Warm-bloodedness of dinosaurs

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Note: in this article "dinosaur" means "non-avian dinosaur", since some experts regard birds as a specialised group of dinosaurs.

Scientific opinion about the life-style, metabolism and temperature regulation of dinosaurs has varied over time since the discovery of dinosaurs in the mid-19^th century:

Richard Owen coined the name "dinosaurs" in 1842 and speculated that they were active and warm-blooded. Most 19^th century scientists and illustrators (e.g. Charles R. Knight) followed this view.
In the first half of the 20^th century scientists emphasized dinosaurs' reptilian heritage and regarded them as sluggish and cold-blooded.
In 1968 Robert T. "Bob" Bakker, inspired by John Ostrom's analysis of Deinonychus, published a paper which proposed that dinosaurs were warm-blooded and active. This started a vigorous debate about the metabolism, activity level and temperature regulation of dinosaurs. At first, scientists broadly disagreed as to whether dinosaurs were capable of regulating their body temperatures at all. More recently, the warm-bloodedness of dinosaurs (more specifically, active lifestyle and at least fairly constant temperature) has become the consensus view, and debate has focused on the mechanisms of temperature regulation and how similar dinosaurs' metabolic rate was to that of birds and mammals.

[edit] Meaning of "warm-blooded" for dinosaurs

"Warm-bloodedness" is a complex and rather ambiguous term, because it includes some or all of:

Endothermy, i.e. the ability to generate heat internally rather than via behaviors such as basking or muscular activity.
Homeothermy, i.e. maintaining a fairly constant body temperature.
Tachymetabolism, i.e. maintaining a high metabolic rate, particularly when at rest. This requires a fairly high and stable body temperature, since: biochemical processes run about half as fast if an animal's temperature drops by 10°C; most enzymes have an optimum operating temperature and their efficiency drops rapidly outside the preferred range.

Since we can't know much about the internal mechanisms of extinct creatures, most discussion focuses on homeothermy and tachymetabolism.

Dinosaurs were around for about 150M years, so it is very likely that different groups evolved different metabolisms and thermoregulatory regimes and that some were very different from the original dinosaurs.

[edit] Evidence and arguments

[edit] Limb posture

Dinosaurs' limbs were erect and held under their bodies, rather than sprawling out to the sides like those of lizards and newts. The evidence for this is the angles of the joint surfaces and the locations of muscle and tendon attachments on the bones. Attempts to represent dinosaurs with sprawling limbs result in creatures with dislocated hips, knees, shoulders and elbows.

Carrier's constraint states that air-breathing vertebrates which have 2 lungs and flex their bodies sideways during locomotion find it very difficult to move and breathe at the same time. This severely limits their stamina and forces them to spend more time resting than moving.

Sprawling limbs require sideways flexing during locomotion (except for tortoises and turtles, which are very slow and rely on armor for protection). But despite Carrier's constraint sprawling limbs are efficient for creatures which spend most of their time resting on their bellies and only move for a few seconds at a time, because this arrangement minimizes the energy costs of getting up and lying down.

Erect limbs increase the costs of getting up and lying down, but avoid Carrier's constraint. This indicates that dinosaurs were active animals because natural selection would have favored the development of sprawling limbs if dinosaurs had been sluggish and spent most of their waking time resting. An active lifestyle requires a metabolism which quickly regenerates energy supplies and breaks down waste products which cause fatigue, i.e. it requires a fairly fast metabolism and a considerable degree of homeothermy.

[edit] Fast growth rates

No dinosaur egg has been found that is larger than a basketball and embryos of large dinosaurs have been found in relatively small eggs, e.g. Maiasaura. It appears that individual dinosaurs were rather short-lived, e.g. the oldest (at death) Tyrannosaurus found so far was 28 and the oldest sauropod was 38. So dinosaurs grew from small eggs to several tons in weight very quickly. This indicates that dinosaurs converted food into body weight very quickly, which requires a fairly fast metabolism both to forage actively and to assimilate the food quickly.

