TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
1 of 39
Why sauropods had long necks; and why giraffes have short necks
Michael P. Taylor, Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, England. firstname.lastname@example.org Mathew J. Wedel, College of Osteopathic Medicine of the Pacific and College of Podiatric Medicine, Western University of Health Sciences, 309 E. Second Street, Pomona, California 91766-1854, USA. email@example.com
Table of Contents
Abstract............................................................................................................................................2 Introduction......................................................................................................................................3 Museum Abbreviations...............................................................................................................3 Long Necks in Different Taxa..........................................................................................................3 Extant Animals............................................................................................................................4 Extinct Mammals........................................................................................................................4 Theropods....................................................................................................................................5 Pterosaurs....................................................................................................................................6 Plesiosaurs...................................................................................................................................7 Sauropods....................................................................................................................................8 Factors Enabling Long Necks..........................................................................................................9 Absolutely Large Body Size.....................................................................................................10 Quadrupedal Stance..................................................................................................................10 Small Head................................................................................................................................10 Numerous Cervical Vertebrae...................................................................................................11 Elongate Cervical Vertebrae......................................................................................................11 Air-Sac System..........................................................................................................................11 Vertebral Architecture...............................................................................................................12 Architecture of Sauropod Necks....................................................................................................12 Pneumaticity of Cervical Vertebrae..........................................................................................12 Extent of Soft-Tissue relative to Size of Vertebrae...................................................................16 Muscle Attachments..................................................................................................................17 Neural Spines............................................................................................................................22 Epipophyses..............................................................................................................................25 Cervical Ribs.............................................................................................................................25 Asymmetric Elongation of Cervical Ribs and Epipophyses.....................................................27 Short Neural Spines in Long Necks..........................................................................................28 Homology and Analogy of Vertebral Features..........................................................................29 Conclusions: Why Giraffes Have Such Short Necks.....................................................................30 Acknowledgments..........................................................................................................................32 References......................................................................................................................................32
TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS ABSTRACT
2 of 39
The necks of the sauropod dinosaurs reached 15 m in length: six times longer than that of the world record giraffe and five times longer than those of all other terrestrial animals. Several anatomical features enabled this extreme elongation, including: absolutely large body size and quadrupedal stance providing a stable platform for a long neck; a small, light head that did not orally process food; cervical vertebrae that were both numerous and individually elongate; an efficient air-sac-based respiratory system; and distinctive cervical architecture. Relevant features of sauropod cervical vertebrae include: pneumatic chambers that enabled the bone to be positioned in a mechanically efficient way within the envelope; and muscular attachments of varying importance to the neural spines, epipophyses and cervical ribs. Other long-necked tetrapods lacked important features of sauropods, preventing the evolution of longer necks: for example, giraffes have relatively small torsos and large, heavy heads, share the usual mammalian constraint of only seven cervical vertebrae, and lack an air-sac system and pneumatic bones. Among non-sauropods, their saurischian relatives the theropod dinosaurs seem to have been best placed to evolve long necks, and indeed they probably surpassed those of giraffes. But 150 million years of evolution did not suffice for them to exceed a relatively modest 2.5 m. KEYWORDS: dinosaur; sauropod; giraffe; neck; cervical vertebra; evolution
TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
3 of 39
INTRODUCTION The necks of the sauropod dinosaurs were by far the longest of any animal, six times longer than that of the world record giraffe and five times longer than those of all other terrestrial animals. We survey the evolutionary history of long necks in sauropods and other animals, and consider the factors that allowed sauropod necks to grow so long. We then examine the osteology of sauropod necks more closely, comparing their cervical anatomy with that of their nearest extant relatives, the birds and crocodilians, and discussing unusual features of sauropods' cervical vertebrae. Finally we discuss which neck elongation features were absent in nonsauropods, and show why giraffes have such short necks. Museum Abbreviations BYU, Earth Sciences Museum, Brigham Young University, Provo, Utah (USA) CM, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania (USA) HMN, Humboldt Museum für Naturkunde, Berlin (Germany) FMNH, Field Museum of Natural History, Chicago, Illinois (USA) IGM, Geological Institute of the Mongolian Academy of Sciences, Ulaan Baatar (Mongolia) ISI, Geology Museum, Indian Statistical Institute, Calcutta (India) MAL, Malawi Department of Antiquities Collection, Lilongwe and Nguludi (Malawi) MCZ, Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts (USA) MIWG, Dinosaur Isle, Sandown, Isle of Wight (UK) OMNH, Oklahoma Museum of Natural History, Norman, Oklahoma (USA) PMU, Palaeontological Museum, Uppsala (Sweden) UA, Université d'Antananarivo, Antananarivo (Madagascar) UJF, University of Jordan Department of Geology Collections, Amman (Jordan) WDC, Wyoming Dinosaur Center, Thermopolis, Wyoming (USA) ZMNH, Zhejiang Museum of Natural History, Hangzhou (China) LONG NECKS IN DIFFERENT TAXA While they reach their apotheosis in sauropods, long necks have evolved repeatedly in several different groups of tetrapods. Although they impose a high structural and metabolic cost, long necks provide evolutionary advantages including an increased browsing range (Cameron and du Toit, 2007) and the ability to graze a wide area without locomotion (Martin, 1987) and probably played some role in mate attraction (Simmons and Scheepers, 1996; Senter, 2006; Taylor et al., 2011). Here we survey the longest necked taxa in several groups of extant and extinct animals (Figures 1, 2).
39. 2007. The typical length of the neck of the ostrich is only 1. plus 8% to allow for intervertebral cartilage) Extinct Mammals The largest terrestrial mammal of all time was the long-necked rhinoceratoid Paraceratherium Forster-Cooper. Arambourgiania scaled from Zhejiangopterus modified from Witton and Naish (2008. Therizinosaurus. 10–20).4 cm. figure 47).95 m from the skeletal reconstruction of Granger and Gregory (1936. The length of its neck can be measured as 1.7 cm
Extant Animals Among extant animals. 36. even though C2 and C7 are reported as of “size class III”. 2. 1913. and no other extant animal exceeds half of this. Alternating pink and blue bars are one meter in height. 1915).6 and 18 cm are given for cervicals 1. Deinocheirus and Gigantoraptor are the longest necked representatives of the three long-necked theropod clades and Arambourgiania is the longest necked pterosaur. p. 1911 (= Baluchitherium Forster-Cooper.3 to give lengths of equivalent “size class I” bones (Granger and Gregory.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
4 of 39
Figure 1. is rather shorter than suggested by the text (pp. The total length of the preserved cervicals would then be 178. Indricotherium Borissiak. figure 1). p. When the lengths of C2 and C7 are multiplied by 1. their lengths become 50.0 m (sum of vertebral lengths in Dzemski and Christian. 2003. 29.1. 65). This length.4 m (Toon and Toon. Other image sources as for Figure 2. 4. to the same scale. Necks of long-necked non-sauropods. adult bull giraffes can attain 2. the ostrich is the longest necked extant bird. 1936. however. The giraffe and Paraceratherium are the longest necked mammals.7 and 23. table 1. 6 and 7. modified here as Figure 2. 399). in which lengths of 39.
1969. Osborn (1916. which were not recovered. at 770 mm. Measured from the skeletal reconstruction of Xu et al. p. 43. as follows. Oviraptorosauria. of which the left humerus is 938 mm long (Osmólska and Roniewicz. If it was similarly proportioned (Figure 2. its neck would have been about 2. its humerus was about 75 cm long. Theropods At least three lineages of theropod dinosaurs evolved long necks.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
5 of 39
even though C3 and C5. 1916.9 times the length of the humerus.e.3). and a total neck length 2. are omitted. 1979 by Paul (1997.5 m range.2 m long. known from incomplete remains. the neck is 2. modified and rescaled here as Figure 2. 9).35 m long. is known only from a pair of forelimbs. A third giant theropod. Therizinosaurus cheloniformis Maleev.8 cm) then the total length of all seven centra is 254. 744–745) gives a humerus length of 310 mm for Struthiomimus. Measuring from Barsbold (1976. it appears to have had a neck 2. figure 1A). If Therizinosaurus were similarly proportioned. Another giant theropod. Deinocheirus mirificus Osmólska and Roniewicz. 2007 belongs to another longnecked group. 1969. In a skeletal reconstruction of the therizinosauroid Nanshiungosaurus Dong. 145).9 cm. figure 1).15 m in length – although this is conjectural as almost no cervical material is known. modified here as Figure 2. The lengths of their necks can be estimated from their incomplete remains. long-necked giant theropod. p. (2007.2.4 and 32. 1954 is a bizarre. 2006) and thus may have had roughly the same proportions as Struthiomimus Osborn. pp.
. Gigantoraptor erlianensis Xu et al..5 times as long. If these vertebrae are tentatively assigned lengths intermediate between those that preceded and succeeded them (i. Deinocheirus probably belongs to the long-necked ornithomimid group of theropods (Kobayashi and Barsbold. more than 30% longer than the illustrated length. the material available suggests a total neck length in the 2–2..4. At any rate. Deinocheirus would have had a neck about 2. though with some uncertainty.
1. as is generally true of pterodacyloid pterosaurs
. ZMNH M1323. Scale bar = 2 m. 1994. Gigantoraptor. table 7) give the lengths of cervicals 3–7 for three specimens. C5 is the longest cervical. 1981): a monographic description is still awaited. p. modified from Xu el al. modified from Granger and Gregory (1936. 4. In all three. plate II. 145). Witton and Naish. Full skeletal reconstructions of selected long-necked non-sauropods. plate XXVI). but have been embargoed since the early 1980s (Langston. figure 1). (2007. In the absence of a complete neck. all length estimates are uncertain. This is due to the lack of any published azhdarchid specimen with a complete neck (Witton and Habib. modified from Cope (1870. 1986. Paraceratherium. Elasmosaurus. scaled from Nanshiungosaurus modified from Paul (1997. scaled from Struthiomimus modified from Osborn (1916.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
6 of 39
Figure 2. Therizinosaurus. Deinocheirus. to the same scale. M1324 and M1328. 2. 2008). figure 47).g. The azhdarchid for which the most complete neck has been described is Zhejiangopterus linhaiensis Cai and Wei. 5. Howse. but it is nevertheless possible to arrive at an approximate length.
Pterosaurs Although it is often noted in general terms that azhdarchid pterosaurs had long necks (e. so we will base our estimates on this species. figure 1). Cai and Wei (1994.. there are no published numeric estimates of neck length in this group. 2010): Quetzalcoatlus specimens at the Texas Memorial Museum may have complete necks. 3.
323). Its type specimen. 1868 (Sachs. 2005.g. p. 4. and their illustrations (figures 5. p. p.0 m. the total neck length of Arambourgiania may have somewhat exceeded 3. p. The cervical vertebrae of Elasmosaurus platyurus holotype ANSP 10081 sum to 610. 2003). it was probably carried on a proportionally shorter and stronger neck. 2002a.04 and 4... the reported total neck length presumably includes the invertebral cartilage. C8 may be between 20% and 50% the length of C5 (Pereda Suberbiola et al. 570). Another azhdarchid. The long necks of elasmosaurid plesiosaurs were constructed very differently from those of sauropods. UJF VF1. which is 3.” Since the neck of Albertonectes was found articulated. 72). Bearing this in mind.85 times that length. p. bears this out. Pereda Suberbiola et al. The preserved part of the vertebra was 620 mm long before the damage. 95). but has since been damaged and is now missing its central portion. but no cervical material is known. and when complete it would have been about 780 mm long (Martill et al. which might amount to 16–39 cm in Arambourgiania. Evans (1993) estimated that the thickness of intercervical cartilage amounted to 14% of centrum
. consisting of many very short cervicals – 76 in the neck of Albertonectes vanderveldei Kubo et al. Despite their marine lifestyle and very numerous cervicals. According to Kubo et al.0 m. translation by Will Downs). The azhdarchid Arambourgiania philadelphiae (Arambourg. showing the atlasaxis as about one quarter the length of C3. 1998. 183. may have been even larger than Arambourgiania. 6) indicate that in at least one specimen the vertebral column is complete. Hatzegopteryx thambema Buffetaut et al. 183). (2012.. For other plesiosaurs. plesiosaurs benefited from the support of water and so lived under a wholly different biomechanical regime than terrestrial animals. p. p. then.60. elasmosaurids did not attain neck lengths even half those of the longestnecked sauropods.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
7 of 39
including azhdarchids (Howse. Since its skull was much more robust that those of other azhdarchids (Buffetaut et al. 86). The total number of cervical vertebrae in Zhejiangopterus is not clear: Cai and Wei (1994) imply that there are seven. total C1–C7 neck length in known Zhejiangopterus specimens was about 3. 2003.. Their figure 6. 92). the length of the C1–C7 region of the neck can be estimated as 3. p. stating only that “the atlas-axis is completely fused and extremely short but morphological details are indistinct due to being obscured by the cranium” (p. a reconstruction of Zhejiangopterus linhaiensis. “The approximately 7 m long neck of Albertonectes is the longest known for elasmosaurs (equal to 62% of total postcranial length). Assuming that the preserved element is C5. 339 and 398 mm. On average. 2012 and 71 in Elasmosaurus platyurus Cope. Cai and Wei (1994) do not give lengths for C1 and C2.5 cm. p. 240). 1959) is the largest pterosaur for which cervical material has been described. Other elasmosaurs may have had equally long necks. we find by adding the lengths of the individual cervicals that the three specimens had necks measuring approximately 511. Using this ratio to estimate the C1–2 lengths for each specimen. at least some azhdarchids seem to have have nine cervical vertebrae (e. but plaster replicas made before the damage indicate the extent of the missing portion. is a single cervical vertebra. It was nearly complete when found. 2002a. Plesiosaurs As marine reptiles. In azhdarchids. 1986.85 times that of C5. However..06 times the lengths of their respective C5s. 318) and Frey and Martill (1996. based on individual vertebral lengths listed by Sachs (2005. although the ninth “cervical” bears a long vertically oriented rib and must have contributed to the length of the torso rather than the neck. Phosphatodraco. as considered likely by Howse (1986... These lengths are 3.
represents a “typical” long-necked sauropod.wikimedia. 2006a). Alternating pink and blue bars are one meter in width. (2012). Another species. M. sinocanadorum Russell and Zheng.org (CC-BY-SA). 1892. its neck can be estimated to have been about 12 m long. Necks of long-necked sauropods.7 m. hochuanensis. plate 3). for which much more complete necks are known.
