G 3. AN ELECTRONIC JOURNAL OF THE EARTH SCIENCES Published by AGU and the Geochemical Society

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1 Geosystems G 3 AN ELECTRONIC JOURNAL OF THE EARTH SCIENCES Published by AGU and the Geochemical Society Article Volume 5, Number 5 7 May 2004 Q05001, doi: ISSN: High-resolution Sr/Ca records in modern Porites lobata corals: Effects of skeletal extension rate and architecture Nicola Allison and Adrian A. Finch School of Geography and Geosciences, University of St. Andrews, Irvine Building, North Street, St. Andrews, Fife KY16 9AL, UK (na9@st-andrews.ac.uk) [1] We used ion microprobe analysis to determine the Sr/Ca composition of fasciculi (deposited during the day) and centers of calcification (COCs, deposited at night) across transects of two Porites lobata corals, of different linear extension rates, from Oahu, Hawaii. The COCs of both corals contained significantly higher Sr/Ca than the fasciculi (at the 95% confidence level). We observed no significant differences between the Sr/Ca ratios of the fasciculi (or of the COCs) of the fast and slow growing corals, and we conclude that variations in the extension rate of each colony have not affected Sr incorporation in these corals. The fasciculi and COCs in both corals exhibit large Sr/Ca heterogeneity, which is not temperature dependent. Our data do not support the hypothesis that COC analyses provide a SST signature which is unaffected by biological or kinetic effects. The heterogeneity of both features may reflect short-term (daily to weekly) variations in calcification rate which are known to occur during the day and night and which influence the relative transport rates of Sr and Ca through the coral tissue. We plotted running means through the fasciculi and COC chronologies and compared maximum and minimum Sr/Ca values in each annual cycle with the corresponding minimum and maximum mean sea surface temperature (SST) values (calculated over equivalent time periods). We found that the constants C and M of the linear equation Sr/Ca = C + (M SST) became smaller as the time interval used to calculate the running means increased from 1 day to 77 days. This decrease in C and M reflects the gradual removal of the short-term Sr heterogeneity (dependent on biological and/or kinetic processes) from the data set as progressively larger numbers of data points are used to calculate the Sr/Ca running mean. We hypothesize that variations in M and C between different published Sr/Ca-SST calibrations may reflect the relative importance of biological or kinetic processes in corals at different locations. Components: 4886 words, 8 figures, 1 table. Keywords: coral; Sr/Ca; skeletal extension rate; sea surface temperature. Index Terms: 1065 Geochemistry: Trace elements (3670); 4267 Oceanography: General: Paleoceanography; 4875 Oceanography: Biological and Chemical: Trace elements. Received 23 January 2004; Revised 4 March 2004; Accepted 23 March 2004; Published 7 May Allison, N., and A. A. Finch (2004), High-resolution Sr/Ca records in modern Porites lobata corals: Effects of skeletal extension rate and architecture, Geochem. Geophys. Geosyst., 5, Q05001, doi:. 1. Introduction [2] Tropical coral skeletons indicate great promise as proxies of past sea surface temperatures (SSTs) as the geochemistry of the skeleton encodes the environment at the time of skeletal deposition. SSTs have been inferred from the Sr/Ca ratios of coral aragonite [e.g., Beck et al., 1992; Beck, 1994] Copyright 2004 by the American Geophysical Union 1 of 10

2 and recent analysis of fossil corals has been used to estimate past SSTs [Gagan et al., 1998; McCulloch et al., 1999]. However, reported palaeothermometer relationships may vary significantly between corals from the same [de Villiers et al., 1995] and different sites [Marshall and McCulloch, 2002]. These differences are caused by biological and/or kinetic effects, which offset the skeletal Sr/Ca from equilibrium values. [3] Corals precipitate skeleton throughout the day and night but calcification follows a diurnal pattern with large variations in calcification and skeletal extension rates, associated with differences in crystal shape and deposition site [Gladfelter, 1983; Marshall and Wright, 1998]. During the night, small (approximately micron sized) equant randomly orientated crystals are deposited at the axial spines of the corallite [Gladfelter, 1983]. These probably form centers