A number of areas of research on dinosaurs have attracted attention far beyond the realm of those who take a purely academic interest in these creatures. This common interest appears to arise because dinosaurs capture the public imagination in a way that few other subjects do. The following topics focus on these topics in order to illustrate the extraordinary variety of approaches and types of information that are used in our attempts to unravel the mystery of dinosaurs and their biology.
Dinosaurs: hot-, cold-, or luke-warm-blooded?
As we have seen in topic 1, Richard Owen, at the time of his invention of the word ‘dinosaur’, speculated about the physiology of dinosaurs. Extracting meaning from the rather long-winded final sentence of his scientific report:
The Dinosaurs … may be concluded to have … [a] superior adaptation to terrestrial life … approaching that which now characterizes the warm-blooded Vertebrata. [i.e. living mammals and birds]
Although the ‘mammaloid’ reconstructions of dinosaurs that he created for the Crystal Palace Park clearly echo his sentiments, the biological implications he was hinting at were never grasped by other workers at the time. In a sense, Owen’s visionary approach was tempered by rational Aristotelian logic: dinosaurs were structurally reptilian, it therefore followed that they had scaly skins, laid shelled eggs, and, like all other known reptiles, were ‘cold-blooded’ (ectothermic).
In a similar vein to Owen, Thomas Huxley proposed, almost 50 years later, that birds and dinosaurs should be considered close relatives because of the anatomical similarities that could be demonstrated between living birds, the earliest known fossil bird Archaeopteryx, and the newly discovered small theropod Compsognathus. He concluded that:
… it is by no means difficult to imagine a creature completely intermediate between Dromaeus [an emu] and Compsognathus [a dinosaur] … and the hypothesis that the … class Aves has its root in the Dinosaurian reptiles; …
If Huxley was correct, it should have been possible to ask: were dinosaurs then conventionally reptilian (physiologically) or were they closer to the ‘warm-blooded’ (endothermic) birds? There appeared to be no obvious way of answering such questions.
Despite such intellectual ‘nudges’, it was close to a century after Huxley’s paper that palaeontologists began to search with greater determination for data that might have a bearing on this central question. The spur to renewed interest in the topic finds an echo in the adoption of the broader and more integrated agenda for the interpretation of the fossil record: the rise of palaeobiology, as outlined in topic 2. We saw there how some wide-ranging observations were strung together by Robert Bakker into a case for endothermy in dinosaurs. Let’s now consider these and other arguments in greater detail.
New approaches: dinosaurs as climatic proxies?
Attempts were being made to investigate the degree to which fossils could be used to reconstruct climates in the ancient world. It is widely recognized that endotherms (basically mammals and birds) are not particularly good indicators of climate because they are found everywhere, from equatorial to polar regions. Their endothermic physiology (and clever use of body insulation) allows them to operate more or less independently of prevailing climatic conditions. By contrast, ectotherms, such as lizards, snakes, and crocodiles, are reliant on ambient climatic conditions, and as a result they tend to be found mainly in warmer climatic zones.
Using this approach to examine the geographic distribution of obvious ectotherms and endotherms in the fossil record proved useful, but then threw up several interesting questions. For example, what about the immediate evolutionary ancestors of endothermic mammals in Permian and Triassic times? Were they also able to control their internal body temperatures? If they did, how would it have affected their geographic distribution? And more pointedly in this context, dinosaurs seemed to have a wide geographic spread, so did this mean that they were capable of controlling their body temperature rather like endotherms?
Patterns in the fossil record
The foundation of Bakker’s approach to endothermy in dinosaurs was the pattern in the succession of animal types in the early Mesozoic. During the time leading up to the end of the Triassic Period synapsid reptiles were by far the most abundant and diverse animals on land.