. Furthermore.5). but by comparing this material with the corresponding elements of M. is known from an individual with a complete neck that is 9. Supersaurus scaled from Diplodocus. The basal eusauropod Mamenchisaurus Young. 1874 and 20% in Cryptoclidus Seeley. modified from elements in Hatcher (1901. Diplodocus. figure 4). to the same scale. 1985 includes a cervical vertebra whose centrum is 138 cm long. 1993 is known only from skull elements and anterior cervical vertebrae. Mamenchisaurus modified from Young and Zhao (1972. 1890.5 m in length (personal measurement. M. 1972. 1954 is known from several species. Using the average of 17% for Elasmosaurus. or about 6. and approximately equal to the 7-m neck length reported for Albertonectes by Kubo et al. very long necks evolved in at least four distinct sauropod lineages (Figure 3).TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
8 of 39
length in Muraenosaurus Seeley.1 m (Figure 2. as above. figure 4-1).
Figure 3. Inset shows Figure 1 to the same scale. Sauroposeidon scaled from Brachiosaurus artwork by Dmitry Bogdanov. This is within 6% of Leidy's (1870) estimate of “almost twenty-two feet”. One. hochuanensis Young and Zhao. via commons. familiar from many mounted skeletons in museums. Puertasaurus modified from Wedel (2007a. The known material of the diplodocid Supersaurus Jensen. MPT).
Sauropods The necks of sauropod dinosaurs greatly exceeded in length those of all other animals (Wedel. we can estimate its total neck length as 7. Comparing this with the lengths of similar vertebrae from the closely related Barosaurus Marsh.
4 6..4 5. What were these features?
.5 12 est. The Sauroposeidon cervicals are on average 37% longer than the corresponding vertebrae of its relative. neck-length limits in the range of two to three meters seem to apply to every group except sauropods. whose necks were subject to different forces from those of terrestrial animals. chosen because of unusually long. 2007a.5 est. and measures 8. and its incomplete centrum can be reconstructed after related titanosaurs as having been 105 cm long.5 est. 15. 1.
Taxon Neck length (m) 9. which exceeded this limit by a factor of five.9 C6 ≤1 3. 1988 is known. cervical count.
9 of 39
Sauroposeidon Wedel et al. it seems likely that sauropods shared a suite of features that facilitated the evolution of such long necks. Whatever mechanical barriers prevented the evolution of truly long necks in other terrestrial vertebrates. Table 1 lists a selection of sauropods. sauropods did not just break that barrier – they smashed it..5 m. 8.0 Cervical Longest count centrum (cm) 19 73 C11 19? 12? 10 15 55 C11 15 64 C14 16? 87 C14 15? ≥ 138 13 100 C10 13? 125 C8 17 28 C11 Longest cervical rib (cm) 210 C14 ≥ 410 ≤ centrum 39 C11 48 C11 < centrum ≤ centrum 290 C7 342 C6 72 C14 Maximum elongation index 2. indicating a complete neck length of about 11. 197).5 11.7 4. Cross-scaling with the related Malawisaurus Jacobset al. including overhanging prezygapophyses.1 est. p.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS suggests a complete neck length in the region of 15 m (Wedel.5 8.5 m. Since four separate sauropod lineages evolved necks three or four times longer than those of any of their rivals. and maximum elongation index.0 est. mostly known from complete or nearly complete necks. showing how they vary in length.9 5.0
Mamenchisaurus hochuanensis Mamenchisaurus sinocanadorum Brachytrachelopan mesai Apatosaurus louisae Diplodocus carnegii Barosaurus lentus Supersaurus vivianae Giraffatitan brancai Sauroposeidon proteles Euhelopus zdanskyi
C4 C7 C8 C5 C6 C4
Table 1.9 6. 5. 1993 yields a total neck length of 9 m. 4. short or complete necks. The single known cervical vertebra is 118 cm in total length. The whole neck of the related brachiosaurid Giraffatitan Paul.. centrum length. cervical rib length. 2000a is a large brachiosaurid known only from a sequence of four articulated cervical vertebrae. 2005 is the largest titanosaur for which cervical material has been described. Puertasaurus Novas et al.
FACTORS ENABLING LONG NECKS Discounting the aquatic plesiosaurs. Neck statistics of some sauropods.1 4.
probably in part for this reason: the increased moment caused by neck elongation in a biped must be counteracted by an equal moment caused by a longer or more massive tail. As well as providing a platform for the evolution of large body size. one possible explanation is that.92 times as long as the neck of Diplodocus. 2011). increasing the physiological cost. ceratopsians and elephants. 388–389). In many clades. the stability of the quadrupedal posture also enabled the evolution of longer necks: although progressive elongation displaced the centre of mass forwards from above the hindlimbs. facilitated by characters such as forelimb elongation. columnar limbs and short metapodials (Wilson and Sereno.5 m used for Diplodocus. p. sauropods did not orally process their food. 1878 as 16. 1905 attained masses of 7 or even 10 tonnes (Hutchinson et al. Sheer size is probably a necessary.. but if Parrish's allometric curve pertained then the true value would have been 2. Deinocheirus and Gigantorapor were probably of comparable size. condition for evolving an absolutely long neck. and did not require special equipment for obtaining food. proboscideans. sauropods were under strong selection for larger feeding envelopes. which drove them to evolve longer necks. and therefore the muscle and ligament mass could be reduced. instead either developing large heads on short necks (ceratopsians.75 m. The reduction in head weight would have reduced the required lifting power of the necks that carried them. but does not in itself suggest a causal link between size and neck length. but Parrish (2006. such as the long beaks of azhdarchids (Chure et al. Sauropod heads were simple cropping devices with a brain and sense organs. pp. (2000b. 377). and the longest single vertebra would have been 187 cm long. Mere isometric scaling would of course suffice for larger animals to have longer necks. it remained in the stable region between fore and hindlimbs. p. Small Head The heads of sauropods were small relative to body mass. Quadrupedal Stance One of the key innovations in the evolution of sauropods was quadrupedality.211.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS Absolutely Large Body Size
10 of 39
It is obviously impossible for a terrestrial animal with a torso the size of a giraffe's to carry a 10 m neck. and other giant theropods including Therizinosaurus. The allometric equation of Parrish (2006) is descriptive. but not sufficient.35 = 2. p. varying with torso length to the power 1. 213) found a stronger result: that neck length is positively allometric with respect to body size in sauropods. Computer modelling shows that theropod dinosaurs such as Tyrannosaurus rex Osborn. 24). This suggests that the necks of super-giant sauropods may have been even longer than imagined: Carpenter (2006. because unlike other large-bodied animals such as hadrosaurs. or 21. 2.21 times the length of 7. indricotheres)
. they did not evolve necks as long as those of sauropods with similar mass. As noted by Wedel et al.9 m. because of their size. 2010. 1998. p. Other groups of large-bodied animals have not evolved long necks. they were further lightened by reduced dentition. 133) estimated the neck length of the apocryphal giant Amphicoelias fragillimus Cope. tyrannosaurs) or a compromise of a medium-sized head on a medium-length neck (hadrosaurs. allowing the necks to be longer than would have been possible with heavier heads. However.35.
with eleven or fewer being more typical. Elongation indexes of therizinosaurs such as Therizinosaurus probably did not greatly exceed 1. 1874. and Erketu Ksepka and Norell. The very numerous vertebrae of Elasmosaurus are not very elongate. in which C12 can attain an EI of 4.0 and not exceeding about 1.4 (measured from Mivart. However. This trend reaches is apotheosis in the trumpet
. If the trachea is narrow. 2001). mammals are all limited to exactly seven cervicals. Air-Sac System One limiting factor on neck length is the difficulty of breathing through a long trachea. p. Multiplication of cervical vertebrae obviously contributes to neck elongation. 2002). By contrast.4 (measured from Sachs. 2. figure 4).5 (measured for Struthiomimus from Osborn. having evolved in swans (Banko. 1936. cranes (Johnsgard. among which C5 of Quetzalcoatlus Lawson. figure 7) and much less for the other vertebrae. 1979. But if the trachea is wider. 1960). Elongate Cervical Vertebrae The shape of cervical vertebrae is quantified by the elongation index (EI). For this reason.0. EI in sauropods routinely exceeded 4.. birds-ofparadise (Frith. 346) as the anteroposterior length of the centrum divided by the midline height of its posterior articular face. figures 1–2). non-avian theropods do not seem to have exceeded the 13 or perhaps 14 cervicals of Neimongosaurus Zhang et al. But other long-necked groups are more limited in their elongation of individual vertebrae. attaining as many as 19 in Mamenchisaurus hochuanensis (Young and Zhao. Modern swans have up to 25 cervical vertebrae. azdarchids are variously reported as having seven to nine cervical vertebrae. 2005. and in some cases exceeded 6. then it is difficult to inhale sufficient air quickly – a problem exacerbated by friction of inhaled air against the tracheal wall. 1972. 2001. 1916. moas (Worthy and Holdaway. 1994) and several other groups. figure 3). 3–7). in which the axis can attain an EI of 4. As shown in Table 1. (2000b. A similar degree of elongation is approached by the ostrich.0: Sauroposeidon C6 attained 6. 2. those of oviraptorosaurs such as Gigantoraptor.3 for C2 (measured from Granger and Gregory. 2006 C5 attained 7.1. figure 4c) and an isolated cervical from the Hell Creek Formation might have achieved 15 (measured from Henderson and Peterson.0 (measured from a photograph by MJW of referred specimen IGM 100/1002 of Khaan mckennai Clark et al. mostly having an EI around 1. plate XXIV).0. With the exceptions of sloths and sirenians.71 (personal measurement of FMNH 34426).TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS Numerous Cervical Vertebrae
11 of 39
Many groups of animals seem to be constrained as to the number of cervical vertebrae they can evolve. its volume is increased. defined by Wedel et al. it would be reasonable to expect animals to evolve the shortest possible trachea. 1975 can attain an astonishing 12. in one clade – birds – an elongate trachea is not unusual. reducing the oxygen content of each breath.4 (measured from Witton and Naish. p. and by the giraffe. Paraceratherium seems have been limited to about 3.. 2006.0 (measured for Nanshiungosaurus from Dong. sauropods repeatedly increased the number of their cervical vertebrae. figure 29). 1983). those of ornithomimosaurs such as (probably) Deinocheirus. 2008. but never more. and a larger quantity of used air in the “tracheal dead space” is re-inhaled in each breath. It is greatly exceeded by azhdarchid pterosaurs. and as noted above the marine reptile Albertonectes had 76 cervical vertebrae.
