The growing knowledge of tetrapod flight

So why did flight evolve? While flying does have its disadvantages, such as high energy use, it has many advantages as well. Flying animals can cover far greater distances than flightless ones and can also more easily pass over geographical barriers such as valleys, highlands and bodies of water. Flying animals can also reach environments that flightless animals might find hard to reach such as islands and treetops, and this could allow flyers to find safer areas to rest or reproduce. Furthermore, getting away from predators is easier when one can just take to the air. All of these factors likely helped promote the evolution of flight in pterosaurs, flying dinosaurs, and bats alike (Witton, 2013).

Figure 1: A couple of anachronistic friends. A Darwinopterus- a pterosaur from the Jurassic, and a European robin- a dinosaur from the Quaternary.  Artist: Mark Witton.

New discoveries are constantly expanding our knowledge of tetrapod flight. Just a few weeks ago, an incredible new winged dinosaur was discovered. Yi was a scansoriopterygid that lived in China around 160 million years ago. Each of its hands had an extremely long third finger as well as a strange long styliform that grew from the wrist. These may have supported a wing membrane, as evidenced by fossilised membranous tissue found in the wrist area. While Yi may not have been capable of true flight, it is still an interesting example of how maniraptoran dinosaurs tried out more than just one wing design (Padian, 2015). Some classify scansoriopterygids as basal avialans (Martyniuk, 2012). Others classify them as more primitive non-avialan maniraptorans (Paul, 2010).

Figure 2: Yi, a membrane winged scansoriopterygid. While it may not have been capable of true flight, perhaps it could flutter.  Artist: Emily Willoughby.

Research has also helped destroy old prejudices about pterosaurs and bats. Once thought to be poor flyers, pterosaurs are now known to have actually been the most effective flying animals ever, with amazingly efficient wings and launching capabilities (Witton, 2013). Bats too, often overshadowed by birds, have been shown to be quite successful and diverse, indeed some of the most diverse of all mammals (Altringham, 2011).

Figure 3: Representatives of each flying tetrapod group flying together with an airplane- a machine invented by some upright apes who wanted to fly too.  Artist: Matteo Bachin.

What does the future hold? Will any other tetrapod group ever evolve flight many millions of years from now? Who knows. Only time will tell.

References
Altringham, J. D. (2011). Bats: From Evolution to Conservation. Oxford University Press: Oxford.
Martyniuk, M. P. (2012). A Field Guide to Mesozoic Birds and Other Winged Dinosaurs. Pan Aves: Vernon, New Jersey.
Padian, K. (2015). Dinosaur up in the air. Nature. 521 (7550), pp. 40-41.
Paul, G. S. (2010). Dinosaurs: A Field Guide. A & C Black Publishers Ltd: London.
Witton, M. P. (2013). Pterosaurs. Princeton University Press: Princeton, New Jersey.

Image sources
Figure 1: Accessed May 26, 2015, from: https://blogger.googleusercontent.com/img/b/R29vZ2xl/AVvXsEhVXAWWt6i-CAOhAYeIKbrpa3Ei9ROTbEWGg1LxKfhN5j8YXUWFiKYanExv6iB8rc1BVAq9Mw2wsICHsbVLe-Mt2mydTLnm4dp7sfgZwkc9RD8UP-WmkL4lHKirrF47pJq4gC7CEtGJgpw/s1600/Darwinopterus+and+Robin+Witton.png
Figure 2: Accessed May 26, 2015, from: http://upload.wikimedia.org/wikipedia/commons/5/56/Yi_qi_restoration.jpg
Figure 3: Accessed May 26, 2015, from: http://pterosauria.weebly.com/uploads/2/2/0/7/2207195/189247.jpg?595

Bat diversity

While bats never reached as great a level of diversity as pterosaurs and birds, they are nevertheless quite diverse. Today bats are the second largest group of mammals, with more than 1100 known living species. The largest group, rodents, have more than twice as many species, but they are less biologically diverse than the bats (Altringham, 2011).

Bats are divided into two groups- the microbats and the megabats. The microbats are the more original bats, while megabats are a younger group with the oldest known megabat, Archaeopteropus, living around 35 million years ago. The names "microbat" and "megabat" are somewhat misleading as there do exist big microbats and small megabats. The real differences in the groups are features such as the more elongated, dog-like, faces of the megabats and the fact that most megabats have lost their echolocation abilities (Altringham, 2011).

Figure 1: A blossom bat pollinates a flower. Despite its small size, this is actually a megabat, showing that size is not the defining feature of the two bat groups.  Photographer: Mike Trenerry.

While most bats have retained the insectivore lifestyle of their ancestors, there are many who have exploited other niches. The megabats and some microbats have become frugivores and nectarivores. There are also bats who have evolved a fishing lifestyle, such as Latin America's bulldog bats, who use echolocation to detect the ripples caused by fish near the surface of rivers and ponds. There are also a number of predatory bats, such as the false vampire bats and the frog eating bats (Levy, 1999).

Figure 2: A bulldog bat catches a tasty fish.  Photographer: J. Scott Altenbach.