of calcification (COCs) [Cohen et al., 2001]. During the day, larger needles shaped crystals are deposited over all surfaces of the precipitating skeleton, in bundles [Gladfelter, 1983] to form fasciculi. The Sr/Ca composition of skeleton deposited during the day is significantly different from that deposited at night, and Cohen et al. [2001] suggest that biological and kinetic effects may be minimized in night material. [4] In this paper we present a study of Sr/Ca variations across fasciculi and COCs along transects of 2 modern Porites lobata coral skeletons which had been deposited at different rates. The impact of skeletal extension rate on Sr incorporation is unclear, and some studies report higher Sr/Ca ratios in slower growing corals [e.g., de Villiers et al., 1995], while others report no significant differences [e.g., Alibert and McCulloch, 1997; Gagan et al., 1998; Mitsuguchi et al., 2003]. It is especially important to constrain the effect of skeletal growth rate on Sr incorporation as fossil corals deposited during cool glacial periods may have lower skeletal extension rates than their modern analogues. 2. Methods and Materials [5] Analyses were performed on heads collected from 2 large (>2 m in diameter) Porites lobata colonies at Lanikai, Oahu, Hawaii in July The two colonies were 10 m apart and both occurred in 2 m depth of water. The skeletons were immersed in 3 4% sodium chlorate(i) solution for 2 hours immediately after collection to remove the coral tissue, rinsed with distilled water, dried and returned to the UK for analysis. The heads were sectioned along the axis of maximum vertical growth into 10 mm thick slices and X-rayed to record density banding patterns. Thin sections were prepared from strips that ran from 0 50 mm and 0 18 mm from the growth surface in the fast and slow growing corals, respectively. High-density band deposition begins in approximately September October in these corals [Schneider and Smith, 1982] and the X-radiographs indicated that these strips spanned 4.5 years (from early 1996-summer 2000) in the fast growing coral and 3.5 years (from early 1997 summer 2000) in the slow growing coral. Sections were fixed in epoxy resin, mounted onto 2.5 cm diameter glass slides and ground to a thickness of 50 mm. Parallel tracks were analyzed along each strip following fasciculi and centers of calcification. Fasciculi and COCs can be readily identified in thin section and the high spatial resolution of ion microprobe analysis allows their independent analysis. COCs may appear as dark spots or lines along the centers of the trabeculae when viewed in transmitted light [Wells, 1956; Wainwright, 1964; Jell, 1974]. We carefully selected suitable areas for analysis (Figure 1), avoiding microborings, and selecting COCs that intersected the surface of the sample. As a result spatial intervals between successive analyses were uneven. The average distances between successive fasciculi and COC analyses were 120 and 250 mm, respectively, in the fast growing coral and 60 and 200 mm, respectively, in the slow growing coral. These distances equate to a fasciculi analysis about every 4 days in both corals and COC analyses every 8 and 14 days in the fast and slow growing corals, respectively. [6] Sr/Ca ratios were determined using a Cameca ims-4f ion microprobe. Thin sections were gold coated and analyzed with a 16 O ion beam, accelerated at 14.5 kev. Instrument conditions were primary beam current = 6 na, energy offset = 2of10

3 Figure 1. Transmitted light micrograph of a thin section showing ion microprobe analyses on fasciculi (left-hand analysis) and on a COC (right-hand analysis). The primary beam produces a burn mark with a diameter of up to 25 mm, but the majority of ions are sputtered from the central 10 mm, where the most intense burn mark is produced. Use of a field aperture limits the collection of secondary ions to those sputtered from this central area. 75 ev, imaged field = 25 mm, field aperture 2(85mm) and contrast aperture 2 (150 mm). The analytical diameter was 10 mm. We used a preanalysis burn-in time of 3 min to remove surface contamination. Each analysis is the sum of ten cycles and for each cycle we collected secondary ions at masses 44 Ca (counting time 2 s) and 88 Sr (counting time 4 s). Count rates were approximately cps and cps, respectively. The total time per analysis (including other isotopes not reported here) was 6 min and during this time the primary beam sputtered the sample to a depth of 2 mm. Internal reproducibility (the Sr/Ca precision at a single point) was calculated from the standard deviation (s) of the ten cycles in each analysis divided by p 10 and was typically 0.5%. External reproducibility (the precision of ten analyses on the standard) was typically 0.3%. The relative ion yield of Sr to Ca was estimated after Figure 2. Sr/Ca of individual fasciculi and COC analyses along transects of (a) a fast growing and (b) a slow growing Porites lobata coral. Note that both y axes on each graph are plotted on the same scale but are offset for clarity. 3of10

