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This special issue of The Anatomical Record explores the recent advances in the functional morphology and paleobiology of dinosaurs. Although Darwin did not study dinosaurs because paleontology was in its infancy a century and half ago, he considered both paleontology and anatomy as essential subjects for establishing the validity of evolution. The study of dinosaurs constitutes a vigorous subdiscipline within vertebrate paleontology, and anatomists and evolutionary functional morphologists constitute an especially creative subgroup within dinosaur paleontology. The collection of 17 papers presented in this issue encompass cranial anatomy, postcranial anatomy, and paleobiology of dinosaurs and other archosaurs. Soft tissue subjects include studies of brain structure, jaw adductor muscles, and keratinous appendages of the skull. Taxonomically, it includes four papers with a focus on theropods, including Tyrannosaurus, five papers dealing with ceratopsians, three papers on hadrosaurs, and one on ankylosaurs. Modern anatomical techniques such as CT scanning, finite element analysis, and high resolution histology are emphasized. The visual presentation of results of these studies is spectacular. Results include the first-ever life history table of a plant-eating dinosaur; a determination of the head orientation of Tyrannosaurus and its relatives based on interpretation of the semicircular canals. The claws of Velociraptor appear to best adapted for tree climbing, but not for horrific predatory activities. Pachyrhinosaurus evidently used its massive head for head butting. The tail club of the armored dinosaur Euoplocephalus had the structural integrity to be used as a weapon. The pages abound with insights such as these. Dinosaurs once dead for millions of years live again! Anat Rec, 292:1240–1245, 2009. © 2009 Wiley-Liss, Inc.
How fitting this year as we bask in the warm glow of the Darwin anniversaries. On February 12, 2009, we were blessed with the 200th anniversary of the birth of Charles Darwin, and November 22, 2009 marks the 150th anniversary of the publication of On the Origin of Species. The gentle Darwin possessed one of the great intellects of the 19th century, and probably of all time. A prolific writer, the facts of Darwin's life are well known and thoroughly documented (Desmond and Moore, 1991; Browne, 1995, 2002). Darwin was a failed medical student at Edinburgh, disliking anatomy (perish the thought!) and despising surgery, as would any sensitive person in those gruesome days before anesthesia. Always an enthusiastic field naturalist, he spent his days at Cambridge collecting insects, riding, and shooting; his physician father despaired that he would amount to anything. He studied botany at Cambridge with John Stevens Henslow, a cherished mentor. He came late to geology, taking a field trip to Wales with Adam Sedgwick after he graduated in 1831. He was preparing for a career in the ministry and intended to live the life of a country parson, a leisurely life that would afford ample opportunity for indulging his passion for natural history. Henslow, however, nominated young Darwin for a 2-year voyage on HMS Beagle with Captain Robert FitzRoy. The intended 2-year voyage stretched to a 5-year circumnavigation of the globe. Darwin was a terrible sailor and never grew accustomed to the rolling and pitching of the ship. Fortunately, as Fitzroy sailed back and forth up and down the east coast of South America, Darwin literally spent two-thirds of his time on land making geological observations and collecting all manner of specimens, including plants, animals, rocks, and fossils. He shipped crate after crate of specimens back to England, a valuable legacy indeed. He became a great disciple of geologist Charles Lyell, whose Principles of Geology (published in three volumes between 1830 and 1833) provided an indispensible resource for interpreting what he observed in South America. He was enthralled by volcanic landscapes, coral atolls, and evidence of tectonic uplift by which vast areas of Patagonia were raised out of the sea in relatively recent geological times. The more evidence he saw for the antiquity of the earth, the more he doubted the historical reliability of the Biblical creation account. Returning at last to England in October 1836, he parceled out biological and paleontological specimens to various experts for description but reserved the geological material for himself. Recognizing his own deficiencies as a biologist, Darwin selected one group of organisms to describe and develop expertise. Initially in 1846, his intention was to describe a new genus and species of barnacle that he had recognized, but as he immersed himself in anatomical minutiae and taxonomic analysis, he became utterly enthralled. He ceased his labors only 8 years later when he had monographed the entire crustacean infraclass Cirripedia both living and fossil. He emerged from the exercise a true biologist, not merely a naturalist. He earned a medal from the Royal Society for his considerable pains.
