that may partially
explain our results was the use of the alkalinity anomaly
technique for the Tisler Reef experiment and the buoyant
weighing technique for the Gulf of Mexico experiment.
While both methods have abundant support in the coral
literature (Maier et al. 2009, 2013b; Ries et al. 2010; Cohen
& Fine 2012; Form & Riebesell 2012; Larsson et al. 2013),
it is plausible that this discrepancy partially explains the
considerably higher net calcification rates in the Tisler Reef
corals. The total alkalinity anomaly technique may overes-
timate calcification if microbial activity considerably
reduces alkalinity during incubations; however, our
seawater-only control chambers did not reveal such an
effect. In addition, the net calcification rates measured in
this study for Tisler Reef corals using the total alkalinity
anomaly (control average of 0.067 0.02%day
) were
comparable to previous rates measured at Tisler Reef
using the buoyant weighing technique (average of
0.046 0.02%day
; Larsson et al. 2013), and studies
directly comparing the two methods have not revealed sig-
nificant differences in either tropical (Holcomb et al.
2010) or cold-water corals (Maier et al. 2013b).
The net calcification rates measured in this study were
well within the range previously reported for L. pertusa
(Maier et al. 2009, 2012; Form & Riebesell 2012; Larsson
et al. 2013; Hennige et al. 2014). However, we observed
considerable variability both within and between the Gulf
of Mexico and Tisler Reef populations. Under control
conditions (pH
=7.9), the net calcification rate of the
Tisler Reef corals was approximately double the rate
observed in the Gulf of Mexico corals. This difference
may be partially due to the smaller size of the Tisler Reef
fragments, as we found that net calcification in the con-
trol treatment was negatively correlated with starting
weight. Previous work has also found that smaller, more
apical L. pertusa fragments have a higher growth rate
(Brooke & Young 2009). High variability was also
observed among individuals from the same site and
within the same treatment. However, published measure-
ments of L. pertusa calcification revealed even greater
variation; in one study alone, net calcification rates ran-
ged from 0.0027%day
to 0.19%day
depending on
the age and position of polyps within colonies (Maier
et al. 2009).
Net calcification in both populations significantly
declined under reduced pH, although only the Gulf of
Mexico corals exhibited the net dissolution of existing
skeletal material under very low pH conditions
=7.6). In contrast, the Tisler Reef corals main-
tained positive net calcification across all pH treatments,
in part because calcification did not decrease as steeply
with reduced pH as in the Gulf of Mexico corals. The
stark contrast in the ability of the Tisler Reef and Gulf of
Mexico corals to maintain calcification in conditions
expected by the end of the century has considerable
implications for their future viability. Previous studies
have also found that L. pertusa from the North Atlantic
maintains positive net calcification even when grown in
undersaturated conditions (e.g. Form & Riebesell 2012;
Maier et al. 2013b; Hennige et al. 2015), while the only
study from the Gulf of Mexico documented net dissolu-
tion in undersaturated conditions (Lunden et al. 2014a).
Recent experimental work has shown that cold-water cor-
als are able to tightly regulate the pH of their internal
calcifying fluid through the active removal of protons
(Anagnostou et al. 2012; McCulloch et al. 2012; Wall
et al. 2015). As a result, the saturation state of the calci-
fying fluid is elevated to several times that of the external
seawater, allowing for CaCO
precipitation even when
the external seawater is undersaturated. However,
decreasing seawater pH considerably increases the energy
required to maintain this large pH gradient, with an esti-
mated 10% energy increase per 0.1 pH unit decrease
(McCulloch et al. 2012). Therefore, while this work pro-
vides a viable mechanism for calcification under acidified
conditions, there are likely to be potential disruptions to
the energy budget of the coral and associated changes to
Marine Ecology ª2016 Blackwell Verlag GmbH 9
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
the rate of calcification and other key physiological
Given the increased energy required to calcify under
reduced pH, the observed calcification response may have
been partially controlled by the metabolic rates of each
population. Respiration has been shown to be coupled to
calcification under both ambient and reduced pH condi-
tions in tropical (e.g. Kaniewska et al. 2012) and cold--
water corals (Maier et al. 2013a). Aerobic respiration is
required to fuel adenosine triphosphate-driven processes
in corals, and is critically linked to the active transport of
and Ca
ions during calcification (Al-Horani et al.
2003). In the present study, Tisler Reef and Gulf of Mex-
ico corals exhibited contrasting metabolic responses to
acidification. The Gulf of Mexico corals experienced sig-
nificantly reduced respiration rates in both low pH treat-
ments, suggesting the onset of metabolic depression, a
mechanism that enhances survival under short-lived dis-
turbances at the cost of some biological functioning
(Guppy & Withers 1999; Thomsen & Melzner 2010). In
contrast, the Tisler Reef corals significantly elevated respi-
ration rates in response to acidified seawater. This meta-
bolic strategy has the potential to supply enough
additional energy to maintain positive net calcification
even under acidified conditions, but may create an ener-
getic imbalance that can only be sustained by catabolizing
energy reserves (Rodrigues & Grottoli 2007) or obtaining
additional energy from the environment.
The ability to increase energy intake from the environ-
ment via elevated feeding has been shown to reduce or
negate the effects of acidification and other stressors in
tropical corals (Cohen & Holcomb 2009). However, no
previous study has assessed whether cold-water corals are
capable of altering their capture rate in response to cli-
mate change conditions. In the present study, the Gulf of
Mexico corals had lower capture rates under control
conditions (pH
=7.9, average rate of 2.1 1.2
A. salinapolyp
) than have previously been mea-
sured for L. pertusa (7.8 A. salinapolyp
; Tsounis
et al. 2010). In contrast, the Tisler Reef corals had a
higher capture rate of A. salina prey under control condi-
tions (pH
=7.9, average rate of 8.6 1.5
A. salinapolyp
), and significantly elevated feeding
under reduced pH conditions. It is possible that the con-
siderably lower baseline feeding rate in the Gulf of Mex-
ico corals was due in part to inter-polyp competition for
prey, as the Gulf of Mexico corals had a higher number
of polyps (10.8 3.2 polypscolony
) compared to the
Tisler Reef corals (5.5 1.5 polypscolony
) but the
same prey concentration was used in both experiments.
Previous research on the effects of intra-specific, inter-
polyp competition in scleractinian corals has had mixed
results, with some studies demonstrating that competition
reduced feeding rates and resource acquisition (Merks
et al. 2004; Einbinder et al. 2009; Wijgerde et al. 2011),
and others finding that denser polyp spacing within colo-
nies enhanced feeding rates (McFadden 1986; Wijgerde
et al. 2012). Inter-polyp competition has not yet been
observed in cold-water corals, and as L. pertusa is capable
of self-recognition to avoid intra-specific competition
(Hennige et al. 2014), it is possible that even closely
spaced polyps do not actively compete for food. Never-
theless, it may be fruitful for future research to explore
the effects of polyp number and spacing on L. pertusa’s
feeding rate, as well as the interactive effects of water
flow, pH and prey density.
Regardless of the mechanism underlying the higher
capture rates observed in the Tisler Reef corals, the
increased energy input from feeding likely facilitated their
elevated respiration (see Larsson et al. 2013) and subse-
quent maintenance of positive net calcification rates in
undersaturated conditions. This type of response would
only be favorable in environments where there is a rela-
tively high-quality and reliable food source, such as the
shallower cold-water coral systems in Norway [average
lateral deposition of particulate organic carbon (POC) at
Tisler Reef of 459 mg Cm
; Wagner et al. 2011].
