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.     

Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration

The well-preserved histology of the geologically oldest sauropod dinosaur from the Late Triassic allows new insights into the timing and mechanism of the evolution of the gigantic body size of the sauropod dinosaurs. The oldest sauropods were already very large and show the same long-bone histology, laminar fibro-lamellar bone lacking growth marks, as the well-known Jurassic sauropods. This bone histology is unequivocal evidence for very fast growth. Our histologic study of growth series of the Norian Plateosaurus indicates that the sauropod sistergroup, the Late Triassic and early Jurassic Prosauropoda, reached a much more modest body size in a not much shorter ontogeny. Increase in growth rate compared to the ancestor (acceleration) is thus the underlying process in the phylogenetic size increase of sauropods. Compared to all other dinosaur lineages, sauropods were not only much larger but evolved very large body size much faster. The prerequisite for this increase in growth rate must have been a considerable increase in metabolic rate, and we speculate that a bird-like lung was important in this regard.     

An alternative sauropod physiology and cardiovascular system that eliminates high blood pressures

Siegwarth, J.D., Smith, C.N. & Redman, P.D. 2010: An alternative sauropod physiology and cardiovascular system that eliminates high blood pressures. Lethaia, Vol. 44, pp. 46–57. The long neck of an adult sauropod has been found structurally unsuitable for high browsing while standing on all four feet. Some juveniles might have used a tripodal stance, but an analysis of the motion of the centre of mass shows a large adult sauropod could not. We propose here that sauropods could have browsed high by sitting, squatting or even kneeling on their hind legs to elevate their heads without a sharp bend at the base of the neck. A large sauropod needs a way to deal with very high blood pressure when high browsing. Arterial pumping is suggested here as a means of avoiding the need for high blood pressure. □Blood pressure, browsing posture, cardiovascular system, form vis‐à‐vis function, neck length, physiology, sauropods, tripodal stance.     

Steneosaurus edwardsi (Thalattosuchia: Teleosauridae), the largest known crocodylomorph of the Middle Jurassic

Teleosaurids were a clade of marine crocodylomorphs that were globally distributed during the Jurassic Period. They evolved a wide range of body sizes, from small (～2–3 m) to very large (> 9 m). Until now, the largest known Middle Jurassic teleosaurid was ‘Steneosaurus’ obtusidens, from the Oxford Clay Formation of the UK. Here, we re‐examine a very large Oxford Clay specimen (ilium, ischium, and femur) that had been tentatively attributed to ‘S.’ obtusidens. Based on comparative anatomical study with the ‘S.’ obtusidens holotype and referred specimens of Steneosaurus edwardsi and Steneosaurus leedsi, we conclude that this very large individual actually pertains to S. edwardsi. Based on comparisons with the Machimosaurus mosae neotype (which has a complete femur and skeleton), we estimate a total length in excess of 7 m for this large S. edwardsi individual, making it the largest known Middle Jurassic teleosaurid. Therefore, along with the closely related genus Machimosaurus, this clade of large‐bodied Middle–Late Jurassic teleosaurids were the largest species during the first 100 million years of crocodylomorph evolution. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●● , ●●–●●.     

Assessing metabolic constraints on the maximum body size of actinopterygians: locomotion energetics of Leedsichthys problematicus (Actinopterygii,Pachycormiformes)

Maximum sizes attained by living actinopterygians are much smaller than those reached by chondrichthyans. Several factors, including the high metabolic requirements of bony fishes, have been proposed as possible body‐size constraints but no empirical approaches exist. Remarkably, fossil evidence has rarely been considered despite some extinct actinopterygians reaching sizes comparable to those of the largest living sharks. Here, we have assessed the locomotion energetics of Leedsichthys problematicus, an extinct gigantic suspension‐feeder and the largest actinopterygian ever known, shedding light on the metabolic limits of body size in actinopterygians and the possible underlying factors that drove the gigantism in pachycormiforms. Phylogenetic generalized least squares analyses and power performance curves established in living fishes were used to infer the metabolic budget and locomotion cost of L. problematicus in a wide range of scenarios. Our approach predicts that specimens weighing up to 44.9 tonnes would have been energetically viable and suggests that similar body sizes could also be possible among living taxa, discarding metabolic factors as likely body size constraints in actinopterygians. Other aspects, such as the high degree of endoskeletal ossification, oviparity, indirect development or the establishment of other large suspension‐feeders, could have hindered the evolution of gigantism among post‐Mesozoic ray‐finned fish groups. From this perspective, the evolution of anatomical innovations that allowed the transition towards a suspension‐feeding lifestyle in medium‐sized pachycormiforms and the emergence of ecological opportunity during the Mesozoic are proposed as the most likely factors for promoting the acquisition of gigantism in this successful lineage of actinopterygians.     

