How and above all where did dinosaurs live ?
Biomechanics of the Vertebral Column and Implications for the Lifestyle
of Dinosaurs and Certain Pelycosaurs
Contrary to former suppositions nowadays all dinosaurs are considered as land-dwellers, although there is no objective proof of this idea. It was created by R. Bakker who in the late sixties and seventies caused some turmoil, based on much fantasy and little physiological knowledge. Such an image of dinosaurs may be attractive and spectacular to children, however it is very questionable from a scientific viewpoint. My own investigations of vertebral columns of dinosaurs on a natural scientific basis have convinced me that there were dinosaurian land-dwellers on the one hand and on the other hand different representatives that lived preferably in shallow or moderately deep fresh water.
The ornithischians with the bird-like pelvic bones and long spinous processes on a strong vertebral column were the land-dwellers. The saurischians, that is theropods and sauropods, with a comparatively weak vertebral column inhabited preferably the water, though not exclusively. This idea is supported by arguments, based on an evaluation of forces acting on the vertebral column. The mechanical loads on a skeleton are considerably higher on land than in water, and the different shapes of spinal columns indicate their load capacity and thereby the preferred milieu of these animals.
Opposed to other suppositions all theropods fed primarily on fish. The ancestors were amphibians or even land-dwellers. However, in connection with the important radiation of fish during the Triassic period, with the time passing on the developing theropods became progressively fish eaters, wading on the ground of rivers and lakes. Several small forms learned hunting fish swimming under water. This behaviour is closely connected with the origin of flight in the air. Many different derived specialized swimmers including ichthyosaurs entered the open seas. Besides, the sauropods specialized in water plants.
Towards the end of the Cretaceous most dinosaurs disappeared. Only birds were mobile and flexible enough to occupy all ecological niches worldwide with large populations. Probably this is the reason of their survival..
Following the mysterious extinction of dinosaurs at the end of the Cretaceous the unoccupied ecological niches were soon taken over by the rapidly developing mammals The land-dwelling ancestors of whales (ungulates!) passed through a corresponding evolution as the saurischians had done. Obviously, fish was a most attractive food source for them. These mammals also entered first fresh water areas wading on the ground. Later on many different derived specialized swimmers such as whales, dolphins and seals entered the open seas. Besides, the sea cows specialized in water plants. However, flying mammals (bats) were unable to supersede the birds.
The spinal column represents a most important skeletal characteristic of vertebrates. Its shape is subject to remarkable differences within the classes of Reptilia and Mammalia. These differences can be regarded as a result of adaptations to loads of different magnitude as well as to different kinds of locomotion and attainable speeds. Details of the spinal column can yield important clues as to its main load distribution and consequently its special main task.
Using a biomechanical approach, recent investigations by Ebel et al. (1998) have demonstrated that the shape of vertebral columns is suitable to serve as an excellent criterion to obtain unmistakable indications as to whether an extinct vertebrate primarily used a bipedal or a quadrupedal gait. For the enigmatic rauisuchian reptile Ctenosauriscus koeneni (v. Huene) we could demonstrate that, contrary to former speculations, the long spinous processes did not serve functions such as thermoregulation or imposing, as incidentally mentioned by Krebs (1969). The investigation of this remarkable vertebral column concerning its function led us to the conclusion that it does not represent an accidental freak of nature, rather its shape follows clearly from biomechanical requirements. The directions of the upper tips of the dorsal processes pass through a common intersection. This point of intersection corresponds to the former position of the knee joint. In addition, the otherwise rare trait of a remarkable rectangular cross-section of the in part strongly curved spinous processes points to the capability of transmitting bending forces. Presumably, a facultative bipedal locomotion on land became possible in Ctenosauriscus only by the evolution of this extremely specialized vertebral column.
Fig. 1. Vertebral column of Ctenosauriscus koeneni (v. Huene) as reconstructed by Krebs (1969), redrawn and modified, functional interpretation as found by Ebel et al. (1998). Since during a step the directions of the resulting force acting on the primarily stressed leg pass through this point successively, most probably this animal utilized a facultative bipedal gait. The long spinous processes characterize Ctenosauriscus unequivocally as a land-dwelling animal. Most probably, this animal is responsible for many of the well-known Chirotherium tracks.
