Jonathan Erez

Experimental paleotemperature equation for planktonic foraminifera

Small live individuals of Globigerinoides sacculifer which were cultured in the laboratory reached maturity and produced garnets. Fifty to ninety percent of their skeleton weight was deposited under controlled water temperature (14° to 30°C) and water isotopic composition, and a correction was made to account for the isotopic composition of the original skeleton using control groups. Comparison of. the actual growth temperatures with the calculated temperature based on paleotemperature equations for inorganic CaCO3 indicate that the foraminifera precipitate their CaCO3 in isotopic equilibrium. Comparison with equations developed for biogenic calcite give a similarly good fit. Linear regression with Craigs (1965) equation yields: t = −0.07 + 1.01t (r= 0.95) where t is the actual growth temperature and t Is the calculated paleotemperature. The intercept and the slope of this linear equation show that the familiar paleotemperature equation developed originally for mollusca carbonate, is equally applicable for the planktonic foraminifer G. sacculifer. Second order regression of the culture temperature and the delta difference (δ18Oc − δ18Ow) yield a correlation coefficient of r = 0.95: t = 17.0 − 4.52(δ18Oc − δ18Ow) + 0.03(δ18Oc − δ18Ow)2t, δ18Oc and δ18Ow are the estimated temperature, the isotopic composition of the shell carbonate and the sea water respectively. A possible cause for nonequilibnum isotopic compositions reported earlier for living planktonic foraminifera is the improper combustion of the organic matter.

The Source of Ions for Biomineralization in Foraminifera and Their Implications for Paleoceanographic Proxies

The global carbon cycle is strongly perturbed by fossil fuel burning leading to atmospheric CO2 increase. Climatic warming followed by polar ice melting and global sea level rise are predicted due to the greenhouse effect of increasing CO2 in the atmosphere (Houghton et al. 1995). The ocean plays a major role in neutralizing the excess CO2 because the amount of inorganic carbon available for exchange with the atmosphere in the ocean is approximately 50–60 times larger than in the atmosphere (e.g., Siegenthaler and Sarmiento 1993). The bulk of the atmospheric CO2 excess will eventually be neutralized by CaCO3 dissolution in the deep marine environment. This is, however, is a relatively slow process that operates on the time scale of ocean circulation (1000 yrs) and is therefore causing an accumulation of CO2 in the atmosphere. This phenomenon will result in potentially severe consequences to the well being of global ecological systems. Obviously the scientific attention of many biogeochemists is focused on processes controlling the response of the marine system to changes in atmospheric CO2 concentrations (e.g., Archer and Maier-Reimer 1994; Broecker 1997; Sigman and Boyle 2000; Berger 2002). ### Foraminifera, corals, and coccolithophores in the global carbon cycle There are four dominant processes involved in neutralizing the excess atmospheric CO2 in the ocean. These are: 1) gas exchange at the air-sea interface and reaction with the carbonate ion to form bicarbonate, 2) net primary productivity, 3) CaCO3 production and dissolution and 4) ocean circulation. Most of these processes are biologically mediated and may have special importance in shallow tropical environments where the exchange with the atmosphere is more direct. In this review we address the mechanism of biomineralization in one of the major groups that precipitates CaCO3 in the ocean—the foraminifera. As we will show, this group …

A biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate

Measurements of SrCa of benthic foraminifera show a linear decrease with water depth which is superimposed upon significant variability identified by analyses of individual foraminifera. New data for CdCa support previous work in defining a contrast between waters shallower and deeper than ∼ 2500 m. Measured element partition coefficients in foraminiferal calcium carbonate relative to sea water (D) have been described by means of a one-box model in which elements are extracted by Rayleigh distillation from a biomineralization reservoir that serves for calcification with a constant fractionation factor (α), such that D = (1 − fα)(1 − f), where f is the proportion of Ca remaining after precipitation. A modification to the model recognises differences in element speciation. The model is consistent with differences between DSr, DBa and DCd in benthic but not planktonic foraminifera. Depth variations in D for Sr and Ba are consistent with the model, as are differences in depth variation of DCd in calcitic and aragonitic benthic foraminifera. The shallower depth variations may reflect increasing calcification rates with increasing water depth to an optimum of about 2500 m. Observations of unusually lower DCd for some deep waters, not accompanied by similar DSr or DBa, may be because of dissolution or a calcification response to a lower carbonate saturation state.

