Metabolic middle ground

Over the past few decades, the original characterization of dinosaurs by early paleontologists as lumbering, slow-metabolizing ectotherms has been challenged. Recent studies propose that dinosaurs were capable of an active lifestyle and were metabolically similar to endothermic mammals and birds (1–3). This debate is of more than heuristic interest; energy consumption is closely linked to life history, demographic, and ecological traits (4). Extant endothermic mammals and birds possess metabolic rates ~5 to 10 times higher than those of reptiles and fish (5, 6), but characterizing the metabolic rates of dinosaurs has been difficult.

A promising method for inferring paleoenergetics comes from studies of ontogenetic growth, in which age is determined from annual rings in bone cross sections and mass is determined from bone dimensions. Ultimately, growth is powered by metabolism, and rates of growth and energy use should correspond. Pioneering work by Erickson and others has led to a growing body of literature on dinosaur growth and generated important insights (7, 8). However, many analyses were hampered by small samples, an outdated comparative data set, and the lack of an appropriate energetic framework. Increasing data availability permits a reassessment of dinosaur growth against a broader spectrum of animals, standardized for environmental temperature. Further, recent advances in metabolic theory provide a theoretical framework for evaluating metabolic rate on the basis of growth.

We used a comparative approach to characterize the energetics of dinosaurs and other extinct taxa. We examined the empirical and theoretical relationship between growth and resting metabolic rate, using a broad database of major vertebrate clades (9), and used our results to examine the energetics of Mesozoic dinosaurs. From empirical studies, we constructed ontogenetic growth curves and determined a maximum rate of growth for each species. Environmental temperature was standardized by only considering growth rates in ectotherms from tropical and subtropical climates or from laboratory settings between 24° and 30°C, comparable to temperatures experienced by dinosaurs during the Mesozoic (10).

Data for dinosaur growth were taken from published reports that provided a minimum of five measurements of size and age. All metabolic rates were converted to watts (W). Where multiple metabolic or maximum growth rates for a species were recorded, the geometric mean was determined. Overall, our data set includes ~30,000 values and was used to characterize growth for 381 species, including 21 species of Mesozoic dinosaurs, 6 extinct crocodilians, and a Cretaceous shark (table S1). Dinosaurs are well represented both temporally (late Triassic to end-Cretaceous) and taxonomically (Theropoda, Sauropodomorpha, Ornithopoda, and Ceratopsia). Values for resting metabolic rates were compiled from the literature and standardized to a common temperature of 27°C (table S1). We performed phylogenetic independent contrasts (PICs) in addition to conventional ordinary least-squares regression (OLS) and standardized major axis regression (table S2).

Data show, within and across species, that resting metabolic rate B scales with body mass m as a power function, B = B₀m^α, where B₀ is a normalization constant representing mass-independent metabolic rate, and α is ~3/4 and ranges from 0.65 to 0.85 (11, 12). Growth rate varies over ontogeny, but use of the maximum growth rate (G_max) standardizes growth and permits interspecific comparisons. Empirical evidence (13) indicates that G_max scales similarly to B, where G_max = G₀M^α. This suggests that B α G_max¹ and thus that metabolic rate may be inferred from growth. However, the relationship between G_max and B across major vertebrate taxa has received little attention, and many uncertainties exist. For instance, Case (13) reported that fish G_max was an order of magnitude lower than that of reptiles, despite similarities in metabolic and thermoregulatory lifestyle (6).

Theoretical assessments of growth complement a strictly empirical approach and can strengthen paleontological inferences. An ontogenetic growth model based on metabolic scaling theory (MST) quantifies the linkages between G_max and metabolic rate from first principles of allometry and conservation of energy (14, 15). According to MST (9), the relationship between B (W) and G_max (g day^-1) at final adult mass M is 

B_M = cG_max¹ (1)

where c ~0.66 (W day¹ g^-1 day). To observe the mass-independent relationship and compare energetic groups, we divide both sides by M^α, yielding

B₀ = cG₀ (2)

To calculate metabolic rate at any ontogenetic mass m from the observed maximum growth rate, we combine Eqs. 1 and 2

B_m = cG₀m^3/4 (3)

MST makes the following theoretical predictions regarding growth and metabolic rate:

(1) G_max scales as M^α, where α ~3/4.

(2) B scales isometrically with G_max if masses are standardized (9). Regression of B against G_max yields a slope of 1 and an intercept of ~0.66.

