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Geochimica et Cosmochimica Acta 75 (2011) 4273–4285

Seawater temperature proxies based on DSr, DMg, and DU

from culture experiments using the branching coralPorites cylindrica

Alrum Armid a,c,⇑, Ryuji Asami b, Tanri Fahmiati c, Mohammed Ali Sheikh d,Hiroyuki Fujimura d, Tomihiko Higuchi d, Eiko Taira e,

Ryuichi Shinjo f, Tamotsu Oomori d,⇑

a Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japanb Trans-disciplinary Research Organization for Subtropical Island Studies (TRO-SIS), University of the Ryukyus, 1 Senbaru,

Nishihara, Okinawa 903-0213, Japanc Department of Chemistry, Faculty of Science, University of Haluoleo, Anduonohu, Kendari 93-232, Indonesia

d Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa

903-0213, Japane Aqua Culture Okinawa Co., Urasoe, Okinawa 901-2131, Japan

f Department of Physics and Earth Sciences, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan

Received 22 February 2011; accepted in revised form 5 May 2011; available online 18 May 2011

Abstract

In order to investigate the incorporation of Sr, Mg, and U into coral skeletons and its temperature dependency, we per-formed a culture experiment in which specimens of the branching coral (Porites cylindrica) were grown for 1 month at threeseawater temperatures (22, 26, and 30 �C). The results of this study showed that the linear extension rate of P. cylindrica haslittle effect on the skeletal Sr/Ca, Mg/Ca, and U/Ca ratios. The following temperature equations were derived: Sr/Ca (mmol/mol) = 10.214(±0.229) � 0.0642(±0.00897) � T (�C) (r2 = 0.59, p < 0.05); Mg/Ca (mmol/mol) = 1.973(±0.302) + 0.1002(±0.0118) � T (�C) (r2 = 0.67, p < 0.05); and U/Ca (lmol/mol) = 1.488(±0.0484) � 0.0212(±0.00189) � T (�C) (r2 = 0.78,p < 0.05). We calculated the distribution coefficient (D) of Sr, Mg, and U relative to seawater temperature and comparedthe results with previous data from massive Porites corals. The seawater temperature proxies based on D calibrations ofP. cylindrica established in this study are generally similar to those for massive Porites corals, despite a difference in the slopeof DU calibration. The calibration sensitivity of DSr, DMg, and DU to seawater temperature change during the experiment was0.64%/�C, 1.93%/�C, and 1.97%/�C, respectively. These results suggest that the skeletal Sr/Ca ratio (and possibly the Mg/Caand/or U/Ca ratio) of the branching coral P. cylindrica can be used as a potential paleothermometer.� 2011 Elsevier Ltd. All rights reserved.

0016-7037/$ - see front matter � 2011 Elsevier Ltd. All rights reserved.

doi:10.1016/j.gca.2011.05.010

⇑ Corresponding authors. Address: Graduate School of Engi-neering and Science, University of the Ryukyus, 1 Senbaru,Nishihara, Okinawa 903-0213, Japan. Tel.: +81 98 895 8099; fax:+81 98 895 8552 (A. Armid), tel.: +81 98 895 8100; fax: +81 98 8958565 (T. Oomori).

E-mail addresses: armid04@yahoo.com (A. Armid), oomori@sci.u-ryukyu.ac.jp (T. Oomori).

1. INTRODUCTION

The presence of trace and minor elements in marine car-bonates provides important historic and current data withregard to seawater chemistry, such as climate changes(Lea et al., 2000), distribution of oceanic nutrients (Leaet al., 1989), anthropogenic metal pollution (Ramos et al.,2004; Chen et al., 2010), and composition of seawater(Adkins et al., 1998). Scleractinian corals are of particular

4274 A. Armid et al. / Geochimica et Cosmochimica Acta 75 (2011) 4273–4285

usefulness because of their annual density banding, whichcan be used for dating. Within this chronology, geochemi-cal proxies of seawater temperature can be measured.

Numerous studies on scleractinian corals, especially mas-sive Porites corals, have been conducted to establish potentialtracers (Sr/Ca, Mg/Ca, and U/Ca ratios) of sea surfacetemperature (SST) (e.g., Beck et al., 1992; Min et al., 1995;Alibert and McCulloch, 1997; Gagan et al., 1998; Weiet al., 2000; Quinn and Sampson, 2002; Fallon et al., 2003).The Sr/Ca ratio of modern and fossil aragonitic coral skele-ton is widely used to reconstruct SST variability (e.g., Weber,1973; Smith et al., 1979; Beck et al., 1992; Shen et al., 1996;Gagan et al., 1998; Linsley et al., 2000, 2006, 2008; Weiet al., 2000; Hendy et al., 2002; Swart et al., 2002; Fallonet al., 2003; Felis et al., 2004; Correge, 2006; Calvo et al.,2007; DeLong et al., 2007; Asami et al., 2009). Other poten-tial paleothermometers have been proposed in corals, includ-ing the Mg/Ca ratio (e.g., Swart, 1981; Oomori et al., 1982;Mitsuguchi et al., 1996; Wei et al., 2000) and the U/Ca ratio(e.g., Min et al., 1995; Shen and Dunbar, 1995; Sinclair et al.,1998; Fallon et al., 1999, 2003; Correge et al., 2000; Wei et al.,2000; Felis et al., 2009).

It should be noted that most previously published pale-othermometers were derived from massive Porites corals.Thus, it is important to evaluate the usefulness of other coralspecies (such as branching Porites corals) as proxies; combin-ing these data with records from massive corals could providemore detailed paleoenvironmental reconstructions with hightemporal and spatial resolution. Recently, some investiga-tions suggested that the Mg/Ca ratio of coral significantly re-flects seawater temperature, as well as skeletal growth effects(Inoue et al., 2007; Reynaud et al., 2007). In order to examinesuch effects, data are needed from culture experiments on cor-al species having variable growth rates.

