Some considerable time ago – it was, I discover to my surprise, April 2010 – I was lucky enough to participate in the Great Crocodilian Dissection Event at the RVC (Royal Veterinary College, UK), planned by the mighty and benevolent Prof John Hutchinson. John actually received a job-lot of numerous crocodilian specimens and arranged to have a large number of them dissected and studied over a period of a couple of weeks. Just about every free citizen involved in archosaur research descended upon the RVC. I’ve never had the chance to dissect a crocodilian before and I learnt a lot; I meant to blog about the event shortly after it occurred, but other things got in the way and it ended up on the backburner.
Here, at long last, I aim to talk you through just a few edited highlights of a croc dissection. Some of the observations concerned are applicable to all crocodilians while others are peculiarities of Osteolaemus, the animal I helped dissect (I couldn’t get to the RVC in time to work on Black caiman Melanosuchus niger or Morelet’s crocodile Crocodylus moreletii, dammit). My thanks to John and also to Vivian Allen for leading the dissection.
Oh, in the intervening TWO YEARS since we did the dissection, John has even started his own blog, titled What’s In John’s Freezer? It’s required reading for any self-respecting frequenter of Tet Zoo. I’d add it to my blogroll, if only I had one that was of any use whatsoever.
Crocodilia, Crocodylia, Crocodyliformes, Crocodylomorpha – why most people remain confused
Firstly – a minor point on nomenclature. This sort of thing has to be discussed whenever crocodilians are. The group of archosaurs conventionally called crocodilians, and frequently termed Crocodilia in the textbooks (that is, living crocodiles, alligators, gharials and all their crocodile-like, alligator-like and gharial-like fossil relatives) is now most typically termed Crocodyliformes. That is, ‘crocodilians’ of tradition are now crocodyliforms (note that the last ‘e’ gets dropped when you convert a ‘-formes’ name to its vernacular version). Within Crocodyliformes, the crown-group (that is, the group that contains the living species and all descendants of their most recent common ancestor) is termed Crocodylia. So, Crocodylia is a clade within Crocodyliformes (Clark in Benton & Clark 1988, Norell et al. 1994, Salisbury & Willis 1996, Brochu 2003).
Crocodyliformes is part of a more inclusive group that also includes the crocodyliform-like sphenosuchians, and this larger clade is termed Crocodylomorpha. In turn, Crocodylomorpha is part of a major archosaur group informally termed the crocodile-branch or crocodile-group archosaurs, the best technical name for which is (unfortunately) Pseudosuchia (how I hate the fact that this name might win out over Crurotarsi, if certain phylogenetic definitions are followed).
In view of the confusion that ensues whenever an attempt is made to explain the use and meaning of these names (I've had to do it several times), I believe that we should stick with what we have: the archosaurs that we imagine as ‘crocodilians’ are now crocodyliforms, and the crocodyliform crown-clade is Crocodylia. However, some workers aren’t happy with this and have argued that we should use Crocodylia in place of Crocodyliformes (Martin & Benton 2008). I can’t see that this does anything useful bar complicate an already confusing situation and I think that we should ignore this proposal. When talking to technical audiences, I tend to use crocodyliform, but I don’t see anything wrong with ‘crocodilian’ being used as a vernacular term for the clades Crocodyliformes or Crocodylomorpha.
The African dwarfs… yes, plural
Anyway, the species under consideration here is Osteolaemus tetraspis, the tropical African crocodile most usually known as the African dwarf crocodile. Other common names include Broad-snouted crocodile and Black crocodile, and there are apparently people who call it the Rough-backed crocodile, Bony crocodile or African caiman. A supposedly distinct kind of African dwarf crocodile from the upper Congo River Basin, named Osteoblepharon osborni, was described in 1919. However, it later became relegated to the status of an Osteolaemus tetraspis subspecies, and there followed suggestions that even this subspecific recognition was unwarranted (e.g., Ross 2006).
