GEOL 104 Dinosaurs: A Natural History

Fall Semester 2021
Dinosaur Physiology

Dinosaurs of the Middle Jurassic Xiashaximiao Formation of China: the sauropod Shunosaurus, the theropod Gasosaurus, and the stegosaur Huayangosaurus, by Gregory S. Paul

Key Points:
•Modern animals are often characterized as "warm-blooded" (mammals, birds) and "cold-blooded" (everything else)
•This is a simplification of several related phenomena: energy source (endothermy vs. ectothermy); metabolic rate (tachymetabolism vs. bradymetabolism); and temperature stability (homeothermy vs. poikilothermy)
•Dinosaur species were initially inferred to be "cold-blooded", but similarity in posture and other traits led Owen to suggest they might have been warm-blooded; since that time various researchers have examined the alternatives.
•Dinosaur posture, locomotion, feeding adaptations, growth rates, bone texture, inferred respiration, and predator-prey ratios point to elevated metabolisms relative to today's non-avian sauropsids.

The Fires of Life: Warm-bloodedness vs. Cold-bloodedness

Among modern vertebrates, some gross generalizations:
Birds and mammals are warm-blooded; that is, they are warmer than the environment around them in typical temperate and colder environments. Crocodilians, lepidosaurs, turtles, amphibians, most fish, and almost all invertebrates are cold-blooded: their bodies are generally only about as warm as the general environment around them, so consequently they feel cool to the touch outside of tropical situations; in contrast, warm-blooded animals have temperatures largely independent of the outside temperature, so they feel warm to the touch. Need to be precise as to definitions of terms. "Warm-blooded" and "Cold-blooded" actually encompass several different (although related) topics:

A typical cold-blooded animal is an ectothermic bradymetabolic poikilotherm: needs to get its energy from the sun and fluctuates with external environment (but can moderate fluctuations by moving from sunlight to shade and vice versa); however, needs very little food (snakes can go weeks without feeding, for example). Cold blooded animals become torpid at night and in colder weather. While cold-blooded animals might have a range of preferred ambient temperatures in which they operate the best, they don't really have a specific body temperature: because they are poikilotherm

A typical warm-blooded animal is an endothermic tachymetabolic homeotherm: its body temperature is stable and activity levels can remain high for long periods of time, at night, and in colder weather; however, needs a LOT of food or will die (imagine the effects of not feeding a cat or dog for weeks...). The actual preferred body temperatures for living endotherms can be very different from species to species. Among living mammals, it ranges from 30°C (86°F) in the naked mole rat Heterocephalus glaber and the egg-laying monotremes to 39.9°C (103.8°F) in the pronghorn Antilocapra americana; and in living birds from 34°C (93.2°F) in various kingfishers and loons to 44.6°C (112.3°F) in the sombre hummingbird Eupetomena cirrochloris. Body temperature roughly approximates overall activity levels and ecology (especially in mammals): burrowers live in thermally insulated environments where they don't lose heat very easily; slower-moving or more sedentary terrestrial mammals tend to have lower temperatures; and more cursorial mammals like cats, dogs, rabbits, and hoofed mammals have the highest.

Note: there are some mammals and birds (particularly on the smaller size) which actually do undergo daily torpor: in this state their body temperatures and metabolic rates go down considerably. Indeed, they may be effectively ecothermic bradymetabolic poikilotherms in this state.

Here are some additional issues to consider:

Why evolve such an expensive trait as endothermy? Some suggestions have included:

Note that it is not just mammals and birds that are "warm-blooded". For example, tunas, billfish (sailfish, swordfish, marlins), lamniform sharks (like great whites and makos), boid snakes (pythons, etc.; but only while brooding), and certain plants (which aren't "blooded" as such, but some can emit internally-generated heat).

Before we leave this introduction, we need to bring up the issue of surface area to volume (SA/V) ratios. We saw examples of the issues of scaling before with regards to biomechanics: as organisms get larger the stresses on their body parts go up, because volume (and mass) increases by cubes while cross-sectional areas go up by squares (assuming the shapes and proportions don't change. The same thing applies to the changes in the surface area (which is how the organism interacts with the outside world) and the volume (how much animal there is):
Side Length Surface Area (SA) Volume (V) SA/V
1 6 1 6/1 = 6
2 24 8 24/8 = 3
3 54 27 54/27 = 2
4 96 64 96/64 = 1.5

Some have proposed the concept of gigantothermy (also called inertial homeothery): sufficiently large animals are effectively homeothermic without having to pay the energy costs of endothermy! Large dinosaurs would definitely have to deal with low surface area/volume ratios, but the small species (and the babies of big ones) would not be affected by this.

Another thing to consider is that not all animals are strictly "warm-blooded" or "cold-blooded". Many show some form of heterometabolism (a changeable rate from tachy- to bradymetabolism). We previously mentioned torpor in some small endotherms, an example of behavioral heterometabolism. Other examples include many sharks during feeding frenzies, or pythons during brooding. Most living animals also have some degree of ontogenetic metabolism, where our metabolic rates are higher as juveniles and subadults and lower to some degree as adults.

Hot- and Cold-Running Dinosaurs?

When dinosaurs were first discovered, they were interpreted as being no more than gigantic cold-blooded lizards. However, as early as 1842 Owen (in the very paper in which he named "Dinosauria") speculated that dinosaurs may have been warm-blooded like mammals. During most of the 20th Century the model of dinosaurs as cold-blooded returned. Work by John Ostrom (of Yale University) and his colleagues and students (especially Robert Bakker) presented new information that dinosaurs were in fact warm-blooded. This hypothesis generated considerable research (both in support and in attempts to falsify it): this change in thinking about dinosaurs and renewed interest in dinosaurian studies has been termed the "Dinosaur Renaissance".

Among the lines of evidence supporting dinosaurian warm-bloodedness:

As Owen pointed out in 1842, dinosaurs all had parasagittal stance, a trait unique to endotherms in the living world. More recent considerations of this point out that the anatomy of dinosaurs shows that they were active striders with large locomotory muscles, and in some cases were even cursorial. These indicate that sustained rates of locomotion, and indeed selection for an active (foraging?) lifestyle. These traits are common in endotherms (who need to procure food more often, and are able to sustain longer term activity) and essentially unknown in ecotherms.

Ostrom pointed out that many dinosaurs had specialized feeding adaptations (whether dental batteries in hadrosaurids, ceratopsians, and rebbachisaurids, or the flesh-shredding teeth of theropods and herrerasaurs, and so forth.) The ability to shred, grind, or chew food is significant because it takes the same volume of food and increases the surface area/volume ratio (as you will see, SA/V is going to play a BIG role in physiology!!), and thus allows an animal to digest the food and get nutrients out of it more quickly. Not all dinosaurs had as complex feeding adaptations as hadrosaurids or ceratopsids, but all of them show some degree of increased chewing or shredding ability compared to a typical lizard or turtle.

Ostrom also showed that dinosaurs (and non-mammalian therapsids) had a wide latitudinal range. In the modern world, the diversity of terrestrial ecotherms is very strongly controlled by ambient temperature, and thus is reflected in the latitude of the ecosystem: tropical ecosystems have tremendous numbers of ecothermic vertebrates, temperate zones much fewer, and polar ones none. Before the 1960s geologists and paleontologists used the high diversity of polar Mesozoic dinosaurs (and Permo-Triassic therapsids) as evidence that those regions were tropical at the time. But he pointed out that if these animals were partly- or fully-endothermic, we would expect a higher diversity even in cooler climates. Additional paleoenivornmental work shows that while these intervals in time were generally warmer than today, the polar regions were far from tropical, and yet therapsids and dinosaurs were common there. Recent work on Late Triassic ecosystems confirms a much broader environmental tolerance for ornithodirans (including dinosaurs) and therapsids (including early mammals) than in contemporary pseudosuchians and amphibians.

An attribute of dinosaurs which has been obvious for a long time but has a bearing on this issue is that big dinosaurs are tall. Ostrom pointed out the reason this is important is that in order to get blood way up the brain requires a very active heart, which requires a high metabolic rate. Big ecotherms can get away with being big because they are or were built low to the ground: the brain wasn't held way above the ground, so the heart need not work as hard and strong.

Bone histology (microscopic analysis of tissue and cellular structure) can test between bradymetabolic and tachymetabolic organisms. Bone becomes reworked (that is, removed then redeposited) as a normal part of vertebrate physiology, as bone is a major store for nutrients like calcium and phosphorus. Bradymetabolic animals show little sign of reworking, as their slower metabolism does not need as much nutrients as quickly. In contrast, tachymetabolic animals show considerable reworking. Examination of the bones of dinosaurs show a high degree of reworking, even as juveniles.

Using skeletochronology, the maximum rate of growth of dinosaurs can be calculated. When plotted against body size, it is found that dinosaurs had much higher growth rates than ectotherms of the same size; in fact, the dinosaur growth rate is about the same as mammals and ground-dwelling birds.

