High browsing skeletal adaptations in Spinophorosaurus reveal an evolutionary innovation in sauropod dinosaurs

Abstract

Sauropods were among the most diverse lineages of dinosaurs, with an ample geographic distribution throughout the Mesozoic. This evolutionary success is largely attributed to neck elongation and its impact on feeding efficiency. However, how neck elongation influenced exactly on feeding strategies is subject of debate. The process of mounting a nearly complete virtual skeleton of Spinophorosaurus nigerensis, from the Middle (?) Jurassic of Niger, has revealed several previously unknown osteological adaptations in this taxon. Wedged sacral and posterior dorsal vertebrae cause the presacral column to deflect antero-dorsally. This, together with elongated scapulae and humeri make the anterior region of the skeleton vertically lengthened. Also, elongated prezygapophyseal facets on the cervical vertebrae and a specialized first dorsal vertebra greatly increase the vertical range of motion of the neck. These characters support this early eusauropod as a more capable high browser than more basally branching sauropods. While limb proportions and zygapophyseal facets vary among Eusauropoda, the sacrum retained more than 10° of wedging in all Eusauropoda. This implied a functional constraint for sauropod species which evolved lower browsing feeding strategies: the antero-dorsal sloping caused by the sacrum had to be counteracted with further skeletal modifications, e.g. a ventrally curved mid to anterior presacral spine to hinder the dorsal slope of the whole presacral series caused by the wedged sacrum. This suggests that at least the last common ancestor of Eusauropoda developed high browsing capabilities, partially due to the modified wedged sacrum, likely a potential synapomorphy of the clade and key in the evolutionary history of the group.

Figure 1

High browsing adaptations in Spinophorosaurus nigerensis. Skeletal reconstruction in osteologically neural pose with bones color-coded according to their provenance, with the holotype in red, paratype in yellow, and bones inferred from close relatives in green. White indicates reconstructed bone. (A) Sacrum, showing the 20° angle wedging. (B) 12^th and 13^th dorsal vertebrae, showing a slight acute wedging. (C) Partially cervicalized 1^st dorsal vertebra. (D) 12^th Cervical Vertebra. (E) First dorsal rib and last cervical rib. (F) Humerus and femur, to scale. Scales A-F = 500 mm.

Figure 2

The verticalization of sauropod feeding envelopes. (A) Increased neck range of motion in Spinophorosaurus in the dorso-ventral plane, with the first dorsal vertebra as the vertex and 0° marking the ground. Poses shown: (1) maximum dorsiflexion; (2) highest vertical reach of the head (7.16 m from the ground), with the neck 90° deflected; (3) alert pose sensu Taylor Wedel and Naish; (4) osteological neutral pose sensu Stevens; (5) lowest vertical reach of the head (0.72 m from the ground at 0°), with the head as close to the ground without flexing the appendicular elements; (6) maximum ventriflexion. Blue indicates the arc described between maximum and minimum head heights. Grey indicates the arc described between maximum dorsiflexion and ventriflexion. (B) Bivariant plot comparing femur/humerus proportion with sacrum angle. The proportion of humerus and femur are compared as a ratio of femur maximum length/humerus maximum length. Sacrum angle measures the angle the presacral vertebral series are deflected from the caudal series by sacrum geometry in osteologically neutral pose. Measurements and taxa on Table 1. Scale = 1000 mm.

Figure 3

Time calibrated sauropodomorph phylogenetic relationships with emphasis on different body proportioned taxa. Different body proportions for sauropodomorph dinosaurs include (1) facultative quadrupedalism and medium height browsing in non-sauropod sauropodomorphs (e.g. Melanorosaurus) with non-wedged sacrum; (2) obligatory quadrupedalism and medium height browsing in basally branching sauropods with longer forelimbs but no wedged sacrum (e.g. Kotasaurus); (3) medium-high browsing in non-neosauropod eusauropods, with longer necks and forelimbs and an acute wedged sacrum (e.g. Spinophorosaurus); (4) medium-ground level browsing in dicraeosaurid and rebbachisaurid diplodocoid sauropods, with short necks, shorter forelimbs than non-neosauropod sauropodomorphs but with acute wedged sacrum and obtuse wedged dorsal vertebrae (e.g. Dicraeosaurus); (5) medium-height browsing in basally branching macronarian sauropods, with a wedge shaped sacrum and retroverted pelvis (e.g. Camarasaurus); (6) extreme high browsing in brachiosaurid sauropods, with extremely elongated necks, humeri longer than femora and extremely wedged sacra (e.g. Brachiosaurus); (7) extreme high browsing in euhelopodid titanosauriforms, with extremely long necks and extremely wedged sacra (e.g. Euhelopus); and (8) medium-low browsing in some lithostrotian titanosaurs, with shorter forelimbs than other titanosaurs and titanosauriforms but still retaining a wedged sacrum and with obtuse wedged dorsal vertebrae (e.g. Saltasaurini). A wedged sacrum is only found in Eusauropoda, and albeit the degree of wedging varies among sauropods, it never returns to the basal condition. Schematic bones obtained directly from digitized 3D models, except in Melanorosaurus, Kotasaurus, Dicraeosaurus^, and Euhelopus, where photographs were used as reference. Femora and humeri are proportioned to each other following Table 1. Schematic bone color coding: rectangular sacra (blue); acute wedged sacra (red); obtuse wedged mid-dorsal vertebrae (yellow and green). Time callibration of nodes after Xu et al..

Figure 4

Skeletal reconstructions of Spinophorosaurus nigerensis. (A) Original skeletal reconstruction of Spinophorosaurus first published in 2009, modified from the original publication. (B) Virtual skeletal reconstruction of Spinophorosaurus. All the skeletal reconstructions have been scaled to the same dorso-sacral sector length (between the last sacral vertebra and the first dorsal vertebra). Previous reconstruction lacked information on precise sacrum morphology, hence the radically different osteologically induced curvatures of the presacral vertebrae. Other bones which differ between the 2009 reconstruction and actual fossils (as further preparation has been carried out) are the ilium, the first three dorsal ribs, the cervicodorsal transition and the anterior caudal vertebrae.