In connection with that investigation further questions arose, namely concerning the significance of strongly elongated spinous processes in further fossil forms such as the pelycosaur Dimetrodon and certain ornithischian dinosaurs on the one hand and the possible reasons of rather short spinous processes in bipedal theropod dinosaurs on the other. The explanation of the vertebral column in Ctenosauriscus as a result of an adaptation to locomotory requirements suggests the conclusion that the underlying physical principles should likewise be transferable to special developments in other forms. As will be discussed later on, the application of mechanical principles to the vertebral columns of dinosaurs and certain pelycosaurs allows an approach to the lifestyle of these extinct vertebrates from an entirely independent viewpoint which, therefore, does not necessarily lean on former suppositions and textbook opinions, mostly dating back to the nineteenth century. Such suppositions were in agreement with the restricted knowledge of those days, but in the meantime there has been some progress in natural sciences and applied physics. This view suggests an idea of extinct vertebrates which is quite different in some respects, but much less spectacular compared to suppositions propagated in various semipopular publications. Nevertheless it does not contradict observational evidence and opens most interesting aspects.
2. Problems associated with biomechanics in biology and palaeontology
Before pointing out the regularities and conclusions to be derived from an examination of vertebral columns as to their biomechanical adaptation, I would like to shed some light on problems with which palaeontology is burdened and by which it is seriously handicapped as to its possibilities to find actually plausible functional explanations. Such problems, unfortunately, make interdisciplinary activities unnecessarily difficult, but these are nevertheless desirable.
Although most important for all vertebrates, for a long time the vertebral column has attracted little attention only by palaeontologists. Abel (1912) barely mentioned it in his palaeobiological investigations of vertebrates. Apparently, remarkable differences of the shape of the various extinct vertebrates did not allow a detailed explanation beyond the commonly assumed carrying function. Certainly, the anatomy of the human skeleton has intensively been studied, e.g. by Pauwels (1965), but it belongs to an upright land-dwelling biped and, therefore, differs remarkably from the majority of vertebrates and is not well suitable for comparisons. Generally, aspects of biomechanical effects concerning the functional interpretation of skeletons of fossil vertebrates, unfortunately, do not play an important part in traditionally historically oriented sciences such as palaeontology, and if considered are mostly misinterpreted. Generally, palaeontologists have to rely mainly on morphological comparisons with extant forms and on functional morphology presumptions. Although the anatomist H. Virchow (1914) in his studies of vertebral columns regretted a missing interdisciplinary co-operation with technically trained people and Wainwright et al. (1976) pleaded for the utilization of mechanical principles in biology, nevertheless starting points based on applied physics as well as the employment of seemingly unusual methods are sometimes regarded with a certain unpleasance, e.g. Erben (1975: 113-114), and with utter disbelief. A missing familiarity with mechanical principles can even provoke unjustified and polemic reactions such as by Pfretzschner (1999). Surely, such reservations are caused by a different educational background. For this reason biomechanical aspects of fossil and even of modern skeletons are commonly poorly understood. Yet, this is merely a consequence of missing knowledge and the inadequate methods employed so far.
The evolution of a bony skeleton is nature’s highly admirable response to biomechanical requirements which only created the pre-condition for vertebrates to leave the water. Apart from certain protective functions the main task of bones consists in the transmission of forces, in particular compressive ones. But contrary to the assumptions in bridge analogies still in vogue, bones are not especially suitable for the transmission of bending moments, although bending loads do happen. Waisted spines (Bailey 1997) point to axial loads, whereas an adaptation to strong bending forces would generally require a triangular spine shape. A remarkable exception is offered by the conspicuous rectangular cross-section of the spinous processes in Ctenosauriscus which clearly points to acting bending moments within the so-called backsail. Generally, bones serve the attachment of muscles and only make possible strong muscular tensile forces and complicated movements such as those of arms and legs. If in the course of an adaptive development remarkable skeletal modifications occur, the investigation of biomechanical reasons should, therefore, have priority. Occasionally, the missing close familiarity of palaeontologists or biologists with physical principles and applied mechanics leads to a mere presumption of functions and thus to the utilization of a trial-and-error method, which cannot demonstrate its plausibility. A general knowledge of functional morphology and a profound one of anatomy is per se not sufficient to unveil the functional background of a skeletal design. Palaeontologists have been dealing with historical-narrative explanations for more than 100 years (Bock 1985), although rarely successfully. Seemingly reasonable conclusions based on common sense considerations can easily be misleading (Regal 1985, Ebel 1999). Objective criteria are preferable. Although the recognition of biomechanical functions and of acting forces requires some thorough experience in the field of applied mechanics, the familiarity with such methods can offer much progress in understanding the functional design of extinct vertebrates and in reconstructing their lifestyle. Palaeontologists can hardly find correct answers if they confine themselves to their normally applied methods and thus exclude important aspects from consideration.