In contrast, the lower food availability at the deeper Gulf
of Mexico VK826 site (modeled POC flux of 46 mg
; Georgian et al. 2014) may not favor this
strategy as pH and saturation state decline. Despite the
apparent resilience conferred on Tisler Reef corals via ele-
vated feeding, predictions that food will become more
limited in future oceans may hamper the ability of in situ
cold-water corals to utilize this strategy in response to cli-
mate change. Ocean acidification has been predicted to
reduce surface phytoplankton by 410%, leading to a
decrease in the POC flux to the deep sea by 613%
(Mora et al. 2013). In some areas, particularly in the Gulf
of Mexico, the anthropogenic eutrophication of marine
systems will act to increase the size and extent of ‘dead
zones’; coupled with the effects of global warming and
deoxygenation, many regions in the deep sea may become
severely food limited in future oceans (Rabouille et al.
2008; Stramma et al. 2010). However, in addition to zoo-
plankton capture, L. pertusa utilizes alternative food
sources including dissolved organic matter, bacteria and
algal detritus (Mueller et al. 2014), and may be able to
increase uptake from these sources.
A number of factors may have been responsible for the
contrasting responses observed in Tisler Reef and Gulf of
Mexico populations, including genetic differences, accli-
mation to local environmental conditions and experimen-
tal differences. Given the limited gene flow between Gulf
of Mexico and Northern Atlantic L. pertusa populations
(Morrison et al. 2011; Lunden et al. 2014a), it is not
10 Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
surprising that they exhibited a very different baseline
physiology as well as a contrasting response to acidifica-
tion. Recent evidence has demonstrated that genetic dif-
ferences may partially explain the considerable intra-
specific variation observed in the physiological tolerance
of tropical coral species (Meyer et al. 2009; Pandolfi et al.
2011). Numerous L. pertusa studies from the Northern
Atlantic and Mediterranean Sea have found higher respi-
ration rates (Hennige et al. 2014), capture rates (Purser
et al. 2010; Tsounis et al. 2010) and calcification rates
(Maier et al. 2009) than measured in the present study or
previously reported for the Gulf of Mexico (Lunden et al.
2014a). If biogeographically separated populations of
L. pertusa exhibit a large variability in their response to
ocean acidification, as suggested by the literature and the
results presented here, some populations may already be
relatively resilient to acidification, giving the species as a
whole a higher adaptive potential to more effectively
respond to acidification and other stressors.
Acclimation to local environmental conditions may
also be partially responsible for the contrasting physiolog-
ical responses of Tisler Reef and Gulf of Mexico popula-
tions. In our study, Tisler Reef corals were collected from
a much shallower depth (100 m) than Gulf of Mexico
corals (450 m). In addition to experiencing a chronically
higher saturation state than the Gulf of Mexico, this
means that the Tisler Reef has a higher influx of high-
quality food (Wagner et al. 2011). Deep-sea environments
are generally food limited because only a fraction of sur-
face productivity is transported to deep waters before
being degraded (Deuser 1986), meaning that both the
quantity and quality of food reaching the sea floor are
highly depth-dependent. Plausibly, Tisler Reef corals are
accustomed to having the necessary resources to increase
their capture rate and subsequently elevate their metabo-
lism in order to allocate additional energy to calcification
during periods of environmental stress.
Cold-water coral habitats are protected as Vulnerable
Marine Ecosystems by the United Nations and have long
been recognized as critical drivers of diversity and ecosys-
tem function in the deep sea (reviewed in Thurber et al.
2014). Considering the potential for major declines in
cold-water coral ecosystems due to ocean acidification
and other stressors, it is imperative to better understand
their potential range of responses. In this study, we found
evidence that corals from the Tisler Reef may be some-
what resilient to acidification over a short time period,
but it is not clear whether this strategy will be sustainable
in the long term given the large increase in feeding
required to maintain calcification under low pH condi-
tions. Importantly, these results demonstrate that the
existing variability among cold-water coral physiological
studies may strongly depend on biogeographic variability,
genetic and environmental differences, and inconsistencies
in experimental designs. Future research would benefit
from comparative studies both within and among large
biogeographic regions that link observed physiological
responses to ocean acidification and other stressors with
differences in local environmental conditions. Such an
approach would provide key insights into the mecha-
nisms underlying the resilience or sensitivity of separated
populations, and identify the environmental conditions
that may drive local adaptation or acclimatization to glo-
bal ocean change. While our current understanding of
the mechanisms and rates of adaptive capacity to envi-
ronmental change does not suggest that the rate of coral
evolution will be able to keep up with the pace of global
changes (Hoegh-Guldberg 2014), it is possible that pre-
existing local adaptations to different or more variable
pH regimes might provide such a capacity at a global
scale (Hofmann et al. 2010). Ultimately, more work is
needed to assess whether natural variability among cold-
water coral populations will provide a significant avenue
of resilience in future oceans.
Funding was provided by the Gulf of Mexico Research
Institute to the Ecosystem Impacts of Oil & Gas Inputs
to the Gulf consortium, and through a National Science
Foundation (NSF) Ocean Acidification Grant (OCE-
1220478 to E.E.C. and to R. Kulathinal). Additional fund-
ing was provided by Integrated Marine Biogeochemistry
and Ecosystem Research and the U.S. Ocean Carbon and
Biochemistry. This work would not have been possible
without support from the crews of the E/V Nautilus and
ROV Hercules, and the R/V Nereus and ROV Sperre SUB-
Fighter 7500. We would like to thank A. Ventura, S.
Schulz and B. Lundve for their assistance at the Kristine-
berg Marine Station. S.D. is funded through a Linnaeus
grant from the Swedish Research Councils Vetens-
adet and The Swedish Research Council Formas.
S.M.S. and A.I.L. were funded by The Swedish Research
Council Formas (contracts 215-2010-1604 and 215-2012-
1134). S.E.G. was funded by the National Science Foun-
dation Graduate Research Fellowship Program (DGE-
1144462) and by the NSF Graduate Research Opportu-
nities Worldwide program. Any opinions, findings and
conclusions or recommendations expressed in this mate-
rial are those of the authors and do not necessarily reflect
the views of the National Science Foundation.
Marine Ecology ª2016 Blackwell Verlag GmbH 11
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
Al-Horani F.A., Al-Moghrabi S.M., De Beer D. (2003) The
mechanism of calcification and its relation to photosynthesis
and respiration in the scleractinian coral Galaxea
fascicularis.Marine Biology,142, 419426.
Anagnostou E., Huang K.F., You C.F., Sikes E.L., Sherrell R.M.
(2012) Evaluation of boron isotope ratio as a pH proxy in
the deep sea coral Desmophyllum dianthus: evidence of
physiological pH adjustment. Earth Planetary Science Letters,
349, 251260.
Anthony K.R.N., Kline D.I., Diaz-Pulido G., Dove S., Hoegh-
Guldberg O. (2008) Ocean acidification causes bleaching
and productivity loss in coral reef builders. Proceedings of
the National Academy of Sciences of the United States of
America,105, 1744217446.
Atkinson M.J., Bingman C. (1998) Elemental composition of
commercial seasalts. Journal of Aquariculture and Aquatic
Barron M.G., McGill C.J., Courtney L.A., Marcovich D.T.
(2010) Experimental bleaching of a reef-building coral using
a simplified recirculating laboratory exposure system.
Journal of Marine Biology,2010, 415167.
Brooke S., Young C.M. (2009) In situ measurement of survival
and growth of Lophelia pertusa in the northern Gulf of
Mexico. Marine Ecology Progress Series,397, 153161.
Canadell J.G., Le Qu
e C., Raupach M.R., Field, C. B.,
Buitenhuis, E. T., Ciais, P., Conway, T. J., Gillett, N. P.,
Houghton, R. A., & Gregg, M. (2007) Contributions to
accelerating atmospheric CO
growth from economic
activity, carbon intensity, and efficiency of natural sinks.
