Tetrapod Zoology

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ResearchBlogging.org

Earlier this year (in June), Channel 4 television here in the UK broadcast series 2 of Inside Nature’s Giants (ING from hereon… titled Raw Anatomy in the US, you poor, poor people). You may have heard it here first. Hopefully you’re familiar with ING series 1 – it looked at the anatomy of elephants, baleen whales, crocodiles and giraffes – and, if you’re not, be sure to check out the Tet Zoo articles starting here. My praise for series 1 was extreme, by which I mean that I thought it was excellent: a real triumph and a major event in both the world of broadcasting, and in bringing good science to the masses.

I’m pleased to say that this was widely recognised: many TV critics said positive things about ING (very memorable example), and in June 2010 the team behind the series (Windfall Films) won a BAFTA award (= British Academy of Film and Television Arts). Nature featured an interview with anatomist Joy Reidenberg – the main [human] star of the series – in June (Gilbey 2010). The interview touched on the educational significance of the series, the importance of bringing evolutionary perspectives on nature to a wide audience, and the fact that anatomy is not a dead, Victorian science (far from it: we are in the midst of an anatomical revolution). Clearly, expectations for series 2 were pretty high.

WARNING: major spoiler for ep 1 ahead, and further spoilers to follow.

The three episodes did not disappoint. Once again, standards were high and a great deal of material that would have been totally novel to the majority of the audience was presented with flair and aplomb, and (admirably) without dumbing-down. Ep 1 looked at the Great white shark, ep 2 was called ‘Monster Python’, and ep 3 was titled ‘The Big Cats’. A 90 minute special episode, ‘Monsters of the Deep’ is due to be screened some time later this year. It’s devoted to giant squid: I’m sure it’ll be excellent, but I won’t be writing about it (hey, not because I don’t like squid).

I need to say at the outset that I failed to take notes while watching series 2, and that (except for the python episode) I haven’t been able to view the episodes online. This is my stupid fault for leaving the writing-up to too late (you know, because I’m lazy). The consequence of all this is that I’ve had to be a bit sparse on some of the details, and have missed the names of some of the experts. Apologies in advance. If you can help by filling in any of the missing data, please do so. I’ll then update the articles accordingly.

As was the case for series 1, some of ING series 2 was filmed at the Royal Veterinary College. The series was presented by Mark Evans (biologist Simon Watt also featured heavily). Richard Dawkins made occasional appearances and, among the several anatomists who featured, Joy Reidenberg was a regular face once again [image below provided by Joy Reidenberg, used with permission].

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So, ep 1 covered Carcharodon carcharias. Even as an obviously dedicated, obsessive tetrapodophile I have to admit that I find sharks cool and fascinating, and lamnids like the White shark are among my favourites. I’m therefore going to break the tetrapods-only rule once again. The shark used in the episode was a particularly large female (4.5 m long and 900 kg in mass), killed following entanglement in a South African beach protection net (note that no animals were killed specifically for the series).

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One of the highlights for me was seeing the jelly that occupies the ampullae of Lorenzini [shown here]. These flask-shaped, electroreceptive organs – well known and familiar to anyone who knows sharks – are distributed across the White shark’s snout and around its jaws, but while many sources show the organs in cross-section, I’ve never actually seen their contents before. That’s because I’m naïve: the jelly extrudes from a freshly dead shark should you squeeze the area around any of the ampullae, apparently. Also interesting (and not mentioned that often in the literature) is that the ampullae extend across the dorsal suface of the head, not just the nose.