One of the fruits of his travels was that in examining so many plants, animals, and fossils during his travels, Darwin came to doubt the fixity of species. Although evolution was truly in the air at this time, no previous writer had ever amassed the amount of reliable data that Darwin did to make the case that evolution had indeed occurred. In preparing the vast synthesis that is The Origin, Darwin drew on every discipline he could, including taxonomy, anatomy, physiology, embryology, biogeography, geology, and paleontology. Moreover, Darwin outlined the underlying mechanism, natural selection, acting on the substrate of natural variability. The Origin sold out instantly following its publication in November, 1859, and quickly enjoyed a second edition in January, 1860; the U.S. edition appeared in 1860, and the book achieved both scientific and popular success. Like Galileo before him, Darwin wrote in language accessible to lay people as well as to scientists, and his ideas achieved broad though not universal acceptance in his lifetime. Only in the 20th century, following the rediscovery of Gregor Mendel's experiments with peas in a monastery garden from 1856 until 1864, did the genetic basis for evolution become known. Today, we are grateful heirs of Darwin's legacy. So, successfully did Darwin make his case that Dobzhansky (1964, 1973), one of the great evolutionary biologists of the 20th century, declared “Nothing in biology makes sense except in the light of evolution.”
For our part, those subjects of greatest interest are the anatomy and paleontology of dinosaurs. Ironically, Darwin made an impact as a collector of fossils on his great voyage. Most famous are the Plio-Pleistocene mammals that Darwin discovered in sea cliffs along the coast of northern Patagonia. These were described by Richard Owen (1804–1892), the great 19th century anatomist and paleontologist who in 1842 gave dinosaurs their name. Actually, Darwin had a near miss on dinosaurs. Drexel University paleontologist Ken Lacovara is today excavating a rich dinosaur site today in southern Patagonia located about a day's hike from the spot where Darwin and a small party from the Beagle turned back from their attempt to march from Atlantic to Pacific across the rugged Andes (Dodson, 2009). Had Darwin persisted 1 more day, he might be remembered in history as a great dinosaur paleontologist. As it was he never found a single dinosaur fossil, and he is honored in only a single dinosaur name, Aniksosaurus darwini (Martínez and Novas, 2006). Dinosaurs played no role in Darwin's arguments. Dinosaur paleontology was then in its infancy. The first dinosaur, Megalosaurus, was named in 1824, and by 1859, barely a dozen had been described.
Fast forward to today, well over a thousand dinosaur names have been proposed, although a significant number of these are technically invalid for a variety of reasons, including inadequacy of type fossils, junior synonymy, or preoccupation (Dodson, 1990; Benton, 2008). The number of dinosaurs that can survive critical scrutiny at the time of this writing is roughly 620 genera. This number has swollen by more than 90 since 2006, when Wang and Dodson (2006) reported the count at 527 genera. In China alone, more than 30 genera of new dinosaurs have been described in 4 years. In 2007, China passed the United States to become the greatest source of dinosaurs on earth. One of the major props of Darwin's argument for evolution is that the fossil record is incomplete and that a better understood fossil record would document evolutionary transitions with greater frequency. Although creationists love to mock the alleged incompleteness of the fossil record, (e.g., Gish, 1995), the growth of the fossil record of dinosaurs, for example, from extremely incomplete to somewhat less so, during the past 2 centuries is a matter of record (Dodson, 1990; Wang and Dodson, 2006). The latter authors estimate that only a third of all dinosaur fossils have yet been recovered. The fossil record has recently offered up several spectacular transitional fossils, including the Late Devonian “fishapod” Tiktaalik rosae intermediate between panderichthyid sarcopterygian “fish” and basal tetrapods (Daeschler et al., 2006) and the Eocene walking whale Ambulocetus (Thewissen et al., 1996). More such transitional forms may be expected in the future as more and more fossils are found. Prothero (2007) documents numerous examples of transitional fossils.
