Respiration of Mediterranean cold-water corals is not affected byocean acidification as projected for the end of the century
C. Maier1,2, F. Bils1,2,3, M. G. Weinbauer1,2, P. Watremez4, M. A. Peck3, and J.-P. Gattuso1,2
1Laboratoire d’Oceanographie de Villefranche, UMR7093, CNRS-INSU, BP 28, 06234 Villefranche-sur-mer, France2Universite Pierre et Marie Curie-Paris 6, Observatoire Oceanologique de Villefranche, 06230 Villefranche-sur-mer, France3University of Hamburg, Institute for Hydrobiology and Fisheries Science, Olbersweg 24, 22767 Hamburg, Germany4Agence des Aires Marines Protegees, 16 quai de la Douane, 29229 Brest, France
Received: 19 April 2013 – Published in Biogeosciences Discuss.: 2 May 2013Revised: 12 July 2013 – Accepted: 22 July 2013 – Published: 27 August 2013
Abstract. The rise of CO2 has been identified as a majorthreat to life in the ocean. About one-third of the anthro-pogenic CO2 produced in the last 200 yr has been taken upby the ocean, leading to ocean acidification. Surface sea-water pH is projected to decrease by about 0.4 units be-tween the pre-industrial revolution and 2100. The branchingcold-water coralsMadrepora oculataandLophelia pertusaare important, habitat-forming species in the deep Mediter-ranean Sea. Although previous research has investigated theabundance and distribution of these species, little is knownregarding their ecophysiology and potential responses toglobal environmental change. A previous study indicatedthat the rate of calcification of these two species remainedconstant up to 1000 µatm CO2, a value that is at the upperend of changes projected to occur by 2100. We examinedwhether the ability to maintain calcification rates in the faceof rising pCO2 affected the energetic requirements of thesecorals. Over the course of three months, rates of respira-tion were measured at apCO2 ranging between 350 and1100 µatm to distinguish between short-term response andlonger-term acclimation. Respiration rates ranged from 0.074to 0.266 µmol O2 (g skeletal dry weight)−1 h−1 and 0.095 to0.725 µmol O2 (g skeletal dry weight)−1 h−1 for L. pertusaandM. oculata, respectively, and were independent ofpCO2.Respiration increased with time likely due to regular feeding,which may have provided an increased energy supply to sus-tain coral metabolism. Future studies are needed to confirmwhether the insensitivity of respiration to increasingpCO2 isa general feature of deep-sea corals in other regions.
1 Introduction
Cold-water corals form unique, deep-sea habitats contain-ing a high biodiversity of organisms (Roberts et al., 2006).The habitat-forming cold-water coralsLophelia pertusaandMadrepora oculataare found in relatively deep waters attemperatures and salinities between 4 and 12◦C (Roberts etal., 2006) and 31.7 and 38.8 (Davies et al., 2008), respec-tively. Recent work on the distribution and abundance ofthese cold-water corals in the Mediterranean Sea (Taviani etal, 2005b; Freiwald et al., 2009; Orejas et al., 2009) indicatesthat they are found at depths below 200 m, at relatively warm(and stable) temperatures (12.5 to 13.5◦C) and high salinity(38 to 39) (Freiwald et al., 2009; Tursi et al., 2004). Biogeo-graphic considerations indicate that the cold-water corals inthe Mediterranean Sea occur at the warm edge of their rangein thermal tolerance (Davies et al., 2008).M. oculatais moreabundant thanL. pertusain the region, which suggests thatthe former may be better adapted than the latter to warmertemperature and more saline waters (Taviani et al., 2005a). Ageneral decline in the presence of Mediterranean cold-watercorals has been reported during the post-glacial time (Delib-rias and Taviani, 1985), and appears to be more pronouncedfor L. pertusathan forM. oculata.
The oceans play a critical role in mitigating the effect ofincreased production of greenhouse gasses on global climateby removing∼ one-fourth to one-third of anthropogenic CO2from the atmosphere (Khatiwala et al., 2009; Sabine et al.,2004). The downside of this process is that, once dissolvedin seawater, CO2 is a weak acid which reduces seawater
Published by Copernicus Publications on behalf of the European Geosciences Union.