With these objectives in mind, we conducted a laboratoryculture experiment using the branching coral Porites cylindri-

ca to examine the incorporation of Sr, Mg, and U into theskeletons at three temperatures (22, 26, and 30 �C); subse-quently, we evaluated the reliability of Sr/Ca, Mg/Ca, andU/Ca ratios as potential seawater temperature proxies. Thepresent study is the first report on temperature calibrationusing the coral species P. cylindrica. The advantage of usingP. cylindrica corals is that they have a faster growth rate (upto �3 cm/year; Custodio and Yap, 1997) compared withmassive Porites corals (up to 1–2 cm/year; Lough andBarnes, 2000). P. cylindrica is a branching stony coral widelydistributed in the tropical-to-subtropical Indian and PacificOceans, and it is very common in shallow water near the coast(Veron, 2000). Hence, the results of this study will providevaluable new data for reconstructing past SST variability,which will contribute to the advancement of paleoceanogra-phy and paleoclimatology.

Fig. 1. The culture setup (continuous flow system).

2. MATERIALS AND METHODS

2.1. Materials and experimental setting

A single colony of the scleractinian branching coralP. cylindrica was collected from the coral reef (1 m depth;average SST �26.8 �C) off the Makiminato coast,

Okinawa-Jima, on 9 November 2008; it was kept for severalmonths under controlled conditions at Aqua CultureOkinawa Co., Japan (ACOJ). Thirteen living fragments,typically �5 cm in length, were separated from the parentcolony, by cutting terminally positioned branches (i.e., eachfragment consisted of one branch), and glued onto ceramicbases. Before initiating the experiment, they were acclima-tized for 7 days in well seawater at 27 �C (i.e., main reser-voir tank of ACOJ) to ensure their survival. At day 7, allfragments were stained for �12 h, using 10 ppm of alizarinred S (ARS) (Lamberts, 1978), to facilitate the identifica-tion of skeletal growth at the conclusion of the experiment.Then, they were transferred into the tanks used for theculture experiment (i.e., four, five, and four fragments inthe 22, 26, and 30 �C experimental tanks, respectively).Coastal well seawater, which was taken from 20 m depthoff the southwestern coast of Okinawa-Jima (26�160N,127�430E), was used as culture solution. Well seawater hasthe same density as natural seawater and an extremely smallamount of microorganisms (Imada et al., 2006). Its useprovides ideal and stable chemical conditions; note thattyphoons occur several times per year, which can causesignificant modifications in seawater chemistry. Theexperiment was conducted from 19 September to 19 October2009. Because of the relatively fast growth rate ofP. cylindrica (Custodio and Yap, 1997), a 1-month experi-ment was sufficient. The experimental tank is shown in Fig. 1.

Seawater temperature in the three experimental tankswas controlled at a constant of 22, 26, or 30 �C by a cooler(GXC-201x, GEX, China) equipped with a heater (Com-pact slim 300, GEX, China). During the experiment, wemanually checked the tank temperatures nearly every dayusing a thermometer (IR100, EXTECH Instruments,USA). The temperatures from the three tanks were22.0 ± 0.1, 26.0 ± 0.1, and 30.1 ± 0.1 �C (n = 24). Eachtank (32 L in volume) was continuously supplied by wellseawater pumped from a reservoir bucket (�90 L in vol-ume), with a circulation rate of �1.8 L/min (Fig. 1). In or-der to maintain a consistent seawater quality during theexperiment, half of the well seawater from each reservoirbucket was changed every 2 days. Light was provided byportable fluorescence lamps (Pixy Neo 24W, KOTOBUKI,Japan), which supplied a light intensity of 300 lmol pho-tons m�2 s�1 and was adjusted to a 12-h light/dark cycle.

Seawater samples for chemical analyses were taken fromeach tank every day for the first 3 days and then once aweek throughout the duration of the experiment. All coral

Fig. 2. A typical slab of the coral P. cylindrica after a 30-dayculture experiment (slab of sub-sample T26-P2.2 in Table B1).Linear extension rate was calculated after the conclusion of theexperiment by measuring the distance from the ARS line (reddishcolor) to the top of the slab. Arrow indicates the axial direction ofcoral extension. (For interpretation of the references to color in thisfigure legend, the reader is referred to the web version of thisarticle.)

Seawater temperature proxies from coral Porites cylindrica 4275

fragments appeared to grow normally during the 1-monthculture period. Coral fragments were collected at the endof the experiment and frozen in individual plastic bags untilelemental analyses were conducted.

2.2. Seawater samples

Approximately 250 ml was filtered using a Millipore HAfilter (0.45 lm pore size); it was subsequently divided into50-ml aliquots for alkalinity and salinity measurements,which were completed within 3 h of sampling. The remain-ing samples were preserved by adding concentrated HCl (topH = 2) and stored for subsequent analyses of Ca, Sr, Mg,and U.

The pH of well seawater was measured using a pH meter(Orion 290APlus, Thermo Fisher Sci. K.K., Japan). Foreach set of measurements, the pH meter was calibratedusing NBS-scaled buffer solutions (TOA, Golden buffer)at pH = 6.863 and 4.006 at 25 �C. The reproducibility ofthe measurements was ±0.001 pH unit (n = 11; 1r). Totalalkalinity was measured potentiometrically using an auto-titration system (TIM 860 Radiometer, TitraLab, France),the reproducibility of which was ±3 lmol/kg (n = 9; 1r).Salinity was measured using a salinometer (Model 8410APORTASALe, Canada) after calibrating it with Interna-tional Association for the Physical Sciences of the Oceanstandard seawater (K15 = 0.99987, S = 34.995). The repro-ducibility of the measurements was ±0.001 (n = 11; 1r).

The Ca concentration was determined by the ethyleneglycol tetraacetic acid titration method (Kanamori andIkegami, 1980) using an auto-titration system (TIM 865Radiometer, TitraLab, France) equipped with a Ca-selec-tive electrode (ISE-25, TitraLab). The equivalence pointfor each titration was obtained by Gran’s plot method(Gran, 1952). The reproducibility of the measurements of400 ppm Ca was ±0.4 ppm (n = 11; 1r). Sr and Mg concen-trations were determined using an inductively coupled plas-ma atomic emission spectroscopy (ICP-AES) (ICPE-9000,SHIMADZU Co., Japan). The reproducibility of the mea-surements of 5 ppm Sr and 1000 ppm Mg was ±0.02 ppm(n = 3; 1r) and ±7.2 ppm (n = 3; 1r), respectively. Forthe determination of U concentration, 15 ml of well seawa-ter was mixed with 30 ml of concentrated HCl and thenpassed through a Cl-form anion exchange resin (Dowex1X8, 100–200 mesh) column to separate U from matrix ele-ments. After washing with 8 N HCl, the sample was elutedby 25 ml of 0.1 N HCl (�98% of U was recovered), and theU concentration was analyzed using an inductively coupledplasma mass spectrometry (ICP-MS) (Agilent 4500,Yokogawa Analytical Systems, Japan) with an Ar–H2 gascarrier for U quantification. The reproducibility of themeasurements of 2 ppb U was ±0.02 ppb (n = 3; 1r).