Methods are available which can yield unmistakable evidence. Hertel (1963) has outlined some applicable procedures. However, such methods have barely ever been applied. The regrettable neglect is very hampering, and persisting uncertainties are reflected by the various competing hypotheses about the lifestyle of extinct vertebrates and never-ending controversial debates among the respective adherents. For example, Bailey (1997) has recently dealt with virtually the same problem as the author of this paper, namely significance and function of elongated spinous processes in the pelycosaur Dimetrodon, in the iguanodontid Ouranosaurus and in other dinosaurs, based on a comparison with Pleistocene ungulate mammals. Although he discussed a likely adaptation to biomechanical loads on the vertebral column of Ouranosaurus as well as the problematical cantilever-bridge analogy of Thompson (1942) and weighty objections against it by Slijper (1946), moreover mentioned the likewise questionable bowstring-bridge analogy, nevertheless he prefers the doubtful conclusion that the elongation of spinous processes in the forms in question is primarily linked with the formation of a hump, as present today for instance in Camelus or Bison, which he believes to have served a fat-storage function and enabled the animals to bridge long distances without sufficient food supply during seasonal migrations. Although he reveals some scepticism as to the ”new image” of pretended warm-blooded dinosaurs, nevertheless in his study he only sets arguments that seem to support a hump function against an unlikely thermoregulatory sail function. The idea that elongated spinous processes are linked with biomechanical loads corresponds to my thorough conviction, too, but the assumption of a predominant hump function cannot be substantiated. Basically, the elongation of the spinous processes in the region of the withers of mammals is entirely independent of the formation of a hump. If some mammals such as Bison store fat in this area this may be an accidental coincidence, but certainly it is not the cause of elongated processes. Although elongated and characteristically arranged spinous processes can be found in all ungulate mammals, the presence of a pronounced hump is rather a rare trait and not necessarily linked with the vertebrae of the shoulder area. As Ebel et al. (1998) have shown the length of the spinous processes follows exclusively from a response to mechanical loads. The hump interpretation appears as a false conclusion. A merely formal comparison of certain features in different forms by an empirical-analytical method without considering particular functional adaptations, as for instance carried out by Bailey (1997), can only describe a skeletal feature but not lead to a convincing explanation of its main function. Thorough observations are per se not sufficient to explain a feature if the physical reasons behind it are poorly understood.
Comparisons of extinct animals with Recent ones concerning their presumable lifestyle have also to take account of the partly enormous time gaps between the respective occurrences and of the fact that the level of development and activity has generally grown in the course of evolution due to competition and new requirements. It is well known that life does not represent a sequence of cyclical events in evolution and does not allow exact iterations, as morphological comparisons sometimes might suggest. It is very likely that the vertebral columns of the various forms discussed in this paper reflect an evolutionary increase of motility and attainable speeds. Different epochs are characterized by different skeletal designs with improving properties, but the underlying physical laws have remained unchanged. Vicious circles are inevitable if, as Kummer (1959: 38) did, the vertebral columns of large and small forms, of mammals, reptiles, and dinosaurs are investigated together in order to find a well fitting function for all types, without regard to their different ages, milieus, and possibly differing lifestyles. An explanation fitting to a Recent form must not automatically be transferred to an extinct one.
3. Criteria for the judgement of size and distribution of the main loads on vertebral columns
Nature has strictly to follow biomechanical requirements imposed by continuously acting forces in order to enable vertebrates to perform their main activities. Above all these are gravitational and inertial forces occurring in connection with locomotion. Extreme designs such as the Triassic Ctenosauriscus are particularly well suited to give an insight into the underlying physical design principles. Fig.1 shows Ctenosauriscus as reconstructed by Ebel et al. (1998) which gave rise to these considerations. The enormously elongated and partly curved spinous processes are a most characteristic feature of this fossil animal. The directions of the respective resultant compressive force acting on the vertebrae and the primarily loaded leg during a stride have been added.
Once a functional explanation has been found for a seemingly extreme, but actually perfectly adapted form, in general corresponding principles can likewise be applied to less conspicuous ones. As I will demonstrate later on, in many further cases the shape of the vertebral column reflects biomechanical requirements in a characteristic manner. In this case the problem is not, as otherwise the normal procedure of engineers, to create an appropriate design for a certain task under given loads, but to find out for a given skeleton or a certain part of it which forces and loads were probably active and have led to a given shape and which was its primary function. Adaptations to physical requirements, that is, to static and particularly to dynamic loads of the skeleton, can easily be recognized in the shoulder region of extant ungulate mammals (Fig.2).