There are even a few bats who evolved to feed on blood. Namely Latin America's vampire bats. As well as the standard echolocation ability, vampire bats also possess two heat sensing pits in their face, to help seek out warm blood vessels near their prey's skin surface. Their razor-sharp triangular teeth shave away overlying tissue and nick the blood vessel and special anticoagulants in their saliva keeps the blood flowing (Levy, 1999).

Figure 3: A vampire bat shows off the tools of the trade- razor-sharp triangular teeth for nicking blood vessels.  Photographers: Michael Fogden & Particia Corbis.

While no bat ever became flightless, New Zealand's lesser short-tailed bat spends much of its time down on the ground, foraging for insects, berries and nectar on the forest floor. Unlike other bats its wings are not attached to the hindlimbs, so it can move about on the ground more easily than other bats can (Fitter, 2009).

Figure 4: A lesser short-tail bat foraging around in a New Zealand forest.  Photographer: Rod Morris.

Next shall be this blog's conclusion.

References
Altringham, J. D. (2011). Bats: From Evolution to Conservation. Oxford University Press: Oxford.
Fitter, J. (2009). New Zealand Wildlife. Bradt Travel Guides Ltd: England.
Levy, C. K. (1999). Evolutionary Wars: A Three-Billion-Year Arms Race. W. H. Freeman and Company: New York.

Image sources
Figure 1: Accessed May 19, 2015, from: http://www.wettropics.gov.au/site/resized/80-08082012022826-0-119-990-389-990x389-cropped-mtlittleblossombat2.jpg
Figure 2: Accessed May 19, 2015, from: http://www.vnews.com/csp/mediapool/sites/dt.common.streams.StreamServer.cls?STREAMOID=H_kR6yEGutZtjodlwCi2aM$daE2N3K4ZzOUsqbU5sYv$HB5zCCfOaoycRvYQB8Y5WCsjLu883Ygn4B49Lvm9bPe2QeMKQdVeZmXF$9l$4uCZ8QDXhaHEp3rvzXRJFdy0KqPHLoMevcTLo3h8xh70Y6N_U_CryOsw6FTOdKL_jpQ-&CONTENTTYPE=image/jpeg
Figure 3: Accessed May 19, 2015, from: http://images.nationalgeographic.com/wpf/media-live/photos/000/005/cache/common-vampire-bat_505_600x450.jpg
Figure 4: Accessed May 19, 2015, from: http://blogs.scientificamerican.com/media/inline/blog/Image/CrawlingBat.jpg

The origin of the bats

The most recent group of tetrapods to evolve flight were a type of mammal. The bats.

The earliest known bat fossils date to around 52 million years ago. However, these early bats were very much like modern microbats in morphology, and their only really primitive features were unfused ribs, some finger features, and the retention of certain teeth absent in modern bats (Benton, 2005). Furthermore, the very early known bats were already very widespread, being found in Eurasia, North America and Australia (Long et al, 2002). This suggests bat origins go back further. A 75 million year old fossil of a noctuid moth egg in Massachussets (noctuids are a group of moths adapted to hear bat echolocation) suggests bats may have been around as long as 75 million years ago (Altringham, 2011).

Figure 1: Icaronycteris, a bat that lived in Wyoming around 52 million years ago.  Artist: unknown.

Earlier in this blog we saw how gliding played no role in the evolution of flight in pterosaurs and dinosaurs. Again, gliding played no role in the evolution of bat flight either. In a study conducted by Kevin Padian and Kenneth Dial, it was found that bat anatomy, physiology and behaviour pointed to an origin as climbing mammals who would hang upside down and fall down towards insect prey, using proto-wings to control their descent in a manner quite different to that of any glider. In time this early fluttering developed into true flight (Kaplan, 2011).

Figure 2: Baby bats cannot fly but if they fall they can flutter to slow their descent, likely a vestige of the fluttering ancestry of bats.  Photographer: Peet van Schalkwyk.

Bat wings are essentially webbed hands. These hand wings are somewhat better airfoils than the feather wings of birds and other flying dinosaurs, though not quite as good as the multi-layer wings of pterosaurs. Bats lack air sacs but compensate by having enormous lungs. Perhaps the bats' most amazing feature though is the ability of echolocation (though this has been lost in most megabats). By emitting ultrasonic pings that bounce off solid objects bats can work out the exact distance and location of said objects regardless of whether they can actually see them. Bat echolocation is remarkable in its precision. Indeed, it is around 1 trillion times more effective than our best sonar detector technologies (Levy, 1999).

Figure 3: A simple explanation of how bat echolocation works. The bat emits ultrasonic pings that bounce off solid objects. From this the bat can determine things like distance, location and, in the case of the moth shown here, which direction something is moving in.

Next post shall be exploring the diversity of these remarkable creatures.