Proceedings of the National Academy of Sciences of the United
States of America,104, 1886618870.
Castillo K.D., Ries J.B., Bruno J.F., Westfield I.T. (2014) The
reef-building coral Siderastrea siderea exhibits parabolic
responses to ocean acidification and warming. Proceedings of
the Royal Society B: Biological Sciences,281, 20141856.
Cohen S., Fine M. (2012) Measuring gross and net
calcification of a reef coral under ocean acidification
conditions: methodological considerations. Biogeosciences
Discussions,9, 82418272.
Cohen A.L., Holcomb M. (2009) Why corals care about ocean
acidification: uncovering the mechanism. Oceanography,22,
Cordes E.E., McGinley M.P., Podowski E.L., Becker E.L.,
Lessard-Pilon S., Viada S.T., Fisher C.R. (2008) Coral
communities of the deep Gulf of Mexico. Deep Sea Research
I,55, 777787.
Davies P.S. (1989) Short-term growth measurements of corals
using an accurate buoyant weighing technique. Marine
Biology,101, 389395.
Davies A.J., Guinotte J.M. (2011) Global habitat suitability
for framework-forming cold-water corals. PLoS ONE,6,
Davies A.J., Wisshak M., Orr J.C., Roberts J.M. (2008)
Predicting suitable habitat for the cold-water coral
Lophelia pertusa (Scleractinia). Deep Sea Research I,55,
Davies A.J., Duineveld G., van Weering T., Mienis, F.,
Quattrini, A. M., Seim, H. E., Bane, J. M., & Ross, S. W.
(2010) Short-term environmental variability in cold-water
coral habitat at Viosca Knoll, Gulf of Mexico. Deep-Sea
Research I,57, 199212.
Deuser W.G. (1986) Seasonal and interannual variations in
deep-water particle fluxes in the Sargasso Sea and their
relation to surface hydrography. Deep-Sea Research I,33,
Dove S.G., Kline D.I., Pantos O., Angly F.E., Tyson G.W.,
Hoegh-Guldberg O. (2013) Future reef decalcification under
a business-as-usual CO
emission scenario. Proceedings of
the National Academy of Sciences of the United States of
America,110, 1534215347.
Drazen J.C., Seibel B. (2007) Depth-related trends in
metabolism of benthic and benthopelagic deep-sea fishes.
Limnology and Oceanography,52, 23062316.
Einbinder S., Mass T., Brokovich E., Dubinsky Z., Erez J.,
Tchernov D. (2009) Changes in morphology and diet of the
coral Stylophora pistillata along a depth gradient. Marine
Ecology Progress Series,381, 167174.
Form A.U., Riebesell U. (2012) Acclimation to ocean
acidification during long-term CO
exposure in the cold-
water coral Lophelia pertusa.Global Change Biology,18,
a J.H., Skjoldal H.R. (2010) Conservation of Cold-Water
Coral Reefs in Norway. Oxford University Press, New York,
NY, USA: 215230.
Georgian S.E., Shedd W., Cordes E.E. (2014) High-resolution
ecological niche modelling of the cold-water coral Lophelia
pertusa in the Gulf of Mexico. Marine Ecology Progress
Series,506, 145161.
Georgian S.E., DeLeo D., Durkin A., Gomez C.E., Kurman M.,
Lunden J.J., Cordes E.E. (2016) Oceanographic patterns and
carbonate chemistry in the vicinity of cold-water coral reefs
in the Gulf of Mexico: implications for resilience in a
changing ocean. Limnology and Oceanography,61, 648665.
Guinotte J.M., Orr J., Cairns S., Freiwald A., Morgan L.,
George R. (2006) Will human-induced changes in seawater
chemistry alter the distribution of deep-sea scleractinian
corals? Frontiers in Ecology and the Environment,4, 141146.
Guppy M., Withers P. (1999) Metabolic depression in animals:
physiological perspectives and biochemical generalizations.
Biological Reviews of the Cambridge Philosophical Society,74,
Hennige S.J., Wicks L.C., Kamenos N.A., Bakker D.C.E.,
Findlay H.S., Dumousseaud C., Roberts J.M. (2014) Short-
term metabolic and growth responses of the cold-water
coral Lophelia pertusa to ocean acidification. Deep Sea
Research II,99,2735.
12 Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
Hennige S.J., Wicks L.C., Kamenos N.A., Perna G., Findlay
H.S., Roberts J.M. (2015) Hidden impacts of ocean
acidification to live and dead coral framework. Proceedings
of the Royal Society B,282, 20150990.
Hoegh-Guldberg O. (2014) Coral reef sustainability through
adaptation: glimmer of hope or persistent mirage? Current
Opinion in Environmental Sustainability,7, 127133.
Hofmann G.E., Barry J.P., Edmunds P.J., Gates R.D., Hutchins
D.A., Klinger T., Sewell M.A. (2010) The effect of ocean
acidification on calcifying organisms in marine ecosystems:
an organism-to-ecosystem perspective. Annual Review of
Ecology, Evolution, and Systematics,41, 127147.
Holcomb M., McCorkle D.C., Cohen A.L. (2010) Long-term
effects of nutrient and CO
enrichment on the temperate
coral Astrangia poculata (Ellis and Solander, 1786). Journal
of Experimental Marine Biology and Ecology,386,2733.
IPCC (2013) Summary for policymakers. In: Stocker T.F., Qin
D., Plattner G.K., et al. (Eds), Climate Change 2013: The
Physical Science Basis. Contribution of Working Group I to
the Fifth Assessment Report of the Intergovernmental Panel on
Climate Change. Cambridge University Press, Cambridge:
Jokiel P.L., Maragos J.W., Franzisket L. (1978) Coral growth
buoyant weight technique. In: Stoddart D.R., Johannes R.E.
(Eds), Monographs on Oceanographic Methodology.
UNESCO, Paris: 529542.
Kaniewska P., Campbell P.R., Kline D.I., Rodriguez-Lanetty
M., Miller D.J., Dove S., Hoegh-Guldberg O. (2012) Major
cellular and physiological impacts of ocean acidification on
a reef building coral. PLoS ONE,7, 34659.
Langer G., Nehrke G., Probert I., Ly J., Ziveri P. (2009) Strain-
specific responses of Emiliania huxleyi to changing seawater
carbonate chemistry. Biogeosciences,6, 26372646.
Larsson A.I., Lund
alv T., van Oevelen D. (2013) Skeletal
growth, respiration rate and fatty acid composition in the
cold-water coral Lophelia pertusa under varying food
conditions. Marine Ecology Progress Series,483, 169184.
Lavaleye M.G., Duineveld T., Lund
alv M., White M., Guihen
D., Kiriakoulakis K., Wolff G.A. (2009) Cold-water corals
on the Tisler Reef. Oceanography,22,7684.
Le Goff-Vitry M.C., Pybus O.G., Rogers A.D. (2004) Genetic
structure of the deep-sea coral Lophelia pertusa in the
northeast Atlantic revealed by microsatellites and internal
transcribed spacer sequences. Molecular Ecology,13, 537
Lessard-Pilon S., Podowski E.L., Cordes E.E., Fisher C.R.
(2010) Megafauna community composition associated with
Lophelia pertusa colonies in the Gulf of Mexico. Deep Sea
Research II,57, 18821890.
alv T., Jonsson L. (2003) Mapping of Deep-Water Corals
and Fishery Impacts in the NE Skagerrak, using Acoustical
and ROV Survey Techniques. Proceedings of the 6th
Underwater Science Symposium, Aberdeen, UK.
Lunden J.J., Georgian S.E., Cordes E.E. (2013) Aragonite
saturation states at cold-water coral reefs structured by
Lophelia pertusa in the northern Gulf of Mexico. Limnology
and Oceanography,58, 354362.