2.3. Coral skeleton treatment and elemental analyses

Thirteen coral fragments were cut along the skeletalgrowth axis using a diamond saw, providing several slabs.The number of slabs varied because of the dissimilar sizeof the coral fragments; we obtained 12, 18, and 7 slabsfor the 22, 26, and 30 �C tanks, respectively. The slabs were

cleaned ultrasonically with ultra-pure (Milli-Q) water(>18.2 MX), prepared with a Millipore Milli-Q water-puri-fication system, and dried at room temperature. The 1-month growth portion of the aragonitic skeleton in eachslab, corresponding to the portion between the ARS lineand the top of the slab (Fig. 2), was divided into severalskeletal chips (called “subsample” hereafter) parallel tothe growth direction using a dental diamond drill. In orderto remove organic material, approximately 10 mg of arago-nite powder from each subsample was reacted with 2 ml of35% H2O2 and heated at 60 �C for �2 h. The H2O2 was dec-anted, and the powder was rinsed three times with 3 ml ofMilli-Q water and centrifuged. After eliminating the Milli-Q water and drying the powder, �5 mg of powder was dis-solved in 8.4 ml of 6 N HNO3; subsequently, 1 N HNO3

was added to attain 50 ml volume, providing a final solu-tion for elemental analyses.

U concentrations were measured by an Agilent 7500ceICP-MS. Minor quantities of He were added to improvethe performance of the Ar gas carrier. The reproducibilityof the measurements of 0.5 ppb U was ±0.001 ppb (n = 3;1r), with an analytical precision of �0.2% (RSD). Thedeterminations of Mg, Sr, and Ca were performed on anICP-AES (Vista Pro, Seiko Instrument, Japan). The repro-ducibility of the measurements for 40 ppm Ca, 1 ppm Sr,and 0.1 ppm Mg (n = 3; 1r) was ±0.1, ±0.01, and±0.005 ppm, respectively, corresponding to an analyticalprecision of �0.25%, 1.0%, and 5.0% (RSD), respectively.The analytical precisions (2r) for Sr/Ca, Mg/Ca andU/Ca ratios were estimated to be 0.2, 0.4 mmol/mol, and0.02 lmol/mol, respectively. In order to correct matrixeffects and instrumental drift, thallium (Tl) and yttrium(Y) were added to all solutions as internal standards.Despite the use of different devices for U and Ca analyses,

pb

)S

r/C

a(m

mo

l/m

ol)

Mg/

Ca

(mo

l/m

ol)

U/C

a(l

mo

l/m

ol)

8.42

4.76

1.08

±0.

148.

45±

0.41

4.75

±0.

061.

08±

0.05

±0.

188.

36±

0.25

4.77

±0.

101.

07±

0.08

±0.

138.

37±

0.09

4.77

±0.

131.

07±

0.05

4276 A. Armid et al. / Geochimica et Cosmochimica Acta 75 (2011) 4273–4285

the calibration using the two internal standards allows foreffective reduction of systematic error incorporated intothe calculated U/Ca ratios.

3. RESULTS

3.1. Well seawater composition

The average seawater composition during the cultureexperiment is shown in Table 1, and the data are listed inTable A1 (Appendix A). The composition of the initial wellseawater (i.e., the original well seawater from the main reser-voir tank of ACOJ) was also measured (Table 1) for compar-ison with those of the experimental treatments. The wellseawater composition during the experiment showed no sig-nificant differences among the three tanks (p < 0.05), with theexception of Ca and Mg concentrations. Despite the varia-tion within each temperature treatment for the two elements,it is important to point out that the element/Ca ratios (i.e.,Sr/Ca, Mg/Ca, and U/Ca) were statistically equivalentduring the experiment (p < 0.05).

Tab

le1

Wel

lse

awat

erco

mp

osi

tio

nd

uri

ng

the

exp

erim

ent.

Tan

kn

pH

Sal

init

yA

lkal

init

y(l

mo

l/k

g)C

a(p

pm

)S

r(p

pm

)M

g(p

pm

)U

(p

Init

ial

18.

1632

.61

2607

401

7.39

1157

2.57

I(2

2�C

)8

8.15

±0.

0632

.47

±0.

4226

01±

6239

5±

77.

30±

0.23

1139

±14

2.55

II(2

6�C

)8

8.17

±0.

1032

.57

±0.

5425

97±

5739

9±

67.

29±

0.12

1153

±10

2.53

III

(30

�C)

88.

20±

0.07

32.6

6±

0.24

2614

±54

402

±5

7.36

±0.

0711

63±

252.

56

nd

eno

tes

nu

mb

ero

fd

ays

that

we

coll

ecte

dth

ese

awat

ersa

mp

les.

Err

ors

rep

rese

nt

stan

dar

dd

evia

tio

ns

(2r

).

3.2. Skeletal Sr/Ca, Mg/Ca, and U/Ca ratios

Fig. 3 shows the relationship between the skeletalelement/Ca ratios of P. cylindrica and temperature treat-ments (data are provided in Table B1, Appendix B). TheSr/Ca ratio of P. cylindrica correlated negatively with wellseawater temperatures, yielding a linear equation, withr2 = 0.59 (p < 0.05): Sr/Ca (mmol/mol) = 10.214 (±0.229)� 0.0642(±0.00897) � T (�C) (Fig. 3a). A negative correla-tion was also found between the skeletal U/Ca ratio andseawater temperature (Fig. 3c), which can be expressedas: U/Ca (lmol/mol) = 1.488 (±0.0484) � 0.0212(±0.00189) � T (�C) (r2 = 0.78, p < 0.05). In contrast, theMg/Ca ratio had a positive correlation with seawatertemperature: Mg/Ca (mmol/mol) = 1.973(±0.302) +0.1002(±0.0118) � T (�C) (r2 = 0.67, p < 0.05) (Fig. 3b).