(3) Plotting G₀ against B₀ will reveal distinct energetic clusters corresponding to endotherms and ectotherms. High-power endotherms will exhibit an elevated G₀ and B₀, and ectothermic organisms the converse. Thermally intermediate taxa, termed mesotherms, such as tuna and lamnid sharks (16), should fall between the upper and lower quadrats. The predicted slope and intercept are 1 and 1.52, respectively. Similar clustering is observed if G_max and B residuals are plotted.

(4) B_predicted = B_observed in extant animals, where B_predicted is calculated from Eq. 3.

Our analyses find broad support for all four predictions. First, growth scales with mass as ~3/4, although taxonomic variation is observed (Fig. 1 and fig. S1, mean α_OLS = 0.73; mean α_PIC = 0.69, table S2). This indicates that larger species acquire their bulk by accelerating their maximum growth rate proportionate to ~M3/4. Second,G_max is a strong predictor of B, where B_M = 0.56G_max^1.03, which is close to theoretical predictions [figs. S3 and S4; slope confidence interval (CI) = 0.97 to 1.10; intercept CI = 0.47 to 0.97; coefficient of determination (r²) = 0.90, n = 118]. Third, we find that the observed relationship between mass-independent growth and metabolic rates corresponds closely to predicted values (slope = 0.90, CI = 0.77 to 1.03; intercept = 1.10, CI = 0.59 to 2.06, r² = 0.61, n = 124). Ectothermic species fall in the lower left quadrat; endotherms in the upper right; and thermally intermediate taxa, including tuna, a lamnid shark, the leatherback turtle, and a prototherian mammal, fall between values for endo- and ectotherms (Fig. 2 and figs. S1, S2, and S5).

These results are robust; the inclusion of cold-water fish, with reduced growth and metabolic rates, simply extends the lower portion of the regression line. Furthermore, the ratio G₀/B₀ (g J^-1), a measure of efficiency in converting energy to biomass, does not differ significantly between endo- and ectotherms, indicating that energy allocation to growth does not vary with thermoregulatory strategy (t statistic = 0.46, P= 0.64, fig. S6). Finally, regression of observed against calculated metabolic rates does not differ significantly from unity (Fig. 3A; slope CI = 0.97 to 1.10; intercept CI = -0.14 to 0.02). We can therefore predict dinosaur resting metabolic rates from growth rate, using either a theoretical model (Eq. 3) or an empirically determined equation (9) 

B_M = 0.6 G_max (4)

Panel A questions

A very large ectotherm is likely to have a higher metabolic rate than a very small endotherm simply because there are more cells in the animal. Figure 2 compares metabolic rate and growth rates per gram of mass. These are mass-independent rates.

A1. Compare and contrast mass-independent metabolic rates and growth rates of endotherms to that of ectotherms.

A2. Which two groups of endotherms do not follow the theoretical prediction (solid line)?

A3. Describe why a high metabolic rate would support an endotherm's thermoregulation. (Hint: Apply the second law of thermodynamics.)

Panel B questions

Let's look more closely at dinosaurs (panel B).

B1. Which variable can be measured in dinosaurs, and how is it measured?

B2. If an organism has a mass-independent growth rate of 10^-2 (g^1/4d^-1) what do you predict its mass-independent metabolic rate would be?

B3. If an organism had a mass-independent growth rate of 10^-3, what thermoregulation type would you predict it to be?

Panel A answers

A1. Regardless of the size of the organism, endotherms have higher mass-independent metabolic rates and growth rates than ectotherms.

A2. Altricial birds and primates, toothed whales. ("Altricial" means born in an undeveloped state, requiring parental care.) Note that birds typically have very high metabolic rates relative to their mass, whereas primates and large mammals have slow growth rates for their size. This slow growth rate is often associated with large brain size and low juvenile mortality that would not be associated with dinosaurs.

A3. According to the second law of thermodynamics, heat is a byproduct of energy conversion. A faster metabolic rate would result in more heat generated through metabolism. This heat would increase the organism's internal body temperature to a level higher than the ambient (surrounding environmental) temperature.

Panel B answers

B1. Growth rate can be measured using the width of growth rings seen in fossilized dinosaur bones. For more information, see: http://www.pbs.org/wgbh/nova/nature/t-rex.html

B2. Mass-independent metabolic rate would be approximately 10^-2 W g^-3/4.

B3. Ectotherm

Questions (observed metabolic rate)

A1. Using panel B, describe the relationship between the mass of a species and its metabolic rate.