However. Amargasaurus. the head length of sperm whales is positively allometric and increases with age even in adults (Cranford. 1963. Basal
.. However. ARCHITECTURE OF SAUROPOD NECKS Pneumaticity of Cervical Vertebrae Not only did sauropods have a soft-tissue diverticular system. Deinocheirus and Gigantoraptor) and pterosaurs also had had air-sac systems.. 1999. it is from the latter that we are able to infer the former. 1947. 1999. The air-sac system. the internal convolution of the nasal airways and the addition of the trachea spanning from the head to the trunk would give the path from blowhole to lungs a total length of perhaps 9 m. 1999.g. 1984). Paraceratherium) did not. Finally. The various aspects of their architecture are discussed in detail in the next section. Indeed. the trachea coils back on itself so many times that its total length exceeds 800 mm. Vertebral Architecture Aside from the factors previously discussed. The largest sperm whales are up to 20 m in total body length (Gosho et al. It is now well established that sauropods had an air-sac system similar to that of extant birds (Wedel. but the diverticula often invaded the vertebrae. Among other long-necked animals. In a male sperm whale (Physeter) with a total body length of 16 m. cited in Cranford. p. The air space proportion (ASP) of a bone is the proportion of its volume taken up by pneumatic cavities (Wedel. 2005). Dicraeosaurids (Dicraeosaurus. 2003). figures 1 and 3). 30 cm. table 1). 2009). the nasal airways in sperm whales do not take a direct path from the blowhole to the lungs but describe sinuous curves through the head (Cranford. showing that trachea at least that long are possible without an air sac system. As in all cetaceans. 2005). facilitating the evolution of longer necks.. 2006). so a 20-m adult might well have a head slightly more than 7 m long.70 (Table 2) – as lightly built as the pneumatic bones of most birds (Wedel. including cervical air-sacs and extensive cervical diverticula running the full length of the neck. Wedel et al. the length of the head is 5. which would give a head length of 7 m if these largest individuals scaled isometrically with the 16-m whales. the elongation of sauropod necks was made possible by the distinctive architecture of their cervical vertebrae. and related taxa) had reduced postcranial pneumaticity compared to other neosauropods. The presacral vertebrae of most neosauropod taxa had ASPs between 0. it is unlikely that the evolution of long necks in terrestrial mammals has been limited by tracheal dead space. nearly three times the total body length of approx. Janensch. and most likely a similarly efficient flow-through lung (Wedel.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
12 of 39
manucode Phonygammus keraudrrenii (Clench. In a sperm whale with a 7-m head.50 and 0. and in the air space proportion (Schwarz and Fritsch. theropods (including Therizinosaurus. both in terms of the number of presacral vertebrae that were pneumatized. would also have served to lighten long necks. leaving extensive excavations and other traces (e..6 m (Nishiwaki et al. These features would have greatly eased the problem of tracheal dead space. 1141 and figure 4). 1978). In some mature males. Alone among extant animals. due to their very efficient lungs and the large tidal volume of the whole respiratory system on account of the voluminous air-sacs. birds are able to cope with such extreme tracheal elongation. the skull of a sperm whale is separated from the ribcage by the highly compressed cervical series. but the mammals (giraffes. 2000b).
85 0. plate 32) Naish and Martill (2001.81
.54 0.65 0. plate 33) MIWG uncatalogued OMNH 01109 “ “ OMNH 01313 “ “ Ostrom and McIntosh (1966.49 0.55 0.40.59
posterior centrum 0.89 0.49 0.51 0. such as Cetiosaurus. (ASPs of Cetiosaurus and Jobaria are estimates based on personal observations of the holotypes and referred specimens).75 0.34 0.73
posterior centrum 0.68 0.6 0.7 0.63 Source OMNH 01094 “ “ “ OMNH 01340 “ “ CM 555 C6 “ “ “ BYU 11998 BYU 11889 BYU 12866 “ “ MIWG 7306 Naish and Martill (2001.52 0. had much lower ASPs. Jobaria.5 0.52 0. plate 23) Ostrom and McIntosh (1966.69 0.67 0. Taxon Apatosaurus Region C condyle mid-centrum cotyle C condyle mid-centrum cotyle C condyle mid-centrum cotyle C C Brachiosaurus C parapophysis cotyle condyle mid-centrum Brachiosauridae C P P P Camarasaurus C condyle mid-centrum cotyle C condyle mid-centrum cotyle D D mid-centrum mid-centrum mid-centrum ASP 0.85 0. around 0.63 0.32 0.52 0.58 0.69 0. and Haplocanthosaurus.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
13 of 39
sauropods outside or near the base of Neosauropoda. plate
posterior centrum 0.
56 0. ramus anterior centrum Supersaurus Tornieria C C C D Cd mid-centrum mid-centrum condyle (sagittal) mid-centrum 0.71 0.74
posterior centrum 0. figure 7)
posterior centrum 0.5) BYU 12613 “ “ Janensch (1950.7 0.56 0.) D Sauroposeidon C prezygapophysis prezyg.47
14 of 39
Ostrom and McIntosh (1966.56 0.62 0.28 0.59 0.62 0.56 0. figure 16) “ “ Powell (1992. plate 23) Naish and Martill (2001. figure 8.66
posterior centrum 0.) condyle mid-centrum Giraffatitan C C D Haplocanthosaurus C condyle condyle (sagittal) mid-centrum condyle mid-centrum cotyle D Malawisaurus C C Phuwiangosaurus Pleurocoelus Saltasaurus C C D mid-centrum condyle mid-centrum condyle mid-centrum mid-centrum mid-centrum centrum (horiz.) mid-centrum neural spine (horiz. plate 15) Powell (1992. figure 16) OMNH 53062 “ “ WDC-DMJ021 Janensch (1947.78 0.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS 23) D Chondrosteosaurus P Diplodocus C mid-centrum centrum (horiz.56 0.55 0.73 0. figure 8) Janensch (1947.55 0.89 0.54 0. figure 2) CM 879-7 “ “ “ CM 572 MAL-280-1 “ MAL-280-4 “ Martin (1994.42
postzygapophysis 0. figure 2) Lull (1911.78 0.57 0.77
.57 0.82 0.36 0.64 0.55 0. figure 70) Janensch (1947. figure 9) Janensch (1947. figure 4) Janensch (1947.39 0. figure 3) Janensch (1947.75 0.
05 for the “bone foam” inside the beak of the toucan (Rhamphastos toco). it is easy to imagine that the density of a typical neosauropod neck may have been less than 0. which had SG as low as 0. 1985). Currey and Alexander. While the impact of soft-tissue diverticula is more difficult to assess. On the other hand. presacral. nor can they be constructed entirely out of marrow. C C C MEAN mid-centrum mid-centrum 0. Although this dataset is almost three times as large as that reported by Wedel (2005). An important effect of postcranial pneumaticity is to broaden the range of available densities in skeletal construction.55 0.
The effects of pneumatization on the mass of the cervical series have been little explored. all pneumatic. are constrained to build their skeletons out of bone tissue (SG = 1. septae.1 for the entire beak. so an element with an ASP of 0. longer trachea and blood vessels cause physiological difficulties: weight support is only one of the problems imposed by a long neck.5 m range. Although pneumaticity was undoubtedly an important adaptation for increasing the length of the neck without greatly increasing its mass. which allows them to have whole-element densities that are much lower.0.4.40) would have an in-vivo SG of 0. and struts that comprised the vertebrae were primarily made of compact bone (Reid. Cd. 1996). For example. The pneumatic bones of pterosaurs and saurischian dinosaurs are made of bone tissue (SG = 1.8–2. including mammals and ornithischian dinosaurs. the whole-element densities of their postcranial bones will always be between 1. The cranial bones of some birds are even lighter.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS Sauropoda indet.7–0.0 and 2. they cannot be more dense than bone tissue. To date. because that mass acts further from the fulcrum of the cervicodorsal joint. and published images. increasing the moment that must be counteracted by the epaxial tension members. 1985. (2005) reported an SG of 0. Sauroposeidon has ASP values up to 0.40 and therefore SG of 1. Measurements are taken from CT sections.89 and therefore SG as low as 0.46
Table 2. and an SG of 0. Also. Seki et al. 455).2 (calculated from data in Currey and Alexander.0) and air space (SG = 0). The centrum walls. dorsal. and pneumatic pterosaurs attained 3 m. it is clearly not sufficient: while three groups of theropods.60.0 in most tetrapods (Spector. While pneumaticity may be necessary for the development of a long neck. P.61 OMNH 01866 OMNH 01867 OMNH 01882
15 of 39
posterior centrum 0. caudal. 1956).1–1. Therefore. Some sauropod vertebrae were much lighter.8– 2.61 compared to 0. a longer neck remains more mechanically demanding than a shorter neck of the same mass. laminae.93.8–2. evolved necks in the 2–2. The specific gravity (SG) of compact bone is 1. 0.54 0. these remain well short of even the less impressive
. cervical. Animals without postcranial pneumaticity. many basal sauropods had ASPs of 0.0) and marrow (SG = 0. Sections are transverse unless otherwise noted. D.2 in some parts of its vertebrae. this is the lightest form of bone known in any vertebrate. The lightest postcranial bones for which data are available are those of Sauroposeidon and some pterosaurs. the mean is the about same. Abbreviations: C. p.8.30–0. Air Space Proportion (ASP) of sections through sauropod vertebrae.60 (and therefore a compact bone proportion of 0.5 kg/dm3. photographs.
and the various published reconstructions of sauropod neck cross sections (e. figure 2). Consider an ostrich neck scaled up by a linear factor of L. figure 2].3 times as tall as the enclosed vertebra (Figure 4. so the stress on the bracing members that support the neck varies linearly with L.1 of the present paper is modified. 2007. the diameter of the neck is three or four times that of the cervical vertebrae that form its core. 2. ostrich neck in cross section from Wedel (2003. It is not that the soft-tissue is reduced but that the vertebra within is enlarged. But life restorations of sauropods going back to the 1800 have been unanimous that this cannot have been the case in sauropods. and is unrealistic.1). (Diplodocus vertebra silhouette modified from Paul 1997.2. figure 2).) If the necks of sauropods were as heavily muscled as those of ostriches. The weight exerted by the neck is proportional to L3 but the cross-sectional area of the bracing members is proportional to only L2. and mass is reduced by extensive pneumaticity in both the bone and the soft-tissue. the small airspace ventral to vertebra was misidentified as the trachea. the muscular part of the neck is twice as wide and 2. The extent of soft tissue depicted greatly exceeds that shown in any published life restoration of a sauropod. In fact it is a complex of diverticula around the carotid arteries.. Stress is force/area. thin-necked animals such as the ostrich. hypothetical sauropod neck with similarly proportioned soft-tissue. then they would have appeared in cross section as shown in Figure 4. More realistic sauropod neck. Even in long. which is proportional to L3/L2 = L. figure 4. (In the caption to Wedel [2003. and if the trachea and skin and included the soft-tissue is included the dorsoventral thickness of the neck is fully 3. (The weight of the neck acts at a distance proportional to L from the torso. Bone is white. Extent of soft tissue on ostrich and sauropod necks. Schwarz et al. as such overmuscled necks would have been too heavy to lift. figure 4A).g. 9E) all agree in making the total diameter including soft-tissue only 105–125% that of the vertebrae alone. 1997. and soft tissue is grey. air-spaces are black.
16 of 39
Figure 4.) Since isometric similarity is precluded the necks of sauropods had to be reengineered in order to attain such great sizes. so these factors cancel out of the balancing moment equation. 2007. and the bracing members acts at a distance proportional to L above the neck-torso articulation. pp. figure 7. Can that have been done by reducing the amount of
. This is a consequence of scaling. 1. 3.3 times that of the vertebra alone (Dzemski and Christian.. which makes it impossible for sauropod necks to be similar to those of ostriches.
Extent of Soft-Tissue relative to Size of Vertebrae In most extant vertebrates including birds and crocodilians. from which Figure 4.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS sauropod necks. 8A. Paul.
In all vertebrates. comparing the restored neck of a sauropod with that of an ostrich scaled to the same body size. only the fossilized bones are available: but using extant animals as guides. Mm. the birds and crocodilians. shown in green. cervicalis ascendens. in left lateral view. the mechanically significant soft tissues of the neck (muscles. muscle and ligament away from the centre so that they acted with greater mechanical advantage: higher epaxial tension members. axial musculature is divided both into left and right sides and into epaxial
. shown in blue. Simply increasing the size of the vertebrae would not be a good strategy for neck support. M. G. lower hypaxial compression members. tendons and ligaments) can be examined and their osteological correlates identified. In birds. 1995). longus colli dorsalis. H. E. plate 24). Specifically: A. shown in red. F. C. Dashed arrows indicate muscle passing medially behind bone. modified from Wedel and Sanders (2002. C. flexor colli lateralis. M. intercristales. intertransversarii. In effect. Vertebrae modified from Gilmore (1936. But as noted above. interspinales. Mm.
Muscle Attachments In extant animals. this muscle originates from the processes carotici. D. because bone is the densest material in the body apart from tooth enamel and dentine.
Figure 5. In extinct animals. Simplified myology of that sauropod neck. it is apparent that the sauropod neck has not so much reduced the size of the neck muscles as increased the size of the cervicals vertebrae themselves (Figure 4. flexor colli medialis. 1992. except in a very few cases of exceptional preservation. sauropod vertebrae were very pneumatic. Muscles inserting on the cervical ribs. and more laterally positioned paraxials. based primarily on homology with birds. figure 2). moving the bone. M. shown in brown. E. A. M. longus colli ventralis. Muscles inserting on the epipophyses. sauropods inflated their vertebrae within the muscular envelope of the neck. D. G. Mm.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS muscle?
17 of 39
In fact. it is necessary first to examine their extant outgroups. H. osteological features can be interpreted as correlates of the absent soft tissue. Muscles inserting on the ansa costotransversaria (“cervical rib loop”). B.3): they are much larger compared to the torso than in the ostrich. F. typically consisting of 60% air. B. In order to do this for sauropods. so that the ligaments and musculature of the extinct animal can be tentatively reconstructed (Bryant and Russell. Muscles inserting on the neural spine. which are absent in the vertebrae of sauropods. M. Witmer.
which point in the four expected directions (Figure 6. the cervical vertebrae do have epipophyses. Abbreviations: cr. 4. fifth cervical vertebra of Alligator mississippiensis Daudin. sauropod osteology is intermediate between the conditions of crocodilians and birds – so the widely recognized similarity of sauropod cervicals to those of birds (e. as expected based on their mechanical importance.3). cervical rib. the epipophyses and cervical ribs are aligned with the expected vectors of muscular forces. Interspinales. eighth cervical vertebra of Giraffatitan brancai (Janensch. figures 8 and 20). flexor colli lateralis. 1896. Meleagris gallopavo Linnaeus. 1993. 1801. which is interpreted as an interspinous ligament scar like that of birds (O'Connor.e. 2004). in posterior and lateral views. having prominent epipophyses and sizable cervical ribs. distinct dorsally projecting tubercles above the postzygapophyses.2). The epipophyses are both larger and taller than the neural spine. Tsuihiji.
. seventh cervical vertebra of a turkey. Non-avian theropods resembled birds in this respect. The large hypaxial muscles (M. courtesy of MCZ.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
18 of 39
and hypaxial (i. Baumel et al. 2007). longus colli dorsalis and M. and M. 2002. The osteology of the cervical vertebrae makes mechanical sense. traced from photographs by MPT. e. Basic cervical vertebral architecture in archosaurs. 1914) paralectotype HMN SII..g. figures 43 and 46). In most sauropods. neural spine. and in non-archosaurian diapsids such as lizards. In this respect. poz. In these taxa. the major muscle insertions are prominent osteological features located at the four “corners” of the vertebrae (Figure 6. ns. 2004).
Figure 6. Wedel and Sanders. longus colli ventralis) insert on the cervical ribs (Figure 5. which attach to the neural spines rather than to epipophyses (Figure 6. 2. M. traced from O'Connor (2007. 1758. the largest and mechanically most important epaxial muscles (M. traced from Janensch (1950. UA 8678.1). yielding four quadrants. snakes. 1. and the main epaxial neck muscles are the Mm. Tsuihiji. epipophysis. In birds. traced from 3D scans by Leon Claessens. postzygapophysis. but the neural spines are as prominent or more so (Figure 6. it leaves little room for muscle attachments to the spine. Epipophyses are absent. 3. fifth cervical vertebra of the abelisaurid theropod Majungasaurus crenatissimus Depéret. flexor colli medialis. Because this scar covers the entire posterior surface of the neurapophysis. The posterior surface of the neurapophysis is covered by a large rugosity. MCZ 81457.4).. dorsal and ventral to the vertebral column) domains.
The cervical architecture is rather different in crocodilians. ichthyosaurs and plesiosaurs: there are no epipophyses.. cervicalis ascendens) insert on the epipophyses of the cervical vertebrae – that is.
should not be accepted unreservedly.
. Since the prominent neural spine serves as the primary attachment site for epaxial muscles in most theropod outgroups.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
19 of 39
while significant. the condition in birds and other theropods is derived. that of sauropods retains aspects of the primitive condition.
This disparity is particularly evident in the cervical vertebrae (Figure 7). now referred to Isisaurus (See Wilson and Upchurch. modified from Ksepka and Norell (2006. and have short. their morphological disparity was much greater than has usually been assumed (Taylor and Naish. cervical 8. cervical ?13. Those of Apatosaurus Marsh. 1560–1561). 1997 holotype ISIR 335/2. plate 12). the cervical centra of Isisaurus colberti Jain and Bandyopadhyay. “Titanosaurus” colberti Jain and Bandyopadhyay. mid-cervical vertebra. 5. cervical 4 in anterior and left lateral views. 1. modified from Janensch (1950. after Jain and Bandyopadhyay (1997. 4. 3. now referred to Apatosaurus excelsus (see Riggs. but have more dorsally located cervical
. in posterior and left lateral views. 1879a holotype YPM 1980. 1877. now referred to Apatosaurus ajax (see McIntosh. plate 15). “Brachiosaurus” brancai paralectotype HMN SII. 1995). 1903). are anteroposteriorly short and dorsoventrally tall. after Ostrom and McIntosh (1966. 1879b holotype YPM 1861. figure 4). after Ostrom and McIntosh (1966. figure 1) is grayed out in posterior view. 1890. in posterior and left lateral views. cervical 8. 2003). plate XXIV). 2007. lateral view reconstructed after Apatosaurus louisae Gilmore. robust cervical ribs mounted far ventral to the centra. Apatosaurus “laticollis” Marsh. 1936 (Gilmore. now referred to Giraffatitan (see Taylor. 1936.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
20 of 39
Figure 7. 2009). plate XXIV). Erketu ellisoni holotype IGM 100/1803. for example. 1997 are even shorter anteroposteriorly. 1936. the portion reconstructed in plaster (Barbour. lateral view reconstructed after Apatosaurus louisae (Gilmore. in posterior and left lateral views.
Although sauropods shared a common bauplan. Disparity of sauropod cervical vertebrae. “Brontosaurus excelsus” Marsh. figures 43–46). pp. 2. figures 5a–d). in anterior and left lateral views.
the small absolute size of birds means that the forces acting on their necks are so different that we can't assume that sauropod necks functioned in the same ways – just as the problems involved in flight through air for high-Reynolds number fliers such as birds are very different than than they are for lowReynolds number fliers such as fruit-flies. the epipophyses are osteological correlates of the M. by contrast. pronounced cervical ribs. cervicalis ascendens epaxial muscles. Interpretation of sauropods as living animals is made especially difficult by the lack of good extant analogues. with different lineages having evolved dramatically different solutions to the problem of neck elongation and elevation. giraffes. camels. mechanical considerations in the construction of their necks were significantly more important than in their outgroups. which must therefore have been present in sauropods. and their necks so much longer. However.1. and even the longest of their necks. which are sigmoid rather than cylindrical. 6. Furthermore. Because sauropods were so much bigger than their relatives. and some birds (e. Towards the middle ground of these extremes fall the cervical vertebrae of Giraffatitan which are anteroposteriorly longer and dorsoventrally shorter than those of Apatosaurus.
. the best extant analogues for sauropod necks nevertheless remain those of birds: they are the only extant animals that share with sauropods epipophyses above their postzygapophyses.4 m. In light of the demanding mechanical constraints that were imposed on sauropods. but not as anteroposteriorly long or as dorsoventrally short as those of Erketu. 2007b). and pneumatic foramina (Figure 6.g. at about 2. The first two of these features were inherited from a common saurischian ancestor. thin cervical ribs mounted only slightly ventral to the centra. whose aerodynamics are dominated by friction drag rather than form drag. Birds are phylogenetically closer to sauropods. the great size and shape disparity between sauropods and their outgroups means that interpretations of cervical soft-tissue anatomy in sauropods cannot be based purely on the extant phylogenetic bracket method: this alone would be no more informative than trying to determine the anatomy of elephants from that of manatees and hyraxes. the cervical vertebrae of Erketu ellisoni Ksepka and Norell. only one sixth the length attained by some sauropods.4). and have long. but this was possible because air sacs and soft-tissue pneumatic diverticula were likely present in the common saurischian ancestor (Wedel. although we can not conclude from this that they were necessarily the dominant epaxial muscles as they are in birds. longus colli dorsalis and M. Among animals with long necks. and other artiodactyls have very different cervical osteology and (we assume) myology. swans and ostriches) have proportionally very long necks. it is surprising that their necks vary so much morphologically. With all these caveats in mind.. Furthermore.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
21 of 39
ribs. The foramina seem to have been independently derived in birds. 2006b. 2006 are relatively much longer and lower. Specifically. These observations enable us to draw conclusions about sauropod neck soft tissue beyond what the extant phylogenetic bracket would allow. the presence in most sauropods of epipophyses similar to those of birds suggests that sauropods were myologically similar to birds.
4). figure 2). 2. W. Hone personal communication. 1. E. Sauropod cervical vertebrae showing anteriorly and posteriorly directed spurs projecting from neurapophyses. which were proportionally long-necked even by sauropod standards. which has since been lost. epipophyses probably dominated neural spines in Apatosaurus (Figure 7. 2008. after Young (1939. (No specimen number was assigned to this material. D.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
22 of 39
Figure 8. cervical 5 of Sauroposeidon holotype OMNH 53062 in right lateral view. from photograph by MPT. and the epipophyses no higher – a surprising arrangement.
.1) but neural spines may have dominated in Isisaurus Wilson and Upchurch. including Erketu and Mamenchisaurus. the neural spines are strikingly low. they were probably of varying mechanical importance in different taxa. but as they were differently developed in different taxa. Among these sauropods with low neural spines. 7.3. 1939 holotype in right lateral view. In some sauropods. based on their relative heights. 3. reversed. cervical 9 of Mamenchisaurus hochuanensis holotype CCG V 20401 in left lateral view. 2003 and Giraffatitan (Figure 7.)
Neural Spines The neural spines and epipophyses of sauropods both anchored epaxial muscles. For example. photograph by MJW. some have rugose neurapophyses with spurs directed anteriorly and posteriorly from the tip of the spine (Figure 8). cervical 7 or 8 of Omeisaurus junghsiensis Young. as low spines would have reduced the lever arm with which the epaxial tension members worked.
photograph by MJW. ligament attachment site.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
23 of 39
These appear either to have anchored discontinuous interspinous ligaments. Bifid presacral vertebrae of sauropods showing ligament scars and pneumatic foramina in the intermetapophyseal trough. 701–702).e. the cervical neural spines are bifid (i. photograph by MJW. 2000b. Camarasaurus sp. figure 20). Abbreviations: las. pneumatic foramen. 1. pfa. 2. 2007. having separate left and right metapophyses and a trough between them).. dorsal vertebrae CM 584 in dorsal view.. as found in the ostrich (Dzemski and Christian. pneumatic fossa.
Figure 9. pp. as found in all birds (see Wedel et al. Apatosaurus sp. pfo. or to have been embedded in a continuous supraspinous ligament. cervical vertebra OMNH 01341 in right posterodorsolateral view. This morphology appears to have evolved at least
In some sauropods.
figure 2B). Janensch. 2007. and most titanosaurs. which bears greater forces than the anterior part. More direct evidence is found in ligament scars in the troughs of some diplodocids: these can be prominent. 2004. CM 584 (Figure 9. figure 4C). they would presumably be found throughout the neck – although the importance of stability. pers. they are rarely split through the whole series: for example. the bifurcation is very slight in the anterior cervicals and probably of little mechanical consequence. 1977) with no apparent reversals (Wedel and Taylor.
.1) and the dorsal vertebrae of Camarasaurus sp. 2004. and the difficulty of attaining it. seems to have been easy for sauropods to gain. Even in Camarasaurus lewisi BYU 9047. 1996b). is greater in the posterior part of the neck. flagellicaudatans.. Pneumatic diverticula are sometimes found between the centropostzygapophyseal laminae even in sauropods with non-bifid spines. however. the first eight cervicals of Barosaurus do not have bifid spines (McIntosh.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
24 of 39
five times (in Mamenchisaurus. Schwarz et al. Such an arrangement seems unlikely. 1790 (Osborn. Casuarius casuarius Brisson. as shown by the isolated brachiosaurid cervical MIWG 7306 from the Isle of Wight (Naish. it was probably not radically different from neural spine function in vertebrae with unsplit spines. Alexander. 13–14. Bifid cervical vertebrae are extremely uncommon in other taxa. the intermetapophyseal trough housed a large ligament analogous to the nuchal ligament of artiodactyl mammals (e. If bifid spines conferred a great advantage. 2005. 1760 (Schwarz et al.. Whatever the advantages of bifid spines. so the presence of soft-tissue diverticula in this location is probably primitive for Neosauropoda at least. Erketu and Opisthocoelicaudia Borsuk-Bialynicka.1.g. then. 60).g. enabling them to contribute to lateral stabilisation and motion as well as vertical. 1929. because pneumatic foramina are often found in the base of the troughs of presacral vertebrae. pp.g. Wilson and Sereno. in which branches of the “nuchal ligament” attach to the base of the trough (Tsuihiji. it seems likely that however they were used mechanically. and among extant animals they are found only in ratite birds. in which every postaxial cervical vertebra is at least partially bifid (McIntosh et al.. brachiosaurids. MJW. for example in the cervicals of Apatosaurus (Figure 9. Camarasaurus Cope. this is similar to the arrangement seen in Rhea americana. A sauropod neck that was supported from above only by a single midline tension member would need additional horizontal stabilization from muscles and ligaments not directly involved in support. e. 1758 (Tsuihiji. ligament cannot have filled the trough as envisaged by Alexander (1985.2). Rhea americana Linnaeus. This morphology. One possible advantage of bifid spines would be to increase the lateral leverage of the ligaments and muscles that attach to the metapophyses. It has often been assumed that in sauropods with bifid cervical spines. 2007. in review). Even in taxa that do have bifid spines.. 2008). obs). as in the doorknob-sized attachment site in the Apatosaurus sp. 1898. figure 3). including the very long-necked Puertasaurus). plate 4. requires only a single dorsal tension member to stabilize it vertically. However. 1985. 1877. figure` 6E). figure 1). A cantilevered beam. which is what a sauropod neck is in mechanical terms. 1998. p.1). a ligament scar and pneumatic foramen occur together in the intermetapophyseal trough (Figure 9. cervical OMNH 01341 (Figure 9. culminating in Sauroposeidon. but two (one on each side) to stabilize it horizontally.. as some sauropod lineages evolved very long necks with unsplit spines (e. they were clearly not indispensable. figure 5B) and Dromaius novaehollandiae Latham. Since bifid spines always occur together with unsplit spines. as lowering the ligament into the trough would reduce its mechanical advantage. In some specimens. but difficult or perhaps impossible to lose.
1996a. it is clear from preserved sequences of Apatosaurus cervicals (Gilmore. figure 5A). but the insertions are not marked by obvious scars or processes and these muscles were probably less important than those attached to the spine. the epipophyses are approximately half as high above the centrum as the neurapophysis (Figure 7. and also in the basal pterosaur Rhamphorhynchus Meyer. 2003. together with those in theropods and birds. 2001 (Curry Rogers and Forster. 1987. (Figure 7. the size and location of the epipophyses is variable: in C8 of Giraffatitan. Epipophyses are found in most. MJW. Upchurch et al. 2005. the epipophyses are higher than the metapophyses (Figure 7. including birds.. figure 3A) and Saltasaurus Bonaparte and Powell. and no major muscles insert above the postzygapophyses (Tsuihiji. see also Figure 5). if not due to damage to the material. 1978 (Sereno. In those sauropods without ostensible epipophyses.4) and Camarasaurus (Osborn and Mook. the ventral tendons are ossified into long. sauropods and theropods. but the tendons that insert on the cervical ribs do overlap and are free to slide past each other longitudinally. it can not necessarily be concluded that muscles did not insert above the postzygapophyses: phylogenetic bracketing suggests that they did.4). 1993. though not all. Lesothosaurus Galton.. No bird has cervical ribs long enough to overlap. In less derived saurischians. the epipophyses are the insertion points of the largest and longest epaxial muscles in birds. 1936. 1962 (Santa Luca. figures 6–9). they are absent in the titanosaurs Malawisaurus (pers.1). McIntosh et al. figure 9. represent secondary losses. Gomani. 1921. The trend is opposite in Erketu. including sauropods. plate LXVII. This further demonstrates the variety of different mechanical strategies used by different sauropods to support their long necks. figure 5) and in outgroups such as Giraffatitan (Figure 7. but their presence in other titanosaurs such as Rapetosaurus Curry Rogers and Forster. in which the epipophyses increasingly dominate neural spines anteriorly. In any event. figure 1). 2001. 1980.5). plate XXIV. 1991. 1846 (Bonde and Christiansen. In sauropods. but it is difficult to be sure as the vertebrae that seem to most closely approach this condition are at least partly reconstructed in plaster (Barbour. suggests that epaxial muscles were inserting above the postzygapophyses at least by the origin of Saurischia.. obs. figure 8A) and Heterodontosaurus Crompton and Charig.g. cervical ribs are the insertion points for the M flexor colli lateralis. 1877 specimens. e. figure 8) and Isisaurus. M flexor colli medialis and M longus colli ventralis hypaxial muscles (Zweers et al.. suggesting that these insertion points were in use at the base of Dinosauria and possibly Ornithodira. the epipophyses are equally as high as the tips of the neural spines (Figure 7..3). plate 1) that in this genus the neural spines are proportionally higher relative to the epipophyses in the anterior cervicals than in the posterior. 1890. figure 29) indicates that their absences in Malawisaurus and Isisaurus. The existence of epipophyses on the cervical vertebrae of most sauropods. 1992. Baumel et al..TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS Epipophyses
25 of 39
As noted above. whereas in crocodilians the epipophyses are non-existent. The null hypothesis is that the long cervical ribs of theropods and sauropods
. overlapping cervical ribs which are secondarily shortened in Diplodocoidea and in Maniraptoriformes. It is possible that in the posterior cervicals of some Apatosaurus ajax Marsh. in anterior cervicals of Erketu. Cervical Ribs In extant birds. 2004). For example. 2005. Epipophyses are also known in basal ornithischians. although the spines are higher in posterior cervicals. 1980 (Powell.
2008. then the need for this stabilization would be reduced in forms with bifid spines. Ossification of the hypaxial tendons into long cervical ribs may have provided several benefits for sauropods:
Long tendons move the bulk of the hypaxial neck muscles closer to the base of the neck. 2000b. Tendon has a much lower Young's modulus than bone. thick one. and can allow a long. The long hypaxial tendons in the necks of sauropod dinosaurs may have been similarly constrained. 1071).
(It has also been suggested by Martin et al. in prep.e. It has been suggested (Wedel et al. But this hypothesis is badly flawed – see Wedel et al. which would have been especially important in taxa with epaxial tension members concentrated on the midline (i.  that the cervical ribs of at least some sauropods functioned as incompressible ventral bracing members. p. 1993. would raise the question of why other taxa with bifid spines (e. such as diplodocids. in the intermetapophyseal trough. 2002.. In birds. and shorter. p. In general. those with non-bifid spines) as discussed above. and reducing the elastic recoil of the hypaxial tendons would have allowed the hypaxial muscles of sauropods to more directly affect the vertebrae to which they were attached. Camarasaurus) also retained elongate cervical ribs. 272–274). However.e. 2000b. while diplodocids shifted theirs laterally. 2002. 1009). Stiff cervical ribs would have helped provide lateral stabilization for the neck. ossification may be the only viable way for birds to advantageously shift the mechanical properties of these tendons. however. Reduced tendon elasticity is known to improve position control of the involved muscles (Alexander. especially long-necked forms such as Barosaurus and Supersaurus. (2) reduces tendon strain at a given stress. which reduces the lever arm of the neck mass.. it is difficult to understand why diplodocids evolved apomorphically short cervical ribs. pp..g. thicker tendons are less extensible and provide less elastic recoil (Biewener. and (4) reduces damage to the tendon (Landis and Silver. (3) accommodates higher load bearing (to a point. If the primary role of long cervical ribs was in providing lateral stabilization for taxa with midline epaxial tension members. as the insertions of long hypaxial muscles. see below).. pp. proportionally longer and thinner tendons are more extensible and allow more elastic recoil. 2002. p. but we know from osteological evidence (see above) that at least some
. 1153).TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
26 of 39
functioned similarly to the short cervical ribs and long tendons of birds. This. which shifted their epaxial tension members laterally as they were attached to the metapophyses. 2089–2090). 380) that elongate cervical ribs may have played a role in ventrally stabilizing the neck. ossification (or at least mineralization) of tendon has many functional effects: it (1) restricts tendon deformation. Ossified tendons in the lower limbs of birds are typically found distal to the knee (Hutchinson.. thin tendon to behave more like a short. preventing involuntary dorsal extension by contracting antagonistically against the stronger epaxial tension members (which had to counteract gravity in addition to shifting the mass of the neck). p. Mineralization or ossification reduces the extensibility of a tendon.. some aspects of muscle insertion in sauropod necks are mysterious and may be illuminated by closer comparisons to their extant relatives. where the tendons are constrained to be long and thin by the overall construction of the limb. i. and in the case of Mamenchisaurus apparently evolved apomorphically long cervical ribs (Russell and Zheng. 379–380 and Wedel et al. It may be that these taxa retained their epaxial tension members primarily on the midline.) If either of the first two hypotheses is accurate. p.
far below the centra on extremely long parapophyses (Figure 7.
First. Even among diplodocids.
27 of 39
Apatosaurus presents a final riddle regarding cervical ribs. and positioned very low. We know that posterior elongation of the epipophyses is developmentally possible in saurischians. 1879a) of cervical ribs held so far below the centrum – an arrangement that seems to make little sense from any mechanical perspective. because those in the tail of Deinonychus Ostrom. Even if this were so. What function can the ribs have evolved to perform? They were much too short to have functioned efficiently in horizontal or vertical stabilization. triangular in cross-section. the second through seventeenth cervical vertebrae of Euhelopus zdanskyi Wiman. 1. plate 3). Figure 10 shows the cervical skeleton of Euhelopus as it actually is. and reconstructed with speculative muscle attachments that would have been more mechanically efficient: why did sauropod necks not evolve this way? In fact. the vertebrae appear better adapted for anchoring hypaxial than epaxial musculature – even though holding the neck up was important and. Modified from Wiman (1929. and in any case seem over-engineered for these functions. 3. it had extraordinary cervical ribs: very short. so that the neck of Apatosaurus must have been. 1929 cotype specimen PMU R233a-δ (“Exemplar a”). 1969a are extended to the length of a centrum (Ostrom. positioning and moving the neck for feeding would have required fine control.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS diplodocids did have ligaments or muscles anchored within the trough. The long ventral neck muscles would have to attach close to the centrum. much more difficult than drawing it down.2). 2. 7. but they are not present in any known sauropod or other non-avian dinosaur. speculative version of cervical 14 with the epipophyses extended posteriorly as long bony processes. perhaps violent intraspecific combat similar to the “necking” of giraffes. Such processes would allow the bulk of both the dorsal and ventral neck muscles to be located more posteriorly in the neck. cervical 14 as it would appear with short cervical ribs. very robust. 4. Real and speculative muscle attachments in sauropod cervical vertebrae. due to gravity. cervical 14 as it actually exists.1.
. there are several reasons.
Figure 10. with prominent but very short epipophyses and long cervical ribs.
Asymmetric Elongation of Cervical Ribs and Epipophyses A central paradox of sauropod cervical morphology is that in the elongation of the cervical ribs. and second. It is tempting to infer that the autapomorphies of the neck in Apatosaurus are adaptations for some unique aspect of its lifestyle. however. it is difficult to see the benefit in Apatosaurus excelsus (Marsh. 1969b. the much greater length of the cervical ribs in most sauropods enabled the hypaxial musculature to be shifted backwards much further than the epaxial musculature. as the epipophyses are not elongate in any known sauropod. figure 37). and may have to be written off as an inexplicable consequence of sexual selection or species recognition. First. the cervical ribs present a greater area for muscle attachment than the epipophyses do.
. may have been connected by strongly pennate muscles. muscles expand transversely when contracted lengthways. as with the long dorsal muscles of birds. the long multisegment epaxial muscles are free to “bowstring” across the dorsal curvature at the base of the neck (van der Leeuw et al. the difficulty is simply one of fitting the muscle into the space available. subjecting them to greater stress than simple longitudinal tension. can be offered. so shorter muscles need a correspondingly larger cross-sectional area. figure 5). Low neural spines. but this is unlikely to have been a common posture for sauropods (Taylor et al. as does Erketu in the preserved. Since excessively long neural spines would impede neck extension by overlapping with each other. able to contract very forcefully but only over a short distance. 2009). anterior. In birds. For epaxial muscles in sauropods necks. it is actually not as strong in tension. A speculative explanation. because they act at high angles of inclination to the long axis of each vertebra. Although muscles attached to a short spine need to exert greater force to allow for the shorter lever arm. cervicals. although bone is much stiffer than tendon. the work it can do varies with volume. at least. Short neural spines do not indicate poor mechanical advantage for these muscles. (The same effect would also have caused some bending of cervical ribs. shorter spines would be advantageous for improving neck flexibility.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS and precise movements requires short levers. this expansion would strongly bend ossified epipophyseal tendons. Tall neural spines increase mechanical advantage of muscles when the vertebrae are held horizontally. It is particularly notable that mamenchisaurids (Mamenchisaurus and Omeisaurus) have very low neural spines. so that an ossified tendon is more likely to break under load.) Another possibility is that taxa with short spines had shifted almost all of their epaxial muscle attachments to the epipophyses. In an animal adopting this low-spine strategy to neck elongation. But these low spines would have reduced the lever arm with which epaxial tension members acted.)
Short Neural Spines in Long Necks In many cases. they correspondingly need contract a shorter distance in order to raise the neck by the same amount. but the lower stresses in ventral musculature would have reduced the effect. the height above the centrum at which a muscle of given size acts has no effect at all on its ability to move the vertebra through a given arc. A lower limit to neural spine length is imposed by the volume of muscle needed to produce the range of motion. Third. and while the force exerted by a muscle is proportional to its cross-sectional area. as in dicraeosaurids. then. the sauropods with the proportionally longest necks are also those whose necks superficially make the least mechanical sense. (Raising the neck is work. 2001. Counter-intuitively.
28 of 39
the muscles of the neural spine were presumably significant. but the only muscles that insert on the spines and adjacent bony ridges are the small and short Mm. the muscles inserting on the neural spine were also laterally displaced. traced from O'Connor (2007. UA 8678. In intermediate forms such as sauropods the situation is more complex. modified from Osborn and Mook (1921. with either or both sets of muscles being significant in sauropods. traced from photographs by MPT. eighth cervical vertebra of Giraffatitan brancai paralectotype HMN SII. seventh cervical vertebra of a turkey. Blue arrows indicate epaxial muscles attaching to neural spines. in extant birds. However. The very short neural spines serve as the origins of long dorsal muscles running anteriorly from each vertebra. so that they as well as the
. 2005.4. such as Camarasaurus (Figure 11. Meleagris gallopavo. as both the neural spines and epipophyses are prominent – to varying degrees in different species. courtesy of MCZ. and there are no epipophyses at all. In sauropods with bifid neural spines. 4. and would have acted primarily along the midline of the neck. the neural spine is very large and anchors essentially all of the large multisegment epaxial muscles (Tsuihiji.1).5). 11. figure 2). traced from Janensch (1950. 2. In extant lizards and crocodilians. In sauropods with unsplit neural spines. figures 43 and 46).2). plate LXVII). 3. traced from 3D scans by Leon Claessens. as in non-avian theropods (Figure 11. and green arrows indicate hypaxial muscles attaching to cervical ribs. the epipophyses are more prominent and significant than the neural spines and serve as insertion points for all of the multisegment dorsal muscles. fifth cervical vertebra of the abelisaurid theropod Majungasaurus crenatissimus.
Homology and Analogy of Vertebral Features Bony attachment sites for the large cervical muscles have varied along the evolutionary line from basal amniotes to birds (Figure 11). The muscles of the epipophyses were also present. red arrows indicate epaxial muscles attaching to epipophyses. but because their insertions are positioned laterally. the action of these muscles would have functioned both in support and in lateral movement. fifth cervical vertebra of Alligator mississippiensis. Showing muscle attachment points in phylogenetic context.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
29 of 39
Figure 11. intercristales. interspinales and Mm. 5. the principle epaxial muscle migrate from the neural spine in crocodilians to the epipophyses in non-avial theropods and modern birds. 1. While hypaxial musculature anchors consistently on the cervical ribs.3). reconstruction within AMNH 5761/X. as in basal archosaurs (Figure 11. such as Giraffatitan (Figure 11. eleventh cervical vertebra of Camarasaurus supremus. figures 8 and 20). “cervical series I”. MCZ 81457. Epipophyses are absent. Archosaur cervical vertebrae in posterior view.
only seven cervical vertebrae.4. so both and air-sac system and vertebral pneumaticity are precluded. It is tempting to imagine an evolutionary pathway in which bifurcation of neural spines was an intermediate step in the evolutionary shift of the insertions of the large multisegment epaxial muscles from the neural spine to the epipophyses.or two-segment Mm. p. However. then. Nevertheless. no air-sac system and no vertebral pneumaticity. almost no mammal has evolved more than seven cervical vertebrae. In defence of giraffes. therizinosaurs and to a lesser
. because they have relatively small torsos. the absolute size constraints imposed by flight make it unlikely that pterosaurs would have greatly exceeded this mark even had they survived the endCretaceous extinction. but is dominated by epipophyses. Birchard and Deeming. 2004. the eggs approach a point at which the shell cannot simultaneously be thick enough to support the egg and thin enough for the hatchling to break out of (Murray and Vickers-Rich. longus colli dorsalis would have had the dual function of support and lateral motion. and the strong mechanical constraints on the latter: as body size increases. their vertebrae have evolved in a way that is analogous with the true bifid spines of sauropods even though it is not homologous. is that from a myological perspective.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
30 of 39
Mm. The three theropod clades mentioned above (ornithomimosaurs. longus colli dorsalis. CONCLUSIONS: WHY GIRAFFES HAVE SUCH SHORT NECKS Reviewing the characters that facilitate the evolution of long necks. they are relative latecomers in evolutionary terms: given a few tens of millions more years. But in some respects they seem locked into a mammalian pattern that will always prevent them from matching the necks of sauropods: extensive oral processing of food requires a large head with heavy teeth. simply because they are small bipeds. Some of the other long-necked taxa listed in Table 3 seem to have been better equipped to evolve longer necks. 2009). they are shorter by a factor of six than those of the longest sauropods. Similarly.5. it is conceivable that they might overcome some of these disadvantages to evolve longer necks. Although the necks of giraffes are the longest of any extant animals. where a small neural spine remains in the cervical of Majungasaurus. It is impressive the azhdarchid pterosaurs seem likely to have achieved 3m while retaining flight: no doubt their pneumaticity was a key feature in making this possible in spite of their large heads. probably because of the tight correlation between adult body size and egg size. intercristales and Mm. despite the prerequisite small heads and avian lung. The sequence instead seems simply have been one of progressive reduction of the neural spine and enlargement of the epipophyses. the one. as shown in Figure 11. relatively large. ostriches seem unlikely ever to evolve really long necks. heavy heads. it is apparent that only sauropods have them all (Table 3). The outcome of this evolutionary sequence. and the mammalian lung has attained a local maximum of efficiency that makes it unlikely ever to evolve into something analogous to the avian flowthrough lung. Birds seem unable to attain sizes exceeding the 500 kg of the “elephant bird” Aepyornis maximus. This is particularly clear in Figure 11. 212. Absence of elongated cervical ribs may also impede neck elongation. modern birds have functionally bifid neural spines: that is. as bifid spines are not known in taxa along the line to birds – only in sauropods and a few modern birds. In sauropods with bifid spines. interspinales shared the function of lateral stabilization and movement with the multisegment Mm. this explanation cannot be correct.
with a 104 cm humerus from the late Norian or Rhaetian indicating a Camarasaurus-sized sauropod only about ten million years after the first known dinosaurs (Buffetaut et al.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
31 of 39
extent oviraptorosaurs) appear to have had small heads. Finally. non-avian theropods would have been the best candidates for evolving sauropod-like neck lengths. it should be noted that all three of the long-necked theropods discussed above are known from incomplete remains that do not include any informative cervical material. If theropods did not evolve larger body size in the 150 million years available to them. The long-necked theropods may not have been under the same selection pressure to evolve long necks as were sauropods. Neck-elongation features by taxon. and potential for large body size. 2002b).. and the demands of bipedal locomotion may have prevented them from evolving the giant body sizes that are required for very long necks. and so has no selective pressure to evolve a yet longer neck. the ostrich is proportionally long-necked but feeds mostly from the ground (Dzemski and Christian. Among extant theropods. On the other hand. they might have gone on to attain larger size. Why did they not evolve necks as long as those of sauropods? Possible reasons include the following:
All theropods were bipedal. sauropods attained large size very quickly in evolutionary terms. If they were omnivorous. for example. All of the largest long-necked theropods lived in the Late Cretaceous. It is possible that neck length was positively allometric in these clades. Were it not for the end-Cretaceous extinction. two of them in the Campanian–Maastrichtian. 2007). and they may have had necks somewhat longer than isometric scaling suggests.
. due to the combination of pneumaticity. as well pneumatic systems that invaded their vertebrae. no other clade has all of the suggested adaptations for long necks that are found in sauropods. then their use of more nutritious food may have mitigated the need for increased feeding envelopes.
Absolutely large body size
Numerous cervical vertebrae
Elongate cervical vertebrae
Human Giraffe Ostrich Paraceratherium Therizinosaurus Deinocheirus Gigantoraptor Arambourgiania Sauropods ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔
Table 3. Had they not died out at the end of the Cretaceous. it seems likely that they did not have the potential to do so. as in sauropods. small heads in some clades.
In summary. proportionally similar in size to those of sauropods.
L. Stadtman. E. M.I. Czaplewski.M. 279:91–101. Nouvelle Série. In Kramarenko. New York. B.. P. Hutt (Dinosaur Isle) for access to specimens. Tendons and ligaments: structure. Claessens (College of the Holy Cross) provided unpublished images of alligator vertebrae.). Y. and Powell. Cambridge.F. North American Fauna Series.A. Jacobs and D. B. and R..E. E. Theropoda). 1890. Zoological Journal of the Linnean Society. Witton (University of Portsmouth) provided helpful discussion on pterosaur necks. Biewener..org/index.E. REFERENCES Alexander. W. 2003. Comparative Biochemistry and Physiology. D. Person (Oklahoma Museum of Natural History). Mechanics of posture and gait of some large dinosaurs. P. J. northwestern Argentina (Sauropoda–Coelurosauria– Carnosauria–Aves).paleoglot. Henrici (Carnegie Museum of Natural History). Collagen: Structure and Mechanics. Breazile. 24:388–400. We used translations of several papers from the Polyglot Paleontologist web-site (http://www.S.cfm).
. 83:1–25.. Rozhdestvensky. p. Luvsandansan. 2008. and S. H. M. Barsbold. Cifelli. P. J. 1993. 217-232.-M. L. Hone investigated the status of the Omeisaurus junghsiensis material and allowed us to note his conclusion.K. B. US Fish and Wildlife Service.H. LLC. N. Notes on the Paleontological Laboratory of the United States Geological Survey under Professor Marsh.Y. nov.. In Fratzl. The Trumpeter Swan. A. P. V. Lamanna. L. Notes et Mémoires sur le Moyen-Orient. 7:229–234. N. Scientific News: 5. The American Naturalist. D. and Mazin. Britt... D.). Bonaparte. A. Mémoires de la Société Géologique de France. Voronin. Paleontology and Biostratigraphy of Mongolia. B.. Sellers (University of Manchester) clarified our understanding of mechanical advantage. I.. Handbook of Avian Anatomy: Nomina Anatomica Avium (second edition). 63.F. A. R. sp. Transactions. and A.E. R. (In Russian) Baumel. M. No. p.. E. A. New information on Therizinosaurus (Therizinosauridae. 1960. Journal of Zoology. R. (eds. Arambourg. C. Winkler (Southern Methodist University). Nauka Press. Titanopteryx philadelphiae nov. ptérosaurien géant. J.N. Moscow.. Springer Science+Business Media. King.C. Washington. and J. C. M. gen. J. Trofimov. 1980. D. L.). 133:1001–1011. Tendon elasticity and muscle function. Alexander.E. W. R. Lovelace (Wyoming Dinosaur Center) provided a cross-sectional photo of a broken Supersaurus cervical for the ASP calculations. 3. N. A continental assemblage of tetrapods from the Upper Cretaceous beds of El Brete. and Reshetov. J.. (eds. and Christiansen. Birchard.. p. London: Geological Society. Joint Soviet-Mongolian Paleontological Expedition. 76– 92.A.C. and Vanden Berge. D. Barbour. G. 269–284. 2009. Bonde.C.. J. D S. C. A. In Buffetaut.M. Ksepka (American Museum of Natural History) provided highresolution versions of the figures from his description of Erketu and L. D. Avian eggshell thickness: scaling and maximum body mass in birds. Banko. 139:19– 28. 1985. Evans. J. Barsbold.J. Nuttall Ornithological Club. (ed. Berman.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS ACKNOWLEDGMENTS
32 of 39
We thank R. W. Evolution and Palaeobiology of Pterosaurs. 1959. and Deeming. The detailed anatomy of Rhamphorynchus: axial pneumaticity and its implications. Scheetz (Brigham Young University). 2002. T. mechanical behavior and biological function. 1976. K. Part A.
The American Naturalist. 1760. The Condor. Ob indrikoterii (Indricotherium n. Mongolia. J. 89:180–184. gen. E. (In Chinese) Cameron. and Wei. The first giant dinosaurs: a large sauropod from the Late Triassic of Thailand. 36:131–137. genres. 1962. and Russell. 1994. sp. 2010. 25:5–10. H. E.A. On a gigantic saurian from the Dakota epoch of Colorado. Cope.M.. 1878. M. Currey. E.B. E. First complete sauropod dinosaur skull from the Cretaceous of the Americas and the evolution of sauropod dentition. A.). Nature.J. 21(2):209–213. 37:5–64. H. 1999. Bauche. Tracheal elongation in birds-of-paradise. M. and Csiki. Ouvrage enrichi de figures en taille-douce. D. J. A new ornithischian from the Upper Triassic of South Africa. Palaeontologia Polonica. & les noms vulgaires. J. Curry Rogers. Paris.B.D. Journal of Zoology. ceux que leur ont donnés les différentes nations. Clark. Z.. 2001. from the Upper Cretaceous of Mongolia. Clench. 1978.. 2002a. Biggest of the big: a critical re-evaluation of the mega-sauropod Amphicoelias fragillimus Cope. and Charig.. 1868. 1915. Suteethorn. Vertebrata PalAsiatica. 97(4): 379–391.