References
Altringham, J. D. (2011). Bats: From Evolution to Conservation. Oxford University Press: Oxford.
Benton, M. (2005). The Rise of the Mammals. Quantum Publishing Ltd: London.
Kaplan, M. (2011). Ancient bats got in a flap over food. Nature.
Levy, C. K. (1999). Evolutionary Wars: A Three-Billion-Year Arms Race. W. H. Freeman and Company: New York.
Long, J., Archer, M., Flannery, T. & Hand, S. (2002). Prehistoric Mammals of Australia and New Guinea. University of New South Wales Press Ltd: Australia.

Image sources
Figure 1: Accessed May 12, 2015, from:  http://age-of-mammals.ucoz.ru/_si/2/24863285.jpg
Figure 2: Accessed May 12, 2015, from: http://farm3.static.flickr.com/2629/3965523629_c86b1ce4e2.jpg
Figure 3: Accessed May 12, 2015, from: http://paulmirocha.com/wp/wp-content/uploads/2011/11/echolocation1.jpg

Flightless birds

As seen earlier in this blog, flight was gained and lost on a number of occasions amongst certain non-avian dinosaurs. The avian dinosaurs are no different, as birds have become flightless many times.

Already by the late Cretaceous, there were various groups of flightless bird, including the marine dwelling hesperorniths and the ground dwelling patagopterygiforms (Buffetaut & Angst, 2013). The ratites also appeared at this time, and throughout their history, ratites have become flightless not just once but numerous times (Harshman et al, 2008).

Figure 1: Garganuavis, a huge patagopterygiform bird from late Cretaceous France. Though it looks a bit like a ratite the wing claws give away its identity as a member of a more primitive group.  Artist: Joschua Knuppe.

Following the Cretaceous-Palaeogene Extinction 65.5 million years ago, there evolved some enormous flightless birds. The gastornids were enormous relatives of ducks who lived in Eurasia and North America around 56-41 million years ago. Once thought to be predators, studies of their bone isotopes and jaw musculature show them to have been large herbivores (Angst et al, 2014). The phorusrhacids, on the other hand, were definitely predatory. Relatives of cranes, they lived in the Americas, Europe, Africa and Antarctica and existed from around 60 million-15,000 years ago (Dyke & Kaiser, 2011).

Figure 2: Some foolish borhyaenids attempt to steal some prey- a small ungulate- from a phorusrhacid. This will probably not end well for them.  Artist: Renata Cunha.

Today flightlessness exists in 18 surviving bird families (Harshman et al, 2008). In some cases, flightless birds took to a more aquatic lifestyle. This was the case with the penguins, who first appeared around 60 million years ago (Ksepka & Clarke, 2010). Penguin wings have become flippers allowing them to "fly" underwater. It is possible future penguins may evolve into fully aquatic animals.

Figure 3: A couple of Gentoo penguins about to go for a swim. Penguins have become superbly adapted to an aquatic lifestyle, with the wings having become flippers.  Photographer: Robert Heil.

Another thing that can lead to flightlessness in birds is living in island habitats. An excellent example of this is New Zealand, which is inhabited by various flightless birds including the kiwi- a ratite, three species of flightless swamp hen, and the kakapo- the world's only flightless parrot (Fitter, 2009).

Figure 4: A kakapo, the world's only species of flightless parrot.  Photographer: Thomas Gibson.

So why did so many birds become flightless? The answer is, surprisingly enough, that birds are just not exceptionally good flyers. Feather wings can be rendered flightless by something as simple as shortening the feathers and, furthermore, as feathers are made of dead tissue the wings are mostly unable to take in sensory information. Additionally, birds can only launch with their hindlimbs and must flap two to three times just to get airborne (Shipman, 1998). No wonder then that many became flightless.

The next post shall introduce the final group of flyers, the bats.

References
Angst, D., Lecuyer, C., Amiot, R., Buffetaut, E., Fourel, F., Martineau, F., Legendre, S., Arbourachid, A. & Herrel, A. (2014). Isotopic and anatomical evidence of an herbivorous diet in the Early Tertiary giant bird Gastornis. Implications for the structure of Palaeocene terrestrial ecosystems. Naturwissenschaften. 101 (4), pp. 313-322.
Buffetaut, E. & Angst, D. (2013). New evidence of a giant bird from the Late Cretaceous of France. Geological Magazine. 150 (1), pp. 173-176.
Dyke, G. & Kaiser, G. (eds.). (2011). Living Dinosaurs: The Evolutionary History of Modern Birds. John Wiley & Sons Ltd: West Sussex.
Fitter, J. (2009). New Zealand Wildlife. Bradt Travel Guides Ltd: England.
Harshman, J., Braun, M. J., Braun, E. L., Huddleston, C. J., Bowie, R. C. K., Chojnowski, J. L., Hackett, S. J., Han, K., Kimball, R. T., Marks, B. D., Miglia, K. J., Moore, W. S., Reddy, S., Sheldon, F. H., Steadman, D. W., Steppan, S. J., Witt, C. C. & Yuri, T. (2008). Phylogenomic Evidence for Multiple Losses of Flight in Ratite Birds. Proceedings of the National Academy of Sciences of the United States of America. 105 (36), pp. 13 462-13 467.
Ksepka, D. T. & Clarke, J. A. (2010). The Basal Penguin (Aves: Sphenisciformes) Perudyptes devriesi and a Phylogenetic Evaluation of the Penguin Fossil Record. Bulletin of the American Museum of Natural History. 337 (337), pp. 1-77.
Shipman, P. (1998). Taking Wing. Touchstone: Rockefeller Center.

