"But above, perched each upon its own stone, tall, gray, and withered, more like dead and dried specimens than actual living creatures, sat the horrible males, absolutely motionless save for the rolling of their red eyes or an occasional snap of their rat-trap beaks as a dragon-fly went past them. Their huge, membranous wings were closed by folding their fore-arms, so that they sat like gigantic old women, wrapped in hideous web-colored shawls, and with their ferocious heads protruding above them. Large and small, not less than a thousand of these filthy creatures lay in the hollow before us." -- description of living pterosaurs by Sir Arthur Conan Doyle, The Lost World (1912)
and
"Hope is the thing with feathers
That perches in the soul
And sings the tune without the words
And never stops at all." Emily Dickinson (1861)
BIG QUESTION: How did birds and pterosaurs arise? How did they differ?
Up, Up, and AWAY! Flying Animals
In the history of life, only four groups of animals have evolved powered flight:
To possess powered flight is to be volant. But there are other forms of aerial locomotion. These include the essentialy vertical parachuting and the more controlled and linear gliding
While there are only three groups of volant vertebrates, there are many modern gliding/parachuting ones: flying fish; flying frogs; flying lizards; flying snakes; sugar gliders (gliding marsupials); flying squirrels; colugos, or "flying lemurs". In addition, there were various extinct gliding reptiles and mammals in the Permian and Mesozoic.
Pterosaurs: Dragons of the Air
The name Pterosauria means "wing reptile". Pterosaurs were ornithodiran archosaurs, the sister group to the dinosauromorphs. Their wing is primarily formed from digit IV of the hand: in other words, their wing finger is their ring finger! (They did not have pinkies!).
But the pterosaurian wing is more complex than that. They had a specialized wrist bone (the pteroid) which controlled a flap of a "front wing". The main wing went from the tip of the finger to the ankle (at least ancestrally). There was another flap of wing running from foot to foot, underneath the tail. But the wing wasn't just skin stretched between limbs: fibers connected to muscles ran through the wing, allowing pterosaurs to reshape their wing under active control.
Pterosaur bones were very hollow: even more hollow than than the bones of birds! Like birds (and at least some other dinosaurs), the pterosaurs had complex air sacs invading vertebrae and limb bones, which lightened the skeleton as was part of an advanced respiratory system.
The body of pterosaurs was covered with a fur named pycnofibers. This fur is not at all homologous to mammalian fur; it MIGHT be homologous with the fuzz in ornithischian and theropod dinosaurs, but uncertainty about the exact phylogenetic distribution of these features means that this is not resolved.
We do not have any good fossil evidence of pre-flying pterosaurs. (It might be that they mostly lived in forests, which are not normally good taphonomically for bone preservation). The oldest known pterosaurs were from the Late Triassic, somewhat younger than the oldest dinosaurs; the youngest go right up until the end of the Cretaceous.
Basal pterosaurs are sometimes called "rhamphorhynchoids", but this is a paraphyletic grade rather than a clade. "Rhamphorhynchoids" often had long tails (at least some of which ended in diamond- or Valentine heart-shaped fins.) They do not seem to have been as effective runners on the ground as their pterodactyloid descendants, and pterosaur ptrace fossils are almost unknown until Pterodactyloidea appears.
There are many varieties of "rhamphorhynchoids": early ones have diverse tooth shapes and a skull reminiscent of theropod dinosaurs; others have short frog-shaped faces; still others have long grasping teeth possible for snatching fish. "Rhamphorhynchoids" range from about the size of a robin to that of an eagle. The last of the "rhamphorhynchoid" pterosaurs disappear in the later Early Cretaceous.
Darwinopterus and other wukongopterids of the Middle and Late Jurassic represent a transition to the true Pterodactyloidea ("wing fingers"). Pterodactyloids first appear near the beginning of the Late Jurassic. They differ from basal pterosaurs by a reduced tail size, a much longer palm of the hand (metacarpus), and a split in the hindwing (so it no longer runs from foot-to-foot). The latter two changes (as well as some in the hips) points to them being better movers on the ground, and indeed pterodactyloid ptracks are fairly common in the Late Jurassic and Cretaceous. Pterodactyloids (at least: maybe other pterosaurs!) launched by using their very powerful forelimbs to push them into the air. (In nearly all other fliers and gliders, the initial launch is from the hindlimbs.)
Many pterodactyloids (and some rhamphorhynchoids, too) had crests on their head: some were bony, others made of firm or soft tissue. There appears in at least some cases to be sexual dimorphism in the size and shape of the crests. Pterodactyloid size ranges were far greater than "rhamphorhynchoids": the smallest were sparrow-sized but the largest were by far the largest fliers of all time: 12-14 m wingspans and the height of a giraffe!