4 Figure 3. Enlarged section of Figure 2 covering an approximate 8 month period of skeletal growth in the fast growing coral. Individual fasciculi analyses are represented by the symbols and the thin line. A 9 point running mean (approximately monthly) is indicated by the thick line. multiple analyses on the carbonate standard OKA carbonatite (Sr/Ca = 13.1 mmol mol 1 ). 3. Results and Discussion 3.1. Sr/Ca Heterogeneity [7] The fasciculi and the COCs profiles of both corals exhibit large Sr/Ca fluctuations, which are deposited approximately days apart, over distances of mm (Figure 2). Fluctuations are typically 0.6 mmol mol 1 in the fasciculi of both corals and 0.5 and 0.3 mmol mol 1 in the COCs of the fast and slow growing corals, respectively. The Hawaiian Institute of Marine Biology (HIMB) monitors seawater temperature hourly at 1.5 m water depth in Kaneohe Bay (10 km from the sampling site at Lanikai). SST measurements at Kaneohe Bay and the coral sampling site throughout July 2000 indicate that the temperatures are in good agreement (within <1 C). The HIMB data indicate that the annual range of average daily temperatures is usually 5 C and that seawater temperature variations over weekly periods are usually <1.0 C. The sensitivity of coralline Sr/Ca to temperature change is typically mmol mol 1 C 1. While adjacent analyses may be deposited under subtly different temperatures, the small scale Sr heterogeneity observed here cannot be solely dependent on variations in SST. Similar heterogeneity has been reported in other corals [Hart and Cohen, 1996; Allison, 1996; Cohen et al., 2001; Meibom et al., 2003] and must reflect biological or kinetic processes during skeletal deposition. The origin of this heterogeneity is as yet unknown however a suitable hypothesis may be found in the recent observation that skeletal Sr incorporation is inversely related to calcification rate [Ferrier-Pages et al., 2002]. Sr and Ca may be transported to the calcification site by different pathways [Ip and Krishnaveni, 1991; Ip and Lim, 1991] and their relative transport rates vary in response to calcification rates [Ferrier-Pages et al., 2002]. Day calcification rates vary in response to changes in irradiance [e.g., Marubini et al., 2001], while night calcification rate varies during the nightly cycle [Vago et al., 1997]. Both day and night calcification rates are affected by zooplankton availability [Houlbreque et al., 2003]. Skeletal extension rates are 30 and 15 mm night 1 in the fast and slow growing corals, respectively, and as the bulk of calcification occurs in the day [Barnes and Crossland, 1980], it is likely that the spatial resolution of ion microprobe analysis (10 mm) allows sampling of <1 day s skeletal growth in 4of10

5 Figure 4. (a) Sr/Ca-SST calibrations, from the fasciculi analyses in the fast growing coral, calculated by plotting runnng means through the Sr/Ca and SST data over different time periods. (b) Plot indicating how the slope (M) and intercept (C) of the Sr/Ca-SST calibration decrease as the time interval used to calculate the running means increased. Approximate time intervals are indicated, in days, next to each point. the fasciculi and COCs of both corals. We propose that the short-term Sr/Ca heterogeneity reflects short-term (daily to weekly) variations in skeletal growth rate during both the day and the night. The large Sr/Ca heterogeneity in the COC analyses in this study is in marked contrast with a previous study which reported a relatively small Sr/Ca range in COC analyses [Cohen et al., 2001]. Our record has a higher density of COC analyses than the previous report and we confirmed that a COC was present at the sample surface for each analysis. Our data do not support the conclusion that COC analyses provide a SST signature which is unaffected by biological or