4. Biomechanical function of the vertebral column in ornithischian dinosaurs
Generally, spinous processes serve a kind of bridge function comparable to an oblique-rope bridge. Dorsal musculature and tendons are suspended on the spinous processes, thus making possible considerable vertical components of tensile forces. These allow the transmission of the occurring weight and inertial forces to the ground (Fig. 2 and 3, previous site). Remarkably elongated spinous processes in the shoulder region represent a response to vertically acting loads in connection with a terrestrial lifestyle.
Strong hints at a terrestrial lifestyle can be found also in many dinosaurs, indicated by elongated spinous processes. The variable shape of the vertebral column of dinosaurs suggests, however, that a terrestrial mode of life cannot be taken for granted in all of such forms, as it is usually done. In addition to the criteria mentioned above concerning the functional adaptations in mammals, in extinct ancient vertebrates the eventuality must be examined whether these were definitely land-dwellers or were possibly restricted to an amphibious lifestyle. The investigation of the likely function of the elongated and uniquely arranged spinous processes in Ctenosauriscus gave rise to the idea that they evolved as an adaptation to requirements of a facultative bipedal gait on firm soil. They can be regarded as a response to relatively large forces and appear as characteristic of a terrestrial cursorial lifestyle. So far, there were no serious doubts about the terrestrial lifestyle of most, if not all dinosaurs, e.g. Norman (1991). Of course, this statement was correct if a distinction from mere aquatic forms such as ichthyosaurs was intended. But an unequivocal proof that all terrestrial dinosaurs inhabited the dry land has never been furnished. The very different shapes of the spinous processes in many dinosaurs point to fundamental differences as to the mechanical loads and thus to the preferred milieu. However, certain regularities are clearly discernible.
Ornithischians and further forms with elongated spinous processes were land-dwellers
A kind of backsail is present also in certain dinosaurs. This feature is caused by elongated spinous processes. These represent a remarkable trait of most ornithischian dinosaurs and are well recognizable in forms such as Iguanodon, Ouranosaurus or the hadrosaur Parasaurolophus. As in Ctenosauriscus this trait suggests an adaptation to hard grounds. In ornithischians as well as in extant ungulate mammals elongated spinous processes appear as an important prerequisite for carrying portions of the body weight and for the transmission of comparatively large forces to the ground. Bailey (1997) has discussed at some length a corresponding suitability in Ouranosaurus. The spinous processes serve the suspension of ligaments and strong muscles respectively a lattice of ossified tendons (Norman & Weishampel 1990). These can be interpreted as a response to continuously acting forces with considerable vertical components. The angle between muscle fibres respectively tendons increases with a growing length of the spinous processes which, within certain limits, makes the tensile forces of tendons decrease. The arrangement of ossified tendons is in good agreement with the suspension of muscles as outlined in Fig.3. Elongated spinous processes are plainly to be expected in land-dwelling dinosaurs, because they cannot make a profit from the weight-reducing effect of the hydrostatic buoyancy in water, in contrast to amphibious forms.
Fig. 4. The iguanodontid Ouranosaurus, redrawn from Carroll (1993). The directions of the tips of the more or less parallel dorsal spinous processes do not pass through a common intersection. This animal is quite untypically depicted as a biped in this sketch. The long spinous processes between pelvis and shoulder girdle characterize this dinosaur as terrestrial. The parallel orientation of elongated spinous processes indicates a quadrupedal gait. The modified claws present additional evidence of this supposition. For purposes of a functional comparison a modern oblique-rope bridge in southern France
Moreover, the arrangement of the spinous processes along the vertebral column between pelvis and shoulder region indicates whether a dinosaur generally moved bipedally or quadrupedally. An extreme specialization as in Ctenosauriscus cannot be found in any dinosaur. Fig.4 shows a sketch of Ouranosaurus from the Lower Cretaceous as an impressive example of an ornithischian dinosaur. Despite the long hindlimbs in such forms a comparison with the arrangement of the vertebrae in Ctenosauriscus makes clear that the elongated spinous processes in ornithischian forms and their orientation do not point to an obligatory bipedal locomotion, rather they hint unequivocally at a quadrupedal gait on land. Moreover, we can assume that the extremely long spinous processes do not represent an overspecialization, but served a function requiring just this length. The more or less parallel processes with approximately equal length extend over the entire trunk to the shoulder girdle. This fact indicates that normally the forelimbs also had to transmit forces to the ground. A primarily bipedal locomotion on land should have resulted in a strong elongation as well as in a similar arrangement of the spinous processes above the hindlimbs as in Ctenosauriscus and in a decreasing length towards the forelimbs.
