PP31A-1468
Quantitative analyse of trace elements with HR-ICP-MS Element2 : an example of application in calcite shell of the Great Scallop Pecten Maximus.
Carbonate minerals are abundant on the Earth's surface, and they are produced by a number of processes, including precipitation from hydrothermal fluids or synthesis by organisms like coral, foraminifera, molluscs, or bacteria. Consequently, they are found in a large variety of environments. Their isotopic compositions (Sr, C, or O ) and trace element concentrations are widely used to understand or reconstruct biological, geological or biogeochimical processes. A large scientific community define the elemental composition of bivalve shells a promising tool as a recorder of environmental parameters like sea surface temperature, salinity and primary productivity. But we have compile evidences that trace elements variation within shells can be species dependant or change in a complex network of environmental interactions. In this context, a better understanding of the incorporation of elements from seawater into biogenic carbonate is necessary to generalize the use of these proxies. Daily shell growth in the calcitic bivalve Pecten maximus has been extensively measured and these daily growth marks can be used to date each subsequent sample of calcium carbonate. In this study, micro- sampling of carbonate powder along the shell was carried out with a high-resolution inductively coupled plasmamass spectrometry (HR-ICP-MS, Finnigan Element2). This method led to a quantitative detection of trace element in biocaronates and to the accurate reconstruction of ontogenetic profiles of elemental ratios with a 3-day temporal resolution. Repeated analyses of different growth layers sections on the same valve showed that the trace elements are homogeneously distributed along the shell. Mo concentration was reproducible for several scallop individuals from a same location over different years and from different coastal temperate environments. Each profile was characterised by a background level punctuated by sharp episodic peaks occurring in spring (may). Some hypotheses will be discussed but the most probable is the ingestion of phytoplankton cells grown upon NO3- which have a large concentration of Mo associated to the activity of nitrate reductase.
PP31A-1469
Inter-Colony Fidelity of Sr/Ca Variability in the Massive Caribbean Coral Siderastrea siderea: a Sub-Fossil Example
Coral-based reconstructions of climate variability in the Atlantic Warm Pool (AWP) in the pre-instrumental period are sparse. Multi-century Sr/Ca records generated from the skeleton of the widely distributed, massive, slow growing (~0.5 cm yr-1) coral Siderastrea siderea have the potential to address this data gap by providing robust proxies of interannual- to centennial-scale sea surface temperature (SST) variability in the AWP. However, before modern and fossil geochemical time series from S. siderea can be interpreted in terms of climate variability, reproducibility tests must be performed on individual coral colonies from the same location. Here we provide one such assessment of inter-colony reproducibility in the geochemistry of S. siderea using cores from the Dry Tortugas National Park (~24°33'N, 82°53'W). Time series of Sr/Ca from a large colony cored live in the summer of 1993 and a second, sub-fossil colony core, with a high-precision mass spectrometric U/Th date of 110 ± 1.7 (2σ) yrs, are compared. The 25-year overlap exhibits excellent reproducibility in both monthly and monthly anomaly space, and the average absolute difference between monthly data from the two time series is within instrumental precision. The results of this work suggest that individual monthly Sr/Ca records from S. siderea can be deemed representative of local SST variability, and that continuous local Sr/Ca records can be successfully spliced together from living and sub-fossil corals using high precision U/Th dating.
PP31A-1470
Seasonal variation in the Mg/Ca ratio and δ18O of the planktonic foraminifera Globigerina bulloides: Results from the Gulf of Tehuantepec, Eastern Equatorial North Pacific
Mg/Ca and δ18O has been measured in the surface dwelling planktonic foraminiferal species Globigerina bulloides from weekly sediment trap samples collected from two depths (460 and 560m) in the Gulf of Tehuantepec (15°38.826 N, 95°16.905 W) between February 2006 and June 2007. The Gulf of Tehuantepec is a region of intense upwelling and undergoes significant seasonal changes in sea surface temperature (SST) (~ 26° - 30°C) and salinity (~ 33.3 - 34.5). This is an ideal setting to study the effects of temperature and salinity on δ18O by comparing it to the temperature dependent, but salinity independent Mg/Ca ratio. Our results show that Mg/Ca and δ18O are negatively correlated (r2 =- 0.61, p < 0.001) with most of the scatter occurring in the region of low Mg/Ca and high δ18O values. A comparison of the Mg/Ca values with monthly temperature measurements yields a strong positive correlation (r2 = 0.91, p = 0.003), while only a weak negative correlation exists between the δ18O and temperature (r2 = -0.23, p = 0.021). The Mg/Ca data were also compared to monthly salinity measurements and showed a weak negative correlation (r2 = - 0.39, p = 0.186), while the δ18O data show no significant correlation with salinity. Temperatures calculated from the Mg/Ca data using the Elderfield and Ganssen (2000) equation range from 24° - 30°C and thus agree fairly well with the measured temperatures. Conversely, temperatures calculated from δ18O using the Bemis et al. (1998) equation ranged from 19° - 30°C. Weekly satellite SST measurements are being acquired and will allow us to better evaluate the relationship between temperature and both Mg/Ca and δ18O.