5672 C. Maier et al.: Cold-water coral respiration
pH causing ocean acidification (Caldeira and Wickett, 2003;Gattuso et al., 1999). This process also increases the con-centrations of bicarbonate ions (HCO3−) and dissolved in-organic carbon (CT) and decreases the concentration of car-bonate ions (CO2−
3 ). The saturation state of calcium carbon-ate,�, is a measure of the solubility of carbonate minerals(e.g. calcite (�c) or aragonite (�a)) in seawater (Kleypaset al., 1999; Feely et al., 2004; Cao et al., 2007), and pro-vides a good indicator of whether calcifying organisms canbuild and maintain their exoskeletons (e.g. corals) and shells(e.g. pteropods). Calcium carbonate dissolution is favouredwhen� is below 1, while calcium carbonate precipitation isfavoured when it is above 1. The saturation state decreaseswith increasing pressure (water depth) and decreasing tem-perature; hence,� is lower at higher latitude (colder) anddeeper waters than in lower latitude (warmer) and shallowerwaters (Orr et al., 2005). Calcifying organisms at high lati-tudes and/or deeper depths will be the first to be subjected toseawater favouring carbonate dissolution (� < 1). At the endof the century,�a is projected to be< 1 within > 70 % ofthe present habitat of cold-water corals (Guinotte et al., 2006#2578).
Previous experiments examining the effect of ocean acidi-fication onL. pertusaandM. oculatasuggest that their ratesof calcification remain positive even in waters where�a is< 1 (Maier et al., 2009; Thresher et al., 2011; Form andRiebesell, 2012). Moreover, recent studies (Form and Riebe-sell, 2012; Maier et al., 2012, 2013) reported that calcifica-tion rates of these species remained positive at a partial pres-sure of CO2 (pCO2) of 1000 µatm, a value that is at the highend of projected changes by 2100 (IPPC, 2007). Calcificationis an energy-demanding process (Goreau, 1959; Allemand etal., 2004), and it is likely that the mechanism(s) responsi-ble for these species maintaining positive rates of calcifica-tion at highpCO2 (lower seawater pH) would be reflectedin higher energetic costs. For example, it has been suggestedthat M. oculataandL. pertusaare able to regulate their in-ternal pH over a large gradient ofpCO2 (McCulloch et al.,2012), which likely increases their metabolic requirements.Unfortunately, very little is known regarding the metabolicrate of these species. No metabolic research has been per-formed onM. oculata, and respiration rates have only beenreported in one study on specimens ofL. pertusacollectedfrom the North Atlantic and maintained under variable tem-perature (Dodds et al., 2007). In that study, a dramatic (50 %)increase in respiration rate occurred between 9 and 11◦C(Dodds et al., 2007), temperatures that are several degreescolder than those experienced by cold-water corals in theMediterranean Sea.
In the present study, respiration rates were measured fortwo habitat-forming cold-water coral species,M. oculataandL. pertusa, from the Mediterranean Sea. Respiration rateswere measured for corals maintained for both short andlong periods of time atpCO2 levels ranging from ambient(350 µatm) to elevated (1100 µatm) levels. This study utilized
the same experimental setup as a previous study demonstrat-ing that elevatedpCO2 had no effect on the rate of calcifica-tion in these two species (Maier et al., 2013). Thus, we testthe hypothesis that the ability to maintain positive rates ofcalcification at highpCO2 is accompanied by higher energyrequirements which could be expressed by increased rates ofrespiration.
2 Material and methods
2.1 Sampling of cold-water corals and experimentalsetup
Colonies of the cold-water coralsM. oculata and L. per-tusa were collected during the MedSeaCan cruise inJune 2009 in the Lacaze-Duthiers canyon at water depthsof 260 m (42◦35.07′ N, 03◦24.14′ E), 267 m (42◦34.98′ N,03◦24.15′ E) and 500 m (42◦32.98′ N, 03◦25.21′ E), using aremotely operated vehicle. Corals were transported to thelaboratory and maintained in a temperature-controlled roomuntil the start of the experiments. Branches were carefullysubdivided into smaller fragments and placed into individualmaintenance vials of 4.5 cm inner diameter and a volume ofca. 300 mL (Table 1). Surface water with a salinity of 38 waspumped into two 110 L storage tanks and maintained at 11◦Cin the temperature-controlled room. Water was delivered tomaintenance vials at a flow rate of 32± 14 mL h−1. The vialswere maintained in four water baths and temperature was ad-justed to 13± 0.1◦C using electronic temperature controllers(Corema) coupled with aquarium heaters (Tetratec HT75).Homogeneity of temperature was achieved by water circula-tion pumps (JBL Pro Flow 500, 500 L h−1).