Maybe, the sketch of Ouranosaurus in Fig. 4 creates the impression as if an orientation of the spinous processes towards a common intersection would be feasible or could be attained by small modifications of the reconstruction, thus suggesting bipedal locomotion. This is, however, not the case. The dorsal vertebrae are not curved as those of Ctenosauriscus. Although fore and hind limbs in this form are equipped with a kind of hooves or flattened claws, instead of sharp ones, this form as well as others with considerably longer hindlimbs than forelimbs is regarded by some authors as a biped, e.g. Carroll (1993). Norman & Weishampel (1990: 531) point to a likely original bipedal gait in iguanodontids, but they consider Iguanodon as well as Ouranosaurus as quadrupeds. The upright leg position in connection with elongated hindlimbs does not automatically mean bipedality, it is a prerequisite only (Charig 1972). The vertebral columns do not yield any indications that ornithischian dinosaurs might have been bipeds. Maybe they were able to move a short distance on their hindlimbs just as well as trained horses or even elephants can do. But nobody would call the latter bipeds for that reason. The feature of elongated spinous processes is not yet as pronounced in early ornithischians such as Fabrosaurus as in later forms and may characterize the transition to the dry land.
A correspondence of the vertebral processes of land-dwelling ornithischian dinosaurs to the jib crane analogy is not as obvious as in ungulate mammals. Apparently, the length is additionally determined by a stiffening effect, although a certain flexibility should have been retained. The stiffening function in these forms is indicated by a lattice-work of ossified tendons which suggests a modification and, compared to earlier vertebrates such as Ctenosauriscus, an evolutionary improvement of the dorsal musculature required for continuous quadrupedal locomotion on land. Furthermore, the design of the vertebral column makes likely that ornithischians had abandoned the sinuous reptile gait, but the stiffness of the backbone presumably did not allow a high running speed. The frequently very different length of fore and hind limbs appears to be inherited from saurischian ancestors and may have been acceptable or even advantageous for browsing on the ground. However, these length differences cannot be regarded as a true advantage for the locomotion of land-dwellers and are indicative of a comparatively low cursorial speed, a supposition which is supported by the length distribution of the neural spines along the trunk that differs considerably from that in ungulate mammals. But apparently low speeds did not involve serious problems for these animals. Presumably, there were no fast predators, as pointed out later on.
The elongated spinous processes, ossified tendons, and the modified claws in ornithischians can be regarded as a feature of a more or less pronounced motility on land. Bailey (1997) opines that Ouranosaurus was a fairly agile animal which lived under dry or sometimes even arid conditions. The remarkably long spinous processes and a relatively short tail are in accord with this statement. Furthermore, the pelycosaur Dimetrodon from the Permian, the Triassic reptile Ctenosauriscus as well as the poorly known Cretaceous theropod Spinosaurus seem to have existed under comparable environmental conditions, to judge from the reddish sediments in which they were embedded. The coincidence of terrestrial sediments and enclosed vertebrates with elongated spinous processes does not appear as a matter of chance. However, despite their adaptation to the dry land none of these forms exhibits indications in the shoulder region that it might have been capable of fast running, galloping, or jumping. The orientation of the spinous processes in the shoulder region of modern ungulates towards the shoulder joint represents an innovation and amplification of former functions of the vertebral column required for increased motility. Alexander (1985) as well as Paul (1991) supposed a galloping ability in Triceratops. But this ability must not be derived from a similar total mass and limb bone strength as in modern mammals. The spinous process length does not support such an idea. On the other hand, in forms such as Tenontosaurus (Ostrom 1970) with relatively short spinous processes and a long and high tail an adaptation to the dry land is not particularly evident. Possibly, a swimming locomotion was still or again part of the normal behaviour in such forms.
The most conspicuous difference between saurischian and ornithischian dinosaurs consists in the arrangement of the pelvis. Abel (1912) regarded the modification of the pelvic bones in ornithischian dinosaurs as an adaptation in connection with the stiffening of the tail which these forms carried above the ground. However, it is more likely that this modification happened in connection with the settlement of the dry land respectively with an increasing independency of the water, and not as a consequence of a developing bipedality as in land-dwelling bipedal birds. Obviously, bipedal theropod dinosaurs which so far are believed to share the milieu with ornithischians retained the saurischian pelvis, and most representatives did not modify length and flexibility of the tail. Insofar Abel’s interpretation was inconclusive and contradictory. The same applies to Abel’s explanation of the differences between the pelvis of ornithipods such as Iguanodon and heavy ornithischians such as Stegosaurus, which he interpreted as caused by a change from bipedal to quadrupedal gait. It appears, however, that this modification in heavy forms is caused only by the enormous weight increase. The modification is not fundamental but gradual.
Different development of the pelvis in dinosaurs
left. saurischian pelvis (Diplodocus),
right. ornithischian pelvis (Stegosaurus),
Armours appear as an additional characteristic of certain land-dwelling dinosaurs, the Thyreophora, which actually may have served a function of heat protection. Buffrénil et al. (1986) discuss several possible functions of the plates in Stegosaurus. The consideration of biomechanical criteria does not reveal a particular function of these structures. Yet, the exact orientation of the plates is still a matter of debate. These authors prefer a function connected with heat exchange and point to the fact that the lithofacies of the Morrison Formation, which has yielded many remainders of Stegosaurus, indicates that these forms preferred relatively dry and open habitats, in contrast to other contemporary dinosaurs. Taking into account further armoured dinosaurs such as the related ankylosaurs one might think of a protective function against dehydration and perhaps increasing direct sun radiation, which became necessary after the transition to a terrestrial lifestyle in a more open habitat. Experiments by Regal (1985) utilizing lizards have demonstrated that enlarged scales can help to reduce the rate of heat uptake. Armours tend to protect mainly the upper parts of the body. By the way, it is noteworthy that only very few footprints attributable to armoured dinosaurs are known (Lockley 1993). Moreover, it is remarkable that during the Triassic age strong armours evolved respectively were enhanced also in several further groups such as the Proganochelydia (tortoises) and the Aëtosauria, which may have occupied corresponding habitats, whereas representatives of most other dinosaur groups did not develop heavy armours. Presumably, as a consequence of their particular lifestyle or preferred milieu the latter did not need it. It appears rather unlikely that such armours evolved without an adaptation to a special requirement, but likewise improbable as a defence against predators, since the ultimately imperfect protection had to be payed with a substantial increase in weight and reduction of motility. Coombs (1978) emphasized the low cursorial adaptation in Stegosaurus.
5. Biomechanical function of the dorsal sails in Dimetrodon and Edaphosaurus
Remarkably elongated spinous processes have their first appearance in certain pelycosaurs such as Edaphosaurus and Dimetrodon from the Upper Carboniferous and Lower Permian, whereas the vertebral columns in other representatives of the Pelycosauria remain inconspicuous. Although the shape of such sails is generally similar to Ctenosauriscus and even more spectacular, in detail arrangement, orientation, and cross-section of the spinous processes are very different.
Probably, the process elongation in these pelycosaurs can likewise be explained as an adaptation to increased vertically acting forces and thus to a terrestrial lifestyle. Unequivocal indications of other functions are not present. A heat regulatory function has been proposed as the most likely one among several others. However, the generally rare occurrence of backsails makes such a function unlikely. If backsails had offered important advantages they should have occurred as a wide-spread trait. A heat regulatory function would not appear particularly advantageous in relatively large animals such as these pelycosaurs as well as in Ctenosauriscus in comparison to considerably smaller ones. Because of relatively big mass they are generally believed to be capable of easily preserving their body temperature and would need rather long time for a change in temperature. Elongated spinous processes cannot be found in contemporary small forms. Bailey (1997) mentions an investigation by Haack (1986) that does not conclusively confirm an advantage of the backsail in a heat transfer function. No physical principle is known that might stimulate a skeletal modification for that purpose. The advantage of a sail would be extremely small at the start of an evolutionary modification. To be effective such a modification should be accompanied by a further function with an immediate benefit. But there is no modern reptile or mammal in which the skeleton or parts of it are determined by primary requirements of thermoregulation. Furthermore would it hardly be possible to prove such a function by evidence from the fossil material (Pfretzschner 1999). It should be kept in mind that the thermoregulatory function is based on mere speculation.
