Physiology of dinosaurs

Note: In this article "dinosaur" means "non-avian dinosaur," since most experts regard birds as an advanced group of dinosaurs.

The physiology of dinosaurs has historically been a controversial subject, particularly thermoregulation. Recently, many new lines of evidence have been brought to bear on dinosaur physiology generally, including not only metabolic systems and thermoregulation, but on respiratory and cardiovascular systems as well.

During the early years of dinosaur paleontology, it was widely considered that they were sluggish, cumbersome, and sprawling cold-blooded lizards. However, with the discovery of much more complete skeletons in the western United States, starting in the 1870s, scientists could make more informed interpretations of dinosaur biology and physiology. Edward Drinker Cope, opponent of Othniel Charles Marsh in the Bone Wars, propounded at least some dinosaurs as active and agile, as seen in the painting of two fighting "Laelaps" produced under his direction by Charles R. Knight.[1] In parallel, the development of Darwinian evolution, and the discoveries of Archaeopteryx and Compsognathus, led Thomas Henry Huxley to propose that dinosaurs were closely related to birds.[2] Despite these considerations, the image of dinosaurs as large reptiles had taken root,[1] and most aspects of their paleobiology were interpreted as being typically reptilian for the first half of the twentieth century.[3] Beginning in the 1960s and with the advent of the Dinosaur Renaissance, views of dinosaurs and the physiology have changed dramatically, including the discovery of feathered dinosaurs in Early Cretaceous age deposits in China, indicating that birds evolved from highly agile maniraptoran dinosaurs.

Contents

History of study

Early interpretations of dinosaurs: 1820s to early 1900s

The study of dinosaurs began in the 1820s in England. Pioneers in the field, such as William Buckland, Gideon Mantell, and Richard Owen, interpreted the first, very fragmentary remains as belonging to large quadrupedal beasts.[4] Their early work can be seen today in the Crystal Palace Dinosaurs, constructed in the 1850s, which present known dinosaurs as elephantine lizard-like reptiles.[5] Despite these reptilian appearances, Owen speculated that dinosaur heart and respiratory systems were more mammal-like than reptile-like.[4]

Changing views and the Dinosaur Renaissance

However, in the late 1960s views began to change, beginning with John Ostrom's work on Deinonychus and bird evolution.[6] His student, Bob Bakker, popularized the changing thought in a series of papers beginning with The superiority of dinosaurs in 1968.[7] In these publications, he argued strenuously that dinosaurs were warm-blooded and active animals, capable of sustained periods of high activity. In most of his writings Bakker framed his arguments as new evidence leading to a revival of ideas popular the late 19th century, frequently referring to an ongoing dinosaur renaissance. He used a variety of anatomical and statistical arguments to defend his case,[8][9] the methodology of which was fiercely debated among scientists.[10]

These debates sparked interest in new methods for ascertaining the palaeobiology of extinct animals, such as bone histology, which have been successfully applied to determining the growth-rates of many dinosaurs.

Today, it is generally thought that many or perhaps all dinosaurs had higher metabolic rates than living reptiles, but also that the situation is more complex and varied than Bakker originally proposed. For example, while smaller dinosaurs may have been true endotherms, the larger forms could have been inertial homeotherms,[11][12] or many dinosaurs could have had intermediate metabolic rates.[13]

Feeding and digestion

The earliest dinosaurs were almost certainly predators, and shared several predatory features with their nearest non-dinosaur relatives like Lagosuchus, including: relatively large, curved, blade-like teeth in large, wide-opening jaws that closed like scissors; relatively small abdomens, as carnivores do not require large digestive systems. Later dinosaurs regarded as predators sometimes grew much larger, but retain the same set of features. Instead of chewing their food, these predators swallowed it whole.[14]

The feeding habits of ornithomimosaurs and oviraptorosaurs are a mystery: although they evolved from a predatory theropod lineage, they have small jaws and lack the blade-like teeth of typical predators, but there is no evidence of their diet or how they ate and digested it.[14]

