Biomechanical Reconstructions and Selective Advantages of Neck Poses and Feeding Strategies of Sauropods with the Example of Mamenchisaurus youngi

A very long neck is a characteristic feature of most sauropod dinosaurs. In the genus Mamenchisaurus, neck length is extreme, greater than 40 percent of total body length. However, the posture, utilization, and selective advantage of very long necks in sauropods are still controversial. An excellently preserved skeleton of Mamenchisaurus youngi, including a complete neck, provides an opportunity for a comprehensive biomechanical analysis of neck posture and mobility. The biomechanical evidence indicates that Mamenchisaurus youngi had a nearly straight, near horizontal neck posture and browsed at low or medium heights. The results differ from the findings for some other sauropod species, like Euhelopus, Diplodocus, and Giraffatitan (Brachiosaurus) that had been analyzed in previous studies with similar methods. The selective advantage of extreme neck length in sauropods is likely advantageous for different feeding strategies.     

Nuchal ligament reconstructions in diplodocid sauropods support horizontal neck feeding postures

Historically, sauropods have been largely perceived as having vertical, ‘S’-curved necks which were hypothesised to allow them to feed from the canopy of trees. Within the past two decades, this popular perception has been questioned, resulting in a debate over neck posture. The osteological differences between sauropods with horizontal neck posture (Diplodocus), and less horizontally inclined necks (Brachiosaurus) suggest differing life and feeding styles. One differing vertebral feature between these polarised bauplans is the bifurcated neural spine. Regardless of the spine condition, sauropods with and without bifurcated spines have been reconstructed exhibiting the same neck posture. Corroborating histology and morphology in extant taxa highlights the presence of modified vertebral ligaments associated with bifurcated spines. Using these extant taxa to better understand the biomechanics of bifurcated spines, this study proposes alternative soft tissue reconstructions. Previous depictions had the bifurcation trough entirely open or harbouring pneumatic diverticula or muscles; conversely this study proposes that the apices of the bifurcated spines were the anchoring points for a split nuchal ligament, and that the trough of bifurcation was predominantly filled with interspinal ligaments. Ligaments provide energy-efficient elastic rebound, and a paired ligament in the cervical series would aid in prolonged, lateral movement in a horizontal plane (i.e. feeding).     

Histology shows that elongated neck ribs in sauropod dinosaurs are ossified tendons

The histology of cervical ribs of Sauropoda reveals a primary bone tissue, which largely consists of longitudinally oriented mineralized collagen fibres, essentially the same tissue as found in ossified tendons. The absence of regular periosteal bone and the dominance of longitudinal fibres contradict the ventral bracing hypothesis (VBH) postulated for sauropod necks. The VBH predicts histologically primary periosteal bone with fibres oriented perpendicular to the rib long axis, indicative of connective tissue between overlapping hyperelongated cervical ribs. The transformation of the cervical ribs into ossified tendons makes the neck more flexible and implies that tension forces acted mainly along the length of the neck. This is contrary to the VBH, which requires compressive forces along the neck. Tension forces would allow important neck muscles to shift back to the trunk region, making the neck much lighter.     

The Effect of Intervertebral Cartilage on Neutral Posture and Range of Motion in the Necks of Sauropod Dinosaurs

The necks of sauropod dinosaurs were a key factor in their evolution. The habitual posture and range of motion of these necks has been controversial, and computer-aided studies have argued for an obligatory sub-horizontal pose. However, such studies are compromised by their failure to take into account the important role of intervertebral cartilage. This cartilage takes very different forms in different animals. Mammals and crocodilians have intervertebral discs, while birds have synovial joints in their necks. The form and thickness of cartilage varies significantly even among closely related taxa. We cannot yet tell whether the neck joints of sauropods more closely resembled those of birds or mammals. Inspection of CT scans showed cartilage:bone ratios of 4.5% for Sauroposeidon and about 20% and 15% for two juvenile Apatosaurus individuals. In extant animals, this ratio varied from 2.59% for the rhea to 24% for a juvenile giraffe. It is not yet possible to disentangle ontogenetic and taxonomic signals, but mammal cartilage is generally three times as thick as that of birds. Our most detailed work, on a turkey, yielded a cartilage:bone ratio of 4.56%. Articular cartilage also added 11% to the length of the turkey''s zygapophyseal facets. Simple image manipulation suggests that incorporating 4.56% of neck cartilage into an intervertebral joint of a turkey raises neutral posture by 15°. If this were also true of sauropods, the true neutral pose of the neck would be much higher than has been depicted. An additional 11% of zygapophyseal facet length translates to 11% more range of motion at each joint. More precise quantitative results must await detailed modelling. In summary, including cartilage in our models of sauropod necks shows that they were longer, more elevated and more flexible than previously recognised.     

Some sauropods raised their necks—evidence for high browsing in Euhelopus zdanskyi

A very long neck that is apparently suitable for feeding at great heights is a characteristic feature of most sauropod dinosaurs. Yet, it remains controversial whether any sauropods actually raised their necks high. Recently, strong physiological arguments have been put forward against the idea of high-browsing sauropods, because of the very high blood pressure that appears to be inevitable when the head is located several metres above the heart. For the sauropod Euhelopus zdanskyi, however, biomechanical evidence clearly indicates high browsing. Energy expenditure owing to high browsing is compared with energy costs for walking a distance. It is demonstrated for Euhelopus as well as for the much larger Brachiosaurus that despite an increase in the metabolic rate, high browsing was worthwhile for a sauropod if resources were far apart.     

Inter-Vertebral Flexibility of the Ostrich Neck: Implications for Estimating Sauropod Neck Flexibility

The flexibility and posture of the neck in sauropod dinosaurs has long been contentious. Improved constraints on sauropod neck function will have major implications for what we know of their foraging strategies, ecology and overall biology. Several hypotheses have been proposed, based primarily on osteological data, suggesting different degrees of neck flexibility. This study attempts to assess the effects of reconstructed soft tissues on sauropod neck flexibility through systematic removal of muscle groups and measures of flexibility of the neck in a living analogue, the ostrich (Struthio camelus). The possible effect of cartilage on flexibility is also examined, as this was previously overlooked in osteological estimates of sauropod neck function. These comparisons show that soft tissues are likely to have limited the flexibility of the neck beyond the limits suggested by osteology alone. In addition, the inferred presence of cartilage, and varying the inter-vertebral spacing within the synovial capsule, also affect neck flexibility. One hypothesis proposed that flexibility is constrained by requiring a minimum overlap between successive zygapophyses equivalent to 50% of zygapophyseal articular surface length (ONP50). This assumption is tested by comparing the maximum flexibility of the articulated cervical column in ONP50 and the flexibility of the complete neck with all tissues intact. It is found that this model does not adequately convey the pattern of flexibility in the ostrich neck, suggesting that the ONP50 model may not be useful in determining neck function if considered in isolation from myological and other soft tissue data.     

Mechanical implications of pneumatic neck vertebrae in sauropod dinosaurs

The pre-sacral vertebrae of most sauropod dinosaurs were surrounded by interconnected, air-filled diverticula, penetrating into the bones and creating an intricate internal cavity system within the vertebrae. Computational finite-element models of two sauropod cervical vertebrae now demonstrate the mechanical reason for vertebral pneumaticity. The analyses show that the structure of the cervical vertebrae leads to an even distribution of all occurring stress fields along the vertebrae, concentrated mainly on their external surface and the vertebral laminae. The regions between vertebral laminae and the interior part of the vertebral body including thin bony struts and septa are mostly unloaded and pneumatic structures are positioned in these regions of minimal stress. The morphology of sauropod cervical vertebrae was influenced by strongly segmented axial neck muscles, which require only small attachment areas on each vertebra, and pneumatic epithelia that are able to resorb bone that is not mechanically loaded. The interaction of these soft tissues with the bony tissue of the vertebrae produced lightweight, air-filled vertebrae in which most stresses were borne by the external cortical bone. Cervical pneumaticity was therefore an important prerequisite for neck enlargement in sauropods. Thus, we expect that vertebral pneumaticity in other parts of the body to have a similar role in enabling gigantism.     

The Articulation of Sauropod Necks: Methodology and Mythology

Sauropods are often imagined to have held their heads high atop necks that ascended in a sweeping curve that was formed either intrinsically because of the shape of their vertebrae, or behaviorally by lifting the head, or both. Their necks are also popularly depicted in life with poses suggesting avian flexibility. The grounds for such interpretations are examined in terms of vertebral osteology, inferences about missing soft tissues, intervertebral flexibility, and behavior. Osteologically, the pronounced opisthocoely and conformal central and zygapophyseal articular surfaces strongly constrain the reconstruction of the cervical vertebral column. The sauropod cervico-dorsal vertebral column is essentially straight, in contrast to the curvature exhibited in those extant vertebrates that naturally hold their heads above rising necks. Regarding flexibility, extant vertebrates with homologous articular geometries preserve a degree of zygapophyseal overlap at the limits of deflection, a constraint that is further restricted by soft tissues. Sauropod necks, if similarly constrained, were capable of sweeping out large feeding surfaces, yet much less capable of retracting the head to explore the enclosed volume in an avian manner. Behaviorally, modern vertebrates generally assume characteristic neck postures which are close to the intrinsic curvature of the undeflected neck. With the exception of some vertebrates that can retract their heads to balance above their shoulders at rest (e.g., felids, lagomorphs, and some ratites), the undeflected neck generally predicts the default head height at rest and during locomotion.     

Biology of the sauropod dinosaurs: the evolution of gigantism

The herbivorous sauropod dinosaurs of the Jurassic and Cretaceous periods were the largest terrestrial animals ever, surpassing the largest herbivorous mammals by an order of magnitude in body mass. Several evolutionary lineages among Sauropoda produced giants with body masses in excess of 50 metric tonnes by conservative estimates. With body mass increase driven by the selective advantages of large body size, animal lineages will increase in body size until they reach the limit determined by the interplay of bauplan, biology, and resource availability. There is no evidence, however, that resource availability and global physicochemical parameters were different enough in the Mesozoic to have led to sauropod gigantism. We review the biology of sauropod dinosaurs in detail and posit that sauropod gigantism was made possible by a specific combination of plesiomorphic characters (phylogenetic heritage) and evolutionary innovations at different levels which triggered a remarkable evolutionary cascade. Of these key innovations, the most important probably was the very long neck, the most conspicuous feature of the sauropod bauplan. Compared to other herbivores, the long neck allowed more efficient food uptake than in other large herbivores by covering a much larger feeding envelope and making food accessible that was out of the reach of other herbivores. Sauropods thus must have been able to take up more energy from their environment than other herbivores. The long neck, in turn, could only evolve because of the small head and the extensive pneumatization of the sauropod axial skeleton, lightening the neck. The small head was possible because food was ingested without mastication. Both mastication and a gastric mill would have limited food uptake rate. Scaling relationships between gastrointestinal tract size and basal metabolic rate (BMR) suggest that sauropods compensated for the lack of particle reduction with long retention times, even at high uptake rates. The extensive pneumatization of the axial skeleton resulted from the evolution of an avian‐style respiratory system, presumably at the base of Saurischia. An avian‐style respiratory system would also have lowered the cost of breathing, reduced specific gravity, and may have been important in removing excess body heat. Another crucial innovation inherited from basal dinosaurs was a high BMR. This is required for fueling the high growth rate necessary for a multi‐tonne animal to survive to reproductive maturity. The retention of the plesiomorphic oviparous mode of reproduction appears to have been critical as well, allowing much faster population recovery than in megaherbivore mammals. Sauropods produced numerous but small offspring each season while land mammals show a negative correlation of reproductive output to body size. This permitted lower population densities in sauropods than in megaherbivore mammals but larger individuals. Our work on sauropod dinosaurs thus informs us about evolutionary limits to body size in other groups of herbivorous terrestrial tetrapods. Ectothermic reptiles are strongly limited by their low BMR, remaining small. Mammals are limited by their extensive mastication and their vivipary, while ornithsichian dinosaurs were only limited by their extensive mastication, having greater average body sizes than mammals.     

Necks for sex: sexual selection as an explanation for sauropod dinosaur neck elongation

The immensely long neck of a sauropod is one of the most familiar and striking of anatomical specializations among dinosaurs. Here, I use recently collected neontological and paleontological information to test the predictions of two competing hypotheses proposed to explain the significance of the long neck. According to the traditional hypothesis, neck elongation in sauropods increased feeding height, thereby reducing competition with contemporaries for food. According to the other hypothesis, which is advanced for the first time here, neck elongation in sauropods was driven by sexual selection. Available data match the predictions of the sexual selection hypothesis and contradict the predictions of the feeding competition hypothesis. It is therefore more plausible that increases in sauropod neck lengths were driven by sexual selection than by competition for foliage.     

Flexibility along the neck of the ostrich (Struthio camelus) and consequences for the reconstruction of dinosaurs with extreme neck length

The gross morphology and the flexibility along the neck of the ostrich (Struthio camelus) were examined using fresh tissue as well as neck skeletons. The results of the morphologic studies were compared with results from observations of living ostriches. The investigation was focused on differences in the morphology and the function between different sections of the neck. Additionally, the function of major dorsal neck ligaments was examined, including measurements of force-strain-relations. Comparative studies of giraffes (Giraffa camelopardalis) and camels (Camelus bactrianus) were conducted to find relations between the flexibility along the neck and the general feeding strategy. The examinations revealed that the neck of the ostrich can be divided into four sections with different functions. The first is the atlas-axis-complex which is responsible for torsion. The adjacent cranial section of the neck is flexible in dorsoventral and lateral directions but this part of the neck is usually kept straight at rest and during feeding. Dorsoventral flexibility is highest in the middle section of the neck, whereas the base of the neck is primarily used for lateral excursions of the neck. For giraffes and camels, the posture and utilization of the neck are also reflected in the flexibility of the neck. For all three species, it is possible to reconstruct the pattern of flexibility of the neck by using the neck skeletons alone. Therefore, it appears reasonable to reconstruct the neck utilization and the feeding strategies of dinosaurs with long necks by deriving the flexibility of the neck from preserved vertebrae. For Diplodocus carnegii the neck posture and the feeding strategy were reconstructed. Two neck regions, one around the 9th neck vertebra and the second at the base of the neck, indicate that Diplodocus, like the ostrich, adopted different neck postures. The neck was probably kept very low during feeding. During interruptions of the feeding, e.g., in an alert, the head could have been lifted in an economic way by raising the cranial section of the neck. During standing and locomotion the head was probably located well above the shoulders.     

A new long-necked ‘sauropod-mimic’ stegosaur and the evolution of the plated dinosaurs

Stegosaurian dinosaurs have a quadrupedal stance, short forelimbs, short necks, and are generally considered to be low browsers. A new stegosaur, Miragaia longicollum gen. et sp. nov., from the Late Jurassic of Portugal, has a neck comprising at least 17 cervical vertebrae. This is eight additional cervical vertebrae when compared with the ancestral condition seen in basal ornithischians such as Scutellosaurus. Miragaia has a higher cervical count than most of the iconically long-necked sauropod dinosaurs. Long neck length has been achieved by ‘cervicalization’ of anterior dorsal vertebrae and probable lengthening of centra. All these anatomical features are evolutionarily convergent with those exhibited in the necks of sauropod dinosaurs. Miragaia longicollum is based upon a partial articulated skeleton, and includes the only known cranial remains from any European stegosaur. A well-resolved phylogeny supports a new clade that unites Miragaia and Dacentrurus as the sister group to Stegosaurus; this new topology challenges the common view of Dacentrurus as a basal stegosaur.     

In vivo strains in the femur of the nine‐banded armadillo (Dasypus novemcinctus)

The capacity of limb bones to resist the locomotor loads they encounter depends on both the pattern of those loads and the material properties of the skeletal elements. Among mammals, understanding of the interplay between these two factors has been based primarily on evidence from locomotor behaviors in upright placentals, which show limb bones that are loaded predominantly in anteroposterior bending with minimal amounts of torsion. However, loading patterns from the femora of opossums, marsupials using crouched limb posture, show appreciable torsion while the bone experiences mediolateral (ML) bending. These data indicated greater loading diversity in mammals than was previously recognized, and suggested the possibility that ancestral loading patterns found in sprawling lineages (e.g., reptilian sauropsids) might have been retained among basal mammals. To further test this hypothesis, we recorded in vivo locomotor strains from the femur of the nine‐banded armadillo (Dasypus novemcinctus), a member of the basal xenarthran clade of placental mammals that also uses crouched limb posture. Orientations of principal strains and magnitudes of shear strains indicate that armadillo femora are exposed to only limited torsion; however, bending is essentially ML, placing the medial aspect of the femur in compression and the lateral aspect in tension. This orientation of bending is similar to that found in opossums, but planar strain analyses indicate much more of the armadillo femur experiences tension during bending, potentially due to muscles pulling on the large, laterally positioned third trochanter. Limb bone safety factors were estimated between 3.3 and 4.3 in bending, similar to other placental mammals, but lower than opossums and most sprawling taxa. Thus, femoral loading patterns in armadillos show a mixture of similarities to both opossums (ML bending) and other placentals (limited torsion and low safety factors), along with unique features (high axial tension) that likely relate to their distinctive hindlimb anatomy. J. Morphol. 26:889–899, 2015. © 2015 Wiley Periodicals, Inc.     

Hearts, neck posture and metabolic intensity of sauropod dinosaurs

Hypothesized upright neck postures in sauropod dinosaurs require systemic arterial blood pressures reaching 700 mmHg at the heart. Recent data on ventricular wall stress indicate that their left ventricles would have weighed 15 times those of similarly sized whales. Such dimensionally, energetically and mechanically disadvantageous ventricles were highly unlikely in an endothermic sauropod. Accessory hearts or a siphon mechanism, with sub-atmospheric blood pressures in the head, were also not feasible. If the blood flow requirements of sauropods were typical of ectotherms, the left-ventricular blood volume and mass would have been smaller; nevertheless, the heart would have suffered the serious mechanical disadvantage of thick walls. It is doubtful that any large sauropod could have raised its neck vertically and endured high arterial blood pressure, and it certainly could not if it had high metabolic rates characteristic of endotherms.     

A New Basal Sauropod Dinosaur from the Middle Jurassic of Niger and the Early Evolution of Sauropoda

Background

The early evolution of sauropod dinosaurs is poorly understood because of a highly incomplete fossil record. New discoveries of Early and Middle Jurassic sauropods have a great potential to lead to a better understanding of early sauropod evolution and to reevaluate the patterns of sauropod diversification.

Principal Findings

A new sauropod from the Middle Jurassic of Niger, Spinophorosaurus nigerensis n. gen. et sp., is the most complete basal sauropod currently known. The taxon shares many anatomical characters with Middle Jurassic East Asian sauropods, while it is strongly dissimilar to Lower and Middle Jurassic South American and Indian forms. A possible explanation for this pattern is a separation of Laurasian and South Gondwanan Middle Jurassic sauropod faunas by geographic barriers. Integration of phylogenetic analyses and paleogeographic data reveals congruence between early sauropod evolution and hypotheses about Jurassic paleoclimate and phytogeography.

Conclusions

Spinophorosaurus demonstrates that many putatively derived characters of Middle Jurassic East Asian sauropods are plesiomorphic for eusauropods, while South Gondwanan eusauropods may represent a specialized line. The anatomy of Spinophorosaurus indicates that key innovations in Jurassic sauropod evolution might have taken place in North Africa, an area close to the equator with summer-wet climate at that time. Jurassic climatic zones and phytogeography possibly controlled early sauropod diversification.     

Sauropod Necks: Are They Really for Heat Loss?

Three-dimensional digital models of 16 different sauropods were used to examine the scaling relationship between metabolism and surface areas of the whole body, the neck, and the tail in an attempt to see if the necks could have functioned as radiators for the elimination of excess body heat. The sauropod taxa sample ranged in body mass from a 639 kg juvenile Camarasaurus to a 25 t adult Brachiosaurus. Metabolism was assumed to be directly proportional to body mass raised to the ¾ power, and estimates of body mass accounted for the presence of lungs and systems of air sacs in the trunk and neck. Surface areas were determined by decomposing the model surfaces into triangles and their areas being computed by vector methods. It was found that total body surface area was almost isometric with body mass, and that it showed negative allometry when plotted against metabolic rate. In contrast, neck area showed positive allometry when plotted against metabolic rate. Tail area show negative allometry with respect to metabolic rate. The many uncertainties about the biology of sauropods, and the variety of environmental conditions that different species experienced during the groups 150 million years of existence, make it difficult to be absolutely certain about the function of the neck as a radiator. However, the functional combination of the allometric increase of neck area, the systems of air sacs in the neck and trunk, the active control of blood flow between the core and surface of the body, changing skin color, and strategic orientation of the neck with respect to wind, make it plausible that the neck could have functioned as a radiator to avoid over-heating.     

Biomechanics and functional preconditions for terrestrial lifestyle in basal tetrapods,with special consideration of Tiktaalik roseae

The fossil Tiktaalik roseae from the Late Devonian induces clear definition of the biomechanical and functional preconditions for a terrestrial lifestyle including quadrupedal standing and locomotion on limbs. Therefore, we determined the internal stresses in this model organism under the influence of gravity using the finite element method. Stress patterns during symmetrical two-forelimb support result from bending of trunk and neck. During asymmetrical one-forelimb support, as occurs during terrestrial locomotion, torsional stresses are higher than those caused by bending. The observed patterns of compressive stresses correspond well with the arrangement of compression-resistant materials: vertebral column, shoulder girdle and ribs. The tensile stresses are in accordance with the arrangement of longitudinal and oblique muscles forming the body wall. Torsional stresses concentrate along the periphery of the trunk, leaving its cavity free from mechanical stresses. Theoretical mechanics indicate that the flat skull and the mobility of the neck were advantageous for lateral snapping, similar to crocodiles. The same movement on land requires sprawling and flexed forelimbs. Our results can be interpreted as explanations for the tetrapod bauplan as well as confirmation and refinement of existing hypotheses about the lifestyle at the border between water and land of this early predecessor of terrestrial tetrapods.     

Understanding selection for long necks in different taxa

There has been recent discussion about the evolutionary pressures underlying the long necks of extant giraffes and extinct sauropod dinosaurs. Here we summarise these debates and place them in a wider taxonomic context. We consider the evolution of long necks across a wide range of (both living and extinct) taxa and ask whether there has been a common selective factor or whether each case has a separate explanation. We conclude that in most cases long necks can be explained in terms of foraging requirements, and that alternative explanations in terms of sexual selection, thermoregulation and predation pressure are not as well supported. Specifically, in giraffe, tortoises, and perhaps sauropods there is likely to have been selection for high browsing. It the last case there may also have been selection for reaching otherwise inaccessible aquatic plants or for increasing the energetic efficiency of low browsing. For camels, wading birds and ratites, original selection was likely for increased leg length, with correlated selection for a longer neck to allow feeding and drinking at or near substrate level. For fish‐eating long‐necked birds and plesiosaurs a small head at the end of a long neck allows fast acceleration of the mouth to allow capture of elusive prey. A swan's long neck allows access to benthic vegetation, for vultures the long neck allows reaching deep into a carcass. Geese may be an unusual case where anti‐predator vigilance is important, but so may be energetically efficient low browsing. The one group for which we feel unable to draw firm conclusions are the pterosaurs, this is in keeping with the current uncertainty about the biology of this group. Despite foraging emerging as a dominant theme in selection for long necks, for almost every taxonomic group we have identified useful empirical work that would increase understanding of the selective costs and benefits of a long neck.     

四川自贡蜥脚类一新属

记述了产自四川省自贡市的一具蜥脚类幼年个体材料。根据枢椎极短而高,颈神经棘低、上缘平直、前后延长,背神经棘呈横宽的板状,中部颈肋的前突分叉等特征将它命名为一新属新种——张氏大安龙Daanosaurus zhangi gen.etsp.nov.,并将它归入巧龙亚科Bellusaurinae。     

Raising the sauropod neck: it costs more to get less

The long necks of gigantic sauropod dinosaurs are commonly assumed to have been used for high browsing to obtain enough food. However, this analysis questions whether such a posture was reasonable from the standpoint of energetics. The energy cost of circulating the blood can be estimated accurately from two physiological axioms that relate metabolic rate, blood flow rate and arterial blood pressure: (i) metabolic rate is proportional to blood flow rate and (ii) cardiac work rate is proportional to the product of blood flow rate and blood pressure. The analysis shows that it would have required the animal to expend approximately half of its energy intake just to circulate the blood, primarily because a vertical neck would have required a high systemic arterial blood pressure. It is therefore energetically more feasible to have used a more or less horizontal neck to enable wide browsing while keeping blood pressure low.