Right at the close of the Triassic and the beginning of the Jurassic Period (205 Ma) the very first true mammals appeared on Earth and were represented by small, shrew-like creatures. In complete contrast, the latter part of the Triassic Period also marks the appearance of the first dinosaurs (225 Ma), and across the Triassic/Jurassic divide the dinosaurs become widespread, very diverse, and clearly dominant members of the land fauna. This ecological balance – rare, small, very probably nocturnal mammals and abundant, large, and increasingly diverse dinosaurs – was then maintained for the next 160 million years, until the close of the Cretaceous Period (65 Ma).
As animals living in the present day, we are comfortable with the notion that mammals are, along with birds, the most conspicuous and diverse of land-living vertebrates. Mammals are self-evidently fast-moving, intelligent, generally highly adaptable creatures, and much of this present-day ‘success’ we attribute to their physiological status: their high basal metabolic rate, which permits the maintenance of a high and constant body temperature, complex body chemistry, comparatively large brains, and consequently high activity levels, and their status as endotherms. In contrast, we generally observe that reptiles are considerably less diverse and quite sharply climatically restricted; this is largely explained by the fact that they have a much lower metabolic rate, rely on external sources of heat to keep the body warm and therefore chemically active, and have much lower and more intermittent levels of activity: the ectothermic condition.
These, admittedly very general, observations permit us to have expectations that can be superimposed on the fossil record. All things being equal, we would predict that the first appearance of true mammals at the Triassic/Jurassic boundary, in a world otherwise dominated by reptiles, would spark the former’s rapid evolutionary rise and diversification at the expense of the latter. So the fossil record of mammals would be expected to show a rapid rise in abundance and diversity in Early Jurassic times, until they completely dominated the ecosystems of the Mesozoic Era. However, the fossil record reveals exactly the opposite pattern: the (reptilian) dinosaurs rose to dominance in the Late Triassic (220 Ma) and the mammals only began to increase in size and diversity after the dinosaurs had become extinct at the end of the Cretaceous period (65 Ma).
Bakker’s explanation for this counterintuitive set of events was that dinosaurs could have succeeded, evolutionarily, in the face of true mammals only if they too had endotherm-like high basal metabolic rates and could be as active and resourceful as contemporary mammals. Dinosaurs quite simply had to be active endotherms – it was to Bakker a self-evident truth. While the pattern revealed by the fossil record was indeed clear, the scientific proof necessary to support his ‘truth’ needed to be assembled and tested.
Legs, heads, hearts, and lungs
Dinosaurs place their feet vertically beneath the body on straight, pillar-like legs. The only living creatures that also adopt this posture are birds and mammals; all the rest ‘sprawl’ with their legs directed sideways from the body. Many dinosaurs were also slender-limbed and apparently built for moving quickly; this line of argument reflects the fact that Nature does not tend to do things unnecessarily. If an animal is built as if it could run fast, it probably did so; it might therefore seem reasonable to expect such a creature to have an energetic ‘motor’, or endothermic physiology, to allow it to move quickly. We do, however, need to be careful, because it is also the case that ectotherms can move very quickly indeed – crocodiles and Komodo dragons can outrun and catch unwary humans! The crucial thing is that crocodiles and Komodo dragons cannot sustain fast running – their muscles build up a large oxygen debt very quickly and the animals then have to rest so their muscles can recover. Endotherms, by contrast, can move quickly for much longer periods of time because their high-pressure blood system and efficient lungs replenish the oxygen in their muscles very quickly.
A further refinement of this argument is the suggestion that the ability to walk bipedally is linked exclusively to endothermy; many mammals, all birds, and many dinosaurs are bipedal. This argument relates not only to posture, but also to how that posture is maintained. A quadruped has the advantage of considerable stability when it walks. A biped is inherently unstable, and to walk successfully a sophisticated system of sensors monitoring balance, as well as a rapid coordinating system (the brain and central nervous system), and rapid-response muscles to correct and maintain balance, are essential.
The brain is central to this whole dynamic ‘problem’ and must have a constant capacity to work quickly and efficiently. This implies that the body is able to provide constant supplies of oxygen, food, and heat to allow the chemistry of the brain to work optimally all the time. The prerequisite for this type of stability is a ‘steady’ endothermic physiology. Ectotherms periodically shut down their activity levels, when cold, for example, and reduce the supply of nutrients to the brain, which is consequentially less sophisticated and closely integrated to overall body functions.
Another posture-related observation can be linked to the efficiency of the heart and its potential to sustain high activity levels. Many birds, mammals, and dinosaurs adopt an upright body posture in which the head is normally held at levels appreciably higher than the position of the heart. This difference in head-heart level has important hydrostatic consequences. Because the head is above the heart, it has to be capable of pumping blood at high pressure ‘up’ to the brain. But the blood that is pumped at the same time with each heartbeat from the heart to the lungs must circulate at low pressure, otherwise it would burst the delicate capillaries that line the lungs. To permit this pressure difference, the heart in mammals and birds is physically divided down the middle, so that the left side of the heart (the systemic, or head and body, circuit) can run at a higher pressure than the right side (the pulmonary, or lung, circuit).
All living reptiles carry their head at roughly the same level as their heart. Their hearts are not divided down the middle like those of mammals and birds because there is no need to differentiate between the systemic and pulmonary circuits. Curiously, the reptilian heart and circulation offers advantages for these creatures; they can shunt blood around the body in ways that mammals cannot. For example, ectotherms spend a lot of time basking in the sun to warm their bodies. While basking, they can preferentially shunt blood to the skin, where it can be used to absorb heat (rather like the water in solar panel central heating pipes). The major disadvantage of this system is that the blood cannot be circulated under high pressure – a feature that is essential in any animal that is behaving very actively and must bring food and oxygen to its hard-working muscles.
The implication from all these considerations is that dinosaurs, because of their posture, had a high-pressure blood circulation system that was compatible with high and sustained activity levels that are only found in living endotherms. This more comprehensive and elaborate set of considerations resoundingly supports Richard Owen’s provocative speculation.
Intimately associated with the efficiency of the heart and circulatory system must be the ability to supply sufficient oxygen to muscles to allow high levels of aerobic activity. In some groups of dinosaurs, notably the theropods and the giant sauropodomorphs, there are some tantalizing anatomical hints concerning lung structure and function. In both these groups of saurischian dinosaurs (but not the ornithischians), there are traces of distinct pouches or cavities (called pleurocoels) in the sides of the vertebrae of the backbone. In isolation, these might not have attracted particular attention; however, living birds show similar features that equate with the presence of extensive air sacs. Air sacs are part of a bellows-like mechanism that permits birds to breathe with remarkable efficiency. It is highly probable that saurischian dinosaurs had bird-like, and therefore extremely efficient, lungs.
33. Bird air sacs provide for a highly efficient respiratory system
This observation certainly supports the contention that some dinosaurs (theropods and sauropodomorphs) had the ability to maintain high aerobic activity levels. However, it also highlights the fact that all dinosaurs (saurischians and ornithischians) should not be presumed to have been the same in all aspects of their physiology, because ornithischians show no trace of an air-sac system.
Dinosaur ‘sophistication’ and brain size
Although the line of argument that follows is not universal to dinosaurs, it is instructive in the sense that it shows what some dinosaurs were capable of doing. The classic example is John Ostrom’s dromaeosaur Deinonychus (Figure 29). As was summarized in topic 2, this dinosaur was a large-eyed visual predator that could clearly run fast, judging by its limb proportions and general build. In addition, it had an unusual stiff, narrow tail, extraordinary gaff-like inner toes on its hind feet, and long, sharply clawed, grasping arms. It is not unreasonable to suggest that this animal was built as a pursuit predator, was capable of using its narrow tail as a dynamic balancing aid (flicking the tail to one side or the other would allow this animal to change direction extremely quickly), and very probably leapt at its prey, which it then disabled using the claws on its feet. We have never seen a Deinonychus in action, but this scenario is based upon observable features of the skeleton, and is partially supported by one remarkable fossil discovered in Mongolia.
The latter comprises two dinosaurs, the small herbivorous ceratopian Protoceratops and a close relative of Deinonychus known as Velociraptor. This extraordinary fossil shows the two creatures caught in a death struggle; they probably choked to death in a dust storm while fighting with each other. The Velociraptor is preserved clinging to the head of its prey using its long arms, and in the very act of kicking at the throat of its unfortunate victim.
Such overall ‘sophistication’ in design, inferred function, and way of life strongly suggests activity levels that are more similar to those exhibited by modern endotherms.
Echoing some of the argument seen in the discussion concerning dinosaurs’ ability to move bipedally, the brains of both mammals and birds are large and both groups exhibit what appears to be intelligent behaviour. In contrast, ectothermic reptiles possess smaller brains and are not usually renowned for their intellectual prowess (though this is in part a fiction that we have propagated). There does, however, appear to be a general link between overall brain size and endothermy. Large brains are highly complex structures that demand constant supplies of oxygen and food, as well as a stable temperature in order to function efficiently. Ectothermic reptiles clearly can supply both food and oxygen to their brains effectively, but their body temperature does vary across a normal 24-hour cycle, and as a consequence they are unable to supply the needs of a large and sophisticated brain.
Tradition has it that dinosaurs were notoriously lacking in brain power (the walnut-sized Stegosaurus brain is often cited as a classic example). However, Jim Hopson at the University of Chicago has done much to rectify this somewhat erroneous view. Comparing the ratio of brain volume to body volume across a range of animals, including dinosaurs, Hopson was able to demonstrate that most dinosaurs had fairly typically reptile-sized brains. Some, however, were unexpectedly well endowed in the ‘brains department’ – not surprisingly perhaps, these were the highly active, bipedal theropods.
Latitudinal distributions
Earlier in this topic it was mentioned that charting distributional data had been one of the spurs to pursuing the physiological status of dinosaurs. Recently, reports have shown numbers of dinosaurs in the Yukon area of North America as well as in Australia and Antarctica. These areas would have fallen within their respective polar regions in Cretaceous times, and have been used to support the idea that dinosaurs must have been endothermic to have survived. It is, after all, clearly the case today that ectothermic land vertebrates are incapable of living at such high latitudes.
However, upon careful consideration, these observations are not as persuasive as they seem at first sight. Evidence from the plant fossil record suggests that Mediterranean and subtropical styles of vegetation existed in these polar regions in Cretaceous times. Unusually, these plants share the habit of seasonal leaf loss, probably in response to low winter light levels and temperatures. The Cretaceous world shows no evidence of polar ice caps and it seems probable that even at high latitudes, during the summer season at least, temperatures were extremely mild. Under such circumstances, it is highly likely that herbivorous dinosaurs migrated north or south, depending upon the season, to take advantage of rich pastures. As a result, discovery of their fossil remains at very high Mesozoic latitudes may reflect their migratory range rather than polar residency.
Ecological considerations
Measuring Mesozoic community structure was one of Bakker’s most innovative suggestions in his search for proxies for dinosaurian physiology. The idea is beguilingly simple: endothermic and ectothermic animals require differing amounts of food in order to survive – these amounts reflect the basic ‘running costs’ associated with being either an endotherm or ectotherm. Endotherms, such as mammals and birds, have high running costs because much of the food that they eat (in excess of 80%) is burned to produce body heat. By contrast, ectotherms need far less food because very little is used to generate body heat. As a rough guide, ectotherms need about 10%, sometimes much less, of the food requirements of similarly sized endotherms.
Based on this observation, and an understanding that the general economy of Nature tends to keep supply and demand more or less in balance, Bakker suggested that censuses of fossil communities might indicate the balance between predator and prey, and by implication the physiology of these animals. He combed through museum collections to gather the data he needed. This included data from ancient (Palaeozoic) reptile, dinosaur (Mesozoic), and relatively more recent (Cenozoic) mammal communities. His results seemed encouraging: Palaeozoic reptile communities indicated a rough equivalence of predator and prey numbers; by contrast, dinosaur and Cenozoic mammal communities indicated a preponderance of prey animals and very small numbers of predators.