Features of other groups of dinosaurs indicate they were vegetarians. These features include:

Sauropods, which were vegetarians, did not chew their food, as their teeth and jaws appear suitable only for stripping leaves off plants. Ornithischians, also vegetarians, show a variety of approaches. The armored ankylosaurs and stegosaurs had small heads and weak jaws and teeth, and are thought to have fed in much the same way as sauropods. The pachycephalosaurs had small heads and weak jaws and teeth, but their lack of large digestive systems suggests a different diet, possibly fruits, seeds, or young shoots, which would have been more nutritious than leaves.[14]

On the other hand ornithopods such as Hypsilophodon, Iguanodon and various hadrosaurs had horny beaks for snipping off vegetation and jaws and teeth that were well-adapted for chewing. The horned ceratopsians had similar mechanisms.[14]

It has often been suggested that at least some dinosaurs used swallowed stones, known as gastroliths, to aid digestion by grinding their food in muscular gizzards, and that this was a feature they shared with birds. In 2007 Oliver Wings reviewed references to gastroliths in scientific literature and found considerable confusion, starting with the lack of an agreed and objective definition of "gastrolith". He found that swallowed hard stones or grit can assist digestion in birds that mainly feed on grain but may not be essential—and that birds that eat insects in summer and grain in winter usually get rid of the stones and grit in summer. Gastroliths have often been described as important for sauropod dinosaurs, whose diet of vegetation required very thorough digestion, but Wings concluded that this idea was incorrect: gastroliths are found with only a small percentage of sauropod fossils; where they have been found, the amounts are too small and in many cases the stones are too soft to have been effective in grinding food; most of these gastroliths are highly polished, but gastroliths used by modern animals to grind food are roughened by wear and corroded by stomach acids; hence the sauropod gastroliths were probably swallowed accidentally. On the other hand he concluded that gastroliths found with fossils of advanced theropod dinosaurs such as Sinornithomimus and Caudipteryx resemble those of birds, and that the use of gastroliths for grinding food may have appeared early in the group of dinosaurs from which these dinosaurs and birds both evolved.[15][16]

Reproductive biology

When laying eggs, females of some bird species grow a special type of bone in their limbs between the hard outer bone and the marrow. This medullary bone, which is rich in calcium, is used to make eggshells, and the birds that produced it absorb it when they have finished laying eggs.[17] Medullary bone has been found in fossils of the theropods Tyrannosaurus and Allosaurus and of the ornithopod Tenontosaurus.[17][18]

Because the line of dinosaurs that includes Allosaurus and Tyrannosaurus diverged from the line that led to Tenontosaurus very early in the evolution of dinosaurs, the presence of medullary bone in both groups suggests that dinosaurs in general produced medullary tissue. On the other hand crocodilians, which are dinosaurs' second closest living relatives after birds, do not produce medullary bone. This tissue may have first appeared in ornithodires, the Triassic archosaur group from which dinosaurs are thought to have evolved.[17]

Medullary bone has been found in specimens of sub-adult size, which suggests that dinosaurs reached sexual maturity before they were fully-grown. Sexual maturity at sub-adult size is also found in reptiles and in medium- to large-sized mammals, but birds and small mammals reach sexual maturity only after they are fully-grown—which happens within their first year. Early sexual maturity is also associated with specific features of animals' life cycles: the young are born relatively well-developed rather than helpless; and the death-rate among adults is high.[17]

Respiratory System

Air sacs

From about 1870 onwards scientists have generally agreed that the post-cranial skeletons of many dinosaurs contained many air-filled cavities (postcranial skeletal pneumaticity, especially in the vertebrae. Pneumatization of the skull (such as paranasal sinuses) is found in both synapsids and archosaurs, but postcranial pneumatization is found only in birds, non-avian saurischian dinosaurs, and pterosaurs.