More recently, morphological (Brochu 2007) and molecular data (McAliley et al. 2006, Eaton et al. 2009) have shown that Congo River Basin dwarf crocodiles can be reliably distinguished from those dwarf crocodiles known from further west. Furthermore, these differences are as significant as those separating uncontroversial species elsewhere in the crocodile tree. Accordingly, O. tetraspis and O. osborni are now recognised as distinct species by some authors.
Furthermore, Eaton et al. (2009) also found that the O. tetraspis population of Gabon and the adjacent countries was significant different from the dwarf crocodiles of more western countries, leading to the suggestion that these should be recognised as distinct species as well (Eaton et al. 2009, Eaton 2010). A formal taxonomy that reflects this discovery has yet to be published (so far as I know). As usual, we’ll get a difference of opinion here. Should we formally name distinct phylogenetic lineages, or do we go with the idea that lumping the lineages together is more practical and sensible?
Total lengths of 1.8 m are on record for Osteolaemus and there are even reports of animals 2.3 m long, so perhaps it isn’t necessarily always the ‘dwarf’ we think it is. This is a crocodile often stated to be of strong terrestrial habits, sometimes reported far (as in, a few kilometres) from water. However, little good data has been collected and published on its habitat preferences and behaviour and, while it might be proficient on land, there are more reasons for thinking that it’s a specialised animal of shallow pools, streams and other flooded habitats in closed-canopy forests. It’s said to be less aggressive than other crocodiles (the term ‘docile’ has been used), and to be especially curious.
Ok, enough preamble, on with the anatomy…
Short snouts, ‘poke-through’ dentitions and big palpebrals
Let’s start with the head. Modern crocodilians are well known for having elongate, superficially tubular snouts where the rostrum is dorsoventrally flattened. This is known as the platyrostral shape, and if you want to know more about it and about what it might mean for crocodilian feeding behaviour, skull loading and so on, see Busbey (1995). However, modern crocs aren’t all like this. Osteolaemus and the dwarf caimans (Paleosuchus) have deeper, proportionally short rostra, and it’s sometimes a matter of opinion whether they’re classified as altirostral or oreinirostral, rather than as platyrostral. ‘Altirostral’ and ‘oreinirostral’ both describe the ‘tall-snouted’ condition where the rostrum is relatively steep-sided and, overall, narrower and more vaulted than it is in platyrostral crocodilians.
In Osteolaemus, the snout is something like 1.3 times longer than it is wide as its base: that’s proportionally shorter than even a subadult Crocodylus crocodile. However, Busbey’s (1995) graph shows the snout of Osteolaemus to be not far removed in morphospace from undisputed platyrostral forms like Alligator, so Osteolaemus cannot be regarded as at all on par with truly altirostral animals like sebecosuchians or pristichampsids (two especially neat fossil crocodilian groups) (Busbey 1995, Rossmann 2000). While on the subject of snouts, something that Osteolaemus never does (apparently) is ‘allow’ its premaxillary bones to be perforated by its mandibular dentition. Yes, as remarkable as it seems to us, in crocodilians of many species, some of the teeth in the anterior part of the lower jaw cause holes to form in the corresponding parts of the upper jaw; the end result being that the teeth poke through specially formed holes. This isn’t unique to crocodilians – among fossil tetrapods it’s especially well known for some temnospondyls and there are also hints of it in pliosaurs.
I mentioned a moment ago that a proportionally short snout like that of Osteolaemus is also present in the Paleosuchus caimans. In fact, Osteolaemus shares other skull features with other short-snouted crocodilians. Osteolaemus and Paleosuchus both have especially large palpebral bones occupying the upper parts of their eye sockets (these are formed from several distinct ossifications that fuse together as the animals mature). Furthermore, their supratemporal fenestrae are proportionally small and become smaller during ontogeny.
Are the two taxa (Osteolaemus and Paleosuchus) especially similar in ecology or behaviour? Both are relatively small crocodilians of tropical forest floors, both are strongly terrestrial in comparison with other living crocodilians, and both may eat more hard-shelled prey (like crabs and snails) than do other crocodilians. Elsewhere within crocodilians, this short-snouted morphology also evolved within the recently extinct mekosuchines (Brochu 2001). Were the species involved similar in ecology and behaviour to Osteolaemus and Paleosuchus as well? Readers with good memories should recall the one or two articles I published on ver 2 about Mekosuchus and related forms.
