Wednesday, May 7, 2008

Pelvic muscles for aquatic locomotion in crocs

It is widely known that crocodilians use a unique form of diaphragmatic breathing (Gans and Clark 1976; Farmer and Carrier 2000). Diaphragmatic breathing in crocodilians employs a hepatic piston or the movement of the liver driven by the diaphragmatic muscle. The diaphragmatic muscle attaches to the pelvis and to the liver. Contraction of the diaphragmatic muscle pulls the liver caudally increasing the volume of the pleural cavity. Farmer and Carrier (2000) further showed that the kinetic pelvis also contributes to breathing in crocodilians. Pelvic muscle activities were correlated with both inspiration (with M. ischiopubis and M. ischiotruncus rotating the pubes ventrally increasing abdominal volume) and expiration (with the M. rectus abdominis and M. transversus abdominis rotating the pubes dorsally). Activation of these four pelvic muscles are independent of locomotion and were presumed to be primarily for breathing function. This allows for a strong breathing capability independent of locomotion, i.e. breath heavily while running, and is in stark contrast to the low metabolic sit-and-wait lifestyles of modern crocodilians. Thus, Farmer and Carrier (2000) suggest that these functional adaptations were strongly selected for early in the evolutionary history of the crocodilian lineage when high metabolic lifestyles were more common amongst the members of the group. This idea that pelvic ventilation is plesiomorphic to archosaurs is consistent with some previous studies such as Ruben et al. (1997), who determined that theropods also used a hepatic piston diaphragm for ventilation, based on similarity of pelvic morphology between theropods and crocodilians – though Codd et al. (2008) argued for an avian-style ventilation in non-avian maniraptoran theropods, based on the presence of uncinate processes in these taxa.

I came across a very intriguing study today, which got me started on this divergence into crocodilian respiration. It is a study on the activities of the respiratory muscles in the American Alligator (Alligator mississippiensis) during aquatic locomotion. Uriona and Farmer (2008) tested the hypothesis that the pelvic muscles involved in pelvic ventilation also functions in aquatic locomotion, primarily in controlling pitch and roll. Electromyography actually showed that except for M. transversus abdominis the pelvic muscles were active during a head dive. Putting weights on their tails to counter head dive resulted in greater activities of these muscles than when weights were attached to the head reinforcing the possible roles of these muscles in this activity. Presumably, when these muscles are active, it displaces the centre of buoyancy enough so that the caudal portion of the body is relatively less buoyant than the cranial portion allowing for a head-dive (Uriona and Farmer 2008). During rolling, the diaphragmatic muscle and rectus abdominis were active unilaterally. Because unilateral muscle activation requires a high amount of neural control, pelvic muscle activity is shown to be important in aquatic locomotion.

Uriona and Farmer’s (2008) inference into the evolution of respiration in crocodilians is very interesting. But I can’t explain it very well so I will cheat and quote them directly.

“We observed that alligators activate the rectus abdominis and the diaphragmaticus in synchrony when diving in water, despite the fact that the rectus abdominis is used for exhalation and the diaphragmaticus for inhalation during ventilation. Both the rectus abdominis and the diaphragmaticus were probably originally derived from the same muscle-group in alligators and the primitive function of the rectus muscle was almost certainly locomotion rather than ventilation. To have a favorable function in aquatic locomotion just one innovation would have been required, a change of the site of insertion of a portion of the rectus from the sternum to the liver. By contrast, to evolve this muscle for the purpose of respiration requires two evolutionary innovations to occur, a deviation of the site of insertion of part of the rectus from the sternum to the liver and the development of new motor recruitment patterns. Thus, the most parsimonius explanation for the origin of the diaphragmaticus is that it arose first for controlling movement in the water and was later recruited for ventilation”.

I find this notion very intriguing; that pelvic muscles involved in the pelvic breathing of crocs initially evolved as a response to aquatic lifestyles and were later recruited for ventilation. However, I’m finding it difficult to follow their logic. Surely, the development of new motor recruitment patterns would have to have occurred even if these muscles were initially adapted for aquatic locomotion? Unless, these motor recruitment patterns are plesiomorphic as well – but then that would mean that evolutionary steps for pelvic ventilation wouldn’t have to deal with developing new motor recruitment patterns and it would cost as much as adaptations for aquatic locomotion...