Given the tremendous growth in our knowledge of dinosaur fossils, it is not surprising that a great intellectual enterprise is devoted to the description and classification of dinosaur fossils, and the reconstruction of their phylogenetic histories. In recent decades, phylogenetic reconstruction has followed the methodology of phylogenetic systematics (a.k.a. cladistics) expressed in the form of cladograms, which began to appear in dinosaur studies in the mid-1980s (e.g., Milner and Norman, 1984; Norman, 1984; Sereno, 1984, 1986; Gauthier, 1986). Cladograms are now commonplace and have achieved considerable sophistication and maturity (e.g., Sereno, 1999). Part of the appeal of cladistics is the apparent precision that the methodology offers as huge datasets of binary characters are examined. For many if not most paleontologists phylogenetic analysis is the principal thrust of their scholarship, and great intellectual capital may be expended in generating and defending cladograms. Cladistics has brought with it an arcane terminology that can be unsettling to the uninitiated. A clade is defined by apomorphies or derived characters (evolutionary novelties) and taxa arrayed on a cladogram may be more derived or may basal. The value-laden terms “primitive” and “advanced” are eschewed. One aspect of cladistics that bears comment for the uninitiated is that of holophyly. It is mandated within the system that monophyletic clades consist of basal taxa plus all descendents. Because birds are now regarded as theropod descendants, birds are now considered as dinosaurs (Kentucky fried dinosaur for lunch, anyone?). If birds are excluded, an artificial paraphyletic group is created. The clumsy phrase “non-avian dinosaur,” designating all dinosaurs not actually birds, is sometimes used. This volume primarily discusses dinosaurs of the non-bird kind, and I beg the reader's indulgence for not using this linguistic contortion.
Contrasting with historical analysis of phylogenetic reconstruction is the ahistorical approach of functional analysis (Weishampel, 1995). Functional studies draw on physical and mechanical properties of biological materials and draw heavily on analogies with living organisms. Functional studies bring dry bones to life and hang living flesh on them, as did Ezekiel of old, creating a true paleobiology. This truly synthetic activity often begins in the dissection laboratory, or the physiology or biomechanics lab, and usually involves information from the soft anatomy of living animals mapped onto fossils. When the two approaches are combined, a true comparative biology emerges. Witmer (1995) has provided paleontologists with a valuable tool for inferring soft tissue structures in extinct organisms, the extant phylogenetic bracket (EPB). The fossil under study is placed in a phylogenetic context, and the bracket consists of living animals phylogenetically on either side of the fossil animal in question. For example, the phylogenetic bracket for a dinosaur consists of crocodilians and birds. If a soft tissue structure is found at both ends of the bracket, then it is a level I inference (highly likely) that the extinct animal also carried the structure in question. For a level II inference, the soft structure is found at one end of the bracket but not at the other end. It may or may not be present in the fossil; it is less certain. If it is found in neither living animal, it is less certain still to have characterized the fossil. A level III inference does not represent impossibility; it just cannot be regarded as anything stronger than a speculation. Four-chambered hearts, for example, are found in both crocodilians and in birds; the existence of a four-chambered heart in dinosaurs is a level I inference, a highly respectable speculation. Crocodilians are ectothermic, birds endothermic. We may speculate that dinosaurs are endothermic; they may well have been, but evidence must be evaluated very carefully. It is no sure thing. Evidence has been discussed for years whether plant-eating dinosaurs had cheeks. The EPB does not support the speculation; it is a level III inference. No bird or croc has cheeks. Nonetheless, the unique inset of teeth from jaw margins and outward-sloping occlusal planes in hadrosaurs and ceratopsids make it a respectable speculation that cheeks were present. It is the unique and unexpected characters and combinations of characters that make dinosaurs such engaging subjects of study and speculation.
When I entered the field of dinosaur paleontology in the late 1960s, it was just emerging from a rather quiet period, although the seeds were being laid for a great renaissance. In the 1960s, the late John Ostrom of Yale University was conducting expeditions to Cretaceous fossil beds in Wyoming and Montana. Ostrom's fossil discoveries, particularly of the immortal raptor Deinonychus (Ostrom, 1969) both directly and indirectly provided Ostrom with the ammunition to make a convincing case for warm-blooded dinosaurs (Bakker, 1968, 1971) and the concept of the dinosaurian ancestry of birds (Ostrom, 1973, 1974, 1975, 1976). Thomas Henry Huxley posited dinosaurian ancestry for birds in 1868, but the idea underwent eclipse when Heilmann (1927) came out in favor of thecodont ancestry. Ostrom was a fine anatomist (Ostrom, 1961) and functional morphologist (1964, 1966, 1974). I am proud to claim John Ostrom as my mentor.
