plospbioPLoS BiolplosbiolPLoS Biology1544-91731545-7885 Public Library of Science San Francisco, USA 10.1371/journal.pbio.0040248 Research Article Evolutionary Biology Evolutionary Biology/Paleontology Physiology Ecology None Dinosaur Fossils Predict Body TemperaturesDinosaur Body Temperatures Gillooly James F 1 * Allen Andrew P 2 Charnov Eric L 3 4 Department of Zoology, University of Florida, Gainesville, Florida, United States of America National Center for Ecological Analysis and Synthesis, Santa Barbara, California, United States of America Department of Biology, University of New Mexico, Albuquerque, New Mexico, United States of America Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon, United States of America Moritz Craig Academic Editor University of California Berkeley, United States of America * To whom correspondence should be addressed. E-mail:

JFG, APA, and ELC conceived and designed the experiments. JFG and APA performed the experiments. JFG and APA analyzed the data. JFG, APA, and ELC wrote the paper.

The authors have declared that no competing interests exist.

8 2006 11 7 2006 48e248 1 11 2005 19 5 2006 2006Gillooly et alThis is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Math and Fossils Resolve a Debate on Dinosaur Metabolism Correction: Math and Fossils Resolve a Debate on Dinosaur Metabolism

Perhaps the greatest mystery surrounding dinosaurs concerns whether they were endotherms, ectotherms, or some unique intermediate form. Here we present a model that yields estimates of dinosaur body temperature based on ontogenetic growth trajectories obtained from fossil bones. The model predicts that dinosaur body temperatures increased with body mass from approximately 25 °C at 12 kg to approximately 41 °C at 13,000 kg. The model also successfully predicts observed increases in body temperature with body mass for extant crocodiles. These results provide direct evidence that dinosaurs were reptiles that exhibited inertial homeothermy.

A model based on growth trajectories estimated from fossils provides evidence that dinosaurs were reptiles whose body temperatures increased systematically with increasing body size.

APA was supported as a Postdoctoral Associate at the National Center for Ecological Analysis and Synthesis, a Center funded by the National Science Foundation (NSF) (DEB-0072909), the University of California, Santa Barbara. ELC was supported during the summer by the Department of Biology at the University of New Mexico. JFG was supported in part by NSF Grant DEB-0083422 through the University of New Mexico, and in part by the Department of Zoology at the University of Florida.

Body temperature regulation in dinosaurs has long been a topic of interest and debate in biology because of its importance to understanding the physiology and life history of these ancient, exceptionally large animals [1]. Some have argued that dinosaurs were endotherms with body temperatures that were high, relatively constant, and internally regulated, just as in contemporary birds and mammals (e.g., [2]). Others have argued that dinosaurs were reptile-like in their metabolism, but that large dinosaurs maintained higher, more constant body temperatures than smaller-sized reptiles due to thermal inertia (e.g., [3, 4]). According to the latter “inertial homeothermy hypothesis,” dinosaur body temperatures were primarily determined by the interaction between environmental temperature and the production and dissipation of heat. The inertial homeothermy hypothesis has thus far been supported by physiological or morphological data from extant ectotherms and endotherms, and by predictions from biophysical models [5, 6]. Resolution of the debate regarding body temperature regulation in dinosaurs has thus far been hampered by a lack of direct evidence [7].

Here we directly test the inertial homeothermy hypothesis by assessing whether dinosaur body temperatures increased with body size. To estimate body temperatures, we use data on the ontogenetic growth trajectories of eight dinosaur species— Syntarsus rhodesiensis, Psittacosaurus mongoliensis, Apatosaurus excelsus, Tyrannosaurus rex, Daspletosaurus torosus, Gorgosaurus libratus, Albertosaurus sarcophagus, and Massospondylus carinatus—that ranged in adult size from 15–25,952 kg, and that lived during the early Jurassic to late Cretaceous periods. These eight growth trajectories were obtained from published work that use newer methods of bone histology and body size estimation [811] to estimate the maximum growth rate, G (kg day−1), and the mass at maximum growth, M (kg), which is about half of the asymptotic adult size (see Materials and Methods).

While data were also available for the dinosaur bird Shuvuuia deserti, this species was excluded from our analysis because it is a feathered species and is therefore fundamentally different than the eight more reptile-like species mentioned above.

