Feathers vs Membranes

A recent discussion arose on the Dinosaur Mailing List that included some questions regarding the relative merits of membrane wings and feathered wings, mostly in the context of pterosaurs vs birds. In that spirit, I thought I'd give a little rundown of the relative advantages/costs of each type of vertebrate wing.

Avian Wings
Birds are the only flying vertebrates to use keratinized, dermal projections (i.e. feathers) to form their wings.  Feathers have the distinct advantage of being potentially separate vortex-generating surfaces, meaning that a bird can split its wing up into separate airfoils, thereby greatly changing its lift and drag profile as required (Videler, 2005).  Tip slots are the most obvious example of this mechanism, whereby the tip of the wing is split into several separate wingtips by spreading the primary feathers of the distal wing.  The alula, which lies along the leading edge of a bird’s wing, and is controlled by digit I, is another example of a semi-independent foil unit (Pennycuick, 1989; Videler, 2005).  The splayed primaries of a slotted avian wingtip passively twist nose-down at high angles of attack (and therefore at high lift coefficients), and this feather twist reduces the local angle of attack at the distal end of slotted avian wings, preventing them from stalling (Pennycuick, 2008).  Slotted avian wingtips may therefore be nearly "unstallable", though this does not prevent the overall wing from stalling (Pennycuick, pers comm.).  Feathered wings can also be reduced in span without an accompanying problem of slack and flutter – the feathers that form the contour of the wing simply slide over one another to accommodate the change in surface area.  Despite these advantages, feathers have some costs as wing components, as compared to membranous wings.  Feathered wings are relatively heavy (Prange et al., 1979) and cannot be tensed and stretched like a membrane wing (which has ramifications for cambering). Theoretically, avian wings should not be able to produce maximum lift coefficients as high as an optimized membrane wing (Cunningham, pers comm.), but experimental data to determine if transient, maximum lift coefficients actually differ significantly between bats and birds are not yet available (Hedenstrom et al., 2009).

Chiropteran Wings
Bats have a wing surface formed primarily by a membrane stretched across the hand, antebrachium, brachium, and body down to the ankle.  Unlike birds, which have a limited number of muscles that produce the flapping stroke (two, primarily: m. pectoralis minor and m. pectoralis major), bats have as many as 17 muscles involved in the flight stroke (Hermanson and Altenbach, 1983; Neuweiler, 2000; Hedenstrom et al., 2009).  The membranous wings of bats are expected to have a steeper lift slope than the stiffer, less compliant wings of birds (Song et al., 2008).  This results from the passive cambering under aerodynamic load that occurs in a compliant wing: as lift force increases, the wing passively stretches and bows upwards, producing more camber, and thereby further increasing the lift coefficient and total lift.  While there are some advantages for a flying animal in having such a passive system, bats presumably must mediate this effect with the many small muscles (and fingers) in their wings – tensing the wings actively while under fluid load will mediate the amount of camber that develops.  This would be important to mediate drag and stall, though no empirical data currently exist to indicate exactly how bats respond to passive cambering.  The work by Song et al. (2008) also indicates that compliant, membrane wings achieve greater maximum lift coefficients than rigid wings, but data have yet to be collected demonstrating that this holds in vivo for bats and birds.  Compared to birds, the distal wing spar in bats is quite compliant (Swartz and Middleton, 2008).

Pterosaur Wings
The structure and efficiency of pterosaur wings is obviously not known in as much detail as those of birds or bats, for the simple reason that no living representatives of pterosaurs are available for study.  However, soft tissue preservation in pterosaurs does give some critical information about their wing morphology, and the overall shape and structure of the wing can be used (along with first principles from aerodynamics) to estimate efficiency and performance.