Circulation in the coral maintenance vials was obtainedby airlift with thin silicon tubes connected to a PVC tube(8 cm long and 1.0 cm in diameter), which was submergedinside each of the vials. The air flow was 50 mL min−1 in ev-ery vial. Corals were fed 1 and 3 times a week with frozenkrill and freshly hatchedArtemianauplii, respectively. Afteran acclimation period of 1 month,pCO2 was adjusted us-ing pre-mixed air generated by high-precision mass flow con-trollers (MFCs, ANALYT MC-GFC17, 0–10 L for air and 0–10 mL for pure CO2) and an air compressor (Jun-Air OF302-25B). FourpCO2 treatments were established: A= 280 ppm(low), B= 400 ppm (ambient), C= 700 ppm (elevated) andD = 1000 ppm (above projected) as described in Maier etal. (Maier et al., 2013).
The seawater of the water baths containing the main-tenance vials was also adjusted to the intendedpCO2 bybubbling with an air stone (HOBBY ceramic air diffuser,150 mm in length). Prior to feeding, the seawater of the wa-ter bath was filtered (Tetratec EX 1200, 1200 L h−1). Anyleftover food was removed via siphon to prevent bacterialrespiration and the build-up of nutrients and organic matter.Corals were maintained under these conditions throughout
C. Maier et al.: Cold-water coral respiration 5673
Table 1.Number of samples (N ), number of polyps per coral fragment (N polyps), skeletal dry weight (SDW), and rates of respiration (R)and calcification (G, Maier et al., 2013) of coral fragments ofL. pertusa(LP) andM. oculata(MO). Values ofR andG of periodsT1 to T4were pooled.
pCO2 Coral N N polyps SDW [g] R [µmolg−1h−1] G [µmolg−1h−1]treatment species mean S.D. mean S.D. mean S.D. mean S.D.
A MO 3 26.7 8.4 2.6 1.9 0.193 0.045 0.117 0.043B MO 6 29.3 7.5 2.0 1.6 0.483 0.453 0.166 0.098C MO 3 29.3 10.3 1.8 0.8 0.450 0.365 0.113 0.047D MO 4 29.5 11.3 1.5 1.0 0.577 0.711 0.169 0.080
mean MO 16 28.9 8.3 2.0 1.3 0.446 0.453 0.148 0.076
the 3-month duration of the experiment except during incu-bations aimed at determining rates of respiration (next sec-tion) or calcification (Maier et al., 2013).
2.2 Determination of respiration rates
Two days (T1) after adjusting to differentpCO2 levels andat about monthly intervals for 3 months (T2–T4), rates ofrespiration were measured using the same coral fragments(repeated measures approach). Respiration was determinedusing optodes (Presens OXY-4 mini) equipped with poly-mer optical fibres (Presens, POF) and small sensors (5 mmdiameter) placed inside the respiration vials. The respira-tion vials (8 cm× 5.5 cm height× diameter) with a screwcap were placed on four submersible magnetic stirrers in atemperature-controlled water bath (13◦C± 0.1◦C). A mag-net was placed below a grid on which the corals were placedduring the incubations. Three vials containing coral frag-ments were incubated for 2.5 h, while a separate vial, withno coral, served as blank and contained a temperature sensor(StarOddi, DST centi-T) logging every 30 s with an accuracyof ± 0.1◦C to make sure temperature was constant duringthe 2.5 h duration of incubation. Any oxygen consumptionrate within the blank, due to either minor changes in tem-perature or prokaryotic respiration, was subtracted from thatmeasured in cold-water corals.