Lunden J.J., McNicholl C.G., Sears C.R., Morrison C.L.,
Cordes E.E. (2014a) Acute survivorship of the deep-sea
coral Lophelia pertusa from the Gulf of Mexico under
acidification, warming, and deoxygenation. Frontiers in
Marine Science,1, 78.
Lunden J.J., Turner J.M., McNicholl C.G., Glynn C.K., Cordes
E.E. (2014b) Design, development, and implementation of
recirculating aquaria for maintenance and experimentation
of deep-sea corals and associated fauna. Limnology and
Oceanography: Methods,12, 363372.
Maier C., Hegeman J., Weinbauer M.G., Gattuso J.P. (2009)
Calcification of the cold-water coral Lophelia pertusa under
ambient and reduced pH. Biogeosciences,6, 16711680.
Maier C., Watremez P., Taviani M., Weinbauer M.G., Gattuso
J.P. (2012) Calcification rates and the effect of ocean
acidification on Mediterranean cold-water corals.
Proceedings of the Royal Society B: Biological Sciences,279,
Maier C., Bils F., Weinbauer M.G., Watremez P., Peck M.A.,
Gattuso J.P. (2013a) Respiration of Mediterranean cold-
water corals is not affected by ocean acidification as
projected for the end of the century. Biogeosciences,10,
Maier C., Schubert A., S
anchez M.M.B., Weinbauer M.G.,
Watremez P., Gattuso J.P. (2013b) End of the century pCO
levels do not impact calcification in Mediterranean cold-
water corals. PLoS ONE,8, e62655.
Marchant H.K., Calosi P., Spicer J.I. (2010) Short-term
exposure to hypercapnia does not compromise feeding,
acid-base balance or respiration of Patella vulgata but
surprisingly is accompanied by radula damage. Journal of
the Marine Biological Association of the United Kingdom,90,
McCulloch M., Trotter J., Montagna P., Falter, J., Dunbar, R.,
Freiwald, A., F
orsterra, G., Correa, M. L., Maier, C.,
uggeberg, A., & Taviani, M. (2012) Resilience of cold-
water scleractinian corals to ocean acidification: Boron
isotopic systematics of pH and saturation state up-
regulation. Geochimica et Cosmochimica Acta,87,2134.
McFadden C.S. (1986) Colony fission increases particle capture
rates of a soft coral: advantages of being a small colony.
Journal of Experimental Marine Biology and Ecology,103,1
Melzner F., Gutowska M.A., Langenbuch M., Dupont, S.,
Lucassen, M., Thorndyke, M. C., Bleich, M., & Portner, H. O.
(2009) Physiological basis for high CO
tolerance in marine
ectothermic animals: pre-adaptation through lifestyle and
ontogeny? Biogeosciences,6, 23132331.
Merks R.M., Hoekstra A.G., Kaandorp J.A., Sloot P.M. (2004)
Polyp oriented modelling of coral growth. Journal of
Theoretical Biology,21, 559576.
Meyer E., Davies S., Wang S., Willis B.L., Abrego D., Juenger
T.E., Matz M.V. (2009) Genetic variation in responses to a
Marine Ecology ª2016 Blackwell Verlag GmbH 13
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
settlement cue and elevated temperature in the reef-building
coral Acropora millepora.Marine Ecology Progress Series,392,
Mienis F., Duineveld G.C.A., Davies A.J., Ross S.W., Seim H.,
Bane J., Van Weering T.C.E. (2012) The influence of near-
bed hydrodynamic conditions on cold-water corals in the
Viosca Knoll area, Gulf of Mexico. Deep Sea Research I,60,
Mora C., Wei C., Rollo A., Amaro, T., Baco, A. R., Billett, D.,
Bopp, L., Chen, Q., Collier, M., Danovaro, R., & Gooday,
A. J. (2013) Biotic and human vulnerability to projected
changes in ocean biogeochemistry over the 21st century.
PLoS Biology,11, e1001682.
Morrison C.L., Ross S.W., Nizinski M.S., Brooke, S.,
Jarnegren, J., Waller, R. G., Johnson, R. L., & King, T. L.
(2011) Genetic discontinuity among regional populations of
Lophelia pertusa in the North Atlantic Ocean. Conservation
Genetics,12, 713729.
Movilla J., Orejas C., Calvo E., Gori, A., L
o, J., Dom
o, C., & Pelejero, C. (2014)
Differential response of two Mediterranean cold-water
coral species to ocean acidification. Coral Reefs,33, 675
Mueller C.E., Larsson A.I., Veuger B., Middelburg J.J., van
Oevelen D. (2014) Opportunistic feeding on various organic
food sources by the cold-water coral Lophelia pertusa.
Biogeosciences,11, 123133.
van Oevelen D., Duineveld G., Lavaleye M., Mienis F., Soetaert
K., Heip C.H.R. (2009) The cold-water coral community as
a hot spot for carbon cycling on continental margins: a
food-web analysis from Rockall Bank (northeast Atlantic).
Limnology and Oceanography,54, 18291844.
Ohde S., Hossain M.M.M. (2004) Effect of CaCO
saturation state of seawater on calcification of Porites coral.
Geochemical Journal,38, 613621.
Orejas C., Ferrier-Pages C., Reynaud S., Gori, A., Beraud, E.,
Tsounis, G., Allemand, D., & Gili, J. M. (2011) Long-term
growth rates of four Mediterranean cold-water coral species
maintained in aquaria. Marine Ecology Progress Series,429,
Otoshi C.A., Arce S.M., Moss S.M. (2003) Growth and
reproductive performance of broodstock shrimp reared in a
biosecure recirculating aquaculture system versus a flow-
through pond. Aquacultural Engineering,29,93107.
Pancic M., Hansen P.H., Tammilehto A., Lundholm N. (2015)
Resilience to temperature and pH changes in a future
climate change scenario in six strains of the polar diatom
Fragilariopsis cylindrus.Biogeosciences Discussions,12, 4627
Pandolfi J.M., Connolly S.R., Marshall D.J., Cohen A.L. (2011)
Projecting coral reef futures under global warming and
ocean acidification. Science,333, 418422.
Parker L.M., Ross P.M., O’Connor W.A. (2011) Populations of
the Sydney rock oyster, Saccostrea glomerata, vary in response
to ocean acidification. Marine Biology,158, 689697.
Pierrot D., Lewis E., Wallace D.W.R. (2006) MS Excel Program
Developed for CO
System Calculations ORNL/CDIAC-105.
Carbon Dioxide Information Analysis Center, Oak Ridge
National Laboratory, U.S. Department of Energy, Oak
Ridge, TN.
Pistevos J.C.A., Calosi P., Widdicombe S., Bishop J.D.D. (2011)
Will variation among genetic individuals influence species
responses to global climate change? Oikos,120, 675689.
Purser A., Larsson A.I., Thomsen L., van Oevelen D. (2010) The
influence of flow velocity and food concentration on Lophelia
pertusa (Scleractinia) zooplankton capture rates. Journal of
Experimental Marine Biology and Ecology,395,5562.
R Development Core Team. (2008). R: A Language and
environment for statistical computing. Vienna: R Foundation
for Statistical Computing. ISBN 3-900051-07-0. http://
Rabouille C., Conley D.J., Dai M.H. (2008) Comparison of
hypoxia among four river-dominated ocean margins: The
Changjiang (Yangtze), Mississippi, Pearl, and Rhone rivers.
Continental Shelf Research,28, 15271537.
Riebesell U., Gattuso J.P. (2015) Lessons learned from ocean
acidification research. Nature Climate Change,5,1214.