kinetic effects and we conclude that there are similar challenges in reconstructing SST records from night carbonate as from day carbonate. [8] We did not observe clear approximately monthly oscillations in Sr/Ca (Figure 3), previously reported by Meibom et al. [2003]. Our sampling frequency (9 analyses month 1 in the fasciculi of both corals) may have been insufficient to detect monthly cycles, particularly as substantial Sr/Ca heterogeneity (>1 mmol mol 1 ) is also superimposed on the monthly cycle [Meibom et al., 2003]. [9] To investigate if the short-term Sr/Ca heterogeneity could be smoothed into a credible SST signal, we plotted running point means through the fasciculi and COC chronologies, calculating the average of successively larger number of data points. We compared maximum and minimum Sr/Ca values in each annual cycle with the corresponding minimum and maximum SST values, calculated by plotting running means through the SST data over equivalent time periods. We found that the relationship between skeletal Sr/Ca and SST changed and the constants C and M of the linear equation Sr/Ca = C + (M SST) became smaller as the number of points used to calculate the maxima and minima increased (Figures 4a and 4b). We observed decreases in the constants C and M of the Sr/Ca-SST equation derived from the fasciculi of the fast coral as the approximate time interval used to calculate the Sr/Ca and SST running means increased from 1 day to 77 days. Increasing the time interval used to calculate the running means beyond this did not significantly decrease M or C. The decrease in C and M reflects the gradual removal of short-term Sr heterogeneity from the data set as progressively larger numbers of data points are used to calculate the Sr/Ca running mean. If only a few points are used to calculate the running mean then the short period fluctuations in the Sr/Ca data set exaggerate the maximum and minimum Sr/Ca values. Maximum and minimum Sr/Ca values reflect the combined effects of SST and biological and/or kinetic processes. As more points are used to calculate the running mean the short period fluctuations become dampened and the effect of SST on maximum and minimum Sr/Ca becomes progressively more important. [10] We observed a similar pattern in the COCs and fasciculi of both the fast and slow growing corals 5of10

6 Figure 5. Plot of the slope (M) and intercept (C) for several Sr/Ca-SST calibrations for Porites corals (points), indicating the temporal resolution of the Sr/Ca and SST data. Sources: 1, Shen et al. [1996]; 2, Schrag [1999]; 3 5, Marshall and McCulloch [2002]; 6 (weekly), Alibert and McCulloch [1997]; 7 (monthly), Beck et al. [1992]; 8, Fallon et al. [1999]; 9, Gagan et al. [1998]; 10, de Villiers et al. [1994]. The relationship observed in the fasciculi of the fast growing coral in this study is also shown (solid line). and minimum values of C and M occurred when the running means were calculated over days in each chronology. The decrease in C and M over this time interval may indicate that the Sr heterogeneity has an approximately monthly - 2 monthly periodicity. Calculating the running mean over an approximately 2 monthly period will remove any Sr heterogeneity which has a cyclical amplitude of this period. An approximately monthly cyclicity would be consistent with the observations of Meibom et al. [2003]. [11] Coral calcification processes may vary on daily (as already discussed), monthly and yearly timescales. For example, dissepiments are deposited on approximately monthly timescales. Dissepiments are thin sheets (10 mm thick) of crystals which are deposited approximately 2 4 mm from the coral skeleton surface and parallel to it. They seal off the bulk of the skeleton from the uppermost layer which is occupied by the coral tissue. During dissepiment deposition normal calcification processes may be suspended (M. le Tissier, personal communication, 2002). In addition, systematic changes in the light available to the coral may occur as tidal changes in water height affect light transmission. Pairs of dense and less dense bands are deposited approximately yearly in many corals reflecting variations in calcification in response to changes in water temperature or light availability. Finally, Porites corals may spawn at approximately monthly or yearly intervals [Richmond and Hunter, 1990] and changes in the coral metabolism at this time may divert resources away from calcification. [12] Marshall