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Authors: Peter Ward

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The utilization of egg laying or live birth has important consequences for land animals. The embryos developed by the live-birth
method are not endangered by temperature change, desiccation, or oxygen deprivation. But the cost is the added volume of the parent, which must invariably make her more vulnerable to predation in addition to needing more food than would be necessary for the adult alone. Egg layers are not burdened with this problem, but have the trade-off of a less safe environment—the interior of an egg outside of the body—that leads to enhanced embryonic death rate through predation or lethal conditions of the external environment.

Before the end of the Mississippian period three great stocks of reptiles had diverged from one another to become independent groups: one that gave rise to mammals, a second to turtles, and a third to the other reptilian groups—and to the birds. The fossil record shows that there are many individual species making up these three. A relatively rich fossil record has delineated the evolutionary pathway of these groups. It has also required a reevaluation of just what a “reptile” is. As customarily defined, the class Reptilia includes the living turtles, lizards, and crocodiles. Technically, reptiles can now be defined by what they are not: they are amniotes that lack the specialized characters of birds and mammals. Less appreciated is that all three of these lineages originated in a world with extensive glaciation and very high oxygen. It is the assumption here that coming from a cold but high-oxygen world would have affected many aspects of the biology of these animals. Let us look at some of these characteristics.

One of the enduring questions about the history of life concerns the history of thermoregulation in animals. There are three distinct kinds: endothermy (warm-blooded), ectothermy (cold-blooded), and a third category (homeothermic) that is essentially neither of the others, and is associated with very large size. The evolution of each of these has long attracted scientific scrutiny, with thermoregulation pathways—most important, the question of whether or not dinosaurs were warm-blooded—being the most discussed and controversial of all. The fact that each of these characteristics is primarily either physiological or involved body parts that only rarely leave any fossil record (such as fur) is in large part responsible for the controversies.

We know that all living mammals and birds are warm-blooded, with the former having hair and the latter feathers, just as we know that all living reptiles are cold-blooded, with neither hair nor feathers. The status of extinct forms remains controversial. Of interest here is whether or not oxygen concentration and/or characteristic global temperatures affected thermoregulation or characteristic body covering in the various stocks in the past.

REPTILE DIFFERENTIATION

The number of openings in the skull is a convenient way of differentiating the three major stocks of “reptiles.”
10
Anapsids (ancestors of the turtles) had no major openings or fenestra in their skulls; synapsids (ancestors of the mammals) had one; and diapsids (dinosaurs, crocodiles, lizards, and snakes) had two. The fossil record suggests that all three arose at a time of high atmospheric oxygen.
11
The earliest member of the latter group, the diapsids, is known from latest Pennsylvanian rocks, and it was small in size, about twenty centimeters in total length. From the time of their origin until the beginning of the fall of oxygen, which probably began in earnest some 260 million years ago, in the middle and late part of the Permian period, this group did little in the way of diversification or specialization. They remained small in size, and while the split to the various diapsid groups may have happened in the latest Pennsylvanian through early Permian (the time of highest oxygen), the animals themselves remained small and lizard-like. They gave no indication that they would be the ancestors of the largest land animals ever to appear on Earth, in the form of the Mesozoic dinosaurs. If the time of highest oxygen stimulated insects to their greatest size, the same cannot be said of the diapsids.

The most pressing questions are whether or not this group was warm-blooded and how it reproduced. No unequivocal Permian eggs are known at all from any group, so we cannot know how they bred. It is presumed that they laid primitive amniotic eggs with a leathery covering on land, but we cannot rule out the possibility of live birth. It was not until the latest Permian—well into the oxygen crisis that was
to culminate in the greatest of all mass extinctions—that the diapsids were stimulated into the diversifications they would become famous for. After all, they gave rise to dinosaurs.

The diapsids evolved shapes allowing movement. They were fleet carnivores. One of the other reptile groups, the anapsids, took another direction. No one would accuse a turtle of being fleet afoot, and that is what the anapsids became: turtles, and before that, huge slow-lumbering monsters known as pareiasaurs, one of the largest of all skeletonized reptiles known from the late Permian world.