PP31A-1471
An Investigation Into the Influences of Temperature and Growth Rate on the Mg/Ca Ratio of Mytilus edulis Calcite
The common blue mussel Mytilus edulis is a fast-growing bivalve with a lifespan of up to 20 years. The fast shell growth in this species makes it possible to obtain LA-ICP-MS analyses of the trace element chemistry of the outer calcite shell layer with weekly to daily resolution. M. edulis shells could therefore have potential as basis for proxies for seasonal environmental variations. There are, however, difficulties in the use of bivalve shell carbonate for environmental proxies. Even within a single species, calcification is dependant on internal as well as external conditions. The development and application of proxies based on bivalve shell trace element chemistry thus face several challenges. Though the uptake of magnesium in M. edulis appears to be influenced by ambient water temperature, factors such as ontogeny and growth rate may also influence the inclusion of magnesium into the shell. An investigation into the influence of ontogeny, growth rate and ambient temperature on the magnesium uptake in the shells of juvenile and adult M. edulis has been carried out. Data from LA-ICP-MS analyses of shell material from a field-based aquaculture experiment carried out in the Dutch Wadden Sea in 2005 and 2006 show that there is a marked difference between the Mg/Ca ratios of shell material deposited right after settlement, and shell deposited after the first few months of life. While there is a clear difference in shell chemistry between early juvenile and later juvenile shell, no obvious differences between the chemistry of the later juvenile and adult shell have been observed. This difference causes an Mg/Ca ratio - temperature relationship found in later juvenile and adult shell to be incorrect for shell formed while a specimen is very young. By measuring the shell lengths of the specimens during the experiment, linear extension growth rates could be calculated. The relationship between growth rate and size of a specimen is in no way straightforward, but two groups occur. Individuals that have just settled have very high growth rates, while adults display growth rates with a seasonal variation. The growth of adults peaks in May and June; the growth rates of the just settled juveniles are consistently higher than the rates of the adults, and the fastest juvenile growth occurs in June and July. Both in the case of adults and juveniles, the shell Mg/Ca ratio displays a relationship with the shell growth rate. This is a contribution to EUROCLIMATE project 04 ECLIM FP08 CASIOPEIA.
PP31A-1472 [WITHDRAWN]
Seasonal Temperature Estimates From Late Holocene Barents Sea cod Otoliths: Problems and Potential
Realistic models of climate change require accurate data of past seasonal temperature regimes. In many marine settings this is difficult to achieve using the marine sedimentary record. This study tests the feasibility to use archaeological cod otoliths to reconstruct changes in the seasonal temperature cycle in the Barents Sea. Potentially, stable oxygen isotope records from cod otoliths could be used to produce records of Holocene temperature change on a seasonal time scale. Human settlements along the coast of northern Norway have exploited the cod (Gadus morhua) population of the Barents Sea from the earliest occupation, through the middle ages, to the present day. A pilot project has been carried out in Bergen to exploit the availability of a collection of cod otoliths from archeological excavations that is housed by the Bergen Museum. Cod otoliths from archaeological excavations in northern Norway, 26 specimens from from Måsøy (Finnmark) and 17 specimens from Vanna (Troms), were selected for this study. These specimens were AMS radiocarbon dated and the ages are spanning approximately 1400 to 1780 AD. Most of the otoliths are from cod that were captured during the Little Ice Age. Seasonal growth patterns were identifiable in the archeological otoliths, comparable to those in modern otoliths. Micromilling was used to sample for stable oxygen isotopes over a 2-year growth period in each of a total of 43 fossil cod otoliths. There are large differences in the temperature ranges experienced by the fish over the 2-year period analyzed. For the Måsøy specimens the temperature range experienced by the fish is between 2.7 to 9.9 °C. The Vanna cod experienced temperature ranges between 1.7 to 7.2 °C. The maximum temperature ranges for both Vanna and Måsøy specimens are higher than the seasonal instrumental measurements for the 0-200 m depth interval in the Kola section in the Barents Sea. The cod otoliths in our study have not yet been divided into different age groups, which is necessary in order to be able to interpret the calculated temperature ranges because the annual temperature cycles experienced by fish at different ages are different. Another problem that needs to address is the annual migration of cod of northern Norway. It is known that both mature and immature cod undertake long seasonal migrations.