Dinosaur studies have exploded in recent years. The total number of dinosaurs known worldwide has roughly quadrupled since 1969. Dinosaur paleontology has attracted some of the brightest minds in science, including two certified geniuses (John Horner, Paul Sereno). In my strictly objective judgment, functional morphologists are la crème de la crème among paleontologists. Many threads in my life have crossed in weaving this special issue of Anatomical Record, the first of which involved reconnecting with my old anatomy tablemate, associate editor of AR Jeffrey Laitman. We were partners in crime at Yale Medical School in 1973, back when we were both intellectual saplings. I vividly remember Jeff's ebullient chatter and wit, which made dead things so much fun! Many years later, we are both established in our careers, I as a veterinary gross anatomist and dinosaur paleontologist, Jeff as medical gross anatomist and professor of otorhinolaryngology. Jeff was an anthropology and anatomy graduate student with a keen interest in the comparative anatomy of the upper respiratory tract in hominid evolution, with a subsequent digression toward marine mammals. Our paths recently crossed when young Benjamin Laitman, Jeff's son, who is a brilliant (and friendly) student at the University of Pennsylvania, began working in a neuroanatomy lab down the hall from my office. One thing led to another, and ultimately this special issue has appeared.
Jeff charged me with putting together a high-level collection of papers on functional morphology of dinosaurs. I thought of the people whose work I greatly admire and issued invitations. Of course not all were able to accept, but those who did have produced some quite dazzling work if I may say so. Many of the authors are at early stages of their careers. It is hardly surprising that young researchers are showing the way and pushing the envelope. This is as it has always been and should be. If my students do not run circles around me, then perhaps I have not selected wisely. The reader may be extraordinarily surprised at the depth of the biological information that our authors have been able to extract from these long-dead beasts. With fatherly pride, I have to point out that my students and my students' students are well represented among the authors. My students include authors Guenther, Schachner, Tanoue, Tumarkin-Deratzian and coauthors, Grandstaff, and You. My students' students include Farke (via Cathy Forster) and Larry Witmer (via David Weishampel); Hieronymus and Holliday are my doctoral great-grandchildren via fellow Witmer. In addition, Chinsamy was my postdoctoral, and I served on the thesis committee of D'Amore (and also Witmer). I should also mention two students not included among the list of authors. Eric Morschhauser and Andrew McDonald are first-year graduate students who have aided me with editorial chores and I am grateful to them. I have no genealogical connection with the authors of five papers. We paleontologists are well aware of intellectual genealogies, and with great pride I can trace mine back to Joseph Leidy (1823–1891), the great anatomist, paleontologist, and microscopist at the University of Pennsylvania (see Laitman, 2009). Leidy is honored as the father of American Paleontology (“Ah yes!” exclaimed Cathy Forster, “But who was the mother?!”). It was Leidy who described the first American dinosaurs and he who first presented evidence for an upright dinosaur as he first reconstructed Hadrosaurus foulkii from New Jersey, the hadrosaur or duck-billed dinosaur known to science. I am honored to share in the fertile legacy of Leidy.
The diverse collection comprises 17 papers, including seven devoted to anatomy of the skull, four to anatomy of the postcranial skeleton, and six using skeletal anatomy to infer aspects of the biology of dinosaurs. Taxonomically, the coverage encompasses four papers with a focus on theropods, including Tyrannosaurus, five papers dealing with ceratopsians or horned dinosaurs, three papers on hadrosaurs, one on ankylosaurs, and one on pterosaurs, which are not dinosaurs but are certainly Mesozoic archosaurs. Several papers are taxonomically broad in scope. The perceptive reader will notice that sauropods and stegosaurs are conspicuously absent, although not intentionally so. A sauropod paper was commissioned but the author was not able to deliver it. Some of the modern techniques delivered include finite element analysis (FEA), CT scanning, and high-resolution histological sampling.