.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
33 of 39
Borissiak.A. A. 196:1074–1077. and du Toit. T. 12:563–566. Comptes Rendus Paleovol. Whitlock. E.P. Loeuff. and Alexander. 1868:92–93. Naturwissenschaften. D. 1:131–134. A. and Wilson. McN. avec les citations des auteurs qui en ont traité. American Journal of Science.. 2001. 1992. A new camarasaurid sauropod Opisthocoelicaudia skarzynskii. S.W. Brisson. M. J.D. J. Journal of Vertebrate Paleontology. 80:423–430. 2002b. The American Naturalist. and Khansubha.W.A. New Mexico Museum of Natural History and Science Bulletin. Series 2. Cai. 32:181–194. 169:130–135..D. Ukhaa Tolgod. n. K. Z. Cuny. Tome V. R. Naturwissenschaften. The thickness of the walls of tubular bones. Tong. Buffetaut. Paleontological Bulletin. and Forster. J. R. Remarks on a new enaliosaurian.g. On Elasmosaurus platyurus Cope.D.D.A. 1870. Last of the dinosaur titans: a new sauropod from Madagascar. Zhejiangopterus linhaiensis (Pterosauria) from the Upper Cretaceous of Linhai. Crompton. F. A laquelle on a joint une description exacte de chaque espece.. 1977. Carpenter. V.N. Winning by a neck: tall giraffes avoid competing with shorter browsers. 2006. Chure.T. 206:453–468. C. n. les noms qu'ils leur ont donnés.. 1985. Proceedings of the Academy of Natural Sciences of Philadelphia. Philosophical Transactions: Biological Sciences. Zhejiang. J. Cope.. Bryant. (In Russian) Borsuk-Bialynicka. The sperm whale's nose: sexual selection on a grand scale? Marine Mammal Science. Norell.Z. 2007. Two new oviraptorids (Theropoda: Oviraptorosauria). 1878. K. The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Geologiskie Vestnik. Britt. Grigorescu.H.. Geology and paleontology: a new species of Amphicoelias. Elasmosaurus platyurus. especes & leurs variétés. and Barsbold. Buffetaut.. M. 15(4):1133–1157. E. 1877. 50(148):140–141. E.A.J. Cope. Upper Cretaceous Djadokhta Formation.. 337:405–418. Cope. B. Ornithologie ou méthode contenant la division des oiseaux en ordres. Nature. 412:530–534. China. Cranford. A new giant pterosaur with a robust skull from the latest Cretaceous of Romania. 1:103–109. H. A. sections.
Annals and Magazine of Natural History. p. Histoire Naturelle. Marine Fisheries Review.J. On the cervical vertebrae of the Pterodactyloidea (Reptilia: Archosauria). C. F. Note sur les dinosauriens sauropodes & théropodes du Cretace Superieur de Madagascar. 1:1–63 and plates I–XIII. 52:138–159. Diplodocus (Marsh): its osteology.. and Christian. 1901. Nanxiong: Science Press.B. and Martill.T. Depéret. 2005. Gomani. 342–350. gigantic fossil rhinoceros of Central Asia. Mesozoic and Cenozoic Red Beds of South China: Selected Papers from the Cretaceous–Tertiary Workshop. Frith. 1911. Journal of Morphology. Zoological Journal of the Linnean Society. 2011. Physeter macrocephalus.27A:1–37. and Peterson. Abhandlungen. 2007. London.B. 1978. Memoirs of the Carnegie Museum. 1801. An azhdarchid pterosaur cervical vertebra from the Hell Creek Formation (Maastrichtian) of southeastern Montana. Paris.C. 1996. C. C. Granger. E. C. Howse. Paraceratherium bugtiense. Journal of Vertebrate Paleontology. Bulletin de la Société Geologique de France. Hutchinson. Dufart. Annals and Magazine of Natural History. Generale et Particuliere des Reptiles.M. Neues Jahrbuch für Geologie und Paläontologie. W.E. D.K. http://palaeoelectronica. 268:701–714. J. Correction of generic name [Thaumastotherium to Baluchitherium]. M. J. PLoS ONE 6(10):e26037. 199:221–247. Palaeontologia Electronica. preliminary notice. 8. and Makovicky.R.1371/journal. The evolution of hindlimb tendons and muscles on the line to crowngroup birds. Adaptive significance of tracheal elongation in manucodes (Paradisaeidae). Frey. 2006. University College London. Molnar. Forster-Cooper. Osteology of Apatosaurus. The sperm whale.M. 787:1–3. 11:175–298. J. E.D. P.). Unpublished MSc Thesis. K. A. 96:552–555. The Condor. Flexibility along the neck of the ostrich (Struthio camelus) and consequences for the reconstruction of dinosaurs with extreme neck length. 8:711–716. J. and Gregory. 1986. 26(1):192–195. Hatcher. and Breiwick. Gilmore. with special reference to specimens in the Carnegie Museum. F.0026037
. V. 24:176–194. 1993.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
34 of 39
Daudin. 133:1051–1086. W. Bates. 1913. Henderson. the basal family of ornithischian dinosaurs (Reptilia: Ornithischia).M. Pterodactyloidea): one of the world's largest flying animals. G. (In Chinese) Dzemski. A revised restoration of the skeleton of Baluchitherium.W. In Institute of Vertebrate Paleontology and Paleoanthropology and Nanjing Institute of Paleontology. 1936. Volume 1.1. M. 1935. (eds.R. and growth. ontogeny. Forster-Cooper. 1994.. M. Rice. Sauropod dinosaurs from the Early Cretaceous of Malawi. Z.htm Gosho. UK.org/2005_1/gomani27/issue1_05.. Memoirs of the Carnegie Museum. Allen. 12:504. a new genus of Rhinocerotidae from the Bugti Hills of Baluchistan. S. Dong. Paläontologische Zeitschrift. doi:10. D.pone.9MB. 1896. 2002. American Museum Novitates. Evans. 1984. Comparative Biochemistry and Physiology. P.M. Galton. 6. Part A. A reappraisal of Arambourgiania (Pterosauria. The Cretaceous dinosaurs of South China.E. 1979. C. A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion. 88:307–328.B. with a restoration of the skeleton. An investigation into the neck flexibility of two plesiosauroid plesiosaurs: Cryptoclidus eurymerus and Muraenosaurus leedsii.. taxonomy and probable habits. J. Hutchinson. Africa. Fabrosauridae. J.W.M. 46(4):54–56.
Marsh. 1983. 183–210 and plates XI–XX. Downs. genera. ipsarumque varietates. S. O. 1911. R. E. ordines. synonimis. R.C. J. 1877. Leigh and Sotheby.A. Series 3.J. Cranes of the World. Croom Helm. and Norell. 45:697–709. and Henderson. Landis. Discovery of the holotype of the
. 133:1135–1157. Ksepka. and Barsbold. Supplement 7. 32:(3): 557–572. 1914. Janensch. 1870. 1985. 1947. American Journal of Science. H.L. 3508:1–16.C. Notice of new Jurassic reptiles. Martill. a long-necked sauropod from Bor Guve (Dornogov Aimag. 2006. American Museum Novitates. 1998. Principal characters of American Jurassic dinosaurs. The structure and function of normally mineralizing avian tendons. complectens avium divisionem in classes. Jensen. Edition 10. 1790. sive systema ornithologiae. American Journal of Science. a new elasmosaur (Reptilia. Systema naturae per regnum tria naturae secundum classes.A. D. O. Could pterosaurs fly? Science.M. Ornithomimids from the Nemegt Formation of Mongolia. R. 17:86–92. Maryland Geological Survey.A. O.. differentiis. (in Russian) Marsh. 1993. Journal of Vertebrate Paleontology.L.M.R. Pneumatizitat bei Wirbeln von Sauropoden und anderen Saurischien. Linnaeus. genera. Palaeontographica. Palaeontographica. Series 3. 18:501–505. species. Maleev. and Gomani. 22:195–207. 1879a. Lull. Langston. W.. Series 2. New material of an Early Cretaceous titanosaurid sauropod dinosaur from Malawi. M. S. Description of new dinosaurian reptiles. E.A. Kubo. D. 17:114–136.M. M. ordines. Three new sauropod dinosaurs from the Upper Jurassic of Colorado. 1981. Lawson. 1879b. 1997. Kobayashi. 14:514–516. Johnsgard. Priroda.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
35 of 39
Jacobs. 2012. 36:523–534. 2002. and Silver. 2006. Lower Cretaceous. Die Wirbelsaule der Gattung Dicraeosaurus. New turtle-like reptile in Mongolia. 2:35–133. Series 3. J.T. Janensch.H. W. DA. W. 1950. Journal of Vertebrate Paleontology.N. American Journal of Science. locis. W. Übersicht über der Wirbeltierfauna der Tendaguru-Schichten nebst einer kurzen Charakterisierung der neu aufgefuhrten Arten von Sauropoden. American Journal of Science. Comparative Biochemistry and Physiology Part A. American Journal of Science. Janensch. 3:27–93. 3:106–108. and Bandyopadhyay. 188:676–677. loci. Stockholm: Salvius.A. J. Frey. Archiv fur Biontologie.T. Die Wirbelsaule von Brachiosaurus brancai. Leidy. Albertonectes vanderveldei. Systematic Paleontology. 3:1–25. 1929..S. 39:81–86. London. Journal of the Paleontological Society of Korea. Marsh. Series 3. 1890. W. Supplement 7. Janensch. Index ornithologicus. T. Y. Mitchell. Palaeontology. Part II. W.C. Notice of new dinosaurian reptiles from the Jurassic formation. Palaeontographica. Erketu ellisoni. descriptionibus. New titanosaurid (Dinosauria: Sauropoda) from the Late Cretaceous of central India.. P. And Khoury. Volume 1. London. 1758. C. Lower Cretaceous: Vertebrata. Winkler. 3:81–110. 1975. D. adjectis synonymis.C. Great Basin Naturalist. E. On the Elasmosaurus platyurus of Cope. W. cum characteribus. Pterosaurs. 1954. L. Jr. Jain.. 49(147):392. Sadaqah. species. 244:92–102 Latham. D. Mongolia). Marsh.. Scientific American. F. Supplement 7. Sauropterygia) from the Upper Cretaceous of Alberta. &c. O.M.
(eds. Sauropod Vertebra Picture of the Week. 1987. H. p. 1996b. F. W. C.E. 1988). E. Nishiwaki. D. 1:1–20.).S. and Agnolin. 1874. V.F. J. J. P. and Carpenter. and Gillette. P. O'Connor. 1996a. 185–241. J.. Magnificent Mihirungs. Boxtree Books. Gaia. downloaded 17 June 2012. Skeletal adaptations of Ornitholestes. 10:219–233.). On the axial skeleton of the ostrich (Struthio camelus).R.. 154-159. McIntosh. 2007. The genus Barosaurus Marsh (Sauropoda..H. p. Neues Jahrbuch für Geologie und Paläontologie. Miller. 1916.S. and Martill. H. Martin-Rolland. China Ocean Press. 119-123. but beams: the biomechanics of sauropod necks. Giant titanosaur (Dinosauria.
. Diplodocidae). Bulletin of Gunma Museum of Natural History. (eds. Mobility and feeding of Cetiosaurus (saurischia. Short Papers. In Martill. Scientific Reports of the Whales Research Institute. 2008. Sauropoda) from the Late Cretaceous of Patagonia. p. The postcranial axial skeleton of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Bulletin of the American Museum of Natural History. K. Fourth Symposium on Mesozoic Terrestrial Ecosystems. Bulletin of the American Museum of Natural History. 1994.com/2008/03/30/invading-the-postzyg/ Naish. D. J. 1846. L. D. P. K. St. Martin. Naish D. D. George.C. Nuevo Serie. 2004. Indiana University Press. 1905. and Naish. 1:1–87. In Sampson. Murray. Calvo. London. 1959 and the status of Arambourgiania and Quetzalcoatlus. Saurischian dinosaurs 1: Sauropods. Novas. In Currie. J. p.). Transactions of the Zoological Society of London.). 1998.). 2001. Beijing. Tyrannosaurus. p. E. 21:259–265. and Vickers-Rich. and Maeda. 17:l– 17. Osborn. Not cranes or masts. Bloomington. 41:73–116. and Krause. M. (eds. http://svpow. Thunder Lizards: the Sauropodomorph Dinosaurs. Change of form in the sperm whale accompanied with growth. Remarks on the North American sauropod Apatosaurus Marsh. H. S. A.. 1:113–120. 2005.v. P.M. In Tidwell. and Wang. 1963. McIntosh. Martin.M. Martin. Dinosaurs of the Isle of Wight. and Parker.F. 10:147–153. Stadtman. D.J. (eds.M. Tokyo. Y. Osborn. In Sun. A new nearly complete skeleton of Camarasaurus. Y.. Osborn. Invading the postzyg. Bloomington. S. Miles. Struthiomimus. Cloward. H. Mivart. Abhandlungen. The Palaeontological Association. Society of Vertebrate Paleontology Memoir 8. Ohsumi. 127-162.F. Drumheller. Palaeontographica. Baby sauropods from the Sao Khua Formation (Lower Cretaceous) in Northeastern Thailand.L. 1995. The osteology of Camarasaurus lewisi (Jensen. sauropoda) – why the long neck?. D.E. 2005. Revista del Museo Argentino dei Ciencias Naturales. 1898. Pterodactylus (Rhamphorhynchus) gemmingi aus dem Kalkschiefer von Solenhofen. (eds.A..G. Oryctos. V...S. 7:37–41. Meyer. and Koster.S. Brigham Young University Geology Studies. Tyrannosaurus and other Cretaceous carnivorous dinosaurs. V. 8(7):385–451. McIntosh. and Frey. J. K.F. McIntosh. 207:57–76.W.. F. Additional characters of the great herbivorous dinosaur Camarasaurus. Indiana University Press. Sixth Symposium on Mesozoic Terrestrial Ecosystems and Biota. Salgado. J. 38-77. Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. J.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
36 of 39
giant pterosaur Titanopteryx philadephiae Arambourg.D.