PP31A-1473
Medieval Warm Period Archives Preserved in Limpet Shells (Patella Vulgata) From Viking Deposits, United Kingdom
The Medieval Warm Period (700-1100 YBP) represents a recent period of warm climate, and as such provides a powerful comparison to today's continuing warming trend. However, the spatial and temporal variability inherent in the Medieval Warm Period (MWP) makes it difficult to differentiate between global climate trends and regional variability. The continued study of this period will allow for the better understanding of temperature variability, both regional and global, during this climate interval. Our study is located in the Orkney Islands, Scotland, which is a critical area to understand climate dynamics. The North Atlantic Oscillation and Gulf Stream heavily influence climate in this region, and the study of climate intervals during the MWP will improve our understanding of the behavior of these climate mechanisms during this interval. Furthermore, the vast majority of the climate archive has been derived from either deep marine or arctic environments. Studying a coastal environment will offer valuable insight into the behavior of maritime climate during the MWP. Estimated seasonal sea surface temperature data were derived through isotopic analysis of limpet shells (Patella vulgata). Analysis of modern shells confirms that growth temperature tracks seasonal variation in ambient water temperature. Preliminary data from MWP shells record a seasonal temperature range comparable to that observed in the modern temperature data. We will extend the range of temperature data from the 10th through 14th centuries to advance our knowledge of seasonal temperature variability during the late Holocene.
PP31A-1474
Oxygen and carbon isotope records of cultured freshwater pearl mussel Hyriopsis sp. shell from Lake Kasumigaura, Japan
We analyzed the relationship between oxygen and carbon isotope ratios and morphological structure to understand the biomineralization of cultured freshwater pearl mussel (Hyriopsis sp.: Unionidae) shells and pearls. The δ18O of the outer shell layer was mainly controlled by water temperature with minor contribution from a variation in δ18O of ambient water especially in rainy season. The constant values of δ13C values with ontogeny suggesting that both temperature and body size had no significant effect on δ13C of shell. We observed nine distinct disturbance rings on the outer surface of the shell. Five distinct disturbance rings coincided with every winter peaks of the δ18O profile. On the other hand, summer disturbance rings were not observed every year. Moreover, some summer rings had strong and multiple discontinuity in inner structure. The relationship between growth rings and δ18O profile suggest that winter growth cessation probably due to inactive growth at low water temperatures (below approximately 10°C) or reproduction, and summer growth cessation was not caused by cyclic event but occasional events, e.g. heavy rain. The δ18O profile and shell structures indicated shell aragonite was precipitated close to an equilibrium condition with respect to oxygen isotope composition of ambient water. The δ18O of a pearl indicated calcification occurred at temperature range of at least 13-23°C.