Prozostrodon brasiliensis,a probainognathian cynodont from the Late Triassic of Brazil: second record and improvements on its dental anatomy

Probainognathian cynodonts are conspicuous elements of the Assemblage Zones of the Triassic Santa Maria Supersequence in southern Brazil. Within this group, the derived clade Prozostrodontia, in which the crown group Mammalia is included, is taxonomic diverse in the Hyperodapedon and Riograndia AZs. We describe here the second known specimen (CAPPA/UFSM 0123) of Prozostrodon brasiliensis, until now only represented by its holotype. CAPPA/UFSM 0123 includes a right dentary with dentition. As in the holotype of P. brasiliensis, it has four lower incisors, pc4 with conspicuous cusp a, and small cusps b, c, and d, pc5-pc6 of ‘triconodont’ type with cusps a > c > b > d, with continuous lingual cingulum bearing up to six small discrete cusps, length of the lower tooth row more than half the length of the dentary, and relatively deep horizontal ramus of the dentary. The new specimen is about 25% smaller than the holotype and there is not a diastema between the canine and postcanine teeth, indicating its juvenile condition. Based on both known specimens of P. brasiliensis, a discussion on tooth replacement is presented, showing that the adult individual has more postcanine tooth morphotypes than the juvenile one.     

A sauropod rib with an embedded theropod tooth: direct evidence for feeding behaviour in the Jehol group,China

Xing, L, Bell, P.R., Currie, P.J., Shibata, M., Tseng, K. & Dong, Z. 2012: A sauropod rib with an embedded theropod tooth: direct evidence for feeding behaviour in the Jehol group, China. Lethaia, Vol. 45, pp. 500–506. A fragmentary rib from the Lower Cretaceous (Barremian) Yixian Formation in northeastern China preserves rare, direct evidence of feeding behaviour by an unidentified theropod. The rib, which comes from the holotype of Dongbetitan, preserves an embedded, broken theropod tooth. Comparison of the tooth with all known theropods from the Yixian Formation suggests that it belongs to a new taxon of medium‐sized theropod. Given the large size difference between the sauropod and the theropod and the absence of reactive bone growth around the tooth, the bite likely occurred post‐mortem during scavenging. Recognition of a new, medium‐sized theropod increases the known diversity of taxa from the Yixian Formation and helps fill a gap in the theropod palaeoecology of that formation, which previously consisted of only small (<2 m) forms. □China, Cretaceous, feeding behaviour, theropod, titanosauriformes, sauropod.     

A Three-Dimensional Skeletal Reconstruction of the Stem Amniote Orobates pabsti (Diadectidae): Analyses of Body Mass,Centre of Mass Position,and Joint Mobility

Orobates pabsti, a basal diadectid from the lower Permian, is a key fossil for the understanding of early amniote evolution. Quantitative analysis of anatomical information suffers from fragmentation of fossil bones, plastic deformation due to diagenetic processes and fragile preservation within surrounding rock matrix, preventing further biomechanical investigation. Here we describe the steps taken to digitally reconstruct MNG 10181, the holotype specimen of Orobates pabsti, and subsequently use the digital reconstruction to assess body mass, position of the centre of mass in individual segments as well as the whole animal, and study joint mobility in the shoulder and hip joints. The shape of most fossil bone fragments could be recovered from micro-focus computed tomography scans. This also revealed structures that were hitherto hidden within the rock matrix. However, parts of the axial skeleton had to be modelled using relevant isolated bones from the same locality as templates. Based on the digital fossil, mass of MNG 10181 was estimated using a model of body shape that was varied within a plausible range to account for uncertainties of the dimension. In the mean estimate model the specimen had an estimated mass of circa 4 kg. Varying of the mass distribution amongst body segments further revealed that Orobates carried most of its weight on the hind limbs. Mostly unrestricted joint morphology further suggested that MNG 10181 was able to effectively generate propulsion with the pelvic limbs. The digital reconstruction is made available for future biomechanical studies.     

