Nicole Klein is a vertebrate paleontologist at the University of Bonn who specializes in sauropodomorph dinosaur bone histology and marine reptiles from the Middle Triassic Muschelkalk deposits of Central Europe. She has done extensive fieldwork in many parts of the world, including Alaska and Nevada in the United States, and Ethiopia.

Kristian Remes has studied sauropodomorph anatomy, functional morphology, and phylogeny. He played a major role in the remounting of the famous Brachiosaurus skeleton in the newly renovated Dinosaur Hall at the Museum für Naturkunde in Berlin. He is now a program director at the German Research Foundation (DFG).

Carole T. Gee, a senior research scientist at the University of Bonn, has worked on the Mesozoic flora for the last 25 years. She is the Research Unit's paleobotanist and answers questions on sauropod herbivory and the Mesozoic vegetation. Her research applies the knowledge of living plants and their ecological preferences to the interpretation of fossil plants and their habitats, and also includes studies on Eocene mangroves, Tertiary fruits and seeds, and plant taphonomy.

P. Martin Sander is a professor of vertebrate paleontology at the University of Bonn and head of the DFG Research Unit 533 "Biology of the Sauropod Dinosaurs: The Evolution of Gigantism." His research interests are the major events in the evolution of tetrapod vertebrates and how the fossil record helps us to understand them. His core expertise is the microstructure of dinosaur bone and the diversity and evolution of marine reptiles.

Biology of the Sauropod Dinosaurs

Understanding the Life of Giants

Indiana University Press

Contents

Sauropod Biology and the Evolution of Gigantism: What Do We Know?

MARCUS CLAUSS

Life scientists are concerned with the description of the life forms that exist and how they work—an inventory of what is. Additionally, life scientists want to understand why life forms are what they are—from both a historical and functional perspective. Evolutionary theory offers a link between both perspectives via the sequence of organisms that have evolved and are constantly adapting to their environment by natural selection. But, still unsatisfied, life scientists want to discover why selection acts in a certain way. We want to understand what is within the framework of what is possible, by distilling universal rules from our inventories to understand the limitations of what could be. Only if we understand what is possible will we be ready to accept historical reasons for the absence of a life form. "It just didn't happen" will only sound plausible and satisfying if we know whether it could have.

With this approach, any expansion of the inventory of what is will automatically lead to a reevaluation of those theories that explain what is possible. Every discovery of a new species or a new ecosystem will make such a reevaluation necessary; the more the new discovery deviates from what has been recorded so far, the more necessary the reevaluation. In this respect, dinosaurs are invaluable to us. They expand the inventory of life forms that have developed at some stage during the existence of our planet and evidently must have been subjected to a similar set of constraints that we assume for extant life forms. Yet because they are different enough, they are a challenge to our concepts —an outgroup against which our biological understanding must be tested. Therefore, as Dodson (1990) put it, advancing our understanding of dinosaurs also means understanding the world we live in.

Sauropods are the ultimate outgroup among terrestrial vertebrates simply because of their size. Their vast dimensions and sheer existence in the history of life oblige us to evaluate any potential limits of body size in terrestrial vertebrates. Whereas many other fossil life forms can fit comparatively easily within existing frameworks, sauropods appear so far out of the range that they are a definite challenge.

However, before the riddle of sauropod size can be solved, the seemingly more profane task of reconstructing these organisms from the fossil record must be carried out (Sander et al. 2010a). This alone can be demanding, as can be nicely traced in the history of sauropod research—for example, the conceptual shift from an aquatic to a terrestrial lifestyle, the shift from a viviparous to an oviparous reproduction, the shift from a sprawling to a columnar stance (McIntosh 1997), or the shift from a digestive system with a gizzard full of gastroliths to a digestive tract with no particle size reduction at all (Wings & Sander 2007). Knowledge about sauropod morphology, systematics, diversity, and evolution has been summarized by Upchurch et al. (2004) and Curry Rogers & Wilson (2005). The latter reference also deals with some aspects of sauropod biology.

With particular reference to the chapters of this book and to the work of our research group, the current knowledge about the history, form, and function of sauropods can be briefly summarized as follows (see also Sander et al. 2010a).