Because each coral fragment was originally taken fromthe same colony, the fragments in each tank might havehad similar behavior upon uptaking elements during theexperiment. As such, we grouped all subsamples from eachtank; the measurements are presented as mean values(Table 2). The mean data indicated that the Sr/Ca ratiodecreased 5.9% when the seawater temperature changedfrom 22 to 30 �C, with a linear equation of Sr/Ca (mmol/mol) = 10.22 � 0.064 � T (�C) (r2 = 0.99). The U/Ca ratiodecreased 16.5% with an increase in seawater temperaturefrom 22 to 30 �C, expressed as: U/Ca (lmol/mol) =1.474 � 0.020 � T (�C) (r2 = 0.98). A positive correlationbetween mean Mg/Ca ratio and seawater temperatureproduced the equation: Mg/Ca (mmol/mol) = 2.185 +0.090 � T (�C) (r2 = 0.80). This value increased by 17.7%when the seawater temperature increased from 22 to 30 �C.It is notable that the linear equations derived from the meanSr/Ca and U/Ca ratios are similar to those calculated fromthe individual Sr/Ca and U/Ca ratios. However, for theMg/Ca ratio, the intercept of the equation using averaged ra-tios (2.185) was slightly greater than the calculations madeusing individual data (1.973), suggesting a significant

Fig. 3. Relationship between P. cylindrica element/Ca ratiosand seawater temperature. Black lines represent regression linescalculated with all data; red lines are from the data without outliers(i.e., red circles, see Table B1). (a) Sr/Ca ratio versus seawatertemperature: black solid line is Sr/Ca = 10.214(±0.229) � 0.0642(±0.00897) � T (r2 = 0.59), red solid line is Sr/Ca = 10.089(±0.225) � 0.0589(±0.00882) � T (r2 = 0.57). (b) Mg/Ca ratioversus seawater temperature: black solid line is Mg/Ca = 1.973(±0.302) + 0.1002(±0.0118) � T (r2 = 0.67), red solid line is Mg/Ca = 1.984(±0.270) + 0.0991(±0.0106) � T (r2 = 0.72). (c) U/Caratio versus seawater temperature: U/Ca = 1.488(±0.0484) �0.0212(±0.00189) � T (r2 = 0.78) (black line) and U/Ca = 1.470(±0.049) � 0.0204(±0.00193) � T (r2 = 0.77) (red line). Dashedlines represent 95% confidence intervals. (For interpretation of thereferences to color in this figure legend, the reader is referred to theweb version of this article.)

Seawater temperature proxies from coral Porites cylindrica 4277

fluctuation in the skeletal Mg/Ca ratios within eachtemperature treatment (Table B1).

Table 2Average skeletal extension and element/Ca ratios of P. cylindrica.

Tank Subsamples (n) Linear extension rate (mm/30-day)

I (22 �C) 12 2.25 ± 0.79II (26 �C) 18 3.30 ± 1.03III (30 �C) 7 1.88 ± 0.72

Errors represent standard deviations (2r).

4. DISCUSSION

4.1. Fluctuation of element/Ca ratios and linear extension

rates

Fig. 3 and Table B1 show that the element/Ca ratios ofthe individual subsamples exhibit large differences at a gi-ven temperature setting. The differences in skeletal Sr/Caratios of 0.47–0.55 mmol/mol between 22 and 30 �C areequivalent to potential temperature differences of �7 to9 �C, applying the Sr/Ca ratio calibration derived from thisstudy. For the U/Ca ratio, the apparent temperature differ-ences among the individual subsamples within a given tem-perature are 4–5 �C; they are between 3 and 6 �C for theMg/Ca ratio.

We examined the effect of skeletal growth rate on ele-ment/Ca ratio fluctuation. The present study used linearextension rate to assess the growth rate of P. cylindrica.The fragments tended to grow faster from the tip than fromthe sides, similar to the pattern found in the branching coralAcropora spp. (Shirai et al., 2008). The linear extensionrates ranged from 1.65–2.95, 2.55–4.40, and 1.20–2.15 mm/30-day at 22, 26, and 30 �C, respectively(Table B1). The results demonstrated that each fragmenthas a variable extension rate, although they were culturedat the same seawater temperature. Our data support theobservation of Custodio and Yap (1997), who reported sig-nificant differences in skeletal extension rates among indi-vidual tips (i.e., “fragments” in this study) of the same P.

cylindrica colony. Furthermore, there was significant vari-ability in skeletal extension rate within the same fragment.For example, three subsamples taken from fragment #1(T22-P1) in tank I (22 �C) had extension rates of 1.65,2.10, and 1.90 mm/30-day (Table B1). Three subsampleshad slightly different element/Ca ratios (e.g., 8.77, 8.78,and 8.99 mmol/mol for the Sr/Ca ratio; 4.03, 4.17, and4.06 mmol/mol for the Mg/Ca ratio; and 1.05, 1.03, and1.05 lmol/mol for the U/Ca ratio). There was no clearlinear correlation between the element/Ca ratios and linearextension rate among the subsamples from the samefragment. Moreover, plots of the element/Ca ratios versusextension rate in subsamples with maximum growth axis(i.e., the longest extension, bold type in Table B1) or inthe entire subsamples (Fig. 4) revealed no recognizablelinear correlation between these two parameters. Therefore,it is considered that the growth rate of P. cylindrica, duringthe month-long culture performed in this study, had littleeffect on the skeletal element/Ca ratios. Interestingly, thecoral extension rates in tank II (26 �C) appear to be rela-tively higher than those in tanks I (22 �C) and III (30 �C)(Fig. 4), suggesting that 26 �C may be close to an optimalseawater temperature for the growth of P. cylindrica. This

Sr/Ca (mmol/mol) Mg/Ca (mmol/mol) U/Ca (lmol/mol)

8.80 ± 0.35 4.06 ± 0.24 1.03 ± 0.058.55 ± 0.27 4.73 ± 0.30 0.93 ± 0.078.28 ± 0.33 4.78 ± 0.17 0.86 ± 0.06

Fig. 4. Relationship between element/Ca ratios and linear extension rates of P. cylindrica (d = tank I at 22 �C; N = tank II at 26 �C;� = tank III at 30 �C).

4278 A. Armid et al. / Geochimica et Cosmochimica Acta 75 (2011) 4273–4285

can be explained by results from the experimental work ofJokiel and Coles (1977). They found that the effect oftemperature on the growth of three common species ofHawaiian reef corals (Pocillopora damicornis, Montipora

verrucosa, and Fungia scutaria) tends to be hyperbolic andthe skeletal growth optimum occurred around 26 �C.

