Hot- and Cold-Running Dinosaurs?
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 enivronments. 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 temperaturs largely independent of the outside temperature, so they feel warm to the touch.

Old debate in dinosaur studies: were they warm-blooded or cold-blooded?

Owen in 1842 suggested dinosaurs might have been warm-blooded, or at least more warm-blooded than typical modern reptiles.

Need to be precise as to definitions of terms. "Warm-blooded" and "Cold-blooded" actually encompass several different (although related) topics:

• Energy Source: whence comes the majority of the energy to "run" the animal?
  • In "Cold-blooded" animals, the main energy source is the sun (and external environments in general): called ectotherms ("outside heat")
  • In "Warm-blooded" animals, the main energy source are specialized sub-cellular structures whose main purpose is to convert food energy to heat energy: called endotherms ("inside heat")
• Metabolic Rate: how much food energy ("fuel") is used up over time?
  • In "Cold-blooded" animals, rate of fuel usage is low: called bradymetabolic ("slow metabolism")
  • In "Warm-blooded" animals, rate of fuel usage is HIGH: called tachymetabolic ("fast metabolism")
• Temperature Variation over Time: how stable is the body temperature over time?
  • In "Cold-blooded" animals, body temperature fluctuates with the external environment: called poikilotherms ("fluctuating heat")
  • In "Warm-blooded" animals, body temperature regulated by internal mechanisms and thus more stable: called homeotherms ("same heat")

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.

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...).

Additional issues to consider:

• Resting metabolic rate (RMR) vs. active metabolic rate (AMR): "warm-blooded animals tend to have RMRs 4-10x that of similar sized "cold-bloods", but AMR is similar in both
• Duration of sustained activity: "warm-blooded" animals tend to have longer durations of sustained activity
• Recovery time between periods of activity: often much shorter for "warm-blooded" animals

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

• Increased aerobic capacity, allowing for greater total activity levels and greater ability to recover from sustained activity
• Greater environmental tolerance: endotherms can live in wider range of latitudes and altitudes
• Increased metabolic efficiency due to homeothermy: can "fine-tune" physiological systems to a narrow range of temperatures
• Increased ability for parental care: both brooding/gestating at constant temperature, and increased ability to watch over young

How can people determine the thermal physiology of extinct animals like non-avian dinosaurs?

Owen suggested dinosaurs might have been warm-blooded because:

• Upright posture: today, all living animals with upright posture are warm-blooded

Many late 19th Century paleontologists considered dinosaurs to be more similar to modern warm-blooded animals in terms of activity levels.

During early 20th Century, shift to lizard-like concept for dinosaurs.

Concept of warm-blooded dinosaurs revived in late 1960s by Ostrom because of a number of lines of evidence:

• Upright posture: as in Owen
  • Problem: No causal relationship ever established: just because all living animals with upright stance are endotherms does not mean that upright stance requires endothermy
• Dental batteries of hadrosaurids and ceratopsids: useful for chopping up food into very fine particles for fast digestion, but bradymetabolic animals don't have fast digestion; suggests tachymetabolism in hadrosaurids and ceratopsids
  • Problem: Most ornithischians and all sauropods lack sophisticated chewing or slicing teeth
    • Does not negate observation that hadrosaurids and ceratopsids have dental batteries
    • Modern herbivorous birds make do without grinding teeth by using gastroliths (gizzard stones) (see video below), which are found in non-hadrosaurid, non-ceratopsid herbivorous dinosaurs
      
      
      Ostrich - feeding behaviourBBC Natural History Unit
      
      
    • However, gastroliths are also found in some ectotherms, so their presence is NOT evidence of endothermy!
• Sickle claw and stiffened tail of dromaeosaurids: suggested a more dynamic mode of attack for dromaeosaurids than in monitor lizards or crocs
• High blood pressure necessary to pump blood into brains of tall theropods, ornithopods, and (most especially) sauropods: requires powerful, active heart
• Latitudinal distribution: dinosaurs (and therapsids) found in Mesozoic (and Permian-Triassic) polar regions, although not as cold as today would still be cooler than climates preferred by typical modern cold-blooded animals
  • Problem: Earth's climate WAS warmer in Mesozoic
    • However, some polar sites contain dinosaurs & mammals but not crocs, lepidosaurs, turtles, etc., while other sites in Alberta of same age are chock-full of known ectotherms
      • Maybe the dinosaurs migrated out of the polar sites during cold winters?
        • BUT energy requirements for large scale migration might arguably require endothermic levels of metabolism!!
        • Also, baby dinosaurs found in these sites: unlikely to have migrated
• Origin of birds from coelurosaurs: birds are known to be warm-blooded, so their immediate relatives might have been, too
  • Problem: Some argue that early birds themselves could have been ectothermic, with endothermy evolving AFTER the avialian line (or some part of it) had diverged from non-avian dinosaurs
• Complex social behaviors for at least some dinosaurs: no causal link, but more typical of modern mammals and birds than crocs, lepidosaurs, and turtles
  • Problem: As with upright stance, no causal link between endothermy and complex social behavior
  • Also, no evidence for such behavior in most dinosaurs