At first the scientific community was impressed with these results; however, considerable doubt now exists about the value of the original data. Using museum collections to estimate numbers of predators or prey is an exceedingly dubious exercise: there is no proof that the animals being counted lived together in the first instance; there are enormous biases in terms of what was (or was not) collected at the time; and all manner of assumptions are being made about what a predator will or will not eat; and, even if there was some sort of biological signal, it would surely only apply to the predator. Additionally, work on communities of living ectotherm predators and their prey has revealed that the predators may be as few as 10% of their potential prey numbers, mimicking the proportions seen in Bakker’s supposedly endotherm communities.
This is an excellent example of a brilliant idea that sadly cannot be supported because the data simply will not yield results that are in any way meaningful scientifically.
Bone histology
Considerable attention has been directed toward understanding fine details of the internal structure of dinosaur bone. The mineral structure of dinosaur bone is generally unaffected by fossilization. As a result, it is often possible to create thin sections of bone that reveal the internal structure (histology) of the bone in amazing detail. Preliminary observations suggested that the bones of dinosaurs were closely similar in internal structure to those seen in living endothermic mammals, rather than those of modern ectotherms.
In general terms, the mammal and dinosaur bones revealed high levels of vascularization (they were very porous), while the ectotherm bones were poorly vascularized. The highly vascularized type of bone structure can arise in different ways. For example, one pattern of vascularization (fibrolamellar) reflects very rapid phases of bone growth. Another pattern (Haversian) represents a phase of strengthening of bone by remodelling that occurs later in the life of an individual.
What can be said is that many dinosaur remains show evidence of them having been able to grow quickly, and an ability to strengthen their bones by internal remodelling. Dinosaurs sometimes exhibit periodic interruptions in their pattern of growth (which mimics the intermittent pattern seen in the bones of living reptiles), but this style of growth is by no means uniform. Equally, and less probably, some endotherms (both bird and mammal) exhibit a style of bone structure (zonal) that displays very little vascularization, while living ectotherms can exhibit highly vascularized bone in parts of their skeletons. There are, surprisingly, no clear correlates between an animal’s physiology and its internal bone structure.
Dinosaur physiology: an overview
The discussion above illustrates the range and variety of approaches that have been used in an attempt to investigate dinosaur metabolism.
Robert Bakker took an unquestioning stance when assessing the significance of the mammalian replacement by dinosaurs on land in the Early Jurassic. This pattern, he argued, could only be explained if dinosaurs were able to compete with his model of the ‘superior’ endothermic mammals: to do so, they simply had to be endothermic. Is this true? The answer is actually: no … not necessarily.
At the close of the Triassic and very beginning of the Jurassic, the world was one that we mammalian humans would not find particularly hospitable. Much of Pangaea at the time was affected by seasonal, but generally arid, conditions in which deserts became widespread globally. Such conditions of high temperatures and low rainfall exert selective pressures on endothermic and ectothermic metabolisms in very different ways.
Ectotherms, as argued above, need to eat less than endotherms and are therefore better able to survive times of low biological productivity. Reptiles have scaly skin that greatly resists water loss in dry, desert conditions; they also do not urinate but instead excrete a dry, pasty material (similar to bird droppings). High ambient temperatures suit ectotherms well because their internal chemistry can be maintained at optimum temperatures with relative ease. All in all, ectotherms, built in the classic reptilian mould, can be predicted to cope well with desert-like conditions.