Prior to respiration measurements,pCO2 levels were ad-justed in bulk seawater in 10 L containers by aeration withthe four air–CO2 mixtures for 24 h. Respiration rates weredetermined from the depletion in O2 during incubation pe-riod. Oxygen sensors were calibrated with oxygen-free (0 %)and oxygen-saturated (100 %) seawater. Oxygen consump-tion curves (% O2) were established at 30 s intervals overan incubation period of 2.5 h, and respiration rates are givenas µmol O2 (g skeletal dry weight)−1 h−1 (Table 1, Fig. 1). Anincubation period of 2.5 h is relatively short with respect to
the size of coral fragments and volume of seawater used, butwas sufficient to detect changes in oxygen consumption andto avoid hypoxia as shown by the oxygen saturation at the endof measurements, which was always above 88 % and wellabove 90 % for most incubations.
2.3 Carbonate chemistry
Samples for total alkalinity (AT) and dissolved inorganic car-bon (CT) were taken from bulk seawater (125 mL,N = 3 foreachpCO2 treatment) prior to incubation and analysed asdescribed in Maier et al. (2012). Other parameters of the car-bonate chemistry, i.e. the partial pressure of CO2 (pCO2),pH on total scale (pHT), and aragonite saturation state (�a)
were calculated usingAT, CT, a salinity of 38, temperatureof 13◦C and hydrostatic pressure of 0 atm using the soft-ware package seacarb running under R (Lavigne and Gattuso,2011). ThepCO2 cannot be adjusted during incubation. Thecarbonate chemistry therefore changed as function of respi-ration, calcification (Maier et al., 2013) and ammonium ex-cretion (Maier et al., 2009). These changes were estimatedusing a stepwise approach whereAT andCT were calculatedin hourly steps for the entire duration of the 2.5 h incubationfor each coral fragment and repeated measurements of respi-ration rates (T1–T4) using the following equations:
AT(t + 1) = AT(t) − 2× G + 0.875× E, (1)
CT(t + 1) = CT(t) + R − G(2), (2)
with calcification rate (G), respiration rate (R) and ammo-nium excretion rate (E) in µmol kg−1 h−1. The alkalinityanomaly technique was used to determineG (Maier et al.,2013) for each coral fragment and respective time interval(repeated measuresT1–T3). This means that only data ofG
and NH4 from Maier et al. (2013) that were measured in
5674 C. Maier et al.: Cold-water coral respirationFigure 1
A (368 µatm) B (534 µatm) C (883 µatm) D (1215 µatm)
pCO2 treatment
0.00
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A (365 µatm) B (523 µatm) C (874 µatm) D (1158 µatm)
pCO2 treatment
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Fig. 1. Respiration rates of(a) L. pertusa(LP) and (b) M. ocu-lata (MO) for repeated measurements (T1–T4) at fourpCO2 treat-ments (A–D; see Tables 2 and 3). Values forpCO2 treatments A–D(parentheses) are mean at end of incubation (Table 3).
parallel to the respiration rates of this study were taken intoconsideration for calculating the parameters of the carbonatechemistry at end of the incubation.
Calcification decreasesAT by 2× G andCT by 1× G, res-piration increasesCT by 1× R (assuming a respiratory quo-tient of 1) and ammonium increasesAT by (14/16)× NH4(Gattuso et al., 1999).
2.4 Statistical analysis
Statistical analyses were conducted using the software Statis-tica 7.0. Data are given as mean± standard deviation (SD).For the comparison of carbonate chemistry among the fourpCO2 treatments (A–D) of bulk seawater prepared atT1–T4,a one-way ANOVA was conducted followed by a Tukey HSDpost hoc comparison. A repeated measures ANOVA was usedto compare respiration rates at the 4pCO2 levels fromT1 toT4 for each coral fragment.
3 Results and discussion
3.1 Carbonate chemistry
The pCO2 of bulk seawater prior to the incubations dif-fered from thepCO2 levels that were adjusted by aera-tion using pre-mixed air–CO2 for treatment A (280 ppm),B (400 ppm), C (700 ppm) and D (1000 ppm). The seawa-ter pCO2 achieved by aeration was on average 350± 20,497± 28, 826± 69 and 1108± 58 µatm for treatments A–D,respectively (Table 2). Therefore, all values tended to behigher than those of air–CO2 mixtures. These levels covereda large range from slightly below ambient to above the levelprojected for the end of the century (IPPC, 2007). Unsurpris-ingly, AT was not affected by changes inpCO2 (one-wayANOVA, p > 0.69). The other parameters of the carbonatechemistry (CT, pCO2, pHT and�a) were significantly dif-ferent between each of the fourpCO2 treatment levels (one-way ANOVA, p � 0.001 and Tukey HSD post hoc compari-son,p � 0.05 for pairwise comparisons between any pair ofthe fourpCO2 treatments).