Our results imply that there is a heterogeneous distribu-tion of Sr, Mg, and U in coral skeletons on a subsample(�<5 mm) or even smaller scale. The relationship betweenelemental distributions and skeletal microstructure mayprovide an avenue to assess the variability of the element/Ca ratios among subsamples, as was reported for Porites

(e.g., Cohen et al., 2001; Allison et al., 2005; Meibomet al., 2007), Pavona spp. (Meibom et al., 2004), anddeep-sea corals (e.g., Shirai et al., 2005; Cohen et al.,2006). The high concentration of Mg is localized to the cen-ters of calcification, whereas the Sr concentration is not(Meibom et al., 2004). Moreover, the centers of calcificationare considered to be formed at night and are expected to bedistinguished by relatively high Sr/Ca ratios (Cohen andMcConnaughey, 2003). Shirai et al. (2008) described thatthe branching coral Acropora consisted of “infilling” skele-ton (secondarily precipitated aragonite) and “framework”

skeleton. By using microscale element analyses, they con-cluded that the main part of the infilling skeleton has a low-er Mg/Ca ratio and higher Sr/Ca and U/Ca ratios thandoes the framework skeleton. Taking into considerationthe results of these studies, we inferred that the element/Ca ratio fluctuations for subsamples in each temperaturetreatment may reflect variable mixing ratio of infilling andframework skeleton analyzed in bulk skeleton powder.

4.2. Sr/Ca thermometry

The possibility of using Sr/Ca ratios in coral skeleton asa paleothermometer was first reported by Weber (1973),who proposed a negative correlation between the concen-tration of Sr in the skeletal aragonite of corals and seawatertemperature. Since the study by Smith et al. (1979), manystudies on Sr/Ca thermometry extensively preserved mas-sive Porites corals (Table 3), including the important dis-covery of using high-precision thermal ionization massspectrometry to measure this ratio (Beck et al., 1992).Our study showed that the Sr/Ca ratio of the branching

coral P. cylindrica is significantly correlated with seawatertemperature, yielding a regression slope (=temperaturedependency) of �0.0642 mmol/mol/�C, with an r2 valueof 0.59 (Fig. 3a). This slope falls within a range of slopesobtained from massive Porites sp. corals and, in particular,is close to the mean value of �0.0607 mmol/mol/�C derivedfrom 38 previous calibrations (Correge, 2006).

Although some studies showed that skeletal growthrate influences the Sr/Ca ratio in aragonitic coral skele-tons (Oomori et al., 1982; de Villiers et al., 1994, 1995;Cohen and Hart, 2004), recent examinations of calibra-tion–verification exercises (Quinn and Sampson, 2002;Felis et al., 2009) and temperature-controlled experiments(Inoue et al., 2007) suggested that skeletal growth effectsdo not influence the Sr/Ca ratios of massive Porites cor-als at a subseasonal resolution. A recent culture studyusing the coral Acropora sp. (Reynaud et al., 2007)showed a good correlation between the coral Sr/Ca ratioand water temperature; the coral Sr/Ca ratio was notsensitive to light intensity or to changes in calcificationrate induced by changes in the light intensity, suggestingthat water temperature is the dominant parameter con-trolling the skeletal Sr/Ca ratio. In the present study,no significant linear correlation between the skeletalSr/Ca ratio and linear extension rate was found for eachtemperature treatment (Fig. 4; Table B1), which may sup-port the conclusion that the effect of growth rate on theskeletal Sr/Ca ratio is “negligible”.

Furthermore, it is important to note that we used wellseawater in incubators, with Sr2+ and Ca2+ concentra-tions differing from that of normal seawater used in pre-vious studies (Table 1). In order to compare our skeletalSr/Ca-temperature calibration with those from previousstudies (Table 3), considering the effect that the differencein solution Sr/Ca ratio may have on skeletal Sr/Ca ratio,the distribution coefficient (D)-temperature calibrationswere derived as shown by Shen et al. (1996). The rela-tionship between Me2+/Ca2+ ratio in seawater and Me/Ca ratio in carbonate can be expressed using the follow-ing equation:

½Me=Ca�carbonate ¼ DMe ½Me2þ=Ca2þ�seawater;

where DMe is an empirical distribution coefficient.

Table 3Sr/Ca paleotemperatures established for massive (previous studies) and branching (this study) Porites corals and inorganic aragonite.

Reference Species Location aA bA r2 Annual cycles(n)

SST data

Beck et al. (1992) P. lobata Amedee, New Caledonia 10.716 �0.06245 6 Oxygen 18B

de Villiers et al. (1994) P. lobata Koko Head, Hawaii 10.956 �0.07952 0.95 2 LocalMitsuguchi et al. (1996) P. lutea Ishigaki-Jima, Japan 10.5 �0.0608 0.73 8 30 km awayShen et al. (1996) P. lobata Nanwan Bay, Taiwan 10.356 �0.0528 0.96 2 LocalMcCulloch et al. (1999) Porites sp. Huon Peninsula, Papua New

Guinea10.7 �0.062 – 10 Local

Correge et al. (2000) P. lutea Amedee, New Caledonia 10.73 �0.0657 0.62 9 LocalWei et al. (2000) P. lutea Sanya Bay, South China Sea 11.422 �0.0817 0.56 9 90 km awayQuinn and Sampson (2002) P. lutea Amedee, New Caledonia 10.073 �0.052 0.84 18 LocalAllison and Finch (2004) P. lobata Hawaii 10.861 �0.080 0.919 4 10 km awayFelis et al. (2004) Porites sp. Eilat, Red Sea 10.781 �0.0597 0.78 5 LocalStephans et al. (2004) P. lutea Amedee, New Caledonia 10.331 �0.0504 0.86 25 LocalSun et al. (2005) Porites sp. Xisha Island, South China Sea 10.327 �0.0534 0.96 LocalYu et al. (2005) P. lutea Leizhou Peninsula, South China

Sea9.836 �0.0424 – 11 1.5 km away

Correge (2006) Porites sp. Uitoe, New Caledonia 10.34 �0.0549 0.92 6 Local/satellite