The first section is devoted to cranial anatomy. Even classical descriptive musculoskeletal anatomy becomes spectacular as visualized for us in the phylogenetically calibrated reconstructions by Holliday (2009). Holliday, a student of the Witmer laboratory, uses unprecedented phylogenetic rigor and comparative of morphology of extant sauropsid reptiles and birds to reconstruct the jaw muscles of dinosaurs, which he does with particular elegance. He plays particular attention to muscles that leave skeletal scars and those that fail to leave such scars. Larry Witmer has established an extraordinarily productive anatomy lab at Ohio University in Athens. He and his students have performed countless dissections of the heads of extant reptiles, birds, and mammals. They have injected arteries, veins, and air sinuses, and have performed all manner of CT scans. Witmer is also expert on the visualization and presentation of three-dimensional data using color and transparency, and his work quite defines the state of the art. Witmer and Ridgley (2009) reconstruct the brain of tyrannosaurs. They confirm enhanced olfactory abilities; infer the capacity for coordinated rapid eye and head movement consistent with active predation, and note a behavioral emphasis on low-frequency sounds. Orientation of the semicircular canals suggests that the skull is oriented slightly below horizontal in Tyrannosaurus, more strongly so in Nanotyrannus. D'Amore (2009) has performed remarkable experiments on feeding Komodo dragons while a student at Rutgers University. In this contribution, he takes a safer course of action by determining the role of denticles in the teeth of small theropods. He develops a model that relates tooth curvature to angle of penetration of the food substrate and proximity to the jaw hinge. The model explains why the distal margin of the tooth is heavily denticulated but the mesial margin has a “dead space” at the base that is free of denticles. David Evans at the Royal Ontario Museum has teamed up with the Witmer laboratory to analyze the brains of lambeosaurine duckbills, the dinosaurs with the elaborate crests on the tops of their heads (Evans et al., 2009). They demonstrate that the small size of the olfactory region of the brain is independent of the elaboration of the crests. Overall brain size is large for dinosaurs, comparable to that of highly derived maniraptoran theropods. The elongate cochlea is consistent with the reception of low-frequency sounds, and the entire assembly suggests social habits in hadrosaurs. Phil Bell is a student of Eric Snively's at the University of Alberta. Bell et al. (2009) compare the forces on the mandible of hadrosaurids versus ceratopsids. Hadrosaurids (duck-billed dinosaurs) and ceratopsids (horned dinosaurs) are quite distinct clades of dinosaurs that share superficially similar dental batteries. The authors use CT scans and FEA analysis to determine the distribution of stress in jaws of each group. They confirm previously hypothesized mandibular rotation in hadrosaurids. Ceratopsids generate greater bite forces than hadrosaurids, directed in an orthal direction.
Kyo Tanoue as a graduate student at the University of Pennsylvania had the privilege of working in China on the exquisite skulls of diverse newly discovered basal horned dinosaurs. Tanoue et al. (2009) determine the progression of bite forces through basal ceratopsian phylogeny. By applying a model of levers, input forces, and resistance arms to the series, Tanoue et al. are able to identify morphological changes that result in the improvement of the ceratopsian masticatory system.
Tobin Hieronymus is another product of the Witmer laboratory. Hieronymus et al. (2009) elegantly tackle the interesting problem of determining the functional significance of the skull of the peculiar hornless horned dinosaur Pachyrhinosaurus. Pachyrhinosaurus lacks bony horn cores but instead bears a thick bony pad. By surveying histological features of rhinoceros, musk oxen, and hornbills, the authors identify key histological features that correlate with osteological features in Pachyrhinosaurus. They conclude that this horned dinosaur possessed a thick cornified pad for head-butting.