Mechanical considerations strongly suggest that it is not the backsail itself which serves a function but its bony structure. The extremely elongated spinous processes in Dimetrodon and Edaphosaurus, which are even more reminiscent of a dorsal sail than those of Ctenosauriscus, suggest that they also have served a function in connection with locomotion on land, because the elongation of the spinous processes in these forms is restricted to the trunk area between hind and fore limbs. Yet, as a whole the design does not well correspond to a bridge analogy. Contrary to Ctenosauriscus the extremely long spinous processes do not possess the curved shape and rectangular cross-section required for bipedal locomotion, but they are straight and rounded. As well as in Ouranosaurus an orientation of the tips towards a distinct intersection point is not present. These differences are probably caused by a different mechanical stress of the backbone compared to Ctenosauriscus, though not a fundamentally different one. The design appears somewhat old-fashioned in comparison to later forms, and its biomechanical function is not so obvious at first view. But certainly the vertebral column did perfectly serve its function.
Fig. 5. A technical disk with its components linked by hinges as an analogue to the dorsal sails in Dimetrodon and Edaphosaurus. Sketch of Dimetrodon, redrawn from Sander (1994). The long spinous processes in Dimetrodon and in Edaphosaurus as well mark these reptiles as terrestrial forms.
Although an exclusively mechanical reason can be supposed for the long spinous processes in Dimetrodon and Edaphosaurus, the load distribution on the vertebral column differs considerably from that of modern ungulate mammals because it is apparently uniformly allocated to fore and hind limbs. Moreover, the length of the delicate and very slender spinous processes is presumably not primarily determined by the suspension of muscles, since according to Fig.3 an extremely large angle between the muscle fibres would not be necessary. A bridge analogy would evenappear problematical, because the sinuous quadrupedal gait of these reptiles requires a pronounced lateral flexibility. Therefore, a somewhat different mechanism is employed. In this case the configuration can best be compared with a technical disk, with its parts connected by vertical hinges, as outlined in Fig.5, together with a sketch of Dimetrodon. The primary mechanical function of a disk is a stiffening effect. Obviously, the backsail of long-spined pelycosaurs also served a stiffening function to prevent a deflection of vertebral column and trunk. This effect of the sail with its long spinous processes is underlined by the fact that these skeletal parts are often preserved in an articulated condition (Carroll 1993). They were apparently covered by voluminous soft parts. In order to make possible an appropriate distance from the ground during quadrupedal locomotion in very shallow water or on dry soil a strong deflection of the vertebral column had to be avoided. On land this problem was intensified by the missing weight-reducing effect of the hydrostatic buoyancy. Because of relatively short limbs in Dimetrodon, which had not yet attained an upright posture, the distance between trunk and ground was very small, and there was a steady hazard of ground contact. Dimetrodon shared a common problem with all land-dwelling vertebrates, namely to achieve sufficient stiffness of the vertebral column on the one hand and to retain sufficient flexibility on the other. Sufficient distance from the ground was established by the stiffening effect of elongated spinous processes. Presumably, this effect was exclusively attained by mechanically stiffening the dorsal shape, but not by an enhancement of the dorsal musculature. Despite the modification of strongly elongated spinous processes, the lateral flexibility as an important prerequisite for the sinuous quadrupedal reptile gait was completely retained. Probably, the special gait was the main reason for this unique vertebral column, which has never again been realized in later forms, as well as for the roundish cross-section of the spinous processes. The delicate spinous processes can serve as indicators of comparatively low dynamic forces. Therefore, it is probable that these pelycosaurs moved very leisurely on land. Presumably, Ctenosauriscus and ornithischians moved somewhat faster. However, a comparison with extant ungulate mammals is certainly inappropriate.
Objections might be raised that long spinous processes are not present in the modern monitor Varanus komodoensis, although it is of corresponding size and lives on land (Auffenberg 1981). It is conceivable that the dorsal musculature of pelycosaurs was not yet suitable to prevent otherwise a strong deflection of the vertebral column continuously. Yet, an extrapolation from modern to extinct forms as to certain properties appears fruitless and even not allowable. Apparently, there were several possible strategies to reinforce the backbone. A completely different mechanism with similar effects was realized by the ossified tendons in ornithischians. On the other hand, all modern monitors are accomplished swimmers (Steel 1996), thereby indicating that they are not completely adapted to a terrestrial lifestyle and possibly retain the option to return to a semiaquatic environment in case it should become necessary or offer advantages.
The effect of stiffening the vertebral column by elongation of spinous processes occurs in Ctenosauriscus, in ornithischian dinosaurs, as well as in the pelycosaurs in question. It is the common feature of these otherwise very different forms. However, in detail mechanical stress and materialized design are very different, as mentioned above. Obviously, this feature evolved independently several times in different forms and epochs, just as required, but in complete accordance with the respective mechanical requirements. On the other hand, long spinous processes are restricted to a few specialized species and can serve as an indication that early vertebrates were unable to settle the dry land without special problems, even after the evolution of a bony skeleton with hind and fore limbs, rather considerable additional efforts as well as favourable environmental conditions were necessary. The disappearance of these conspicuous pelycosaurs in the course of the Permian points to the fact that a continuous settlement of the dry land was not yet attractive.
Since a strong modification of the vertebral column by process elongation seems to have happened for the first time in these pelycosaurs, they may have been the first large vertebrates at all which adapted to a primarily terrestrial lifestyle. None of the vertebrates from the Devonian, Upper Carboniferous, or Permian apart from these pelycosaurs, not even the large pareiasaurs, exhibits features of the vertebral column which might unequivocally be interpreted as truely terrestrial. All of these forms exhibit relatively short spinous processes, with a particularly uniform length distribution along the trunk, pointing to a life mainly in the water, though not necessarily as swimmers. A small length of the spinous processes can be used as an independent argument confirming conclusions by Clack (1997) that tetrapod tracks do not necessarily demonstrate that the trackmakers lived on the dry land. Early tetrapods cannot automatically be regarded as terrestrial (Coates & Clack 1990). A foot-like structure could be useful as well for manoeuvring on the ground in very shallow streaming or agitated water. It is possible that such forms could leave the water for a short time but the increased loads on the vertebral column outside the water did not find a reflection in the spinous process length and, therefore, appear to have been unimportant. Probably, the completed transition from fresh water to the dry land cannot be defined solely by the presence of legs and feet (Clack 1997), and the skeletal differences between early land-dwellers and amphibians may be very small. Nevertheless, the vertebral column should yield some indications. Curiously enough, up to now it has never been used as a criterion to distinguish between swimmers and land-dwellers. Unfortunately, there are still many uncertainties about the origin of land-dwelling tetrapods (Clack 1997). Although it may be opposed to our feelings as land-dwellers, nevertheless it appears more probable that the limbs of the ancestral vertebrates did not evolve in connection with the settlement of the dry land. Apart from attractive food sources in shallow water, presumably an important adaptive goal was the development and perfection of lung respiration, which required a supporting skeleton and powerful forelimbs for raising the head above the water surface. Strong forelimbs are now supposed in Ichthyostega (Clack 1997), the tail of which indicates a capability of swimming locomotion. Moreover, respiration by the gills is considered still important in such forms (Coates & Clack 1991). The improved respiration could lead to a considerably increased activity level when the oxygen content of the air had attained a sufficient extent and was then an enormous advantage, even for descendants which later returned to an aquatic lifestyle. Whereas today the air contains approximately 21 % oxygen per volume, in water it is normally about 0,7 %. The lung respiration was a most important precondition for the settlement of the dry land after it had become attractive (Hölder 1989).