Ries J.B., Cohen A.L., McCorkle D.C. (2010) A nonlinear
calcification response to CO
-induced ocean acidification by
the coral Oculina arbuscula.Coral Reefs,29, 661674.
Rodrigues L.J., Grottoli A.G. (2007) Energy reserves and
metabolism as indicators of coral recovery from bleaching.
Limnology and Oceanography,52, 18741882.
Sabine C.L., Feely R.A. (2007) The oceanic sink for carbon
dioxide. In: Reay D., Hewitt N., Grace J., Smith K. (Eds),
Greenhouse Gas Sinks. CABI Publishing, Oxfordshire: 3149.
Schroeder W.W. (2002) Observations of Lophelia pertusa and
the surficial geology at a deep-water site in the northeastern
Gulf of Mexico. Hydrobiologia,471,2933.
Seibel B.A., Drazen J.C. (2007) The rate of metabolism in
marine animals: environmental constraints, ecological
demands and energetic opportunities. Philosophical
Transactions of the Royal Society B: Biological Sciences,362,
Seibel B.A., Walsh P.J. (2003) Biological impacts of deep-sea
carbon dioxide injection inferred from indices of
physiological performance. Journal of Experimental Biology,
206, 641650.
Smith S.V., Key G.S. (1975) Carbon dioxide and metabolism
in marine environments. Limnology and Oceanography,20,
Stramma L., Schmidtko S., Levin L.A., Johnson G.C. (2010)
Ocean oxygen minima expansions and their biological
impacts. Deep Sea Research I,57, 587595.
Stumpp M., Wren J., Melzner F., Thorndyke M.C., Dupont
S.T. (2011) CO
induced seawater acidification impacts sea
urchin larval development I: elevated metabolic rates
decrease scope for growth and induce developmental delay.
Comparative Biochemistry and Physiology Part A: Molecular
& Integrative Physiology,160, 331340.
14 Marine Ecology ª2016 Blackwell Verlag GmbH
Response of L. pertusa to reduced pH Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes
Sunday J.M., Crim R.N., Harley C.D.G., Hart M.W. (2011)
Quantifying rates of evolutionary adaptation in response to
ocean acidification. PLoS ONE,6, e22881.
Thomsen J., Melzner F. (2010) Moderate seawater acidification
does not elicit long-term metabolic depression in the blue
mussel Mytilus edulis.Marine Biology,157, 26672676.
Thresher R.E., Tilbrook B., Fallon S., Wilson N.C., Adkins J.
(2011) Effects of chronic low carbonate saturation levels on
the distribution, growth and skeletal chemistry of deep-sea
corals and other seamount megabenthos. Marine Ecology-
Progress Series,442,8799.
Thurber A.R., Sweetman A.K., Narayanaswamy B.E., Jones
D.O.B., Ingels J., Hansman R.L. (2014) Ecosystem function
and services provided by the deep sea. Biogeosciences,11,
Tomoda T., Fushimi H., Kurokura H. (2005) Performance of
a closed recirculation system for larviculture of red sea
bream, Pagrus major.Fisheries Science,71, 11791181.
Tsounis G., Orejas C., Reynaud S., Gili J.M., Allemand D.,
es C. (2010) Prey-capture rates in four
Mediterranean cold water corals. Marine Ecology Progress
Series,398, 149155.
Wagner H., Purser A., Thomsen L., Jesus C.C., Lund
alv T.
(2011) Particulate organic matter fluxes and hydrodynamics
at the Tisler cold-water coral reef. Journal of Marine
Wall M., Ragazzola F., Foster L.C., Form A., Schmidt D.N.
(2015) Enhanced pH upregulation enables the coldwater
coral Lophelia pertusa to sustain growth in aragonite
undersaturated conditions. Biogeosciences Discussions,12,
Wijgerde T., Diantari R., Lewaru M.W., Verreth J.A.J., Osinga
R. (2011) Extracoelenteric zooplankton feeding is a key
mechanism of nutrient acquisition for the scleractinian coral
Galaxea fascicularis.Journal of Experimental Biology,214,
Wijgerde T., Spijkers P., Karruppannan E., Verreth J.A.,
Osinga R. (2012) Water flow affects zooplankton
feeding by the scleractinian coral Galaxea fascicularis on a
polyp and colony level. Journal of Marine Biology,2012,
Wild C., Huettel M., Klueter A., Kremb S.G., Rasheed M.Y.M.,
Jørgensen B.B. (2004) Coral mucus functions as an energy
carrier and particle trap in the reef ecosystem. Nature,428,
Wittmann A.C., P
ortner H. (2013) Sensitivities of extant
animal taxa to ocean acidification. Nature Climate Change,
3, 9951001.
Marine Ecology ª2016 Blackwell Verlag GmbH 15
Georgian, Dupont, Kurman, Butler, Str
omberg, Larsson & Cordes Response of L. pertusa to reduced pH
... The same set-up used for physiological measurements (containers inside a water bad) was used for the feeding experiments, except the containers were not sealed. Coral fragments were taken in random order from the aquaria and placed inside the containers to allow conditioning of the coral (1 h prior to the addition of the prey), as indicated by the expansion of their polyps (e.g., Gori et al. 2015;Georgian et al. 2016b). After conditioning, all trials lasted four hours (4 h). ...
... Orejas et al. (2016) also found similar capture rates for L. pertusa, which ranged between 10 and 22 zooplankton polyp −1 h −1 in average. In a comparison of Gulf of Mexico and Norwegian populations, Georgian et al. (2016b) found capture rates between 1 and 12 Artemia nauplii polyp −1 h −1 with capture rates decreasing under ocean acidification in the Gulf of Mexico population but increasing in the Norwegian population. ...
... The capacity for coral populations to shift their range (i.e., move poleward) are dependent on larval dispersion and availability of suitable habitat (Price et al. 2019). However, the evidence that L. pertusa colonies within a region have disparate physiological (Kurman et al. 2017) and genetic expression (Glazier et al. 2020) responses to stress, and that different populations behave quite differently under similar conditions (Georgian et al. 2016b), coupled with the apparent flexibility in the L. pertusa microbiome (Meistertzheim et al. 2016) suggest that this species may be able to adapt at the same pace as the predicted environmental conditions. More experimental studies are needed with CWC populations form highly variable environments to help project future outcomes of climate change on ecosystem function, especially if we take into consideration the observed consequences of the arrival of surface warm waters on CWC performance at 700 m depth. ...
Seawater temperature is one of the main variables that determines cold-water coral distribution worldwide. As part of an initiative to explore new areas of deep-sea habitats along the Southeast United States (SEUS) continental margin, a series of expeditions were carried out as part of the Deep-Sea Exploration to Advance Research on Corals/Canyons/Cold seeps (DEEP SEARCH) project. During these explorations, a cold-water coral reef complex composed mainly of Lophelia pertusa was located off the coast of South Carolina at 650–850 m depth. In this geographic area the species normally has a thermal tolerance between 6 and 12 °C with the capacity to form extensive calcium carbonate structures, thus creating complex habitat for a variety of associated species. Owing to the paucity of these structures and the unusual environmental conditions of this geographic area, with regular arrival of warm surface waters from the Gulf Stream, the main aim of this study was to understand the physiological response of L. pertusa to the variation in extreme temperature events in this region. Short-term experiments simulated the rate of temperature increase from the ambient temperature (8 °C) to the environmental maximum (14 °C) (heat-wave treatment). We found that temperature had a significant effect on the metabolic functions through an increase in respiration (0.108 to 0.247 µmol O2 g−1DW h−1) and excretion rates (0.002 to 0.011 µmol NH3 g−1DW h−1) at 14 °C. Oxygen to Nitrogen ratios (O:N) also showed an effect of temperature where corals switched from lipid-dominated toward a mix of lipid-protein and protein-dominated catabolism. To further characterize the metabolic response, feeding assays (capture rate of Artemia) were performed at the same temperature range with an overall three-fold decrease in capture rates under 14 °C compared to ambient temperature, thus increasing the probability of temperature-induced metabolic stress. Our results suggest that temperature variations affect the metabolic response of cold-water corals, particularly along the SEUS continental margin. Since the incursion of warm surface water to deeper zones is predicted to increase in frequency and duration due to climate change, L. pertusa may be implicated negatively, followed by ecological consequences for the survival and functionality for the ecosystem it supports.