Correge (2006) Mean calibration 10.553 �0.0607 –Ourbak et al. (2006) Porites sp. Uitoe, New Caledonia 10.248 �0.054 0.64 4 LocalOurbak et al. (2006) Porites sp. Uitoe, New Caledonia 10.451 �0.062 0.55 4 LocalDeLong et al. (2007) P. lutea Amedee, New Caledonia 10.451 �0.054 0.88 32 LocalInoue et al. (2007) Porites spp. Culture experiment 10.31 �0.057 0.69Mitsuguchi et al. (2008) Porites sp. Con Dao Island, South China Sea 10.105 �0.04469 0.951 10 LocalKinsman and Holland(1969)

Inorganicaragonite

10.66 �0.039 –

Dietzel et al. (2004) Inorganicaragonite

11.27 �0.043 –

This study P. cylindrica Culture experiment 10.214 �0.0642 0.59

A Sr/Ca (mmol/mol) = a + b � water temperature (�C).B SSTs were calculated based on the equation: d18Oc � d18Ow = 0.594 � 0.209 � SST (�C), where d18Oc and d18Ow are the isotopic

compositions of the coral and seawater, respectively.

Seawater temperature proxies from coral Porites cylindrica 4279

To use the skeletal Sr/Ca ratio for paleothermometry, itis a prerequisite to assume that the Sr/Ca ratio of seawateris constant through time (Correge, 2006). It is generally ac-cepted that the behavior of Sr and Ca in seawater is conser-vative and their concentrations and the Sr/Ca ratio are notsignificantly affected by the biological and chemical reac-tions that take place within the main body of the oceans.However, de Villiers et al. (1994) found that variations inthe Sr/Ca ratio of coral reef waters was significantly differ-ent, potentially resulting in temperature uncertainties of upto �2.5 �C. Later studies (de Villiers et al., 1995; de Villiers,1999) found larger differences, with 2–3% spatial gradientsin the Sr/Ca ratio of seawater. Therefore, in order to calcu-late DSr of corals, it is necessary to use the Sr/Ca ratio ofseawater around their growth sites. In this study, the Sr/Ca ratios of coral reef water samples from Hawaii, the wes-tern Pacific Ocean, the northeast Pacific Ocean (de Villierset al., 1994), New Caledonia (Beck et al., 1992; Shenet al., 1996), Nanwan Bay (Shen et al., 1996), Xisha Island(Sun et al., 2005), and the Red Sea (Enmar et al., 2000) wereused to produce DSr–SST calibrations of associated loca-tions from previous studies (Table 3) for comparison withour DSr-temperature calibration (Fig. 5).

It is clear that the relationship between DSr and wellseawater temperature in this study appears to be consistentwith the relationships of DSr–SST calibrations from

previous studies (Fig. 5). However, Fig. 5 illustrates differ-ences in the y-intercepts of calibrations among studiesunlike the slopes. The observed differences in the Sr/Capaleothermometers may be the results of several factorsincluding differences in analytical methods, lack of aninternational standard used for precise determining ofSr/Ca ratio among laboratories, differences in SST databaseused for calibration (Quinn and Sampson, 2002; Correge,2006), sampling resolution (Ourbak et al., 2006), andenvironmental differences between study sites (DeLonget al., 2007). The DSr-temperature calibration calculatedfrom the present study is DSr = 1.180(±0.0280) �0.0062(±0.0011) � T (�C) (r2 = 0.48, p < 0.05). The slope(�0.0062) of our DSr-temperature calibration falls withina range of slopes (�0.005 to �0.01 per 1 �C) calculatedfrom other studies cited in Table 3. In particular, the tem-perature dependency of our calibration is quite similar tothe results of Shen et al. (1996) and Quinn and Sampson(2002).

4.3. Mg/Ca thermometry

In addition to the well-known Sr/Ca ratio (e.g., Shenet al., 1996; Correge, 2006; Felis et al., 2009), the skeletalMg/Ca ratio of corals has been considered an alternativecandidate for a proxy of seawater temperature. Previous

Fig. 5. Relationship between DSr and seawater temperature. Boldline represents the result of this study (errors represent standarddeviations, 2r). Thin lines represent estimated DSr-temperaturecalibrations for massive Porites corals. Dashed lines representinorganic aragonites. References are given in Table 3.

Fig. 6. Relationship between DMg and seawater temperature. Boldline represents the result of this study (errors represent standarddeviations, 2r); thin lines are estimated DMg-temperature calibra-tions for massive Porites corals from other studies listed in Table 4.

4280 A. Armid et al. / Geochimica et Cosmochimica Acta 75 (2011) 4273–4285

investigations elucidated the potential relationships be-tween coral Mg/Ca ratio and seawater temperature (e.g.,Chave, 1954; Oomori et al., 1982; Mitsuguchi et al., 1996;Wei et al., 2000). In contrast, it was recently noted that cor-al Mg/Ca ratio reflects seawater temperature, as well asother parameters, such as biological/metabolic effects andmicroenvironmental variations, the latter of which seemto have a greater influence (e.g., Meibom et al., 2004; Inoueet al., 2007; Reynaud et al., 2007; Mitsuguchi et al., 2008).Although the fidelity of the coral Mg/Ca ratio-basedthermometer remains controversial, we compared the rela-tionship between coral Mg/Ca ratio and SST from the pres-ent study with those from previous studies (Mitsuguchiet al., 1996; Sinclair et al., 1998; Fallon et al., 1999; Weiet al., 2000; Quinn and Sampson, 2002; Fallon et al.,2003; Yu et al., 2005) (Table 4).

Results of the present study revealed that the skeletalMg/Ca ratio of P. cylindrica has a correlation with seawatertemperature (r2 = 0.67, p < 0.05; Fig. 3b), providing aregression slope (0.1002 mmol/mol/�C) that is consistentwith previous studies (Table 4). DMg-temperature calibra-tions were calculated to normalize the differences in Mg/Ca ratio in the solution phase between this study andprevious studies (Fig. 6). Our DMg-temperature calibrationDMg (�10�4) = 4.123 (±0.609) + 0.211(±0.0238) � T (�C)

Table 4Mg/Ca paleotemperatures established for massive (previous studies) and

Reference Species Location

Mitsuguchi et al. (1996) P. lutea Ishigaki-Jima, JapanSinclair et al. (1998) P. mayeri Great Barrier Reef, AustraliFallon et al. (1999) P. lobata Shirigai Bay, JapanWei et al. (2000) Porites sp. Sanya Bay, South China SeaQuinn and Sampson (2002) P. lutea Amedee, New CaledoniaFallon et al. (2003) Porites sp. Great Barrier Reef, AustraliYu et al. (2005) P. lutea Leizhou Peninsula, South CThis study P. cylindrica Culture experiment

A Mg/Ca (mmol/mol) = a + b �Water Temperature (�C).