The recent availability of these data, along with recent advances in understanding the effects of body size and temperature on growth [12, 13], allow us to apply a novel approach to estimate dinosaur body temperatures. Specifically, we analyze these data using a recently published model that predicts the combined effects of body size and temperature, Tb (°C), on maximum growth rate [12, 13]:

Equation 1 builds on a previously published model that predicts growth rates for a broad assortment of ectotherms and endotherms [14]. It has now been used successfully to predict rates of embryonic growth in diverse taxa [13], rates of post-embryonic growth in zooplankton [13], rates of individual-level biomass production [15], and rates of population-level growth in diverse taxonomic groups [16]. Here go is a normalization constant that is independent of temperature and body size [11, 12]. The temperature term, , describes the exponential effects of body temperature on whole-organism growth rates. Specifically, it assumes that the biochemical reactions controlling growth have an activation energy of 0.6–0.7 eV, reflecting the temperature dependence of individual metabolic rate [17, 18]. The value represents the mid-point of this range of activation energies. The use of this temperature term is supported by recent work for a broad assortment of organisms [11], and by work conducted near the beginning of the last century (i.e., Krogh's curve) [19]. The body size term, M3/4, is theoretically predicted [14, 20] and empirically supported by extensive data [12], including maximum growth-rate data for extant reptiles [21] and mammals [22]. Given that the coefficient go is similar for taxa with different modes of body temperature regulation (∼2 × 10−4 kg1/4 day−1 for ectotherms and endotherms; see Materials and Methods), we can rearrange the terms in Equation 1 to estimate the body temperature of each dinosaur species as:

based on its estimated maximum growth rate, G, and mass at the time of maximum growth, M (see Materials and Methods).


Equation 2 yields body temperature estimates for each of the eight dinosaur species. Results for seven of the eight species indicate that body temperature increases curvilinearly with the logarithm of body size (Figure 1). The eighth species, Sy. rhodesiensis, is clearly an outlier, and is therefore excluded from subsequent analyses (but see discussion below). For the remaining species, body temperature increases by only 2 °C with size from the 12-kg P. mongoliensis to the 614-kg Al. sarcophagus, but then increases by nearly 15 °C from the 218-kg Al. sarcophagus to the 12, 979-kg Ap. excelsus. These results suggest that the smallest dinosaurs, with body temperatures of about 25 °C, had temperatures close to environmental temperatures, as observed for smaller-sized extant reptiles [5]. We can characterize this increase in body temperature with size by fitting a non-linear least squares regression model to the data depicted in Figure 1 ( Tb = 23.3 + ( M/44.4)0.5, where 23.3 °C, 44.4 kg/°C2, and 0.5 are all fitted parameter estimates). Interestingly, the intercept of this equation, 23.3 °C, is the estimated average environmental temperature for these dinosaurs. This estimate is in agreement with most paleotemperature estimates during the dinosaur age, which generally range between 20 and 30 °C across latitudes [5]. We note that our body temperature estimates for dinosaurs should be relatively insensitive to the modest variation that exists in go between reptiles and mammals (see Materials and Methods), because the effect of go on Tb is only logarithmic in Equation 2. More importantly, the relative increase in body temperature with body mass predicted by the model is entirely independent of go.

10.1371/journal.pbio.0040248.g001 A Plot of the Relationship between Average Body Temperature (°C) and the Logarithm of Body Mass for Dinosaurs and Extant Crocodiles

For dinosaurs, body temperatures were estimated from Equation 2 using data on ontogenetic growth trajectories determined from bone histology (see Materials and Methods). Body mass is expressed as the size at which maximum growth rates occur, which is about half of asymptotic adult size. The fitted line includes the following species in ascending order of weight: P. mongoliensis (12 kg), M. carinatus (140 kg), Al. sarcophagus (614 kg), G. libratus (622 kg) , D. torosus (869 kg), T. rex (2,780 kg), and Ap. excelsus (12,979 kg) [811]. The line was fit to the data using non-linear least squares regression in order to generate predictions on the change in body temperature with body mass for crocodiles (Figure 2). This line does not include the two additional species shown here, the dinosaur bird Sh. deserti (1 kg), which was not considered because it was feathered, and Sy. rhodesiensis (11 kg), which was excluded because it was an outlier (see text). For crocodiles, body temperature estimates are based on the previously observed relative increase in body temperature with body size for individuals (32–1,010 kg) held under natural conditions, and by assuming a mean annual environmental temperature of 25 °C [5].

10.1371/journal.pbio.0040248.g002 A Plot of the Observed versus the Predicted Increase in Average Body Temperature (°C) with Body Mass for Crocodiles

The observed increase in average body temperature for crocodiles ranging in mass from 32–1,010 kg [5] was plotted versus the predicted increase in average body temperature with body mass for these crocodiles based on the line fit to the dinosaur data shown in Figure 1 and predicted from Equation 2.

The relationship depicted in Figure 1 also suggests that dinosaur body temperatures changed over the ontogeny of an individual, sometimes dramatically. More specifically, it suggests that body temperatures increased by less than 3 °C over ontogeny for species reaching adult sizes of 300 kg, but by more than 20 °C for species reaching sizes of approximately 25,000 kg, such as Ap. excelsus. If we extrapolate the model depicted in Figure 1 up to what is perhaps the largest dinosaur species (∼55,000 kg for an adult Sauroposeidon proteles [23]), the estimated body temperature at the mass of maximum growth is approximately 48 °C, which is just beyond the upper limit tolerated for most animals (∼45 °C). These findings suggest that maximum dinosaur size may have ultimately been limited by body temperature.

Model predictions regarding the change in body temperature with body size are strongly supported by a test using data from extant crocodiles ranging in size from 32–1,010 kg. The observed increase in body temperature with size for crocodiles [5] appears continuous with our estimates for dinosaurs if we assume that the average annual environmental temperature for crocodiles was 25 °C, close to empirical measures [5] (Figure 1). However, even without making any assumptions about environmental temperature, the relative change in body temperature predicted by the dinosaur model is similar to the empirically observed increase in temperature with size for extant crocodiles (see Materials and Methods). Specifically, a plot of the predicted versus observed change in body temperature with size for crocodiles yields a slope of 0.79, and an r2 value of 0.86 (Figure 2). Furthermore, the intercept of this relationship is near 0 (−0.09), suggesting that environmental temperatures for dinosaurs were similar to those of extant crocodiles. Note that using a fitted non-linear regression model that includes the outlier S. rhodesiensis in Figure 1 ( Tb = 26.31 + ( M/393.76)0.78) still gives a highly significant relationship between predicted and observed body temperatures for crocodiles ( r2 = 0.86, p < 0.01).

The results presented here provide what is perhaps the first direct evidence that dinosaurs were reptiles whose body temperatures increased systematically with body size, consistent with the inertial homeothermy hypothesis [4, 6, 5, 24]. The increase in body temperature with body size shown here for dinosaurs (26–41 °C in Figure 1) is far greater than for any animals living today. This would explain the observation that large dinosaurs grew at rates similar to those of extant eutherian mammals [8, 9], which generally maintain body temperatures of 36–38 °C [25], but that small dinosaurs grew at rates similar to extant reptiles [8, 9], which generally have lower body temperatures of 25–35 °C [26] (Figure 2). In other words, our model and these results indicate that the reason the body size scaling of maximum growth rate may be steeper than M3/4 for dinosaurs, but not for reptiles, birds, or mammals [8, 9, 27, 28], is largely due to the confounding effects of increasing temperature with increasing body size over this large size range. An increase in body temperature of more than 15 °C from the smallest to largest dinosaurs (Figure 1) would likely have had important consequences for many aspects of dinosaur life history.

Materials and Methods Estimating size and maximum growth.

Ontogenetic growth curves of dinosaur species were fitted using the equation m( t) = ( a/(1 + exp[ b( tc)])) + m0 , where m( t) is the mass at time t, m0 is the mass at t = 0, and a + m0 is the asymptotic adult mass [8, 9]. The fitted parameters in references [8, 9] yielded estimates for the maximum growth rates, G = − ab/4, and the mass at the time of maximum growth, M = a/2 + m0 . Given the difficulty in estimating G and M, and possible errors associated with different methodologies, we only included species from references [8, 9] where G and M were estimated using the same methodology. These criteria exclude the one other known species of dinosaur for which a growth trajectory has been established [29]. See references [811] for more information on the methods used to estimate sizes and ages of individuals.

Estimating <italic>g <sub>o</sub> </italic>.

The value of go used here was estimated from data on the scaling of maximum growth rates for reptiles [21] and mammals [22]. Linear regression models of the form log( G) versus log( M) were fitted to both sets of data. The slopes of both relationships include the value predicted by Equation 1 of 0.75 (95% confidence intervals: 0.58–0.84, n = 12, for reptiles and 0.69–0.75, n = 163, for mammals). Therefore, go was separately calculated as the geometric mean of the 12 estimates of GM−3/4e−0.1 Tb for reptiles and the 163 estimates of GM−3/4e−0.1 Tb for mammals. Taking Tb to be 37 °C for mammals [25] and 30 °C for reptiles [26] yielded geometric mean estimates for go that were remarkably similar for reptiles (1.7 × 10−4 kg1/4 day−1) and mammals (2.3 × 10−4 kg1/4 day−1). We therefore used the average of these two estimates (2 × 10−4 kg1/4 day−1) for our calculations of dinosaur body temperatures.