Image sources
Figure 1: Accessed May 5, 2015, from http://fc07.deviantart.net/fs70/i/2011/184/b/e/gargantuavis_by_hyrotrioskjan-d3kv3rf.jpg
Figure 2: Accessed May 5, 2015, from http://41.media.tumblr.com/tumblr_mdbbqeRTk21rqeszyo1_1280.png
Figure 3: Accessed May 5, 2015, from http://images.nationalgeographic.com/wpf/media-live/photos/000/247/cache/gentoo-penguins-jumping-in-water_24700_600x450.jpg
Figure 4: Accessed May 5, 2015, from http://kleberly.com/data_images/wallpapers/9/282092-kakapo.jpg

The origin and diversification of birds

Birds are a group of deinonychosaurs who are unique in being the only dinosaurs known to have survived to the present day.

The first bird is traditionally thought to have been Archaeopteryx, which lived in what is now Germany around 150 million years ago. While a somewhat poor flyer it could nevertheless fly. It may also have been able to use its wings to climb and to swim (Paul, 2010). Archaeopteryx's status of "first bird" has however been challenged by China's Aurornis, thought to have lived around 160 million years ago. As well as potentially revising knowledge of bird origins, Aurornis has also added to phylogenetic data suggesting birds are actually most closely related to troodonts rather than to dromaeosaurs (Godefroit et al, 2013).

Figure 1: Archaeopteryx (left) and Aurornis (right) arguing over who gets the title of "first bird".  Artist: Emily Willoughby.

Archaeopteryx and Aurornis still had long tails and lacked such avian features as a beak and a sternal keel (like non-avian flying dinosaurs they used deltoid muscles instead). The first known tailless, beaked, sternal keel possessing bird was Confuciusornis, who lived in China around 142-121 million years ago. Though lacking tails, male Confuciusornis possessed long tail feathers for display, like many birds today (Shipman, 1998).

Figure 2: A male Confuciusornis perches on a tree branch. Though it still had wing claws, Confuciusornis was recognisably avian.  Artist: Kevin Yan.

Confuciusornis belonged to an extinct group of birds called the enantiorniths. However, most known birds, including all modern birds and many extinct groups, belong to another group called the ornithurines, of which the oldest known member is China's Liaoningornis, which was contemporary with Confuciusornis. Interestingly, Liaoningornis and other early ornithurines had toothed jaws. All modern birds belong to a group of toothless ornithurines called the neorniths. The earliest known neornith groups, present by the late Cretaceous, were things like ratites, water fowl, loons, and wading shorebirds (Shipman, 1998). There is also possible fossil evidence of late Cretaceous parrots and possible molecular evidence for many other modern groups having a Cretaceous origin (Stidham, 1998). This is far from conclusive though.

Figure 3: A loon carries its chicks across some water. Loons are a group of birds that have been around since the Cretaceous.  Photographer: Bill Maynard.

Birds have gone on to be the dinosaurs' greatest success story, with more than 10,000 known living species. They have filled numerous niches including fishers, divers, predators, insectivores, frugivores, folivores, nectarivores, filter feeders, and oppurtunists.

Figure 4: Hummingbirds are an excellent example of how modern birds have filled an amazing variety of niches.  Photographer: Finca Lerida.

Next post shall discuss how many birds lost their ability to fly.

References
Godefroit, P., Cau, A., Dong-Yu, H., Escuillie, F., Wenhao, W. & Dyke, G. (2013). A Jurassic avialan dinosaur from China resolves the early phylogenetic history of birds. Nature. 498 (7454).
Paul, G. S. (2010). Dinosaurs: A Field Guide. A & C Black Publishers Ltd: London.
Shipman, P. (1998). Taking Wing. Touchstone: Rockefeller Center.
Stidham, T. A. (1998). A lower jaw from a Cretaceous parrot. Nature. 396 (6706), pp. 29-30.

Image sources
Figure 1: Accessed April 21, 2015, from http://emilywilloughby.com/gallery-data/images/full/the-earliest-birds.jpg
Figure 2: Accessed April 21, 2015, from http://fc06.deviantart.net/fs9/i/2006/015/3/e/Confuciusornis_sanctus_by_yty2000.jpg
Figure 3: Accessed April 21, 2015, from http://coolwildlife.com/wp-content/uploads/galleries/post-357/Loon%20Pictures%20012.jpg
Figure 4: Accessed April 21, 2015, from http://phenomena.nationalgeographic.com/files/2014/08/Hummingbird-990x618.jpg

Flight in non-avian dinosaurs

It has become a well accepted fact that birds are a type of flying dinosaur. Less well known is that they were not the only dinosaurs to take to the air.