Pterosaur diets varied: some may have been insectivores, others piscivores (fish-eaters), still others filter feeders (like modern flamingos), some herbivores, some durophagous (eating hard objects), and a few carnivorous. None seem to have been true raptorial forms in the sense of hawks and eagles, though.
Pterosaur eggs were definitely more leathery than dinosaurs' (which were crispy, as in the living dinosaur [aka bird] eggs). The embryos show the same wing proportions as free-living babies, and it seems that they could fly from birth. However, this does not mean that they abandoned their young: after all, crocodilians, birds, and mammals with freely-moving young often have extensive parental care.
Like non-avian dinosaurs, pterosaurs grew faster than living cold-blooded animals, achieving full body size in less than a decade. As noted above, they seem to have had complex air sacs that could pump air through their body efficiently. Their growth rates, respiration, fur, ability to use powered flight, bone texture, and other features point to them having a fully warm-blooded metabolism. (In fact, it had been proposed they were warm-blooded even before Dinosauria was discovered!)
Aves is the Word: What is a "Bird"?
Aves is the traditional Linnaean name for birds, and is used presently for crown-group birds (i.e., all descendants of the concestor of all living birds.) Avian is the adjective for issues of or concerning for members of Aves.
Pterosaurs are not birds. Nor are they dinosaurs. In contrast, EVERY bird species is a dinosaur! (Recall that Dinosauria = the concestor of Iguanodon, Megalosaurus, and Diplodocus and all of its descendants.)
At present there are between 9600 to 18,000 living species (depending on whether you are a lumper or splitter) of birds, and just 2000 years ago this number was probably an additional 3,000 more. (The difference was due to the extinction of many species of birds unique to individual islands of the Pacific and Indian Oceans: these suffered greatly as Polynesians (and later, Europeans) introduced pigs, rats, dogs, and goats to the islands.) In contrast, living mammals consist of some 4500-5600 species or so.
Many features make birds distinctive from their close living relatives among the reptiles:
It is almost impossible to mistake a bird for any other group of animal in the modern world, and vice versa. But as we will see, this is not true in the fossil record.
The fossil record of transitional forms between Aves and other reptiles was greatly improved by the discovery of Archaeopteryx lithographica from the Late Jurassic Solnhofen Lithographic Limestone of Bavaria, Germany. The first specimen (a feather) and the first skeleton (found in 1861; acquired by the Natural History Museum (London) in 1863) showed an animal that had:
The skeleton was not complete, but still achieved considerable attention. In the 1860s paleontologist T.H. Huxley used the London specimen as evidence that the newly discovered Dinosauria were more closely related to birds than to other groups of living or fossil reptiles.
In 1874 (or 1875) an even more complete skeleton of Archaeopteryx was discovered; in 1881 it was acquired by the Humboldt Museum in Berlin. This confirmed the presence of teeth in its jaws, and showed presence of individual fingers with claws.
In the 1870s Yale paleontologist described Cretaceous birds from the Niobrara Chalk of Kansas. These included flightless swimming Hesperornis and flying Ichthyornis. Both were far more closely related to modern birds than was Archaeopteryx, but still retained teeth in their jaws.
In the late 19th Century and earliest 20th Century several models of bird origins were suggested:
With the discovery of coelurosaurian dinosaurs like Compsognathus and Ornitholestes some paleontologists and others were convinced of the latter idea. When writing of Ornitholestes, H.N. Hutchinson (1910, Extinct Monsters and Creatures of Other Days) wrote:
The dinosaurian origin of bird hypothesis, however, was deflected by the well-meaning work of anatomical illustrator and amateur paleontologist Gerhard Heilmann (1855-1946). He wrote a series of articles in Danish between 1913 and 1916 which were collected and translated into English in 1923 as The Origin of Birds. He conclusive showed what Huxley and others had proposed: birds were some kind of archosaur. He compared birds to various groups of dinosaurs; to pterosaurs; to early crocodylomorphs; and to "thecodonts" (the then-fashionable name for the paraphyletic grade of basal archosauriforms, non-crocodylomorph pseudosuchians, and non-pterosaur, non-dinosaur ornithodirans).
Heilmann showed considerable shared derived features between birds and coelurosaurian theropods. But as no one had yet demonstrated a clavicle in a theropod, there was no feature that could evolve into a furcula. So the similarities between birds and dinosaurs had to be convergences. Instead, Heilmann pointed to "thecodonts" (in this case, basal archosauriforms) such as the then-recently discovered Euparkeria of the Middle Triassic of South Africa, which he deemed "sufficiently primitive" to be a bird ancestor.
Heilmann also proposed a scenario for the origin of birds: quadrupedal thecodonts which had adapted to life in the trees. These grew elongated scales which served as gliding surfaces on the arms, body, and tail in a long-armed hypothetical "proavis", which was the ancestor of Archaeopteryx and thus to later birds.