The most spectacular growth rate may be that of Tyrannosaurus rex (Erickson et al, 2004; Horner and Padian, 2004):

1 ton at age 10
very rapid growth to around 6 tons in the mid-teens (about 1 ton per year).
negligible growth after the mid-teens.

[edit] Polar dinosaurs

Dinosaur fossils have been found in Australia and Antarctica, where they would have experienced cold winters with no sunlight for several months. When these dinosaurs were alive Antarctica was near the South Pole and Australia was joined to Antarctica, but the polar regions were not permanently covered with ice. The polar dinosaurs were no better adapted for burrowing than other dinosaurs and, even if they conserved heat by insulation and huddling together, they must have been able to generate heat in order to survive the long winters.

Although the Mesozoic climate was warmer than today's, no fossils of undisputably cold-blooded land vertebrates (crocodilians, lizards or turtles / tortoises) have been found at the "polar dinosaur" sites.

[edit] Bone structure

Armand de Ricqles discovered Haversian canals in dinosaur bones. These canals are common in "warm-blooded" animals and are associated with fast growth and an active life style because they help to recycle bone in order to facilitate rapid growth and to repair damage caused by stress or injuries. The presence of Haversian canals in dinosaur bones was hailed as evidence of warm-bloodedness, but several researchers (including de Ricqules) later pointed out that dinosaur bones also often contained growth rings, which are associated with slow growth and slow metabolisms.

The presence of fibrolamellar bone (produced quickly and having a fibrous, woven appearance) in dinosaur fossils was also hailed as evidence of warm-bloodedness. But other researchers pointed out that fibrolamellar bone is also found in crocodilians, lizards and turtles, while the long bones (e.g. femurs) of many dinosaurs contain both fibrolamellar bone and lamellarzonal bone (layered bone associated with slow growth).

[edit] Feathers

There is now no doubt that many dinosaur species had feathers, including Shuvuuia, Sinosauropteryx and Dilong (an early tyrannosaur). These have been interpreted as insulation and therefore evidence of warm-bloodedness.

But impressions of feathers have only been found in coelurosaurs (which includes the ancestors of both birds and tyrannosaurs), so at present feathers give us no information about the metabolisms of the other major dinosaur groups, e.g. coelophysids, ceratosaurs, carnosaurs, sauropods or ornithischians.

In fact the fossilised skin of Carnotaurus (an abelisaurid) shows an unfeathered, reptile-like skin with rows of bumps. But an adult Carnotaurus weighed about 1 ton, and mammals of this size and larger have either very short hair or naked skins, so the skin of Carnotaurus tells us nothing about whether smaller non-coelurosaurid dinosaurs had feathers.

[edit] Dinosaur respiratory systems

This subject is currently the subject of intense and sometimes acrimonious debate (see for example A Reply to Ruben on Theropod Physiology.

[edit] Bird-like air sacs?

From about 1870 onwards scientists have generally agreed that the post-cranial skeletons of many dinosaurs contained many air-filled cavities (pleurocoels), especially in the vertebrae. For a long time these cavities were regarded simply as weight-saving devices, but Bakker (1972) proposed that they contained air sacs like those which make birds' respiratory systems the most efficient of all animals'.

Researchers have presented evidence and arguments for air sacs in:

sauropods (e.g. Wedel 2003)
ceratosaurs (e.g. O'Connor and Claessens 2005)
coelurosaurs (Naish et al. 2004 reports a preserved air sac)

If dinosaurs had bird-like air sacs, their respiratory systems were capable of sustaining higher activity levels than mammals of similar size and build can sustain.

John Ruben et al (1997, 1999) disputed this and suggested that dinosaurs had a crocodile-like respiratory system powered by a hepatic piston mechanism - muscles move parts of the abdominal skeleton, the bones move the liver backwards and forwards, and this compresses and expands the lungs. Other paleontologists disagreed, arguing that the crocodilian hepatic piston requires a broad, mobile and short pubis while dinosaurs had narrow, immobile and long pubic bones.

[edit] No respiratory turbinates?

Respiratory turbinates† (often referred to as "nasal turbinates" or "respiratory conchae") are convoluted structures of thin bone in the nasal cavity. In most mammals and birds these are present and lined with mucous membranes which warm and moisten inhaled air and extract heat and moisture from exhaled air, to prevent desiccation of the lungs.

Ruben et al have argued in several papers (1996, 1997, 1999, 2000) that dinosaurs lacked respiratory turbinates and therefore could not have sustained the breathing rate required for a mammal-like or bird-like metabolic rate, because their lungs would have dried out.

Objections raised against this argument include:

Respiratory turbinates are very delicate structures and unlikely to be preserved by fossilisation. The features which Ruben et al. regarded as evidence of the presence of respiratory turbinates in Mesozoic mammals are ambiguous.
Some birds (e.g. ratites, Procellariiformes and Falconiformes) and mammals (e.g. whales, anteaters, bats, elephants, and most primates) lack respiratory turbinates but are fully endothermic and in some cases very active (especially birds, bats and primates).

† Mammals' and birds' nasal passages also contain olfactory turbinates, which improve the sense of smell by increasing the area available for absorbing airborne chemicals. That is why this section uses the term "respiratory turbinates."

[edit] Internal organs

Fisher, Russell et al. (2000) reported that they had found a dinosaur's heart in South Dakota and that it was 4-chambered, like that of mammals and birds and unlike the 3-chambered hearts of lizards and snakes. This was greeted by some as evidence that dinosaurs were warm-blooded. But an increasing number of paleontologists suspected that it was an accidental concretion of iron-rich material rather than a heart (see for example Dinosaur with a Heart of Stone), and discussion of it ceased rather quickly.

[edit] Predator-prey ratios

Bakker argued that:

cold-blooded predators need much less food than warm-blooded ones, so a given mass of prey can support far more cold-blooded predators than warm-blooded ones.
the ratio of the total mass of predators to prey in dinosaur communities was much more like that of modern and recent warm-blooded communities than that of recent or fossil cold-blooded communities.
hence predatory dinosaurs were warm-blooded. And since the earliest dinosaurs (e.g. Staurikosaurus, Herrerasaurus) were predators, all dinosaurs must have been warm-blooded.

This argument was criticised on several grounds and is no longer taken seriously:

Estimates of dinosaur weights are just educated guesses.
Fossil beds may not accurately represent the actual populations, e.g. smaller and younger animals have less robust bones and are therefore less likely to be preserved.
There are no communities of large, cold-blooded animals to-day, so we have no grounds for assuming that such communities would have higher predator-prey ratios.
How do we know what ate what? For example most predators are also scavengers and large scavengers face competition from a lot of small scavengers (bacteria, fungi, insects, etc.). And in the modern world there is no relationship between metabolism and what preys on what, for example roadrunners eat anything they can catch and many reptiles prey on mammals.
We don't know much about how non-predator dinosaurs might have defended themselves, and a well-defended prey population would support fewer predators than a poorly-defended population.

[edit] Oxygen isotope ratios

The ratio of ¹⁶O and ¹⁸O in bone depends on the temperature at which the bone was formed - the higher the temperature, the more ¹⁶O.

Barrick and Showers (1999) analyzed the isotope ratios in two theropods that lived in temperate regions with seasonal variation in temperature, Tyrannosaurus (USA) and Giganotosaurus (Argentina):

dorsal vertebrae from both dinosaurs showed no sign of seasonal variation, indicating that both maintained a constant core temperature despite seasonal variations in air temperature.
ribs and leg bones from both dinosaurs showed greater variability in temperature and a lower average temperature as the distance from the vertebrae increased.

Barrick and Showers concluded that:

both dinosaurs were endothermic but at lower metabolic levels than modern mammals.
inertial homeothermy was an important part of their temperature regulation as adults.

