BOX 2.4 Evolutionary Relationships in Ornithopoda
A little more than 160 million years ago, the Middle Jurassic saw the emergence of relatively small (2 m long), bipedal, herbivorous dinosaurs called ornithopods. From the Late Jurassic, and especially through the Cretaceous, these ornithopods were among the dominant terrestrial forms around the world. Some ornithopods, such as Hypsilophodon and Orodromeus, were small (approximately 2 m long) and fast running, while others, like the larger iguanodontians, are probably the most familiar of all ornithopods. Their namesake, Iguanodon, was one of the first-discovered dinosaurs and is a charter member of Owen’s Dinosauria. This 10 m long ornithopod from the Early Cretaceous of Europe had a long, straight tail, a stocky body, and large spikes serving as thumbs. Hadrosaurids, often called duck-billed dinosaurs, are among the remaining iguanodontoideans; they look like an unlikely evolutionary cross between a duck and a horse. They, too, probably had muscular cheeks, but with strong and closely packed upper and lower teeth that formed roughened grinding surfaces.
Note: See Horner et al. 2004; Norman 2004; Norman et al. 2004; Weishampel et al. 2003. See especially Butler et al. 2008 for the most recent assessment of the taxonomic composition of Ornithopoda.
So Zalmoxes has now received its name, but how is it related, phylogenetically, to other ornithopods? Our cladistic analyses clearly indicated that its closest relative was Rhabdodon. Together, Zalmoxes and Rhabdodon form a clade called Rhabdodontidae, which is most closely related to the group of ornithopods known as iguanodontians, the latter including animals such as Tenontosaurus, Iguanodon, hadrosaurids, and many other forms.
Now that we can recognize Zalmoxes as distinct from Rhabdodon and other ornithopods, we can also begin to understand its form and lifestyle (Plate V, top). The bones suggest a moderate-sized ornithopod (3–4 m long). Its body was stocky, it had a bipedal stance, and its back was held nearly horizontally, with its long muscular tail counterbalancing the front half of the body at the hip joint. The features of the bones of the fore- and hind limbs suggest that these regions were well muscled, whereas the ribcage seems more barrel-shaped than in other ornitho-pods. Limb proportions indicate that Zalmoxes was probably not a particularly fast runner, scurrying along at no more than 25 km/hour.74 Although it would be great if we had numerous trackways of Zalmoxes to test these calculations, there is a track site in the Vurpăr Formation near Sebeş (the only footprints known from the Late Cretaceous of Transylvania) that consists of two hind footprints thought to have been made by Zalmoxes. These tracks indicate a more leisurely walking speed of less than 7 km/hour.75
Figure 2.18. Skeletal reconstructions of Zalmoxes (above) and Rhabdodon (below). Scale = 100 cm. (Rhabdodon after Garcia et al. 1999)
The skull of Zalmoxes is relatively large but compact, with a short face (figure 2.19). Some individuals have a stout transverse crest above the eyes, perhaps a sign of sexual dimorphism or a sign of age. The narrow, toothless beak was probably covered in life with a sharp rhamphotheca (as also discussed for Struthiosaurus), and was thus likely to have been able to cut through tough foliage and fruits. Both the upper and lower jaws were strongly built, containing at least ten large, closely packed teeth. Patterns of tooth wear reveal that Zalmoxes chewed its food well, using a transverse grinding motion. The teeth are recessed from the sides of the face, suggesting—as in the case of Struthiosaurus and other ornithischians—that cheeks covering this region may have prevented food from slipping out of the sides of the mouth.
Figure 2.19. A reconstructed skull of Zalmoxes robustus. Scale = 10 cm. (After Weishampel et al. 2003)
We don’t know much about the sociality, growth and development, and reproductive behavior of Zalmoxes. On these matters, the fossil record has been silent. We do know that this ornithopod is probably the most common element within the Transylvanian assemblages, but whether it was truly gregarious or merely appeared frequently amid the fauna is unknown. Similarly, there are no data to suggest colonial nesting and parental care—or rule it out. For these aspects of a dinosaur’s life, we need to turn to the Transylvanian hadrosaurids.
The Transylvanian Ornithopods: Telmatosaurus transsylvanicus
The duckbills of the Late Cretaceous—members of Hadrosauridae—were among the most diverse forms of plant-eating dinosaurs, known principally from North America and Asia (figure 2.20). Many hadrosaurids are known from well-preserved fossils, including those of embryos, hatchlings, juveniles, teenagers, and adults. From these specimens, and from abundant nesting sites, we are learning more about parental care of offspring, group nesting, and the rapid growth rates that appear to characterize these ornithopods.
As we have noted previously, the first dinosaur described from the Haţeg Basin was a new genus and species of hadrosaurid dinosaur that Nopcsa named Telmatosaurus transsylvanicus. Virtually the entire skull and the majority of the postcranial skeleton of T. transsylvanicus, based on more than 100 cranial and postcranial elements, are known from a number of individuals of various body sizes collected at numerous localities in the Haţeg Basin and Transylvanian Depression.76 At an adult length of about 5 m, Telmatosaurus was one of the smallest hadrosaurid dinosaurs (Plate V, bottom), much smaller than hadrosaurids elsewhere in the world or their more distant relatives (such as Iguanodon), both of which ranged upwards of 10 m in length.77 We will return to this issue of body size and its evolutionary significance in chapter 6.
Even though the original material of Telmatosaurus that Nopcsa described in 1899 was severely crushed, we were able to compare it with other, subsequently discovered specimens and thereby reconstruct what the skull must have looked like in three dimensions (figure 2.21). What emerged from the reconstruction is a long, somewhat horselike cranium, reminiscent of Iguanodon and other hadrosaurids.78 The front of the snout (the premaxilla) is narrow, toothless, and crenulated, most probably supporting a rhamphotheca. Both the upper and lower jaws contain as many as 30 vertical positions for the teeth, far more toothy than the jaws of non-hadrosaurid iguanodontians, but considerably less so than in most other hadrosaurids. Both the upper and lower sets of teeth consisted of hundreds of functional and replacement teeth, interlinked to form dental batteries (figure 2.22). Such a complex arrangement of teeth, coupled with well-developed jaw muscles and a unique masticatory system, would have made short work of the toughest vegetation.79 Behind the head, the skeleton of Telmatosaurus looks much like that of both more primitive iguanodontians (such as Ouranosaurus and Iguanodon) and other hadrosaurids (like Brachylophosaurus and Maiasaura).80 However, its body was smaller than these taxa, and therefore not unduly bulky. Similar to other ornithopods (including Zalmoxes), the long tail, stiffened and strengthened by crisscrossing bony tendons, acted to counterbalance the front half of the body.
Figure 2.20. Diversity of skull morphology in hadrosaurids: Gryposaurus (above left), Edmontosaurus (above right), Saurolophus (below left), and Corythosaurus (below right). Scale = 10 cm. (After Weishampel and Horner 1990)
In 1993, Telmatosaurus was subjected to cladistic analyses to see where it fit within hadrosaurid evolution (box 2.5).81 Based on this work, which has been borne out in subsequent studies,82 Telmatosaurus appears to fit best as the sister group of both lambeosaurines and hadrosaurines. In 1993, Weishampel et al. called this latter clade Euhadrosauria, but most paleontologists have followed a more historical path, considering hadrosaurines and lambeosaurines as the sole members of Hadrosauridae; this makes Telmatosaurus a non-hadrosaurid hadrosauroid. In either taxonomy, the relationships remain the same: Telmatosaurus is a (or perhaps the most) primitive outsider to all other hadrosaurids. We will discuss the significance of the position of Telmatosaurus with respect to ornithopod evolution, especially in relationship to its small body size, later in this book.
Figure 2.21. A reconstruction of the skull of Telmatosaurus transsylvanicus (left) and a reconstruction of its head (right). Scale = 10 cm
Figure 2.22. A hadrosaurid dental battery (left), indicating
the complex interlocking pattern of replacement teeth (right). Scale = 5 cm
Large ornithopods in general were not particularly fleet of foot, and Telmatosaurus was no exception. Based both on hadrosaurid trackways and on limb proportions, these bipedal forms probably were able to reach a top speed of 15–20 km/hour during a sustained sprint, but at slower speeds and at rest, they apparently assumed a quadrupedal posture. In this position, Telmatosaurus most likely browsed no higher than a meter or so above the ground, probably using its forelimbs to grasp at leaves and branches in order to bring the foliage closer to its mouth.
BOX 2.5 Evolutionary Relationships in Hadrosauridae
Hadrosaurids, arguably the most important group of herbivorous dinosaurs at the end of the Cretaceous, especially in North America and Asia, are now known from more than 30 species. Traditionally, these have been placed in two subgroupings: hadrosaurines, with a solid crest or a flat head, on the one hand, and hollow-crested lambeosaurines on the other. Cladistic analyses of these species demonstrate the monophyly of both Lambeosaurinae and Hadrosaurinae (although support for the latter is not strong), which together form the larger Euhadrosauria. In addition, an ever-increasing number of taxa do not fit into the euhadrosaurian clade. Among them is the Transylvanian hadrosaurid Telmatosaurus transsylvanicus. Another is Bactrosaurus johnsoni, from the Late Cretaceous of northern China and southern Mongolia. Bactrosaurus has been interpreted as a lambeosaurine hadrosaurid and as a non-hadrosaurid hadrosauroid. Here we will treat Bactrosaurus as an unresolved basal hadrosaurid.
Note: For Euhadrosauria, see Horner et al. 2004; Weishampel et al. 1993. For non-hadrosaurid hadrosauroids, see Godefroit et al. 1998.
From Gryposaurus (with its arched snout), to Saurolophus (with its supracranial spine), to Parasaurolophus (with its hollow, plumelike crest), these dinosaurs stand out from the crowd with their wild headgear. In 1975, Jim Hopson of the University of Chicago examined the functional significance of these cranial adornments. He argued that the arches, spikes, hollow crests, and other cranial decorations evolved in the context of complex intraspecific social behavior. These crests were used in intraspecific aggression and display, both visual and vocal; in courtship displays; and in mate rivalries. Crests and the rest presumably helped hadrosaurids recognize kin, avoid enemies, display to each other and to members of different species, communicate with offspring, and establish social hierarchies—an amazing evolutionary achievement that placed hadrosaurids in the top ranks of complex social behavior among dinosaurs.
As a basal member of the group, Telmatosaurus may have something to tell us about the origin of these aspects of hadrosaurid sociality. New Telmatosaurus material indicates that this dinosaur had a pair of sinuous ridges that ran along the sides of the snout. Though less dramatic than the headdresses of more evolved hadrosaurids, these ridges would have made its face more visually interesting than those of more primitive ornithopods. Were the ridges parts of a display apparatus, perhaps a progenitor to the exhibitionists yet to come? Were these sigmoidal ridges sexually dimorphic? We don’t yet know. Nor can we say with certainty whether Telmatosaurus was territorial, or engaged in parental behavior. The only other aspect of behavior known in this Transylvanian hadrosaurid is an ever-so-brief glimpse into its early growth and development, which comes from the discovery of embryo or baby bones associated with some eggs unearthed in the late 1980s.
The Haţeg Dinosaur Egg Nests
Nests and nesting horizons are among the most exciting dinosaur discoveries in Romania over the past decade and a half. The first announcement of Haţeg Basin eggs came in 1989, through work near the village of Tuştea by researchers from Universitatea din Bucureşti.83 Another site, Toteşti-baraj, was discovered by the joint expedition from Universitatea Babeş-Bolyai Cluj Napoca, Romania, and Brussels’ Institut Royal des Sciences Naturelle de Belgique in 2000.84 The eggs within these nests seem to be laid in a somewhat organized, curvilinear fashion.85 In life, the eggs would have been nearly spherical, approximately 15 cm in diameter, and nearly a liter in volume (figure 2.23). On average 2.4 mm thick, the eggshell is covered with an irregular pattern of small, hemispheric tubercles. This locality has thus far produced forty eggs distributed in eleven different nests. It is not certain what the conformation of each nest is, but the eggs themselves, although deformed, also appear to be subspherical in shape, with a diameter of about 15 cm.
Figure 2.23. A reconstruction of the dinosaur nest from Tuştea. Scale = 15 cm. (After Grigorescu et al. 2010)
In addition to their macroscopic features, still more information can be discerned about these eggs under the microscope (figure 2.24). At a magnification of about 80 power, the eggshell reveals its mineral structure. The eggshell is calcite, organized into structural units that vary characteristically among different egg-laying species. Circa the early 1990s, Karl Hirsch and Konstantin Mikhailov erected a classification scheme for these structural units.86 They identified basic types, each broken down into subgroupings to produce a taxonomy of names that trip up the most dexterous tongue: dendrospherulitic, angusticanalicu-late, Laevidoolithidae. Still, it’s often difficult to attribute these categories to particular kinds of egg-laying animals, in large part because we generally lack a direct connection between eggs and moms. However, some truly remarkable occurrences—embryonic remains preserved in fossil eggs—have proven to be a Rosetta Stone. Consequently, we know that eggs found in Montana, which fall within the Mikhailov/Hirsch category termed Spheroolithidae, were laid by the hadrosaurid called Maiasaura, because they were found with the embryonic or hatchling bones of this dinosaur.87 On a similar basis, we know that oviraptorid theropods laid elongatolithid eggs, and, based on discoveries in Argentina made in 1998, titanosaur sauropods laid megaloolithid eggs.88
Figure 2.24. One of the eggs recovered from Tuştea (left), indicating the surface texture (above right) and a shell cross-section (below right). Scale = 10 cm. (After Weishampel et al. 1991)
Based on their architecture, the Tuştea eggs likewise belong to the Megaloolithidae category, sharing similarities in microstructure, pore organization, size, and shape with some of the eggs from southern France. The only principal difference is in nest structure: the French megaloolithid eggs apparently were laid in sweeping curves instead of curvilinearly.89 Although no embryonic remains associated with these eggs have ever been recovered in France, they are thought to have been laid by a titanosaur sauropod, an animal of the right size to have laid such an egg and one common in the Late Cretaceous fauna of the region. Realizing that we also had sauropods in the Haţeg fauna, at first we suggested, in 1990, that these eggs may have been laid by one or the other titanosaur from Transylvania.90
Even more significantly, the bones of either full-term embryos or newborn hatchlings (technically called perinatal remains) were also discovered at the same site, in fact from the same bedding planes that yielded the Tuştea egg clutches. Consisting of partially articulated skeletons and additional associated remains, the specimens can be identified with confidence as those of a hadrosaurid (most probably Telmatosaurus), even though the joint surfaces of the bones are very porous and the surface texture of their shafts is immature (figure 2.25).91 Their proximity to the Tuştea eggs suggested that the perinatal remains belong with the eggs; that is, the female who laid the eggs would have been the mother of the babies whose small bones we found. This question of who laid the Tuştea clutches has brought some consternation to dinosaur “egg-ologists”: the structure of the Tuştea eggs resembles that of titanosaur sauropods (thereby implicating Magyarosaurus as the egg-layer), whereas the perinatal fossils come from a hadrosaurid (suggesting that the parent was Telmatosaurus).92 This conflict might be solved if we found identifiable embryonic remains preserved inside the Tuştea eggs and not alongside them. Some scanning electron microscopic photographs have been taken,93 but they are far from conclusive.
This conundrum—titanosaur or hadrosaurid eggs—has been indirectly solved by discoveries made half
way around the world, in the badlands of Patagonia in the southern half of Argentina.94 It was here, at a site known as Auca Mahuevo, that an extensive nesting ground—covering more than a square kilometer and littered with tens of thousands of large, unhatched eggs—was discovered in 1997 by an expedition led by Luis Chiappe from the Natural History Museum of Los Angeles County, Lowell Dingus from the American Museum of Natural History in New York, and Rodolfo Coria from the Museo Municipal Carmen Funes in Plaza Huincal, Argentina. Unlike the Haţeg clutches, those from Argentina were organized into clusters of between 15 and 34 eggs. Most spectacularly, and of particular relevance here, was the fact that a high proportion of these eggs contained embryonic skeletons, some with the impressions of embryonic skin! Moreover, these imprisoned embryos, many of them in near articulation, possess nearly complete skulls that clearly belong to titanosaur sauropods.
Figure 2.25. Perinatal hadrosaurid remains from Tuştea: a distal femur (left) and a proximal tibia (right). Scale = 10 mm. (After Weishampel et al. 1993)
Transylvanian Dinosaurs Page 6