Endotherms, such as mammals, are physiologically stressed in high-temperature conditions. Mammals are ‘geared’ to being able to lose heat to the environment from their bodies (their bodily thermostats maintain their temperature on average higher than normal environmental conditions) and adjust their physiology accordingly. When cold, mammals are able to reduce heat loss from the body by raising their fur to trap air and increase its insulatory efficiency, use ‘shivering’ to quickly generate extra muscular heat, or raise their basal metabolic rate. However, under conditions of high ambient temperature, the need to lose heat to the environment to prevent lethal overheating becomes vital. Evaporative cooling is one of the few options available; this is achieved either by panting or sweating through the skin surface. Both of these processes remove large volumes of water from the body. In desert conditions, losing water, which is in short supply, can prove fatal. To compound matters further, mammals remove the breakdown products of their metabolism from the body by urinating, which flushes wastes out of the body in a watery solution. In addition to the problems of heat load and water loss, mammals require large quantities of food to maintain their endothermic physiology. Deserts are areas of low productivity, so food supplies are restricted and not capable of sustaining large populations of endotherms.
Looked at from this purely environmental perspective, perhaps the Late Triassic/Early Jurassic world was unusual. It was a time when the environment probably favoured ectotherms and restricted early mammals to small size and primarily nocturnal niches. In deserts today, nearly all mammals (with the exception of those truly remarkable creatures known as camels) are small, exclusively nocturnal rodents and insectivores. They survive the extreme heat of the day by burrowing under the sand surface, where conditions are cooler and more damp, and they come out at night once the temperature has dropped and they can use their acute senses to find insect prey.
The striking aridity of the Late Triassic/Early Jurassic eventually ameliorated, as Pangaea began to disintegrate and shallow epicontinental seas spread across and between areas of land. The general climatic regime appears to have become extremely warm and wet, and these conditions prevailed across very broad latitudinal bands. It should be emphasized that there were no ice-covered polar regions throughout the time of the dinosaurs. The type of world we inhabit today is very unusual, when compared to much of the history of the Earth, in that it has both north and south poles covered in ice and consequently unusually narrowly confined latitudinal climatic bands. Under these relatively lush Jurassic conditions, productivity rose dramatically; major Jurassic coal deposits were laid down in areas where long-lived and densely forested areas existed. So it is perhaps not surprising to discover that the range and variety of dinosaurs surged during Jurassic times.
Dinosaur physiology: was it unique?
Dinosaurs are noteworthy as being large creatures; even medium-sized ones ranged between 5 and 10 metres in length, which is still very big by most standards – the average size of all mammals is probably about the size of a cat or small dog today. It is certainly true that no dinosaurs were mouse-sized (except as hatchlings).
Under some conditions, being large has advantages. Most notably, larger animals tend to lose heat to and gain heat from the environment very much more slowly than small ones. For example, adult crocodiles maintain a very stable internal body temperature day and night, whereas hatchlings exhibit a body temperature range that exactly mirrors the day and night changes. So, being dinosaur-sized means that your internal body temperature changes little over time. Being large also means that postural muscles need to work hard to prevent the body from collapsing under its own weight. This constant muscular ‘work’ generates significant quantities of energy (in the same way that we become ‘flushed’ with heat after muscular exercise), and this heat can assist in maintaining internal body temperature.
In addition to these advantages of size, we have seen that the probable agility as well as posture of dinosaurs, many with heads raised significantly above chest level, indicates the strong likelihood that they had highly efficient, fully divided hearts that were capable of rapidly circulating oxygen, food, and heat around the body, as well as removing harmful metabolism by-products. The fact that saurischian dinosaurs probably possessed a bird-like lung system further emphasizes their ability to provide the oxygen that their tissues needed during energetic, aerobic exercise.
Considering these factors alone, it seems very likely that dinosaurs possessed many of the attributes that we associate today with endothermy as seen in living mammals and birds. In addition, dinosaurs were typically large and therefore relatively thermally inert. They also lived during a time of constantly warm, non-seasonal, global climate.
It could be the case that dinosaurs were the happy inheritors of an ideal type of biology that enabled them to prosper in the unique climatic conditions that prevailed in the Mesozoic Era. But, however convincing this argument might seem at this point, it does not take into account one other crucial line of evidence that has emerged over the last few years: the intimacy of dinosaur-bird relationships.