Also, the changes for parameters of the carbonate chem-istry that took place during the 2.5 h closed-system incu-bation were estimated as a function of respiration, calcifi-cation and ammonium excretion (for details see “Methods”Sect. 2.3.). During the 2.5 h incubations, there was an aver-age increase ofpCO2 of 6± 2 % (range 3 to 13 %) and anaverage decrease of�a of 5± 1 %. Changes in the other pa-rameters were below 1 % of the initial values (Table 3).
3.2 Respiration rates at differentpCO2 levels and overtime
The 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 at different times of incubationandpCO2 treatments forL. pertusaandM. oculata, respec-tively (Fig. 1). Despite the large range ofpCO2 levels acrossthe four treatments, there was no effect betweenpCO2 treat-ment levels on respiration rates (two-way repeated measuresANOVA, p = 0.767 andp = 0.357 forM. oculataandL. per-tusa, respectively). ForL. pertusa, there was an increase inrespiration fromT1 to T3 and a decrease again atT4 inde-pendent ofpCO2 levels studied and a significant effect oftime of incubation (two-way repeated measures ANOVA, p� 0.001). A similar pattern of increasing respiration fromT1to T3 could be observed forM. oculata, but it was not asconsistent among thepCO2 treatments as that forL. per-tusa. In addition, there was no significant effect betweenrepeated measurementsT1–T4 (two-way repeated measuresANOVA, p = 0.104). To our best knowledge, this is the firstreport of the effect ofpCO2 on respiration on the two cold-water coral speciesL. pertusaand M. oculata. In contrastto our results, a significant decrease in respiration at elevatedpCO2 (D. Piepenburg and M. Bartz, unpublished results) was
C. Maier et al.: Cold-water coral respiration 5675
Table 2. Parameters of the carbonate chemistry at the beginning of the incubations. Total alkalinity (AT) and dissolved inorganic carbon(CT) were measured, while pH on total scale (pHT), partial pressure of CO2 (pCO2) and the aragonite saturation state (�a) were calculated.T is the period at which the incubations were performed (at approximately monthly intervals).T1–4 displays the pooled data forT1 to T4.
T pCO2 N AT CT pHT pCO2 �atreatment [µmol kg−1] [µmol kg−1] [µatm]
mean S.D. mean S.D. mean S.D. mean S.D. mean S.D.
1 A 3 2565 1.5 2297 6.6 8.10 0.01 380 11.0 2.90 0.062 A n/a n/a3 A 3 2548 1.6 2261 3.0 8.14 0.01 342 6.1 3.08 0.044 A 3 2552 7.7 2255 3.2 8.15 0.02 327 14.4 3.18 0.11
mentioned by Form and Riebesell (2012), but no data wereprovided. A decrease in respiration at elevatedpCO2 wouldbe surprising as it would not be in agreement with the hy-pothesis that more energy must be allocated to up-regulateinternal pH and maintain constant calcification.
3.3 Respiration and calcification
To date, calcification is the only parameter investigated withrespect to the effects of ocean acidification on cold-watercorals. It generally appears to be constant over a large rangein pCO2 levels (Thresher et al., 2011; Form and Riebesell,2012; Maier et al., 2012, 2013). It has been proposed thatcold-water corals can up-regulate their internal pH and main-tain a constant rate of calcification even when seawater is un-dersaturated in aragonite (McCulloch et al., 2012). Since theup-regulation of internal pH and maintenance of high calcifi-cation rates is an energy-requiring process mediated throughCa-ATPase (McConnaughey and Whelan, 1997; Allemand etal., 2004; Zoccola et al., 2004), the question arises whetherup-regulation of internal pH at elevatedpCO2 alters the en-ergy balance. For example, more energy would be requiredto up-regulate the internal pH if ambient pH decreased, andit was therefore expected that this would induce a higher
rate of respiration. However, the results presented here re-veal that respiration is independent ofpCO2 level in thecorals tested. The response of calcification of the same coralfragments is similar overpCO2 levels ranging from 380 to930 µatm (Maier et al., 2013). Calcification correlates sig-nificantly with respiration (Fig. 2), indicating a strong cou-pling of calcification and general metabolic performance.The slope of the regression equation between skeletal growth(G) and respiration rates (R) was steeper forL. pertusathanfor M. oculata, which suggests that more energy is allocatedto calcification inL. pertusathan inM. oculata(Fig. 2).