Impact of biomineralization processes on the Mg content of foraminiferal shells: A biological perspective

The Mg/Ca ratio in foraminiferal shells is widely used as a proxy for paleotemperatures. Nevertheless, it seems that the basic Mg content of foraminifera is determined by biological factors, as can be concluded from the large inter species and intrashell variability and the frequent deviations from inorganic behavior. This paper discusses three possible ways by which foraminifera can control or modify the Mg content in their shell: (1) involvement of organic matrix in the precipitation process that may alter the partition coefficient of Mg in biogenic calcite, (2) controlled conversion of transient amorphous phases to calcite, and (3) modification of the Mg concentration in the parent solution from which the crystals precipitate. The first two mechanisms are probably responsible for the precipitation of high-Mg calcite phases (whole shell or sublayers), while the third mechanism leads to the formation of low-Mg calcite phases. We propose a model adapted from epithelial cells that allows massive Mg2+ removal from the biomineralization site. This model is especially relevant to the planktonic and deep benthic low-Mg foraminifera that are frequently used for paleotemperature reconstructions. We discuss the possible biological roles of Mg in the shell in terms of the calcite polymorph conservation, the in vivo chemical stability of the shell, the functions of Mg as a stabilizer of transient phases and as a controlling agent of the precipitation process. Several temperature sensitive biological processes that may influence the Mg/Ca ratio of the shell are suggested and a model that combines biogenic and inorganic considerations is presented. The model uses Mg heterogeneity in the shell together with temperature response (biologic and inorganic) of biomineralization processes, to account for the deviation of planktonic foraminifera from inorganic calcite at equilibrium with seawater.

Uranium in foraminiferal calcite as a recorder of seawater uranium concentrations

We present results of an investigation of uraniumcalcium ratios in cleaned foraminiferal calcite as a recorder of seawater uranium concentrations. For accurate reconstruction of past seawater uranium content, shell calcite must incorporate uranium in proportion to seawater concentration and must preserve its original uranium composition over time. Laboratory culture experiments with live benthic (Amphistegina lobifera) and live planktonic (Globigerinella calida) foraminifera show that the UCa ratio of cleaned calcite tests is proportional to the concentration of uranium in solution. After correcting results for the presence of initial calcite, the apparent distribution coefficient D = (UCa)calciteUCa)solution = 10.6 ± 0.3 (×10−3) for A. lobifera and D = 7.9 ± 0.1 (×10−3) for G. calida. UCa ratios in planktonic foraminifera from core tops collected above 3900 m in the equatorial Atlantic and above 2100 m in the Pacific Ocean show no significant difference among the species analyzed. D estimated from core top samples ranges from 7.6 ± 0.4 (× 10−3) for O. universa to 8.4 ± 0.5 (×10−3) for G. ruber. In benthic species C. wuellerstorfi, D = 7.0 ± 0.8 (×10−3). UCa and Mg/Ca in G. tumida and G. sacculifer from core tops taken near and below the regional lysocline decrease with water depth. Smaller decreases in UCa and MgCa with depth were observed in C. wuellerstorfi. In the planktonic species, we believe that UCa and MgCa are lower in the more dissolution-resistant fraction of calcite, leading to lower UCa in more highly dissolved samples.

Comparison of isotopic composition of planktonic foraminifera in plankton tows, sediment traps and sediments

Planktonic foraminifera from plankton tows, sediment traps and sediments in the central North Atlantic were studied in order to understand what determines their oxygen and carbon isotope composition. A clear separation of species and genera on a δ18O vs. δ13C plot for all samples suggests that their isotopic composition is controlled to a certain degree by biological factors. Within a species population, the globorotaliids show a positive linear correlation between δ18O and δ13C, while the shallow-dwelling spinose species (mostly Globigerinoides species) do not show a definite trend. The latter species, when collected in plankton tows, often show slight negative deviations from isotopic equilibrium with respect to oxygen. All species deviate from carbon isotope equilibrium by −1.5 to −6‰. These deviations from equilibrium are probably caused by incorporation of isotopically light metabolic CO2 into the skeleton, which is enhanced by the activity of symbiotic algae. During their ontogeny the average weight per individual of most species increases which indicates that calcification continues to a depth of about 100 m. This additional skeleton (roughly 50% by weight) is isotopically heavier because temperatures are lower and photosynthesis of symbiotic algae stops below the photic zone. Therefore, the skeleton of foraminifera collected in sediment traps below 400 m has an overall oxygen isotope composition that seems to be in equilibrium for CaCO3 deposited in the upper 100 m.

Effect of aragonite saturation, temperature, and nutrients on the community calcification rate of a coral reef

(1) In this study we investigated the relations between community calcification of an entire coral reef in the northern Red Sea and annual changes in temperature, aragonite saturation and nutrient loading over a two year period. Summer (April-October) and winter (November-March) average calcification rates varied between 60 ± 20 and 30 ± 20 mmolm � 2 � d � 1 , respectively. In general, calcification increased with temperature and aragonite saturation state of reef water with an apparent effect of nutrients, which is in agreement with most laboratory studies and in situ measurements of single coral growth rates. The calcification rates we measured in the reef correlated remarkably well with precipitation rates of inorganic aragonite calculated for the same temperature and degree of saturation ranges using empirical equations from the literature. This is a very significant finding considering that only a minute portion of reef calcification is inorganic. Hence, these relations could be used to predict the response of coral reefs to ocean acidification and warming.