For a long time these cavities were regarded simply as weight-saving devices, but Bakker proposed that they contained air sacs like those that make birds' respiratory systems the most efficient of all animals'.[9]

John Ruben et al. (1997, 1999, 2003, 2004) disputed this and suggested that dinosaurs had a "tidal" respiratory system (in and out) powered by a crocodile-like hepatic piston mechanism - muscles attached mainly to the pubis pull the liver backwards, which makes the lungs expand to inhale; when these muscles relax, the lungs return to their previous size and shape, and the animal exhales. They also presented this as a reason for doubting that birds descended from dinosaurs.[19][20][21][22][23]

Critics have claimed that, without avian air sacs, modest improvements in a few aspects of a modern reptile's circulatory and respiratory systems would enable the reptile to achieve 50% to 70% of the oxygen flow of a mammal of similar size,[24] and that lack of avian air sacs would not prevent the development of endothermy.[25] Very few formal rebuttals have been published in scientific journals of Ruben et al.’s claim that dinosaurs could not have had avian-style air sacs; but one points out that the Sinosauropteryx fossil on which they based much of their argument was severely flattened and therefore it was impossible to tell whether the liver was the right shape to act as part of a hepatic piston mechanism.[26] Some recent papers simply note without further comment that Ruben et al. argued against the presence of air sacs in dinosaurs.[27]

Researchers have presented evidence and arguments for air sacs in sauropods, "prosauropods", coelurosaurs, ceratosaurs, and the theropods Aerosteon and Coelophysis.

In advanced sauropods ("neosauropods") the vertebrae of the lower back and hip regions show signs of air sacs. In early sauropods only the cervical (neck) vertebrae show these features. If the developmental sequence found in bird embryos is a guide, air sacs actually evolved before the channels in the skeleton that accommodate them in later forms.[28][29]

Evidence of air sacs has also been found in theropods. Studies indicate that fossils of coelurosaurs,[30] ceratosaurs,[27] and the theropods Coelophysis and Aerosteon exhibit evidence of air sacs. Coelophysis, from the late Triassic, is one of the earliest dinosaurs whose fossils show evidence of channels for air sacs.[29] Aerosteon, a Late Cretaceous allosaur, had the most bird-like air sacs found so far.[31]

Early sauropodomorphs, including the group traditionally called "prosauropods", may also have had air sacs. Although possible pneumatic indentations have been found in Plateosaurus and Thecodontosaurus, the indentations are very small. One study in 2007 concluded that prosauropods likely had abdominal and cervical air sacs, based on the evidence for them in sister taxa (theropods and sauropods). The study concluded that it was impossible to determine whether prosauropods had a bird-like flow-through lung, but that the air sacs were almost certainly present.[32] A further indication for the presence of air sacs and their use in lung ventilation comes from a reconstruction of the air exchange volume (the volume of air exchanged with each breath) of Plateosaurus, which when expressed as a ratio of air volume per body weight at 29 ml/kg is similar to values of geese and other birds, and much higher than typical mammalian values.[33]

So far no evidence of air sacs has been found in ornithischian dinosaurs. But this does not imply that ornithischians could not have had metabolic rates comparable to those of mammals, since mammals also do not have air sacs.[34]

Three explanations have been suggested for the development of air sacs in dinosaurs:[31]

Calculations of the volumes of various parts of the sauropod Apatosaurus’ respiratory system support the evidence of bird-like air sacs in sauropods:

On this basis, Apatosaurus could not have had a reptilian respiratory system, as its tidal volume would have been less than its dead-space volume, so that stale air was not expelled but was sucked back into the lungs. Likewise, a mammalian system would only provide to the lungs about 225 − 184 = 41 liters of fresh, oxygenated air on each breath. Apatosaurus must therefore have had either a system unknown in the modern world or one like birds', with multiple air sacs and a flow-through lung. Furthermore, an avian system would only need a lung volume of about 600 liters while a mammalian one would have required about 2,950 liters, which would exceed the estimated 1,700 liters of space available in a 30-ton Apatosaurus′ chest.[35]