For zooxanthellate corals, it had been proposed that the en-ergy for calcification is derived to a large part from photosyn-thesis (Gattuso et al., 1999; Al-Horani et al., 2003), an energysource that is not available to cold-water corals. Due to thelogistically challenging access to cold-water coral habitats,no quantitative data are available on the food supply and nat-ural feeding regime of cold-water corals. It is therefore dif-ficult to mimic the in situ feeding during experiments. Dur-ing the experiments lasting several months, sufficient foodwas provided in order to avoid starvation, which might im-pede respiration or calcification as shown in a previous study(Naumann et al., 2011). Abundant food supply was shown
5676 C. Maier et al.: Cold-water coral respiration
Table 3.Estimated parameters of the carbonate chemistry at the end of the incubations of coral fragments ofL. pertusa(LP) andM. oculata(MO). Mean valuesAT 2.5 h andCT 2.5 h were used to calculate the other parameters of carbonate chemistry (pHT 2.5 h, pCO22.5 h and�a2.5 h). The difference between the end and the beginning of the incubations is also shown (1). T is the period at which the incubationswere performed (at ca. monthly intervals).T1−4 displays the pooled data forT1 to T4.
T pCO2 Coral N AT2.5 h CT2.5 h pHT2.5 h pCO22.5 h �a2.5 htreatment [µmolkg−1] [µmolkg−1] [µatm]
C. Maier et al.: Cold-water coral respiration 5677
Figure 2
Fig. 2. Rate of calcification (G, from Maier et al., 2013) asa function of respiration rate (R) for L. pertusa (LP) andM. oculata (MO). The equations of the regression lines areGLP = 0.0217+ 0.3091× R;(r = 0.4182;p = 0.0004;n = 68),and GMO = 0.1009+ 0.1051× R;(r = 0.4877;p = 0.00004;n = 64).
to counterbalance a negative response of invertebrates to el-evatedpCO2 both in the laboratory and in the field (e.g.Thomsen et al., 2013). However, it was not an issue in thepresent experiment as the continuous flow of water exponen-tially diluted the prey concentration. With a dilution factor of10.7 % h−1 (flow rate of 32 mL h−1 and a maintenance vol-ume of 300 mL), the corals received an initial pulse of foodwhich decreases by 93.3 % d−1. This means that after oneday, only 6.7 % of prey is left, and after a further two or threedays, before vials were cleaned and new food was provided,prey is reduced to 0.44 % and 0.03 % of the initial prey con-centration, respectively. It is unclear, what caused the syn-chronous increase of calcification and respiration during the2–3-month-long experiment at differentpCO2 levels (thisstudy and Maier et al., 2013). One likely explanation is thatthe regular feeding triggered an increase in coral metabolism(calcification and respiration). Whatever the cause of this in-crease is, it was observed in allpCO2 treatments and resultedin large changes in the rates of respiration and calcificationover time. The possibility that an effect ofpCO2 was maskeddue to an unrealistic feeding regime due to either starvationor overfeeding can be excluded.