Heilmann's book was phenomenally successful, and dominated thinking on bird origins until the 1970s. Standard pictures for archosaur evolution showed birds, pterosaurs, ornithischian dinosaurs, saurischian dinosaurs, and crocodylomorphs all radiating independently from a common thecodont stock. (Note: dinosaurs were considered at best diphyletic [two independent origins] within Archosauria.) And the arboreal gliding proavis was the standard model for the origin of avian flight.
In 1969 John Ostrom of Yale described the dromaeosaurid Deinonychus. This was the first raptor dinosaur (deinonychosaur) known from relatively complete material, and showed considerable similarity with Archaeopteryx. In fact, Ostrom discovered a specimen of Archaeopteryx (miscatalogued as a specimen of pterosaur!) in a museum in the Netherlands. From comparisons of their skeletons, Ostrom demonstrated that deinonychosaurs (and some other coelurosaurs) and birds shared many traits, such as:
Ostrom revived the dinosaurian origin of birds hypothesis, which a new specific sister-group relationship between Deinonychosauria and birds. Subsequently Heilmann's primary objection was removed: it was found that theropods did not merely have clavicles; they in fact ALL possessed a furcula!
The initial cladistic analyses of dinosaurs and archosaurs in general (in the early 1980s) focused on testing the dinosaurian origin of birds hypothesis. Ostrom's idea stood up to this test. In 1986 Jacques Gauthier (who would a decade or so later have Ostrom's chair at Yale after the latter's retirement) coined the name "Avialae" ("bird wings") for the group comprised of Aves and all taxa sharing a more recent common ancestor with Aves than with Deinonychosauria. At the time non-avian members of Avialae were still restricted basically to Archaeopteryx, Hesperornis, and Ichthyornis.
This hypothesis was not without its detractors. Prominent among these were paleornithologists Alan Feduccia and Larry Martin and physiologist John Ruben. At conferences in the 1980s, 1990s, and 2000s they referred to themselves as the "BAND" (for "Birds Are Not Dinosaurs"). Their primary arguments during the 1980s and 1990s were that Heilmann was correct and the similarity between coelurosaurs and birds were just convergences. Instead they argued that newly-discovered Middle or Late Triassic quadrupedal "thecodonts" (actually not even archosauriforms, but primitive diapers) such as Megalancosaurus and Longisquama were the ancestors of birds.
Simultaneous with these arguments, an explosion of discoveries (which has definitely NOT stopped!) of Mesozoic avialians has gone on. These are primarily due to several Lagerstätten yielding dozens of new genera (and literally thousands of specimens, often nearly complete skeletons and feather impressions):
Because of this, many steps and morphological transitions along the lineage leading to Aves are now documented among Jurassic and Cretaceous avialians and other coelurosaurs. Indeed, uniquely among flying vertebrates we have a problem in indicating exactly when "birdiness" is achieved, because we have so many gradual transitions in between. (In contrast, both pterosaurs and bats appear in the fossil record as pterosaurs and bats, not proto-pterosaurs and proto-bats.)
It was not just avialians that were discovered in these Lagerstätten. These also revealed the presence of feathers in non-avialian dinosaurs. The first discovered of these (in 1996) were simple apparently hollow down-like tufts: plumulose structures dubbed protofeathers on the compsognathid coelurosaur Sinosauropteryx. Subsequently similar structures were found on numerous other types of primitive coelurosaurs, including 1 ton tyrannosaurs such as Yutyrannus. And their presence in the ornithischians Tianyulong and Kulindadromeus hints at the possibility that protofeathers are basal to all dinosaurs. (And if pterosaurian pycnofibres are homologous to protofeathers, these might be basal to all Ornithodira).
Protofeathers obviously don't have a flight function, since they don't form an aerodynamic surface. However, they might serve other functions:
More derived are strap-like protofeathers: broad surfaces rather than tufts.
Four major clades of coelurosaurs (Avialae, Deinonychosauria, Oviraptorosauria, and Ornithomimosauria) show broad pennaceous feathers on the arms; in the first three (collectively called Pennaraptora) have them both on the arms and the tail. These same pennaraptoran dinosaurs are also characterized by sideways-oriented shoulder joints, semilunate carpals, and direct brooding of the eggs. In Deinonychosauria and primitive members of Avialae (but not in Oviraptorosauria, at least as far as we know), there are long leg feathers as well.
Pennaceous feathers are very diverse in modern birds: found in flight feathers on the wings and tail; contour feathers over the body; and various decorative feathers. All have a similar structure: a central shaft (rachis), with barbs coming off of it, barbules coming off the barbs, and hooklets coming off the barbules. Developmental biology shows that plumulose down and pennaceous feathers have the same developmental pattern, just with genes emphasizing different rates of development of various parts of the developing structure. These developmental stages match the observed stages in the fossil record.