The second section treats topics on postcranial anatomy. Andy Farke is a ceratopsian researcher at the Alf Museum in Claremont, CA. Farke and Alicea (2009) CT scan cross sections of the femora of terrestrial birds and non-avian theropods to test whether orientation of the femur can be determined. Contrary to expectation, the authors reject their hypothesis, a result that will disappoint some paleobiologists. Phil Manning is a paleontologist at University of Manchester who uses among other research tools the linear accelerator at Stanford University. Manning et al. (2009) use 3D FEA to compare the functionality of an owl claw to that of Velociraptor. The authors conclude that the recurved claws of Velociraptor were suitable for both climbing and prey capture, but not for killing of prey. Arbour and Snively (2009) at the University of Alberta apply FEA to tail clubs of ankylosaurs and confirm the usefulness of these structures for delivering lateral blows to predators, but they warn that large tail clubs might have been susceptible to structural failure. Guenther of Elmhurst College (2009) uses a novel method of event-pairing to compare ontogenetic trajectories of several iguanodontians. She interprets differences between members of the two terminal clades of hadrosaurids, the Lambeosaurinae and the Hadrosaurinae, in terms of differences in sequence heterochrony.
The third section addresses questions of paleobiological interest. The first contribution is from the highly productive laboratory of John Hutchinson at the Royal Veterinary College. Hutchinson is famous for his detailed studies of locomotion in Tyrannosaurus. Understanding mode of locomotion in extinct animals is a great challenge. To do this, it is necessary to be able to estimate accurately mass, density, and center of gravity from skeletal remains. Allen et al. (2009) performed high-resolution CT scanning of juvenile and adult Crocodylus johnstoni, and Gallus gallus, juvenile and adult junglefowl and domestic broiler chickens. Ontogenetic shifts in center of gravity were determined. Errors of 15% in estimation of mass may be expected with living animals and up to 50% in fossils.
Anusuya Chinsamy is an expert on the microscopic anatomy of dinosaur bones. She spent 2 fruitful years in my laboratory at the University of Pennsylvania before returning to her native South Africa, where her career has been greeted with acclaim. Chinsamy et al. (2009) describe skeletal growth in the Brazilian pterosaur Pterodaustro. The authors conclude that Pterodaustro reached sexual maturity at age 2 years with a wing span of 1.25 m and doubled in size to 2.5 m in 4 years. They also report apparent bird-like medullary bone as a calcium reservoir for eggshell production. Chinsamy and Tumarkin-Deratzian (2009) report unusual histological features in a bone of a modern turkey vulture (Cathartes aura) and a Transylvanian dinosaur. Both specimens show endosteal deposits in the medullary cavity. The endosteal bone in the vulture is unrelated to reproduction, and the authors urge caution in accepting reports of medullary reproductive bone in Tyrannosaurus and other dinosaurs. Allison Tumarkin-Deratzian was my student at the University of Pennsylvania. She is now working independently at Temple University. Tumarkin-Deratzian (2009) has done carefully calibrated studies of bone surface textures during the ontogeny of extant archosaurs. She applies this knowledge to series of centrosaurine ceratopsids, but so far is only able to confirm juvenile textures in the fossils. Emma Schachner is studying a basal archosaur for dissertation research at the University of Pennsylvania, but her mind is already racing ahead toward the evolution of birds from theropods. Dissecting alligators and ostriches, she is contemplating the origin of avian respiration. Schachner et al. (2009) address the question of whether theropod dinosaurs had a crocodile-like, mammal-like, or an avian-style respiratory system. They conclude that the morphology of the bicapitate ribs is compatible only with an avian-style respiratory system.
Greg Erickson has established a renowned program in paleobiological research in his laboratory at Florida State University. Among many other things, he has applied skeletochronology to the remains of dinosaurs and has determined the growth rate and longevity of Tyrannosaurus and of several other dinosaurs. Erickson et al. (2009) use skeletochronology to construct the first-ever life history table for an ornithischian, Psittacosaurus lujiatunensis. Surprisingly, this small herbivorous dinosaur lived to an age of 11 years and shows a pattern of prolonged adult survival like that of large birds and mammals that is also seen in the large tyrannosaurs, suggesting that adult survival may characterize all dinosaurs, both large and small.
In summary, we present the finest contemporary scholarship in dinosaur paleobiology, using exciting modern anatomical tools. Would Darwin not have been excited about how dinosaurs have come alive?