3.4 Energy requirements and temperature
A study of the cold-water coralDesmophyllum di-anthus, revealed that both respiration and calcificationrates were lower in starved than fed colonies (Naumannet al., 2011). Also, feeding increases both the skele-tal and tissue growth in zooxanthellate corals (Ferrier-Pages et al., 2003; Houlbreque et al., 2003; Rodolfo-Metalpa et al., 2008). Mean respiration rates pooled for
pCO2 treatment levels and repeated measurements (T1–T4)
were 0.16± 0.08 µmol O2 (g skeletal dry weight)−1 h−1 and0.45± 0.45 µmol O2 (g skeletal dry weight)−1 h−1 for L. per-tusa and M. oculata, respectively (Table 1). So far, onlyone study (from Mingulay Reef, northeast Atlantic) hasreported the respiration rates forL. pertusa (Dodds etal., 2007) and respiration rates ofM. oculata have, toour best knowledge, never been measured. ForL. pertusa,Dodds et al. (2007) reported respiration rates of speci-mens from the NE Atlantic at ambient temperature thatwere higher than those measured here in individuals col-lected from the Mediterranean Sea (0.23 vs. 0.16 µmol O2(g skeletal dry weight)−1 h−1, Table 1). This is surprisingsince Mediterranean cold-water corals live in habitats thatare, on average, 4◦C warmer than temperatures reportedat the Mingulay collection site (13 vs. 9◦C). Furthermore,Dodds et al. (2007) showed that respiration increased by50 % (0.23 to 0.33 µmol (g skeletal dry weight)−1 h−1) withan increase of 2◦C (from 9 to 11◦C) suggesting that res-piration rates for Mediterranean cold-water corals subjectedto 13◦C would be expected to be well above those foundfor North Atlantic specimens. The temperature coefficientof respiration (Q10) of MediterraneanL. pertusais lowerthan that of North AtlanticL. pertusa(on average 4.0 and7.2, respectively, SI 1 and Dodds et al., 2007). A lowerQ10might be indicative of acclimation (Barnes, 2001), and thelower Q10 for a temperature of up to 16.7◦C could meanthat cold-water corals, due to their adaptation to the higherMediterranean temperature, might be less sensitive to tem-perature changes than their North Atlantic congeners. Nau-mann et al. (2013) reported a high thermal tolerance of calci-fication in two Mediterranean deep-sea corals. Compared toan ambient temperature of about 12◦C, at 17.5◦C, calcifica-tion increased inDendrophyllia cornigeraand was similar inDesmophyllum dianthus.
This is the first study to measure the respiration rates ofM. oculata and, consequently, no data for comparison areavailable. Due to the lack of data from other regions andtemperature ranges, it remains unknown whetherM. ocu-lata is better adapted to the relatively warm temperatures ex-perienced in Mediterranean Sea deep-water habitats. How-ever, respiration not only depends on temperature but alsoon other parameters, e.g. salinity (Ferrier-Pages et al., 1999),food availability (Naumann et al., 2011) and intrinsic fac-tors regulating metabolism (Hochachka and Somero, 2002).M. oculata is more commonly found in the Mediterraneanthan L. pertusa(Freiwald et al., 2009; Gori et al., 2013),which suggests that it is better adapted to environmental fac-tors prevailing in that region. Respiration rate normalized bythe skeletal dry weight was 2.7 times higher inM. oculatathan inL. pertusa,and with higher respiration, more energywould be required to sustain coral metabolism. However, res-piration is a surface-dependent process (Barnes, 2001), andskeletal weight might thus not be a good biomass estimator tonormalize metabolic processes. Surface area, tissue biomass
5678 C. Maier et al.: Cold-water coral respiration
or number of polyp are likely more suitable units to relatemetabolic processes or prey capture. The ratio of skeletalarea versus polyp number is approximately 3 times higherin L. pertusathan inM. oculata(373 vs. 126 mm2 polyp−1)
(Maier et al., 2011). Using this ratio and the ratio of polypnumber to skeletal weight (Table 1) reveals that respirationnormalized to surface is similar inL. pertusaandM. oculata(0.022 and 0.024 µmol O2 cm−2 h−1, respectively).
Since the food uptake plays a significant role for both res-piration and calcification (Naumann et al., 2011), the similarrespiration rate for the two species does not allow for anyconclusion to be drawn as to whether both species would besimilarly well acclimatized to high Mediterranean tempera-tures.L. pertusahas bigger, but less numerous, polyps thanM. oculata, which might indicate that the efficiency of preycapture differs in the two species, depending on the amountand size of food available. Food capture rates were not mea-sured in the present study, but Tsounis et al. (2010) reportedtotal carbon uptake rates of 3731 and 1072 µg C polyp−1 h−1,respectively, inL. pertusaandM. oculatafrom the Mediter-ranean Sea (Tsounis et al., 2010). This translates to a carbonuptake of 83.4 µmol C cm−2 h−1 and 70.9 µmol C cm−2 h−1
(Maier et al., 2011, and Table 1). Therefore, both specieshave a similar prey capture efficiency despite the differenceof polyp size, which is possibly compensated by the highernumber of polyps per unit surface area or skeletal weight inM. oculata. It can therefore be inferred that the two speciesingested a similar amount of C in our experiment. It shouldbe pointed out that calcification rates normalized to sur-face area were also similar in the two species (0.010 and0.008 µmol CaCO3 cm−2 h−1 for L. pertusaandM. oculata,respectively, Maier et al., 2013). There is relative uniformityof the two species with the overall lack of response topCO2,as well as the similar rates of carbon uptake, respiration, cal-cification and the reported increase over time of respirationrates independent ofpCO2. This could indicate thatM. oc-ulata and L. pertusawill exhibit a similar response to fu-ture global environmental change. However, more studies areneeded to confirm this hypothesis.