The ING team began by discussing (and dissecting) the jaws and gills. One really bizarre and interesting fact is that the cartilaginous jaws are not solid, but flexible enough for the teeth to be wiggled back and forth. This makes it all the more remarkable – or, if you like, ridiculous – that the White shark has a bite force that can perhaps exceed 1.8 tons (Wroe et al. 2008). The jaws are mobile relative to the snout and braincase, and during biting the snout is lifted and the jaws are protruded forwards. This ‘lift and lunge’ biting process – which you might have seen on film (if you’ve seen it in real life, you’re either very lucky or very unlucky) – is very rapid, taking between 0.75 and 1.78 secs (Ellis & McCosker 1991). Like many animals assumed to have a homodont dentition, Carcharodon is actually quite heterodont: the upper jaw teeth are wider and stouter than the lower jaw teeth, the teeth decrease markedly in size towards the corners of the mouth, and the crown of the third upper jaw tooth is short compared to its neighbours, and has a peculiar curvature that directs its apex toward the midline. There are 26 upper and 24 lower jaw teeth, with numerous replacements lined up behind, of course [image of Carcharodon jaws below provided by Joy Reidenberg, used with permission]

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Later in the dissection, they turned the animal onto its back and cut open its belly in order to reveal the liver. It’s well known (I hope) that sharks use a large, oily liver as a buoyancy organ (no swim bladder), but the size of this organ in Carcharodon has to be seen to be believed… it was enormous, bigger than a person [adjacent photo shows the extracted liver: people for scale]. The Carcharodon liver can constitute as much as a quarter of the shark’s weight (Ellis & McCosker 1991). The team also looked at the spiral valve intestine: the shark gut is short and looks like a simple tube, but when cut open it reveals a tightly spiralling structure that obviously maximises the absorption surface. Like the ampullae, the spiralling structure of the intestine is something you see referred to in every single shark book (frequently illustrated in diagrammatic form), but actually seeing it is a rare and wonderful thing… if, that is, you’re not a shark specialist (and I’ll admit here that I’ve never properly dissected a shark).

Something that should be more widely known about the Great white (and a few other lamnid sharks) is that it’s endothermic. More specifically, it exhibits regional endothermy; the ability to generate (and retain) heat in the viscera, brain, eyes and slow-twitch muscle fibres. This heat is transferred to the surrounding tissues, and Great whites and other endothermic fish are able to maintain internal temperatures as much as 14° C higher than the surrounding water (Carey et al. 1982, Dickson & Graham 2004, Bruce 2006). The heat-generating muscles in the tail were obvious (being deep red) in dissection, compared to the surrounding whiter muscles [image below: did I say that Great white sharks are among the most awesome creatures on the planet? South African breaching shark, photo © Chris Brunskill/Ardea.com].

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Much more was covered – this is but the briefest of summaries. While there’s clearly no shortage of stuff to talk about when discussing animal anatomy, I’ve become increasingly impressed with how much information ING managed to pack into each episode. And, even to someone with a reasonable amount of prior knowledge about shark anatomy, seeing such things as the liver were memorable firsts. The episode also did a good job of showing what a wonderful, beautiful animal the Great white is when alive, and of how it deserves conservation status and legal protection. So – watch the episode if you can!

For the Tet Zoo reviews on series 1 of ING, see…

Many thanks to Zach Buchan for invaluable assistance, to Joy Reidenberg, and to Tom Mustill at Windfall. More on ING series 2 coming soon.

Refs – –

Bruce, B. D. 2006. The Biology and Ecology of the White Shark, Carcharodon carcharias. In Camhi, M. D., Pikitch, E. K. & Babcock, E. A. (eds) Sharks of the Opean Ocean: Biology, Fisheries and Conservation. John Wiley & Sons, pp. 69-81.

Carey, F. G., Kanwisher, J. W., Brazier, O., Gabrielson, G., Casey, J. G. & Pratt, H. L. 1982. Temperature and activities of a white shark, Carcharodon carcharias. Copeia 1982, 254-260.

Dickson KA, & Graham JB (2004). Evolution and consequences of endothermy in fishes. Physiological and biochemical zoology : PBZ, 77 (6), 998-1018 PMID: 15674772

Ellis, R. & McCosker, J. E. 1991. Great White Shark. Stanford University Press (Stanford, California).

Gilbey, J. 2010. Q&A: Prime-time dissection with Joy Reidenberg. Nature 465, 1013.

