•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.
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 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 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)
Energy Source: whence comes the majority of the energy to "run" the animal?
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 (and now we know in rebbachisaurids)
Problem: Most ornithischians and sauropods lack quite as sophisticated chewing or slicing teeth
Does not negate observation that hadrosaurids, ceratopsids, and rebbachisaurids 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
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 was 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
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)
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 ectotherms. 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).
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!
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
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
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 pseudosuchians, 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
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
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:
Eat or be Eaten: Dinosaur Paleoecology
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
Pseudosuchian-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
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 ñ 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, independent 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:
From geometry, as linear dimensions double, the surface area goes up by squares, and the volume by cubes:
Surface Area (SA)
6/1 = 6
24/8 = 3
54/27 = 2
96/64 = 1.5
As size increases, SA/V decreases.
The mass of an animal, and the heat it produces, is based on its volume.
The rate at which an animal can gain and lose heat is based on its surface area.
Therefore, with bigger body size it takes longer and longer for heat to be lost or gained:
Become homeothermic without having the energy costs of endothermy!
Problem: No good living models (elephants once thought to be partial gigantotherms, but does not now seem true; marine leatherback turtles are, but are not in same type of environment)
Also, gigantothermy might apply to large dinosaurs, but would not apply to small species or to babies.
Changeable metabolic rate: tachy- to bradymetabolic.
Two main types: behavioral and ontogenetic:
Normally operate as bradymetabolic, but shift into "high gear" in certain circumstances
Living examples: sharks in feeding frenzy; pythons while brooding
Some have suggested that specialized breathing structures may have let dinosaurs be "turbo-charged", but have fully ectothermic physiologies
In most animals, metabolic rates slow down as age (and thus size) increases
Perhaps in dinosaurs was more extreme
Problem: No good living examples
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:
Most extinct outgroups to the living crocodilians had a more upright stance (in fact, many of them parasagittal) allowing for more aerobic breathing (and at least one genus shows growth rates comparable to dinosaurs, pterosaurs, and mammals)
Crocs retain many ancestral features (unidirectional flow in the lungs; four chambered heart; etc.) that are useful for endotherms but not at all required for ectotherms (since lepidosaurs, turtles, and amphibians do fine without them)
Crocs have mitochondria of the "leaky" type used in endotherms to generate extra heat: however, they have far fewer of them per cell than living birds and mammals.
Living crocodilians are aquatic ambush predators living in thermally stable environments: these are conditions which would favor selection away from high metabolic rates to slower ones
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?
A New(-ish) Idea: Mesothermy
In 2014 a study came out proposing that dinosaurs were intermediate between endotherms and ecotherms, and the authors termed them "mesotherms". (In fact, Dr. Scott Sampson had proposed the concept and the name "mesothermy" years earlier...). The particular study estimated both the maximum growth rate of fossil dinosaurs and their inferred metabolic rate (based in part on growth rate, so the whole study may wind up being a circular argument...). They found that most Mesozoic dinosaurs (including Archaeopteryx) fell in a range intermediate between where modern endotherms and modern ectotherms plotted (but in the same region as
such animals as tunas, sharks, echidnas, etc.)
The authors interpreted this to mean that dinosaurs had the ability to generate internal heat, but did not greatly regulate their body temperature. So in fact, what they call "mesothermy" is technically not intermediate between endothermy and ectothermy, but between homeothermy and poikiliothermy. And thus dinosaurs in their interpretation would be in terms of this course endothermic mesotherms. In their interpretation, the rise of actual warm-bloodedness in the bird lineage occurred somewhere well within Pygostylia. Future analyses will have to be done to see if this model is upheld.