... Such compensatory effects may, however, require additional energy or lead to depression of other physiological processes as observed in the tropical scleractinian Pocillopora damicornis (Jiang et al. 2018). Despite the general perception that increased energetic demands can be met by increased feeding rates as observed in some tropical corals (Holocomb et al. 2010;Edmunds 2011), recent studies have shown that not all corals can utilize additional food to compensate for extra energy demands under elevated pCO 2 conditions, including tropical (Houlbrèque et al. 2015) and coldwater corals (Georgian et al. 2016;Büscher et al. 2017;G omez et al. 2018). ...
... Metabolic rates indicate the energy expenditure of an organism and can be estimated indirectly from oxygen consumption (respiration) rates. In cold-water corals, respiration ranged from significantly increased rates under sudden temperature elevations (Dodds et al. 2007) to significantly depressed rates under elevated pCO 2 (Hennige et al., 2014a; Georgian et al. 2016) or elevated temperature (Hennige et al. 2015), to unchanged rates under prolonged acidification (Maier et al. 2013a) and/or warming (Hennige et al. 2015). Little has been reported on combined measurement of growth and metabolic activity, although these physiological processes are closely interlinked and may be impacted differently by changing environmental conditions (Hennige et al. 2015). ...
... Some warm-water scleractinians are able to counteract enhanced energy costs by an increased feeding rate. For some scleractinian species, however, it was observed that food capture rates could not be enhanced to meet additional nutritional demands under acidified conditions, including L. pertusa from various spatially distinct populations (Georgian et al. 2016;Büscher et al. 2017;G omez et al. 2018). The diet of L. pertusa consists of a mix of particulate and dissolved suspended organic matter, with zooplankton being the preferentially assimilated food source at Norwegian reefs (Müller et al. 2014;Maier et al. 2019). ...
Full-text available
Physiological sensitivity of cold‐water corals to ocean change is far less understood than of tropical corals and very little is known about the impacts of ocean acidification and warming on degradative processes of dead coral framework. In a 13‐month laboratory experiment, we examined the interactive effects of gradually increasing temperature and pCO2 levels on survival, growth, and respiration of two prominent color morphotypes (colormorphs) of the framework‐forming cold‐water coral Lophelia pertusa, as well as bioerosion and dissolution of dead framework. Calcification rates tended to increase with warming, showing temperature optima at ~ 14°C (white colormorph) and 10–12°C (orange colormorph) and decreased with increasing pCO2. Net dissolution occurred at aragonite undersaturation (ΩAr < 1) at ~ 1000 μatm pCO2. Under combined warming and acidification, the negative effects of acidification on growth were initially mitigated, but at ~ 1600 μatm dissolution prevailed. Respiration rates increased with warming, more strongly in orange corals, while acidification slightly suppressed respiration. Calcification and respiration rates as well as polyp mortality were consistently higher in orange corals. Mortality increased considerably at 14–15°C in both colormorphs. Bioerosion/dissolution of dead framework was not affected by warming alone but was significantly enhanced by acidification. While live corals may cope with intermediate levels of elevated pCO2 and temperature, long‐term impacts beyond levels projected for the end of this century will likely lead to skeletal dissolution and increased mortality. Our findings further suggest that acidification causes accelerated degradation of dead framework even at aragonite saturated conditions, which will eventually compromise the structural integrity of cold‐water coral reefs.
... Extremes values are values more than 3 times the IQR. Outliers and extreme values were not removed from the overall data analysis, taking into consideration that coral nubbin standardization for use in the different cones was challenging and that it was uncertain whether outliers were true incorrectly measured data or a true expression of the large intra-and inter-individual response variability that corals nubbins can show (see [34,39]). Also, with relatively few coral nubbin replication (n = 3 to 4 nubbins per cone), removal of outlier values would reduce the number of observations and weaken the statistical validity of the analysis. Prior to analysis, the nested factor "replicate tank" was tested for equal distribution of coral measurement variance across the replicate tanks and, given the few number of coral nubbins in each tank (n = 4 to 6), a nonparametric analysis was used. ...
... This is not uncommon and is challenging to harmonize for experimental work with D. pertusum. In other studies, it has been shown that young polyps grow faster than old ones [39,46]. Hence, the variation observed is most likely explained by the differences in polyp age of the coral nubbins used in the experiments. ...
... from T1 to T2 (ΔT2T1) (Fig 3). These values are very much consistent to previous laboratory measurements for L. pertusa [28,29,32,34,39], field measurements [12] and other CWCs [42]. Compared to the DC experiment, mean skeleton growth rate of control D. pertusum nubbins in the BABE experiment was lower (ΔT1T0: 0.009%± ...
Full-text available
Cold-water coral (CWC) reefs are numerous and widespread along the Norwegian continental shelf where oil and gas industry operate. Uncertainties exist regarding their impacts from operational discharges to drilling. Effect thresholds obtained from near-realistic exposure of suspended particle concentrations for use in coral risk modeling are particularly needed. Here, nubbins of Desmophyllum pertusum ( Lophelia pertusa ) were exposed shortly (5 days, 4h repeated pulses) to suspended particles (bentonite BE; barite BA, and drill cuttings DC) in the range of ~ 4 to ~ 60 mg.l ⁻¹ (actual concentration). Physiological responses (respiration rate, growth rate, mucus-related particulate organic carbon OC and particulate organic nitrogen ON) and polyp mortality were then measured 2 and 6 weeks post-exposure to assess long-term effects. Respiration and growth rates were not significantly different in any of the treatments tested compared to control. OC production was not affected in any treatment, but a significant increase of OC:ON in mucus produced by BE-exposed (23 and 48 mg.l ⁻¹ ) corals was revealed 2 weeks after exposure. Polyp mortality increased significantly at the two highest DC doses (19 and 49 mg.l ⁻¹ ) 2 and 6 weeks post-exposure but no significant difference was observed in any of the other treatments compared to the control. These findings are adding new knowledge on coral resilience to short realistic exposure of suspended drill particles and indicate overall a risk for long-term effects at a threshold of ~20 mg.l ⁻¹ .
... Thus, SEUS data would not capture a lower limit for L. pertusa suitability and a model trained solely on current SEUS climatology would not predict an influence of pH declines in future scenarios, despite the known relevance of pH in this range to the species' distribution and survival (Davies et al., 2008;Georgian, DeLeo, et al., 2016;Hennige et al., 2020;Lunden et al., 2014;Morato et al., 2020). Thus, there may be regional variability in L. pertusa climate-stressor tolerance in the SEUS that was not captured in our models (e.g., Georgian, Dupont, et al., 2016). capability of long-distance dispersal (Strömberg & Larsson, 2017). ...
... Our models generalize the climate response of the species from the whole of North Atlantic to the SEUS. It is possible that because L. pertusa in this region-especially near the shelf break-are already exposed to some of the warmest temperatures recorded for this species, there may be a degree of acclimatization or adaptation as hypothesized in the Gulf of Mexico for acidification (Georgian, Dupont, et al., 2016;Kurman et al., 2017) or for hypoxia on the west Angolan margin (Hebbeln et al., 2020). Although acclimatization for marine calcifiers does not appear to be a viable strategy in shallow waters (Comeau et al., 2019), it may be achieved deeper where climate change proceeds slower. ...