Wroe, S., Huber, D. R., Lowry, M., McHenry, C., Moreno, K., Clausen, P., Ferrara, T. L., Cunningham, E., Dean, M. N. & Summers, A. P. 2008. Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? Journal of Zoology 276, 336-342.

Comments

  1. #1 Dartian
    September 1, 2010

    Later in the dissection, they turned the animal onto its back and cut open its belly in order to reveal the liver.

    Was there anything (or anyone) in the belly?

    the size of this organ in Carcharodon has to be seen to be believed… it was enormous, bigger than a person

    Truly awesome indeed! I had no idea the liver was that big.

  2. #2 IanW
    September 1, 2010

    “…does Carcharodon bite?”

    What bites is not being able to see a live megalodon. From a safe distance, of course!

  3. #3 Darren Naish
    September 1, 2010

    I don’t remember the stomach contents (if there were any) – does anyone else?

    On “does Carcharodon bite?”, I should perhaps explain what this means. For years now, I’ve been using it to affirm a statement; a sort of replacement for “is the Pope catholic?”. I stole it from a Kate Charlesworth cartoon where a pterosaur said “Does T. rex bite?”.

  4. #4 Sven DiMilo
    September 1, 2010

    it exhibits regional endothermy; the ability to generate heat in the viscera, brain, eyes and slow-twitch muscle fibres. This heat is transferred to the surrounding tissues

    It’s not so much the ability to generate heat as it is the ability to retain some of the heat generated.

  5. #5 David Marjanović
    September 1, 2010

    Electroreceptive organs on the top of the head are also known in aquatic life stages of lissamphibians and seymouriamorphs.

    It’s devoted to giant squid: I’m sure it’ll be excellent, but I won’t be writing about it (hey, not because I don’t like squid).

    Heh. The disclaimers that have to be added these days! :-D

  6. #6 Jerzy
    September 1, 2010

    Boring, boring,

    I will wait a year or so for a film where a shark, crocodile, python etc. are each given a human to eat.

  7. #7 Jerzy
    September 1, 2010

    “aquatic life stages of lissamphibians and seymouriamorphs.”

    Actually, you reminded me of something. Parietal eye. Can I ask about the history of this among vertebrates? Were there ever animals with three equally functional eyes?

    I heard that juvenile tuatara has pretty complex parietal eye, complete with lenses and retina. If the only function of p.e. was setting a circadian rythm, lenses and retina are overkill for it. This pretty well suggests that tuatara ancestors had three about equal eyes.

  8. #8 Mark Lees
    September 1, 2010

    On the matter of dissecting sharks, when I did my A-level zoology – (almost 30 years ago now!) – dissecting dogfish was one of the mainstays of the practical sylabus (along, of course, with rats). I recall one Friday afternoon practical session, when the person on the bench next to me broke the stomach of her dogfish (the recognisable contents mostly seemed to consist of sea squirts), the smell was overpowering almost gut wrenching, and the fact that I’d had fish for lunch didn’t help.

  9. #9 SimonG
    September 1, 2010

    IIRC, when first shown the shark had its stomach everted, so there weren’t really any contents. Apparently this is normal behaviour for sharks when they’ve eaten something that disagrees with them, and presumably was a panic response at being stuck in the net.

    IIdon’tRC that’s all cobblers, of course.

    These programs have been superb. Seeing things I’d only read about, or didn’t even know about; all dealt with in an enthusiastic but not sensationalist way.

  10. #10 Amber
    September 1, 2010

    Is there any hope for this series hitting DVD? I just did a quick search and found nothing.

  11. #11 Nathan Myers
    September 1, 2010

    Joy Reidenberg is a World Heritage Treasure.

    Does anybody know why the cat and squid dissections haven’t shown up on YouTube yet?

  12. #12 Ben S-R
    September 1, 2010

    Did they talk about the retes used to retain metabolic heat and the internalization of red muscle?

  13. #13 Adam F
    September 1, 2010

    Sharks may not be tetrapods, but they still have two sets of paired limbs…which brings me to my question: when did the “two sets of paired limbs” pattern originate? I know some early fish only had one pair, and did any group wind up with three?

