Preliminary thin-section work relating to when particular developmental stages occur during the lifetime of dinosaurs has been done on some of the ones from Transylvania. Ragna Redelstorff, Zoltán Csiki, and Dan Grigorescu conducted histological studies of a series of femora from Telmatosaurus transsylvanicus, to test whether the largest among them (464 mm long) come from small adults (i.e., dwarfed taxa) or from juveniles of more normal-sized taxa.52 Histologically, these femora exhibit up to eight lines of arrested growth, and the outermost layer of the largest femur is very thin and avascular, indicating that growth had either slowed down considerably or ceased. Such bone microstructure indicates that the largest femora belong to fully adult dwarfed individuals, not juveniles of much larger forms. The reduction in body size was presumably caused by a slowdown of their growth rate.
A decidedly different bone histology is encountered in Magyarosaurus dacus.53 Thin-sections were again made of different sizes of long bones (femora 346–545 mm long, humeri 223–488 mm long) but, unlike the situation in Telmatosaurus, the overwhelming majority of the cortex in each of these sections is extensively remodeled by secondary bone. There is almost no preservation of primary bone that could record lines of arrested growth, even in the smallest individuals. Koen Stein and his coworkers noted that the intense secondary remodeling in the bones of Magyarosaurus is closest to that of other individual sauropods of very late histological ontogenetic stages. Although lacking a thin avascular outer layer that would indicate reduction or cessation of growth (as in Telmatosaurus, above), the early appearance of secondary remodeling in Magyarosaurus suggests an early onset of sexual maturity and a short lifespan.
Finally, there is Zalmoxes robustus. As before, with Telmatosaurus, Redelstorff and her coworkers studied the histology of a series of femora (164–355 mm long) to test whether the largest of these represent dwarfed adults or juveniles of normal-sized taxa.54 The long-bone histology reveals a slow growth rate in Zalmoxes, indicated by the high number (15) of narrow-spaced lines of arrested growth. However, vascular canals in the cortex open onto the bone surface, which indicates that growth had not plateaued at the time of death. Thus it is likely that the existing material of Zalmoxes represents bones not yet fully grown, and this ornithopod can probably be characterized by an extreme slowdown of its growth rate and an extended growth period.
We began this chapter describing the ways in which dinosaurs have pushed the envelope of body size, and, in so doing, they have provided a heterochronic context for their enormity. Although peramorphosis appears to be the main driving force in the evolution of nonavian dinosaurs,55 several examples of paedomorphosis have also been identified in this group,56 and these claims have led us to consider the importance of heterochrony more generally in dinosaurian evolution. Nopcsa’s notion that the dinosaurs from Transylvania were dwarfed could well be equivalent to seeing them as an assemblage of heterochronic Peter Pans. To this end, we have begun exploring both ontogenetic and phylogenetic aspects of both size and shape changes in the hadrosaurid Telmatosaurus, as well as in the titanosaurian sauropod Magyarosaurus and the primitive ornithopod Zalmoxes.
Who, What, Where, and When: Optimization and Cladograms
Optimization is our tool of choice when placing characters in their phylogenetic context. Once we have an explicit, well-supported cladogram for a particular group of organisms, we can then use this tree to determine the most parsimonious distribution of other aspects of this taxon, be it adaptation, coevolution, historical biogeography, biomechanics, or ecology. The use of phylogenetic trees as the basis for determining the most parsimonious sequences of evolutionary transformations for these additional characters—known as character optimization—does not help build trees, but instead is used for evaluating the behavior of other features on trees that are already constructed.57 This a posteriori method has been used to evaluate historical biogeographic relationships, to infer soft-tissue anatomy in extinct vertebrates, and to project the function and behavior of living organisms into the past.58
Let’s look at some simple examples of how a posteriori character optimization works. Figure 5.6a illustrates four taxa with a known relationship, all of which also share the same character (here we go with geographic distributions—they are all known from area A—but the characters to be optimized might be soft anatomy, biomechanics, physiology, or other features not included in the original cladistic analysis). Where is the ancestor of taxon 1 and taxon 2 (node 5) likely to have come from? Of course, it could be anywhere, but the most parsimonious interpretation is that this ancestor shared the same locale (area A) as its two descendants. When further relationships are considered (taxa 3, 4), since they all come from area A, then it’s obvious that the ancestors (nodes 6, 7) are also inferred to have come from area A. Once we’re at the base of the tree (character generalization), we then, in figure 5.6b, double check our ancestral characters back up the tree to resolve any ambiguities that may be left (character optimization). In this case, there is none—all of the nodes have A as their ancestral area. In other words, the evolution of this clade would be considered to be endemic to area A.
