Friday, September 08, 2006

Literally, flying lemurs (and not dermopterans)

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 (go here). 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.

Among the 50-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, have been scientifically known since the 1800s, while the third, the Golden-crowned sifaka P. tattersalli (yes, 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.

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 Giraffes: set for change, Giant furry pets of the Incas, and The many babirusa species: laissez-faire lumping under fire again) 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.

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 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.

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 am 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.

Other strepsirrhine primates also seem to slow their leaps by spreading their arms and using skin membranes, including galagos (Charles-Dominique 1977). 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 that this was partly due to the relatively large surface area to body mass ratio they exhibited. 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’ theory 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 apparently small-bodied proficient tree climbers, 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 evolved in the trees, and I’ve argued such in some not particularly good, and much overlooked, articles (Naish 2000a, b).

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.

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. 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.

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 are in the same place and seem to serve the same function, so it seems appropriate to give them this 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.

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. For the latest news on Tetrapod Zoology do go here.

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, 373-385.

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 (two volumes). The Johns Hopkins University Press (Baltimore and London).


Anonymous Anonymous said...

"the ornithologist who should be best known for his work on Neotropical passerines"

Heh heh. That's a great way to say it!

11:12 AM  
Anonymous Anonymous said...

Personally I can't see that a fringe of hair can act as an airfoil. An airfoil generates lift by deflecting air downwards which requires a certain degree of stiffness.
However the hairy fringe can still have an aerodynamic function. Aerodynamic efficiency is measured by L/D "Lift over Drag", and while the hairs can't increase L they can decrease D by smoothing the airstream around the limb.

8:02 PM  
Blogger Darren Naish said...

Response to Tommy... I should have clarified: the hair fringe was supposed by Feduccia to function as the drag-reducing part of the airfoil while the patagium and bony limb spar was thought to be the part generating lift.

12:25 PM  
Blogger Karen McL said...

I think I've seen them *dance* too! And not just Fly.

Can we Rhumba?

9:53 PM  
Anonymous Anonymous said...

I remember something about Propithecus verreauxi (or is it one of the "new" species?) being successfully bred in captivity. Maybe in time there will be enough animals in captivity to make same experiments.

A nice galery of sifaka movies (P. verreauxi) can be found here. Of course, after your post I'm not sure if these are really P. verreauxi.

10:43 PM  
Anonymous Anonymous said...

Watching the sifakas in "Life On Earth" I was impressed (in or before 1985) by the fact that they were apparently obligate bipeds on the ground, and wondered if this was a clue to hominid evolution. I found published tables of data on limb proportions, where it turned out that indriid lemurs are closer to Homo in femur:tibia:pes ratios than any other primates. No primatologist or anthropologist seems to have made anything of this, but I've yet to see anything that would rule out an arboreal leaping stage in (small) hominids that would explain the transition to walking bipedalism (indriids can't do this with their huge divergent hallux, but we grip branches with the instep instead).

5:11 AM  
Blogger Darren Naish said...

Thanks John for your comment - those are interesting observations.

The similarities observed between indriids and hominoids have a history of discussion given that, curiously, bipedal humans share a few features with indriids and other strepsirrhines, including their limb proportions and their low centre of gravity (close to the acetabulum). And both groups practise hindlimb-dominated locomotion and erect trunk postures. So Gunther et al. (1992) titled a paper 'Can prosimian-like leaping be considered a preadaptation to bipedal walking in hominids'. Sarmiento (1998) reviewed this area and provided lots of additional citations.

A very detailed discussion of all the characters involved is provided by Sarmiento (1995). Hominoids exhibit a large number of features that, in other primate groups, correlate with cautious climbing (and I should note that I am a big fan of Sarmiento's argument that ancestral hominoids were cautious climbers). These include dorsally migrated scapulae, a broad thorax, laterally directed humeral glenoids, an increased number of sacral vertebrae, a reduced/absent tail and less fasciculated back musculature. Cautious climbers tend to be folivores with a relatively low metabolism, large body size and long gestation (all of which are correlated).

In contrast, indriids and other primates that employ vertical clinging and leaping differ from cautious climbers (including hominoids) in having a more mobile back, a relatively rigid ankle joint, coordinated muscular action across two or more lower limb joints, and other features: 'As such leaping is non-compatible with the lower limb and body anatomy of cautious climbers', including hominoids (Sarmiento 1995, p. 303).

So while it's true that indriids (and other leaping strepsirrhines) do have a few morphological similarities with hominoids, the body of evidence indicate that our lineage went through a cautious climbing, folivorous phase, and not a leaping indriid-like one. I strongly recommend Sarmiento's papers if you want to read up on this.

Refs - -

Gunther, M. M., Preuschoft, H., Ishida, J. & Nakano, Y. 1992. Can prosimian-like leaping be considered a preadaptation to bipedal walking in hominids? In Matano, S., Tuttle, R. H., Ishida, J. & Goodman, M. (eds) Topics in Primatology. Tokyo University Press, pp. 153-165.

Sarmiento, E. E. 1995. Cautious climbers and folivory: a model of hominoid differentiation. Human Evolution 10, 289-321.

- . 1998. Generalized quadrupeds, committed bipeds, and the shift to open habitats: an evolutionary model of hominid divergence. American Museum Novitates 3250, 1-78.

12:42 PM  

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