Calibration of Stable Oxygen Isotopes in Siderastrea Radians (Cnidaria:Scleractinia): Implications for Slow-Growing Corals

Article Geochemistry 3 Volume 7, Number 9 Geophysics 20 September 2006 GeosystemsG Q09007, doi:10.1029/2005GC001196 G ISSN: 1525-2027 AN ELECTRONIC JOURNAL OF THE EARTH SCIENCES Published by AGU and the Geochemical Society

Click Here for Full Article Calibration of stable oxygen isotopes in Siderastrea radians (Cnidaria:Scleractinia): Implications for slow-growing corals

Christopher S. Moses Division of Marine Geology and Geophysics, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149, USA

Now at College of Marine Science, University of South Florida, 140 7th Avenue South, St. Petersburg, Florida 33701, USA ([email protected]) Peter K. Swart Division of Marine Geology and Geophysics, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149, USA Richard E. Dodge National Coral Reef Institute, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, Florida 33004, USA

[1] Geochemical proxies in the skeletons of corals used for the purpose of reconstructing environmental records have typically been obtained from relatively fast-growing corals (usually >8 mm yr1) and from only a few key genera (most commonly Porites and Montastraea). In many areas, however, there are no suitable fast-growing corals available for such reconstructions. Here, we investigate the potential of Siderastrea radians, a slow-growing Atlantic and Caribbean zooxanthellate coral, as an archive of sea surface temperature (SST) and salinity over the period from 1891 to 2002. Sampling the skeleton of three corals from the Cape Verde Islands, we were able to reproduce a clear seasonal signal, but with limited correlation to monthly SST, arising from inadequate chronologic constraint of the individual samples. The SST-18O calibration slopes for different sampling scales on several cores can range from about 9°C %1 to +2°C %1 (compared to other published values of around 5to4°C %1). Careful treatment 18 produced a O–SST calibration equation where SST(°C) = 12.56(±1.20) 3.86(±0.39)*(c–w). The recognition of the limitations of calibration at such small growth rates due to skeletal complexity and suspicion of environmental interferences suggests the need for careful consideration in the interpretation of climate proxy results from S. radians and other slow-growing corals.

Components: 7637 words, 9 figures, 2 tables. Keywords: coral; isotopes; paleoclimate; sampling strategy; Siderastrea; Cape Verde Islands. Index Terms: 4220 Oceanography: General: Coral reef systems (4916); 4924 Paleoceanography: Geochemical tracers; 4215 Oceanography: General: Climate and interannual variability (1616, 1635, 3305, 3309, 4513); 1041 Geochemistry: Stable isotope geochemistry (0454, 4870). Received 22 November 2005; Revised 8 March 2006; Accepted 29 June 2006; Published 20 September 2006.

Moses, C. S., P. K. Swart, and R. E. Dodge (2006), Calibration of stable oxygen isotopes in Siderastrea radians (Cnidaria:Scleractinia): Implications for slow-growing corals, Geochem. Geophys. Geosyst., 7, Q09007, doi:10.1029/2005GC001196.

structions due to its limited lifespan (40 years) 1. Introduction locally [Moses, 2005].

[2] The skeletons of scleractinian corals are the [4] The slow-growing nature of S. radians intro- most common high-resolution biogenic proxy duces several complications to the analysis of their archives for sea surface temperature (SST) and skeletal proxy record. In addition, some potential salinity in the shallow tropical oceans of the world environmental complications are suggested to in- [Dodge and Lang, 1983; Dunbar and Wellington, fluence the accuracy of the proxy records. This 1981; Fairbanks and Dodge, 1979; Leder et al., investigation resulted in the recognition of sam- 1996; Linsley et al.,2004;Weil et al.,1981; pling limitations in the use of S. radians,and Wellington and Dunbar, 1995]. For the most part, perhaps other slow-growing zooxanthellate corals, studies of coral skeletal proxies in the Atlantic have as robust proxy archives. lagged behind those in the Pacific in quantity and length of records, largely because of interest in El 2. Methods and Definitions Nin˜o-Southern Oscillation (ENSO) dynamics [Linsley et al., 2004; Wellington and Dunbar, 2.1. Sample Collection and Preparation 1995]. Unlike the Pacific or western Atlantic, there is a relative paucity of suitable corals for long-lived [5] Field work for this project was carried out on the proxy records in the eastern tropical north Atlantic island of Sal in the Cape Verde Islands (Figure 1). [Laborel, 1974; Morri and Bianchi, 1995; Wells, Corals were cored using a 16 h.p. hydraulic drill 1988]. However, because of the emerging signifi- fitted with a 10 cm diameter diamond-tipped core cance of tropical North Atlantic climate variability barrel. Since the pavements of S. radians were [Curry et al., 2003; Enfield and Mayer,1997; extensive in some areas, choosing the best location Enfield et al., 2001; Schmidt et al., 2004], prein- to take a core directly along the growth axis strumental climate records from the eastern tropical [Goreau, 1977] was often difficult. The coring North Atlantic are more desirable than ever. was performed by a team of trained scientific divers using SCUBA. The corals were collected [3] Within the Cape Verde Islands (Figure 1), from depths of 4–6 m, thus avoiding the potential the only suitable zooxanthellate coral for use as problems from vital effects reported with depths a preinstrumental proxy archive is Siderastrea around 20 m [Erez, 1978; Fairbanks and Dodge, radians. This slow-growing species of Siderastrea 1979; Weber, 1973; Weber et al., 1976; Weber and is common throughout the tropical areas of the Woodhead, 1972]. eastern and western Atlantic as well as the Carib- bean [Veron, 2000]. In the Caribbean, S. radians is [6] Immediately after collection, the cores were generally a small, unobtrusive zooxanthellate coral soaked in fresh water for a few hours, rinsed with species that is found predominantly in areas with fresh water to remove the bulk of the organic higher sedimentation [Lirman et al., 2003]. Like- material present in the living portion of the coral, wise, in the Cape Verde Islands, these corals are and then air dried. No bleach (sodium hypochlo- very successful in areas where they are periodically rite; NaClO ) or hydrogen peroxide (H2O2) was buried under 1–2 cm of shifting coarse sands. used to remove organics or otherwise clean the Unlike the Caribbean and western Atlantic where skeletons. S. radians grows to a maximum size of commonly [7] A masonry saw was used to slice the corals for less than 10 cm in diameter [Lirman et al., 2003] and 1 sclerochronology, resulting in coral slabs 5–6 mm has an annual extension rate between 5–12 mm yr thick. After being washed, sonicated and dried, [Corte´s and Risk, 1985], the same species forms coral slabs were then X-rayed using a dental X-ray broad expanses of coral pavements commonly 1–3 m machine and Kodak Industrex AA400 X-ray film in diameter and an average of 10–15 cm thick [Hudson et al., 1976; Knutson et al., 1972]. Set- [Laborel, 1974; Moses et al., 2003]. These corals tings for the X-ray machine are fixed at 15 mA and also have an unusually slow extension rate of 1.3 1 70 kV, leaving time of exposure as the only (±0.3) mm yr (N = 161) leading to some diffi- variable. An aluminum wedge was used to cali- culty in the accurate interpretation of sclerochro- brate density, and exposure times ranged from 7– nology by X-radiograph (Figure 2). Porites 11 seconds. astreoides is also present in the Cape Verde Islands, 13 but it is less common than S. radians and not useful [8] Sample preparation for stable carbon ( C) for decadal-scale or preinstrumental climate recon- and oxygen (18O) isotope analyses was performed

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Figure 1. Location map of the Cape Verde Islands study area. The arrow points to the island of Sal, where the cores were collected. at the University of Miami, RSMAS Stable Isotope 2.2. Modified Sampling Technique Lab (SIL) using a hand held, low speed dental drill TM [9] Normal recommended sampling methods, such and a high precision New Wave micromill. Cor- as restricting sampling to a single skeletal element als SAL-6 and CV-22 were sampled initially at a [Leder et al., 1996], did not work well because rate of one sample per year using the hand held such individual structures as the thecal wall are dental drill in order to look quickly for any extremely fine in S. radians and are much more decadal-scale trends. This was carried out by narrow ( 50 m) than the drill bit of the micro- continuous milling parallel to the axis of growth mill. In these corals, the diameter of the average along the thecal wall between two corallites using a polyp is 3 mm, thus we restricted the total width 1.6 mm diameter burr bit. Sample increments were of the sample to less than half of that. In order to determined by the annual density banding using further limit time transgression in the horizontal high resolution scans of the x-radiographs en- (perpendicular to the growth axis) dimension, the hanced by computer. The annual sampling by hand transect was centered on the exotheca of two produced enough powder that each sample was neighboring corallites. With this positioning, the analyzed in duplicate. Coral SAL-4, however, was drill progressed only 1/4 of the way across each not sampled annually by hand. All corals were corallite and was restricted to the least curved sampled with the micromill by continuously mill- portion of the septa and dissepiments, remaining ing along the thecal wall between two corallites. within a growth surface. The average micromill Setting the step increment of the micromill to 104 m 1 sample on SAL-6 was 1344 m wide and 450 m maintained a sampling rate of 10–15 samples yr deep at a step increment of 104 m. This removed despite the subtle changes in growth rate within a volume of 6.3 102 mm3 for each sample each coral and from coral to coral. The drilling was allowing the recovery of 40–70 g of powder. The performed in a direction perpendicular to the axis exact amount of CaCO powder recovered of growth at each step increment, progressing 3 depended on the skeletal density and porosity of parallel to the axis of growth from step to step. the sample volume.

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[12] ‘‘Annual’’ samples (indicated as CoralAnn) are those taken with a dental drill by hand based on sclerochronology at a frequency of one sample yr1 (continuous milling). Annual samples were analyzed as two replicate samples, and reported as the average value of these analyses.

[13] Samples referred to as ‘‘monthly’’ (indicated as CoralMo) were taken using the micromill as described above at a frequency of 10–15 samples yr1 (continuous milling). The range in number of samples is the result of the constant sampling distance (104 m) applied over the slightly variable annual extension rates. These samples were then interpolated to a standard 12 samples per year and assigned to a specific month as described above.

[14] ‘‘Annual average’’ values (indicated as CoralAnnAvg) are single values representing the mean of the 12 values in a given year. These data were produced by microdrilling at the higher sampling frequency for monthly samples, but were then reduced to a single data value per year for purposes of data analysis.

2.5. Environmental Data Figure 2. X-radiograph of the slab of coral SAL-6 prior to microdrilling. Many of the annual density band [15] The SST data set used in this study is the couplets are relatively poorly defined. In some areas of National Climate Data Center (NCDC) Extended the core, annual bands are even functionally undefined. Reconstruction SST (ERSST) (v.2) with a monthly Years are marked at decadal intervals. 2° 2° data set spanning January 1854–present [Smith and Reynolds, 2004]. The NCDC ERSST data set for the grid cell centered at 16°N, 24°W was used for the local Sal SST record in the 2.3. Conversion of Sample Locations From absence of an otherwise complete instrumental Space to Time record. Comparison of the NCDC data with an in [10] The high-resolution micromill samples taken situ thermistor over 18 months indicated an RMS at 10–15 samples per year were linearly interpo- difference of ±0.6°C, and a linear relationship very lated to 12 ‘‘monthly’’ values. The chronology was close to 1.0, indicating that the NCDC data suffi- obtained using a combination of sclerochronology ciently represented the actual SST at the study site. and the annual cycle of the 18O values. A Mat- labTM routine was written to accurately handle the 3. Results of Siderastrea radians interpolation. The linear interpolation method an- Calibration chored two endpoints (chosen based on the occur- rence of the high-density band and the lowest 18O value) and used weighted distance to preserve the 3.1. Bulk Stable Isotope Results 18 proportional location of any missing or offset data [16] The average O value for Cape Verde points. The most negative (warmest) 18O value in Siderastrea radians, taken from annual samples, each interpolated annual set was assigned to Octo- is 3.12 (±0.15) % (N = 112) for SAL-6Ann and ber, characteristically the month with the warmest 2.91 (±0.23) % (N = 62) for CV-22Ann. The SST in the Cape Verde Islands (26.5°C). mean difference between replicate annual samples for SAL-6Ann is 0.01 (±0.10) % and for CV-22Ann it is 0.02 (±0.10) %, both within 2.4. Terminology machine error. Slightly different average 18Ovalues [11] In this report, three terms of data sampling resulted from the monthly samples, yielding frequency are used to describe sampling as follows: 2.94 (±0.13) % (N = 882) and 3.10 (±0.22)

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Figure 3. Records of SAL-6 monthly 18O and SST shown for the period of calibration (1980–2000). The thick green line is 18O and the thin black line is SST at Sal. These three transects were sampled parallel to each other in the same coral slab over a total horizontal distance of only 1.5 cm. The 18O axis in % VPDB has been inverted in the traditional manner. Monthly data generally track the seasonal cycle in SST, but the signal varies from transect to transect.

1 % (N = 588) for SAL-4Mo and SAL-6t3Mo a relationship of about 9°C % . This slope is respectively, and 2.82 (±0.28) % (N = 348) quite large compared to the commonly accepted 18 18 for CV-22Mo. The mean O of monthly sam- relationship between O and SST [Leder et al., ples for the three corals are significantly different 1996; Weber and Woodhead, 1972; Wellington from each other at the 99% confidence interval and Dunbar, 1995], and is even higher than the (one-way ANOVA; P < 0.01). The annual average relationship reported by Bagnato et al. [2004] for 18O for the three corals were almost identical Diploastrea from the south Pacific (Table 1). to the annual and monthly values, with 2.94 However, when monthly isotope values are con- (±0.13) % (N = 74) for SAL-4AnnAvg, 3.10 sidered rather than just the annual range, this (±0.13) % (N = 49) for SAL-6t3AnnAvg, and steep relationship is reduced, but still suffers a 2.81 (±0.11) % (N = 29) for CV-22AnnAvg. The wide range of values from coral to coral and even results for SAL-4 were identical across sampling within corals (Figures 4 and 5). Compared to scales, and the range in the 18O means for SAL-6 other published values for the relationship of and CV-22 is not statistically significant, indicat- coral skeletal 18O to ambient SST, these values ing that overall, the annual, monthly and annual widely straddle the range of published 18O average sampling methods will all accurately thermometer calibrations (Table 2). represent the bulk 18O value of the coral. The 13C averages for the corals, using monthly values, [18] Of particular interest is the wide range of SST – 18O calibration slopes (Figure 5) and monthly were 0.60 (±0.30) % (N = 882) for SAL-4 , Mo 18O records (Figure 3) found in the neighboring, 0.48 (±0.15) % (N = 588) for SAL-6t3 , and Mo parallel transects of SAL-6 (Figure 5). The most 0.26 (±0.22) % for CV-22 . Mo likely cause of this difference is the time transgressiveness of the sampling procedure, and is 3.2. Results From Monthly Data discussed in more detail below.

[17] The interpolated monthly data from these corals displays a clear seasonal signal (Figure 3), 3.3. Results From Annually Averaged Data 18 with an average absolute annual O range [19] Over the period of calibration, these corals of 0.5–0.6%. When compared to the average track SST with annually averaged 18O, but with annual temperature span of 5.4°C, this represents some variability. Using the composite annual aver-

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Table 1. Selected Published Values for the Relationship Between 18O and SSTa Growth Rate, Study Species mm/yr a b N r2

Epstein et al. [1951] bivalves, gastropods, – 11.88 5.91 13 – and brachiopods Epstein et al. [1953] bivalves, gastropods, – 16.5 4.3 21 – and brachiopods Weber and Woodhead [1972]b Favia sp. – 6.38 4.18 164 – Galaxea sp. – 7.91 4.00 71 – Porites sp. – 11.21 3.31 421 – Pocillopora sp. – 9.05 3.82 224 – Montipora sp. – 12.82 3.41 234 – Acropora sp. – 12.24 3.57 835 – Stylophora sp. – 9.19 4.54 102 – Dunbar and Wellington [1981] Pocillopora damicornis 36 7.0 3.6 – – Weil et al. [1981] Pocillopora damicornis 17 3.76 4.29 25 0.79 Montipora verrucosa 19 3.58 4.61 19 0.74 Wellington and Dunbar [1995] Porites lobata – 0.13 5.09 – 0.74 Pavona clavus – 3.29 5.54 – 0.83 Pavona gigantean – 4.26 4.42 – 0.81 Leder et al. [1996] Montastraea annularis 1–8 5.33 4.52 – – Gagan et al. [1998] Porites lutea 12 0.01 5.75 – 0.98 Porites lutea 25 2.37 5.29 – 0.98 Abram et al. [2001] Porites lutea 4–13 2.18 5.37 – 0.96 Bagnato et al. [2004] Diploastrea heliopora 5–6 5.60 6.67 235 0.84 (septal 18O)

a 18 18 Coefficients are written in the equation form of T(°C) = a ± b * ( Ocoral Owater). The methods used to derive the calibrations listed above vary slightly from one manuscript to another and should be considered in the comparison of the results. The reader is referred to each manuscript for specifics. b Weber and Woodhead [1972] used bulk samples for each coral and calibrated those bulk samples against the long-term average SST for that 18 locality, and did not measure Owater at the given locations. This causes a general reduction in the accuracy of their equations. The equations listed here are a small representation of the total list of numerous calibrations published in their paper.

18 ages built from the monthly data, it is evident that Ocoral more than SST on an interannual basis some of the range in calibration of these corals at [Moses et al., 2006]. the monthly level is propagated to the annual averages. While SAL-6t2AnnAvg has a reasonable 3.4. Results From Annual Data SST – 18O calibration slope of 3.38 (±1.69) 1 [20] Annual samples were only taken in corals °C % , the neighboring parallel transect, SAL-6t3 (about 1 cm away in the same slab), SAL-6 and CV-22. Each annual sample was split AnnAvg for duplicate analyses, and the difference between has an annually averaged slope of 0.41 (±0.83) 1 replicates was within machine precision. Neither °C % .SAL-4AnnAvg has a slope of 2.53 1 SAL-6 or CV-22 showed any relationship (±0.92) °C % , which is similar to the slope Ann Ann 18O and SST. The slopes are 0.03 of the monthly samples, but with a tighter corre- between (±0.70) C %1 and 0.10 (±0.38) C %1 for lation. As the most severe example of an unor- ° ° SAL-6Ann and CV-22Ann, respectively. For both thodox calibration in these corals, CV-22AnnAvg 2 actually expresses a positive SST – 18O slope of nearly horizontal calibration slopes the r -value is 1 <0.01. This lack of a significant relationship is 2.02 (±1.44) °C % (Table 2). The monthly oxygen isotope values were negatively correlated likely a result of the temporally imprecise nature of with SST as expected, but the annually averaged bulk sampling. Overall, annual samples in these values of that same monthly data yields a notably particular slow-growing corals fall well out of the positive correlation. This is possible to explain range of other published values (Figure 6). because the seasonal SST signal is much greater 18 than the difference in mean annual SST from one 3.5. A Robust SST– O Calibration year to the next. The positive slope is likely [21] When we applied modified sampling techni- caused by environmental factors that effect ques to the three colonies and multiple transects