[edit] The crocodilian puzzle

Crocodilians present some puzzles if one regards dinosaurs as active animals with fairly constant body temperatures. Crocodilians evolved shortly before dinosaurs and, second to birds, are dinosaurs' closest living relatives - but modern crocodilians are cold-blooded. This raises some questions:

If dinosaurs were to a large extent "warm-blooded", when and how fast did warm-bloodedness evolve in their lineage?
Modern crocodilians are cold-blooded but have several features associated with warm-bloodedness. How did they acquire these features?

[edit] Evolution of warm-bloodedness in dinosaurs and their ancestors

It appears that the earliest dinosaurs had the features on which the arguments for warm-blooded dinosaurs are based - especially erect limbs. This raises the question "How did dinosaurs become warm-blooded?" The most obvious possible answers are:

"Their immediate ancestors (archosaurs) were cold-blooded, and dinosaurs developed warm-bloodedness very early in their evolution." This would imply that dinosaurs developed warm-bloodedness in a very short time, less than 20M years and probably less than 10M years. But in mammals' therapsid ancestors the evolution of warm-bloodedness seems to have taken at least twice as long, starting with the beginnings of a secondary palate around the beginning of the mid-Permian (Kermack and Kermack 1980) and going on at least until the appearance of hair (the first known occurrence is possibly in the early-Triassic Thrinaxodon).
"Dinosaurs' immediate ancestors (archosaurs) were at least fairly warm-blooded, and dinosaurs evolved further in that direction." This answer raises 2 problems: (A) The early evolution of archosaurs is still very poorly understood - large numbers of individuals and species are found from the start of the Triassic but only 2 species are known from the very late Permian (Archosaurus rossicus and Protorosaurus speneri); (B) Crocodilians evolved shortly before dinosaurs and are closely related to them, but are cold-blooded (see below).

[edit] "Warm-blooded" features of crocodilians

Modern crocodilians are cold-blooded but have several features associated with warm-bloodedness because they improve the animal's oxygen supply:

4-chambered hearts. Mammals and birds have 4-chambered hearts. Non-crocodilian reptiles have 3-chambered hearts, which are less efficient because they allow oxygenated and de-oxygenated blood to mix and therefore send some de-oxygenated blood out to the body instead of to the lungs. Modern crocodilians' hearts are 4-chambered, but are smaller relative to body size and run at lower pressure than those of modern mammals and birds. They also have a bypass which makes then functionally 3-chambered when under water, conserving oxygen.
a secondary palate, which allows the animal to eat and breathe at the same time.
a hepatic piston mechanism for pumping the lungs. This is different from the lung-pumping mechanisms of mammals and birds but similar to what some researchers claim to have found in some dinosaurs.

So why did natural selection favor the development of these features, which are very important for active warm-blooded creatures but of little apparent use to cold-blooded aquatic ambush predators which spend the vast majority of their time floating in water or lying on river banks?

Some experts believe that crocodilians were originally active, warm-blooded predators and that their archosaur ancestors were warm-blooded (Summers 2005; Seymour, Bennett-Stamper, Johnston, Carrier, and Grigg 2004). Developmental studies indicate that crocodilian embryos develop fully 4-chambered hearts first and then develop the modifications which make their hearts function as 3-chambered under water. Using the principle that ontogeny recapitulates phylogeny, the researchers concluded that the original crocodilians had fully 4-chambered hearts and were therefore warm-blooded and that later crocodilians developed the bypass as they reverted to being cold-blooded aquatic ambush predators.

If this view is correct, the development of warm-bloodedness in archosaurs (reaching its peak in dinosaurs) and in mammals would have taken similar amounts of time. It would also be consistent with the fossil evidence:

The earliest crocodilians, e.g. terrestrisuchus, were slim, leggy terrestrial predators.
Other archosaurs appear to have had erect limbs, and those of rauisuchians are very poorly adapted for any other posture.

[edit] How could dinosaurs have maintained stable, fairly high temperatures?