Anchiornis was an early deinonychosaur that lived in what is now China around 160 million years ago. It had some parachuting ability thanks to the large feathers on its arms and legs. These feathers were not proper airfoils despite the great length of the arms, suggesting a reduction in flight ability from a possible flying ancestor (Paul, 2010). This would mean both that flight in dinosaurs goes back earlier than previously thought and that the first flying dinosaurs may have been non-avian.

Figure 1: An Anchiornis chases a small mammal through a late Jurassic forest. Artist: Emily Willoughby.

The dromaeosaurs were a group of deinonychosaurs containing members who possessed genuine powered flight. A good example of flying were the microraptorines, small omnivorous dromaeosaurs living in China and North America around 130-75 million years ago. While microraptorines have often been claimed to have been mere gliders their skeletal features show them to have been not only capable of flight, but in fact better flyers than the "first bird" Archaeopteryx (Paul, 2010). Their shoulders were placed so high they could easily perform full vertical flight strokes with their long forewings. Unlike birds, they did not use a sternal keel to assist in flight but instead used powerful deltoid muscles (Agnolin & Novas, 2013).

Figure 2: A Microraptor flies to a landing perch. Artist: Justine Lee.

Another flying dromaeosaur was the unenlaginine Rahonavis, who lived in Madagascar around 75-70 million years ago. Other known unenlaginines, as well as other larger dromaeosaurs such as Velociraptor and Deinonychus had lost the ability to fly. As adults that is. It is, however, possible the chicks still possessed some flight ability (Paul, 2010).

Figure 3: Some Rahonavis up in some trees. Artist: Vasika Yasnjith Udurawane.

The oviraptorosaurs were a group of short-tailed cousins to the deinonychosaurs who, while flightless, may have descended from flying ancestors (Paul, 2002 & 2010). Additionally, the therizinosaurs were cousins of the deinonychosaurs and oviraptorosaurs who may have come from gliders, who may in turn have come from flyers. As strange as it seems, even such groups as the ornithomimosaurs and the tyrannosaurs may ultimately have come from flying ancestry (Paul, 2002).

Figure 4: A family of Caudipteryx- a type of early oviraptorosaur. Oviraptorosaurs may have been secondarily flightless dinosaurs descended from flying ancestors.  Artist: Emily Willoughby.

Next post shall discuss the most well known flying dinosaurs- the birds.

References

Agnolin, F. L. & Novas, P. E. (2013). Avian Ancestors A Review of the Phylogenetic Relationships of the Theropods Unenlagiidae, Microraptoria, Anchiornis and Scansoriopterygidae. Springer: Netherlands.

Paul, G. S. (2002). Dinosaurs of the Air. The John Hopkins University Press: Baltimore, Maryland.
Paul, G. S. (2010). Dinosaurs: A Field Guide. A & C Black Publishers Ltd: London.

Image Sources
Figure 1: Accessed April 14, 2015, from http://fc02.deviantart.net/fs71/f/2010/082/1/d/Anchiornis___new_version_by_Ferahgo_the_Assassin.jpg
Figure 2: Accessed April 14, 2015, from https://gwawinapterus.files.wordpress.com/2013/04/picture.png
Figure 3: Accessed April 14, 2015, from http://fc04.deviantart.net/fs71/f/2011/357/1/3/rahonavis_ostromi_by_vasix-d4jyevw.jpg
Figure 4: Accessed April 14, 2015, from  https://blogger.googleusercontent.com/img/b/R29vZ2xl/AVvXsEjo2FX3KUM9e-FogVGhEjxAkmRLmDJnzRC1lXN_-e_XnjQI1Cofk0Xz_3enBapjiDRe7xOjjVJXQuPf2b3OHc5pAqwbcpKsKMIeWQ3siMIHGjXYtrdz_U1grzUrDF9ahFIxlqgZ9IpVcA/s1600/Caudipteryx.jpg

From feathers to flying dinosaurs

The next group to take flight were dinosaurs, a group of archosaurs of whom the only known survivors are birds.

One unique aspect of dinosaur flight is that wing's airfoil is primarily comprised of modified insulatory structures- the feathers. Feathers started out as hollow keratin fibres. Over time, these grew more and more complex, becoming bundles of fibres, then developing unbranched barbs, then barbs and barbules, and finally becoming fully-developed flight feathers. Fully-developed flight feathers are found on birds and on their closest relatives, such as dromaeosaurs. Many of the more distantly related theropods had fibres or bunches of fibres- "protofeathers" as it were. Additionally, filamentous structures were found on some ornithischian dinosaurs. This suggests the precursors of feathers may go all the way back to early basal dinosaurs in the Triassic (Clarke, 2013).

Figure 1: The evolution of feathers. 1- Simple fibres. 2- Bundles of fibres. 3- Unbranched barbs. 4- Barbs and barbules. 5- Fully-developed flight feathers.  Artist: Emily Willoughby.

As with the pterosaurs, a sophisticated system of air sacs evolved in certain dinosaurs, specifically in theropods (except the earliest ones) and in sauropods. The air sac systems of theropods, sauropods and pterosaurs all appear to have evolved independently of one another (Paul, 2010).