Colleague from France: Armand de Ricqlès added additional line of evidence:

• Bone microstructure: lots of signs of reworking (bone being resorbed as mineral source in metabolism, and redeposited), lots of Haversian canals.
• Typical bradymetabolic animals have little reworking and few Haversian canals; typical tachymetabolic animals have lots. Dinosaurs resembled tachymetabolics.
  • Problem: Suggestion that very old bradymetabolic animals might develop tissue similar to younger tachymetabolic animal
    • However, even baby dinosaurs show endothermic-style bone tissue

Ostrom's undergrad student Robert T. Bakker: main advocate for the "hot-blooded" dinosaurs model. Added his own observations:

• Ecological replacement: many paleontologists argued that therapsids were at least partly warm-blooded, but were replaced by archosaurs.
  • Problem: We do not know for certain that an ectothermic group would necessarily be out competed by endotherms
  • Also, other possible selective factors (i.e., water retention)
• Predator-Prey ratios: we'll discuss these in more detail below.

Additional lines of evidence (primarily from 1980s and 1990s):

• Oxygen isotopes: can determine body temperature and (importantly) variation of body temperature over time: dinosaurs show stable temperatures, while contemporary non-dinosaurian reptiles show larger variation.
  • Problem: Large bodied animals expected to have stable temperatures:
    • See gigantothermy below
  • However, baby dinosaurs match adults in stable temperature; don't match poikilotherms from same environment
  • More exhaustive study of isotopes for dinosaurs done during the 21st Century show that across the clade and across body sizes, dinosaur body temperatures seem independent of their environment! So the evidence unequivocally now points to homeothermy (however it ws achieved).
• Growth rate: fantastic growth rate (see earlier lecture) suggests tachymetabolism.
  • Problem: Maybe due to very favorable conditions of Mesozoic: allow fast growing ectotherms
    • However, known contemporary ectotherms (like giant crocs) show typical slow-growing rate comparable to modern ectotherms
• Presence of feathers on non-avian coelurosaurs and of dinofuzz in some ornithischians: since not flight features, might have been for insulation (which small endotherms need or they lose too much heat).
  • Problem: Not all dinosaur clades show feathers

Not everyone convinced that dinosaurs were fully endothermic tachymetabolic homeotherms.

Two main types of evidence to the contrary:

• Evidence suggested to counter claims of dinosaur endothermy (shown as Problems in the text above)
• Evidence suggest to support dinosaurian ectothermy

Lines of evidence supporting dinosaurian ectothermy:

• Small brain size:
  • Most dinosaurs characterized by brain sizes expected in crocs or lizards of that size; modern endotherms all have much larger brains!
    • Problem: However, no causal link established between brain size and metabolism
    • Also, coelurosaurs at least have larger brains than typical dinosaurs, and proportionately larger brains than contemporary mammals (which are accepted as endotherms)
• Small head size in herbivores:
  • Lack the big maws of large herbivorous mammals: how could they get enough food?
    • Problem: However, many large flightless birds have tiny heads, yet they are endotherms
• Lack of specialized teeth in most herbivorous dinosaurs:
  • Non-hadrosaurid, non-ceratopsid ornithischians and sauropods lack sophisticated chewing or shearing teeth
    • Problem: These other dinosaurs are known to have gizzards, which could process the food
• Overheating:
  • Because Mesozoic was warm, large dinosaurs would overheat if endothermic, so must have been ectotherms
    • Problem: Very large mammals (known endotherms) are found in comparably warm periods of Cenozoic
    • Some dinosaurs may have thermal "radiators" to dump heat (see below)
• Growth lines:
  • Dinosaur bones show "growth rings" (Lines of Arrested Growth, or LAGs), typical of reptiles and (once thought to be) lacking in mammals
    • Problem: Now known in perfectly good endothermic mammals
    • Are a symplesiomorphic feature of vertebrate bone growth; may not signal any aspect of thermal physiology
• Conspicuous potential solar collectors &/or radiators:
  • Stegosaur plates, neoceratopsian frills, sails in mid-K equatorial dinosaurs might be good radiators to dump heat or collectors to get heat
    • Problem: However, might be for display instead
    • Additionally, some endotherms (like elephants and their ears) have large solar radiators

And now, some 21st Century evidence:

• 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.
  • And the data for small dinosaurs and dinosauromorphs are at least consistent with endothermy for walking, and require endothermy if they were even moderate runners (as their skeletons and foot print evidence shows).
• 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.

