Body temperatures of modern and extinct vertebrates from ¹³ C- ¹⁸ O bond abundances in bioapatite

Abstract

The stable isotope compositions of biologically precipitated apatite in bone, teeth, and scales are widely used to obtain information on the diet, behavior, and physiology of extinct organisms and to reconstruct past climate. Here we report the application of a new type of geochemical measurement to bioapatite, a "clumpedisotope" paleothermometer, based on the thermodynamically driven preference for 13 C and 18 O to bond with each other within carbonate ions in the bioapatite crystal lattice. This effect is dependent on temperature but, unlike conventional stable isotope paleothermometers, is independent from the isotopic composition of water from which the mineral formed. We show that the abundance of 13 C-18 O bonds in the carbonate component of tooth bioapatite from modern specimens decreases with increasing body temperature of the animal, following a relationship between isotope "clumping" and temperature that is statistically indistinguishable from inorganic calcite. This result is in agreement with a theoretical model of isotopic ordering in carbonate ion groups in apatite and calcite. This thermometer constrains body temperatures of bioapatite-producing organisms with an accuracy of 1-2°C. Analyses of fossilized tooth enamel of both Pleistocene and Miocene age yielded temperatures within error of those derived from similar modern taxa. Clumped-isotope analysis of bioapatite represents a new approach in the study of the thermophysiology of extinct species, allowing the first direct measurement of their body temperatures. It will also open new avenues in the study of paleoclimate, as the measurement of clumped isotopes in phosphorites and fossils has the potential to reconstruct environmental temperatures.apatite | isotope | paleoclimate | thermophysiology | paleothermometry T he mechanisms by which animals regulate their body temperatures are among the most fundamental aspects of their biology. The acquisition of endothermy, the ability to maintain high and stable body temperatures through internal heat production, is a major physiological change that occurred at an unknown stage during the evolutionary transition to mammals and birds from their ancestors among the nonmammalian therapsids and nonavian dinosaurs, respectively (1). Approaches to understanding the physiology of extinct animals and the evolution of endothermy have largely focused on biophysical modeling, anatomical observations, growth rate analysis from bone histology, and behavioral studies such as estimating predator/prey ratios (1-7). The validity of each of these approaches is uncertain (for contrasting viewpoints on approaches to dinosaur thermoregulation see refs. 4 and 5).Modern endothermic mammals and ectotherms, such as alligators and crocodiles, generally have significant differences in average body temperatures. With rare exceptions, mammals have high and stable body temperatures around 36-38°C regardless of their environment, whereas the body temperatures of ectotherms are generally lower on average and often fluctuate depending o...

Modeling the effects of diagenesis on carbonate clumped-isotope values in deep- and shallow-water settings

“…Specifically we use the calibration of Ghosh et al (2006) as given in the absolute reference frame by Dennis et al (2011) to convert  47 values to apparent clumped-isotope temperatures for samples measured here. Although this calibration is based on the precipitations of inorganic calcite at only 4 distinct temperatures, it has been verified in subsequent studies of biogenic samples with known carbonate formation temperatures measured at the California of Institute of Technology (Ghosh et al, 2007;Came et al, 2007;Eagle et al, 2010;Tripati et al, 2010;Thiagarajan et al, 2011;Eagle et al, 2015). To demonstrate this, we compiled previous measurements made at Caltech for samples with known formation temperatures (both inorganic and biogenic) form 1 to 1650°C in the absolute reference and compared it to the Ghosh et al (2006) calibration from 1-50°C (see Fig.…”

“…The equation is  47 = 0.00173 x (10 6 /T 2 ) 2 + 0.0203 x 10 6 /T 2 + 0.261 where T is the temperature in Kelvin. Data used in this calibration comes only from measurement made at the Caltech laboratories Ghosh et al, 2007;Came et al, 2007;Guo et al, 2009;Tripati et al, 2010;Eagle et al, 2010;Thiagarajan et al, 2011;Dennis et al, 2011;Stolper and Eiler, 2015;Eagle et al, 2015;Spooner et al, 2016;Bonifacie et al, 2017). …”

Evolution of Neoproterozoic Wonoka–Shuram Anomaly-aged carbonates: Evidence from clumped isotope paleothermometry

“…Clumped isotope-derived temperatures can be combined with ␦ 18 O carb to uniquely determine ␦ 18 O w through application of an appropriate carbonate-water oxygen isotope fractionation factor (Kim and O'Neil, 1997;Vasconcelos et al, 2005). The tool has been used for a range of applications including the study of primary and diagenetic processes in terrestrial and marine samples of a wide range of ages (Came et al, 2007;Affek et al, 2008;Dennis and Schrag, 2010;Eagle et al, 2010Eagle et al, , 2011Eagle et al, , 2013Passey et al, 2010;Tripati et al, 2010Tripati et al, , 2014Bristow et al, 2011;Ferry et al, 2011;Finnegan et al, 2011;Huntington et al, 2011;Keating-Bitonti et al, 2011;Loyd et al, 2012aLoyd et al, , 2013aLoyd et al, , 2014Passey and Henkes, 2012;Swanson et al, 2012;Dale et al, 2014).…”

Determining the Diagenetic Conditions of Concretion Formation: Assessing Temperatures and Pore Waters Using Clumped Isotopes

“…18 O Schauble et al 2006;Eiler 2007;Eagle et al 2010;Tripati et al 2010;Eiler 2011), including d 18 O pw (Huntington et al 2011). The abundance of mass 47 CO 2 (mostly the 13 C-18 O-16 O isotopologue) that is produced upon phosphoric-acid digestion of carbonate minerals is reported using the notation D 47 , and represents the abundance of this isotopologue in a sample relative to a stochastic distribution (in units of permil, %).…”