Also as with the pterosaurs, gliding does not have appear to have factored into the evolution of flight in the dinosaurs. While it has been proposed dinosaurs like Archaeopteryx and Microraptor were gliders, studies of their skeletal structure show them to have been true flyers. Incidentally, the therizinosaurs may have come from gliding ancestors but rather than evolving flight they, on the contrary, became more ground based (Paul, 2010).

Figure 2: A male Therizinosaurus shows off to an unimpressed female. Therizinosaurs may have come from gliding ancestors but rather than evolving into flying creatures these gliding ancestors evolved into large ground based forms.  Artist: Mark Witton.

How dinosaurian flight first evolved is not completely clear. It is quite possible the precursors of flying dinosaurs were, like the precursors of the pterosaurs, arboreal leapers. Alternatively, flying dinosaurs may have evolved from ground dwelling running forms. These hypothetical ancestors would have run and jumped into the air and flapped their feathery arms, which over time became a more and more sophisticated airfoil structure (Shipman, 1998).

Figure 3: The Ascent of Bird.  Artist: Matthew Martyniuk.

Before moving onto birds, we shall next see some of the non-avian dinosaurs that also evolved flight.

References
Clarke, J. (2013). Feathers Before Flight. Science. 340 (6133), pp. 690-692.
Paul, G. S. (2010). Dinosaurs: A Field Guide. A & C Black Publishers Ltd: London.
Shipman, P. (1998). Taking Wing. Touchstone: Rockefeller Center.

Image sources
Figure 1: Accessed April 7, 2015, from http://fc02.deviantart.net/fs70/i/2012/190/2/1/feather_evolution_by_ewilloughby-d56msug.png
Figure 2: Accessed April 7, 2015, from  https://blogger.googleusercontent.com/img/b/R29vZ2xl/AVvXsEijkQFc6zmdlTerZuehDU8dvxlXXzZqH613zK9zC0JVC4RN_2wwYD9Kh4vTapIPyaFCT_QuIVllkU9NU7qCdxLqSHGEGTChXZ-gMzs3i2liqLC7gj66dHxMFNcGKZce7evkuvMr8ZPChK4/s1600/She's+not+interested+2015+Witton+low+res.jpg
Figure 3: Accessed April 7, 2015, from http://fc00.deviantart.net/fs71/i/2013/093/a/7/the_ascent_of_bird_by_mattmart-d5jygt0.png

Pterosaur diversity

From their humble beginnings as arboreal leapers, the pterosaurs went on to become a very diverse group of flyers, filling a wide range of different niches. The Triassic pterosaurs appear to have been primarily small piscivorous and insectivorous forms. However, the Jurassic saw the evolution of a wide variety of new forms, including the small predator Dimorphodon, the piscivorous rhamphorhynchids, the insectivorous anurognathids, the filter-feeding ctenochasmids, the opportunistic dsunganipterids, and more (Wellnhofer, 1991).

Figure 1: Anurognathus, a small insectivorous pterosaur from the late Jurassic. Artist: Maija Karala.

While pterosaurs had started out with long tails used to help with stability, more short-tailed pterosaurs showed up in the Jurassic and by the Cretaceous only short-tailed forms remained. Many Cretaceous pterosaurs became both larger and stranger than ever before. One of the strangest pterosaurs to have ever lived would have to have been the ctenochasmid Pterodaustro, from the early Cretaceous of Argentina. While ctenochasmids had been filter-feeding since the late Jurassic, Pterodaustro took it to an extreme degree. Each side of its lower jaw had almost 500 elastic, baleen-like "teeth" used to sift out small aquatic organisms, much like what flamingos do today (Wellnhofer, 1991).

Figure 2: The bizarre filter-feeding pterosaur Pterodaustro. Artist: Julio Lacerda.

Many pterosaurs filled predatory niches, such as the stork-like azdarchids and the vulture-like istiodactylids (Witton, 2012). In contrast, there were also pterosaurs that preferred a more plant-based diet, such as the tapejarines, who fed on fruits and nuts (Vullo et al, 2012).

Figure 3: A pair of Tupandactylus, a type of tapejarine from the early Cretaceous. Artist: Mark Witton.

While no pterosaur ever became flightless, some like the dsunganipterids and the azhdarchids, developed more ground dwelling lifestyles. The azdarchids had lifestyles akin to giant storks and could grow to a massive sizes, with the largest having wingspans of 10-11 metres and body masses of 200-250 kilograms, making them the largest flying animals to have ever lived. Pterosaurs could reach greater sizes than flying birds, due to their wings being stronger and providing more lift than bird wings and due to their quadrupedal launch giving more launch power than the bipedal launch of birds (Witton & Habib, 2010).

Figure 4: An azhdarchid tries to keep its prey- a dromaeosaur- away from some thieving dsunganipterids. Artist: Mark Witton.

This post merely scratches the surface of pterosaur diversity but hopefully gives a good taste of it. Next up we shall see the evolution of a new group of flyers- birds and other flying dinosaurs.