and McCulloch [2002] reported a similar relationship between the slope of the calibration equation (M) and the intercept (C) in different Sr/Ca-SST calibrations from Porites corals from different locations. We have reproduced some of the calibrations in Figure 5 and have indicated the temporal resolution of the Sr/Ca and SST records used to generate them. A least squares regression through these calibrations (M = * C ) is not significantly different (at the 95% confidence level) from the regression produced from the data in the current study (Figures 4b and 5). We hypothesize that variations in M and C between published calibrations may reflect the importance of biological or kinetic processes and SST on Sr incorporation in corals at different locations. We observed no obvious trend between sampling resolution of these calibrations and magnitude of M or C. However, coral calcification processes may vary significantly, even over small geographical areas. For example, Brown et al. [1986] described asynchronous deposition of dense skeletal bands in Porites lutea corals from different sites around the south east peninsula of Phuket, Thailand (over distances <1 km). They related dense skeletal band deposition to high water turbidity at each site, dependent on wind direction. We hypothesize that differences in the Sr/Ca-SST equations reported from different locations may reflect the relative importance of biological and/or kinetic processes at each site Comparing Sr/Ca Records Between Corals [13] To compare the seasonal Sr/Ca trends recorded by fasciculi and COCs in each of the corals, we have plotted Sr/Ca chronologies using the 77 day running means (Figure 6), which should remove much of the biological/kinetic heterogeneity. By matching maximum and minimum Sr/Ca values in 6of10

7 Figure 6. Smoothed (running 2 month means) Sr/Ca chronologies of fasciculi and COCs in each coral. The distance from the coral surface is plotted on a linear scale in each coral and runs from 0 to 50 and 0 to 20 mm in the fast and slow growing corals, respectively. A running 70 day mean of average daily SST values over the approximate period in which the skeletons were deposited is included. each annual cycle with corresponding SST data (Figure 7), we calculate that the Sr/Ca-SST equation for the fasciculi of the fast growing coral is: Sr/Ca = (0.080 SST). This is similar to the other published Sr/Ca-SST equation for Porites corals from Hawaii [de Villiers et al., 1994] (see Figure 7). The Sr/Ca-SST equation calculated from the fasciculi of the slow growing coral was not significantly different from this. However, the 95% confidence limits of these equations are large (e.g., for the fasciculi in the fast growing coral, Sr/Ca = ± 0.60 (0.080 ± SST), reflecting the small number of data points (6 8) used to calculate each regression. [14] We used ANOVA to test for differences in the composition of each feature in the outermost 3.5 years of skeleton in each coral. The mean Sr/Ca and 95% confidence limits are summarized in Table 1. The Sr/Ca in the COCs of both corals were significantly higher than in the fasciculi (at the 95% confidence limit). COCs are usually enriched in Sr/Ca compared to the surrounding fasciculi by mmol mol 1 (Figure 6). Average SSTs during sunlight hours are C warmer than night temperatures at this site, Figure 7. The Sr/Ca-SST relationships for fasciculi and COCs from matched Sr/Ca values and SSTs in the fast growing coral. The Sr/Ca-SST relationship previously published for Porites corals in Hawaii [de Villiers et al., 1994] is shown by the thick black line. 7of10

8 Table 1. Mean Sr/Ca Ratios (±95% Confidence Limits) of Fasciculi and COCs in Each Coral Fasciculi COCs Fast growing coral ± ± Slow growing coral ± ± however this temperature offset is insufficient to account for the Sr/Ca discrepancy between fasciculi and COCs. The bulk of calcification occurs in the day [Barnes and Crossland, 1980] and the reduction in calcification rate at night may explain the general increase in Sr/Ca ratios in night material. Alternatively, crystal habit (shape) is markedly different between the fasciculi (acicular crystals) and the COCs (equant crystals). The selective partitioning of trace elements onto different crystal faces is well established in many mineral systems. For example, Paquette and Reeder [1995] showed that Sr had different distribution coefficients for different faces in calcite at