Part 1: Introduction: introduction to bony tissues. 2005. 30:2082–2095.A.D. Actas del Segundo Curso de Paleontologia en Cuenca. Sachs.L.W. Ornithischia) from the Stormberg of South Africa. N. Spain. 21:5–19. J. 1997. G.S. and Mook. D.D. (eds. T. Pneumaticity and soft-tissue reconstructions in the neck of diplodocid and dicraeosaurid sauropods.M. A. Instituto Juan de Valdés. 2006. Yale University Press. D.S. Geological Series.. Philadelphia. Blob. D. E. Jouve. Ostrom. M.). and Meyer. 129-154. an unusual theropod from the Lower Cretaceous of Montana. A new theropod dinosaur from the Lower Cretaceous of Montana. 128:1–17. Cuenca. Eclogae Geologicae Helvetiae.R. 1903.F. Hunteria. Special Publications. 1988. Pneumatic structures in the cervical vertebrae of the Late Jurassic Tendaguru sauropods Brachiosaurus brancai and Dicraeosaurus.2003. Field Columbian Museum. and Buscalioni. Annals of the South African Museum. 99:65–78. H. 5:92–106. Pereda-Suberbiola.08 Powell.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
37 of 39
Bulletin of the American Museum of Natural History. p.SP.J.217.H. London. and using them to estimate the mass of dinosaurs. p. 30:1– 165. 79:159–211. Geological Society. and Rosenberg. (eds. X.). The brachiosaur giants of the Morrison and Tendaguru with a description of a new subgenus. 2:1– 14. Marsh's Dinosaurs: the Collections from Como Bluff. Amphicoelias and other sauropods of Cope.E. Giraffatitan. and a comparison of the world's largest dinosaurs. 165-230. U. C.S.A. Parrish. Schwarz. Dinosaur models: the good..T. Russell.H.C. doi: 10. G. G.. 41:25–72. E.E. Palaeontologia Polonica. Canadian Journal of Earth Sciences. 2006. J.A.. J.. and McIntosh. Osteology of Deinonychus antirrhopus. (eds. 1921. Los Dinosaurios y su Entorno Biotico. The origins of high browsing and the effects of phylogeny and scaling on neck length in sauropodomorphs. 2007. J. and Amaghzaz. A large mamenchisaurid from the Junggar Basin.. Bouya. p. a new family of theropod dinosaurs. B. Ostrom. R. Z. Paul. Bulletin of the Peabody Museum of Natural History. 1966. Chicago.01. Santa Luca. 35:733–771. Dinofest International: Proceedings of a Symposium Held at Arizona State University.H. J. A new azhdarchid pterosaur from the Late Cretaceous phosphates of Morocco. Paul. New Series.. and Fritsch. Osmólska. Structure and relationships of opisthocoelian dinosaurs. Academy of Natural Sciences.. 217:79–90. 2003.
.S. M. New Haven. M. Reid. E. 2:165–196. 1992. Osborn.). Frey. C. R. Schwarz. University of Chicago Press.S. Postilla. J. Gaudin. G. J. H. A. Paludicola. Iarochène. Ayuntamiento de Cuenca. S. 1980. Riggs. S. Bardet. Camarasaurus. People's Republic of China. 1969b.1144/GSL. 1993. D. Xinjiang. the bad. E.P. Brigham Young University Geology Studies. and Wible. Apatosaurus Marsh. 3:247–387. 201-224. and Zheng. 1969. Deinocheiridae. Amniote Paleobiology. Memoirs of the American Museum of Natural History. and Roniewicz. Ostrom. 52:167–188. Stump. J. In Wohlberg.H. In Carrano. In Sanz. 1969a. Redescription of Elasmosaurus platyurus Cope 1868 (Plesiosauria: Elasmosauridae) from the Upper Cretaceous (Lower Campanian) of Kansas. Part I. Acta Palaeontologica Polonica. Bone histology of the Cleveland-Lloyd dinosaurs and of dinosaurs in general. 1996.L. Osteología de Saltasaurus loricatus (Sauropoda–Titanosauridae) del Cretácico Superior del Noroeste Argentino. The postcranial skeleton of Heterodontosaurus tucki (Reptilia.
2011. Taylor.P. and Toon. W.. and Curry Rogers. 2005. Journal of Zoology.J.).' and the early evolution of Ornithischia.S. Seki. Taylor. Wedel. Winning by a neck: sexual selection in the evolution of giraffe. Paleobiology. London. M. T. H. Sereno. van der Leeuw. G. air sacs. M. neck length. 1996. 53:5281–5296. M. V. Philadelphia. Head and neck posture in sauropod dinosaurs inferred from extant animals. M. M.. A re-evaluation of Brachiosaurus altithorax Riggs 1903 (Dinosauria. Necks for sex: sexual selection as an explanation for sauropod dinosaur neck elongation. Okapis and giraffes. Journal of Vertebrate Paleontology. M. Kleiman.E. and Scheepers. Gale Group. Simmons. University of California Press.B. Wedel. Taylor.P.A. Hone. P. Structure and mechanical behavior of a toucan beak. In Wilson. (eds.J.J.J. Vertebral pneumaticity. Taylor. USA. Berkeley. Integrative Zoology. K. Sauropoda) and its generic separation from Giraffatitan brancai (Janensch 1914).E. 2011. 26(Supplement to Number 3):137A. (ed. Acta Palaeontologica Polonica. p. and Naish. 30:197–208. Postcranial skeletal pneumaticity in sauropods and its implications for mass estimates. Proceedings of the Royal Society. Y. Wedel. 2006b. and Meyers. Spector.P. Saunders.1111/j. Geist. D. and body size in sauropods. 2005. 2:80–85. The long necks of sauropods did not evolve primarily through sexual selection. Journal of Vertebrate Paleontology. doi:10. Michigan.G. M. Wedel. Origin of postcranial skeletal pneumaticity in dinosaurs. The Sauropods: Evolution and Paleobiology.G. Y. and McDade. p. 1874. 51:119–151. Lesothosaurus. 271:45–53.1469-7998. California. Wedel. 54(2):213–220. Palaeontology. Journal of Zoology. M. Journal of Vertebrate Paleontology. M. and waterfowl.. National Science Museum Monographs. a plesosaurian from the Oxford Clay.. American Naturalist. Vol 15: Mammals IV (second edition). D. On Muraenosaurus leedsii. Upchurch.).. P.TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
38 of 39
Seeley. England. Evolutionary morphology of the neck system in ratites. London. 2003. Tsuihiji. University of California. and Naish.00824. Handbook of biological data. 2006a. 2007.G. and Zweers. Homologies of the transversospinalis muscles in the anterior presacral region of Sauria (crown Diapsida). The ligament system in the neck of Rhea americana and its implication for the bifurcated neural spines of sauropod dinosaurs.J. M. Berkeley. 'fabrosaurids. A. and Barrett. Seeley.A. Pneumaticity.H. 2004. Quarterly Journal of the Geological Society.P. The nature of the shoulder girdle and clavicular arch in the Sauropterygia.S. A. 201-228. A new specimen of Apatosaurus ajax (Sauropoda: Diplodocidae) from the Morrison Formation (Upper Jurassic) of Wyoming. Wedel. USA.. 2001. 1892. D. Grzimek's Animal Life Encyclopedia. 2009.B. Wedel.W. fowl. M. R. L.. 2005. P. Unpublished PhD Thesis. In Hutchins. 51(2):243–262. P. T. 263:151–178. 2003. M. Farmington Hills. 148:771–786. 1991. (eds. 285(2):150–161. Postcranial pneumaticity in dinosaurs and the origin of the avian lung. H. 2007a. 299-409. M. An unusual new neosauropod dinosaur from the Lower Cretaceous Hastings Beds Group of East Sussex.J. Acta Materialia. D. W. and Naish. 50:1547–1564. Journal of Vertebrate Paleontology. M. Tomida. M.J. S. Journal of Morphology. D.) 1956.x Toon. Bout. 2006.
. Schneider. Tsuihiji.M. 2009. 11:168–197. 2005. R.J. and the physiology of sauropod dinosaurs.A. 26:1–110. Netherlands Journal of Zoology. J. 24:165– 172.. Senter. 29:243–255. 29:787–806.C.
Part I: Anatomy of the cervical column in the chicken (Gallus gallus L.0013982 Witton. Zhao. Osteology..J. the use of birds as pterosaur analogues and comments on pterosaur flightlessness. C. Zweers. P. Indiana University Press.). a new sauropod from the Early Cretaceous of Oklahoma. X. Witmer. 2002. 1987. Part A. 2000b. and Zhao. Tan. J. Functional Morphology in Vertebrate Paleontology. M. P. 2003. 20:109–114. and Batten. 25:131–155. L. doi:10.L. J. 3:e2271.J.-J. The Lost World of the Moa.H.J. T. Journal of Vertebrate Paleontology. with notes on other fragmentary reptiles from Szechuan. PaleoBios. and Sanders. R.. Cifelli. 2000a. 311:611–828. M.pone. Early evolution and higher-level phylogeny of sauropod dinosaurs. Series I 8:1–30. People’s Republic of China. 2002. 1998. 2001. Szechuan. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Young.000227 Worthy. On a new Sauropoda. X.1371/journal. Zhao.. 1929. 447:844–847.. Wilson. and Naish. 45:343–388. (In Chinese) Zhang. and Tan. X. M. 19:279–315.C. 22(3):1–6. 2010. PLoS ONE. On the size and flight diversity of giant pterosaurs. Palaeontologia Sinica. and Sanders.M. Journal of Experimental Zoology. Wedel. and Upchurch. Society of Vertebrate Paleontology Memoir. D.P. Vertebrata PalAsiatica.. 2009. Nature. nov. Sauroposeidon proteles. 1:125–160. with comments on the cervical ribs of Apatosaurus. Cambridge. Series C. 39(4):282–290. A long-necked therizinosauroid dinosaur from the Upper Cretaceous Iren Dabasu Formation of Nei Mongol. the first dinosaur genus with a 'Gondwanan' distribution. and Koppendraier.-W. doi:10..TAYLOR AND WEDEL – LONG NECKS OF SAUROPOD DINOSAURS
39 of 39
Wedel. Wilson. R. 2008. 3:491–504. M. P. Wiman.-C. J. Institute of Vertebrate Paleontology and Paleoanthropology Monograph. Xu. Cifelli. PLoS ONE. What pneumaticity tells us about 'prosauropods'. C. 1972. Acta Palaeontologica Polonica. 2007. and relationships of the sauropod dinosaur Sauroposeidon. Evidence for bird-like air sacs in saurischian dinosaurs. X. M. A reappraisal of azhdarchid pterosaur functional morphology and paleoecology. Acta Morphologica Neerlando-Scandinavica. p. and Holdaway.). China. M.J.P. R.M. and Tan. 207-222. C. 77. Journal of Systematic Palaeontology. Mamenchisaurus hochuanensis sp. (eds.J. Die Kreide-Dinosaurier aus Shantung.). Wang.-C... Vanden Berge.-C. p. and Habib. and Sereno.N. R. 1995. M. Osteological correlates of cervical musculature in Aves and Sauropoda (Dinosauria: Saurischia). Young. and vice versa.A. Wedel.B.
. Avian cranio-cervical systems.pone. C. J.K. Young.1371/journal. 5:1–68. J.L. Bloomington. X. Wedel.A. P. Cambridge University Press. X. Bulletin of the Geological Society of China. Witton. D. 5(10):e13982. 1954. Evolution and Palaeobiology of Early Sauropodomorph Dinosaurs. paleobiology. 2007b. On a new sauropod from Yiping. A gigantic bird-like dinosaur from the Late Cretaceous of China. In Barrett.C. In Thomason.-H. (ed. 19-33. Special Papers in Palaeontology.. Xu. G.K. Acta Scientia Sinica. A revision of Titanosaurus Lydekker (Dinosauria – Sauropoda).J. Q. R. Wedel.. M. Sereno..A. L. L. X. 1939. R. Kwang. and Sanders RK. 6:1–67.J.