References
Vullo, R., Marugan-Lobon, J., Kellner, A. W. A., Buscalioni, A. D., Gomez, B., Fuente, M. d. l. & Moratalla, J. J. (2012). A New Crested Pterosaur from the Early Cretaceous of Spain: The First European Tapejarid (Pterodactyloidea: Azhdarchoidea): e38900. PloS One, 7 (7).
Wellnhofer, P. (1991). The Illustrated Encyclopedia of Pterosaurs. Crescent Books: New York.
Witton, M. P. & Habib, M. B. (2010). On the Size and Flight Diversity of Giant Pterosaurs, the Use of Birds as Pterosaur Analogues and Comments on Pterosaur Flightlessness. PloS One, 5 (11).
Witton, M. P. (2012). New Insights into the Skull of Istiodactylus latidens (Ornithocheiroidea, Pterodactyloidea): e33170. PloS One, 7 (3).

Image sources
Figure 1: Accessed March 31, 2015, from http://41.media.tumblr.com/e5584185d859a6e0d7b91f6e78d4698e/tumblr_mvcyy72ht01rbztl0o1_1280.jpg
Figure 2: Accessed March 31, 2015, from http://fc03.deviantart.net/fs71/f/2012/131/2/1/feeding_off_a_mirror_by_karkajou1993-d4vg3i3.png
Figure 3: Accessed March 31, 2015, from http://invivomagazin.sk/admin/obrazky/382051192tupan%20witton.jpg
Figure 4: Accessed March 31, 2015, from http://scienceblogs.com/tetrapodzoology/wp-content/blogs.dir/471/files/2012/05/i-18b8cd89e1c14b6727ca53eca47ca33c-Witton-dsungaripterids-hound-azhdarchid-Sept-2010.jpg

Pretty pycnofibres, wondrous wings and amazing air sacs

The first important feature needed to be a flying tetrapod is a warm-blooded metabolism in order to produce enough energy to sustain powered flight. Pterosaurs had this. For insulation they had a thick pelt of hair-like structures called pycnofibres. A pterosaur's pelt could be quite dense. For example, the Jurassic pterosaur Rhamphorhynchus had about 20 pycnofibres per square millimetre and each one was 2-3 millimetres long (Benton, 1998).

Figure 1: On this Rhamphorhynchus the hair-like pycnofibres are clearly visible. Artist: Luis Rey.

The most important feature for flight though are of course wings and the pterosaur wing was one of the most amazing structures to have ever evolved. The fourth finger had become extremely elongated, while the fifth finger had vanished. From the elongated fourth finger was attached a large membrane that served as an airfoil surface. This membrane was comprised of layers of skin, muscle tissue and air pockets. Supporting the wing were special fibres called the aktinofibrils. As well as reinforcing the flight membrane, the aktinofibrils also prevented wobbling in flight and allowed pterosaurs to change their wing shape for better maneuverability (Wellnhofer, 1991).

Pterosaurs launched into the air in a quadrupedal fashion where the hind limbs were used to provide forward momentum while the forelimbs (wings) were used to provide a vertical heft that launched the pterosaur into the air (Habib, 2008). At least some pterosaurs were even able to launch from water (Habib & Cunningham, 2010).

Figure 2: Cretaceous pterosaur Ornithocheirus launching from water. Artist: Mark Witton.

 Pterosaurs also had another amazing feature. As well as lungs they also possessed an advanced system of air sacs that extended into their skeleton leaving openings in the bones. The only other animals known to possess such a system are saurischian dinosaurs (inlcuding birds). As with the dinosaurs, the air sacs of the pterosaurs allowed air to flow in a single direction and get utilised as efficiently as possible. Pterosaur air sacs, however, also ended up evolving a feature not possessed by dinosaur air sacs. The larger pterosaurs could inflate subcutaneous air sacs in their wings to alter their mechanical properties, such as relative stiffness (Claessens et al, 2009).

Figure 3: This cutaway of Cretaceous pterosaur Anhanguera shows lungs (red), neck air sacs (green) and wing air sacs (blue). Artist: Mark Witton.

Next up will be pterosaur diversity before moving onto the next group of flyers- birds and other dinosaurs.

References
Benton, M. (1998). The Reign of the Reptiles. Eagle Editions: Hertfordshire.
Claessens, L. P. A. M., O'Connor, P. M., & Unwin, D. M. (2009). Respiratory Evolution Facilitated the Origin of Pterosaur Flight and Aerial Gigantism. PloS one, 4 (2).
Habib, M. B. (2008). Comparative evidence for quadrupedal launch in pterosaurs. Zitteliana. B28, pp. 159-166.
Habib, M. B. & Cunningham, J. (2010). Capacity for water launch in Anhanguera and Quetzalcoatlus. Acta Geosci. Sin 31, pp. 24-25.
Wellnhofer, P. (1991). The Illustrated Encyclopedia of Pterosaurs. Crescent Books: New York.

Image sources
Figure 1: Accessed March 24, 2015, from http://pterosaur.net/species/Rey%20Rhamphorhynchus.jpg
Figure 2: Accessed March 24, 2015, from http://www.markwitton.com/communities/6/004/009/119/796/images/4618976279.jpg
Figure 3: Accessed March 24, 2015, from http://i.livescience.com/images/i/000/002/908/i02/090217-pterosaur-ballooning-02.jpg?1296073588

The origin of the pterosaurs

The first tetrapods to evolve powered flight were the pterosaurs. These were a group of archosaurs related to the dinosaurs, but not dinosaurs themselves. The earliest known pterosaur was Eudimorphodon, who lived in what is now Italy around 230-220 million years ago, in the late Triassic. However, while the earliest known pterosaur, Eudimorphodon had specialised multi-cusped teeth not found in any of the later pterosaurs, so it would not have been ancestral to them but rather part of a distinct pterosaur lineage that died out in the Triassic. Furthermore, both Eudimorphodon and other late Triassic pterosaurs are "completely" developed, having all the typical pterosaur skeletal characteristics. This suggests the origins of pterosaurs may lie even further back in the past, in the earlier Triassic or perhaps even in the Permian (Wellnhofer, 1991).

Figure 1: Triassic pterosaurs Eudimorphodon (right) and Peteinosaurus (left). In the background a Ticinosuchus wanders about. Artist: John Sibbick.

No fossils of the pterosaurs' immediate ancestors are known. The most likely theory on their origins is that they evolved from arboreal creatures that would leap from branch to branch, flapping their forelimbs to stay airborne longer. Pterosaur hips had great freedom of movement, their knees and ankles were hinge-like and their feet were plantigrade. The knees and ankles did not permit the necessary rotation for them to move bipedally, so pterosaurs were obligate quadrupeds (though they may have had bipedal ancestors). A possible explanation for these features is that the early pterosaurs or proto-pterosaurs were arboreal creatures that evolved powerful leaping from branch to branch as an active mode of transport not dissimilar to that of arboreal leaping primates (Christopher, 1997). These arboreal leapers would not have been gliders, who merely fall slowly downwards and forwards with the help of special flaps, but rather creatures utilising a quite different form of locomotion, one that led them to eventually having their forelimbs evolve into more and more sophisticated flapping airfoils.

Figure 2: A hypothetical series of pterosaur ancestors. Artist: Maija Karala.

The next blog post shall delve into more detail on the anatomical and physiological features that made the pterosaurs such great fliers.

References
Christopher, B. S. (1997). The arboreal leaping theory of the origin of pterosaur flight. Historical Biology. 12 (3).
Wellnhofer, P. (1991). The Illustrated Encyclopedia of Pterosaurs. Crescent Books: New York.

Image sources
Figure 1: http://www.moensklint.dk/media/37420/eudimorphodon_large.jpg
Figure 2: https://gwawinapterus.files.wordpress.com/2014/02/tumblr_mrseawh0qk1sx3tcvo1_1280.jpg

When tetrapods learned to fly

The earliest animals to fly were insects and for a long period these were the only flyers on Earth. Later on, however, flight also evolved independently in more than one group of tetrapod.

If one includes gliding as a form of flight, then the earliest flying tetrapods would have been the weigeltisaurs of the Permian (Benton, 1998). Since then, gliding has independantly evolved in numerous different groups of tetrapod. However, if one is referring to true powered flight then the first flying tetrapods were the pterosaurs, who first appeared in the Triassic. Later, powered flight evolved in certain maniraptoran dinosaurs, including the birds. Later still it evolved in a group of mammals, the bats.

Coelurasauravus, a gliding creature from the Permian.

In all of these groups, the forelimbs evolved into a new type of structure- wings. A wing is an aerofoil structure, with a curved top and a flat bottom. This causes air flowing across the wing to "stretch" over the top, resulting in lower air pressure above the wing than below it and resulting in the higher air pressure below pushing the wing upwards. Each of the groups of flying tetrapod had forelimb-derived wings utilising this basic principle. However, each group had a very different type of wing design. The pterosaurs had "finger wings" in which an elongated fourth finger supported a membranous wing reinforced by stiffening fibres. Birds and other flying dinosaurs had "arm wings" comprised primarily of feathers. Bats had "hand wings" in which a leathery elastic membrane stretched between adjacent fingers. (Raymer, 1988 & Shipman, 1998). These different designs of structures used for the same purpose show how evolution can produce differing solutions to a single problem.

Bird, bat and pterosaur wings all derive from the forelimbs but each in a different way.

 Future blog posts will go into further detail on the origins and evolution of the pterosaurs, the birds and other flying dinosaurs, and the bats, and on the wide diversity that evolved within all these groups of flyers.

References
Benton, M. (1998). The Reign of the Reptiles. Eagle Editions:Hertfordshire.
Raymer, J. M. W. (1988). The evolution of vertebrate flight. Biological Journal of the Linnaean Society, 34 (3), pp. 269-287.
Shipman, P. (1998). Taking Wing. Touchstone: Rockefeller Center.

Image sources
http://f.tqn.com/y/dinosaurs/1/S/j/a/-/-/ABcoelurasauravus.jpg
http://ncse.com/files/images/Wing_morphology.img_assist_custom.jpg