A2. Describe what panel B illustrates regarding the metabolic rates of endotherms, mesotherms, and ectotherms.

A3. How would the amount of food required to support a 10-gram endotherm compare to the amount needed to support a 10-gram ectotherm?

A4. What would be the advantage and disadvantage of being an endotherm versus an ectotherm?

Answers A

A1. As the mass of an animal increases, so does its metabolic rate. A large organism has more cells, resulting in a higher energy demand.

A2. At any given size (mass) endotherms have a higher metabolic rate than ectotherms. Mesotherms have an intermediate metabolic rate.

A3. To support a higher metabolic rate, the 10-gram endotherm will need to eat more food than the 10-gram ectotherm.

A4. Endotherm: Advantage: can use heat generated through a high metabolic rate to maintain an optimal body temperature despite fluctuations in the surrounding temperature. This allows endotherms to live in cooler climates. Disadvantage: A high metabolic rate will have a higher caloric cost, requiring the animal to eat more food.

Ectotherm: Advantage: A lower metabolic rate means a lower caloric demand, which, in turn, allows the animal to spend less time on hunting and foraging for food. Disadvantage: The animal has to use behavioral strategies, such as sun basking, to maintain optimal body temperature. Moreover, the metabolic rate decreases when the ambient temperature falls. As a result, the animal is much less active at cooler temperatures. Ectotherms may therefore be restricted to warmer climates, which limits their overall distribution.

Questions (predicted metabolic rate)

Panel B shows the metabolic rate of dinosaurs as gray squares and the dashed line. Recall that the metabolic rate of an extinct species cannot be directly measured.

B1. How did the researchers determine the predicted metabolic rate of the dinosaurs?

B2. How does the graph in panel A contribute to the validity of the dinosaur prediction?

B3. How do you think a mesothermic metabolism benefited the dinosaurs?

Answers B

B1. To determine the metabolic rate of different dinosaur species, the researchers used two of the available pieces of information in the fossil record: adult mass and maximum growth rate (bone growth rings).

B2. Panel A illustrates that using maximum growth rate is a reliable way to accurately predict the metabolic rate in extant (living) species. It should therefore also be a reliable approach to predict the metabolic rate of extinct species.

B3. Because of their large size, dinosaurs would have required an enormous amount of food for growth and being active. A mesothermic metabolic rate could have allowed them to use some metabolic heat to maintain a higher body temperature, allowing them to increase their range and maintain activity level when the ambient temperature fluctuated. Their large size and insulating feathers may have been enough to maintain an optimal body temperature without the high caloric cost of a true endothermic fast metabolic rate.

Our analyses are robust to variation in the scaling exponent, phylogenetic correction, inclusion of captive versus wild animals, critiques of dinosaur growth studies, and uncertainty in estimating M and metabolic temperature (9).

Our results find that mass-independent growth rates in dinosaurs were intermediate to, and significantly different from, those of endothermic and ectothermic taxa (table S2). Although some dinosaur growth rates overlap with high-power ectotherms or low-power endotherms, they cluster closest to energetically and thermally intermediate taxa, such as tuna (Fig. 2). Further, our analyses uphold the somewhat surprising finding that feathered dinosaurs, including protoavian Archaeopteryx (17), did not grow markedly differently from other dinosaurs (Fig. 4). It appears that modern avian energetics did not coincide with feathers or flight, which is consistent with fossil evidence that modern bone histology in birds did not appear until the late Cretaceous (18).

Phylogeny

This figure shows a phylogenetic tree of the animal groups compared by the researchers. Phylogenetic trees outline the evolutionary relationships of organisms. These relationships are determined by the number of homologies shared between the organisms that are compared.

Homologies are inherited features such as similar anatomical structures, DNA and protein sequences, and metabolic processes that provide evidence for common ancestry. The more homologies there are between two species, the more recently they shared a common ancestor. The most closely related species will share the longest branch before separating from each other.

This link provides more information regarding how DNA sequences are used to construct phylogenetic trees. http://www.hhmi.org/biointeractive/creating-phylogenetic-trees-dna-sequences

Phylogeny questions

1. Which group of organisms do dinosaurs share a more recent common ancestor with: fish (sharks, groupers, tuna), mammals (placentalia, echidna), reptiles (turtles, crocodiles), or birds (paleognathae)? Explain your answer.

2. Which likely evolved first in the ancestors of modern birds: feathers or a high metabolic rate to support endothermy? Provide evidence to support your claim.