Texture of bone also shows signs of the rate of growth. Dinosaurs show fast rates similar to mammals; pseudosuchians and other archosauriforms show an intermediate rate; and ectotherms show a slow growth rate.

Related to the above are estimates of bone apposition rate (the rate at which new bone is added onto older bone. Once again, pseudosuchians and other non-dinosaurian archosauriforms show a higher rate than in extant ecotherms. Within dinosaurs, the non-theropod dinosaurs show rates comparable to modern mammals, and Mesozoic theropods show rates comparable to modern birds (the fast living bone-growers.)

Examining the nutrient foramina (holes for blood vessels into and out of bones) in dinosaurs shows that the amount of blood flowing through dinosaurs greatly exceeded modern ectotherms, and even modern mammals. This suggests that the metabolic rate of dinosaurs was indeed very high.

The size of the blood vessels inside bone give us an approximation of maximum blood cell size. It has been found that on average, ecotherms have larger blood cell sizes than endotherms: because smaller objects have a larger surface area/volume ratio, a smaller red blood cell can more quickly dump off its waste carbon dioxide and pick up fresh oxygen than a bigger one. Based on blood vessel size, silesaurids and Mesozoic dinosaurs had red blood cells comparable in size to modern flightless birds and the pre-mammal therapsids. (Modern flying birds have even smaller red blood cells, and mammals (who have lost the nucleus in their red blood cells) are the smallest of all.)

Comparison of the bone oxygen isotope data of dinosaurs with known ectotherms of the same environment (modern-style crocodilians, turtles, and amphibians) finds that the dinosaurs show lower body temperatures in the hottest environments and lower body temperatures in moderate and colder environments. This suggest that dinosaur body temperatures were independent of the local environment.

A related approach is to look at egg oxygen isotope data. The egg shell takes on the isotopic characteristics of the temperature at which it formed, which was inside the mother! It has been found that titanosaur eggshell show high temperatures, but these could conceivably reflect gigantothermy rather than endothermy. However, ornithischian and theropod eggs of much smaller dinosaurs show similar temperatures, but these temperatures would be too high to explain by size-based temperatures.

Computer models of the required metabolic rates required for even walking and slow running for large bipedal dinosaurs exceeds the metabolic rate of ecotherms. So if they actually moved, big theropods HAD to have been endotherms. In fact, the proportionately massive hindlimb muscles of all dinosaurs likely generated enough heat to keep the temperature elevated.

Predator-Prey ratios (first considered by R.T. Bakker) looks at the trophic relationships in communities to try and determine the thermophysiology of dinosaurs and other extinct forms. While most of the approaches to understanding thermophysiology look at the properties of individuals, Bakker's technique looks at aspects of the ecosystem:

Basics of Physiology

Let's consider the equations of life. First, the aerobic respiration equation, the primary means by which animal cells operate:

C6H12O6 + 6O2 yields 6CO2 + 6H2O + Energy

(That is, food (glucose) plus oxygen yields waste carbon dioxide and waste water, plus energy).

If an animal's cells can't get enough oxygen, there is a second way of getting energy: the anaerobic respiration equation:

C6H12O6 yields 2C3H6O3 + Energy

(That is, food yields lactic acid plus energy (although much less than the aerobic respiration.) Lactic acid itself needs oxygen to break down, so you cannot run on anaerobic respiration for very long.

If you want to evolve endothermy, you need to:

So, where do we stand on dinosaur metabolism?

What would be necessary to justify the above observations?

Is there evidence for these features in dinosaurs? YES!

Dinosaur Respiration and Circulation:

Most tetrapods breath by gulping air and by rib breathing to some degree. Primitive tetrapods are subject to Carrier's Constraint: the same muscles for breathing are used for locomotion (bending from side-to-side). Thus, most primitive tetrapods tend to hold their breath while breathing, meaning that they rely more on anaerobic respiration and require long recovery intervals.

In living mammals, rate and volume of respiration is increased using a system independent of the side muscles. In particular, mammals have a diaphragm muscle separating the lungs and heart anteriorly from the liver, digestive system, etc., posteriorly. As the diaphragm moves forwards and back, the volume of the lungs decreases or expands (respectively) and the mammal breathes out and in (again, respectively). A consequence of this is that mammals have their trunk region subdivided into a thoracic section containing the lungs and heart (where the vertebrae have ribs) and a ribless lumbar section posterior to that for the guts. Mammal-style diaphragm breathing is actually an advanced therapsid feature; many advanced therapsids have dorsal vertebrae into thoracic and dorsal sections.

Specialized lizards such as varanids (monitors) developed neck pump breathing separate from rib breathing. As with mammalian diaphragm breathing, this allows them to pump air into their lungs while moving, giving them the ability to have sustained locomotion.

Living dinosaurs (birds) have extremely specialized breathing:

Crocodilians have their own specialized breathing, the liver pump:

This has led to speculation that the ancestral archosaur (technically, archosauriform) trait was belly breathing: Furthermore, strong evidence that theropods and sauropods (at least) had air sacs like those of birds:

Dinosaur Hearts:

Among modern amniotes:

Since both birds and crocodilians have four-chambered hearts, assumption is that all extinct archosaurs, including non-avian dinosaurs, did too. It is noteworthy that all animals with a parasagittal stance (mammals, ornithodirans, and advanced pseudosuchians including the ancestors of crocodilians) are forms known or inferred to have a four-chambered heart. It is likely that the separation of lung- and body-blood pressure is a prerequisite for an upright body. Furthermore, it might be necessary for a TALL body (one where the head is held high, and thus requiring a quite high body blood pressure.)

Keeping the Heat In: Insulation Issues:

So dinosaurs likely had efficient means to get fresh oxygen, spread it around the body, pick up the waste carbon dioxide, and flush that out of the body. That part of the requirements of being an endotherm were taken care of. What about controlling heat?

One problem that small-bodied organisms encounter is the fact that a small organism has a much higher surface area/volume ratio than a large one. Because of this, small animals tend to lose heat much faster than big ones. In contrast, large animals lose heat to or gain heat from the outside world only gradually. This has led some people to suggest the possibility that large dinosaurs exhibited "gigantothermy": effective homeothermy achieved because of large body size. However, this would not apply to small-bodied dinosaurs: either adults of small species or the hatchlings of giants. So how could these keep warm?

There is strong evidence that many--if not most--of the theropods had a fuzzy body insulation over the body: true feathers in the advanced groups, simpler "protofeathers" in the primitive ones. Such fuzz would help keep the warmth in the body. In fact, this is the primary function of the fur of mammals, and one of the functions of body feathers in birds. The recent discovery of 1.4 t Yutyrannus demonstrates that even some giant theropods were fuzzy.

Recent discovery of the early Late Jurassic Chinese ornithischian Tianyulong and the similar aged Kulindadromeus of Siberia showed they too had a fuzzy body covering over at least part of its body! If this is found to be homologous to the protofeathers of tetanurine theropod saurischians it would suggest that the concestor of all dinosaurs was fuzzy, and that dinosaurs were thus fuzzy ancestrally! (In the case of Kulindadromeus, there are also also scales, plates, and additional bizarre tufted plates.) At present, however, there is enough uncertainty to make the homology between Tianyulong's fuzz, Kulindadromeus's diverse integument, and theropod protofeathers suspicious. (But do not be terribly surprised if in the future we discover that most dinosaurs were fuzzy to some degree or another! All we need is a fuzzy primitive sauropodomorph, and it is basically a done deal!)

Dumping Heat: Mechanisms to Remove Heat

While small animals have an issue of keeping heat in, larger animals (with their low SA/V values) often have the reverse problem: they need to be able to dump heat. Similarly, small active animals sometimes need to quickly dump heat, too (for instance, when it is hot or after a bout of acivity).

There are two main pathways to getting rid of heat:

The large body size of many dinosaurs gives them a low surface area/volume ratio, so that it is hard for them to lose internal heat. Many of them have structures which increase their surface area without greatly increasing their body volume: these may serve, in part, as radiative coolers. Some dinosaurs, for instance, have conspicuous large sails or plates or frills or long necks or long tails that might have been used to dump waste heat. (Many of the same structures probably had display functions as well, since both behaviors require many of the same attributes: in particular, increasing the surface of the animal.) However, other structures may have also been used to regulate temperature.

One possible function for the paranasal sinus (the structure that is housed in the antorbital fenestra (and which in various theropods also forms the promaxillary and maxillary fenestrae) may have kept the skull cooler. Some sauropods have traces of numerous blood vessels on their snout and inside their mouth, where it could also cool things down. Whether this was more radiative or evaporative is difficult to say.

But a key feature in dumping heat many larger dinosaurs seems to have been evaporative cooling through enlarged and/or elaborate narial regions. The enlarged narial regions may support tissues for another function as well: recovery of moisture. In living endotherms, rapid rate of respiration would dry out lungs if not for some specialized tissues called nasal turbinates:

An secondary advantage of using respiratory turbinates to dump heat is that it helps direct some of the air flow onto the part of the nasal chamber associated with olfaction:

An important aspect of putting cooling structures (either radiative cooling or evaporative cooling) in the nose and mouth is that the next stop along the pattern of blood flow is the brain.