(r2 = 0.69, p < 0.05) showed a similar trend to that seen inprevious studies, with slopes of �0.2. However, the DMg

values largely differ among studies (Fig. 6). Note that theMg/Ca ratios of P. cylindrica revealed in this study (3.9–5.1 mmol/mol; Table B1) are consistent with other studies,for example, those of massive Porites spp. (�3.5 to5.5 mmol/mol) reported by Inoue et al. (2007). Althoughit is suggested that the Mg/Ca ratio of massive Porites cor-als is strongly influenced by skeletal extension rate (with anegligible contribution from seawater temperature), ourresults did not reveal any significant linear correlation ofP. cylindrica coral Mg/Ca ratios with linear extension rate(Fig. 4; Table B1). This could not explain the large discrep-ancy in the DMg values between this study and previousstudies. A possible explanation is that the well seawatercomposition or environmental conditions used for our cul-ture experiment might have significantly influenced theincorporation of Mg into coral skeletons. Another applica-ble constraint may come from a species-dependent effect(Fallon et al., 1999). Other investigators found various dis-crepancies in the results when using skeletal Mg/Ca ratio asa paleothermometer (Sinclair et al., 1998; Fallon et al.,1999, 2003; Mitsuguchi et al., 2001, 2003; Watanabeet al., 2001; Marshall and McCulloch, 2002). Most of themsupported the argument by Amiel et al. (1973), that up to

branching (this study) Porites corals.

aA bA r2 Annual cycles (n) SST data

1.15 0.129 0.85 8 30 km awaya 0 0.16 – 3 Local

1.38 0.088 0.44 14 Local1.635 0.1117 0.94 9 90 km away2.638 0.105 0.61 18 Local

a 1.044 0.1123 0.53 3 Local/satellitehina Sea 1.32 0.110 – 11 1.5 km away

1.973 0.1002 0.67

Fig. 7. Relationship between DU and seawater temperature. Boldline represents the result of this study (errors represent standarddeviations, 2r); thin lines are estimated DU-temperature calibra-tions for massive Porites corals from other studies listed in Table 5.

Seawater temperature proxies from coral Porites cylindrica 4281

30% of the Mg is located in adsorbed sites and in organiccompounds, and that the various amounts of organic com-pounds in corals might affect its incorporation. Further-more, by using ion-microprobe imaging to analyze thearagonite skeleton of the coral Pavona clavus, Meibomet al. (2004) demonstrated that the distribution of Mg washighly correlated with the fine-scale structure of the coralskeleton. The existence of such effect of the skeletalstructure on the distribution of Mg in the skeleton may bea reason why our P. cylindrica Mg/Ca ratios tend to havea second order polynomial relationship with temperaturetreatment: Mg/Ca = �0.01922 � T2 + 1.089 � T � 10.60(r2 = 0.87) (Fig. 3b; data are tabulated in Table B1).Although the correlations between coral Mg/Ca ratio orDMg and seawater temperature (Figs. 3b and 6) imply thatP. cylindrica may serve as an alternative coral species foruse as a paleothermometer via its Mg/Ca ratio, more studiesare needed to fully clarify the reason for the large discrep-ancy in DMg values.

4.4. U/Ca thermometry

The use of coral U/Ca ratio as a potential paleother-mometer was first demonstrated by Min et al. (1995) andShen and Dunbar (1995). Several subsequent studies fromdifferent locations have provided inconsistent conclusionsabout the factors controlling the incorporation of U intocoral skeletons (Sinclair et al., 1998; Wei et al., 2000; Fallonet al., 2003). However, recent studies suggested that U/Caratios in massive Porites corals are a relatively robust proxyfor SST (e.g., Correge et al., 2000; Quinn and Sampson,2002; Ourbak et al., 2006; Felis et al., 2009).

The DU-temperature calibration was established to com-pare it with those estimated from previous studies (Fig. 7;Table 5), as seen in Sr/Ca and Mg/Ca thermometers. Theresidence time of Ca and U in the ocean is predicted tobe 1.1 � 106 years (Broecker and Peng, 1982) and�3 � 105 years (Ku et al., 1977), respectively. As a conse-quence, significant temporal and spatial changes in the U/Ca ratio in the oceans would not be expected over the pastfew hundred thousand years. Thus, a U concentration of3.2 ppb (Ku et al., 1977; Broecker and Peng, 1982; Chenet al., 1986; Armid et al., 2008a) and a Ca concentrationof 412 ppm (Culkin, 1965; Broecker and Peng, 1982) in sea-water were used for estimating the DU values from previousstudies.

The DU of P. cylindrica corals correlates wellwith seawater temperature, which can be expressed asDU = 1.329(±0.0438) � 0.0175(±0.0017)� T (�C) (r2 = 0.75,p < 0.05) (Fig. 7). The DU-temperature calibrations frommassive Porites corals (Fig. 7) have similar sensitivities toseawater temperature, but their DU values differ by �8%(at 25 �C), implying that a discrepancy was also encoun-tered when using the U/Ca ratio from massive Porites coralas an SST proxy (Shen and Dunbar, 1995). Our DU-temper-ature calibration with a relatively gentle slope indicated thatthe DU value of P. cylindrica coral obtained in this study isin agreement with those of massive Porites corals reportedby Min et al. (1995), Sinclair et al. (1998), Quinn and Samp-son (2002) and Ourbak et al. (2006) for growth at 22 �C; by

Fallon et al. (1999) and Correge et al. (2000) for growth at26 �C; and by Wei et al. (2000) and Felis et al. (2009) forgrowth at 30 �C.