Climate change is reorganizing the planet’s biodiversity, necessitating proactive management of species and habitats based on spatiotemporal predictions of distributions across climate scenarios. In marine settings, climatic changes will predominantly manifest via warming, ocean acidification, deoxygenation, and changes in hydrodynamics. Lophelia pertusa, the main reef‐forming coral present throughout the deep Atlantic Ocean (> 200m), is particularly sensitive to such stressors with stark reductions in suitable habitat predicted to accrue by 2100 in a business‐as‐usual scenario. However, with new occurrence data for this species along with higher‐resolution bathymetry and climate data, it may be possible to locate further climatic refugia. Here, we synthesize new and published biogeographic, geomorphological, and climatic data to build ensemble, multi‐scale habitat suitability models for L. pertusa on the continental margin of the southeast United States (SEUS). We then project these models in two timepoints (2050, 2100) and four climate change scenarios to characterize the occurrence probability of this critical cold‐water coral (CWC) habitat now and in the future. Our models reveal the extent of reef habitat in the SEUS and corroborate it as the largest currently known essentially continuous CWC reef province on earth, and also predict abundance of L. pertusa to identify key areas, including those outside areas currently protected from bottom‐contact fishing. Drastic reductions in L. pertusa climatic suitability index emerged primarily after 2050 and were concentrated at the shallower end (< ~550 m) of the regional distribution under the Gulf Stream main axis. Our results thus suggest a depth‐driven climate refuge effect where deeper, cooler reef sites experience lesser declines. The strength of this effect increases with climate scenario severity. Taken together, our study has implications for the regional and global management of this species, portending changes in the biodiversity reliant on CWC habitats and the critical ecosystem services they provide.
... The physiological response of CWCs to changing temperature, pH and aragonite saturation (Ω arag ) has so far been mainly investigated in laboratory studies under controlled conditions [15][16][17][18][19][20] . However, laboratory studies are usually conducted under constant conditions and do not consider the variability of environmental conditions that corals experience in their natural habitat. ...
... In long-term studies under constant conditions, the effect of elevated temperatures on the performance of different CWC species varies and differs between locations 54 as well as species 53,64 , ranging from a positive effect on calcification to no effect or even a negative response (Table 1). Similar variable results are found for the effect of pH with differences between locations 16 , species 65 as well as short-and long-term exposure 19,52 . Reduced pH either reduces calcification rates of CWCs, has no effect on their calcification or even slightly enhances long-term calcification rates of CWCs 52 (Table 1). ...
Full-text available
The stratified Chilean Comau Fjord sustains a dense population of the cold-water coral (CWC) Desmophyllum dianthus in aragonite supersaturated shallow and aragonite undersaturated deep water. This provides a rare opportunity to evaluate CWC fitness trade-offs in response to physico-chemical drivers and their variability. Here, we combined year-long reciprocal transplantation experiments along natural oceanographic gradients with an in situ assessment of CWC fitness. Following transplantation, corals acclimated fast to the novel environment with no discernible difference between native and novel (i.e. cross-transplanted) corals, demonstrating high phenotypic plasticity. Surprisingly, corals exposed to lowest aragonite saturation (Ωarag < 1) and temperature (T < 12.0 °C), but stable environmental conditions, at the deep station grew fastest and expressed the fittest phenotype. We found an inverse relationship between CWC fitness and environmental variability and propose to consider the high frequency fluctuations of abiotic and biotic factors to better predict the future of CWCs in a changing ocean. The cold-water coral Desmophyllum dianthus benefits from stable environmental conditions in deep waters of Comau Fjord (Chile) and is able to acclimatise quickly to new environmental conditions after transplantation.
... The systems for regulating calcifying fluid pH (pH CF ) within azooxanthellate corals may therefore differ from zooxanthellate corals. Azooxanthellate corals exhibit reduced skeletal density [34], reduced calcification rate [35], and altered rates of respiration and feeding [36] in response to OA, but increased calcification rates under elevated temperature [35,37]. ...
Full-text available
Corals are globally important calcifiers that exhibit complex responses to anthropogenic warming and acidification. Although coral calcification is supported by high seawater pH, photosynthesis by the algal symbionts of zooxanthellate corals can be promoted by elevated pCO2. To investigate the mechanisms underlying corals’ complex responses to global change, three species of tropical zooxanthellate corals (Stylophora pistillata, Pocillopora damicornis, and Seriatopora hystrix) and one species of asymbiotic cold-water coral (Desmophyllum pertusum, syn. Lophelia pertusa) were cultured under a range of ocean acidification and warming scenarios. Under control temperatures, all tropical species exhibited increased calcification rates in response to increasing pCO2. However, the tropical species’ response to increasing pCO2 flattened when they lost symbionts (i.e., bleached) under the high-temperature treatments—suggesting that the loss of symbionts neutralized the benefit of increased pCO2 on calcification rate. Notably, the cold-water species that lacks symbionts exhibited a negative calcification response to increasing pCO2, although this negative response was partially ameliorated under elevated temperature. All four species elevated their calcifying fluid pH relative to seawater pH under all pCO2 treatments, and the magnitude of this offset (Δ[H+]) increased with increasing pCO2. Furthermore, calcifying fluid pH decreased along with symbiont abundance under thermal stress for the one species in which calcifying fluid pH was measured under both temperature treatments. This observation suggests a mechanistic link between photosymbiont loss (‘bleaching’) and impairment of zooxanthellate corals’ ability to elevate calcifying fluid pH in support of calcification under heat stress. This study supports the assertion that thermally induced loss of photosymbionts impairs tropical zooxanthellate corals’ ability to cope with CO2-induced ocean acidification.
... Decreased productivity will affect entire food webs, reducing growth rates and body size (Ruhl et al., 2008), increasing mortality while decreasing abundance (McClain et al., 2012), altering species distributions (Tittensor et al., 2010), lowering species richness and diversity (Corliss et al., 2009), and reducing ecosystem functions and services including carbon cycling (Van Oevelen et al., 2011;Eddy et al., 2021). These changes will also reduce ecosystem resilience as food availability modulates the response of marine organisms to other stressors (Georgian et al., 2016). ...
In 2017, more than 15,000 scientists from 184 countries signed a second warning letter to humanity to caution against our continued wholesale destruction of global ecosystems (Ripple et al., 2017). Here, we reaffirm their message with a similar warning specifically focused on the ocean: humanity must immediately and significantly alter our harmful trajectory in order to avoid irrevocably damaging our oceans in multiple ways that will further affect ocean health for both us and future generations. The ocean is the world's largest realm, housing an astonishing array of biodiversity that provides critical ecological functions that ultimately support life on Earth. In this paper, we outline some of the significant ongoing and imminent activities that degrade ocean health, including destructive fishing practices, oil and natural gas extraction, seabed mining, coastal development, shipping, pollution, and greenhouse-gas emissions. We end by offering potential avenues to mitigate these impacts, including the cessation of particularly harmful activities, restoration of damaged habitats, strong protection of key and representative ecosystems, reduction in waste and emissions, and global policy shifts that prioritize ecosystem health.