A Voucher Specimen for <Emphasis Type="Italic">Macaca munzala</Emphasis>: Interspecific Affinities,Evolution, and Conservation of a Newly Discovered Primate

Sinha, A., Datta, A., Madhusudan, M. D., & Mishra, C. (2005. Macaca munzala: A new species from western Arunachal Pradesh, northeastern India. International Journal of Primatology, 26, 977–989) discovered Arunachal macaques (Macaca munzala), a species new to science, in the eastern Himalaya of Arunachal Pradesh in northeastern India. They depicted the holotype and paratypes of the species in photographs, and a specimen of the species had been unavailable for preservation and examination. In March 2005, we obtained an entire specimen of an adult male Macaca munzala, which we propose as a voucher specimen for the species. We provide detailed morphological and anatomical measurements of the specimen and examine its affinities with other macaques. Macaca munzala appears to be unique among macaques in craniodental size and structure, baculum, and aspects of caudal structure, while exhibiting affinities with the other members of the sinica-group to which it belongs. We summarize our insights on the origins and phylogeny of Macaca munzala. Finally, we review the current conservation status of the macaques, which are threatened by extensive hunting in the only 2 districts of Arunachal Pradesh where they are documented to occur.     

A nearly complete skeleton of an early juvenile diplodocid (Dinosauria: Sauropoda) from the Lower Morrison Formation (Late Jurassic) of north central Wyoming and its implications for early ontogeny and pneumaticity in sauropods

A nearly complete skeleton of a juvenile sauropod from the Lower Morrison Formation (Late Jurassic, Kimmeridgian) of the Howe Ranch in Bighorn County, Wyoming is described. The specimen consists of articulated mid-cervical to mid-caudal vertebrae and most appendicular bones, but cranial and mandibular elements are missing. The shoulder height is approximately 67 cm, and the total body length is estimated to be less than 200 cm. Besides the body size, the following morphological features indicate that this specimen is an early juvenile; (1) unfused centra and neural arches in presacral, sacral and first to ninth caudal vertebrae, (2) unfused coracoid and scapula, (3) open coracoid foramen, and (4) relatively smooth articular surfaces on the limb, wrist, and ankle bones. A large scapula, short neck and tail and elongate forelimb bones relative to overall body size demonstrate relative growth. A thin-section of the mid-shaft of a femur shows a lack of annual growth lines, indicating an early juvenile individual possibly younger than a few years old. Pneumatic structures in the vertebral column of the specimen SMA 0009 show that pneumatisation of the postcranial skeleton had already started in this individual, giving new insights in the early ontogenetic development of vertebral pneumaticity in sauropods.

The specimen exhibits a number of diplodocid features (e.g., very elongate slender scapular blade with a gradually dorsoventrally expanded distal end, a total of nine dorsal vertebrae, presence of the posterior centroparapophyseal lamina in the posterior dorsal vertebrae). Although a few diplodocid taxa, Diplodocus, cf. Apatosaurus, and cf. Barosaurus, are known from several fossil sites near the Howe Ranch, identification of this specimen, even at a generic level, is difficult due to a large degree of ontogenetic variation.     

Body Mass Estimates for Eocene Eosimiid and Amphipithecid Primates Using Prosimian and Anthropoid Scaling Models

We estimated body masses for middle to late Eocene East Asian eosimiids and amphipithecids from the crown areas of cheek teeth. First, we calculated body mass estimate equations via an extant primate sample of 11 prosimian and 30 anthropoid species, and compared the reliability of the resulting body mass estimate regressions. M ^1–2 and M _1–2 are better body mass estimators, especially for fossils with few samples, because of their low intraspecific variations in dimensions. Moreover, body masses derived from M _1–2 tend to indicate lower estimate error than those from other cheek teeth. The relationships between tooth crown areas and body mass differ between prosimians and anthropoids; the estimated body mass from crown area of P ⁴ or any molar will be larger if anthropoids, instead of prosimians, are used as a reference taxon. Second, We applied the regressions to the fossil primates. The estimated body masses in kg are as follows: Eosimias centennicus, 0.16; E. sinensis, 0.14; Eosimiidae indet. from the Pondaung Formation, 0.41; Bahinia pondaungensis, 0.57; Myanmarpithecus yarshensis, 1.8; Amphipithecus mogaungensis, 6.8; Pondaungia cotteri, 5.9; Pondaungia savagei, 8.8; Siamopithecus eocaenus, 5.9. Eosimiids fit the prosimian model better than the anthropoid model. Amphipithecids do not fit one model particularly better than the other, as the estimates vary considerably according to the tooth used and the reference taxon. The anthropoid model gives smaller differences between upper- and lower-molar-based body mass estimates, but premolars are relatively much smaller in amphipithecids than in extant prosimians and anthropoids.     