Dinosaur respiratory systems with bird-like air sacs may have been capable of sustaining higher activity levels than mammals of similar size and build can sustain. In addition to providing a very efficient supply of oxygen, the rapid airflow would have been an effective cooling mechanism, which is essential for animals that are active but too large to get rid of all the excess heat through their skins.[34]

Uncinate processes on the ribs

Birds have spurs called "uncinate processes" on the rear edges of their ribs, and these give the chest muscles more leverage when pumping the chest to improve oxygen supply. The size of the uncinate processes is related to the bird's lifestyle and oxygen requirements: they are shortest in walking birds and longest in diving birds, which need to replenish their oxygen reserves quickly when they surface. Non-avian maniraptoran dinosaurs also had these uncinate processes, and they were proportionately as long as in modern diving birds, which indicates that maniraptorans needed a high-capacity oxygen supply.[36][37]

Plates that may have functioned the same way as uncinate processes have been observed in fossils of the ornithischian dinosaur Thescelosaurus, and have been interpreted as evidence of high oxygen consumption and therefore high metabolic rate.[38]

Nasal turbinates

Nasal turbinates (often referred to as "turbinals" or "conchae") are convoluted structures of thin bone in the nasal cavity. In most mammals and birds these are present and lined with mucous membranes that perform two functions. They improve the sense of smell by increasing the area available to absorb airborne chemicals—and they 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 that:[19][20][21][39][40]

However, objections have been raised against this argument:

Cardiovascular system

In principle one would expect dinosaurs to have had two-part circulations driven by four-chambered hearts, since many would have needed high blood pressure to deliver blood to their heads, which were high off the ground, but vertebrate lungs can only tolerate fairly low blood pressure.[34] In 2000, a skeleton of Thescelosaurus, now on display at the North Carolina Museum of Natural Sciences, was described as including the remnants of a four-chambered heart and an aorta. The authors interpreted the structure of the heart as indicating an elevated metabolic rate for Thescelosaurus, not reptilian cold-bloodedness.[46] Their conclusions have been disputed; other researchers published a paper where they assert that the heart is really a concretion of entirely mineral "cement". As they note: the anatomy given for the object is incorrect, for example the alleged "aorta" is narrowest where it meets the "heart" and lacks arteries branching from it; the "heart" partially engulfs one of the ribs and has an internal structure of concentric layers in some places; and another concretion is preserved behind the right leg.[47] The original authors defended their position; they agreed that the chest did contain a type of concretion, but one that had formed around and partially preserved the more muscular portions of the heart and aorta.[48]

Regardless of the object's identity, it may have little relevance to dinosaurs' internal anatomy and metabolic rate. Both modern crocodilians and birds, the closest living relatives of dinosaurs, have four-chambered hearts, although modified in crocodilians, and so dinosaurs probably had them as well. However such hearts are not necessarily tied to metabolic rate.[49]

Growth and lifecycle

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.[50] Like mammals, dinosaurs stopped growing when they reached the typical adult size of their species, while mature reptiles continue to grow slowly if they have enough food. Dinosaurs of all sizes grew faster than similarly sized modern reptiles; but the results of comparisons with similarly sized "warm-blooded" modern animals depend on their sizes:[51][52]

Weight (kg) Comparative growth rate of dinosaurs Modern animals in this size range
0.22 Slower than marsupials Rat
1 - 20 Similar to marsupials, slower than precocial birds (those that are born capable of running) From guinea pig to Andean Condor
100 - 1000 Faster than marsupials, similar to precocial birds, slower than placental mammals From Red Kangaroo to Polar Bear
1500 – 3500 Similar to most placental mammals From American Bison to rhinoceros
25000 and over Very fast, similar to modern whales; but about half that of a scaled-up altricial bird (one that is born helpless) - if one could scale up a bird to 25,000 kilograms (25 long tons; 28 short tons) Whales

Tyrannosaurus rex showed a "teenage growth spurt":[53][54]