Scutes, and some muscles
Crocodilians are well known for possessing dermal scutes, or osteoderms. In Osteolaemus, the nuchal shield (the field of scutes covering the dorsal surface of the neck) is separated from the dorsal shield (the field of scutes covering the animal's back) by a band of skin. There are (usually) only four nuchal scutes, hence the specific name ‘tetraspis’. The dorsal shield (understood to contain all scutes on the back anterior to the sacrum) is formed by 17 transverse rows of vaguely squarish scutes; each row consists of 4-8 (but usually 6) scutes (Ross & Mayer 1983). Croc scutes are almost certainly multifunctional. They provide protection from predators, they play some role in sociosexual display, they contribute to the collection and transfer of solar heat, and they perhaps function as part of a self-carrying system in which muscles attached to both the ventral surfaces of the scutes and to the vertebrae help the animal fight gravity (Frey 1988, Salisbury & Frey 2000).
A neat thing about the scutes is that they’re not all flat. Those at the lateral edges of the nuchal and dorsal shields have distinct medial and lateral parts in many crocodilians, with longitudinal keels positioned at the junction between the two. This is especially obvious in the large nuchal scutes of Osteolaemus. As you remove the nuchal shield of an Osteolaemus, the four scutes remain attached as a single unit and form a sort of neat little inverted box. If this was flipped upside down, you could keep it on your desk and use it as a container for paper-clips and drawing pins.
Having removed the scutes and accompanying epidermis, we got to see the transversospinalis capitis musculature that runs along the dorsal surface of the neck. This was both deep and narrow, and also extremely pink, but I don’t know if that means anything in particular. If you dissect closer to the posterior border of the head, you of course get to see the gigantic depressor mandibulae and pterygoideus muscles, both of which take up an impressive amount of space about the back of the lower jaw and quadrate. Actually, while I’m familiar with the appearance and relative size of these muscles in Crocodylus crocodiles, I don’t know what they look like in Osteolaemus and I didn’t get to find out in this particular dissection. Oh well, maybe next time.
The hindlimbs and tail
Finally, some brief comments on the hindlimbs and tail. Crocodilians have crazy complex hindlimb muscles, and I got to see many of those during the dissection. On the outermost surface of the thigh, the large and bulky ilio-tibialis is located more anteriorly than the flexor-tibialis externus – the muscle that forms the posterior border to the thigh. The ilio-tibialis actually has three distinct segments, all of which are attached to the dorsal edge of the ilium and all of which merge somewhere in the knee region. They overlie the two heads of the ambiens (one head originates from just anterior to the acetabulum, the other from the base of the pubic bone), the ilio-femoralis, the different parts of the femora-tibialis and various other muscles.
There’s also the ilio-fibularis, sandwiched in between some of the ilio-tibialis components but emerging distinctly on the lateral surface of the knee. Here, this muscle runs through a weird ‘tendon sling’ attached to the side of the femur and gastrocnemius (Romer 1923). Of course, I’ve hardly mentioned most, let alone all, of the pelvic and hindlimb muscles here: there are as many as 23 different muscle heads crossing the pelvis in crocodilians, and the interplay between them “is extremely difficult to resolve” (Gatesy 1997, p. 208).
One of the most distinctive features of archosaurs is a prominent muscle attachment site on the posterolateral part of the femur. Known as the fourth trochanter, it’s the attachment site for the caudofemoralis longus (cfl for short) – a large muscle that also attaches to the sites of the caudal vertebrae and is involved in retracting the femur during locomotion. I’ve never dissected out a cfl before and wanted to see both how clearly differentiated it was from the adjacent caudal muscles, and also how far it extended along the tail.