Considering this offset and the low sensitivity of our DU-temperature calibration, factors other than temperatureseem to influence U incorporation into P. cylindrica. In gen-eral, three potential factors relate to the U/Ca ratio in corals:skeletal growth rate (Cross and Cross, 1983), U content ofseawater (Swart and Hubbard, 1982), and U speciation inseawater (Swart and Hubbard, 1982; Min et al., 1995; Shenand Dunbar, 1995). Based on our data, the effect of skeletalgrowth rate on the coral U/Ca ratio (and finally, DU) is notconvincing, because there was no significant linearcorrelation between the coral U/Ca ratio and linear extensionrate of P. cylindrica at each culture temperature (Fig. 4;Table B1). Another potential effect may have arisen fromthe difference in U concentration (of�20%) between well sea-water used in this study and normal seawater (Table 1). How-ever, given that the difference in the U/Ca ratio in solutionphase was not significant, such an effect on DU-temperaturecalibrations can be ignored. With regard to the U speciationfactor, U in seawater exists as a uranyl ion, UO2þ

2 (Ku et al.,1977), and as three uranyl carbonate complexes, UO2CO0

3,UO2ðCO3Þ2�2 , and UO2ðCO3Þ4�3 (Swart and Hubbard, 1982;Grenthe et al., 1992). However, the mode of U incorporationinto coral skeletons, which is very sensitive to pH and the car-bonate ion activity of solutions, remains unclear (Armidet al., 2008b). Accordingly, some researchers suggested thatU is incorporated into coral as UO2þ

2 , substituting for Ca2+

in the skeletal lattice (Kitano and Oomori, 1971; Broeckerand Peng, 1982; Min et al., 1995), whereas other investigatorssupported UO2ðCO3Þ2�2 (Swart and Hubbard, 1982; Shenand Dunbar, 1995; Sinclair et al., 1998) or UO2ðCO3Þ4�3 (Ree-der et al., 2000) as the U species being incorporated into andsubstituting for CO2�

3 in the coral skeletons. Based on theabove considerations, the gentle slope of our DU-tempera-ture calibration relative to those of other studies (Fig. 7)may arise from the fact that well seawater, which was usedfor our culture experiments, has a slightly greater alkalinity

Table 5U/Ca paleotemperatures established for massive (previous studies) and branching (this study) Porites corals.

Reference Species Location aA bA r2 Annual cycles (n) SST data

Min et al. (1995) Porites Amedee, New Caledonia 2.232 �0.0465 – 5 LocalSinclair et al. (1998) P. mayeri Great Barrier Reef, Australia 2.24 �0.046 – 3 LocalFallon et al. (1999) P. lobata Shirigai Bay, Japan 2.26 �0.044 0.71 14 LocalCorrege et al. (2000) P. lutea Amedee, New Caledonia 2.106 �0.0367 0.79 9 LocalWei et al. (2000) Porites sp. Sanya Bay, South China Sea 1.957 �0.029 0.72 9 90 km awayQuinn and Sampson (2002) P. lutea Amedee, New Caledonia 1.847 �0.029 0.44 18 LocalOurbak et al. (2006) Porites Uitoe, New Caledonia 1.928 �0.033 0.71 9 LocalFelis et al. (2009) Porites sp. Ogasawara Island, Japan 2.057 �0.034 0.68 19 LocalThis study P. cylindrica Culture experiment 1.488 �0.0212 0.78

A U/Ca (lmol/mol) = a + b �Water Temperature (�C).

4282 A. Armid et al. / Geochimica et Cosmochimica Acta 75 (2011) 4273–4285

(2600 lmol/kg) compared with normal seawater (2300 lmol/kg). Accordingly, the difference in carbonate ion activity be-tween the two types of seawater might have influenced U spe-cies incorporation into coral skeletons. Additionally, becauseP. cylindrica was used in the experiment, a species-dependentfactor cannot be dismissed. Nevertheless, the relatively highcorrelations of the coral U/Ca ratio (r2 = 0.78) and DU

(r2 = 0.75) with seawater temperature revealed by this study(Figs. 3c and 7) demonstrated that P. cylindrica might serveas another useful coral proxy for seawater temperature viaits U/Ca ratio.

Furthermore, temperature sensitivities of DSr, DMg, andDU calibrations of the branching coral P. cylindrica, definedas the variation in DMe value relative to median DMe/seawa-ter temperature difference, were estimated as 0.64%/�C,1.93%/�C, and 1.97%/�C, respectively. These resultssuggested that the U/Ca thermometer is highly sensitive toseawater temperature, further supporting that the P. cylind-

rica U/Ca ratio may be a useful proxy for paleo-seawatertemperature.

5. SUMMARY

We conducted temperature-controlled culture experi-ments on branching corals (P. cylindrica) to evaluate thereliability of skeletal Sr/Ca, Mg/Ca, and U/Ca ratios aspaleothermometers. The coral Sr/Ca and U/Ca ratios,and possibly the Mg/Ca ratio, correlated linearly with sea-water temperature and were not significantly influenced bylinear extension rate. However, the potential influence ofgrowth rate (calcification rate or skeletal extension rate)on the element/Ca ratios remains a matter of debate, andit should be addressed to fully clarify the link between theparameters.

Comparison of our DMe-temperature calibrations withthose of previous studies showed that seawater temperaturedependency of DSr and DMg of P. cylindrica seems to beconsistent with that of massive Porites corals. This studydemonstrated that the branching coral P. cylindrica canbe a good alternative and unique coral species for develop-ing a potential paleothermometer using its Sr/Ca ratio (andpossibly the Mg/Ca and U/Ca ratios). In addition, therelatively high growth rate of P. cylindrica may recordinformation about environmental changes at a greater tem-poral resolution relative to massive corals. Further investi-gations using different colonies and longer culture periods

(>1 month) are needed to establish the use of element/Caratios of branching P. cylindrica corals as robustpaleothermometers.

ACKNOWLEDGMENTS

We thank the staff of the Okinawa Environmental Researchand Technology Center for the use of ICP-MS and the staff ofthe Instrumental Research Center (University of the Ryukyus)for the use of ICP-AES. We also thank Anders Meibom and fouranonymous reviewers for very constructive comments on this man-uscript. This work was supported by a Grant-in Aid from theJapan Society for the Promotion of Science Research Funds Nos.17201006, 20310014, and 20398308 and by the Rising Star Programfor Subtropical Island Sciences, University of the Ryukyus.

APPENDIX A. SUPPLEMENTARY DATA

Supplementary data associated with this article can befound, in the online version, at doi:10.1016/j.gca.2011.05.010.

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Associate editor: Anders Meibom