A 2008 study of one skeleton of the hadrosaur Hypacrosaurus concluded that this dinosaur grew even faster, reaching its full size at the age of about 15; the main evidence was the number and spacing of growth rings in its bones. The authors found this consistent with a life-cycle theory that prey species should grow faster than their predators if they lose a lot of juveniles to predators and the local environment provides enough resources for rapid growth.[55]

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.[53] Predation was probably responsible for the high death rate of very young dinosaurs and sexual competition for the high death rate of sexually mature dinosaurs.[56]

Metabolism

Scientific opinion about the life-style, metabolism and temperature regulation of dinosaurs has varied over time since the discovery of dinosaurs in the mid-19th century. The activity of metabolic enzymes varies with temperature, so temperature control is vital for any organism, whether endothermic or ectothermic. Organisms can be categorized as poikilotherms (poikilo - changing), which are tolerant of internal temperature fluctuations, and homeotherms (homeo - same), which must maintain a constant core temperature. Animals can be further categorized as endotherms, which regulate their temperature internally, and ectotherms, which regulate temperature by the use of external heat sources.

The current consensus view suggests that dinosaur metabolism did not closely match any found in living vertebrates, and, consequently, that they cannot be categorized as either "warm" or "cold-blooded." Rather, they lie somewhere on the spectrum between poikilothermy and homeothermy. Consequently, current research focuses on mechanisms of metabolism and temperature regulation, and the similarities between dinosaurian, avian and mammalian metabolisms.[57]

What the debate is about

See also: Gigantothermy

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

Large dinosaurs may also have maintained their temperatures by inertial homeothermy, also known as "bulk homeothermy" or "mass homeothermy". In other words, the thermal capacity of such large animals was so high that that it would take two days or more for their temperatures to change significantly, and this would have smoothed out variations caused by daily temperature cycles. This smoothing effect has been observed in large turtles and crocodilians, but Plateosaurus, which weighed about 700 kilograms (1,500 lb), may have been the smallest dinosaur in which it would have been effective. Inertial homeothermy would not have been possible for small species nor for the young of larger species.[34] Vegetation fermenting in the guts of large herbivores can also produce considerable heat, but this method of maintaining a high and stable temperature would not have been possible for carnivores nor for small herbivores or the young of larger herbivores.[59]

Since the internal mechanisms of extinct creatures are unknowable, most discussion focuses on homeothermy and tachymetabolism.

Assessment of metabolic rates is complicated by the distinction between the rates while resting and while active. In all modern reptiles and most mammals and birds the maximum rates during all-out activity are 10 to 20 times higher than minimum rates while at rest. However in a few mammals these rates differ by a factor of 70. Theoretically it would be possible for a land vertebrate to have a reptilian metabolic rate at rest and a bird-like rate while working flat out. However an animal with such a low resting rate would be unable to grow quickly. The huge herbivorous sauropods may have been on the move so constantly in search of food that their energy expenditure would have been much the same irrespective of whether their resting metabolic rates were high or low.[60]

Metabolic options

The main possibilities are that:[34]

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

If all or some dinosaurs had intermediate metabolisms, they may have had the following features:[34]

Robert Reid has suggested that such animals could be regarded as "failed endotherms". He envisaged both dinosaurs and the Triassic ancestors of mammals passing through a stage with these features. Mammals were forced to become smaller as archosaurs came to dominate ecological niches for medium to large animals. Their decreasing size made them more vulnerable to heat loss because it increased their ratios of surface area to mass, and thus forced them to increase internal heat generation and thus become full endotherms. On the other hand dinosaurs became medium to very large animals and thus were able to retain the "intermediate" type of metabolism.[34]

Bone structure

Armand de Ricqlès discovered Haversian canals in dinosaur bones, and argued that they were evidence of endothermy in dinosaurs. 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 to facilitate rapid growth and repair damage caused by stress or injuries.[61] Dense secondary Haversian bone, which is formed during remodeling, is found in many living endotherms as well as dinosaurs, pterosaurs and therapsids. Secondary Haversian canals are correlated with size and age, mechanical stress and nutrient turnover. The presence of secondary Haversian canals suggests comparable bone growth and lifespans in mammals and dinosaurs.[62] Bakker argued that the presence of fibrolamellar bone (produced quickly and having a fibrous, woven appearance) in dinosaur fossils was evidence of endothermy.[9]