  14. #14 Allen Hazen
    September 1, 2010

    Adam F–
    One of the groups of Palaeozoic jawed fish, the Acanthodians (often deemed the sister taxon to Osteichthyes: more closely related to bony fish than to sharks!) had a series of … projections … along their sides: up to about 7, i think. Jury seems still to be out as to whether these are homologous to the paired appendages of Sharks and Osteichthyes. (Tetrapods are a subclade of O.) Palaeozoic jawless fishes seem to have had a maximum of two paired appendages: again unclear if they are homologous to our legs and arms.

    One of the mid-line fins of a Coelacanth (second dorsal?) is very similar structurally to the arm and leg fins, and I have seen speculation that it originated as a sort of unpaired ectopic “paired” fin, or at least that the coding for development and structure of paired fins somehow got copied into the program for unpaired…

  15. #15 Jim Thomerson
    September 1, 2010

    I vaguely recall seeing projection slides of the skull of some fossil amphibian(?) which had paired parietal eye openings; four eyes total.

  16. #16 David Marjanović
    September 2, 2010

    If the only function of p.e. was setting a circadian r[h]ythm, lenses and retina are overkill for it.

    Without a retina, there are no photoreceptors, so a retina is not overkill!

    The lens isn’t overkill either, because it allows the pineal/parietal organ to be smaller because it gathers light. Interestingly, it’s not serially homologous to the lenses of the other eyes, but to the layer with the blood vessels… I think. It’s simpler and less evaginated.

    I vaguely recall seeing projection slides of the skull of some fossil amphibian(?) which had paired parietal eye openings; four eyes total.

    Please try to find that again, I’ve never heard of it. (Even though the parietal and the pineal organ are left and right or the other way around, I forgot.)

    the Acanthodians (often deemed the sister taxon to Osteichthyes: more closely related to bony fish than to sharks!)

    Nope, they’re not monophyletic. Some acanthodians are stem-chondrichthyans, others are stem-osteichthyans. And the placodonts form a paraphyletic series of stem-gnathostomatans. Source: SVP talks and Nature papers by Martin Brazeau from the last 2 years or so.

    Palaeozoic jawless fishes seem to have had a maximum of two paired appendages: again unclear if they are homologous to our legs and arms.

    By far the most parsimonious assumption is that these are the forelimbs. The hindlimbs arose a bit later by ectopic expression of the same Hox genes.

  17. #17 Darren Naish
    September 2, 2010

    Oop…. placoderms :)

  18. #18 Dartian
    September 2, 2010

    And the placodonts[sic] form a paraphyletic series of stem-gnathostomatans.

    What, David Marjanović makes mistakes too? I’m so disillusioned right now.

  19. #19 MIke Simpson
    September 2, 2010

    ING is an utterly superb series and the shark episode was absolutely amazing. I was astounded to learn that the jaw is not part of the cartilaginous skeleton per se but an adapted gill ring and that the teeth have no connection with normal vertebrate teeth but are actually the tooth-like micro-spikes that cover the skin adapted to be bigger and sharper. I’m no marine biologist but I’ve never seen either of these – really very fundamental and deeply cool – facts mentioned in any previous book or documentary that has come my way.

    They’re doing a giant squid? That’s made my day!

  20. #20 Cameron
    September 2, 2010

    Allen,
    Oddly, both the anal fin and second dorsal of Latimeria are limb-ish – after a cursory search, I couldn’t find any other coelacanths with morphology developed to a similar degree. This is never really commented on in popular sources, as I suppose “Ol’ Four Legs with Two Other Legs in Another Axis” doesn’t have quite the same ring.

  21. #21 Jerzy
    September 2, 2010

    @David
    Parietal eye of Tuatara has a retina.

    Lenses, cornea and retina etc in parietal eye in juvenile Tuatara are interpreted as a vestigial remains of a fully functional eye (that is good for seeing) in some not too distant ancestors of living Tuatara species.