3.5 Perspective on the response of cold-water corals toglobal environmental change
In the range ofpCO2 studied so far, up to 1215 µatm, nosignificant change in respiration was found as a functionof increasingpCO2. However, to better predict future re-sponses of organisms to global change, it is critical to iden-tify potential interactive effects between ocean acidificationand other parameters such as temperature and food availabil-ity. Considering all published information, a potential tippingpoint for calcification of the two cold-water species would beabove apCO2 of 1000 µatm and at an�a below 1 (Maier etal., 2009, 2012, 2013; Thresher et al., 2011; Form and Riebe-sell, 2012; McCulloch et al., 2012, #3512), and the samemight be true for the respiration response as indicated in the
present study. For calcification rates ofL. pertusa, there isindirect evidence from short-term closed system incubations(Maier et al., 2009) that this tipping point would be wellabove 1000 ppm and at an�a below 0.9 (Table 3, Maier etal., 2009).
This study provides the first evidence that respiration ratesof cold-water corals are not affected by elevatedpCO2 andthat the ability of our two target species to maintain ratesof calcification at highpCO2 was not via compensatory re-sponses in metabolic losses. This means that for the mainte-nance of high calcification rates over a large range ofpCO2of up to 1000 ppm, there is no evidence for a direct energyallocation from food uptake to calcification in order to com-pensate for higher energy required to maintain calcificationconstant despite a decrease in pH. However, it is possiblethat as-yet-unidentified changes in metabolic pathways en-able a more efficient supply of necessary energy for pH up-regulation to maintain constant calcification rates at increas-ing pCO2. It is also possible that cold-water corals use lipidreserves, which would be reflected in a lower respiratory quo-tient. However, this would mean that respiration would not besustainable over a longer timescale, as lipid reserves wouldget exhausted and would not be replenished due to the higherenergy allocated to calcification. Therefore, future studies areneeded to investigate in more detail the mechanisms that al-low for cold-water corals to cope with highpCO2 levels. Forzooxanthellate corals, molecular techniques looking at geneexpression revealed that ocean acidification strongly sup-presses metabolism and enhanced extracellular organic ma-trix synthesis and had complex effects on genes involved incalcification (Moya et al., 2012; Kaniewska et al., 2012). Theresponse of other parameters important for coral functioning,e.g. reproduction and resilience to other environmental stres-sors (food reduction, temperature rise, predation, etc.) alsoneeds attention in order to better predict whether and howcold-water corals will be able to cope with global environ-mental changes.
Supplementary material related to this article isavailable online at:http://www.biogeosciences.net/10/5671/2013/bg-10-5671-2013-supplement.pdf.
Acknowledgements.We would like to thank the captain, crew andscientific shipboard staff of RVMinibex(COMEX). Cruises on RVMinibex were part of a project on canyons of the MediterraneanSea (MedSeaCan) lead by the French Marine Protected AreasAgency (AAMP), France. Our thanks go to A. Schubert for helpwith the experiments. Financial support was provided by theEuropean Commission through a Marie Curie Fellowship to CM(MECCA, project no 220299) and the project COMP via thePrince Albert II of Monaco Foundation. FB acknowledges supportfrom the German Academic Exchange Service (DAAD). This work
C. Maier et al.: Cold-water coral respiration 5679
is a contribution to the “European Project on Ocean Acidification”(EPOCA) which received funding from the European Community’sSeventh Framework Programme (FP7/2007-2013) under grantagreement no. 211384.
Edited by: G. Herndl
The publication of this articleis financed by CNRS-INSU.
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