Full-text available
Cold-water corals (CWCs) are the engineers of complex ecosystems forming unique biodiversity hotspots in the deep sea. They are expected to suffer dramatically from future environmental changes in the oceans such as ocean warming, food depletion, deoxygenation, and acidification. However, over the last decades of intense deep-sea research, no extinction event of a CWC ecosystem is documented, leaving quite some uncertainty on their sensitivity to these environmental parameters. Paleoceanographic reconstructions offer the opportunity to align the on- and offsets of CWC proliferation to environmental parameters. Here, we present the synthesis of 6 case studies from the North Atlantic Ocean and the Mediterranean Sea, revealing that food supply controlled by export production and turbulent hydrodynamics at the seabed exerted the strongest impact on coral vitality during the past 20,000 years, whereas locally low oxygen concentrations in the bottom water can act as an additional relevant stressor. The fate of CWCs in a changing ocean will largely depend on how these oceanographic processes will be modulated. Future ocean deoxygenation may be compensated regionally where the food delivery and food quality are optimal.
Lophelia pertusa plays an important role as a major contributor to many cold-water coral reefs, supporting a high diversity of associated benthic and benthopelagic species. Due to the high sensitivity of L. pertusa to human activity, it has been classified as indicator species for Vulnerable Marine Ecosystems. However, the global spatial distribution of L. pertusa is far from well known. In this study, a database of L. pertusa presence data was compiled derived from the large number of L. pertusa occurrence records appearing in recent years. In conjunction with data layers covering a range of environmental drivers, habitat suitability for L. pertusa was predicted using the Random Forest approach. Suitable habitat for L. pertusa was predicted to occur primarily on continental margins, with the most suitable habitat likely to occur in the North East Atlantic and South Eastern United States of America. Aragonite saturation state, temperature and salinity were identified as the most important contributors to the habitat suitability model. Given the high vulnerability of reef-forming cold-water corals to anthropogenic impacts, habitat suitability models are critical in developing worldwide conservation and management strategies for biodiverse and biomass rich cold-water coral ecosystems.
Full-text available
The ability of the cold-water coral Lophelia pertusa to exploit different food sources was investigated under standardized conditions in a flume. The tested food sources, dissolved organic matter (DOM, added as dissolved free amino acids), bacteria, algae, and zooplankton (Artemia) were deliberately enriched in 13C and 15N. The incorporation of 13C and 15N was traced into bulk tissue, fatty acids, hydrolysable amino acids, and the skeleton (13C only) of L. pertusa. Incorporation rates of carbon (ranging from 0.8–2.4 μg C g−1 DW d–1) and nitrogen (0.2–0.8 μg N g−1 DW d–1) into coral tissue did not differ significantly among food sources indicating an opportunistic feeding strategy. Although total food assimilation was comparable among sources, subsequent food processing was dependent on the type of food source ingested and recovery of assimilated C in tissue compounds ranged from 17% (algae) to 35% (Artemia). De novo synthesis of individual fatty acids by L. pertusa occurred in all treatments as indicated by the 13C enrichment of individual phospholipid-derived fatty acids (PLFAs) in the coral that were absent in the added food sources. This indicates that the coral might be less dependent on its diet as a source of specific fatty acids than expected, with direct consequences for the interpretation of in situ observations on coral nutrition based on lipid profiles.
Full-text available
The rise of CO2 has been identified as a major threat to life in the ocean. About one-third of the anthropogenic CO2 produced in the last 200 yr has been taken up by the ocean, leading to ocean acidification. Surface seawater pH is projected to decrease by about 0.4 unit between the pre-industrial revolution and 2100. The branching cold-water corals Madrepora oculata and Lophelia pertusa are important, habitat-forming species in the deep Mediterranean Sea. Although previous research has investigated the abundance and distribution of these species, little is known regarding their ecophysiology and potential responses to global environmental change. A previous study indicated that the rate of calcification of these two species remained constant up to 1000 μatm CO2 a value that is at the upper end of changes projected to occur by 2100. We examined whether the ability to maintain calcification rates in the face of rising pCO2 affected the energetic requirements of these corals. Over the course of three months, rates of respiration were measured at a pCO2 ranging between 350 and 1100 μatm to distinguish between short-term response and longer-term acclimation. Respiration rates ranged from 0.074 to 0.266 μmol O2 (g skeletal dry weight)−1 h−1 and 0.095 to 0.725 μmol O2 (g skeletal dry weight)−1 h−1 for L. and M. oculata, respectively, and were independent of pCO2. Respiration increased with time likely due to regular feeding which may have provided an increased energy supply to sustain coral metabolism. Future studies are needed to confirm whether the insensitivity of respiration to increasing pCO2 is a general feature of deep-sea corals in other regions.
Full-text available
To accurately assess the threat that global climate change poses to marine systems, a detailed baseline of the current carbonate chemistry and other oceanographic conditions is required. Despite the heightened vulnerability of deep-sea communities to ocean acidification, there have been relatively few studies investigating the carbonate chemistry immediately above cold-water coral reefs. Here, we present data collected during five cruises from 2010 to 2014 in the northern Gulf of Mexico and quantify the carbonate system and other oceanographic parameters in offshore surface-waters, the water column, and at deep benthic sites. Benthic sites containing the scleractinian cold-water coral L. pertusa occurred in waters with a relatively wide temperature range (6.8-13.6 degrees C), low potential density (sigma(theta)=26.9 +/- 0.3 kg m(-3)), low dissolved oxygen concentration (111.3 +/- 2.0 mu mol kg(-1)), low pH(T) (7.87 +/- 0.04), low Omega(ARAG) (1.31 +/- 0.14), and a low availability of carbonate ions (94.4 +/- 9.2 mu mol kg(-1)) compared with L. pertusa habitats in other regions. Based on previous modelling and experimental results, these values place L. pertusa at the edge of its viable niche in the deep Gulf of Mexico. However, significantly elevated total alkalinity (+139-44 mu mol kg(-1)) was detected above large L. pertusa mounds, suggesting that carbonate dissolution within the mounds may be partially ameliorating the direct effects of ocean acidification. Together, these results provide an important baseline for assessing future oceanographic changes in the Gulf of Mexico and for predicting the resilience of cold-water coral reefs to global climate and ocean change.
La profesion –formacion- docente es un tema crucial en los actuales debates educativos. La existencia de dos decretos y el desplazamiento del verdadero sentido del ser maestro reclaman de los analisis un ejercicio de comprension del orden discursivo oficial. La calidad es el sustrato de la sociedad de control. En este marco se agencia nuevas practicas de subjetivacion del maestro los cuales podriamos situar en la calidad, flexibilidad, adaptabilidad, eficiencia, eficacia. En cualquier caso, el esfuerzo por hacer del maestro un intelectual de la educacion fue borrado. La gran cuestion consiste en saber que discursos regula el saber del docente a la luz de la sociedad de control.
The azooxanthellate scleractinian coral Lophelia pertusa has a near-cosmopolitan distribution, with a main depth distribution between 200 and 1000 m. In the northeast Atlantic it is the main framework-building species, forming deep-sea reefs in the bathyal zone on the continental margin, offshore banks and in Scandinavian fjords. Recent studies have shown that deep-sea reefs are associated with a highly diverse fauna. Such deep-sea communities are subject to increasing impact from deep-water fisheries, against a background of poor knowledge concerning these ecosystems, including the biology and population structure of L. pertusa. To resolve the population structure and to assess the dispersal potential of this deep-sea coral, specific microsatellites markers and ribosomal internal transcribed spacer (ITS) sequences ITS1 and ITS2 were used to investigate 10 different sampling sites, distributed along the European margin and in Scandinavian fjords. Both microsatellite and gene sequence data showed that L. pertusa should not be considered as one panmictic population in the northeast Atlantic but instead forms distinct, offshore and fjord populations. Results also suggest that, if some gene flow is occurring along the continental slope, the recruitment of sexually produced larvae is likely to be strongly local. The microsatellites showed significant levels of inbreeding and revealed that the level of genetic diversity and the contribution of asexual reproduction to the maintenance of the subpopulations were highly variable from site to site. These results are of major importance in the generation of a sustainable management strategy for these diversity-rich deep-sea ecosystems.