It has just recently been recognized that the expanded frontopareital fossa (anteriorly-expanded sections of the supratemporal fenestrae) were filled by vascular tissue and fat rather than by muscle. So these areas may have helped to radiate heat to keep the brains of dinosaurs cool (they seem to have that function in modern crocodilians):

A Complication: Ancient Atmospheres

Even as dinosaurs were evolving, the atmosphere they were breathing was evolving, too. Geochemists have seen that the ratios of various gases, including oxygen, have varied over geologic time. At least some models suggest that the Middle Jurassic though the end of the Cretaceous had oxygen levels exceeding the present 20%. This would mean that every breath a dinosaur took would have more oxygen, making it easier to power a high metabolism.

Furthermore, experiments of growing plants of Mesozoic varieties under Mesozoic-style atmospheres suggests that their productivity (essentially, the amount of nutrients they produce per area per unit time) could go up 2 to 3 times present day conditions. If so, then there would have been more food available per unit area for the herbivores (and from this up the energy pyramid), again making it easier to be an endotherm in these conditions.

Another Complication: Is Crocodilian Ectothermy a Reversal?

Most studies assume that endothermy evolved sometime after the bird lineage (Ornithodira) and the crocodilian lineage (Pseudosuchia) diverged from each other. This is because crocodilians are ectotherms, as are all the next several outgroups (lepidosaurs, turtles). However, what if crocodilians were not ancestrally ectotherms, but instead reverted to a cold-blooded physiology from warm-blooded ancestors?

There is some evidence that this is the case:

This has led to speculation that the ancestral archosaurs were in fact more warm-blooded than crocodilians, and that the latter evolved "cooler blood" after the divergence of their lineage from other types of pseudosuchians. Thus, the origin of avian warm-bloodedness would not have occurred within Dinosauria, but at least in part before the bird line-croc line split.

Are Varanids (Monitor Lizards) a Model for Proto-Endotherms? Today's Varanidae (the monitor lizards, such as Australian goannas and Indonesia Komodo dragon) may give insight what the ecotherm-endotherm transition might have been like. Varanids have long been noticed to have a higher level of sustained activity (and consequently larger home range) than other lizards. They also have ziphodont dentition (recall that Megalosaurus teeth were specifically compared to monitor lizards!) for tearing and shredding meat rather than swallowing their food whole, allowing for faster digestion. They even have a heart that "cheats" and acts like a proto-four chambered heart, so that the lung and body blood pressures are different! These changes could be what was present in the ancestral archosaur, giving an ectothermic animals the capacity for higher endurance and activity levels, as a stepping stone to becoming true endotherms.

Mighty Mites: The Possible Role of Miniaturization in the Rise of Endothermy

It has long been observed that the two major groups of terrestrial endotherms (mammals and birds) both originated as quite small animals compared to their relatives. Furthermore, the ancestral lineages from which they were derived show indications of elevated metabolisms that don't rise to the level of full endothermy. So some have suggested that proto-endothermy arose in pre-mammalian therapsids and non-avian theropods to allow increased activity levels, and that the shift to tiny size (and its necessity for such things as increased insolation and the general allometric aspect of increased metabolic rate in smaller animals anyway) pushed them to true endothermy.

There is some merit to this thinking, but in your instructor's opinion the transition in avian history did not occur WITHIN Theropoda, or even Dinosauria. The shrinking of body size at the base of Eumaniraptora is not the only case of miniaturization in the lineage leading to birds. As you recall, the first members of Ornithodira were small-bodied forms (Scleromochlus, lagerpetids, lagosuchids, etc.), and from that point onward both pterosauromorphs and dinosauromorphs show considerable evidence for high metabolic rates. Indeed, we have evidence of insulation in both Pterosauria and (possibly) at the base of Dinosauria, and quite frankly no positive evidence of its absence in other pterosauromorphs and dinosauromorphs: fuzz might well be an ornithodiran trait!

So one reasonable hypothesis is that the switch to some form of endothermy occurred not with the origin of birds, but rather with the origin of Ornithodira.

Summing it All Up

So where do we stand on the question of "were dinosaurs warm-blooded"?:

A relevant video:

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Last modified: 23 July 2021

The fuzzy neornithischian Kulindadromeus by Andrey Atuchin (2014)