3. Is endothermy a shared homology between birds (paleognathae) and mammals (placentalia)? Why or why not?

Phylogeny answers

1. Dinosaurs share the longest branch with birds (paleognathae). This means they share the most recent common ancestor with birds, followed by reptiles, and mammals. They are most distantly related to fish.

2. Feathers evolved prior to the high metabolic rate of birds. Tyrannosaurs, Trodon, and Archaeopteryx were feathered but had slower growth rates, indicating a slower metabolic rate characteristic of a mesothermic organism.

3. Endothermy likely evolved independently in birds and mammals. Birds share more homologies and therefore more recent ancestors with reptiles, which have the metabolic rates and growth rates of ectotherms and mesotherms, than with mammals.

Endothermy in birds and mammals is an example of convergent evolution in which similar selective pressures have results in the selection for and evolution of similar characteristics.

At the largest body masses, the growth rates of the largest dinosaurs and mammals overlap (Fig. 1B). This pattern is driven by two factors. First, dinosaurs have a relatively high slope (α_OLS = 0.82, but α_PIC = 0.76). This value is consistent with suggestions of thermal inertia for larger taxa; the removal of sauropods yields a reduced OLS slope of 0.77. Second, significantly reduced growth rates are observed in several large mammalian taxa, particularly primates, elephants, and toothed whales, whereas small shrews and rodents have relatively high rates, leading to a low overall slope for placental mammals (α_OLS = 0.64, α_PIC = 0.63; table S2 and fig. S11). The slow growth of many large endothermic mammals is associated with large brain size and low juvenile mortality (19, 20); this is unlikely to be relevant to most dinosaurs.

Our results highlight important similarities and differences from previous studies. For example, our work agrees with assessments by Erickson (7, 17) that dinosaurs grew at rates intermediate to most endo- and ectotherms. However, we find considerably more similarity in ectothermic growth rates than reported by Case (13) and significantly higher growth rates for fish (~seven times higher), marsupials (~four times higher) and precocial birds (~two times higher; fig. S8). We attribute these differences to enhanced sampling and standardization of the thermal environment for ectotherms (e.g., Case included temperate fish). Moreover, our expansion of the comparative growth framework indicates that dinosaurs grew and metabolized at rates most similar to those of active sharks and tuna (Fig. 2 and fig. S1), rather than those of endothermic marsupials, as has been suggested (17).

Past work has often struggled to fit dinosaurs into a simple energetic dichotomy; our work suggests that an intermediate view (17, 21) is more likely. Although dinosaur growth rates vary, they cluster most closely to those of thermally intermediate taxa (Figs. 1 and 2), which we term mesotherms. Mesothermic tuna, lamnid sharks, and the leatherback turtle rely on metabolic heat to raise their body temperature (T_b) above the ambient temperature (T_a) but do not metabolically defend a thermal set point as endotherms do (16, 22). This reliance on metabolic heat distinguishes them from other large homeothermic reptiles, such as crocodiles (23), which bask to elevate T_b. The echidna, while maintaining a set point of ~31°C, shows remarkable lability, because T_b values can range over 10°C while it is active (24). Unlike hibernating mammals or torpid hummingbirds, this variability is externally imposed. Collectively, these animals are distinguished from endotherms and ectotherms by a weak or absent metabolic defense of a thermal set point but sufficient internal heat production to maintain T_b > T_a when T_a is low [see (9) for further discussion]. Although some feathered dinosaurs may have been endotherms, they would have been uniquely low-powered compared to extant birds and mammals. We suggest that mesothermy may have been common among dinosaurs, ranging from modest metabolic control of T_b, as seen in furred echidnas, to the absent metabolic defense observed in tuna and leatherback turtles. Analysis of fossil isotopes, which can shed light on body temperatures, will be useful in testing this hypothesis. In particular, attention to neonate and juvenile dinosaurs in seasonally cool environments, such as polar regions, may help distinguish among thermoregulatory states.

Dinosaurs dominated the flux of matter and energy in terrestrial ecosystems for more than 135 million years. Consequently, our results have important implications for understanding ancient Mesozoic ecosystems. We emphasize the primary importance of comparative energetics for integrating form, function, and diversity. Knowing only two facts from the fossil record—adult mass and maximum growth rate—we show that the metabolic rates of extinct clades can be predicted with accuracy. Such an approach will be useful in resolving the energetics of metabolically ambiguous taxa, such as pterosaurs, therapsids, and Mesozoic birds.

Supplementary Materials

References and Notes

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