The authors thank J. H. Brown, J. Harte, R. M. Sibly, and G. B. West for helpful discussions and comments on this work. JFG also thanks G. Erickson and A. Chinsamy-Turan for helpful discussions on growth ring analyses, and on their respective studies, without which this work would not have been possible. The authors also thank S. White for help with graphics. Finally, we thank two reviewers, F. Seebacher and T. Kemp, for many helpful and insightful comments.

References Farlow JO Dodson P Chinsamy A Dinosaur biology. Ann Rev Ecol Systemat 1995 26 445 471 de Ricqlès AJ Evolution of endothermy: Histological evidence. Evol Theory 1974 1 51 80 Colbert EH Cowles RB Bogert CM Rates of temperature increase in dinosaurs. Copeia 1947 141 142 Spotila JR Lommen PW Bakken GS Gates DM A mathematical model for body temperature of large reptiles: Implications for dinosaur ecology. Am Nat 1973 107 391 404 Seebacher F Dinosaur body temperatures: The occurrence of endothermy and ectothermy. Paleobiology 2003 29 105 122 O'Connor MP Dodson P Biophysical constraints on the thermal ecology of dinosaurs. Paleobiology 1999 25 341 368 Farlow JO Weishampel DB Dodson P Osmolska H Introduction. The dinosauria 1990 Berkeley University of California Press 43 55 Erickson GM Rogers KC Yerby SA Dinosaurian growth patterns and rapid avian growth rates. Nature 2001 412 429 432 Erickson GM Makovicky PJ Currie PJ Norell MA Yerby SA Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 2004 430 772 775 Chinsamy A Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeontol Afr 1990 27 77 82 Chinsamy A Bone histology and growth trajectory of the prosauropod dinosaur Massopondylus carinatus Owen. Mod Geol 1993 18 319 329 Gillooly JF Brown JH West GB Savage VM Charnov EL Effects of size and temperature on metabolic rate. Science 2001 293 2248 2251 Gillooly JF Charnov EL West GB Savage VM Brown JH Effects of size and temperature on developmental time. Nature 2002 417 70 73 West GB Brown JH Enquist BJ A general model for ontogenetic growth. Nature 2001 413 628 631 Ernest SKM Enquist BJ Brown JH Charnov EL Gillooly JF Thermodynamic and metabolic effects on the scaling of production and population energy use. Ecol Lett 2003 6 990 995 Savage VM Gillooly JF Brown JH West GB Charnov EL Effects of body size and temperature on population growth. Am Nat 2003 163 429 441 Charnov EL Gillooly JF Thermal time: Body size, food quality and the 10 °C Rule. Evol Ecol Res 2003 5 43 51 Gillooly JF Allen AP Savage VM West GB Brown JH Response to Clarke and Fraser: Effects of temperature on metabolic rate. Funct Ecol 2006 200 400 404 Krogh A The quantitative relations between temperature and standard metabolism in animals. Int Z Phys Chem Biol 1914 1 491 508 West GB Brown JH Enquist BJ A general model for the origin of allometric scaling laws in biology. Science 1997 276 122 126 Andrews RM Gans C Pough FH Patterns of growth in reptiles. Biology of the reptilia 1982 New York Academic Press 273 305 Case TJ On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q Rev Biol 1978 53 243 282 Wedel MJ Cifelli RL Sanders RK Osteology, paleobiology, and relationships of the sauropod dinosaur Sauroposeidon. Acta Palaeontol Pol 2000 45 343 388 Seebacher F Grigg GC Beard LA Crocodiles as dinosaurs: Behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures. J Exp Biol 1999 202 77 86 Schmidt-Nielsen K Animal physiology 1997 New York Cambridge University Press Brattstrom BH Body temperatures of reptiles. Am Midl Nat 1965 73 376 422 Erickson GM Brochu CA How the ‘terror crocodile' grew so big. Nature 1999 398 205 206 Padian K de Ricqlès AJ Horner JR Dinosaurian growth rates and bird origins. Nature 2001 412 405 408 Horner JR de Ricqlès AJ Padian K Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum Growth dynamics and physiology based on an ontogenetic series of skeletal elements. J Vertebr Paleontol 2000 20 115 129