Jelle Bijma

Reevaluation of the oxygen isotopic composition of planktonic foraminifera: Experimental results and revised paleotemperature equations

Cultured planktonic foraminifera, Orbulina universa (symbiotic) and Globigerina bulloides (nonsymbiotic), are used to reexamine temperature:δ18O relationships at 15°–25°C. Relationships for both species can be described by linear equations. Equations for O. universa grown under low light (LL) and high light (HL) share a slope of −4.80 (0.21‰ °C−1) with a HL-LL offset of −0.33‰ due to symbiont photosynthetic activity. The effect of [CO32−] on O. universa is −0.002‰ µmol−1 kg−1 and is insensitive to temperature. For G. bulloides, ontogenetic effects produce size-related trends in temperature:δ18O, whereby larger shells are enriched in 18O relative to smaller specimens. The O. universa temperature:δ18O relationships are more accurate than previously published equations for describing plankton tow data. Our equations do not explain planktonic core top data with the same precision but provide a good fit to benthic Cibicidoides data below 10°C. Temperature:δ18O relationships for G. bulloides provide good agreement with field data for this species from the northeast Pacific.

Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes

Stable oxygen and carbon isotope measurements on biogenic calcite and aragonite have become standard tools for reconstructing past oceanographic and climatic change. In aquatic organisms, 18O/16O ratios in the shell carbonate are a function of the ratio in the sea water and the calcification temperature. In contrast, 13C/12C ratios are controlled by the ratio of dissolved inorganic carbon in sea water and physiological processes such as respiration and symbiont photosynthesis. These geochemical proxies have been used with analyses of foraminifera shells to reconstruct global ice volumes, surface and deep ocean temperatures,, ocean circulation changes and glacial–interglacial exchange between the terrestrial and oceanic carbon pools. Here, we report experimental measurements on living symbiotic and non-symbiotic plankton foraminifera (Orbulina universa and Globigerina bulloides respectively) showing that the 13C/12C and 18O/16O ratios of the calcite shells decrease with increasing seawater [CO32−]. Because glacial-period oceans had higher pH and [CO32−] than today, these new relationships confound the standard interpretation of glacial foraminiferal stable-isotope data. In particular, the hypothesis that the glacial–interglacial shift in the 13C/12C ratio was due to a transfer of terrestrial carbon into the ocean can be explained alternatively by an increase in ocean alkalinity. A carbonate-concentration effect could also help explain some of the extreme stable-isotope variations during the Proterozoic and Phanerozoic aeons.

Assessing the reliability of magnesium in foraminiferal calcite as a proxy for water mass temperatures

Though many studies on the Mg contents in the calcitic tests of foraminifers exist, the processes controlling its uptake are still a matter of debate. Laboratory cultures offer an excellent opportunity to reveal these mechanisms. The Mg concentrations within single chambers of the planktic foraminifer Globigerinoides sacculifer (BRADY) maintained under controlled laboratory conditions were measured (1) at variable temperatures (19.5–29.5 °C) and constant salinity and (2) at variable salinity (22–45‰) and constant temperature. The experimental results suggest that under natural conditions, temperature is the leading mechanism controlling the Mg/Ca ratio. Temperature and magnesium are related proportionally. A temperature increase of ca. 10 °C gives rise to an increase of the magnesium concentrations of ca. 130%. Drastic (unnatural) salinity changes dominate the effects of temperature. A 110% change in the Mg/Ca ratio was observed when salinity was elevated or reduced by more than ca. 10‰. Specimens which underwent gametogenesis reveal significantly higher Mg concentrations than specimens that did not release gametes. Partition coefficients for Mg in foraminiferal calcite are orders of magnitude lower than values from inorganically precipitated calcite. When comparing observed Mg/Ca ratios of foraminiferal tests with predicted Mg/Ca ratios calculated according to empirical equations, it becomes evident that foraminiferal tests are undersaturated with respect to Mg for the water temperature they have experienced. Apparently, foraminifers are capable of controlling their Mg concentration. The physiological processes presumably responsible for such depressed Mg/Ca ratios appear to be temperature-controlled as deduced from the close relationship of the observed Mg/Ca ratios and water temperature. This study demonstrates that variations in temperature and salinity are definitely reflected in the Mg content of foraminiferal tests. Magnesium may thus serve as a paleo-proxy for past surface water temperatures, as long as postdepositional changes and salinity variations are of subordinate importance or can be excluded.