As you can see from the photo here, it is in fact pretty easy to dissect the cfl out separately from the adjacent, dorsally sited longissimus and the more ventrally sited ilio-ischiocaudalis and other tissues, so long as you’re careful. The cfl looks weird for a tail muscle – it isn’t ‘segmented’ into myosepta and hence looks more like a limb muscle than an axial one. I’m not an especially huge fan of eating meat, but I can certainly appreciate how people might look at the cfl and think “Wow, that archosaurian caudofemoralis longus sure like looks it would make a good fillet”. If you’ve been paying attention to the dinosaur literature you’ll know that long-tailed dinosaurs have, it turns out, long been reconstructed with inadequately sized cfls; there’s now a push to give dinosaurs thicker, more muscular tails (Hutchinson et al. 2011, Persons & Currie 2011).
There is a ton more that could be said – crocodilian pelvic and belly musculature, their respiratory anatomy, their amazing heart anatomy, their shoulder joints and jaw muscles have all been recent areas of substantial interest. But I have to move on. We’ll be coming back to crocodilians real soon.
And I also haven't much covered the affinities of Osteolaemus with respect to other crocodilians. Work on fossil species seems to show that Osteolaemus is the only extant member of a once diverse clade that includes various small, mid-sized and large crocodylid crocodilians of Africa and the Indian Ocean. Some of these animals have been written about on Tet Zoo ver 2 – in view of what's just happened to that site (read on), I don't think it's worth my while adding links anymore.
Two unconnected announcements
Two more things while I’m here. If you’ve been keeping an eye on the comments here at ver 3, you’ll have seen the discussion about changes just made to ver 2 (archived at ScienceBlogs). ScienceBlogs has just migrated to WordPress, meaning that Tet Zoo ver 2 now has a totally new look. As usual, things are not better than they were, but worse. The blogroll has totally gone, the formatting of the articles has been royally screwed with (annoyingly, all accented characters have been removed), and – most devastatingly – all the comments have gone. That’s a major loss. As regular readers will know, the (often substantial) comment threads attached to many of the articles included a huge amount of debate and accessory information. I’ve managed to get behind the scenes at WordPress, and I’m sorry to say that there’s no sign of the comments whatsoever – they seem to be totally gone. I know that there are ways of accessing old webpages (Wayback Machine and so on), and people tell me all the time how difficult it is to ever really remove anything from the web… nevertheless, this (at least superficial) loss is a major blow to the value and content of Tet Zoo. Seeing as I’m not with ScienceBlogs anymore, there’s nothing I can do, nor was I at all aware of these impending changes. Comments were open at Tet Zoo ver 2 yesterday but a huge flood of spam caused me to turn off commenting site-wide.
On to the second thing… Those of you interested in open access and in publishing ethics will know that some academic publishers have been doing their very best to prevent open access to publicly funded research. Yes, you read that right. They believe that the public should not be allowed to freely access the scientific literature it funds. A substantial amount of digital ink has been spilt on this matter in recent months, as you’ll know if you read SV-POW! or if you’re aware of the internet in general. One of the latest developments in this saga is that a petition organised by Whitehouse.gov is currently taking signatures to allow publicly-funded research to be openly available to the public, as of course it ethically should be. This will be presented to the Obama Administration. If you support open access, and if you believe (as I do) that publishing companies have no right to keep publicly-funded research behind paywalls, please sign now, and encourage others to do likewise.
Refs - -
Benton, M. J. & Clark, J. M. 1988. Archosaur phylogeny and the relationships of the Crocodylia. In Benton, M. J. (eds) The Phylogeny and Classification of the Tetrapods, Volume 1: Amphibians, Reptiles, Birds. Clarendon Press (Oxford), pp. 295-338.
Brochu, C. (2001). Crocodylian Snouts in Space and Time: Phylogenetic Approaches Toward Adaptive Radiation Integrative and Comparative Biology, 41 (3), 564-585 DOI: 10.1093/icb/41.3.564
- . 2003. Phylogenetic approaches toward crocodylian history. Annual Review of Earth and Planetary Science 31, 357-397.