This trait makes them well suitable for comparisons with extinct forms to find out conformities, but also important differences and the likely reasons. In modern quadrupedal herbivorous mammals the length of the neural spines in the shoulder area is apparently deter- mined by several factors:
- Size and mass of the head and the inclination of the neck during browsing on the ground. The inclination angle has an effect on the
muscular force required for raising the head or for holding it in a low position.
- Size and mass of the whole animal as well as the attainable maximum and continuous speeds, because these parameters affect
the magnitude of dynamic forces during running, galloping, and jumping.
- The condition of the ground on which an animal preferably moves, either on fairly soft or on hard soil. The hardness of the ground
respectively its elasticity has as well an effect on the magnitude of dynamic forces during running, galloping, and jumping
Fig. 2. Sketch of a Pleistocene elk skeleton as an example of an ungulate mammal demonstrating the orientation of the spinous processes towards the shoulder joint in this area. Length and direction of the spinous processes represent an adaptation to high motility enabling this animal of running and jumping on hard grounds.
These conditions can occur separately or in combination and thus can lead to quite different vertebral columns. For example, the length of the spinous processes in the shoulder region of elephants, which are unable to gallop or jump, is not determined by a high running speed but by the high weight of head and tusks. On the other hand, the remarkably long spinous processes in Bison antiquus antiquus, shown by Bailey (1997), and in further Pleistocene species can probably be traced back to big mass, high running speed as well as additionally to frozen grounds. This is likely to apply also to the elk skeleton shown in Fig. 2.
Bridge analogies discussed so far (Thompson 1942, Slijper 1946) do not offer a sufficiently exact simulation of the functional conditions of vertebral columns (Kummer 1959), in particular in the shoulder region. Such analogies can only be regarded as a rough approximation (Wainwright et al. 1976). Their main weakness consists in the fact that they did not consider but static conditions. However, the skeleton of a vertebrate is not designed to serve a function at rest, rather to withstand the much more important dynamic loads during locomotion.
Fig. 3. Skeleton of Bison antiquus as an example for demonstrating the effect of elongated spinous processes on the muscular tensile force required for the transmission of a given force to the ground. Short spinous processes would result in higher tensile forces (dashed line)
which are accompanied by larger forces of variable directions (Figs.1 and 2). Fig.3 presents a Bison skeleton as an example for schematically demonstrating the effect of a modified spinous process length on the magnitude of muscular forces. The predominating oblique direction of the neural spines takes primarily account of the largest forces and of their directions occurring on arrival on the ground during jumping and galloping. As can easily be recognized, the muscular tensile force T depends on the length of the spinous processes and consequently on the angle between muscles or tendons. It increases with shortening processes if a force of given magnitude has to be transmitted to the ground. The downwards acting compressive force is composed of gravitational vertical and inertial horizontal components. Inertial forces occur in connection with locomotion and can easily be felt if it is suddenly stopped by an obstacle.
Obviously, the increased length of the spinous processes in the shoulder area is advantageous for a reduction of muscular forces. Until recently, the functionally determined orientation of the spinous processes towards the shoulder joint in ungulate mammals had not been recognized. Consequently, a satisfactory explanation of this very characteristic feature of many big mammals was not available. On the other hand, it is very advantageous that any vertebral column reflects exactly its adaptation to mechanical loads and thus to the animal’s particular lifestyle. For example, a comparison of the vertebral columns of modern ungulates and climbing primates reveals aggravating differences. These can be interpreted as a result of a different locomotory behaviour.
Once having recognized the connection between main mechanical load and shape of the vertebral column in extant mammals, it becomes much easier to understand the differences present in fossil forms and to find out important indications of their presumable function in connection with lifestyle and milieu. The following skeletal features have been utilized in this paper as criteria for statements about gait and milieu of the regarded fossil reptiles:
- The length of the dorsal spinous processes in relation to the size of vertebrae.
- The relative length of the spinous processes compared to the adjacent ones. For example, ichthyosaurs possess relatively long
spinous processes, but the uniform length distribution due to a strong longitudinal musculature along the vertebral column
is a characteristic of aquatic forms.
- The length distribution of spinous processes in the region between pelvis and shoulder girdle.
- The length of the spinous processes of the cervical vertebrae compared to that of the dorsal vertebrae.
- Length and shape of the tail and its vertebrae.
There are some further traits pointing to the probable former lifestyle, apart from features of the vertebral column, which in addition can be useful.