It is known from specimens preserving soft tissue impressions that pterosaur wings were soft tissue structures, apparently composed of skin, muscle, and stiffening fibers called actinofibrils, though the exact nature and structure of actinofibrils has been the topic of much debate (Wellnhofer 1987; Pennycuick 1988; Padian and Rayner 1993; Bennett 2000; Peters 2002; Tischlinger and Frey 2002).  Associated vasculature is also visible in some specimens, especially with UV illumination (Tischlinger and Frey, 2002).  Recent work on the holotype of Jeholopterus ningchengensis (IVPPV12705) seems to confirm that the actinofibrils were stiffening fibers, imbedded within the wing, with multiple layers (Kellner et al., 2009).  The actinofibrils were longer and more organized in the distal part of pterosaur wings than in the proximal portion of the wing, which may have implications for the compliance of the wing going from distal to more proximal sections.  The inboard portion of the wing (proximal to the elbow) is called the mesopatatgium, and was typified by a small number of actinofibrils with lower organization, which would have made this part of the wing more compliant than the outboard wing.

The outer portion of the wing, which was likely less compliant the mesopatagium, is termed the actinopatagium (Kellner et al., 2009).   Because pterosaurs had membrane wings, they could presumably generate high lift coefficients, but exactly how high depends on certain assumptions regarding their material properties and morphology (pteroid mobility and membrane shape being two of these factors).

Now, for some punchlines...
Based on the structural information above, we might expect the following regarding pterosaurs and birds:

- Pterosaurs would have a base advantage in terms of maneuverability and slow flight competency.

- Pterosaurs would also have had an advantage in terms of soaring capability and efficiency

- Pterosaurs would have been better suited to the evolution of large sizes (though this was affected more by differences in takeoff - see earlier posts about pterosaur launch).

- Birds will perform a bit better as mid-sized, broad-winged morphs (because they can use slotted wing tips and span reduction).

- Birds would have an advantage in steep climb-out after takeoff at small body sizes (because they can work with shorter wings and engage them earlier).  This might pre-dispose them to burst launch morphologies/ecologies.

Interestingly enough, the fossil record as we currently know it seems to back up all of these expectations.  For example, the only vertebrates that seem to have been adapted to dedicated sustained aerial hawking in the Mesozoic were the anurognathid pterosaurs.  Large soaring morphs in the Mesozoic were dominated by pterosaurs, also.  On the other hand, mid-sized arboreal forms in the Cretaceous were largely avian.

Full references for all of the above literature is available upon request.  I'll post the full refs here as soon as I have a chance, but just email me in the meantime if need be (currently traveling in Boston).

The Strength of Color

Had a great extended dinner meeting with a friend and collaborator this evening to get a project rolling on the micromechanics of feathers.  One of the key features will be sorting out how pigments and structural colors affect the mechanical properties of feathers.  It's well documented that some pigments (melanins, particularly) strengthen feathers - but we don't know yet how much, by exactly what mechanism, and the relative effects on performance.  Other pigments probably also have an impact, but that's even more mysterious. 

Why do we care how feathers work?  Well, as a biologist with a strong interest in the evolution of flight in birds, I obviously have a personal stake in knowing more about feather mechanics.  But here are some traits of feathers that might make them interesting models for those with a more applied interest:

- Feathers have a high strength to mass ratio (particularly with regards to bending)
- Feathers are abrasion resistant
- Feathers are good thermal insulators
- Feathers are fast to replace - they are manufactured quickly with precision
- Feathers absorb impacts well
- Feathers are water resistant
- Feathers have notable aerodynamic properties (duh)

That's a rather solid set of attributes for a single biological structure.  With growing interest in biomaterials, we expect that feathers might hold some very intriguing clues about efficient material use and pigment effects.  Here's hoping!

Microraptor: Odds and Ends

The top image on the left is from Hone et al. (2010) and shows the holotype of Microraptor gui under UV light.  The image below, by Mick Ellison, shows a life restoration of Microraptor, and was taken from here (note: the hindlimbs could not actually get into the position shown in the image; that was done to show off all of the airfoils at once for comparative purposes).   One of the key questions regarding flight in Microraptor is whether it evolved flight independently of avialans, or if it represents a morphology that was a more direct precursor to flight in birds proper.