similar crystal growth rates (10 40 mm day 1 ) to those of corals. The incorporation of Sr is controlled by the density of dislocations on the growing crystal surface, which vary from face to face and as crystal growth rate changes [Paquette and Reeder, 1995]. Such behavior means that calcite crystals formed with different habits under the same conditions will have different Sr contents. Aragonite, like calcite, is a dominantly ionic solid and similar mechanisms may control trace element uptake. Furthermore differences in element partitioning between crystal faces in aragonite may be more marked since aragonite has a lower symmetry than calcite and therefore has potentially a greater number of crystallographically distinct crystal faces. Sr heterogeneity in aragonite speleothems has been used to infer that Sr is indeed partitioned differently between different aragonite crystal faces [Finch et al., 2003]. [15] We observed no significant differences between the mean Sr/Ca ratios of the fasciculi of the fast and slow growing corals over the outermost 3.5 years of skeleton. We also observed no significant differences between the mean Sr/Ca ratios of the COCs of the two corals. To compare the amplitude of the Sr/Ca trends in each coral, we also compared the maximum and minimum Sr/Ca ratios deposited in each annual cycle in the chronologies presented in Figure 6 (Figure 8). Again we observed no significant differences between the Sr/Ca ratios of the fasciculi (or of the COCs) of the fast and slow growing corals and we conclude that the growth rate of each colony has not affected Sr incorporation in these corals. In the previous sec- Figure 8. Maxima and minima Sr/Ca (from Figure 6) in the fasciculi and COCs in each coral over three annual cycles. 95% confidence limits are shown. 8of10

9 tion we have discussed variations in skeletal growth as a suitable hypothesis to explain Sr heterogeneity within a coral. However, adopting this hypothesis raises questions as to why different coral colonies from the same site may have significantly different skeletal growth rates but exhibit similar Sr/Ca-SST relationships. As yet it is not clear why adjacent corals may calcify at significantly different rates and how this may affect Ca and Sr transport. If Ca and Sr are transported in similar proportions, in both fast and slow growing corals, then the corals may deposit similar Sr/Ca ratios. Further work is needed to clarify these processes. Acknowledgments [16] This work was supported by UK Natural Environment Research Council grants NER/A/S/2001/00642 and NER/M/ 2000/ Access to the ion microprobe analyses was provided by NERC Scientific Services and we are indebted to Richard Hinton (University of Edinburgh) for his assistance with the analyses. We wish to thank Cindy Hunter (Waikiki Aquarium) and Ross Langston (HIMB) for field work assistance, Martin Le Tissier (University of Newcastle upon Tyne) for sharing his expertise in coral calcification processes and Fenny Cox (HIMB) for providing the HIMB SST data. We also thank Anders Meibom and an anonymous reviewer for insightful reviews. References Alibert, C., and M. T. McCulloch (1997), Strontium/calcium ratios in modern Porites corals from the Great Barrier Reef as a proxy for sea surface temperature: Calibration of the thermometer and monitoring of ENSO, Paleoceanography, 12, Allison, N. (1996), Comparative determinations of trace and minor elements in coral aragonite by ion microprobe analysis, with preliminary results from Phuket, South Thailand, Geochim. Cosmochim. Acta, 60, Barnes, D. J., and C. J. Crossland (1980), Diurnal and seasonal-variations in the growth of a staghorn coral measured by time-lapse photography, Limnol. Oceanogr., 25, Beck, J. W. (1994), Sea-surface temperature from coral skeletal strontium calcium ratios, Science, 264, 891. Beck, J. W., R. Edwards, E. Ito, F. W. Taylor, J. Recy, F. Rougerie, P. Joannot, and C. Henin (1992), Sea-surface temperature from coral skeletal strontium calcium ratios, Science, 257, Brown, B. E., M. D. A. Le Tissier, L. S. Howard, M. Charuchinda, and J. A. Jackson (1986), Asynchronous deposition of dense skeletal bands in Porites lutea, Mar. Biol., 93, Cohen, A. L., G. D. Lane, S. R. Hart, and P. S. Lobel (2001), Kinetic control of skeletal Sr/Ca in a symbiotic coral: Implications for the palaeotemperature proxy, Paleoceanography, 16, de Villiers, S., G. T. Shen, and B. K. Nelson (1994), The Sr/Ca-temperature