The discovery of feathers on other groups of theropods has reduced the number of uniquely bird traits in Archaeopteryx. Indeed, discovery of new Jurassic feathered dinosaurs closely related to Archaeopteryx results in some phylogenetic analyses in which this "Archaeopterygidae" is not necessarily a basal clade of Avialae, but instead is a basal clade in Deinonychosauria or the sister group to Deinonychosauria and Avialae.
(Note: in response to the discovery of fully-feathered deinonychosaurs and oviraptorsaurs, the BAND have decided that these clades are NOT dinosaurs, but are basal birds convergent on coelurosaurs!)
So where do "birds" begin? Would we use Pennaraptora? Or Avialae? Or Aves (the toothless crown group)? Or some spot in between?
Our knowledge of the phases of the origin of bird flight (anatomical, phylogenetic, and behavioral) have all greatly increased in the last decade. But before we see this newer understanding, let's review some terms and take an historical look at the problem.
Some key terms:
(NOTE: during the 1970s-1990s, this debate was tangled up with a scientifically separate debate; that is, where birds fit phylogenetically among the archosaurs. The media in particular made the equation "'arboreal model = non-dinosaurian origin of birds'; 'cursorial model = dinosaurian origin of birds'". But these were actually separate debates. Even among those who recognized the dinosaurian origin of birds, some argued for the trees-down model, and others for the ground-up.)
This debate was primarily waged prior to the new discoveries of Early Cretaceous feathered coelurosaurs, which greatly increased our knowledge of the anatomy (integumentary and skeletal) of the basal members of the coelurosaur clades. Additionally, important observations of modern birds revealed a very significant locomotory behavior, previously overlooked.
Note that these birds are NOT climbing in the typical sense: they are literally running up the sides of trees. Dial and his team studied the ontogenetic (growth) changes in the ability for birds to use this behavior, and also experimented by trimming the feathers of birds to different lengths.
They found:
Additional work has shown that this behavior is widespread among modern birds.
The apparatus required to use WAIR is:
All these attributes are present in many pennaraptorans (oviraptorosaurs, dromaeosaurids, troodontids, basal avialians). Additionally, modern birds use WAIR to escape predators: certainly a selective factor present in the Mesozoic, too! Furthermore, there are net selective advantages to slight increases in the length and breadth of the feathered arm surface: the sort of material that can easily be increased by natural selection.
WAIR might represent a "stepping stone" or "behavioral missing link" in the origin of flight. Small (or juvenile) maniraptorans might have used this method to escape predators. Now that they had the ability to get up into trees and other high spots, some lineages of maniraptorans might become specialized for life up on these high spots. Additional natural selection could favor further development of wing size and shape as an aid for getting back down off of high places (controlled flapping descent), or (eventually) from branch-to-branch.
Thus, WAIR serves as a functional link between cursorial and arboreal models (and organisms). It is a cursorial model in that wings begin in part as an aid to running locomotion (just vertical running); it is an arboreal model in that once pennaraptorans have an ability to get into the trees, evolution can further develop the forelimbs to get them back down to the ground. And all of these behaviors are still found in modern animals: no speculation of behaviors not currently seen needed.
A NEW SCENARIO FOR BIRD FLIGHT ORIGINS: The various recent discoveries of the skeletal and integumentary anatomy of various coelurosaurs (including basal avialians) and the behavioral and biomechanical evidence of modern birds suggests a more complete possible scenario for bird flight evolution than the historical "ground up" or "trees down" versions. Note that as with all evolutionary scenarios this would be a simplification, but the following is consistent with our current evidence: The various recent discoveries of the skeletal and integumentary anatomy of various coelurosaurs (including basal avialians) and the behavioral and biomechanical evidence of modern birds suggests a more complete possible scenario for bird flight evolution than the historical "ground up" or "trees down" versions. Note that as with all evolutionary scenarios this would be a simplification, but the following is consistent with our current evidence:
In contrast, Mesozoic birds show much less diversity of wing form than either modern birds or pterosaurs. Many show a flap-and-bounding flight like some of the shorter-distance fliers in the modern world. Indeed, very basal birds do not seem to have been able to do the full flight stroke of derived fliers of today. (Intriguingly, early dromaeosaurids like Microraptor may have been equally-good [or bad!] fliers.) So these feathered dinosaurs do not seem to have been masters of the air like their own descendants or their pterosaurian cousins.
Examining the size and aerodynamics of Cretaceous pterosaurs and avialians shows that they really were not in competition. They were flying in different ways, and almost certainly occupying different niches.
Dinosaurs and feathers:
The largest pterosaurs:
