7. Biomechanical function of the vertebral column in theropod dinosaurs
Theropods with short spinous processes inhabited preferably shallow water and were fish eaters
In most theropods, popularly regarded as terrifying land-dwelling carnivorous beasts, the spinous processes are rather short. This fact leads to the question why or whether the process length in these forms was sufficient to transmit the body weight to the ground and to make a bipedal locomotion possible, in connection with a predatory lifestyle on land . Traditionally, early Triassic dinosaurs are commonly interpreted as bipeds, at least during fast running (Sander 1994). These ideas can already be found in early considerations about the dinosaurian lifestyle, e.g. v. Huene (1907/08) or Abel (1912). Recent ground birds and kangaroos were regarded as possible analogues in those days. These ideas have strongly influenced reconstructions of theropods as to posture and gait up to the present day. A bipedal gait on land appeared obvious, as well as the head being carried as in an ostrich. Apart from these old ideas, speculations concerning posture, gait, and cursorial speeds seem to be based largely on the very different length of fore and hind limbs as well as on morphological comparisons with modern vertebrates, in part also on trackways. Nevertheless, the reasons for this supposition remain somewhat unclear. Various fanciful attempts to reconstruct lifestyle and habitat of dinosaurs in semipopular publications cannot obscure the fact that these reptiles are still poorly understood and that the knowledge about them is very restricted.
Comparison between the vertebral columns of a land-dwelling ornithischian (Ouranosaurus) and a large theropod (Tyrannosaurus). The differences are obvious.
Until recently, the shape of the vertebral column did not play a role in considerations concerning the lifestyle. Here I suggest a different idea of theropod dinosaurs. The conception of bipedality in terrestrial theropods does not appear well founded. Yet, the shape of the vertebral columns with short neural spines becomes easily understandable if we assume that theropod dinosaurs normally lived in moderately shallow water, though not necessarily as swimmers, but as waders hunting fish. Off course, for rest they had to leave the water, as seals do, and for egg deposition, maybe also for incubation. In some respect, the lifestyle and habitat of theropods is comparable with crocodiles, in other respects with seals, but they did not exclusively live on the dry land, preferably on small islands in a rather flat environment.
Indeed, it is conceivable that the vertebral column of carnivorous theropods reflects an adaptation to such a lifestyle. By this assumption the reasons of the very different length of fore and hind limbs become clearer. The probability that these animals utilized a bipedal locomotion continuously on land appears rather low because of the unspecialized vertebrae, and such a behaviour would not be typical. Although certain modern four-legged reptiles are capable of a two-legged locomotion (Christian et al. 1994) they cannot use this gait continuously and for long distances. The longer hindlimbs are an ancient feature, inherited from the eosuchians (R. Wild, communication by letter, 1995). On the other hand, the strong hindlimbs certainly suggest a bipedal locomotion. Yet, conspicuous differences between the vertebral columns of theropods and of Ctenosauriscus point to the idea that theropods were not adapted to the dry land. Moreover, the differences between the spinal columns of ungulate mammals and dinosaurs hint at different locomotory capabilities. Apparently, so far useful criteria to judge the suitability of dinosaur skeletons for bipedal gait, fast locomotion, or a preferred milieu were not available.
Compsognathus from the Upper Jurassic, the smallest known theropod that lived in the Solnhofen area in a lagoon and was a contemporary of Archaeopteryx. The tail is long, but not stiffened as in A. The spinous processes are very short.
The figure below presents a skeleton of Tyrannosaurus rex as another example of a theropod dinosaur with short spinous processes. Such forms exhibit strong differences also among each other, depending in particular on the overall size. Certainly, these differences cannot be traced back to different design principles. It is very curious and remarkable that in theropods an increasing size is accompanied by an increasing reduction of the forelimbs which do not appear any more suited for locomotion or a grasping function. Apparently, the forelimbs of such forms had lost their former function, maybe in analogy to the wings of ratite birds. But surely this atrophy cannot be regarded as an adaptation to bipedality on land, as suggested between the lines by Coombs (1978).