Yet what if there is a mixture in where the members of a clade come from? In figure 5.6c, half of the taxa (1–4), those to the right, are from area A, while those from the other half (5–8), on the left, are from area B. Generalizing down the tree, we know that the ancestors reconstructed at nodes 9, 10, and 11 would also have been found in area A, using the same logic we applied when confronting the situation in figure 5.6a. But what about the ancestral area at node 12—is it area A or B? Clearly something happened here, but we don’t yet know what it is. In truth, it could be either one, so we register it as “?A/?B” and then move down the tree yet another step to node 13. Here, we compare the area for taxon 6 and that for node 12. Area B is held in common with node 12, so we infer that the ancestral area at node 13 is B. Thereafter, down the tree, area B is inferred to the ancestral areas at nodes 14 and 15.
Figure 5.6. A posteriori character optimization (see text for explanation)
In order to resolve what’s going on at node 12, in figure 5.6d we optimize the characters back up the tree. The ancestral area at nodes 15, 14, and 13 is clearly B. We then compare node 13 with taxon 5 to resolve the ambiguity that we encountered during the generalization phase at node 12. Area B is held in common between node 13 and taxon 5, so we infer that the ancestral area at node 12 is B. With all remaining ancestral areas already identified as A, figure 5.6e shows that the shift from area B to area A occurred between nodes 12 and 11.
These examples have been simple and direct, but you can imagine how strenuous it would be to do this by-hand effort for clades with many members from disparate geographic regions. This problem is even more acute for sets of cladograms that are equally the most parsimonious ones. Fortunately, a posteriori optimization of characters on a tree is more easily accomplished by using any of the available numerical cladistic algorithms, such as PAUP, MacClade, and Winclada.59
Getting Small, Telmatosaurus-Style
Combing through the drawers of fossil bones and teeth, often in dusty, dark basement rooms in museums and universities, is very much like being in the field. You never know what you might discover next. Perhaps it will be some bone that indicates something new, something different, or something overlooked by the people who had studied it before.
Imagine yourself inside the Hungarian Geological Survey building, with its picturesque blue-and-white checked ceramic roof and rooms with vaulted ceilings, being turned loose among the collection of fossils by Dr. László Kordos, curator of these bones and teeth. Here, amid the pleasant smells of pipe smoke and hearty coffee, is where the considerable fossil remains from the Late Cretaceous of Transylvania are stored.
Our trek through these specimens yields the usual assortment: isolated vertebrae and limb bones, trays of teeth, and indeterminate scraps of bone. No surprises there—we’ve seen the likes of these before, and it’s easy to assign them to p
articular kinds of dinosaurs. Then, from one of the drawers, we find something totally unexpected. According to the label, these teeth are supposed to belong to Telmatosaurus, but they certainly don’t look like any sort of hadrosaurid teeth we’ve seen before. They’re relatively wide, somewhat like the teeth of Iguanodon, and they don’t display the typical strongly developed, vertical ridge of other hadrosaurids; instead, there are several low ridges on the enameled side of each tooth (figure 5.7, middle). Excitedly, we think we’ve discovered a new form of dinosaur, previously overlooked by Nopcsa and all who have come after him. At least that’s our first reaction. However, we must be sure whereof we speak, so it’s off to the literature. There, in black-and-white on plate VI, figure 3, in Nopcsa’s 1900 monograph on Telmatosaurus, are these same teeth: he had clearly recognized that they belonged to this hadrosaurid and, furthermore, that this lower dentition had a different morphology than do the teeth in the upper jaws.60 Disappointed and chastened, we are nevertheless enlightened and perplexed at the same time. What are these teeth of Telmatosaurus telling us?
Figure 5.7. The lower teeth of Iguanodon (left), Telmatosaurus (middle), and Maiasaura (right). Scale = 1 cm
In order to answer this question, we need to look at the teeth of a wide array of iguanodontian ornithopods, such as Iguanodon, Ouranosaurus, Camptosaurus, and Tenontosaurus, and try to understand how they changed during the process of tooth replacement. Morphologically, the squat, lozenge shape of the teeth of these forms is regarded as the primitive condition for the Iguanodontia. As these ornithopods grow during their lifetime, their “baby” teeth are rather small, but, as these teeth are replaced throughout life, they become proportionately much larger. Concomitantly, the number of teeth necessary to fill up the jaws doesn’t increase very much, compensating instead by an increase in tooth size during ontogeny. Take Iguanodon, for example (figure 5.7, left). As it grows, its teeth get much larger as they are replaced (a 300% increase in tooth size during ontogeny), but the number of tooth positions remains roughly the same (about a dozen tooth positions from juvenile to adult).
Compared with this more primitive system of replacement, hadrosau-rids do something entirely different. In these ornithopods, the dentary teeth increase in size only slightly during ontogeny. With adult teeth nearly the size of the “baby” teeth, it is the enormous increase in the number of tooth positions in the jaws that compensates for increasing jaw size as the animal gets larger during ontogeny. For example, Maiasaura hatchlings have a dentary dentition consisting of approximately 10 tooth positions filled by 6 mm wide teeth, whereas adults have jaws containing 40–45 tooth positions filled by 8 mm wide teeth (figure 5.7, right). Compared with the primitive ornithopod condition, hadrosaurids have added teeth like crazy, expanding not only the length of the dentition as the jaw grows, but also providing the possibility of having a greater number of closely packed replacement teeth at one time. In this way, the classic hadrosaurid dental battery is created.61
Figure 5.8. Telmatosaurus as a dwarf. The solid silhouette represents an iguanodontian ornithopod of ancestral body size; the open silhouette represents Telmatosaurus. Scale = 2 m
Fitting Telmatosaurus into this picture, our Haţeg hadrosaurid is little different morphologically from the somewhat more basal iguanodontians Ouranosaurus or Iguanodon, except in two respects—its smaller body size (figure 5.8) and the size and shape of its teeth (figure 5.9). The upper teeth of Telmatosaurus are narrow, diamond-shaped, and equipped with a single, centrally placed ridge; in other words, they are most like the juvenile condition seen in non-hadrosaurid iguanodontians. Its lower teeth, in contrast, are wider, asymmetrical, and bear several low ridges, making them intermediate between those of other hadrosaurids and more primitive iguanodontians. These teeth, too, were small, but they most resemble the shape of adults of non-hadrosaurid iguanodontians.
How this baby-toothed condition arose in hadrosaurids can be evaluated by optimizing body size and tooth development onto the cladogram of Iguanodontia (figure 5.10). Optimization is an a posteriori method for identifying the most parsimonious sequence of character changes by reference to an explicit phylogenetic tree. As we learned in chapter 2, the majority of hadrosaurids belong to two major subgroups, the hollow-crested lambeosaurines and the flat-headed, nasal-arched, solid-crested hadrosaurines, which together form the group called Euhadrosauria. Several hadrosaurids, Telmatosaurus prominent among them, are positioned below this clade of euhadrosaurians, but above non-hadrosaurid iguanodontians such as Ouranosaurus and Iguanodon.62 When body and tooth size are optimized on this cladogram, they fall out as a peramorphocline from the base of Iguanodontia to the base of Hadrosauridae. At this nexus, something happens to this ever-increasing relationship: body size trends reverse themselves, and the basal members of the hadrosaurid clade then undergo downsizing, not only in body size, but also in the size of their teeth. Thereafter, the evolutionary history of tooth size is decoupled from that of body size—as body size trends become peramorphic again, the teeth remain miniaturized, like those of juveniles.
Figure 5.9. The relationship between dentary tooth width and tooth row length for both non-hadrosaurid iguanodontians and hadrosaurids. Note that Telmatosaurus transylvanicus plots among juvenile hadrosaurids and not far from the juveniles of non-hadrosaurid iguanodontians.
Figure 5.10. A cladogram of higher iguanodontian ornithopods, indicating the dwarfing event leading to Telmatosaurus and Tethyshadros. The bar immediately below Hadrosauridae indicates the acquisition of miniaturized maxillary teeth.
In summary, we regard the small adult size seen in Telmatosaurus as the trigger for the evolution of the dental battery of duck-billed dinosaurs, the hallmark of Hadrosauridae. By arriving at adulthood having a smaller body size than its ancestors did, Telmatosaurus was assured that its teeth would resemble those in the younger ancestral stages. This juvenilization of their teeth amounts to arrested growth, otherwise known as paedomorphosis. Thereafter, euhadrosaurians increased in body size, but retained their juvenile dentitions into adulthood. This juvenile dentition, which was organized into a closely packed battery of miniaturized teeth with a complex occlusal surface, was passed on to their descendants.63 In this way, the Peter Pan syndrome provided the means by which the duckbills developed their complex dentitions.
Magyarosaurus: The Smallest of the Largest
Being the largest of all terrestrial organisms, sauropods assuredly packed a lot of weight onto their limbs. Standing still, an average adult Apatosaurus had to withstand 10 metric tonnes on its forelimbs and 24 metric tonnes on its hind limbs and, to amble across the Mesozoic countryside, these same limbs would have to have been built to withstand double or triple these loads.64
The stresses on the limbs of sauropods smaller than Apatosaurus obviously would have been less. This would also have been the case for juveniles and subadults of Apatosaurus and of youngsters of other species. Does that mean that the limb bones of adults should display different scaling properties when compared with those of a growth series? Because Magyarosaurus adults are the smallest among sauropods, we were interested to find out.
At a length of 5–6 m, and weighing in excess of 750 kg, Magyarosaurus is certainly among the smallest of all known sauropods (figure 5.11), as originally noted by Nopcsa in 1915.65 Although there are no complete or even partially articulated skeletons, this sauropod is known from abundant material representing nearly the entire skeleton, all collected from the Upper Cretaceous rocks of Transylvania.
In addition to gaining a reasonably good understanding of the anatomy of Magyarosaurus, we are also coming to learn more about its position in the evolutionary history of sauropods. Since their original discovery and the fulsome years of exploration in the American West, the excavations at Tendaguru (Tanzania), the finds in Sichuan (China), and the discoveries from Patagonia in South America, the phylogeny of sauropods was anything but clear. However, thanks to a number of recent phylogenetic analyses, their internal relationships are
becoming much better understood.66 For our purposes, it is important to remember that Magyarosaurus is a titanosaur, a clade of sauropods that includes Rapetosaurus, Saltasaurus, and Malawisaurus, and it is more closely related to Brachiosaurus and its relatives than it is to other sauropods such as Diplodocus (chapter 2). Together, all of these sauropods play an important role in providing the evolutionary context for understanding the heterochronic significance of Magyarosaurus.
In the late 1990s, the two of us, along with Jason Mussell, then a graduate student at the Johns Hopkins University, decided to approach growth and development in these sauropods by examining the size and shape of the humerus and femur. We collected a variety of measurements from our specimens and analyzed the significance of these data, using both statistics and phylogeny. For our statistical analyses, we assembled one series consisting solely of adults and another that combined growth stages drawn from a mixture of 25 titanosaurs and brachiosaurs that are closely related to Magyarosaurus.67 By focusing on the long bones of these sauropods, we sought patterns of heterochrony using young and adult individuals, in this case in terms of the biomechanics of long-bone design. A limb bone must obviously be built to withstand, without fracturing, the great loads that pass down their length. A bone’s ability to resist this kind of load is proportional to the area of its cross-section, so for sauropods, long-bone proportions are particularly sensitive to changes in body size. Naturally, we wanted to see just what kind of humeral and femoral dimensions Magyarosaurus and other sauropods, young and old, have relative to each other, by examining them in a way that reflects their strength. This again is a exercise in scaling, so we set about determining the relationship between the length of these long bones and their midshaft widths, dividing the sauropod sample into individuals thought to be fully adult, and other individuals that could be assembled into a growth series from smallest to largest. Age classing of humeri and other bones is often difficult with ever-growing animals such as dinosaurs. However, as we have already seen in the case of Telmatosaurus and the other ornithopods we compared it with, it was possible to get an idea about the approximate maturity of an individual sauropod. The features we looked at were the degree of fusion of the bones of the braincase and vertebrae, the maturity of the joint surfaces of the limb bones, overall body size, and (sometimes) anecdotal comments in the literature. In nearly all cases, the largest individuals of a species were identified as adults.
Transylvanian Dinosaurs Page 13