The role of seawater endocytosis in the biomineralization process in calcareous foraminifera

Foraminifera are unicellular organisms that inhabit the oceans in various ecosystems. The majority of the foraminifera precipitate calcitic shells and are among the major CaCO3 producers in the oceans. They comprise an important component of the global carbon cycle and also provide valuable paleoceanographic information based on the relative abundance of stable isotopes and trace elements (proxies) in their shells. Understanding the biomineralization processes in foraminifera is important for predicting their calcification response to ocean acidification and for reliable interpretation of the paleoceanographic proxies. Most models of biomineralization invoke the involvement of membrane ion transporters (channels and pumps) in the delivery of Ca2+ and other ions to the calcification site. Here we show, in contrast, that in the benthic foraminiferan Amphistegina lobifera, (a shallow water species), transport of seawater via fluid phase endocytosis may account for most of the ions supplied to the calcification site. During their intracellular passage the seawater vacuoles undergo alkalization that elevates the CO32− concentration and further enhances their calcifying potential. This mechanism of biomineralization may explain why many calcareous foraminifera can be good recorders of paleoceanographic conditions. It may also explain the sensitivity to ocean acidification that was observed in several planktonic and benthic species.

Coral Calcification Under Ocean Acidification and Global Change

Coral reefs are unique marine ecosystems that form huge morphological structures (frameworks) in today’s oceans. These include coral islands (atolls), barrier reefs, and fringing reefs that form the most impressive products of CaCO3 biomineralization. The framework builders are mainly hermatypic corals, calcareous algae, foraminifera, and mollusks that together are responsible for almost 50% of the net annual CaCO3 precipitation in the oceans. The reef ecosystem acts as a huge filtration system that extracts plankton from the vast fluxes of ocean water that flow through the framework. The existence of these wave resistant structures in spite of chemical, biological, and physical erosion depends on their exceedingly high rates of calcification. Coral mortality due to bleaching (caused by global warming) and ocean acidification caused by atmospheric CO2 increase are now the major threats to the existence of these unique ecosystems. When the rates of dissolution and erosion become higher than the rates of precipitation, the entire coral ecosystem starts to collapse and will eventually be reduced to piles of rubble while its magnificent and high diversity fauna will vanish. The loss to nature and to humanity would be unprecedented and it may occur within the next 50 years. In this chapter, we discuss the issue of ocean acidification and its major effects of corals from the cell level to the reef communities. Based on the recently published literature, it can be generalized that calcification in corals is strongly reduced when seawater become slightly acidified. Ocean acidification lowers both the pH and the CO 3 2− ion concentration in the surface ocean, but calcification at the organism level responds mainly to CO 3 2− and not to pH. Most reports show that the symbiotic algae are not sensitive to changes in the carbonate chemistry. The potential mechanisms responsible for coral sensitivity to acidification are either direct input of seawater to the biomineralization site or high sensitivity of the enzymes involved in calcification to pH and/or CO2 concentrations. Increase in pH at the biomineralization site is most probably the most energy demanding process that is influenced by ocean acidification. While hermatypic corals and other calcifiers reduce their rates of calcification, chemical and biological dissolution increase and hence net calcification of the entire coral reef is decreasing dramatically. Community metabolism in several sites and in field enclosures show in some cases net dissolution. Using the relations between aragonite saturation (Ωarag) and community calcification, it is possible to predict that coral reefs globally may start to dissolve when atmospheric CO2 doubles.

Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification

The mechanisms behind the transfer of molecules from the surrounding sea water to the site of coral calcification are not well understood, but are critical for understanding how coral reefs are formed. We conducted experiments with the fluorescent dye calcein, which binds to calcium and is incorporated into growing calcium carbonate crystals, to determine the permeability properties of coral cells and tissues to this molecule, and to determine how it is incorporated into the coral skeleton. We also compared rates of calcein incorporation with rates of calcification measured by the alkalinity anomaly technique. Finally, by an electrophysiological approach, we investigated the electrical resistance of coral tissues in order to better understand the role of tissues in ionic permeability. Our results show that (i) calcein passes through coral tissues by a paracellular pathway, (ii) intercellular junctions control and restrict the diffusion of molecules, (iii) intercellular junctions should have pores of a size higher than 13 Å and lower than 20 nm, and (iv) the resistance of the tissues owing to paracellular junctions has a value of 477 ± 21 Ohm cm2. We discuss the implication of our results for the transport of calcium involved in the calcification process.