However as a result of other, mainly later research, bone structure is not considered a reliable indicator of metabolism in dinosaurs, mammals or reptiles:

Nevertheless de Ricqlès persevered with studies of the bone structure of dinosaurs and archosaurs. In mid-2008 he co-authored a paper that examined bone samples from a wide range of archosaurs, including early dinosaurs, and concluded that:[69]

Growth rates

Dinosaurs grew from small eggs to several tons in weight relatively quickly. A natural interpretation of this is that 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.[70] Developing bone found in juveniles is distinctly porous, which has been linked to vascularization and bone deposition rate, all suggesting growth rates close to those observed in modern birds.

But a preliminary study of the relationship between adult size, growth rate, and body temperature concluded that larger dinosaurs had higher body temperatures than smaller ones had; Apatosaurus, the largest dinosaur in the sample, was estimated to have a body temperature exceeding 41 °C (106 °F), whereas smaller dinosaurs were estimated to have body temperatures around 25 °C (77 °F)[71] – for comparison, normal human body temperature is about 37 °C (99 °F).[72][73] Based on these estimations, the study concluded that large dinosaurs were inertial homeotherms (their temperatures were stabilized by their sheer bulk) and that dinosaurs were ectothermic (in colloquial terms, "cold-blooded", because they did not generate as much heat as mammals when not moving or digesting food).[71] These results are consistent with the relationship between dinosaurs' sizes and growth rates (described above).[51][52] Studies of the sauropodomorph Massospondylus and early theropod Syntarsus (Megapnosaurus) reveal growth rates of 3 kg/year and 17 kg/year, respectively, much slower than those estimated of Maiasaura and observed in modern birds.[62]

Oxygen isotope ratios in bone

The ratio of the isotopes 16O and 18O in bone depends on the temperature the bone formed at: 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):[74]

Barrick and Showers concluded that both dinosaurs were endothermic but at lower metabolic levels than modern mammals, and that inertial homeothermy was an important part of their temperature regulation as adults. Their similar analysis of some Late Cretaceous ornithischians in 1996 concluded that these animals showed a similar pattern.[75]

However this view has been challenged. The evidence indicates homeothermy, but by itself cannot prove endothermy. Secondly, the production of bone may not have been continuous in areas near the extremities of limbs – in allosaur skeketons lines of arrested growth ("LAGs"; rather like growth rings) are sparse or absent in large limb bones but common in the fingers and toes. While there is no absolute proof that LAGs are temperature-related, they could mark times when the extremities were so cool that the bones ceased to grow. If so, the data about oxygen isotope ratios would be incomplete, especially for times when the extremities were coolest. Oxygen isotope ratios may be an unreliable method of estimating temperatures if it cannot be shown that bone growth was equally continuous in all parts of the animal.[34]

Predator-prey ratios

Bakker argued that:[76]

This argument was criticized on several grounds and is no longer taken seriously (the following list of criticisms is far from exhaustive):[77][78]

Posture and gait

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.[79]

Carrier's constraint states that air-breathing vertebrates with two lungs that flex their bodies sideways during locomotion find it difficult to move and breathe at the same time. This severely limits stamina, and forces them to spend more time resting than moving.[80]

Sprawling limbs require sideways flexing during locomotion (except for tortoises and turtles, which are very slow and whose armor keeps their bodies fairly rigid). However, despite Carrier's constraint, sprawling limbs are efficient for creatures that 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 retention of sprawling limbs if dinosaurs had been sluggish and spent most of their waking time resting. An active lifestyle requires a metabolism that 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.

Additionally, an erect posture demands precise balance, the result of a rapidly functioning neuromuscular system. This suggests endothermic metabolism, because an ectothermic animal would be unable to walk or run, and thus to evade predators, when its core temperature was lowered. Other evidence for endothermy includes limb length (many dinosaurs possessed comparatively long limbs) and bipedalism, both found today only in endotherms.[81] Many bipedal dinosaurs possessed gracile leg bones with a short thigh relative to calf length. This is generally an adaptation to frequent sustained running, characteristic of endotherms which, unlike ectotherms, are capable of producing sufficient energy to stave off the onset of anaerobic metabolism in the muscle.[82]

Bakker and Ostrom both pointed out that all dinosaurs had erect hindlimbs and that all quadrupedal dinosaurs except the ceratopsians and ankylosaurs had erect forelimbs; and that among living animals only the endothermic ("warm-blooded") mammals and birds have erect limbs (Ostrom acknowledged that crocodilians' occasional "high walk" was a partial exception). Bakker claimed this was clear evidence of endothermy in dinosaurs, while Ostrom regarded it as persuasive but not conclusive.[9][83]

A 2009 study supported the hypothesis that endothermy was widespread in at least larger non-avian dinosaurs, and that It was plausibly ancestral for all dinosauriforms, based on the biomechanics of running.[84]

Feathers

Main article : Feathered dinosaurs

There is now no doubt that many theropod dinosaur species had feathers, including Shuvuuia, Sinosauropteryx and Dilong (an early tyrannosaur).[85][26][86] 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 and therefore not a coelurosaur) shows an unfeathered, reptile-like skin with rows of bumps.[87] But an adult Carnotaurus weighed about 1 ton, and mammals of this size and larger have either very short hair or naked skins, so perhaps the skin of Carnotaurus tells us nothing about whether smaller non-coelurosaurid theropods had feathers.

Skin-impressions of Pelorosaurus and other sauropods (dinosaurs with elephantine bodies and long necks) reveal large hexagonal scales, and some sauropods, such as Saltasaurus, had bony plates in their skin.[88] The skin of ceratopsians consisted of large polygonal scales, sometimes with scattered circular plates.[89] "Mummified" remains and skin impressions of hadrosaurids reveal pebbly scales. It is unlikely that the ankylosaurids, such as Euoplocephalus, had insulation, as most of their surface area was covered in bony knobs and plates.[90] Likewise there is no evidence of insulation in the stegosaurs. Thus insulation, and the elevated metabolic rate behind evolving them, may have been limited to the theropods, or even just a subset of theropods.

Polar dinosaurs

Dinosaur fossils have been found in regions that were close to the poles at the relevant times, notably in southeastern Australia, Antarctica and the North Slope of Alaska. There is no evidence of major changes in the angle of the Earth's axis, so polar dinosaurs and the rest of these ecosystems would have had to cope with the same extreme variation of day length through the year that occurs at similar latitudes today (up to a full day with no darkness in summer, and a full day with no sunlight in winter).[91]

Studies of fossilized vegetation suggest that the Alaska North Slope had a maximum temperature of 13 °C (55 °F) and a minimum temperature of 2 °C (36 °F) to 8 °C (46 °F) in the last 35 million years of the Cretaceous (slightly cooler than Portland, Oregon but slightly warmer than Calgary, Alberta). Even so, the Alaska North Slope has no fossils of large cold-blooded animals such as lizards and crocodilians, which were common at the same time in Alberta, Montana, and Wyoming. This suggests that at least some non-avian dinosaurs were warm-blooded.[91] It has been proposed that North American polar dinosaurs may have migrated to warmer regions as winter approached, which would allow them to inhabit Alaska during the summers even if they were cold-blooded.[92] But a round trip between there and Montana would probably have used more energy than a cold-blooded land vertebrate produces in a year; in other words the Alaskan dinosaurs would have to be warm-blooded, irrespective of whether they migrated or stayed for the winter.[93] A 2008 paper on dinosaur migration by Phil R. Bell and Eric Snively proposed that most polar dinosaurs, including theropods, sauropods, ankylosaurians, and hypsilophodonts, probably overwintered, although hadrosaurids like Edmontosaurus were probably capable of annual 2,600 km (1,600 mi) round trips.[94][95]