If dinosaurs were at least fairly warm-blooded (which is still subject to debate), one has to ask how they maintained stable, fairly high temperatures. Several mechanisms have been proposed, and at least some dinosaurs may have used combinations of mechanisms or different mechanisms at different stages in their lives.

[edit] Inertial homeothermy

Inertial homeothermy is found in many large creatures - because of their low ratios of surface area to volume, they lose and gain heat very slowly. But the earliest dinosaurs, many later dinosaurs and the young of all dinosaurs were too small to benefit from inertial homeothermy.

[edit] Gut fermentation

When large animals eat coarse vegetation, digestion takes so long that the food ferments and generates heat. But this mechanism is impossible for carnivores and for the small dinosaurs mentioned above.

[edit] Behavioral methods

Some dinosaurs, e.g. Spinosaurus and Ouranosaurus, had on their backs "sails" supported by spines growing up from the vertebrae. (This was also true, incidentally, for the Synapsid Dimetrodon.) Such dinosaurs could have used these sails to:

take in heat by basking with the "sails" at right angles to the sun's rays.
to lose heat by using the "sails" as radiators while standing in the shade or while facing directly towards or away from the sun.

But these were a very small minority of all the dinosaur species which are known.

[edit] Metabolic heat generation

Birds and mammals generate heat by converting fat into energy - this is known as endothermy.

If dinosaurs were at least fairly warm-blooded, endothermy is the only known thermoregulatory mechanism which would have been available to small species and to very young dinosaurs.

[edit] References

Bakker, R. T. (1972). Anatomical and ecological evidence of endothermy in dinosaurs. Nature 238:81-85.
Erickson, G., et al (2004). Nature, August 2004. (Paper on T rex growth rates).
Fisher, P.E., D.A. Russell, M.K. Stoskopf . . . M. Hammer, et al. (2000). 'Cardiovascular evidence for an intermediate or higher metabolic rate in an ornithischian dinosaur. Science 288(April 21):503-505
Horner, J. R., and Padian,K. (2004). Age and growth dynamics of Tyrannosaurus rex. Proceedings of the Royal Society of London B 271: 18751880.
Kermack, D.M. and Kermack, K.A. (1984). The evolution of mammalian characters. Croom Helm Kapitan Szabo Publishers, London. pp 149. ISBN 0-7099-1534-9
Naish, D., Martill, D. M. & Frey, E. (2004). Ecology, systematics and biogeographical relationships of dinosaurs, including a new theropod, from the Santana Formation (?Albian, Early Cretaceous) of Brazil. Historical Biology 16, 57-70.
O'Connor, P., and Claessens, L. (2005). Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs, Nature 436, 253 - 256
Ricqles, A. J. de. (1974). Evolution of endothermy: histological evidence. Evolutionary Theory 1: 51-80
Ruben et al. (1996). The metabolic status of some Late Cretaceous dinosaurs. Science 273: 120-147.
Ruben et al. (1997). Lung structure and ventilation in theropod dinosaurs and early birds. Science 278: 1267-1247.
Ruben et al. 1998. Lung ventilation and gas exchange in theropod dinosaurs. Science 481: 4748
Ruben et al. 1999. Pulmonary function and metabolic physiology of theropod dinosaurs. Science 283: 514-516.
Ruben, J. & Jones, T. D. (2000). Selective factors associated with the origin of fur and feathers. American Zoologist 40(4): 585-596
Seymour, R. S., Bennett-Stamper, C. L., Johnston, S. D., Carrier, D. R. and Grigg, G. C. (2004). Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiol. Biochem. Zool. 77: 1051?1067
Summers, A.P. (2005). Evolution: Warm-hearted crocs. Nature 434: 833-834
Wedel, M.J. (2003). Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29(2):243-255 (currently online at findarticles.com

[edit] Links

Thermophysiology and Biology of Giganotosaurus: Comparison with Tyrannosaurus by RE Barrick and WJ Showers (1999)
Heart of a Dinosaur Is Reported Found
Crocodile evolution no heart-warmer

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Categories: Dinosaurs | Paleontology | Paleozoology