Sauropod Dinosaur Gigantism and the Evolution of Maximum Body Size in Other Dinosaurs and Mammals
P. Martin Sander, University of Bonn, Germany
Sauropod dinosaurs like Brontosaurus where the largest animals to ever walk the land. Immediately recognizable not only by their sheer size but by their extremely long neck bearing a diminutive head, sauropods are some of the most iconic dinosaurs (Fig. 1). Sauropods were not only huge but also hugely successful, both in terms of their temporal range and their geographic distribution. Unlike horned dinosaurs (ceratopsians), that are only found in eastern Asia and in western North America, sauropod bones have been found on all continents and in rocks spanning the entire age of dinosaurs, from the Later Triassic to the end of the Cretaceous. Sauropod dinosaurs exclusively fed on plant matter, and you could say they were the most successful of all herbivores. Having considered all this, we need to return to their extraordinary size or gigantism.
Figure 1. Reconstruction of the skeleton of the giant sauropod Argentinosaurus from the Late Cretaceous of Argentina. The author is the red spot between the front legs of the skeleton which is 40 m long. The reconstruction illustrates the enormously long neck of sauropods. Photo Frank Luerweg, University of Bonn.
Several years ago, evolutionary biologists realized that sauropod gigantism is not easily explained in the face of all the other large plant eaters that lived at the time of the dinosaurs (i.e., ornithopod dinosaurs, including ceratopsians and duck-billed dinosaurs or hadrosaurs) and afterwards, during the age of mammals (titanotheres, brontotheres, rhinos, and elephants) that all remain much smaller. To put it simply: Why are there no 50-t elephants today? This question makes it clear that by understanding sauropod gigantism, we will gain a better understanding of body size and its limits in other land animals. Thus, sponsored by the German Research Foundation, a group of scientists of wide-ranging specializations set out to answer this question by first understanding how sauropods functioned as living animals and then by exploring what this meant for the evolution of gigantism. The group formed the Research Unit 533 â€œBiology of the Sauropod Dinosaurs: The Evolution of Gigantismâ€. It includes experts from geochemistry and zoology, materials science and animal nutrition, paleobotany and ecology, and, yes, paleontologists as well. This essay is about the theory that this team of scientists is putting forth to explain sauropod gigantism and what it tells us about maximum body size in mammals and other dinosaurs.
Figure 2. Life reconstruction of the brachiosaur Giraffatitan from the Late Jurassic of Africa. Note that the neck is held in an intermediate position between upright and horizontal, representing a compromise between these two hotly debated alternatives. Image courtesy of the Osaka Museum of Natural History.
Everybody has seen a photograph of a sauropod skeleton in a museum or a life reconstruction produced by painting or computer graphics (Fig. 2) . But what sources of information do we really have about sauropods? Sure, there are their skeletons, in varying states of completeness, with most laking the head. But there are several other kinds of fossils left behind by these giants, including eggs, footprints, and fossilized skin. In addition, the internal structures of the vertebral column, bone microstructure as observed under the microscope, and the chemical composition of the bones offer important clues to understand sauropods as living animals. We have identified a unique combination of four factors in the biology of sauropod dinosaurs that contributed to their gigantism, the absence of at least some of which limited body size in other dinosaurs and in mammals.
Figure 3. Comparison of maximum body size in the different groups of land-living animals. The sauropod dinosaurs Brachiosaurus (a) and Argentinosaurus (b) were much larger than the largest bird-hipped dinosaurs Shantungosaurus (c) and Triceratops (d), the fossil rhinoceros Indricotherium (e, the largest known land mammal), the African elephant (f), the giraffe (g), and the Galapagos tortoise (the largest living herbivorous reptile). Modified from Rauhut 2007.
It is worth having a closer look at these size difference (Fig. 3). The trivial observation that all dinosaurs are large appears to be true, with larger species being very common and smaller species being rare. In fact, like in elephants, small species of sauropods could only evolve on islands. Mammals, on the other hand are characterized by being generally small, from a few grams to a few kilograms, and there are only a few large ones. Another important observation is that largest meat-eaters are always much smaller (as measured in body mass) than plant eaters, the difference being 1 to 10. This is because making a living as a meat eater consumes so much more energy than peacefully munching on plants. All giants, sauropod, ornithopod or mammals, are thus vegetarians (Fig. 3). This observation also indicates that body size has something to do with energy, its uptake as well as its loss. Trends in body size evolution of predators are apparently tied to gigantism in herbivores, their prey. Sauropods being able to convert more energy from the environment into body mass than mammals or ornithopods meant predator hunting sauropods also had a larger energy base and could evolve to larger individual size.