Sauropods evolved from basal sauropodomorphs, although exact phylogenetic relationships are not resolved (Chapter 8). They are characterized by a quadrupedal stance with columnar legs, a long neck and tail, and a comparatively small head (Chapters 8, 11, 15). Regardless of the large taxonomic diversity of sauropods, this basic body plan hardly varies (Chapter 8). Sauropods can be broadly grouped into forms with longer front legs, a presumably upright neck, and a rather cranial center of gravity, and forms with longer hind legs, a presumably more horizontal neck, and a rather caudal center of gravity (Chapters 8, 14). The reconstruction of their muscular and skeletal anatomy reflects biomechanical particularities of their body shape and size at the macroscopic as well as the microscopic level (Chapters 8–11, 15). Niche diversification in sauropod taxa can be inferred from differences in dental and cranial anatomy, neck length, and posture (Chapters 2, 10, 14, 15) as well as from isotope studies (Chapter 4). Sauropods were herbivores that did not chew their food and most likely did not possess other means of food particle size reduction, such as a gizzard with gastroliths (Chapter 2). They probably relied on symbiotic microflora in a massive hindgut to ferment plant material (Chapter 2), using the available plant resources of their time, as extant herbivores do today (Chapters 3, 4). They probably had heterogeneous "bird-like" lungs with air sacs and pneumatization of various bony structures, in particular the neck vertebrae (Chapter 5). It is generally thought that sauropods had a metabolic rate higher than that of extant ectotherms, although the difference in rates is still under debate; an ontogenetic decrease of metabolic rate has been suggested (Sander & Clauss 2008). Even more controversially debated is their cardiovascular system, for which consensus has not been reached, apart from assuming that they had fourchambered hearts (Chapter 7). Sauropods were oviparous and laid hard-shelled eggs, probably in numerous small clutches (Sander et al. 2008), which also facilitated fast population regrowth (Chapter 16). The young grew rapidly and reached sexual maturity in their second decade of life (Chapter 17). Parental care was probably absent and juvenile mortality high (Chapter 16), with different predators of the time feeding on the various ontogenetic stages of sauropods (Hummel & Clauss 2008). Although evidence has been hard to come by, it is likely that sauropods lived in groups or herds, some of which appear to have been age segregated (Coombs 1990; Myers & Fiorillo 2009).

All of the above does not sound particularly exceptional. However, sauropods did all this while achieving adult body masses between 15 and 100 metric tons (Chapter 6; Appendix). No other groups of terrestrial vertebrates have ever reached such a size. Because the advantages of a large body size (Chapter 12) apply to terrestrial vertebrates in general, the obvious question haunting life scientists (including paleontologists) is: what factors allowed the sauropods—and the sauropods alone—to become so large?

The easy way out is to simply answer that it is the combination of all the factors mentioned above that allowed these terrestrial vertebrates to become giants. In other words, to become as large as a sauropod, you have to be a sauropod. In a historical sense, this is probably true. In a functional approach, however, characteristics that are independent of body mass, characteristics that just follow body mass, and characteristics that truly facilitate gigantism should be differentiated from one another.

For example, many biomechanical adaptations of sauropods were a precondition for, and a consequence of, their large body size (Chapters 8–11, 15), but these adaptations appear easy to achieve by other vertebrates in the sense of convergent evolution and thus do not appear to be the crucial factors triggering gigantism. Actually, it is the universal applicability of the laws of static and dynamic mechanics that facilitates our understanding of these convergent adaptations. The origin of these adaptations, according to mechanical principles, makes them particularly suitable for investigations by computer modeling based on these principles (Chapters 10, 11, 13, 14). These studies are crucial for our understanding of how a giant works, but they cannot explain the origin—and the uniqueness—of sauropod gigantism. Similarly, the botanical (Chapters 3, 4) and nutritional (Chapter 2) composition of potential sauropod food and the presumably enormous digestive tract of sauropods (Chapter 2) can be described, but again, these factors do not set sauropods apart from other vertebrates. Unless we are thinking of absolute limits to skeletal static due to gravity (Hokkanen 1986; Alexander 1989), it seems that both the vertebrate musculoskeletal and the digestive system can accommodate any given body size, whether large or not.

Whether the same can be assumed for the cardiovascular system is a topic of intensive scientific debate (Seymour 2009a; Sander et al. 2009; Chapter 7). The peculiar neck of sauropods, which has been suggested to have been held in many sauropods in an upright, distinctly inclined or curved posture based on skeletal reconstructions and in analogy with extant amniotes (Taylor et al. 2009; Chapter 15), poses a dramatic conceptual problem in terms of the mechanics and energetics of the cardiovascular system (Seymour 2009a, 2009b). To me—an animal nutritionist and digestive physiologist with no background in cardiovascular physiology or musculoskeletal reconstructions—both sets of arguments appear convincing; the resolution of this scientific issue is a major challenge for future studies on sauropod paleobiology. However, it is noteworthy that the posture of a particular body part, not the giant body size in general, is the bone of contention here. Whether the topic of thermoregulation in sauropods (Chapter 7) is only interesting for the biology of these particular animals, or whether thermoregulation —and hence metabolism—is crucial for the evolution of gigantism is also subject to ongoing scientific debate. Different authors have claimed that gigantic body size poses a constraint on heat dissipation and hence the level of metabolism at which a giant can operate. However, at the First International Workshop on Sauropod Biology and Gigantism held by our research group in Bonn in 2008, Roger Seymour explained that data on the body temperature (Clarke & Rothery 2008), metabolic rate (Paladino et al. 1981), and geographic distribution of elephants do not point out particular problems with overheating in these animals and suggested that in previous models, the immediate transport of heat to the body surface via the vascular system had not been appropriately considered. Evidently, more elaborate models are needed to understand the potential implications of heat production and heat loss in giant organisms. At the gigantic size of sauropods, thermal inertia will have undoubtedly guaranteed a comparatively constant core body temperature. Analogy with extant "mass homoiotherms," such as giant tortoises, however, might raise doubts that their high level of activity (as inferred from sauropod trackways, for example) can be accounted for by mass homoiothermy alone. Growth rates assumed for sauropods (Chapter 17) are hard to imagine without high metabolic rates, and it has been suggested that gigantism as observed in sauropods is not possible for ectothermic animals (Head et al. 2009). As a convenient compromise between the different aspects of sauropod metabolism, we could consider the ideas of Farlow (1990) and Sander & Clauss (2008), who suggest an ontogenetic drop in metabolic rate (indicated by the dashed arrow in Fig. 1.1) that facilitated the rapid growth of juveniles but eased heat stress and nutritional requirements in adults. This hypothesis awaits further corroboration.