PP31A-1475
The Accuracy of Paleoenvironmental Reconstructions Based on Spring and Wetland Gastropod Ô18O Values: A Field Study
Paired live gastropods and water samples were collected monthly for over two years from two localities near Reno, Nevada: a relatively stable cold, low-flow spring and a highly-variable wetland. Shell samples from gastropods (Gyraulus, Physella, Planorbella, Stagnicola) were crushed to a homogeneous powder and analyzed for stable isotopes (n=115). Annual δ18O water values varied between -15.6 and - 14.8‰ (SMOW) and water temperature varied between 12 and 23° C at the spring locality. Shell δ18O values at the spring locality ranged from 15.5 to 19.9‰ (SMOW). The gastropod δ18O values exhibited the general pattern of seasonal variability (lower values in warm months and higher values in cold months) although they were offset from the expected equilibrium fractionation value, possibly reflecting a vital effect, calcification in a microhabitat, or error in estimating the timing (e.g., month) of calcification. The offset averaged 0.8‰ for Physella and 2.8‰ for Stagnicola. In contrast to the spring, the wetland annual δ18O water varied between -13.0 and -2.4‰, while water temperature varied between 4 and 26° C. Shell δ18O values ranged from 20.7 to 30.2‰ reflecting seasonal extremes of hydrologic input (springflow and runoff) to output (evaporation) in the wetland and possibly diurnal and monthly variability in the system and differential seasonal or diurnal shell growth. Different hydrologic systems have characteristic isotope systematics. This study shows that δ18O gastropod shell values are useful to infer seasonal changes and annual variability in hydrologic settings. Settings with limited seasonal variability host mollusks with relatively limited shell δ18O variability and vice versa. Life strategies (e.g., mobility, behavior, reproduction, and longevity) and possibly physiology (e.g., gills, lungs, or pseudobranch) of different genera, however, can affect isotopic values in the same setting and therefore, may be of critical importance when interpreting isotopic data. Isotopic values of individuals of a single genus can provide a general sense of the variability of the system, whereas values of individuals from several genera record system variability as well as different life strategies and vital effects.
PP31A-1476
What is hiding behind ontogenic d13C variations in mollusk shells: New insights from scallops.
We examined d13Ccalcite variations along scallop shells (Pecten maximus) sampled in Norway, France and Spain. Time series of shell calcite d13C show a consistent pattern of decreasing d13C with age. This almost linear d13C trend reflects an increasing contribution of metabolic CO2 to skeletal carbonate throughout ontogeny. We have removed this ontogenic trend to try to extract other information from our shell calcite d13C dataset. Scallops from the Bay of Brest (western Brittany, France) were then used to interpret the data as many environmental parameters were available for this site. d13Ccalcite variations were compared to d13C of dissolved inorganic carbon (DIC) and Chl a. The detrended calcite d13C profiles seem to follow a seasonal pattern, but surprisingly are inversely related to the d13C DIC and chlorophyll a concentrations measured within the water column. Theses results suggest that shell d13C variations are not controlled by isotopic variation of DIC. Since scallops eat phytoplankton and microphytobenthos cells, and, as a consequence respire organic mater largely depleted in 13C, we therefore suggest that in mollusk suspension feeders the shell d13Ccalcite might still be used to track the annual number of phytoplankton blooms when d13C values of calcite are detrended. We must consider this trend as a potential biological filter hiding precious environmental records.
PP31A-1477
Phosphorus in coral skeleton: Evidence and species-specific global calibrations for a novel seawater phosphate proxy
A proxy for surface water nutrient concentrations recorded in coral skeleton would provide novel records of sub-seasonal to centennial scale variations in nutrient dynamics and primary production in the past. Such records of tropical euphotic zone nutrient supply and uptake could link climate oscillations to low latitude carbon fixation more directly than existing paleo-SST/upwelling proxies alone. A new coral proxy for seawater phosphate, P/Ca, would complement records from established but quantitatively uncertain surface water upwelling proxies such as coralline Cd/Ca and Ba/Ca. Using solution phase HR-ICP-MS methods, we have constructed mean global "calibrations" for P/Ca in three species of surface-dwelling corals: Pavona gigantea, Porites lutea, and Montastrea faveolata. We show that for all three species, average skeletal P/Ca in colonies growing in distinct nutrient regimes show a good linear positive correlation with average local surface phosphate concentrations, relatively similar slopes (Δ P/Ca coral/ Δ P/Ca seawater = ~1-2), but different y-intercepts (~0-50 P/Ca coral (μmol/mol)) for each species calibration. Further, a 4-year record along the growth axis of a Pavona gigantea coral growing under seasonally varying nutrient levels in the upwelling regime of the Gulf of Panamá shows repeated annual cycles of P/Ca (~75 -230 μmol/mol), with maxima occurring during cool upwelling periods, tracking the ~3 fold seasonal variations of surface water phosphate (LaVigne et al., 2008). Based on chemical cleaning experiments and inorganic phosphorus measurements in the aragonite, we hypothesize that this P/Ca signal reflects a combination of inorganic and organic intracrystalline phases, incorporated in proportion to ambient seawater phosphate. We plan to further test the validity of this new proxy in several coral species by comparing skeletal P/Ca to time series seawater phosphate records in the Gulf of Panamá and the Florida Keys.
PP31A-1478
Do the corals off Molokai,Hawaii preserve a long-term groundwater discharge record?
Understanding long-term trends in coastal groundwater discharge on the island of Molokai, Hawaii, may provide important clues to better understand the nature of exchange across the land/sea interface and the impact of climate change. Human pressure also affects such exchange through changes in withdrawals rates. In response to increased urbanization, demand for coastal groundwater has also risen, as has the potential for coastal groundwater contamination. Coral cores were collected from several shallow sites along the south shore of Molokai and analyzed for a suite of trace elements, including select groundwater tracers. Long-term (1913-2002) stream discharge records from Molokai reveal a downward trend in base flow that imply a decrease in rainfall and coastal groundwater flow. In the Molokai corals, there was a statistically significant downward trend in monthly resolved yttrium and rare earth to calcium ratios over the last several decades. Thus the coral geochemical records appear to respond to changes in groundwater discharge associated with a decrease in base flow since 1913. These findings are further explored by testing naturally occurring radium isotopes as a groundwater tracer and oxygen isotopes as a freshwater tracer in the coral record.
PP31A-1479
Reconstruction of the East China Sea paleoenvironment at 16 ka by comparison of fossil and modern Faviidae corals from the Ryukyus, southwestern Japan
We conducted paired measurements of the Sr/Ca ratio and oxygen and carbon stable isotopes of a fossil Faviidae coral specimen (MYK90), age 16 ka, collected from near Miyako Island, the Ryukyus, southwestern Japan. Our study aimed to reconstruct the paleoenvironment in the East China Sea at 16 ka by comparing the fossil sample with modern Faviidae corals. Our data with annual or longer time resolution may be very suitable for paleoceanographic reconstruction, although no general calibration method for Faviidae corals has been reported. Our calibration showed that the annual mean sea surface temperature was approximately 5°C lower and sea surface salinity (SSS) at the study site was locally higher at 16 ka than at present. Weak summer monsoon activity during the last glacial, which decreased summer precipitation over the Asian continent, and an enhanced winter monsoon, which may have led to more evaporation, likely contributed to the inferred high SSS at the study site.
PP31A-1480
Seasonal variability in the oxygen isotopic composition of planktonic foraminifera (Neogloboquadrina pachyderma) in the northwestern North Pacific
Planktonic foraminifera provide a record of the upper ocean environment through their species assemblage and individual tests. Neogloboquadrina pachyderma is a common polarsubpolar planktonic foraminifer, and this species is used extensively for reconstruction of the paleo-environment. To investigate the relationship between isotopic composition of N. pachyderma (sinistral) and oceanographic conditions, we analyzed seasonal variation in oxygen isotope ratio of N. pachyderma in the northwestern North Pacific by using sediment trap samples collected biweekly at Site 50N (50°N, 165°E) from 1998 to 2001. We also focused on the differences in isotopic record between small (125-180 μm) and large (180-250 μm) shell of foraminifera. Oxygen isotopes of both size decreased in summer and increased in winter, and the difference of oxygen isotopic composition between small and large shell increased in summer (August to October) under a well-developed stratification of water column. The maximum difference value between both sizes was 0.6 permil in summer, corresponding to a 2.7 degree difference in water temperature. Seasonal profile of oxygen isotope of N. pachyderma was almost consistent with that of sea surface temperature (SST), however summer peaks in SST were not recorded in isotopic ratio. It would be caused by the sub-surface habitat of N. pachyderma.
PP31A-1481
Fluxes and Stable Isotope Dynamics of N. pachyderma (sin.) and T. quinqueloba in the Irminger Sea
We present an almost three year long record of planktonic foraminifera fluxes, oxygen and carbon isotopes of Turburotalita quinqueloba and Neogloboquadrina pachyderma s. from moored sediment traps and surface plankton samples from the central Irminger Sea. The mooring area is characterised by a large annual sea surface temperature cycle, whereas temperatures at depth remain almost constant, resulting in a highly stratified upper water column during summer and virtually no stratification during winter as is evident from daily salinity and temperature measurements at approximately 200 m water depth, satellite derived sea surface temperature and occasional sea surface temperature and salinity measurements. Since salinity variability both at depth and at the surface is very small, the site is ideally suited to study the effects of thermal stratification on the fluxes and stable isotopic composition of T. quinqueloba and N. pachyderma s. The flux of N. pachyderma s. peaks twice a year (in spring and autumn), a typical productivity pattern for the sub-arctic setting. Both growing seasons account for >95% of the total annual flux and contribute about equally to the total flux. The shell flux of T. quinqueloba however, shows only a single broad peak (September), more resembling flux patterns of the arctic domain. The δ18O N. pachyderma s. from surface plankton is practically identical to the expected value; at the site N. pachyderma s. thus seems to calcify in equilibrium with seawater. Its apparent export calcification depth varies during the season: ~50 m during the spring bloom, but closer to the surface during the autumn bloom period; in both cases shallower than often reported. The average δ18O N. pachydermas. in the Irminger Sea thus reflects sea water temperature between 0 and 50 m depth. The δ18O of T. quinqueloba in plankton pump samples shows slightly lighter values than expected from inorganic calcite precipitates, but isotope values of trap samples are extremely heavy (too cold) indicating a positive offset from equilibrium values. This offset is of opposite sign than all previous studies and may question the species' suggested paleoceanographic potential. In any case the Δδ18O N. pachyderma s.- T. quinqueloba does not reveal any thermal stratification of the upper ocean as has been proposed for the Nordic Seas. The δ13C and flux of N. pachyderma s. show a good correlation (r2 = 0.65), probably reflecting a shared governing factor for both parameters, i.e. productivity. The flux and δ13C of T. quinqueloba seem to be independent (r2 = 0.16), which might be related to the activity of symbionts in this taxon.
PP31A-1482
Seasonal Coral Skeletal 87Sr/86Sr Anomaly As A New Potential Proxy Of Tracing Water Masses
Coral skeletal 87Sr/86Sr anomaly is proposed to be as a potential proxy of distinguishing water masses, especially in the coastal regime. A seasonal 87Sr/86Sr record for 1992-2002 from a living coral Porites head, collected in Nanwan Bay, southernmost Taiwan (21°55'N, 12°47'E), is presented, which is done by using multi-collector inductively coupled mass spectrometry with standard bracketing methods. 87Sr/86Sr ratio ranges from 0.709172-0.709180 in winters and 0.709171- 0.709203 in summers. Two features, a seasonal change of 4-40 ppm and interannual summer differences of 40-50 ppm, are discovered. By checking corresponding Sr/Ca and δ18O values, the possibility of thermal effect and fresh water income can be both ruled out. Two possible controlling factors therefore are supposed to explain above annual Sr isotope fluctuation: horizontal mixing of different water masses, and perpendicular water column flow. It suggests that the 87Sr/86Sr ratio recorded in coral skeleton may serve as a new potential proxy to decipher different water end members for further understanding modern and past ocean circulations.
PP31A-1483
Relationship Between Photosynthetic Light Dosage and Metabolic Isotope Effects in the Long-term Cultured Porites Coral Skeleton
A long-term culture experiment of Porites spp. corals were conducted at different light dosages (light intensity, 100, 300, or 500 micro mol m-2 s-1; daily light period, 10 or 12 h) at constant temperature to examine the contribution of photosynthetic activity to skeletal carbon isotope composition. As the daily dose of photosynthetically active radiation increased, the rate of annual extension also increased. Mean isotope compositions shifted; the carbon isotope compositions became heavier and the oxygen isotope compositions became lighter at higher radiation dose. Whereas chlorophyll a (Chl a) content per both unit area and cell decreased as light dosage increased, carotenoids/Chl a increased. Skeletal oxygen isotope compositions decrease coincided with increasing skeletal growth rate, indicating the influence of so-called kinetic isotope effects. The observed carbon isotope compositions increase should be subject to both kinetic and metabolic isotope effects. Using a vector approach in the carbon-oxygen isotope compositions' plane (Omata et al., 2005), we discriminated between kinetic and metabolic isotope effects on carbon isotope compositions. The metabolic carbon isotopic fractionation-light was similar to the photosynthesisirradiance curve, indicating the direct contribution of photosynthetic activity to metabolic isotope effects. In contrast, the fractionation of carbon isotope related to kinetic isotope effects gradually increased as the growth rate increased.