Figure 4. The unique combination of primitive traits and evolutionary innovations that made sauropod gigantism possible is visualized as a slider panel which also shows the settings for modern reptiles, ornithischian dinosaurs, and mammals. See text for explanation.
So what about these four factors? They are: 1) a high basal metabolic rate (BMR), 2) egg laying, 3) not chewing, and 4) a bird lung (technically: heterogeneous avian-style respiratory system) (Fig. 4). Bone microstructure, which preserves beautifully in dinosaur bone and is very well studied in sauropods and other dinosaurs, tells us that they all were growing fast (Fig. 5), on the order of mammals of similar size, but unlike cold-blooded reptiles that grow much more slowly. Fast growth is necessary to reach a large size in a relatively short time, because if you grow too slowly, the odds of surviving to the reproductive age are low. This is probably the explanation why never any multi-tonne ectothermic reptiles such as giant turtles or giant lizards evolved. Apart from requiring a lot of food, a high BMR creates another problem for large animals, which is overheating of the body. With increasing body mass, the surface area through which the animal can loose heat generated by exercise becomes relatively ever smaller. Special cooling surfaces, such as the African elephant's large ears, are necessary.
Figure 5. Fossilized sauropod bone as seen under a microscope in a petrographic thin section. The microstructure is well preserved and reveals a kind of bone tissue known as fibrolamellar bone. This kind of bone is only seen in fast-growing endotherms (birds and mammals) today and indicates high growth rates in sauropods. The inset shows the complex structure of fibrolamellar bone with a scaffold of woven bone filled in lamellar bone.
Next comes reproduction. It is an intriguing idea that laying eggs allowed dinosaurs in general to grow to a much larger size than mammals. Letâ€™s see how this idea works: comparison between living egg layers such as birds and crocodiles and mammals indicate that the number of young decreases with increasing body size in mammals but not in crocs or birds. Elephants and whales are a good example. Mammals opted for taking care especially well of their few offspring, which is a successful strategy under normal conditions. However, if conditions deteriorate and populations crash catastrophically, a population of mammals will be much slower to recover than a population of as similar-sized egg layers and will go extinct if another catastrophe strikes. Extinction can only be avoided by having a large enough population, but a large population means that the individuals in the population cannot be too big because resources are (almost always) limited. Dinosaurs, on the other hand, could have existed at much lower population densities, meaning that more resources went to the individual, allowing it to be bigger. This is the theory, but it fits very well with the observations on sauropod eggs (Fig. 6) which are very small (at most 5 kg) compared to the adult, meaning that the mother would have laid dozens or hundreds of eggs each year. Thus, very few but large sauropod individuals were enough to avert extinction of the species. Note that this observation applies to dinosaurs in general and thus does not explain why sauropods got so much bigger than other dinosaurs. It does, however, explain nicely why dinosaurs in general were so much larger than modern mammals.
Figure 6. A sauropod egg from the Late Cretaceous of southern France belonging to Megaloolithus, a name used for titanosaur eggs. Note the small size of the egg compared to size of the mother that must have weighed many tons. Since eggs cannot be much larger than 10 l in volume for biomechanical reasons, sauropod babies must have been very small compared to their parents. The small size of the eggs meant that the mother would lay many of them. Photo Georg Oleschinski, University of Bonn.
As mammals, we take chewing our food for granted, but we need to keep in mind that chewing is an evolutionarily advanced behavior that is not seen in primitive reptiles and evolved independently in ornithopod dinosaurs and mammals. In fact, ceratopsians and hadrosaurs have highly refined cheek tooth batteries that must have allowed them to chew their food finely and evenly. Not so sauropods, who only bit off the plant parts and then swallowed them as fast as they could, letting the digestive tract do the job of breaking down the plant matter. We know this because of the simply shape of sauropod teeth (Fig. 7) and because there is no indication of cheek muscles. However, not chewing and wolfing down the food was crucial for sauropod gigantism because only this strategy allowed the very small head, as seen in Camarasaurus and Diplodocus for example, and the very long neck to evolve. The larger a mammal or a ceratopsian gets, the disproportionally larger the head is getting. This is because the energy demand of the animal increases faster than its chewing power. A large head with heavy chewing muscles and big teeth cannot be carried on a long neck. And the long neck, so pervasive in sauropod evolution, is what seems to have conveyed the energetic advantage to sauropods, being a major factor allowing their gigantism. This is because the long neck made continuous feeding possible, without moving the heave body. The large size of adult sauropods would also have obviated the need for chewing because the large body cavity would have provided enough room for the slower fermentation of the larger plant particles that were just bitten off, not chewed.
Figure 7. Part of an isolated upper tooth row of the island dwarf sauropod Europasaurus from the Jurassic of northern Germany. The teeth are relatively week and thin and were continuously worn down and replaced. The dashed line marks the midline of the tooth row. Photo Georg Oleschinski, University of Bonn.