Skeleton of Tyrannosaurus rex as an example of a large theropod, redrawn from Carroll (1993). The short spinous processes in the region between pelvis and shoulder girdle indicate that the stress of the vertebral column was relatively low, and therefore the animal does not appear to have been adapted to a terrestrial environment and probably lived as a wading hunter of large fishes in moderately shallow water. Note the extremely long tail, which curiously is regarded by palaeontologists as a counter-weight.
Because of the short spinous processes in connection with a lightweight design of the dorsal vertebrae (Norman 1991, Brooks et al. 1998) we can assume that the vertical stress of the vertebral column due to static and dynamic loads was comparatively low. For land-dwelling carnivorous dinosaurs such a shape of the spinal column obviously does not correspond to its supposed carrying function. Whereas the spinous processes of land-dwelling ungulate mammals are remarkably elongated in the shoulder region, in particular in Pleistocene species adapted to frozen grounds, on the contrary the short processes of theropods suggest an adaptation to very soft grounds at least to say or to a lifestyle in moderately shallow water. The rudimental forelimbs are particularly difficult to understand, because it is hardly conceivable why a land-dwelling predator should completely abandon the use of its arms. Obviously, they had no function in connection with quadrupedal gait. Certainly, the development of relatively weak vertebral columns and short spinous processes as well as the adherence to the saurischian pelvis has adaptive reasons, insofar as there was no urgent need for a strong modification of the skeleton as in ornithischian dinosaurs, which extended their habits to the dry land. But all of these features can be harmonized with a kind of amphibious lifestyle. It is well known from our own experience that moving the legs under water, either wading or paddling, is much more strenuous than on land. Therefore, the caudo-femuralis muscle had to remain an important limb retractor in these dinosaurs, and there was a strong necessity to adhere to the saurischian pelvis. Sharp claws and frequently a long flexible tail appear as additional characteristic features of such a lifestyle. Claws could be helpful for ensuring the position in streaming shallow water or for locomotion. On land long claws would tend to be hampering, and they have actually been modified by ornithischians. A long tail could be useful for slow swimming using an undulating locomotion as Recent crocodiles do.
The obvious differences between dinosaurs with short and long neural spines are very likely caused by different lifestyles. Modern reconstructions of the dinosaurian mode of life do not take account of these differences, although the occurrence of tracks generated by different forms (Lockley 1993) points to different preferences as to the environment. Early ornithischians such as Fabrosaurus resemble saurischians by the presence of short spinous processes, but the new trait of ossified tendons hints at a change in loads on the spinal column and hence in lifestyle. Despite the different length of fore and hind limbs this form does not show indications of bipedality on land. Maybe, the skeletal shape reflects the transition to the dry land being in progress. From a biomechanical viewpoint land-dweller in this context can only mean independency of the weight-reducing effect of the hydrostatic buoyancy which represents the only main difference, but a very far-reaching one, regarding the load on the vertebral column between vertebrates living on land or in the water.
Widespread flattened continental landscapes with islands, shallow lagoons, delta basins, lakes, sluggish rivers bordered by gallery forests on the one hand and desert-like dry land with only few huntable animals on the other (Erben 1975: 274) could have been a main reason for theropods to stay predominantly in the water where fish for instance was an abundant as well as attractive food source. A corresponding specialization is particularly well recognizable in Baryonyx with its crocodile-shaped skull (Charig & Milner 1986). For this purpose the presence of arms was not required. Many modern wading birds catch fish using their beaks only. Since a swimming locomotion is hardly feasible in shallow swampy regions with dense vegetation and is expensive in streaming water, bipedal locomotion using ground contact by the hindlimbs was a useful alternative, with the body being more or less submerged and supported by its buoyancy. Certainly, theropods were bipeds and well adapted to the existing climatic and environmental conditions, but their skeletal shape makes likely that they utilized this gait predominantly in moderately shallow water
Ornitholestes, another representative of theropods, about 2m long, that shows a long tail and short spinous processes as well as Compsognathus and Tyrannosaurus
There are some indications which can serve as evidence that theropods actually were water-dwellers. In a way, their lifestyle may have resembled crocodiles, in another way that of seals. Coombs (1980) as well as Mossman & Sergeant (1983) depict a track generated only by the hindlimb claws of a theropod floating or walking in moderately shallow water. This track indicates that theropods used a bipedal gait in the water. Furthermore, several theropods such as Compsognatus have even been found in marine sediments. Up to now, this fact has not sufficiently been appreciated. Generally, such remainders are believed to have been washed in from a coast and thus to represent untypical conditions. However, the good preservation of the Bavarian specimen of Compsognathus makes unlikely that it has been washed in. Presumably, this animal as well as Archaeopteryx and pterosaurs lived on a nearby island, the presence of which is indicated by terrestrial plant remainders in the Solnhofen Lithographic Limestones (Viohl 1985).
A large theropod swimming in moderately shallow water. It has produced a track by the claws of the hindlimbs only, after Mossman & Sergeant (1983).
The comparatively incomplete ossification of the leg joints in all saurischian dinosaurs (Coombs 1978) which did not allow but modest accelerations and a relatively short stride length (Carroll 1993) can be mentioned as an additional support of a lacking adaptation to hard grounds on land. Presumably, there was no stimulus for these animals to leave the water. The questionable advantages of a life on the dry land could not yet compensate for the disadvantages, for example the steady danger of dehydration and lack of food.
It is conceivable that only a slow regression of the water level created a stimulus or a necessity for Cretaceous theropods such as Acrocanthosaurus or Spinosaurus to adapt to very shallow water or to terrestrial conditions. The short spinous processes in most theropods indicate that they moved so slowly on land, if at all, that the dynamic forces remained low. However, if they were not capable of a continuous bipedal locomotion on land, then forms with hind and fore limbs of very different length cannot have been suited either for a fast quadrupedal locomotion. Not a single dinosaurian vertebral column presents indications that these animals might have been capable of jumping and galloping, contrary to claims in the literature, e.g. by Bakker (1971) or Alexander (1985). In that case a characteristic elongation and orientation of the spinous processes towards the shoulder joint of quadrupedal forms such as ceratopsids should have been present as in quadrupedal mammals capable of galloping, because fast locomotion and the arrival on the ground following a jump is connected with increased dynamic forces which may considerably exceed the static ones. Possibly, carnosaurs such as Tyrannosaurus just as crocodiles utilized a lifestyle of lurking for prey in moderately shallow water. On the other hand, small theropods, the coelurosaurs, must be regarded as active predators as stated earlier, e.g. by Ostrom (1990: 279). However, their hunting activity should have been restricted to a shallow water environment.
Disadvantages of dinosaurs compared to the later following whales
All dinosaurs, in particular the large ones, were hampered by an important handicap, which possibly was a main reason for their extinction, presumably even a more probable one than speculative catastrophic scenarios They had to deposit their eggs on land, not far away from the water. This condition was connected with the permanent risk that the eggs could get lost by predators. Moreover, in case of profound environmental.changes the offspring was much more endangered than adult individuals because of imperfect or completely missing brood care. On the other hand, to be able to deposit their eggs on land saurischians had to retain the ability to walk on land. Therefore, they could not afford to abandon the strong hindlegs and to specialize in swimming. Thus, their preferred milieu remained restricted to the proximity of the land. The large spectacular forms such as Tyrannosaurus represent final members of a line which because of their size increase ended in a deadlock of the evolution, unable to react to a major change of environmental conditions and thereby condemned to extinction.
Whales were in a comparatively favourable situation. As viviparous animals, obviously, they succeeded soon to bring forth their offspring safely also in the water and to become completely independent of the nearness of land. Thus, they could become perfect swimmers and settle all seas.
A saving escape for small theropods
Small theropods found the escape from the limiting conditions of large forms by changing the method of hunting fish. Instead of wading in the water they began hunting by swimming under water, using the arms for the generation of propulsion. It was a decisive improvement of the maniraptors to extend the action radius of their environment. Several small forms such as descendants of Rhamphorhynchus or Archaeopteryx even succeeded in learning to fly in the air. Thereby, they were able to escape from all problems, and later the various evolving birds could settle all milieus with large populations due to better broodcare.
In my eyes, the small theropods are the most interesting dinosaurs, because they gave rise to the birds. As long as no older representative is known Archaeopteryx remains a very important form although this theropod used to be regarded as somewhat marginal or even a side line of the evolution. But this animal was the first known feathered theropod specialized in hunting fishes such as Leptolepides sprattiformis by swimming under water.
Arms and hands generated propulsion, the the stiffened tail was used for control. Since Archaeopteryx was small she, the old feather, had a favourable relation of power available to mass which made the achievement of a considerable speed possible. Finally, the transition from water to flying in the air became feasible. However, Archaeopteryx was not the first dinosaur to hunt fish in this manner, and certainly not the last one. The first were the pterosaurs with forms such as Rhamphorhynchus from.the Upper Triassic. Similarities as to the skeleton can also be found in Deinonychus from the Upper Cretaceous. This theropod also exhibits a remarkably stiffened tail and elongated arms. As J. Ostrom stated, the formation of the hand is very similar to Archaeopteryx. These conformites can be found in further theropods from the Upper Cretaceous, in maniraptors such as Velociraptor, Sinornithoides and Coelurus. Presumably, these forms presented an upper limit for theropods, hunting by underwater swimming. Larger forms were restricted to catching fish wading on the ground.
Deinonychus as a particularly instructive example of semiaquatic theropods is shown below in its typical posture (Ostrom 1969). In the water the submerged body would assume almost automatically a near-horizontal attitude. This lifestyle did not confront the animal with the problems of balance control during bipedal locomotion in the same severity as a land-dweller. For this reason an alignment of the spinous processes to the knee joint as in Ctenosauriscus was not necessary. The tail of Deinonychus is very remarkable because it shows an apparently adaptively acquired restricted flexibility. This feature is present as well in Archaeopteryx and in rhamphorhynchoids. In Deinonychus it may have served an analogous function, namely steering during swimming (Ebel 1996) in connection with a modified propulsion generated by the forelimbs.
Deinonychus, a moderately large theropod with a length of about 3m and long arms from the Upper Cretaceous and Archaeopteryx from the Upper Jurassic. These theropods display skeletal similarities which may be traced back to a similar lifestyle, that is hunting fish in the water. As in Archaeopteryx in Deinonychus also the tail is stiffened
Exceptions such as Acrocanthosaurus from the Upper Cretaceous with elongated spinous processes show a certain adaptation to life on the dry land or in very flat water
Acrocanthosaurus from the late Cretaceous as a rare example of a theropod with elongated spinous processes pointing to a lifestyle in very shallow water or even on land. By the way, it is doubtful whether the reconstruction of the missing bones is correct.
In carnivorous theropods ranging from Compsognathus to Tyrannosaurus a lengthening of the spinous processes in the trunk area between pelvis and shoulder can only rarely be observed. For example it occurs in Acrocanthosaurus. There must be a special reason for the short processes in most theropods. If such forms had really been true terrestrial bipeds, then the spinal column should show at least distant similarities, for example remarkably elongated spinous processes in the pelvis region, with Ctenosauriscus which is unique in this respect.
The large ground bird Diatryma from the Early Tertiary of the northern hemisphere shows a good adaptation to bipedal locomotion on the dry ground by elongated spinous processes above the hind limbs as well as rudimentary arms. Apparently, the direction of the spinous processes corresponds to the area where the respective foot is in contact with the ground.