One thing I noticed a few years back is that it seems that Microraptor had a different set of "solutions" to the problem of aero control, as compared to living birds.  I have since put some math to it, and the calculus bears out the intuition.  Myself, Justin Hall, David Hone, and Luis Chiappe are writing this up now (see earlier cryptic blog post), but Justin has given a couple of talks on the hindwing use recently and some of you out there know that that I have been murmuring about the tail being used in aero control.  All will be revealed in the full manuscript (WFTP moment) but I do think it is quite interesting that the aero control surfaces in Microraptor took advantage of pre-existing maniraptoran anatomy.  In other words, you don't have to do much to your average dromaeosaurid to get it into the air.

This is a potentially critical observation.  For one, it suggests that the origin of flight in dinosaurs may have been more simple than previously supposed.  It also suggests that flight control may have had more to do with the gains and losses of aerodynamically active morphology we see near the origin of birds than simple weight support.  I am sad to say that most paleontologists don't seem to have a particularly good grip on what lift actually is, how it is used, and how it is generated.  Many of my colleagues also seem to struggle with how drag fits into the whole scheme.  Of course, I have lots of gaps in my knowledge, too, so I can't go pointing fingers.  Nonetheless, I suspect that we are going to see a major overhaul of the models for dinosaur flight evolution in the year or two.

The Ellison image is associated with a recent paper by Li et al. (2012) in Science.  The authors favor display characteristics for some of the feathered morphology, particularly the tail fan.  I don't discount this function at all, but it should be noted that it doesn't take much to provide a decent stabilizer or control surface for a mid-sized flying animal, and display surfaces don't have to be aerodynamically useless or costly.  (Just to shore a common myth, that is not the same as saying that tail fans, crests, flaps, etc would act as rudders on flying animals.  As a general rule, rudder use does not work well for a non-fixed wing flyer.  Even fixed-wing aircraft do not initiate turns by using rudders; the rudder systems are for stabilization).

References
Hone DWE, Tischlinger H, Xu X, Zhang F (2010) The Extent of the Preserved Feathers on the Four-Winged Dinosaur Microraptor gui under Ultraviolet Light. PLoS ONE 5(2): e9223. doi:10.1371/journal.pone.0009223


Li Q, Gao KQ, Meng Q, Clarke JA, Shawkey MD, D'Alba L, Pei R, Ellison M, Norell MA, Vinther J. 2012. Reconstruction of Microraptor and the Evolution of Iridescent Plumage. Science 335 (6073): 1215-1219

Munich Archaeopteryx

Perhaps the most iconic fossil of a (potentially) flying animal is Archaeopteryx.  Debates on the flight ability of Archaeopteryx abound in the literature.  One of the more recent investigations of this issue considered feather strength, which is an interesting approach, but may suffer from significant error is feather measurements or body mass estimates are imprecise.  I take my own approach to the problem, which is to look at the bending strength of the bones, rather than the feathers.  I've done this for a wide range of living birds, but only a couple of specimens of Archaeopteryx, which is why I have yet to formally publish the results (though I have given a conference presentation on them at SVP).  One of the specimens I have data for is the Munich Archaeopteryx, shown in the photo at left.  It's not the best photo, but I managed to grab it quickly while measuring the specimen at the BSPG in Munich, Germany.  Regardless of the ultimate flight status of Archaeopteryx, working with a specimen of this historical importance was a real treat.  My special thanks goes out to David Hone, who organized the meeting where I examined the specimen.

I will be writing more on Archaeopteryx and other species relevant to the origin of birds in the coming months.  I have quite a few posts lined up on the topic; some more quantitative than others.  For now, however, it is back to my teaching duties, so today's installment is necessarily brief.

Giant, Feathered Tyrannosaur

Alright, it doesn't fly, but this is relevant to the evolution of feathers and, more importantly, is sheer awesome in fossil form.  The embargo on this literally ended 14 minutes ago.  It is hot off the press.

A giant, feather dinosaur from the Lower Cretaceous of China

Also a blog description over at Archosaur Musings here.