relationship in coralline aragonite Influence of variability in (Sr/Ca) seawater and skeletal growth parameters, Geochim. Cosmochim. Acta, 58, de Villiers, S., B. K. Nelson, and A. R. Chivas (1995), Biological controls on coral Sr/Ca and d 18 O reconstructions of sea surface temperatures, Science, 269, Fallon, S. J., M. T. McCulloch, R. van Woesik, and D. J. Sinclair (1999), Corals at their latitudinal limits: Laser ablation trace element systematics in porites from Shirigai Bay, Japan, Earth Planet. Sci. Lett., 172, Ferrier-Pages, C., F. Boisson, D. Allemand, and E. Tambutte (2002), Kinetics of strontium uptake in the scleractinian coral Styophora pistillata, Mar. Ecol. Prog. Ser., 245, Finch, A. A., P. A. Shaw, K. Holmgren, and J. Lee-Thorp (2003), Corroborated rainfall records from aragonitic stalagmites, Earth Planet. Sci. Lett., 215, Gagan, M. K., L. K. Ayliffe, D. Hopley, J. A. Cali, G. E. Mortimer,J.Chapell,M.T.McCulloch,andM.J.Head (1998), Temperature and surface ocean water balance of the mid-holocene tropical western Pacific, Science, 279, Gladfelter, E. H. (1983), Skeletal development in Acropora cervicornis. II: Diel patterns of calcium carbonate accretion, Coral Reefs, 2, Hart, S. R., and A. L. Cohen (1996), An ion probe study of annual cycles of Sr/Ca and other trace elements in corals, Geochim. Cosmochim. Acta, 60, Houlbreque, F., E. Tambutte, and C. Ferrier-Pages (2003), Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata, J. Exp. Mar. Biol. Ecol., 296, Ip, Y. K., and P. Krishnaveni (1991), Incorporation of strontium (90Sr2+) into the skeleton of the hermatypic coral Galaxea fascicularis, J. Exp. Zool., 258, Ip, Y. K., and A. L. L. Lim (1991), Are calcium and strontium transported by the same mechanism in the hermatypic coral Galaxea fascicularis?, J. Exp. Biol., 159, Jell, J. S. (1974), The microstructure of some scleractinian corals, paper presented at 2nd International Coral Reef Symposium, Great Barrier Reef Comm., Brisbane, Australia. Marshall, J. F., and M. T. McCulloch (2002), An assessment of the Sr/Ca ratio in shallow water hermatypic corals as a proxy for sea surface temperature, Geochim. Cosmochim. Acta, 66, Marshall, A. T., and A. Wright (1998), Coral calcification: Autoradiography of a scleractinian coral Galaxea fascicularis after incubation in 45 Ca and 14 C, Coral Reefs, 17, Marubini, F., H. Barnett, C. Langdon, and M. J. Atkinson (2001), Dependence of calcification on light and carbonate 9of10

10 ion concentration for the hermatypic coral Porites compressa, Mar. Ecol. Prog. Ser., 220, McCulloch, M. T., A. W. Tudhope, T. M. Esat, G. E. Mortimer, J. Chappell, B. Pillans, A. R. Chivas, and A. Omura (1999), Coral record of equatorial sea-surface temperatures during the penultimate deglaciation at Huon Peninsula, Science, 283, Meibom, A., M. Stage, J. Wooden, B. R. Constantz, R. B. Dunbar, A. Owen, N. Grumet, C. R. Bacon, and C. P. Chamberlain (2003), Monthly strontium/calcium oscillations in symbiotic coral aragonite: Biological effects limiting the precision of the paleotemperature proxy, Geophys. Res. Lett., 30(7), 1418, doi: /2002gl Mitsuguchi, T., E. Matsumoto, and T. Uchida (2003), Mg/Ca and Sr/Ca ratios of Porites coral skeleton: Evaluation of the effect of skeletal growth rate, Coral Reefs, 22(4), Paquette, J., and R. J. Reeder (1995), Relationship between surface-structure, growth-mechanism, and trace-element incorporation in calcite, Geochim. Cosmochim. Acta, 59, Richmond, R. H., and C. L. Hunter (1990), Reproduction and recruitment of corals: Comparison among the Caribbean, the Tropical Pacific and the Red Sea, Mar. Ecol. Prog. Ser., 60, Schneider, R. C., and S. V. Smith (1982), Skeletal Sr content and density in Porites spp in relation to environmental factors, Mar. Biol., 66, Schrag, D. P. (1999), Rapid analysis of high-precision Sr/Ca ratios in corals and other marine carbonates, Paleoceanography, 14, Shen, C. C., T. Lee, C. Y. Chen, C. H. Wang, C. F. Dai, and L. A. Li (1996), The calibration of D[Sr/Ca] versus sea surface temperature relationship for Porites corals, Geochim. Cosmochim. Acta, 60, Vago, R., E. Gill, and J. C. Collingwood (1997), Laser measurements of coral growth, Nature, 386, Wainwright, S. A. (1964), Studies of the mineral phase of coral skeletons, Exp. Cell Res., 34, Wells, J. W. (1956), Scleractinia, in Treatise on Invertebrate Paleontology, Part F, Coelenterata, edited by R. C. Moore, pp , Univ. of Kansas Press, Lawrence. 10 of 10