The cranial anatomy,ontogeny, and relationships of Karpinskiosaurus secundus (Amalitzky) (Seymouriamorpha,Karpinskiosauridae) from the Upper Permian of European Russia

The Upper Permian seymouriamorph tetrapod Karpinskiosaurus from European Russia includes two species: Karpinskiosaurus secundus and Karpinskiosaurus ultimus. Karpinskiosaurus secundus is represented by two specimens with skull lengths of about 75 mm. All specimens of K. ultimus are smaller than those of K. secundus. Revision of the cranial anatomy of all previously known and several new specimens of Karpinskiosaurus shows that the specimens of K. secundus and most of the specimens of K. ultimus represent the ontogenetic series of one species: K. secundus. The holotype specimen of K. ultimus requires revision, with the aim to find out whether it represents a second species of Karpinskiosaurus or not. The available material permits new reconstructions of the largest, holotype skull, and one smaller skull with a length of about 36 mm. Karpinskiosaurus secundus is included in a cladistic analysis for the first time here. The analysis shows it to form a sister taxon to Discosauriscidae. The clade comprising Karpinskiosaurus secundus plus Discosauriscidae forms a sister group to Seymouriidae. Karpinskiosaurus secundus has a large postorbital and a short preorbital region, and the orbits are placed in the posterior portion of the anterior half of the skull length. Among all seymouriamorphs, such cranial proportions are exhibited only by the largest known specimens of Discosauriscus austriacus. None of the specimens of K. secundus described here exhibits the presence of sensory grooves; thus, all specimens composing the ontogenetic sequence of K. secundus are considered to be terrestrial. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010.     

Nonconformance of standard metabolic rate with body mass in Hawaiian Honeycreepers

Summary Among four species of Hawaiian Honeycreepers, three from Hawaii (Vestiaria coccinea, 15.0 g; Himatione sanguinea, 12.9 g; Loxops virens, 10.7 g) and one from Kauai (Loxops parva, 7.9 g), standard metabolic rate (in ml O₂/g·h) was positively related to body mass, the opposite of that predicted by conventional endothermic allometry. SMR of V. coccinea conformed to the predicted value, but in the remaining species was progressively reduced below expected levels as body mass decreased. All four species occur predominantly in Metrosideros collina forests, where their preferred food is the nectar of its blooms. At least on Hawaii and during periods of moderate bloom the species are aligned along a dominance hierarchy, with the largest species most dominant and most successful at nectar exploitation. I believe that nonconformancy of SMR with body mass in the smaller species reflects an energy-conserving measure, the degree of which is dictated by social position and relative success in nectar exploitation.     

AN UNUSUAL NEW NEOSAUROPOD DINOSAUR FROM THE LOWER CRETACEOUS HASTINGS BEDS GROUP OF EAST SUSSEX, ENGLAND

Abstract:  Xenoposeidon proneneukos gen. et sp. nov. is a neosauropod represented by BMNH R2095, a well-preserved partial mid-to-posterior dorsal vertebra from the Berriasian–Valanginian Hastings Beds Group of Ecclesbourne Glen, East Sussex, England. It was briefly described by Lydekker in 1893, but it has subsequently been overlooked. This specimen's concave cotyle, large lateral pneumatic fossae, complex system of bony laminae and camerate internal structure show that it represents a neosauropod dinosaur. However, it differs from all other sauropods in the form of its neural arch, which is taller than the centrum, covers the entire dorsal surface of the centrum, has its posterior margin continuous with that of the cotyle, and slopes forward at 35 degrees relative to the vertical. Also unique is a broad, flat area of featureless bone on the lateral face of the arch; the accessory infraparapophyseal and postzygapophyseal laminae which meet in a V; and the asymmetric neural canal, small and round posteriorly but large and teardrop-shaped anteriorly, bounded by arched supporting laminae. The specimen cannot be referred to any known sauropod genus, and clearly represents a new genus and possibly a new 'family'. Other sauropod remains from the Hastings Beds Group represent basal Titanosauriformes, Titanosauria and Diplodocidae; X. proneneukos may bring to four the number of sauropod 'families' represented in this unit. Sauropods may in general have been much less morphologically conservative than is usually assumed. Since neurocentral fusion is complete in R2095, it is probably from a mature or nearly mature animal. Nevertheless, size comparisons of R2095 with corresponding vertebrae in the Brachiosaurus brancai holotype HMN SII and Diplodocus carnegii holotype CM 84 suggest a rather small sauropod: perhaps 15 m long and 7600 kg in mass if built like a brachiosaurid, or 20 m and 2800 kg if built like a diplodocid.     

Body mass and locomotor habits of the smallest darter,Anhinga minuta (Aves,Anhingidae)

During the Neogene of South America, Anhingidae was represented by several species, mainly with greater sizes than the extant members. In the present contribution, body mass and locomotor habits of Anhinga minuta, the smallest known darter, were inferred. Body mass was estimated using two methods, one with measures of a tibiotarsus (the holotype) and the other, with measurements of a humerus; locomotor habits were inferred through muscular reconstructions and wing parameters (wing span, wing area and wing loading). Estimates of wing span and wing area were based on the length of humerus, assuming a condition of isometry with respect to Anhinga anhinga; wing loading was obtained through a relation formula between wing area and body mass. The results obtained indicate a body mass of about 729 g, a wing span of 0.958 m, a wing area of 0.117 m² and a corresponding wing loading of 61 N/m². These values and also the proximal insertion of the musculus pectoralis are consistent with those of a soaring bird but with more frequent flapping than extant anhingids. Furthermore, the inferred musculature for tibiotarsus indicates abilities for swimming, climbing and moving through the vegetation as in extant representatives.     

Body size evolution in Titanosauriformes (Sauropoda,Macronaria)

Titanosauriformes is a conspicuous and diverse group of sauropod dinosaurs that inhabited almost all land masses during Cretaceous times. Besides the diversity of forms, the clade comprises one of the largest land animals found so far, Argentinosaurus, as well as some of the smallest sauropods known to date, Europasaurus and Magyarosaurus. They are therefore good candidates for studies on body size trends such as the Cope's rule, the tendency towards an increase in body size in an evolutionary lineage. We used statistical methods to assess body size changes under both phylogenetic and nonphylogenetic approaches to identify body size trends in Titanosauriformes. Femoral lengths were collected (or estimated from humeral length) from 46 titanosauriform species and used as a proxy for body size. Our findings show that there is no increase or decrease in titanosauriform body size with age along the Cretaceous and that negative changes in body size are more common than positive ones (although not statistically significant) for most of the titanosauriform subclades (e.g. Saltasaridae, Lithostrotia, Titanosauria and Somphospondyli). Therefore, Cope's rule is not supported in titanosauriform evolution. Finally, we also found a trend towards a decrease of titanosauriform mean body size coupled with an increase in body size standard deviation, both supporting an increase in body size variation towards the end of Cretaceous.     

Genetic analysis of the Linnaean Ulva lactuca (Ulvales,Chlorophyta) holotype and related type specimens reveals name misapplications,unexpected origins,and new synonymies

Current usage of the name Ulva lactuca, the generitype of Ulva, remains uncertain. Genetic analyses were performed on the U. lactuca Linnaean holotype, the U. fasciata epitype, the U. fenestrata holotype, the U. lobata lectotype, and the U. stipitata lectotype. The U. lactuca holotype is nearly identical in rbcL sequence to the epitype of U. fasciata, a warm temperate to tropical species, rather than the cold temperate species to which the name U. lactuca has generally been applied. We hypothesize that the holotype specimen of U. lactuca came from the Indo‐Pacific rather than northern Europe. Our analyses indicate that U. fasciata and U. lobata are heterotypic synonyms of U. lactuca. Ulva fenestrata is the earliest name for northern hemisphere, cold temperate Atlantic and Pacific species, with U. stipitata a junior synonym. DNA sequencing of type specimens provides an unequivocal method for applying names to Ulva species.