Finally, the respiratory system of sauropods must have contributed in several ways to gigantism, both through direct energy savings and by making the long neck possible. Sauropod vertebrae are amazingly complex anatomical structures, consisting of thin ridges of bone surrounding deep excavations and even holes in the sides of the vertebrae (Fig. 8). Such holes, called pleurocoels, are only found in birds among living animals. Pleurocoels allow the entry of parts of the respiratory system into the interior of the bone, filling it with air and thus lightening the skeleton. In birds, this is possibly because there is a strict separation in the respiratory system between the parts that manage the airflow and the gas exchange parts, the actual lungs. Pleurocoels and the shape of the vertebrae indicate that already the ancestor of theropods, of which birds are a surviving group, and of sauropods had this complex heterogeneous avian-style respiratory system we call a bird like lung.
Figure 8. An anterior neck vertebra of the of the island dwarf sauropod Europasaurus. The beautifully preserved vertebra is seen in left lateral view. Note the complex shape with the abbreviations used to describe this morphology. The many cavities in the side of the bone indicate that air sacs extended into the interior of the vertebra. From Carballido & Sander 2013.
The advantages for sauropods were not only that the bird lung lightens the skeleton, and in particular the neck, but that it takes up oxygen continuously and solves the â€œdead-space problemâ€ caused by a long neck. The intricate air management system of the bird lung, consisting of air sacs, funnels fresh air into the gas exchanger even upon exhaling and not only upon inhaling. Obviously, less energy needs to be spent on breathing that way. The dead space problem is encountered when the windpipe has a volume that is more than one tenth of that of the lung, leading to stale air being pushed back and forth in the windpipe. As neck length increases, so does windpipe volume. A long neck thus requires a huge lung volume, provided by the air sacs in birds. The mammalian lung design, on the other hand, would preclude the evolution of a neck as long as that of a sauropod. An added benefit of the bird lung is that it could have solved the overheating problem of sauropods by providing internal heat exchange surfaces, the animal cooling itself simply by breathing, as is known from living birds. A unique combination of primitive traits combined with evolutionary novelties thus can be seen to directly and indirectly (by making the long neck possible) allow sauropod gigantism. Primitive traits are egg-laying and not chewing plant food, and evolutionary novelties are the high basal metabolic rate and the heterogeneous avian-style respiratory system. The long neck is the ultimate evolutionary novelty, central to giving sauropods an energetic advantage over other dinosaurs and mammals, allowing a larger body size. Looking at the distribution of these primitive traits and evolutionary novelties among the other very large herbivores to have evolved in the history of life on Earth, i.e., ornithopod dinosaurs and mammals, it now becomes clear why their body size ceiling hung so much lower than that of sauropods (Fig. 4): Mammals were limited in body size by live-bearing, not chewing, and their lung anatomy, thus staying smaller than ornithopod dinosaurs that were primarily limited by chewing and possibly by lung structure (Note that we know very little about ornithopod lungs except that they do not seem have been of the avian type). It also becomes apparent that modern reptiles, which are rarely herbivorous, are generally so small because of their inability to grow fast, caused by a low BMR. The other aspect of a low BMR, i.e., a low body temperature, also makes it difficult to subsist on plant matter because its digestion trough microbial fermentation works much better at higher temperatures, unlike the enzymatic digestion of animal matter. So, despite laying eggs and not chewing, and despite having a somewhat heterogeneous lung, their inability to evolve a high BMR severely limits reptile body size. This seemingly coherent picture faces a few challenges, however, and raises a few questions. For example, maybe environmental conditions during the reign of the sauropods were so much better than before and after that sauropods could evolve to a larger size? Such environmental factors would be atmospheric composition and global temperature. While global temperature was higher than today, oxygen content was lower, but, more importantly, these parameters shifted throughout the Mesozoic without maximum dinosaur body size shifting with them. In addition, favorable environmental conditions should have allowed ornithopod gigantism at the same order of magnitude as that of sauropods, which is not the case. Environmental factors are thus an unlikely explanation for sauropod gigantism. Another question arising from these considerations is why no multi-tonne herbivorous ground-living birds evolved in the Cretaceous or Tertiary, after the disappearance of the sauropods? This one is harder to answer and points the way to future research. Birds have the same favorable constellation for gigantism (long neck, high BMR, egg-laying, not chewing and a highly heterogeneous lung) as did sauropods. This puzzle helps in focussing on other constraints in bird evolution, yet to be discovered. Nevertheless, the approach taken here to understanding sauropod gigantism is of general applicability, not only explaining body size limits in other terrestrial animals but also providing a justification for studying dinosaurs as model organisms in evolutionary research.
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