It is more difficult to determine the climate of southeastern Australia when the dinosaur fossil beds were laid down 115 to 105 million years ago, towards the end of the Early Cretaceous: these deposits contain evidence of permafrost, ice wedges, and hummocky ground formed by the movement of subterranean ice, which suggests mean annual temperatures ranged between −6 °C (21 °F) and 5 °C (41 °F); oxygen isotope studies of these deposits give a mean annual temperature of 1.5 °C (34.7 °F) to 2.5 °C (36.5 °F). However the diversity of fossil vegetation and the large size of some of fossil trees exceed what is found in such cold environments today, and no-one has explained how such vegetation could have survived in the cold temperatures suggested by the physical indicators – for comparison Fairbanks, Alaska presently has a mean annual temperature of 2.9 °C (37.2 °F).[91] An annual migration from and to southeastern Australia would have been very difficult for fairly small dinosaurs in such as Leaellynasaura, a vegetarian about 60 centimetres (2.0 ft) to 90 centimetres (3.0 ft) long, because seaways to the north blocked the passage to warmer latitudes.[91] Bone samples from Leaellynasaura and Timimus, an ornithomimid about 3.5 metres (11 ft) long and 1.5 metres (4.9 ft) high at the hip, suggested these two dinosaurs had different ways of surviving the cold, dark winters: the Timimus sample had lines of arrested growth (LAGs for short; similar to growth rings), and it may have hibernated; but the Leaellynasaura sample showed no signs of LAGs, so it may have remained active throughout the winter.[96] A 2011 study focusing on hypsilophodont and theropod bones also concluded that these dinosaurs did not hibernate through the winter, but stayed active.[97]

Evidence for behavioral thermoregulation

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:

But these were a very small minority of known dinosaur species. One common interpretation of the plates on stegosaurs' backs is as heat exchangers for thermoregulation, as the plates are filled with blood vessels, which, theoretically, could absorb and dissipate heat.[98]
This might have worked for a stegosaur with large plates, such as Stegosaurus, but other stegosaurs, such as Wuerhosaurus, Tuojiangosaurus and Kentrosaurus possessed much smaller plates with a surface area of doubtful value for thermo-regulation. However, the idea of stegosaurian plates as heat exchangers has recently been questioned.[99]

Other evidence

Respiration

Endothermy demands frequent respiration, which can result in water loss. In living birds and mammals, water loss is limited by pulling moisture out of exhaled air with mucous-covered respiratory turbinates, tissue-covered bony sheets in the nasal cavity. Several dinosaurs have olfactory turbinates, used for smell, but none have yet been identified with respiratory turbinates.[100]

Brain size

Because endothermy allows refined neuromuscular control, and because brain matter requires large amounts of energy to sustain, some speculate that increased brain size indicates increased activity and, thus, endothermy. The encephalization quotient (EQ) of dinosaurs, a measure of brain size calculated using brain endocasts, varies on a spectrum from bird-like to reptile-like. Using EQ alone, coelosaurs appear to have been as active as living mammals, while theropods and ornithopods fall somewhere between mammals and reptiles, and other dinosaurs resemble reptiles.[100]

The crocodilian puzzle and early archosaur metabolism

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

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:

Modern crocodilians are cold-blooded but can move with their limbs erect, and have several features normally associated with warm-bloodedness because they improve the animal's oxygen supply:[103]

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

It was suggested in the late 1980s that that crocodilians were originally active, warm-blooded predators and that their archosaur ancestors were warm-blooded.[80][103] More recently, developmental studies indicate that crocodilian embryos develop fully four-chambered hearts first—then develop the modifications that make their hearts function as three-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.[105][106]

More recent research on archosaur bone structures and their implications for growth rates also suggests that early archosaurs had fairly high metabolic rates and that the Triassic ancestors of crocodilians dropped back to more typically "reptilian" metabolic rates.[69]

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

See also

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