Morphology of the axial skeleton of the titanosaurid dinosaurs (Saurischia, Sauropoda) of Minas Gerais state, Brazil

Facultad de Ciencias Naturales

Universidad Nacional de Tucumán

Translated by:

Jeffrey A. Wilson

Department of Organismal Biology & Anatomy

University of Chicago

May 1997

The axial skeleton of titanosaurid dinosaurs (Saurischia-Sauropoda) referred to the Subfamily Titanosaurinae, of the the Baurú Group (Upper Cretaceous) of Peirópolis, Minas Gerais State, Brasil, is described. The preliminar study of this well preserved and partially articulated material, which includes the first complete presacral section known within the titanosaurids, proves that the vertebral column is composed of 13 cervical vertebrae, 10 dorsals, 6 sacrals fused to the ilia by the sacral ribs. Incomplete series of articulated caudals include up to 18 proximal elements. The neural spines of the cervicals and dorsals are undivided and laterally compressed. There is no evidence of hyposphene-hypantrum ariculation on the dorsals. The caudals are procelic except in the one of the preserved caudal series, where the first in biconvex. A sacrum with biconvex articular ends suggests that a taxon has a procoelic condition on the first caudal. Despite the fact that the appendicaular elements associated have not being described and interpreted so far, the morphology of the caudals suggests that they belong to the Titanosaurinae (sensu Powell, 1986) and to Titanosaurus Lydekker, The phylogenetic significance of some morphologycal features is discussed.

The titanosaurid dinosaurs constitute a very conspicuous group among the large reptiles of the South American Upper Cretaceous. The discovery of isolated pieces is frequent in the Senonian continental beds. In South America there are more than 48 known localities in Argentina, Uruguay, Brazil, and Chile (Powell, 1986), of which at least 7 correspond to Brazil.

In spite of the existence of abundant collections, well conserved, partially articulated or associated skeletons pertaining to one individual are scarce. For this reason, many characters of taxonomic importance within sauropods could not be described or validated by the pioneers of the South American titanosaurs: Lydekker (1898) and Huene (1929)

Field work completely recently by L. I. Price starting in 1947 in Brazil and Dr. J. F. Bonaparte from 1965 in Argentina have provided very complete material, partially articulated or associated, which has permitted broader analyses so that aspects of morphology and their taxonomic and phylogenetic implications can be defined with more precision. For a ample bibliography on the Brazilian titanosaurs, I direct the reader to Leonardi and Dusczak (1977).

The present contribution has as an objective to bring to knowledge aspects of the morphology of the axial skeleton of titanosaurids of the subfamily Titanosaurinae (sensu Powell, 1986) of Minas Gerais, Brasil. These were obtained thanks to the work of Dr. LL. I. Price, part of the material being studied by this investigator at the moment of his death. The importance of this collection was emphasized by Price (1951, 1955, 1961).
ACKNOWLEDGMENTS

I would like to express my thanks to Dr. Diógenes de Almeida Campos who placed at my disposal the material in the collection of the Museum of the D. G. M., Río de Janeiro, Brasil and who generously provided me with valuable information about the localities. I thank as well Dr. José Fernando Bonaparte for a critical reading of the

manuscript of my Doctoral Thesis, of which this contribution formed a part. I extend my gratitude to Mr. Simón Castro for the photographic work. This work was made possible thanks to the support provided in various ways by the Consejo Nacional de Investigaciones Científicas y Técnicas, the Facultad de Ciencias Naturales and the Consejo de Invesitigaciones de la Universidad Nacional del Tucumán.
MATERIAL

The material utilized in the descriptions pertain to the collections of the Museum of Divisao de Geologia y Minerologia de la Dirección Nacional of Produçao Minerologia, Río de Janeiro, Brazil, here abbreviated as DGM and accompanied by a field number (Series A, Series B. and Series C).

1. Cervical Vertebrae

a. DGM Series A. Titanosaurinae indet. In addition to the axis, eleven cervical vertebrae are preserved, representing the complete cervical series which was surely found articulated.

The axis has a body relatively large in relation to that of Saltasaurus loricatus (Bonaparte and Powell, 1980; Powell, 1986) and the neural spine is more inclined posteriorly.

The other vertebrae are characterized by being large, slender, and relatively short. In general, the ventral face of the vertebral centrum is concave in the front and somewhat convex in the posterior third. The lateral walls show a wide depression where, in some cases, a small pleurocoel is observed. The parapophyses and laminae are fixed to the anterior part of the centrum following a plane parallel to its long axis, differentiating them from those of Saltasaurus and Neuquensaurus, where they are more extensive (Powell, 1986). The diapophyses of the anterior cervical vertebrae are practically flat distally; they present a ridge to the vertebral axis, becoming more convex in the posterior cervical vertebrae, starting with the eighth. The prezygapophyses and postzygapophyses are relatively short, projecting very little anteriorly and posteriorly beyond the centrum. This differentiates them from Saltasaurus and Neuquensaurus, where the postzygapophyses are situated nearly on the diapophyses. The neural arch is also short and extensive anteroposteriorly. The neural spine is very low and inclined posteriorly after the sixth vertebra. Starting with seventh, they become taller and stouter. All the vertebrae exhibit prespinal and postspinal fossae. The latter are located behind the neural spine and between the arms of the postzygapophyses, and are always deep.

Various vertebrae of the series have been preserved with their corresponding rib articulated. In the eighth cervical vertebra, for example, the rib is completely preserved

(Plate I:3). The ribs are long and narrow, extending more or less parallel to the axis of the vertebral centrum, both forward and backward. The anterior projection is incomplete in the preserved ribs and extends beyond the anterior extreme of the centrum. The posterior projection extends at least 11cm beyond the posterior border of the vertebral centrum.

Starting with the incompletely preserved ninth or tenth cervical vertebrae (Plate I:4, 6) the length of the centrum diminishes appreciably, shortening more abruptly at the transition to the dorsal series.

b. DGM Series B. Titanosaurinae indet. The cervical vertebrae are larger than those of Series A and some of them are shorter and more robust. The last cervical vertebra, which in the Series A was represented by a fragment, is well conserved here. It is a vertebra with a relatively stout body, wider than tall, with a neural arch long and laterally expanded. The diapophyses are strong and have facets directed upwards and backwards. The prezygapophyses and postzygapophyses are short and have large-sized articular facets. The neural spine is short and is reinforced by thickened laminae: a spino-prezygapophyseal, a supra-diapophyseal, and a supra-postzygapophyseal.
2. Dorsal vertebrae

a. DGM Series A. Titanosaurinae indet. Of this series, the three anterior dorsal vertebrae are preserved. They document the cervical-dorsal transition, of which little was known previously in titanosaurids.

The first dorsal vertebra (Plate I:8) is very short relative to the posterior cervical vertebrae, its body being relatively wider. The pleurocoel is reduced and is situated immediately behind the parapophysis. The neural arch is long and wide. The diapophyses are fat, wide, and project laterally and somewhat forward, being supported by infra-diapophyseal laminae which are equally inclined forward. The articular facets of the diapophyses are oriented laterally and upwards. The facets of the prezygapophyses and postzygapophyses are supported by broad columns formed by the thickened

infraprezygapophyseal and suprapostzygapophyseal laminae. The neural spine is relatively low, diminishing notably in thickness from bottom to top. It is reinforced by median prespinal and postspinal laminae, in addition to the longitudinal elevations or columns which form from the spino-prezygapophyseal and supradiapophyseal laminae.

The second dorsal vertebra is short and its body is less voluminous than the first dorsal vertebra. The neural arch is very short and wide. The diapophyses are not as large; they are directed forward, and the infradiapophyseal laminae which support them are inclined 45 degrees anteriorly.

The third dorsal vertebra is very distinct from the anterior ones and more closely resembles the rest of the dorsal vertebrae. The body is broad and short, but has a better developed pleurocoel. The neural arch is short and wide, the parapophysis is located on its lateral face. The diapophysis is situated approximately in the middle of the vertebral body, projecting outwardly and forwards. The infradiapophyseal lamina supports it in an almost vertical plane. The neural spine is inclined somewhat backward and is situated more towards the posterior extreme of the vertebral body. It is reinforced by a prespinal lamina, a postspinal lamina, and a thick supradiapophyseal laminae. There are no spino-prezygapophyseal lamina as were present in the first and second dorsal vertebrae.

b. DGM Series B. Titanosaurinae indet. (Plate 2). The dorsal sequence has been completely preserved in Series B. The first dorsal (Plate 2:1a, b) has a body which is noticeably shorter than that of the last cervical centrum. The pleurocoel is more reduced and defined by sharp borders. The ventral face of the centrum is totally convex due to the ascent of the parapophysis. The neural spine is incomplete, but it can be deduced from preserved portion that the it was short and undivided, tightly united to the postzygapophyses and reinforced anteriorly by laminae as in Series A.

This vertebra is somewhat different from the first dorsal vertebra in Series A by having less prominent neural spine laminae and by having accentuated other characters of typical dorsal vertebrae. The second dorsal vertebra has a pleurocoel more reduced than

the first, with parapophyses situated somewhat higher, but still on the vertebral body. The diapophysis is broad and inclined somewhat forwards, as is the lamina which supports it. The neural spine is inclined somewhat posteriorly and firmly joined to the postzygapophyses. The distance between the prezygapophyses and postzygapophyses is the least of the cervical and dorsal series, and is interpreted as the point of maximum curvature, of the dorsal convexity of the cervical-dorsal of the vertebral column. There are details which differentiate this vertebra from its equivalent in Series A, such as the distance between the prezygapophyses and postzygapophyses and the size of the neural spine.

The third dorsal vertebra (Plate 2:2a, b) has a body which is elongate and short relative to saltasaurines and argyrosaurines (Powell, 1986). The parapophysis is found higher, situated on the lateral face of the neural arch, which has some depressions. The neural spine is long and inclined posteriorly some 45 degrees, clearly differentiating it from the first and second dorsal vertebrae. Various other differences can be observed in this vertebra with respect to those already described. The depression situated between the prezygapophysis and the diapophysis is more developed and more extended anteriorly, the arms of the diapophyses are notably wider in dorsal view.

The fourth dorsal vertebra (Plate 2:3a, b) has a centrum longer than the third and with a elongate pleurocoel. The neural arch is long and relatively low. The parapophysis is large and situated immediately below the prezygapophysis. The neural spine is long and straight. It is inclined at approximately 45 degrees with respect to the edge of the vertebral body. It is laterally compressed and not expanded distally, as it is in Saltasaurus loricatus. The prespinal lamina is particularly well developed.

The fifth dorsal vertebra (Plate 2:3a, b) has a centrum and neural arch very similar to that of the fourth, but differs by the more elevated position of the parapophysis and the increase in distance between the parapophysis and diapophysis, which corresponds to an increase in the size of the anterior infradiapophyseal depression. Another

important difference is observed in the neural spine, which is reinforced anteriorly by the notable development of a prespinal lamina and an accessory spinodiapophyseal lamina which unites the diapophysis with the prespinal lamina.

The sixth, seventh, and eighth dorsal vertebrae (Plate 2: 4a, b) resemble each other substantially. The first two have relatively long and slender centra, while the eighth is somewhat shorter. The pleurocoel is elongate, clearly differing from Saltasaurus loricatus, Neuquensaurus australis (Powell, 1986), and ?Argyrosaurus superbus (Powell, 1986) which have short centra, as is the case in the last species. The neural arches are relatively long and have structures somewhat inclined anteriorly. The parapophysis and the diapophysis approach the same height; the former is found at the level of the prezygapophysis. The diapophyses are broader in dorsal view and have a flattened dorsal surface at their distal extreme. They are reinforced by thick laminae in the manner of columns widening both above and below, where they fuse to the neural arch. The anterior infradiapophyseal fossa is wide and deep. It is located below the horizontal lamina, between the parapophysis and diapophysis. A well developed posterior horizontal lamina, which firmly unites the postzygapophysis and diapophysis in Saltasaurus loricatus, is not observed. Instead, a barely noticeable lamina exists in this position. The spine is laterally compressed and does not have a distal enlargement. It is inclined posteriorly as in the preceding vertebra, but it is much more reinforced. The prespinal lamina is well developed, particularly towards its distal extreme. The accessory supradiapophyseal lamina persists in the case of the sixth and seventh, but not in the eighth. This accessory supradiapophyseal lamina has a novel architecture; near the spine it is divided into two laminae in the form of a “V.” This is not observed in the eighth. The postspinal lamina is equally developed. In the eighth, this structure divides just before reaching the level of the postzygapophyses to unite their medial portion, contributing, along with suprapostzygapophyseal laminae, to the support of the articular facets.

The ninth dorsal vertebra (Plate 2:5a, b) has a body and neural arch very reminiscent of the eighth, differences are observed in the relative positions of the diapophysis and parapophysis. These are found very close to each other, the former found a bit in front and somewhat below the latter.

The tenth dorsal vertebra (Plate 2:5a, b) has a centrum which is appreciably shorter. The neural spine, which until the ninth was compressed and inclined posteriorly, is here oriented vertically and with a distal expansion, as in Saltasaurus loricatus. The diapophyses and the infradiapophyseal laminae which support them are inclined forward. The incipient posterior horizontal lamina, scarcely developed in preceding vertebrae, is here better developed. The anterior infradiapophyseal depression has been notably reduced relative to other vertebrae.

a. DGM Series ?B Titanosaurinae indet. Of the three sacral vertebrae preserved, one seems to correspond to Series B by the size of the sacral vertebrae, as well as the morphological and preservational characteristics. This pelvis is exposed on its dorsal surface and lacks the right ilium and the superior portions of the sacral ribs on the same side.

The sacrum has six vertebrae. The articular surfaces are convex as in Saltasaurus (Bonaparte and Powell, 1980). The first sacral vertebra is a sacralized dorsal. It has a short rib articulated in the manner of dorsal vertebrae, which passes over the superior border of the preacetabular portion of the iliac lamina. All the sacral vertebrae except for the last two have the superior portion of the extreme of the diapophysis, as occurs in the last dorsal vertebrae. The distance from this facet to the axial plane is shortest in the first and last sacral vertebrae, and increases both anteriorly and posteriorly before reaching its maximum at the midlength of the sacrum, at the level of the third or fourth sacral vertebra, where this structure is found on the transverse process. The last sacral vertebrae is a

incorporated caudal vertebra. It has large process which connects to the ilia at their thickened distal ends, resembling in this sense the first caudal vertebra of Saltasaurus loricatus. The neural spines are large and rounded at their extremes; this enlargement is progressively reduced starting with the third sacral vertebra. The neural spines are reinforced by pre- and postspinal laminae, diapophyseal or supradiapophyseal laminae, as well as diapophyseal-prezygapophyseal and diapophyseal-postzygapophyseal laminae in some vertebrae.

In lateral view, the neural spines rise above the superior margin of the ilium.

b. DGM unnumbered. ?Titanosaurinae indet. A sacrum of larger size, with convex articular extremes and articulated to the right ilium and two dorsal vertebrae. It has an ossified ligament connecting the tops of the neural spines of the second, third, fourth, and part of the fifth sacral vertebrae, as documented in Epachthosaurus sciuttoi (Powell, 1986). The dorsal surface of the ligament has longitudinal striations which indicate the fiber orientation. These are distributed almost parallel to the vertebral axis, and diverge somewhat anteriorly. The presence of the ligament indicates that the posterior dorsals and sacrum of titanosaurids had limited mobility.

a. DGM Series C. Titanosaurus sp. (Plate 3). The proximal caudals (1st to 9th; Plate 3:1). The first caudal vertebra is biconvex, its anterior face has a smaller radius of curvature than does the posterior face.

The vertebral centra of the anterior caudal vertebrae of this series are comparatively longer than those of Series B. The inferior edge of the lateral face is appreciably shorter in this series and the concavity on the lateral face is less pronounced. The transverse processes of the first caudals are relatively short and simple, differing in this respect from Saltasaurus loricatus, which has elongate transverse processes on the anterior caudal vertebrae. The neural arch is short and oriented anteriorly. The neural

spine is inclined somewhat posteriorly. Although it is robust, the width does not exceed the length in a cross-section near the apex of the spine, as it does in Saltasaurus loricatus. The spine is reinforced by well developed pre- and postspinal laminae. Its anterior margin forms an obtuse angle with the superior border of the prezygapophysis. These are not as large as in Aeolosaurus (Powell, 1986) and the Series A from Peirópolis. The postzygapophyses are oriented laterally and are situated in the posterior half of the centrum, that is, in a position more posterior than the Series B from Peirópolis, which will be described later, and much posterior than in Aeolosaurus.

The middle caudal vertebrae are characterized by noticeably tall, very narrow centra. The centra have nearly vertical, slightly concave lateral walls which are in the shape of a rectangle. The transverse processes are barely noticeable prominences. The ventral face is narrow, especially in the middle of the centrum where it attains its minimum width. (Plate 3:7). In these vertebrae, the spine is much more laterally compressed.

Caudal vertebrae 12, 13 (Plate 3:5), and 14 (Plate 3:6a, b) resemble those of the type of Titanosaurus indicus Lydekker 1877 in their morphology and proportions. The Indian species differs by having more laterally compressed centra and more prominent chevron facets, which determine the formation of the concavities, front and back, of the ventral face of the centrum.

b. DGM Series B. Titanosaurinae indet.

Pertains to short centra which are especially narrow ventrally. The neural arch is inclined forwards. The prezygapophyses are strongly inclined; their facets form an acute angle with respect to the sagittal plane. The prezygapophyses are extended anteriorly, although not as much is in Aeolosaurus rionegrinus. Consequently, in comparison with this species, the postzygapophyes are situated more posteriorly, approximately at midlength along the centrum.

The neural spine has a well developed prespinal lamina distally, and two spinoprezygapophyseal laminae at its base. Posteriorly, it has a medial postspinal lamina and supraprezygapophyseal laminae.
DISCUSSION

Unfortunately, it has not been possible, for the moment, to adequately study the appendicular bones or their possible association with the vertebral series in the collections of the DGM in Río de Janeiro. This information can likely be found in the field notes of L. I. Price, which were not available at the time of this study. It is planned in the near future to analyze this information in conjunction with Dr. Diógenes Almeida Campos of the DGM of the DNPM of Río de Janeiro, Brazil. This study could possibly adequately evaluate and classify the specimens to a specific level, allowing more precise knowledge and definition of the subfamily Titanosaurinae.

We analyze the aspects which arise from this evidence: 1) the vertebral formula in titanosaurids, 2) significance of some peculiar structures in the titanosaurids, and 3) chronological aspects of the titanosaurids from Peirópolis.
1. The vertebral formula in titanosaurids

One of the problems stated by Heune (1929) was the impossibility of establishing the presacral formula of the axial skeleton because of the lack of articulated material. Nevertheless, he suggested on the basis of a series of observations that the titanosaurids may have had 14 cervical and 10 dorsal vertebrae. The evidence analyzed in this work coincide almost perfectly with his inference, only that in the articulated portions the count is 13 cervicals and 10 dorsal vertebrae. The number of sacrals coincides with what Heune (1929) observed. For the number of caudal elements, no concrete evidence exists. Among the Peirópolis material exist proximal caudal segments of up to 18 articulated vertebrae, but articulated material is not known for the distal extreme of the tail. Gilmore

(1946) has described an example assigned to the North American species Alamosaurus sanjuanensis which included a articulated caudal series containing 30 pieces. Heune estimated that around 48 caudal elements existed.
2. Significance of some peculiar structures in the titanosaurids

The excellent preservation of these series permits corroboration of important morphological characteristics in the context of sauropods: a) the titanosaurids did not have divided neural spines, and b) they lack the hyposphene-hypantrum.

a. Undivided neural spines. In the majority of sauropods there exist neural spines divided in the form of a hairpin in the posterior cervical and anterior dorsal vertebrae. This fork has the form of a “U” in Camarasaurus or a “V” (Diplodocus, Apatosaurus, Dicraeosaurus) and may or may not have a tubercle at the point of division of the two rami. This peculiar type of neural spine may constitute an adaptation tied to particular behavioral and functional significance, like the possibility of lowering the head, as suggested by Borsuk-Bialynicka (1977), without its presence representing a phylogenetic relation (synapomorphy).

The undivided neural spine is, without a doubt, a primitive character, and the sauropods which possessed them are derived from similar forms. With this we can exclude the camarasaurids, diplodocids and euhelopodids as ancestors of the titanosaurids.

b. Absence of accessory articulations (hyposphene-hypantrum). The hyposphene-hypantrum is an accessory articulation present in the posterior dorsal vertebrae of many sauropods, and contributes to give better support to the vertebral column. Within sauropods, we find them in camarasaurids, diplodocids, brachiosaurids and cetiosaurids. In accordance with the observations of Bonaparte and Powell (1980) and Powell (1986), and contrary to Gauthier (1986) this structure is not present in titanosaurids (=titanosaurs sensu Gauthier, 1986).

It follows to analyze if this condition is primitive or derived within titanosaurs. Charig (1982) has interpreted the presence of this structure as a “synapomorphy of the sauropods.” Nevertheless, it is probable that the absence of this structure constitutes, on the other hand, an apomorphic character, taking into account its presence within the rest of sauropods, and also prosauropods, (among others, Riojasaurus Bonaparte 1971) and theropods (Deinonychus Ostrom 1969; Allosaurus Madsen 1976).

Nevertheless, the possibility that this structure arose more than one time, within sauropodomorphs and also within other thecodonts of large size as is known in rauisuchids like Fasolasuchus (Bonaparte, 1981), should not be discarded.

Considering the lack of hyposphene-hypantrum as a primitive character, the titanosaurids are separated early from the trunk of sauropod evolution, starting from insufficiently documented lineages. If they are interpreted, as is more probable, as derived characters, we find a synapomorphy of titanosaurids, which along with other traits such as procoely of caudal vertebrae (except, occasionally, the first and some distal caudal vertebrae) and the lightening developed in the presacral vertebrae (Powell, 1986) which define them as a monophyletic group.

In accordance with the evidence obtained in Argentine titanosaur localities we find saltasaurines in sedimentary units corresponding to ?Campanian-Maastrichtian (Powell, 1986). This subfamily is limited to this stretch of time. The titanosaurines, on the other hand, seem to have a broader biochron, such that they are documented in association with sauropods with amphiplatyan vertebrae which are not known in upper Senonian levels in South America (Powell, 1986). The absence of saltasaurines may indicate a Senonian age (?preCampanian-Maastrichtian) for the levels of the Baurú Group, which have provided the materials here analyzed.

1. The titanosaurid dinosaurs of Peiropólis, Minas Gerais State correspond to the subfamily Titanosaurinae (Powell, 1986).

2. The presacral vertebral formula of the titanosaurines, and of the titanosaurids is the following: 13 cervical and 10 dorsal vertebrae.

3. The levels of the Baurú Group, which have provided these fossils in Peirópolis (Minas Gerais State) are probably of Senonian age (?precampanian-maastrichtian) on the basis of the absence of saltasaurine titanosaurs.

(scale = 5cm)

(1) 7th cervical vertebra and articulated rib fragment in lateral view

(2)10th cervical vertebra with complete rib in lateral view

(3) 8th cervical vertebra in lateral view

(4) 9th cervical vertebra in lateral view
Plate 2. Titanosauridae indet., Series B:

(1) Last cervical and first dorsal vertebrae in (a) lateral and (b) dorsal views

(2) 2nd and 3rd dorsal vertebrae in (a) lateral and (b) dorsal views

(3) 4th and 5th dorsal vertebrae in (a) lateral and (b) dorsal views

(4) 6th, 7th, and 8th dorsal vertebrae in (a) lateral and (b) dorsal views

(5) 9th and 10th dorsal vertebrae in (a) lateral and (b) dorsal views

(1) Last sacral, 1st, and 2nd caudal vertebrae in lateral view

(2) 3rd, 4th, and 5th caudal vertebrae in lateral view

(3) 6th, 7th, and 8th caudal vertebrae in lateral view

(4) 9th, 10th, and 11th caudal vertebrae in lateral view

(5) 12th and 13th caudal vertebrae in lateral view, the first are a stereoscopic pair

(6) 14th caudal vertebra in (a) lateral, and (b) posterior stereoscopes

(7) 12th caudal vertebra in (a) ventral, and (b) anterior stereoscopes