Unless I am an idiot and missing something obvious, I don’t really see why it is most parsimonious to think functions for aquatic locomotion are primitive. In any case, I’d be curious to see what kind of new research can test this further.


References:
Codd, J. R., P. L. Manning, M. A. Norell, and S. F. Perry. 2008. Avian-like breathing mechanics in maniraptoran dinosaurs. Proceedings of the Royal Society B-Biological Sciences 275:157-161.
Farmer, C. G., and D. R. Carrier. 2000. Pelvic aspiration in the American alligator (Alligator mississippiensis). Journal of Experimental Biology 203(11):1679-1687.
Gans, C., and B. Clark. 1976. Studies on Ventilation of Caiman crocodilus (Crocodilia-Reptilia). Respiration Physiology 26(3):285-301.
Ruben, J. A., T. D. Jones, N. R. Geist, and W. J. Hillenius. 1997. Lung structure and ventilation in theropod dinosaurs and early birds. Science 278(5341):1267-1270.
Uriona, T. J., and C. G. Farmer. 2008. Recruitment of the diaphragmaticus, ischiopubis and other respiratory muscles to control pitch and roll in the American alligator (Alligator mississippiensis). Journal of Experimental Biology 211(7):1141-1147.

Carnotaurus sastrei

I got a request from Zach to draw Carnotaurus so here is my attempted reconstruction of C. sastrei. Funnily enough I have never drawn or even attempted to draw Carnotaurus previous to this - that is except for the unsatisfactory precursor to this picture...It took me forever to finish but for a first attempt I kinda think it turned out pretty good.

There are some really strange things with Carnotaurus, the first obvious being the skull. Staring at Bonaparte et al.'s (1990) skull reconstruction and photos for a prolonged time and reading their description, I noticed that the postorbital region of the skull in Carnotaurus is really strongly deflected ventrally while the sagittal crest is extremely high. This results in the supratemporal fenestrae having their lateral borders ventrally displaced compared to the medial borders. The sagittal crest in reptiles generally serves as the attachment sites for jaw adductor muscles, namely the M. pseudotemporalis superficialis (MPsTs), M. adductor mandibulae externus medialis (MAMEM), and MAME profundus (MAMEP) (Holliday and Witmer 2007), so an enlargement of the sagittal crest can allow for increased attachment area for these muscles. On the other hand, the posterior face of the transverse projection of the dorsal crest of the parietals serve as the attachment sites for the neck muscles namely the M. transversospinalis capitis (Snively and Russell 2007). The high position of the attachment site allows for a higher leverage for dorsiflexion of the skull by this muscle.

But then, perhaps the most striking feature of Carnotaurus is the frontal horns. For some reason I've always thought the horns were flatter and bladelike but on closer inspection, I was surprised to find how thick they actually are, though the dorsal surface is flat - hmm...I guess my reconstruction kind of looks like they're conical than flat on top...The horns have "a system of shallow grooves" making the surface quite different from that of the rest of the skull (Bonaparte et al. 1990). Apparently, the structure of the horns is not so different from that of horn cores in modern bovid so it is likely that horns in Carnotaurus also had some corneous covering making them longer in life.

Lastly, I was rather intrigued by the strange forelimbs. The ulna and radius are extremely short (1/4 the length of the humerus) and features on the articulation with the humerus indicate that the bones did not rotate significantly. This ristricted movement in the anteroposterior direction. Further, the parallel positions of the ulna and radius forced the palmer side of the manus to face dorsally/anteriorly (and laterally?) as opposed to ventrally/medially as in other theropods (Bonaparte et al. 1990). So apparently, the palms of Carnotaurus face outwards as opposed to inwards. Now this came as a complete surprise for me. The bones of the manus themselves are preserved but not in articulation and the distribution of the bones were interpretted tentatively (Bonaparte et al. 1990). Coria et al. (2002) report of an articulated manus in Aucasaurus providing a better understanding of abelisaurid manual morphology. In Aucasaurus, as in Carnotaurus, there are four metacarpals (mc I ~ IV). It seems unlikely that mc I and IV carried any phalanges, while mc II and III are joined to one and two phalanges respectively, but with no clear indications whether claws were present or not (Coria et al. 2002). Unlike Aucasaurus mc IV in Carnotaurus is more elongate and has a large articulation for the ulna.

So all in all, strange beast...