Hearts, Lungs, and Faces: So You Want to Be An Endotherm?

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:

• Increase glucose intake, plus...
• Increase oxygen intake, plus...
• Increase the speed of distribution of glucose and oxygen throughout the body, plus...
• Deal with excess carbon dioxide, water, and heat.

So, where do we stand on dinosaur metabolism?

• All living dinosaurs (Aves) are endothermic tachymetabolic homeotherms
• The living outgroups (crocodilians, lepidosaurs, turtles) are all ectothermic bradymetabolic heterotherms
• Non-avian dinosaurs show many anatomical features suggesting levels of activity higher and/or more continuous than that seen in modern "cold-blooded" animals
• Non-avian dinosaurs show growth patterns comparable to those of modern endotherms, and unlike those of modern and extinct ectotherms

What would be necessary to justify the above observations?

• Non-avian dinosaurs would need active ventilation (breathing) to power the muscles and to fuel the growing tissue
• Non-avian dinosaurs would need strong, active heart to get the oxygen to the muscles and tissues
• Non-avian dinosaurs would need structures to control heat

Is there evidence for these features in dinosaurs? YES!

Dinosaur Breathing:

• Primitive tetrapods are subject to Carrier's Constraint: the same muscles for breathing are used for locomtion (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.
• Mammal-style diaphragm breathing is an advanced therapsid feature; most tetrapods breath by gulping air and by rib breathing
• Specialized lizards developed neck breathing separate from rib breathing
• Living dinosaurs (birds) have extremely specialized breathing:
  • Pump their lungs by rocking their hips up and down
  • Special air sacs in the torso, vertebrae, and limbs help keep the air flowing in one direction, rather than a simple in-and-out
• Crocodilians have their own specialized breathing:
  • Pubis is mobile, and rocks back and forth pushing & pulling the liver
  • Functions like the mammalian diaphragm, to have additional active breathing
  • Recent analysis shows that they, like birds, had unidirectional flow through their lungs (with passages rather than airsacs)
• Speculation: belly breathing is an archosaurian synapomorphy:
  • In primitive archosaurs, primitive crurotarsans, and most dinosaurs other than birds, muscles from the pelvis would pull gastralia down, which would inflate the lungs
  • This would give these animals extra oxygen for their metabolism
  • Becomes modified in crocodilians (liver pump with mobile pubis), pterosaurs (a mobile "prepubis"; another liver pump?), birds, and ornithischians (mobile pubes or other parts of the pelvis in some ornithischian groups)
  • Additionally, the air flow in all archosaurs would have been unidirectional
• Furthermore, strong evidence that theropods and sauropods (at least) had air sacs like those of birds:
  • Chambers in vertebrae are very similar to those of birds
  • Air sacs may have been present in other dinosaurs, but apparently did not enter the vertebrae

For more on vertebrate breathing, check out the website of experimental work on modern amphibians and non-avian reptiles.

Dinosaur Hearts:

• Turtles and lepidosaurs have three chambered hearts
• Birds and mammals have four chambered hearts:
  • A "double pump" system, so the heart acts as a control between lungs and body
  • Shunts blood to lungs before going out to body, so all the blood getting to the tissues are fully oxygenated
  • Also, can allow these animals to be taller, since the heart pressure control separates lungs and body, and therefore pressure on lung blood vessels won't get too high
• Crocodilians actually have specialized (NOT primitive) four-chambered hearts:
  • Operate as four-chambered heart on land, shifts to two chambered underwater since doesn't need to get blood to lungs
• Since both birds and crocodilians have four-chambered hearts, assumption is that all extinct archosaurs, including non-avian dinosaurs, did too

Dinosaur Temperature Regulators:

• Some dinosaurs have conspicuous large sails or plates or frills or long necks or long tails that might have been used to dump waste heat
• However, other structures may have also been used to regulate temperature:
  • The antorbital fenestra (also the promaxillary and maxillary fenestrae of various theropods) housed soft tissue air sacs
    • These air sacs may have been useful to transport waste heat
  • Also, many larger dinosaurs have enlarged and/or elaborate nares
    • These may have been useful in dumping waste heat

The enlarged narial regions may support tissues for a different function: recovery of moisture. In living endotherms, rapid rate of respiration would dry out lungs if not for some specialized tissues called nasal turbinates:

• Rare or small in modern ectotherms
  • Click on the "Dynamic Cutaway: Coronal" animation on this website to see the lack of turbinates in a CAT scan of the modern Chinese crocodile lizard
• Extremely large in mammals, where they are scroll work of bone in the snout, supporting thin tissues which trap moisture going out, and rewets on way back in
  • Click on the "Dynamic Cutaway: Coronal" animation on this website to see the turbinates in a CAT scan of a house mouse
• Fairly large in many birds, but are cartilage rather than bony
• Also, some birds seem to rely on air sac system for this purpose
• Most non-avian dinosaurs do not show much evidence for internal nasal turbinates, but the air sac system and/or tissues in the enlarged narial regions of bigger dinosaurs may have served this function

Eat or be Eaten: Dinosaur Paleoecology

As a review, ecology is NOT what most people think it is!
It is not environmental activism. Instead:

• Ecology is the scientific study of the factors which control the abundance and distribution of organisms.

Therefore, ecology isn't about saving the whales, but it WILL tell us something about HOW to save the whales...

Paleoecology is attempting to reconstruct the ecology of extinct forms.

Some aspects about paleoecology:

• Ecological niche: the "way of life" of a particular taxon
• Species ranges: how large an area did a particular species occupy at a given point in time (very difficult for most dinosaurs, as they are known from very few specimens)
• Trophic relationships: aka "who eats who". Often restored as a food web
  • Can get some good idea about carnivores vs. herbivores, but difficult to establish exactly which carnivores ate which herbivores, and which herbivores ate which plants.

Bakker used his interpretations of trophic relationships to try and determine the thermophysiology of dinosaurs and other extinct forms. His technique:
Predator-Prey ratios:

• In modern endothermic communities very few predators compared to many herbivores (tachymetabolic predators require a lot of food, so only a few can survive in a given region).
• Bradymetabolic predators require a lot less food, so same amount of potential food can support many bradymetabolic predators.
• In order to calculate P/P ratios, Bakker had to consider the different sizes of the various populations. Used biomass (# kgs or tons of flesh) rather than number of individuals
• Found that modern populations had P/P ratios of 0.5-4 %
• Looking at fossil record, found:
  • Basal synapsid-dominated faunas of the Early Permian: 25-30%, much higher than modern populations. Most paleontologists have accepted this as a cold-blooded community
  • Therapsid-dominated faunas of the Middle and Late Permian and earliest Triassic: 10-20%, seemingly between endo- and ectothermic populations
  • Crurotarsan-dominated faunas of the Middle and Late Triassic: 10-20%, as in 2nd
  • Dinosaur-dominated faunas of the Jurassic and Cretaceous: 0.5-3.5%, as in modern endotherms!
  • Mammal-dominated faunas of the Cenozoic: 0.5-4.5%, known endotherms
• Problems:
  • How do you know the dinosaur mass estimates are correct?
  • How do you know that the numbers accurately sample fossil populations?
    • At least the basal synapsid and mammal faunas seem to match expectations (but new finds from Germany may show almost mammal-like levels for upland basal synapsid communities!)
  • How do you know which dinosaurs ate which?
  • At best can only give the thermal physiology of predators!
    • For herbivores would need a Herbivore Biomass – Plant Productivity ratio
    • Some preliminary evidence suggests that MORE herbivores per acreage in dinosaur populations than in modern or fossil mammal populations

So, P/P ratios are problematic, at best. Some ways in which dinosaurs are distinctly different from modern mammalian communities:

• Much higher rate or production: dozen eggs per year, independant of size vs. litter size and gestation period scaled to body size
  • From this, dinosaur populations could absorb many more fatalities and survive than equivalent-sized mammals
• Also, dinosaurs occupied many more niches in their lifetime than a mammal, because all dinosaurs begin very small

• Is this whole debate a false dichotomy?
• Is everything EITHER an endothermic tachymetabolic homeotherm OR an ectothermic bradymetabolic poikilotherm?

Some additional possibilities: