Webb’s morphofunctional classification of osteichthyans
However, these various reconstructions have at least two important drawbacks : they are not based on a comparison with living animals and/or do not take into account the possible existence of different ecological specialisations within the same general locomotory adaptations.
Webb (1984) proposed a classification of the swimming modes of living osteichthyans, also extended to chondrichthyans, which correlates shape with function. It comprises three categories :
- The first one includes median paired fin propulsion or manoeuvrability swimmers.
- The second category comprises caudal fin propulsion or sustained swimmers. Animals in this category typically display stiff, hydrodynamic bodies. Their caudal peduncle is narrow with a seleniform caudal fin. Sustained swimmers are open sea, epipelagic organisms.
- The last one is represented by caudal fin transient propulsion or accelerator swimmers. The skull is flattened dorso-ventrally.
The centre of gravity is displaced backward. Fin area is maximal in order to increase the area of support on water during acceleration. The body is flexible. This kind of swimming is practised by stalking hunters.
Webb’s classification enables comparison between the shape of primary swimmers shape (i.e. fishes) and secondary swimmers (i.e. marine tetrapods), both groups sharing the same biotope due to their “hydrodynamic convergence”.
Webb’s classification and the paleoecological reconstruction of metriorhynchids (Crocodylia, Mesosuchia)
Some of the metriorhynchid morphological characters seem to belong to accelerator swimmers or marine stalking hunters, kinds of predators well exemplified by living freshwater crocodilians. From the skull to the tail, the following characters could be relevant to this category. The skull is dorsoventrally flattened allowing quick lateral attacks. The external nares are not raised as in most living and fossil sustained swimmers (Langston, 1973). An important osseous porosity affects the skull probably contributing to the backward displacement of the centre of gravity, the increase of cranial buoyancy and the reduction of cranial inertia during quick lateral bites. One possible advantage of cranial porosity could have been to make easier the emergence of the external nares during long immobile stays just beneath water surface (see below). On the postcranial skeleton, accelerator swimmer characters in the metriorhynchids are the following : loss of osteoscutes resulting in a reduction of skin mass reduction and to an increase in the trunk flexibility. The shape of the tail is remininiscent of the carchariniform type, and not of the lamniform one. As shown by Thomson (1976) and Thomson & Simanek (1977), these sharks display a large range of swimming modes. The various characters quoted above would be consistent with the interpretation of metriorhynchid locomotion as closer to the accelerator swimmers or marine stalking hunters (for more details see Hua, 1994) than to any other other mode of aquatic propulsion.
Conversely, some other morphological characters could indicate an adaptation for sustained swimming : especially the hydrofoil shape of the fore limbs which look similar to those of other sustained swimmers like sharks or cetaceans.
In fact, the Metriorhynchidae may be regarded as epipelagic accelerator swimmers but the search for scattered preys made some sustained swimmer adaptations necessary, making them generalist swimmers. The animal may have floated gently near the surface thanks to its great skull porosity, lying in wait for its preys which were caught by sudden acceleration. Hua (1994) proposed this on a morphological basis, but without any other clue until now.
Histological data as a clue for the interpretation of the paleoecology of marine tetrapods
Two histological tendencies, reflecting two distinct ways of life, are shown by the skeleton of secondary swimmers.
Coastal forms poorly adapted adapted at a morphological or physiogical level to sustained swimming in the open sea display a general or local increase in skeletal mass. This process is due to osteosclerosis (inner bone compaction), pachyostosis (hyperplasy of compact cortices) or a combination of them (de Ricqlès, 1989). The increase in the skeletal mass consequently increases body inertia and the energetic of swimming. According to Taylor (1994), this process is found among slow swimmers grazing or hunting fixed or non elusive prey near the sea floor. Their increased skeletal mass is apparently used for hydrostatic control of buoyancy and trim for instance in sirenians.
The second tendency in bone structural specialization characterizes sustained swimmers, capable of long cruises in open seas. Contrary to the first process, bones are considerably lightened. Bone structure is highly cancellous with very thin compact cortices (osteoporitic-like state) (Felts & Spurrell, 1965 for cetaceans and de Buffrénil et al., 1987 for ichthyosaurs for example).
Moreover, histology gives us another information about heat regulation. Indeed, endotherms have a primary tissue and remodelling activity different from ecto-poïkilotherms (fibrous bone vs lamellar zonar bone). Endothermy is found among organisms practising sustained swimming during long cruises (Webb & Buffrénil, 1990) and furnishing an important muscular work.
Histological study of Metriorhynchidae : preliminary data
In order to confirm or falsify the hypothesis that the Metriorhynchidae were epipelagic stalking hunter, a histological analysis was performed on samples of metriorhynchid skeletons: skull, humerus, vertebrae, ribs, femur and fibula. The previous histological study was realized only on ribs by Nopcsa and Heidseck in 1934. Our specimens come from the Callovian of the Anglo-Parisian Basin, from the collections of the Natural History Museums of Le Havre, Boulogne-sur-Mer and Stuttgart. Bones have been studied in 100 µm thin sections which for most of them were normal to diaphyseal sagittal axis.
The metriorhynchid post-cranial skeleton does not clearly show any of the two histological specializations encountered in secondary swimmers and their skeletal histology does not differ significantly from living crocodilians. Their bones belong to the lamellar-zonar type, which is a classic configuration among poïkilo-ectothermic reptiles (de Ricqlès, 1976). In living crocodilians, an ecto-poïkilotherm physiology is consistent with the incapacity of these animals to perform sustained effort (i. e. fast swimming or long distances). Conversely, fossil reptiles supposedly sustained swimmers display quite a different type of bone structure (highly remodelled fibres or pseudolamellar bone tissue of marine reptiles, such as ichthyosaurs, de Buffrénil et al., op.cit.).
Hence, metriorhynchid histology suggest that these marine crocodilians were physiologically closer to modern crocodilians than to sustained swimmers. Nevertheless, all Mesozoïc marine reptiles show an osteoporotic process of lightening of the skeleton. Metriorhynchids share with them this process but it is exclusively restricted to the skull, the femur and to a lesser extent the ribs.
Extensive resortive attack of periosteal cortices give the skull its remarkably cancellate aspect : for example, 50 to 60% on the Metriorhynchus superciliosus rostral area whereas it represents only 17% there in Crocodylus cataphractus, a living longirostrine form used as a reference for our study (fig. 2 ). From a histological point of view, the inner organisation does not differ significantly from the rest of the skeleton. The selective anterior lightening may have altered the static position in water and induced a passive oblique trim. Indeed, external nares emerged without any muscular control. On land, their morphology must have made them excessively vulnerable. This oblique posture may have helped them in their thermoregulation process, to bask in hot superficial waters (fig.1).
Their ectothermic physiology is not compatible with a hunter pursuing its preys by sustained swimming. Instead, another kind of hunt may be envisaged, such as stalking, as in crocodilians living in freshwater. The reduction of skull mass, which reduces inertia, rendered movements faster, and more efficient by quick lateral attack in the vision field. The lightening of the calvaria has induced a backward displacement of the centre of gravity, comparable to that of accelerator swimmers.
The addition of histological and morphological data give us a precise picture of metriorhynchid paleoecology. First, metriorhynchids were ecto-poïkilotherms. Second, morphological characters and some of the histological properties seem to show an ambiguousness between stalking predators and sustained swimmers. Here, we propose a hypothesis conciliating morphological and histological characters according to which metriorhynchids were epipelagic stalking predators just beneath the surface.
In conclusion, the conjunction of histology and good living models helps us to validate a hypothesis about the way of life of a marine organism without recent equivalents. Thanks to the confrontation between morphofunctional analysis and physiological, and more precisely here histological, constraints, a better picture of metriorhynchid paleocology can be given.
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Figure 2 : Schematic aspect of the microanatomic organization in the snout of A.Metriorhynchus superciliosus and B. Crocodylus cataphractus.