Reassessing Foraminiferal Stable Isotope Geochemistry: Impact of the Oceanic Carbonate System (Experimental Results)

Laboratory experiments with living planktic foraminifers show that the δ13C and δ18O values of shell calcite decrease with increasing sea water pH and/or carbonate ion concentration. The effect has been quantified in symbiotic (Orbulina universa) and non-symbiotic (Globigerina bulloides) species and is independent of symbiont activity and temperature. It is concluded that a kinetic fractionation process affects both the carbon and oxygen isotopic composition of the shell simultaneously. At present it cannot be determined definitively whether the relationship is controlled by the pH dependent balance between hydration and hydroxylation of CO2 or by [CO3 2-] related variations in the calcification rate. However, independent of which factor ultimately controls the relationship between the carbonate chemistry and isotopic fractionation, in the real ocean [CO3 2-] and pH covary linearly across the relevant pH range. The true relationship between shell isotopic composition and the bulk carbonate chemistry is masked by the fact that host respiration and symbiont activity locally modify the carbonate system. Respiration lowers and photosynthesis increases ambient pH and [CO3 2-]. This translates into modified absolute shell values but leaves the slope between the shell isotopic composition and the bulk carbonate chemistry unaffected. A second level of shell isotopic modification is introduced by the incorporation of respired carbon, enriched in 12C, which depletes the shell δ13C value. In symbiont bearing species this depletion is partially negated by a shell δ13C enrichment in the light. As an alternative to the RUBISCO hypothesis (enrichment via preferential removal of 12CO2), we propose that scavenging of respired CO2 during photosynthesis, raises the shell δ13C value. Our results have partly been documented before (Spero et al. 1997) and demonstrate that the carbonate chemistry is undoubtedly a major control on temporal geochemical variability in the fossil record. For instance, the sea water carbonate system of the pre-Phanerozoic world (Berner 1994; Grotzinger and Kasting 1993) or during glacials (Sanyal et al. 1995) was significantly different from today confounding direct interpretation of foraminiferal stable isotope data using existing relationships (see companion paper in this volume by Lea et al.).

Model for kinetic effects on calcium isotope fractionation (δ44Ca) in inorganic aragonite and cultured planktonic foraminifera

The calcium isotope ratios (δ44Ca = [(44Ca/40Ca)sample/(44Ca/40Ca)standard −1] · 1000) of Orbulina universa and of inorganically precipitated aragonite are positively correlated to temperature. The slopes of 0.019 and 0.015‰ °C−1, respectively, are a factor of 13 and 16 times smaller than the previously determined fractionation from a second foraminifera, Globigerinoides sacculifer, having a slope of about 0.24‰ °C−1. The observation that δ44Ca is positively correlated to temperature is opposite in sign to the oxygen isotopic fractionation (δ18O) in calcium carbonate (CaCO3). These observations are explained by a model which considers that Ca2+-ions forming ionic bonds are affected by kinetic fractionation only, whereas covalently bound atoms like oxygen are affected by kinetic and equilibrium fractionation. From thermodynamic consideration of kinetic isotope fractionation, it can be shown that the slope of the enrichment factor α(T) is mass-dependent. However, for O. universa and the inorganic precipitates, the calculated mass of about 520 ± 60 and 640 ± 70 amu (atomic mass units) is not compatible with the expected ion mass for 40Ca and 44Ca. To reconcile this discrepancy, we propose that Ca diffusion and δ44Ca isotope fractionation at liquid/solid transitions involves Ca2+-aquocomplexes (Ca[H2O]n2+ · mH2O) rather than pure Ca2+-ion diffusion. From our measurements we calculate that such a hypothesized Ca2+-aquocomplex correlates to a hydration number of up to 25 water molecules (490 amu). For O. universa we propose that their biologically mediated Ca isotope fractionation resembles fractionation during inorganic precipitation of CaCO3 in seawater. To explain the different Ca isotope fractionation in O. universa and in G. sacculifer, we suggest that the latter species actively dehydrates the Ca2+-aquocomplex before calcification takes place. The very different temperature response of Ca isotopes in the two species suggests that the use of δ44Ca as a temperature proxy will require careful study of species effects.

