Tetrapod Zoology

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I’m away right now, and haven’t had time to prepare new stuff. So, here’s something from the archives again: by which I mean, something written in 2006. It’s still pretty interesting (in my humble opinion), but I would definitely do some things differently were I to re-write it today [gliding sifaka below from Demes et al. (1991): read on].

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Mention ‘flying primate’ and most zoologists will think you’re referring to the well known, controversial theory of John Pettigrew of the University of Queensland. And if that sentence sounds familiar, it’s because I used it previously to introduce a post all about Pettigrew’s controversial theory that megabats are not close relatives of microbats, but are instead close relatives of us primates. As reviewed in that post, currently the data does not favour the idea that the two bat groups evolved independently, and the ‘flying primate’ theory has not won widespread acceptance. The term ‘flying primate’ might be better attached however to another group of mammals, and this time they really are undeniable primates. They are lemurs, and they fly. Well… fly sort of.

And, no, I am not talking about the flying lemurs, aka colugos, aka dermopterans: they aren’t primates, though they are close relatives.

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Of the 50-odd 100-odd living lemur species, among the most charismatic and distinctive are the sifakas or simponas, a group of relatively large, long-tailed arboreal indriids. If you’re wondering, ‘sifaka’ is an onomatopoetic reference to their alarm call, and is pronounced ‘shee-fak’ (or something similar if you use your imagination). With tail, they get to about 1 m long, and they weigh up to 7 kg. Most sources will tell you there are three species – two of which, the Diademed sifaka Propithecus diadema and Verreaux’s sifaka P. verreauxi [shown here], have been scientifically known since the 1800s, while the third, the Golden-crowned sifaka P. tattersalli (named after primatologist Ian Tattersall), wasn’t named until 1988. The latter is one of several lemur species that have been named very recently. They include Cleese’s woolly lemur Avahi cleesei, Seal’s sportive lemur Lepilemur seali, the Mitsinjo sportive lemur L. mitsinjonensis, Goodman’s mouse lemur Microcebus lehilahytsara and the Northern giant mouse lemur Mirza zaza, all named in 2005, and Mittermeier’s mouse lemur Microcebus mittermeieri, Jolly’s mouse lemur M. jollyae, Simmons’ mouse lemur M. simmonsi, and the new sportive lemurs Lepilemur sahamalazensis, L. aeeclis and L. randrionasoli, all named in 2006 [UPDATE: please remember that this article was written in 2006! Many new lemurs have been named more recently].

However, several taxa conventionally regarded as Diademed and Verreaux’s sifaka subspecies are extremely distinct, and in view of my previous comments on ‘unlumping’ (see Giant furry pets of the Incas and Laissez-faire lumping under fire) you probably won’t be surprised to learn that some mammalogists now recognize these ‘subspecies’ as valid species. Of the forms previously included within P. diadema, Milne-Edward’s sifaka P. edwardsi, the Silky sifaka P. candidus and Perrier’s sifaka P. perrieri are now regarded by some as distinct species, and among those taxa previously included within P. verreauxi, we now have Coquerel’s sifaka P. coquereli, the Crowned sifaka P. coronatus and Decken’s sifaka P. deckeni raised to species level by some primatologists. Taxonomic revisions have thus upped the number of sifaka species from three to nine.

Actually, there may be a few more. A population discovered at Tsinjoarivo in 1999, originally thought referable to P. diadema, is morphologically distinctive and might represent a new species. Known informally as the Tsinjoarivo sifaka, it is small, with distinctive black patches on its limbs, and with duller yellow-orange on its limbs, and less white facial hair, than definite P. diadema.

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Sifakas are what is known as ‘arboreal clingers and leapers’, a locomotor category first identified by Napier & Walker (1967). Climbing mostly on vertical trunks, including those of the horrendously spiky Didiereaceae trees, sifakas are able to propel themselves with their long and powerful hindlimbs for considerable distances: up to 10 m and perhaps more in cases. As they leap, they extend their arms forwards and outwards, and flaps of furry skin extend around their arms. Most people interested in animals know this because they’ve seen it depicted on TV, most memorably perhaps in episode 12 (‘A Life in the Trees’) of Attenborough’s BBC series Life on Earth (funnily enough, previously mentioned in The Cultured Ape and Attenborough on gorillas). The comical prancing behaviour that sifakas employ when on the ground [shown below] is also often featured on TV documentaries. Anyway, the flaps of skin that extend as a sifaka jumps appear to function in gliding, and indeed the entire arm seems to function as an airfoil. They are gliding primates.

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You might be surprised to learn that there is an extensive literature discussing the apparent gliding behaviour of lemurs and other primates, much of it reviewed in Demes et al.’s 1991 paper ‘They seem to glide’. Demes and colleagues were quoting J. J. Petter’s 1962 article in which Petter noted of indris* that “Pendant le saut leur corps est parfaitement horizontal et ils semblent planer”. In fact, suggestions that the extendable skin around the arms of indriids might have an aerodynamic function can be traced back to French explorer Alfred Grandidier who thought as much in 1875. Grandidier was among the first to properly study and document Madagascan wildlife, publishing (with A. Milne-Edwards) his observations in the 32-volume Histoire Physique, Naturelle, et Politique de Madagascar.

* The Indri Indri indri is of course not a sifaka, but it is a close relative, and a large one given that it reaches 70 cm in total length and 7.5 kg. Unlike sifakas it has only a vestigial tail, but like sifakas it adopts a spread-eagle position when leaping.

Most popular and semi-technical works on primates fail to mention any of this stuff, however, which amazes me given that it’s rather interesting to say the least. I’m happy to report that Nowak (1999, p. 527), at least, says of sifakas “the short arms are limited in their movement by small gliding membranes”. This is the sixth edition of Walker’s Mammals of the World: I checked the fourth edition (1983), which I also own, and this also contains the same line.

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Other strepsirrhine primates also seem to slow their leaps by spreading their arms and using skin membranes, including galagos (Charles-Dominique 1977) [Galago elegantulus in ‘gliding descent’, from Demes et al. (1991)].

So to test the idea that these leaping primates might really be enjoying an aerodynamic effect from their arms and associated membranes, Demes et al. (1991) estimated the effects of lift and drag on these primates based on velocity at takeoff, body mass, surface area and other variables. They found that aerodynamic lift and drag could significantly affect the flight path of leaping indriids, and also concluded that this was due (in part) to the relatively large surface area to body mass ratio exhibited by these primates. This large surface area comes predominantly from the skin membranes. However, they weren’t able to go beyond theory and do anything practical like wind-tunnel tests, mostly because there aren’t that many spare sifakas kicking around for use in laboratory tests. Indeed the species involved here are endangered and protected.

As hinted at by the fact that it’s not much mentioned in the books, the supposed gliding habits of sifakas and other primates are not as well known among mammalogists as they might be. In fact, these habits have been most widely brought to attention in the literature on bird origins. Rightly or wrongly, the debate over avian origins has long been dichotomized into a ‘ground up’ school, and a ‘trees down’ school. It is absolutely wrong to argue – as some workers have – that the ‘trees down’ hypothesis is at odds with the very robust and well supported body of evidence showing that birds are theropod dinosaurs, given that basal birds, and the theropods closest to birds, were small-bodied animals almost certainly capable of at least occasional tree climbing, and not big cursorial Deinonychus-like predators as some would have it. If small, scampering scansorial predators were the ancestors of birds, I find the evidence to better support the idea that flight involved at least a bit of tree-climbing, and I’ve argued such in some not particularly good, and much overlooked, articles (Naish 2000a, b).

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What have gliding lemurs got to do with all this, I hear you ask. Alan Feduccia, the ornithologist who should be best known for his work on Neotropical passerines but is unfortunately far better known for his various attempts to poke holes in the bird-dinosaur theory, has repeatedly used sifakas and other gliding primates as models for the early stages in the development of avian flight (Feduccia 1993, 1995, 1996, Geist & Feduccia 2000). In other words, Feduccia proposed that sifakas might serve as an analogy illustrating how feathers and flight might have evolved from leaping arboreal prototypes [leaping sifaka image, and close-up of sifaka arm hair, from Feduccia (1993)].

Hold on: feathers? Well, Feduccia not only drew attention to the presence and role of the skin membranes in sifakas, he also discussed the presence of a thick, posteriorly projecting mat of hair on the sifaka forearm [see image above, from Feduccia (1993)]. In some specimens this mat provides c. 64% of the total width of the combined forearm + mat surface, and during leaping it appears to form the trailing edge of what is effectively an airfoil (the stiff leading edge of which is formed by the bony forearm and its associated membrane). The hair mat, Feduccia suggested, might give us an insight into how enlarged scales on the trailing edge of a proto-bird’s arm might, by incremental enlargement as they became increasing feather-like, have provided an aerodynamic advantage. Feduccia (1993, p. 162) stated that “there can be no doubt that an airfoil is produced by the sifaka’s arms and the partial incorporation of a “lift mechanism” would advantageously augment the horizontal extent of a “leap””. The current data from theropods shows that quill-like integumentary structures were present in theropods before one lineage gave rise to scansorial proto-birds. Furthermore, there are reasons for thinking that proto-birds were flapping their wings from the start, and it’s debatable as to whether or not they ever went through a leaping and gliding phase. Even so, with their arboreal behaviour, skin membranes and specialized brachial integument, sifakas might still be informative.

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In birds, bats and other volant tetrapods, the skin membranes that function in flight are termed patagia. The membrane that extends along the leading edge of the arm (usually from the shoulder to the wrist) is the propatagium while that connecting the trailing edge of the upper arm to the body is the plagiopatagium. While the extendable flaps of indriids and some other primates are proportionally smaller than the patagia of most gliding and flying tetrapods, they’re in the same place and seem to serve the same function. It therefore seems appropriate to give them the same name. Some workers have done this: Charles-Dominique (1977) likened the skin membranes of galagos to incipient patagia, and Feduccia (1993) used the term patagium in connection with sifakas [image above, from Demes et al. (1991), shows the patagia in a sifaka, with the extent of the fur shown in grey around the body].

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Now, even without all this stuff on patagia, gliding behaviour and bird origin theories, sifakas are pretty cool and interesting mammals. But I still can’t help thinking that the gliding behaviour makes them particularly interesting, and I’m therefore surprised that more isn’t made of it. From the point of view of the big picture, it perhaps has significance in suggesting that gliding, or proto-flight or whatever, is actually reasonably easy to evolve, even in relatively large animals. Given that most mammals have flexible skin extending from the upper arm to the body that might provide drag and/or lift in leaping, it’s even conceivable that more mammals ‘seem to glide’ than we presently acknowledge. Indeed there are anecdotal accounts of semi-gliding, or parachuting, in such things as palm civets. Among primates, Feduccia (1996) and Geist & Feduccia (2000) also pointed to gliding behaviour in the sakis (Pithecia), a group of frugivorous South American monkeys that can reportedly “maneuver accurately while airborne to a target tree trunk, often adjusting their bodies so that they glide upwards at a steep angle just before contact” (Geist & Feduccia 2000, p. 668-669) [The accompanying photo, taken from Graeme Elliott’s flickr site, depicts a White-faced saki P. pithecia].

So – getting back to sifakas and other lemurs – I think it’s not just that they ‘seem to glide’. It seems that they really do. There’s something else really neat I wanted to say about sifakas: the fact that they’re transitional creatures, caught in the middle of an evolutionary change that they’re struggling to adapt to. It’s a story that involves the extinction of other lemurs, giant fossas and eagles, and a social system that has yet to be properly ironed out. But it’ll have to wait to another time.

Primates haven’t been much featured on Tet Zoo – they’re just one other of those groups I’ve never gotten round to focusing on, yet – but do check out…

Refs – –

Charles-Dominique, P. 1977. Ecology and Behaviour of Nocturnal Primates. Duckworth (London).

Demes B, Forchap E, & Herwig H (1991). They seem to glide. Are there aerodynamic effects in leaping prosimian primates? Zeitschrift fur Morphologie und Anthropologie, 78 (3), 373-85 PMID: 1909482

Feduccia, A. 1993. Aerodynamic model for the early evolution of feathers provided by Propithecus (Primates, Lemuridae). Journal of Theoretical Biology 160, 159-164.

– . 1995. The aerodynamic model for the evolution of feathers and feather misinterpretation. Courier Forschunginstitut Senckenberg 181, 65-77.

– . 1996. The Origin and Evolution of Birds. Yale University Press (New Haven & London).

Geist, N. R. & Feduccia, A. 2000. Gravity-defying behaviors: identifying models for Protoaves. American Zoologist 40, 664-675.

Naish, D. 2000. Theropod dinosaurs in the trees: a historical review of arboreal habits amongst nonavian theropods. Archaeopteryx 18, 35-41.

– . 2000. 130 years of tree-climbing dinosaurs: Archaeopteryx, ‘arbrosaurs’ and the origin of avian flight. The Quarterly Journal of the Dinosaur Society 4 (1), 20-23.

Napier, J. & Walker, A. C. 1967. Vertical clinging and leaping – a newly recognized category of locomotor behaviour of primates. Folia Primatologica 6, 204-219.

Nowak, R. M. 1999. Walker’s Mammals of the World, Sixth Edition. The Johns Hopkins University Press (Baltimore and London).

Comments

  1. #1 Brian
    August 12, 2010

    Really interesting article! The image of a saki or a palm civet jumping and steering in mid-‘flight’ is a very odd one, I must say.

  2. #2 Raka
    August 12, 2010

    “transitional creatures, caught in the middle of an evolutionary change that they’re struggling to adapt to”

    That’s… poetic, but seems awfully evocative of the all-too-common “ladder of evolution” misconception.

  3. #3 Paul from NH
    August 12, 2010

    Either fix the URL or republish this in December… Right now, it says /12/ instead of /08/.

    Anyway, very cool article! The feather-hairs were particularly interesting. It makes me wonder, though… if we were to show one of these guys to a YEC, would they identify it as being a transitional animal, or just clearly part of the Lemur Kind? ;-)

  4. #4 Paul from NH
    August 12, 2010

    Sorry, I meant that the “more” link from the main page says “/12/”, not the actual URL of this post.

  5. #5 Alan
    August 12, 2010

    There is a tiny captive population of P.coronatus in Europe. For those who want to see these amazing primates, ISIS lists them as being held at the following zoos:

    Apeldoorn (3)(Netherlands)
    Belfast (4)
    Besancon (2)(France)
    Cotswold Wildlife Park (3)
    Port Lympne (2)
    Mulhouse (1))(France)

  6. #6 Mike from Ottawa
    August 12, 2010

    Off-topic, but I reckon if anyone knows it will be Darren or one of the usual erudite (i.e. not me) commenters here:

    Jerry Coyne, at his blog Why Evolution is True, remarked “We find a plate of rotten meat repulsive, but to a vulture it’s the equivalent of an ice cream sundae.”

    and I wondered, has anybody studied whether vultures prefer rotten meat to fresh given the choice?

  7. #7 derek
    August 12, 2010

    I’m not an expert, but I wouldn’t have thought vultures would have much opportunity to develop a taste for rotten meat. That would imply meat that had lain within sight of vultures, and also within reach of the land animals that a vulture is competing with from the air, for long enough to go rotten. My impression is that the meat eaten by vultures is all too fresh.

  8. #8 CS Shelton
    August 12, 2010

    SAKI MONKEY! Spot the saki monkey in my girlfriend’s painting:

    http://borfy.com/Paint_Summoner.html

    Hint: She’d seen a few pics but never one in scale, and did very little research, so it is depicted way larger than the real animal. She just liked the impression they give of being thoughtful and morose.

    I love sifakas! In the USA, they’re probably most famous for being in the children’s show “Zoobamafoo.” I had no idea they were gliders, but also of interest to me: No idea they were related to indris. So cool!

    Was it Tet Zoo where I learned that natives thought of indris as related to man? No, maybe an Aron-Ra video. I like that anecdote, because it fits with my view that common descent is brilliantly obvious enough to be arrived at by anyone paying attention.

  9. #9 Kilian Hekhuis
    August 13, 2010

    “It’s a story that involves the extinction of other lemurs, giant fossas and eagles, and a social system that has yet to be properly ironed out. But it’ll have to wait to another time.”

    Love to hear more about that, any chance it’ll be coming at all?

  10. #10 Jerzy
    August 13, 2010

    Sakis are, unlike sifakas, common in zoos. I wonder why nobody studied their gliding abilities closer?

  11. #11 Jerzy
    August 13, 2010

    About origin of flight in birds, I think, flight might have evolved first among juveniles, which had better surface to mass ratio. Parallel are some birds like Giant Coot or Steamer Ducks, which can fly as juveniles but become flightless later.

  12. #12 Jerzy
    August 13, 2010

    Re: vultures prefer fresh meat.

    Actually, I remember a hiking trip when a girl observed particularily magnificent ‘eagles’. She was shocked when i told hear that ‘eagles’ were in fact Griffon Vultures. And then, that carrion they eat is much fresher that the packaged dried meat and soybean chops which we were munching on. I wouldn’t mind a juicy chunk of young ibex then.

  13. #13 Bill
    August 13, 2010

    Depends on whether the vultures find meat by scent (new world) or sight (old world). I’m not sure but new world vultures have pretty thin beaks (generally) and so might prefer meat a little deliquescent to allow better handling – and if they scented it out then it would be pretty rotten anyway so there might not be selection for big tough, fresh flesh ripping beaks. Old world ones seem to rely on big-beaked ones like lappet-faced vultures to rip open carcasses, so again rotten meat may be easier to handle generally for them. Having said that, captive vultures (new wordl and old) will eat ‘fresh’ small pieces of meat, so it is probably nothing to do with taste. Birds have pretty few taste buds anyway don’t they?

  14. #14 CS Shelton
    August 14, 2010

    I checked my girlfriend’s web stats and my posting a link here caused about as much of a spike as her posting one to her modest list of facebook friends, despite there being far more visitors here than there. So incurious! It was at least as closely related to the topic as vulture taste.

    BTW, with the senses of taste and smell being closely related in mammals, assuming dinosaurs are similar on that front (I know, naughty), we can suppose new world vultures would have a sense of what they’re eating. Yuck.

    The scent of death is stronger than the scent of life and therefore a lure to scavengers, so one might imagine they’d find putrefaction tasty as well. Does anyone know of anything more substantial than speculation and anecdotes on this one?

    In visiting Kansas I noted dozens more turkey vultures roadside than I’d ever see here (Washington), but also hundreds less crows. Interesting to see such a visible show of the effects of competition. As crows have increased in population in recent decades, have turkey vultures decreased?

  15. #15 Dartian
    August 16, 2010

    Regarding the gliding capabilities of sifakas: These prosimians are about three times heavier (i.e., 6-7 kg) than the largest gliding mammals with well-developed patagia (that is, colugos, giant flying squirrels, and the Australian greater glider, which all reach maximal body weights of about 1.5-2 kg). This seems to suggest that the sifakas are above the body size threshold for being highly specialised glider/parachuters, and that were the sifakas to conquer Madagascar’s empty ‘colugo niche’ they would need to evolve a smaller body size.

  16. #16 CS Shelton
    August 16, 2010

    Dartian- It is suggestive and may well be right, but isn’t necessarily so. Maximal weights for avian flight are often suggested and seem to be refuted by the fossil evidence in the form of teratorns. Ditto pterosaurs, with large ones getting “OK, this time it really IS the largest ever” for years.

    And some humans (insane insane humans) glide with very small artificial patagia for sport. They seem to work well despite our weight.

  17. #17 Dartian
    August 17, 2010

    CS:

    It is suggestive and may well be right, but isn’t necessarily so. Maximal weights for avian flight are often suggested and seem to be refuted by the fossil evidence in the form of teratorns. Ditto pterosaurs, with large ones getting “OK, this time it really IS the largest ever” for years.

    I did have that in mind when I wrote my earlier comment, and it is of course possible that the currently existing morphological diversity of animals may not be representative. Still, if there are extinct mammalian gliders* that are substantially larger than the extant ones in the fossil record, it is a bit surprising that we haven’t found any evidence of them yet (at least as far as I know; I’ll be happy to stand corrected on this issue).

    * Incidentally, the largest known mammalian flyers, i.e., the largest pteropodid bats, may reach weights of about 1.5 kg, which puts them in the same general size class as those largest mammalian gliders.

  18. #18 CS Shelton
    August 17, 2010

    I thought of mentioning mammals but I didn’t because you’re right. Could be the mechanisms of mammalian flight (or gliding) don’t work well above a certain size. Indeed, maybe teratorns rep the upper limit for birds, which is quite a lot smaller than the upper limit of pterosaurs and so on. It’s just really hard to know any of that.

  19. #19 Bob Gotschall
    August 18, 2010

    Thanks for the article on flying lemurs. News to me.

    As to evolution of birds, the most parsimonious explanation for me is that they are descended from cursorial feathered theropods. And yes last I heard Dr. Feduccia doesn’t like the idea of feathered theropods much. Yes they could have become arboreals, but at the end of the day all living birds that can fly can take off from the ground and most of them are once again cursorial bipeds. So even if we are talking about reversing evolution, they still had to evolve to take off from the ground right? What did climbing in trees gain them?

    bob

  20. #20 biologion
    August 24, 2010

    Pretty cool article. Gliding mammals are very interesting and unique. It’s quite amazing how a large animal like the sifakas that you’ve mentioned is able to glide. Especially when the patagium is not fully developed, as in flying squirrels for example. The reasons why a mammal would become a gliding one and moreover the context in which this procedure took place are very interesting.

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