- . 2007. Morphology, relationships, and biogeographical significance of an extinct horned crocodile (Crocodylia, Crocodylidae) from the Quaternary of Madagascar. Zoological Journal of the Linnean Society 150, 835-863.
Busbey, A. B. 1995. The structural consequences of skull flattening in crocodilians. In Thomason, J. J. (ed) Functional Morphology in Vertebrate Paleontology. Cambridge University Press (Cambridge), pp. 173-192.
Eaton, M. J. 2010. Dwarf Crocodile Osteolaemus tetraspis. In Manolis, S. C. & Stevenson, C. (eds) Crocodiles. Status Survey and Conservation Action Plan. Third Edition, pp. 127-132. Crocodile Specialist Group, Darwin.
Eaton, M. J., Martin, A., Thorbjarnarson, J. & Amato, G. 2009. Species level diversification of African dwarf crocodiles (genus Osteolaemus): a geographic and phylogenetic perspective. Molecular Phylogenetics and Evolution 50, 496-506.
Frey, E. 1988. Das Tragsystem der Krododile [sic] - eine biomechanische und phylogenetische Analyse. Stuttgarter Beiträge zur Naturkunde Serie A (Biologie), 426, 1-60.
Gatesy, S. M. 1997. An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion. Journal of Morphology 234, 197-212.
Hutchinson, J. R., Bates, K. T., Molnar, J., Allen, V. & Makovicky, P. J. 2011. A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLoS ONE 6(10): e26037. doi:10.1371/journal.pone.0026037
Martin, J. E. & Benton, M. J. 2008. Crown clades in vertebrate nomenclature: correcting the definition of Crocodylia. Systematic Biology 57, 173-181.
McAliley, L. R., Willis, R. E., Ray, D. A., White, P. S., Brochu, C. A. & Densmore, L. D. 2006. Are crocodiles really monophyletic? – Evidence for subdivisions from sequence and morphological data. Molecular Phylogenetics and Evolution 39, 16-32.
Naish, D. 2001. Fossils explained 34: Crocodilians. Geology Today 17 (2), 71-77.
Norell, M. A., Clark, J. M. & Hutchison, J. H. 1994. The Late Cretaceous alligatoroid Brachychampsa montana (Crocodylia): new material and putative relationships. American Museum. Novitates 3116, 1-26
Persons, W. S. & Currie, P. J. 2011. The tail of Tyrannosaurus: reassessing the size and locomotive importance of the M. caudofemoralis in non-avian theropods. The Anatomical Record 294, 119-131.
Romer, A. S. 1923. Crocodilian pelvic muscles and their avian and reptilian homologues. Bulletin of the American Museum of Natural History 48, 533-552.
Ross, F. D. 2006. African dwarf-croc quandary persists. Crocodile Specialist Group Newsletter 25, 19-21.
- . & Mayer, G. C. 1983. On the dorsal armor of the Crocodilia. In Rhodin, A. G. J. & Miyata, K. (eds) Advances in Herpetology and Evolutionary Biology. Museum of Comparative Zoology (Cambridge, Mass.), pp. 306-331.
Rossmann, T. 2000. Studies on Cenozoic crocodiles: 4. Biomechanical investigation on the skull and the neck of the Palaeogene crocodile Pristichampsus rollinatii (Eusuchia: Pristichampsidae). Neues Jahrbuch fur Geologie und Paläontologie, Abhandlungen 215, 397-432.
Salisbury, S. W. & Frey, E. 2000. A biomechanical transformation model for the evolution of semi-spheroidal articulations between adjoining vertebral bodies in crocodilians. In Grigg, G. C., Seebacher, F. & Franklin, C. E. (eds) Crocodilian Biology and Evolution. Surry Beatty & Sons (Chipping Norton, Aus.), pp. 85-134.
- . & Willis, P. M. A. 1996. A new crocodylian from the Early Eocene of eastern Queensland and a preliminary investigation of the phylogenetic relationships of crocodyloids. Alcheringa 20, 179-226.