Seawater pH control on the boron isotopic composition of calcite: evidence from inorganic calcite precipitation experiments

Experiments involving boron co-precipitation with calcite have been carried out inorganically under controlled pH conditions (7.9 ± 0.05, 8.3 ± 0.05 and 8.6 ± 0.05) to determine the dependence of the boron isotopic composition (δ11B) of calcite on the pH of seawater. Another purpose of these experiments was to estimate the magnitude of the biogenic influence on the δ11B value of foraminifera by comparing their boron isotopic composition with that of the inorganic calcite over a common pH range. The results show a clear relationship between δ11B of inorganic calcite and the pH of artificial seawater. The variation of boron isotopic fractionation between seawater and calcite with pH, estimated from these experiments, is similar to that estimated for cultured O. universa and the theoretically predicted trend. The results also support the hypothesis that B(OH)4− is the dominant species incorporated into the calcite structure. However, the boron isotopic fractionation between seawater and inorganic calcite is lower than that estimated for O. universa indicating the presence of a biogenic effect on the boron isotopic composition at least of this species of foraminifera. Most importantly, the results imply that in spite of a small biogenic influence on the boron isotopic composition of foraminifera, the variation in δ11B of foraminiferal shells with pH (at least for O. universa) is comparable to that for inorganic calcite, supporting the potential of this isotopic signature in foraminifera as a reliable paleo pH proxy.

Clues to Ocean History: a Brief Overview of Proxies

The reconstruction of ocean history employs a large variety of methods with origins in the biological, chemical, and physical sciences, and uses modern statistical techniques for the interpretation of extensive and complex data sets. Various sediment properties deliver useful information for reconstructing environmental parameters. Those properties that have a close relationship to environmental parameters are called “proxy variables” (“proxies” for short). Proxies are measurable descriptors for desired (but unobservable) variables. Surface water temperature is probably the most important parameter for describing the conditions of past oceans and is crucial for climate modelling. Proxies for temperature are: abundance of microfossils dwelling in surface waters, oxygen isotope composition of planktic foraminifera, the ratio of magnesium or strontium to calcium in calcareous shells or the ratio of certain organic molecules (e.g. alkenones produced by coccolithophorids). Surface water salinity, which is important in modelling of ocean circulation, is much more difficult to reconstruct. At present there is no established method for a direct determination of this parameter. Measurements associated with the paleochemistry of bottom waters to reconstruct bottom water age and flow are made on benthic foraminifera, ostracodes, and deep-sea corals. Important geochemical tracers are δ13C and Cd/Ca ratios. When using benthic foraminifera, knowledge of the sediment depth habitat of species is crucial. Reconstructions of productivity patterns are of great interest because of important links to current patterns, mixing of water masses, wind, the global carbon cycle, and biogeography. Productivity is reflected in the flux of carbon into the sediment. There are a number of fluxes other than those of organic carbon that can be useful in assessing productivity fluctuations. Among others, carbonate and opal flux have been used, as well as particulate barite. Furthermore, microfossil assemblages contain clues to the intensity of production as some species occur preferentially in high-productivity regions while others avoid these. One marker for the fertility of sub-surface waters (that is, nutrient availability) is the carbon isotope ratio within that water (I3C/12C, expressed as δ13C). Carbon isotope ratios in today’s ocean are negatively correlated with nitrate and phosphate contents. Another tracer of phosphate content in ocean waters is the Cd/Ca ratio. The correlation between this ratio and phosphate concentrations is quite well documented. A rather new development to obtain clues on ocean fertility (nitrate utilization) is the analysis of the 15N/14N ratio in organic matter. The fractionation dynamics are analogous to those of carbon isotopes. These various ratios are captured within the organisms growing within the tagged water. A number of reconstructions of the partial pressure of CO2 have been attempted using δ13C differences between planktic and benthic foraminifera and δ13C values of bulk organic material or individual organic components. To define the carbon system in sea water, two elements of the system have to be known in addition to temperature. These can be any combination of total CO2, alkalinity, or pH. To reconstruct pH, the boron isotope composition of carbonates has been used. Ba patterns have been used to infer the distribution of alkalinity in past oceans. Information relating to atmospheric circulation and climate is transported to the ocean by wind or rivers, in the form of minerals or as plant and animal remains. The most useful tracers in this respect are silt-sized particles and pollen.