    Collecting light for pineal/parietal organ to be smaller? Sensitivity of endocrine organs is not a function of size. And hiding a light-sensitive organ inside the skull is madness – unless it is an evolutionary remaint.

  22. #22 John Harshman
    September 2, 2010

    (and I’ll admit here that I’ve never properly dissected a shark)

    What? Not even a dogfish? Around here, every undergrad course in comparative vertebrate anatomy does that.

  23. #23 Cameron
    September 2, 2010

    Re: Comment 20 (now readable, yay!), Forey’s History of Coelacanth Fishes (p. 216) explains that only the basal plates of the second dorsal fin and anal fin are typically preserved in fossilization – so presumably Latimeria isn’t a total freak.

  24. #24 Alan
    September 2, 2010

    Re:parietal eyes – the parietal opening on a bearded dragon (Pogona vitticeps) is quite obvious as it is surrounded by a ring of scales between the true eyes and shows as a dark spot. I believe I am correct that the Pogona parietal eye has an optic nerve and retina but no lens – can anyone confirm?

  25. #25 Andreas Johansson
    September 2, 2010

    @Cameron: I know I read a bit about it in some popular book or another. I want to say The Ancestor’s Tale but I’m not sure.

    @David Marjanović: So we’re all placoderms. Cool.

    Is there, incidentally, a name for the gnathostomatan total group?

  26. #26 darwinsdog
    September 2, 2010

    #15:

    I vaguely recall seeing projection slides of the skull of some fossil amphibian(?) which had paired parietal eye openings; four eyes total.

    You’re probably thinking of lampreys, which have two rudimentary ‘eyes,’ one derived from the pineal & the other from the parietal gland.

    #16:

    And the placodonts form a paraphyletic series of stem-gnathostomatans.

    An odd phylogenetic reconstruction, that.

  27. #27 Allen Hazen
    September 2, 2010

    Cameron (comments 20 & 23)– Thanks! I thought both the anal and second-dorsal fins were limb-like, but couldn’t remember for sure and chose a cautious wording. … But since it IS both, if they are somehow derived from the programing for limbs, Latimeria IS a vertebrate with three pairs of pair fins (Grin!).

    David (comment 16)– well, the Acanthodians HAVE often been DEEMED to be a sister group of the Osteichthyes (grin!). But thanks for the reminder about the Brazeau article: I remember seeing it and thinking it was exciting that the traditional Acanthodes might be paraphyletic with respect to BOTH Ost. and Chond.

    Ref: Martin D. Brazeau, “The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins,” Nature, vol. 457 (2009), pp. 305-308

  28. #28 John Scanlon, FCD
    September 3, 2010

    Like many animals assumed to have a homodont dentition, Carcharodon is actually quite heterodont

    Typical mammalocentric terminology. Even if we save ‘hetero-‘ and ‘homo-‘ for fully discrete categories of tooth form (canines, molars etc. – which is almost orthogonal to actual shapes and functions), there are lots of other terms for describing diversity in shape and size along tooth rows.

    Re pineal eyes: I’m dubious whether Sphenodon would have had a recent three-eyed ancestor (named Blinky?); what is pretty clear from squamates is that the pineal eye and foramen are relatively large and obvious in hatchlings and more or less reduced in adults. Also big and obvious in Sphenodon and most iguanians (with generally similar body form etc), more than most other lizards. Maybe this is just the same pattern as the regular eyes, but it might mean the main function occurs during prenatal development. Not that it’s something I’ve looked into much: snakes seem to manage OK without any pineal foramen at all (though colubroids, nested deep within the snake clade, have a pair of tiny parietal foramina in a similar position; function unknown AFAIK). Given that it can be lost, why haven’t more lizards lost it?

  29. #29 David Marjanović
    September 3, 2010

    AAAAAAAAAAAARGH! Placodonts are crown-gnathostomes! :-D

    Parietal eye of Tuatara has a retina.

    Yes, and I explained why: because enough light-sensitive cells together are called “retina”.

    Sensitivity of endocrine organs is not a function of size.

    The sensitivity of sensory organs is of course a function of size.

    And hiding a light-sensitive organ inside the skull is madness -

    Not if the skull is thin and therefore transparent enough. Then it’s actually a good idea, for protection.

    the teeth have no connection with normal vertebrate teeth but are actually the tooth-like micro-spikes that cover the skin adapted to be bigger and sharper.

    Isn’t that the exact same thing?

    Is there, incidentally, a name for the gnathostomatan total group?

    Can’t think of one right now, and don’t have time to check Mikko Haaramo’s phylogeny archive.

  30. #30 Mike Simpson
    September 3, 2010

    “the teeth have no connection with normal vertebrate teeth but are actually the tooth-like micro-spikes that cover the skin adapted to be bigger and sharper.”
    “Isn’t that the exact same thing?”

    Is it? I don’t know anywhere near enough about evolutionary biology.

    The impression I got from the programme was that dentition in sharks – with its endless rows of teeth in a jaw unattached to the skull – had evolved separately and independently from dentition in vertebrates, with our single set of teeth firmly embedded into a part of our skull.

    If it’s true that our own teeth are, if you go back far enough, adapted skin roughness, then it’s even more amazing that I’ve never heard of this before.

  31. #31 David Marjanović
    September 3, 2010

    our single set of teeth firmly embedded into a part of our skull

    Our sets of teeth are hardly more single than those of sharks. Sharks just replace theirs more than once, and they do so much faster than most other vertebrates.

    The parts of the skull that our teeth attach to are bones that sharks simply lack, while our homologues to the jaw cartilages of sharks don’t reach anywhere near our gums.

  32. #32 Allen Hazen
    September 4, 2010

    Andreas Johansson (re comment 25)–
    “Total group gnathostomata” would be… all chordates more closely related to Mus than to Petromyzon (mice>lampreys)? This would probably include a lot of Paleaozoic jawless forms, but just which still isn’t clear (my sense is that the relationships of Paleozoic non-gnathostomes are still a bit hazy, and that even the people who think they know which ones are closest to Lampreys aren’t very confident about it), so at present it probably isn’t a very useful clade to refer to.
    Mikko Haaramo uses “Gnathostomatomorpha” (but in scare quotes, meaning, I guess, that it isn’t a name in official use) for the clade of Gnathostomes+Furcacaudiformes (fork-tailed Thelodonts, thought by some to be the Paleozoic jawless group closest to Gnathostomes).

    In the other direction, Toby White
    http://palaeos.com/Vertebrates/Units/070Chondrichthyes/070.100.html#Eugnathostomata
    uses “Eugnathostomata” for Chondrichthyes+Osteichthyes which (as far as anybody knows(Grin!)) is crown Gnathostomata. (White last updated his cladogram several years ago, back in the days when Acanthodians were often deemed the sister group of Osteichthyes: he has a supposed clade “Teleostomi” comprising Acanthodians+O.)

  33. #33 Andreas Johansson
    September 5, 2010

    Mus > Petromyzon is indeed the group I’m refering to. I’m of the impression it’s likely to include almost all Palaeozoic agnaths.

    “Gnathostomatomorpha” is unfortunately preoccupied by a nematode group (named for the genus Gnathostoma). Or perhaps not so unfortunately, as it’s rather a mouthful!

  34. #34 Jura
    September 6, 2010

    Just finished watching the program online. This was a great episode that really brought to light information on sharks that TV docs have never touched before. I do wish they would have gone a bit more in depth on how white pointers are “warm-blooded,” and I could have lived without them continuing to perpetuate the myth of a creature called “Megalodon” (Carcharocles or Carcharodon. Pick one, but quit omitting the genus name).

    All in all it was very fantastic to watch. The highlight for me would have to be when Joy opened up the brain and did something that no other documentary has done before. Instead of focusing on the small size of the brain, she pointed out how remarkably specialized it is for processing multiple sensory data. I really wish more documentaries (or books/journals/talks) would take this approach when talking about brains in a comparative manner, instead of making useless “who’s smarter” comparisons.

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