When comparing sauropods to giant terrestrial mammals, anatomical and physiological features set sauropods apart—in particular their mode of reproduction, long neck, respiratory system, and lack of mastication. In contrast, growth rates and possibly metabolism were similar enough to some degree in these groups (Chapters 2, 5, 15–17). Therefore, the hypothesis that it was a combination of these factors that made sauropod gigantism possible comes to mind (Sander & Clauss 2008; Fig. 1.1). However, each of these factors will have to be scrutinized for plausibility and, if possible, tested.

Testing physiological features in extinct animals is obviously problematic. More precise concepts of niche partitioning are difficult to evaluate because the fossil record does not provide sufficient resolution to associate specific dinosaurs with specific plants (Butler et al. 2009, 2010; Chapter 4). Bone and dental tissue can yield information on growth through histological analyses (Chapter 17), as well as additional information on diet, thermoregulation, and migration through isotope analyses (Tütken et al. 2004; Amiot et al. 2006; Fricke et al. 2009; Chapter 4). Isotopic studies in particular have the advantage that they present alternative approaches to questions that have previously been answered with other methods; in this respect, they represent true tests. So far, such tests appear to be in accordance with our hypotheses.

Unfortunately, generating hypotheses that are based on skeletal features that can be tested by other skeletal features alone is rarely possible. The association of features that facilitate the rearing of a sauropod on its hind legs and the mobility of its neck (Chapter 14) represents such a rare example. For other hypotheses—such as the possible role of a long neck, the presence of a bird-like respiratory system, and the absence of mastication—more theoretical approaches, often involving allometric extrapolations, have to be used. Because sauropods invariably lie outside the range of the data from which the allometric regressions have been derived, such an approach must always remain speculative. Only the qualitative difference between vivipary and ovipary is so evident that its relevance for population survival can be immediately understood (Chapter 16).

Whether a long neck represents an energetic advantage, as suggested in Chapter 12, that might have enhanced the evolution of giant body size, or whether it simply represents a feature that most nonchewing herbivores could evolve independently of body size has been hotly debated within our research group. As long as model calculations on the energetic costs and benefits of long necks over the entire body size range covered by juvenile to adult sauropods are lacking, this issue will remain unresolved (Seymour 2009a, 2009b; Sander et al. 2009). Similarly, the potential advantage of bird-like lungs remains speculative as long as physiological models that take a comparative approach in quantifying particular lung functions—for example, that of heat exchange—for "mammal-like" and "bird-like" systems are lacking. However, even if the direct link between bird-like lungs and gigantism is not yet compelling, its absence in both terrestrial mammals and the Ornithischia (Wedel 2006; Fig. 1.1), which both did not attain the giant sizes of sauropods, is a strong indication for the relevance of such a system in the evolution of gigantism. Unfortunately, we still lack a model demonstrating that mammal-like lungs constrain body size.

However, for another sauropod characteristic, such a constraint can be comfortably assumed, and it is with the narrow-mindedness of a researcher trapped in his own research field that I state here that its connection to gigantism can be considered relatively obvious: the absence of mastication (Sander & Clauss 2008; Sander et al. 2010a, 2010b). As with the respiratory system, sauropods differ from both mammalian and ornithischian herbivores in this respect (Fig. 1.1). Among terrestrial mammalian herbivores, which all display formidable adaptations for masticatory particle-size reduction of their food, the percentage of time spent feeding increases in an allometric fashion with body mass that would require feeding for more than 100% of the day (Owen-Smith 1988; Chapter 2) in animals weighing more than approximately 18 metric tons. Because this threshold coincides with mass estimates for the largest terrestrial mammal (Indricotherium; Fortelius & Kappelman 1993), the largest ornithischian (Shantungosaurus; Horner et al. 2004), and roughly with the lower body-mass range of the adults of many sauropod taxa, the interpretation appears attractive that herbivores, once they had evolved the very efficient adaptation of mastication, were prevented from evolving giant body size because this would have necessitated a secondary loss of mastication. Thus, it seems that a primitive feature of sauropods—the absence of mastication—allowed them to enter the niche of giants. From a certain body size onward, food particle size will be determined by plant morphology alone and hence will remain rather constant, while gut capacity will further increase with increasing body size. Therefore, sauropods might represent a rare example of herbivores that actually benefit from an increase in body size in terms of a larger gut and a longer retention of food in that gut without incurring the disadvantage of decreasing chewing efficiency (Chapter 2).