The Diversity and Distribution of Modern Planktic Foraminiferal Small Subunit Ribosomal RNA Genotypes and their Potential as Tracers of Present and Past Ocean Circulations

Molecular phylogenetic analysis of the small subunit ribosomal RNA gene of planktic spinose foraminifers shows that morphospecies may represent clusters of different and often highly divergent genotypes. In some cases the level of divergence may justify separate taxonomic status as distinct “cryptic” species. Molecular evolution rate estimates, based on fossil record evidence, suggest that the cryptic divergences may have occurred many millions of years ago. An investigation of their distribution in the Caribbean (tropical zone), Coral Sea and Mediterranean Sea (subtropical zone), and Southern California Bight (transitional zone) indicates that genotypes are transported across water mass boundaries, and it is proposed that the direction of gene flow follows the prevailing global ocean surface circulation pattern. At the present time the prevailing currents transport tropical/subtropical genotypes from the Pacific to Atlantic around the South African Cape. Cooler water transitional genotypes may transit from Pacific to Atlantic in gene corridors opened during glacial periods.

Temperature influence on the carbon isotopic composition of Globigerina bulloides and Orbulina universa (planktonic foraminifera)

Laboratory experiments with the planktonic foraminifera Orbulina universa (symbiotic) and Globigerina bulloides (nonsymbiotic) were used to examine the effects of temperature, irradiance (symbiont photosynthesis), [CO32-], [HPO42-], and ontogeny on shell d13C values. In ambient seawater ([CO32-] = 171 mmol kg-1), the d13C of O. universa shells grown under low light (LL) levels is insensitive to temperature and records the d13C value of seawater TCO2. In contrast, the d13C of high light (HL) shells increases ~0.4‰ across 15-25°C (+0.050‰/°C). This suggests that the d13C enrichment due to symbiont photosynthetic activity is temperature-dependent. A comparison of HL O. universa grown in elevated [CO32-] seawater with ambient specimens shows that temperature does not affect the slope of the d13C/[CO32-] relationship previously described [Spero et al., 1997]. The d13C of G. bulloides shells decreases across the 15-24°C temperature range and d13C:temperature slopes decrease with increasing shell size (-0.13, -0.10, and -0.09‰/°C in 11- 12-, and 13-chambered shells, respectively). The pattern of lower d13C values at higher temperatures likely results from the incorporation of more respired CO2 into the shell at higher metabolic rates. The d13C of HL O. universa increases with increased seawater [HPO42-].

Population dynamics of the planktic foraminifer Globigerina bulloides from the eastern North Atlantic

Abstract A cumulative data set from the eastern North Atlantic was compiled and analysed to study the population dynamics of Globigerina bulloides . Data were generated from samples collected with a multiple opening and closing plankton net from the upper ocean (0–500 m). We analysed the total assemblage > 125 μm. The habitat of G. bulloides in the eastern North Atlantic is restricted mostly to the upper 60 m of the water column and depends on the availability of its food resources and, therefore, on the general hydrographic pattern. The temporal distribution of tests at different depths reveals a systematic succession that is related to the lunar cycle. We suggest that G. bulloides reproduces mainly within the upper 60 m of the ocean. Gametogenesis is unusual in test size classes below 125 μm but frequent in specimens larger than 150 μm. Reproduction takes place during the first week after new moon. Maturation of specimens takes place during the second half of waxing moon and during waning moon. Large numbers of mature specimens [gametogenic calcification (GAM) specimens > 250 μm] occur during the time of main reproduction.