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18 Figure 4. SST – O calibrations for CV-22Mo and SAL-4Mo. Axes are on the same scale. Calibration equations are listed in Table 2. Dashed red lines represent the 95% confidence interval for the regression line. within colonies, all sampled at the monthly scale ing species that are available in order to gain the (N = 2158), a robust SST – 18O calibration can best temporal resolution. In the Pacific, corals be proposed for Siderastrea radians (Figure 7; from the genus Porites are the most commonly Table 2): used [Gagan et al., 1994; Linsley et al., 2004; SSTðCÞ¼12:56ð1:20Þ3:86ð0:39Þð Þð1Þ McCulloch et al., 1994; Watanabe et al., 2003; c w Weber and Woodhead, 1972; Wellington and The slope of this equation is actually very similar Dunbar, 1995]. The skeletal structure of Porites to other published values [Abram et al., 2001; is small enough that it is impossible to sample a Bagnato et al., 2004; Dunbar and Wellington, single corallite or skeletal element by convention- 1981; Epstein et al., 1951, 1953; Gagan et al., al microdrilling techniques. Accurate subannual 1998; Leder et al., 1996; Watanabe et al., 2003; sampling of Porites for 18O is thus inherently Weber and Woodhead, 1972] (Table 1). dependent on the fast extension rate to ensure monthly or better sampling resolution. 4. Discussion [23] In the Caribbean and Atlantic, the coral of choice for isotope studies has classically been 4.1. Considerations for a Record Retrieved Montastraea sp. [Dodge and Lang, 1983; from S. radians Fairbanks and Dodge, 1979; Goreau, 1977; Leder 18 [22] In the past, calibration studies for coral O et al., 1991, 1996; Swart et al., 1996]. Extension thermometers have typically used the faster grow- rates for Montastraea sp. in the Caribbean and

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18 Figure 5. SST – O calibrations for SAL-6 monthly data. When SAL-6t3Mo is calibrated only over the same length of time as SAL-6t2Mo, the slope is 4.45(±1.54) ± N = 64; r = 0.58), not statistically different from the slope of SAL-6t3Mo over the entire record. The same is true for SAL-6t5Mo [slope = 6.04(±1.97) (N = 64; r = 0.56)]. Therefore the steep slope exhibited in SAL-6t2Mo cannot be attributed to a function of the short record or the particular time span of the record. Axes are on the same scale. Calibration equations are listed in Table 2. Dashed red lines represent the 95% confidence interval for the regression line. tropical western Atlantic generally range between from the Niger and Congo rivers. Guzmań and 5–10 mm yr1 with well developed density band- Tudhope [1998] showed, similarly, that over a ing in-depths shallower than 20 m [Dodge and period from April 1991–April 1992 about 60% Thomson, 1974; Fairbanks and Dodge, 1979; of the 18O signal in S. siderea from Panama could Hubbard and Scaturo, 1985; Hudson et al., 1976]. be linked to SST and that the remaining 40% of the 18O signal was an indirect indicator of salinity. [24] In contrast, the genus Siderastrea has only S. siderea has also been reported to suffer from been used as a source of climate records in a few ‘‘significant and unexplained between-colony’’ cases [Guzmań and Tudhope, 1998; Swart et al., 18 18 variations in O records [Guzmań and Tudhope, 1998]. Swart et al. [1998] used a 65-year O 1998]. It is likely that much of the ‘‘unexplained’’ record from Siderastrea sp. as a means of recon- variability seen by Guzmań and Tudhope [1998] structing rainfall records in the Gulf of Guinea and between colonies resulted from their coarse sam- 18 showed that their O record was dominated by pling method which involved sample sizes of 1 mg the annual salinity signal created by river discharge

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Table 2. Results of This Study for Values for the Relationship Between 18O and SST in Siderastrea radiansa Growth Rate, Sampling Scheme Species/Coral ID mm/yr a (S.D.) b (S.D.) N r2

Monthly Siderastrea radians 1–2 SAL-4 18.32 (±1.01) 1.96 (±0.33) 882 0.11b SAL-6t2c 2.48 (±5.71) 8.90 (±1.85) 64 0.59b SAL-6t3c 11.11 (±1.54) 4.23 (±0.49) 588 0.30b SAL-6t5c 5.98 (±2.30) 6.39 (±0.79) 276 0.45b CV-22 15.48 (±1.68) 2.90 (±0.59) 348 0.19b Annual averages SAL-4 24.32 (±1.18) 0.03 (±0.39) 74 0.01 SAL-6t2c 9.05 (±16.19) 5.09 (±4.36) 6 0.71d SAL-6t3c 22.97 (±2.64) 0.41 (±0.83) 49 0.02 SAL-6t5c 19.90 (±4.56) 1.57 (±1.51) 23 0.18d CV-22 29.32 (±4.18) 2.02 (±1.44) 29 0.20d Best fit calibration All samples 12.56 (±1.20) 3.86 (±0.39) 2,158 0.26b

a 18 18 Coefficients are written in the equation form of T(°C)=a±b*( Ocoral Owater). b Significant at the 99% confidence interval. c These three transects were drilled parallel to each other over a total distance of about 1.5 cm in the same coral slab. d Significant at the 95% confidence interval.

(±0.30 mg) of CaCO3 per sample. This would half of the desired monthly proxy resolution. likely have similar effects to the annual sampling Periodic burial by sediment directly interferes with method of this study where much of the analyzed the growth of corals [Corte´s and Risk, 1985; sample is actually time-transgressive, that is to say, Dodge and Vaisnys, 1977; Rice and Hunter, not limited to a single, discrete time interval. 1992; Riegl, 1995]. Indeed, sublethal burial in

[25] Weber and Woodhead [1972] asserted that the majority of the difference in SST – 18O calibrations were found between corals in different genera rather than just between different species. However, there are considerable morphological and ecological differences between S. radians and S. siderea that could be a concern for proxy records. Most notably, the morphology of the Cape Verde S. radians is flat and pavement-like [Laborel, 1974; Moses et al., 2003], which leads to frequent burial in sediment, whereas S. siderea is typically hemispherical to spherical, often rising 0.5 m or more above the substrate. This is exemplified by the extension rate for S. siderea of 3–7 mm yr1 in a similar depth range [Guzma´n and Tudhope, 1998; Hubbard and Scaturo, 1985] which is an average of 385% faster than the growth rate reported in this study for S. radians from the Cape Verde Islands. Figure 6. Ranges of calibration slopes for SST to 18O generated by different sampling and analytical scales. 4.2. Possible Environmental Complications The horizontal shaded box represents the range of in the Cape Verde Islands published and generally accepted values for the calibration of coralline 18O values and SST. In some [26] The periodic complete burial of these corals in cases, positive correlations slopes were obtained sediment due to the high energy conditions around between 18O and SST. While seemingly incorrect, the Cape Verde Islands could have an unknown 18 one possibility is that these positive relationships are effect on their O record. Colonies of S. radians derived at annual and annual average sampling scales were shown by Rice and Hunter [1992] to be able where interannual salinity variations could be the to survive longer than two weeks of complete dominant influence on the coral skeletal 18O instead burial (LT50 = 13.6 days), a period of time about of SST. 9of14 Geochemistry Geophysics 3 moses et al.: calibration of stable oxygen isotopes 10.1029/2005GC001196 Geosystems G

Figure 7. Robust SST – 18O calibration slope for Siderastrea radians. The slope resulting from modified methods is very similar to, though vertically offset from, other published relationships. The solid black line through the data points is the calibration for this report. Dashed red lines represent 95% confidence interval on the calibration. The dashed black lines represent the other published calibrations as labeled. See footnotes in Table 1 regarding other published calibrations.

S. radians has been demonstrated to be manifested Verde Islands. Considering the reported ability of in reduced radial growth rates in Florida [Lirman et Siderastrea to record salinity variations [Guzma´n al., 2003]. Repeated burial and excavation during and Tudhope, 1998; Swart et al., 1998], it is the year could thus be expected to cause the slow- possible that even minimal interannual variability ing or cessation of extension for the given time in the SSS, on the order of ±0.1–0.2 psu, could intervals, making the assignment of a discrete date be corrupting the SST – 18O relationship at the to a particular isotope value nearly impossible even annual and interannual scales resulting in the with sampling at a higher resolution than was used apparent lack of correlation [Moses et al., 2006]. in this project. Focused investigation into the effects of such burial on coral skeletal geochemical 4.3. Time-Transgressive Nature of records would be an important contribution to this Sampling field. [28] One limiting constraint on the sampling of [27] Another possible complication could be salin- coral skeletons with a drill, or even a microdrill, ity variability, which would affect the oxygen arises from the complicated three-dimensional isotope record of the coral skeleton [Epstein and nature of coral skeletal architecture. Sampling a Mayeda, 1953; Swart and Coleman, 1980]. The particular location in a coral skeleton with a drill Cape Verde Islands are a dry archipelago in gen- in an attempt to obtain a sample from a discrete eral, and the island of Sal, where these corals were time interval actually incorporates skeletal mate- collected, has little or no terrestrial freshwater rial deposited over a range of time. This sampling runoff. Recently, Curry et al. [2003] have proposed of a range of time can be referred to as the the idea of secular changes in sea surface salinity sampling being ‘‘time-transgressive.’’ (SSS) in the western tropical and subtropical At- lantic based on 40 years of instrumental data. [29] The time-transgressive nature of sampling Sclerosponges (Porifera:Sclerospongea, a type of corals and other biological accretionary skeletons cryptic, calcifying sponge) from the Bahamas sup- is a factor that may often be easily overlooked, but port this assertion with proxy records recording needs to be recognized as a limiting constraint on substantial salinity variations at depths below the minimal resolution of the paleo-proxy derived 100 m [Rosenheim et al., 2005]. Unfortunately, from that organism. In S. radians and other slow- there is no coherent record of SSS in the Cape growing corals, this problem becomes more significant than it is in corals with faster extension rates.

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[30] To properly record approximately monthly [33] To further complicate the problem, the coral values, more than 12 samples should be taken per slabs that researchers work with are not the two year in order to insure that at least one relatively dimensional objects they are often considered to discrete sample is taken for each monthly period of be. Instead, the coral slab which is being drilled is time. It has been shown that in order to measure the actually a complex three dimensional structure of full amplitude of the subannual range in SST (and skeletal elements and polyp growth ‘‘tracts.’’ As a other environmental parameters) that the number of result, the time-transgressive nature of the drilling samples per year is directly proportional to the occurs in the full three dimensions (Figure 8). The relative fraction of the total amplitude that is sample can be simultaneously time-transgressive in recorded [Leder et al., 1996]. Leder et al. [1996] the direction of the drill tract and in two more were able to achieve the best representation of the orthogonal dimensions. full amplitude in the 18O derived SST signal by drilling 50 samples yr1. One reason they needed [34] As an example, SAL-6 was microdrilled at monthly such a high sample density was the roughly 10°C resolution twice (SAL-6t2Mo and SAL-6t3Mo). These range in south Florida SST. The annual SST range two parallel transects were only about 1 cm apart, but in Cape Verde is about half that amount, so it is the calibrations calculated from each varied widely likely the full 18O amplitude could be retrieved at from one another (Figure 3). The most likely a rate of fewer than 50 samples yr1. explanation for this is the time-transgressive effect of the sampling. Even at the 104 m step [31] However, in Cape Verde S. radians a rate of increment used here, it is likely that in the two even 25–30 samples yr1 would be impossible to transects the percent ‘‘month composition’’ of a achieve. Micromilling 30 samples yr1 in this specific month varied from one transect to the species would require a step increment of 40 m, next. The ‘‘monthly’’ intervals that were sampled well below the useful range of the micromill for in these two transects actually extracted some this procedure. The drill mechanism, itself, is CaCO3 belonging to the previous and following capable of 1 m step increments, however such months. accuracy in drilling in one dimension (x) is wasted in the other two (y and z). Even if the drill bit were [35] Hypothetically, a sample designated as March not time-transgressive by itself at a 40 m step in the first transect may have contained, in addition interval (x), the lateral extent (y) or depth (z) of to skeletal material from March, 20% material from February, and 10% material from April. Then, drilling required to produce enough CaCO3 powder to analyze by mass spectrometry would make the because of the small scale skeletal structures and extreme precision in the growth direction mean- three-dimensionality of the coral skeleton, the ingless. Herein lies the limiting resolution of this neighboring transect sample for the same March species of coral, and others like it with slow may have consisted of 5% February and 20% extension rates. April. The result would be a calibration for the first transect that leaned toward a ‘‘cooler’’ SST – 18 [32] At the annual sampling scale, it is easy to see O relationship than the second transect sample that as much as 20–30% (exact amount will vary which consisted of a higher percentage of skeleton based on size and shape of the drill bit) of the deposited during warmer SSTs (Figure 9). sampled skeletal material may be from the previous or following year, rather than strictly limited to the 4.4. Minimizing Time Transgression and target year. Even with a fine-scale drill bit, and a Calibration computer controlled step motor that is accurate at micrometer scale, time-transgressive sampling is [36] Our modified methods described in section 2.2 unavoidable (Figure 8). While this issue is unnoticed provide one alternative to minimizing the time in faster growing corals like Porites or Montastraea, transgression of sampling by micromill. By sam- where it is easy to take >25 samples yr1, the pling along growth surfaces, and only over a effect becomes progressively more pronounced in minimal length of growth surface, each sample in corals with slower growth rates, as in S. radians. S. radians is less time-trasngressive than samples Attempting to sample at a step interval below the attempted to be taken from individual skeletal resolution of the coral, when each of those components. For other corals, the best method for samples is time-transgressive, produces less accu- minimizing time transgression will vary dependent rate ‘‘smeared’’ data instead of the desired higher on the sampling mechanism (drill bit diameter, resolution results. minimum step increment, etc.) and the skeletal structure of the species of coral.

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Figure 8. Time-transgressive sampling is a function of the size and shape of the drill bit and the growth rate of the coral. This simple illustration is set to the relative scale of microdrilling S. radians. The alternating dark and white bands represent theoretical ‘‘monthly’’ growth intervals of approximately 100 m. Their zigzag pattern is tied to centers of calcification in the septa of S. radians. Notice that even with a modest depth of penetration (here shown as 150 m), the drill bit begins to sample a volume that is time-transgressive. Thus the sample that is analyzed in the mass spectrometer is truly representative of a time segment longer than the target interval (in this case, one month) or offset from the target time interval. The full height and width (5 mm 100 mm) of the coral slab have been greatly reduced here for the purpose of illustration. The schematic of the volume removed is enlarged for detail and is at a different scale than the rest of the drawing. After the initial sample taken by the microdrill, the subsequent samples created by continuous milling have the shape and dimensions shown here in the volume removed and are not actually the rectangular boxes they are often considered to be.

18 [37] The calibration of Ocoral to SST for a coral the recovery of a well calibrated SST record from is expected to be robust. That is to say, calibrations these S. radians are the unusually slow extension rate should be applicable to the same species in similar coupled with the time-transgressive nature of tradi- environmental conditions, and/or geographic tional drilling and microsampling methods. Recov- ranges, and/or time periods. In addition to using ery of a reliable SST signal depends on a modest the modified technique of sampling along growth subannual sampling rate (10–15 samples yr1)in surfaces described here, the final calibration pro- the least time-transgressive means possible. We have posed for S. radians in equation (1), is based on shown results that sampling rates of less than more than a single transect or a single core. This 4 samples yr1, or higher than 15 samples yr1, further helps to minimize the effects of time- produce unreliable or inaccurate SST – 18O cali- transgressive sampling on the final calibration. brations. In addition, drilling along skeletal growth surfaces, rather than restricting to a specific skeletal 5. Conclusions element (i.e., a thecal wall), minimizes the time transgressiveness of the sampling. In the case of the

38 Cape Verde Islands, the possibility of secular salin- [ ] This work has demonstrated that techniques 18 which are sufficient or efficient for the analysis of ity variations masking the expected SST – O geochemical proxies in other, faster growing spe- relationship adds another complication for proper cies of corals have proven ineffective for use in calibration. However, with care for sampling these slow growing corals, and an understanding slow-growing Siderastrea radians from the Cape 18 Verde Islands. The primary limiting factors against of the environmental influences on their O

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Figure 9. Results of time-transgressive sampling model. This figure represents 20 runs of a simple model simulating a recovery of 50–70% of the total sample from the target interval. The remaining amount is recovered from the preceding and following intervals. All amounts are calculated randomly. Model input is actual Cape Verde SST. The vertical separation of the highest and lowest values at a given point (such as #25) represents the actual range @SST of error (1.5°C) that could be expected. Error in SST measurement is worst where the absolute value of @t is greatest, such as during the late spring or late fall. records, it is possible to retrieve robust proxy Dodge, R. E., and J. C. Lang (1983), Environmental correlates records from S. radians in areas where there are of hermatypic coral (Montastrea annularis) growth on the East Flower Gardens Bank, northwest Gulf of Mexico, Lim- few other sources for high resolution biogenic nol. Oceanogr., 28, 228–240. proxy records. Dodge, R. E., and J. Thomson (1974), The natural radioche- mical and growth records in contemporary hermatypic corals from the Atlantic and Caribbean, Earth Planet. Sci. Lett., 23, Acknowledgments 313–322. Dodge, R. E., and J. R. Vaisnys (1977), Coral populations and [39] This research was supported by the NSF (OCE0081770; growth patterns: Responses to sedimentation and turbidity P.K.S.) and the Mary Roche Fellowship (C.S.M.). Special associated with dredging, J. Mar. Res., 35, 715–730. thanks go to K. Helmle for assistance in fieldwork and core Dunbar, R. B., and G. M. Wellington (1981), Stable isotopes in preparation, and the staff of the SIL for assistance with branching coral monitor seasonal temperature variation, Nat- analysis. Great appreciation goes to the staff of Instituto ure, 293, 453–455. Nacional de Desenvolvimento da Pesca (INDP) of the Cape Enfield, D. B., and D. A. Mayer (1997), Tropical Atlantic sea surface temperature variability and its relation to El Nin˜o- Verde Islands, and especially S. Merino and O. Melı´cio, for Southern Oscillation, J. Geophys. Res., 102, 929–945. their assistance with sample collection. The authors also thank Enfield, D. B., et al. (2001), The Atlantic multidecadal oscilla- A.C.C., D.B.E., and L.C.P. for their critical reviews of this tion and its relation to rainfall and river flows in the con- manuscript. tinental U.S., Geophys. Res. Lett., 28, 2077–2080. Epstein, S., and T. K. Mayeda (1953), Variation of the O18 content of waters from natural sources, Geochim. Cosmo- References chim. Acta, 4, 213–224. Epstein, S., et al. (1951), Carbonate-water isotopic temperature Abram, N. J., et al. (2001), Biological response of coral reefs scale, Bull. Geol. Soc. Am., 62, 417–426. to sea surface temperature variation: Evidence from the Epstein, S., et al. (1953), Revised carbonate-water isotopic raised Holocene reefs of Kikai-jima (Ryukyu Islands, Japan), temperature scale, Bull. Geol. Soc. Am., 64, 1315–1326. Coral Reefs, 20, 221–234. Erez, J. (1978), Vital effect on stable-isotope composition Bagnato, S., et al. (2004), Evaluating the use of the massive seen in foraminifera and coral skeletons, Nature, 273, coral Diploastrea heliopora for paleoclimate reconstruction, 199–202. Paleoceanography, 19, PA1032, doi:10.1029/2003PA0000935. Fairbanks, R. G., and R. E. Dodge (1979), Annual periodicity Corte´s, J. N., and M. J. Risk (1985), A reef under siltation of the 18O/16O and 13C/12C ratios in the coral Montastrea stress, Cahuita, Costa Rica, Bull. Mar. Sci., 36, 339–356. annularis, Geochim. Cosmochim. Acta, 43, 1009–1020. Curry, R., et al. (2003), A change in the freshwater balance of Gagan, M. K., et al. (1994), High-resolution isotopic records the Atlantic Ocean over the past four decades, Nature, 426, from corals using ocean temperature and mass spawning 826–829. chronometers, Earth Planet. Sci. Lett., 121, 549–558.

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