Based on their earliest members, however, it would have been hard to predict that the anapsids would become so slow and lumbering and hiding inside armor. They were initially smaller, faster, and very successful during the Late Pennsylvanian, but less so into the Permian. As the glaciers receded from the long ice age spanning the first half of the Permian period, they evolved into giant forms, including cotylosaurs and the even larger pareiasaurs. These were armored giants, surely slow moving, and herbivores that lived right until the end of the Permian. It is very likely that the gigantic size of the earlier Permian anapsids was allowed by high oxygen.

The last major reptilian group was the synapsids, and these were our own ancestors. If diapsids did little during the Pennsylvanian through the early Permian oxygen high, the same cannot be said of the third group of amniotes from this time, the synapsids, or mammal-like reptiles. Like the diapsids, the most primitive are known from Pennsylvanian rocks, and also like the diapsids of this time, these ancestors of the mammals had a small, lizard-like shape and mode of life in all probability. It is assumed that like the diapsids (and the amphibians that they came from), these early synapsids were cold-blooded. They, in turn, gave rise to two great stocks: the pelycosaurs, like early Permian
Dimetrodon
, and their successors, the therapsids, the lineage giving rise to the mammals. It is this latter group that is also called the mammal-like reptiles.

Unlike the diapsids, the synapsids diversified during the oxygen high and at the peak of oxygen became the largest of all land vertebrates. In the latter part of the Pennsylvanian, the pelycosaurs probably
looked and acted like large monitor lizards, or even the iguanas of today, with splayed limbs. By the end of the Pennsylvanian some attained the size of the Komodo dragon of today, and they may have been fearsome predators. By the beginning of the Permian period, some 300 million years ago, they made up at least 70 percent of the land vertebrate fauna. And they diversified in terms of feeding as well. Three groups were found: fish eaters, meat eaters, and the first large herbivores.

Both predators and prey could attain a size of close to fifteen feet in length, and some, such as
Dimetrodon
, had a large sail on the back that would have made them appear even larger. They also either partially or totally solved the reptilian problem of not being able to breathe while running by changing their stance. The synapsids show an evolutionary trend of moving their legs into a position so that they were increasingly under the trunk of the body, rather than splayed out to the side, as in modern lizards. This created a more upright posture, and removed or at least greatly decreased the lung compression that accompanies the sinuous gait of lizards and salamanders. While there was still some splay of the limbs to the sides of the trunk, it was certainly less than in the first tetrapods. With the evolution of the therapsids in the Middle Permian, the stance became even more upright.

The sail present on both carnivores and herbivores of the Late Pennsylvanian and early Permian is a vital clue to the metabolism of the pelycosaurs; it was a device used to rapidly heat up the animal in the morning hours. By positioning the sail so as to catch the morning sun, both predators and prey could rapidly warm their large bodies, allowing rapid movement. The animal first attaining warm internal temperature would have been the winner in the game of predation or escape, and hence natural selection would have worked on this. But the larger clue from this is that during the oxygen high, the ancestors of the mammals had not yet evolved endothermia, or “warm-bloodedness.” So when did this trait first appear? That revolutionary breakthrough must have happened among the successors to the pelycosaurs, the therapsids. We must note as well that this period, while a time of oxygen high, was a period of low temperatures. There was a great glaciation known from this interval, and a sizable portion of the
polar regions of both hemispheres would have been covered in ice, both continental and sea ice.

While much of our understanding of pelycosaurs’ evolution comes from fossils found in North America, younger beds in this region have few vertebrate fossils. The transition to the therapsids is best seen in Europe and Russia, but even here the transition is poorly known because of few fossiliferous deposits of the critical age. This gap in our knowledge of the synapsid fossil record extends from perhaps 285 million years ago to around 270 million years ago. Two main regions tell us about the history of this group: the Russian area around the Ural Mountains, and the Karoo region of South Africa. The record in the Karoo begins with glacial deposits perhaps as much as 270 million years in age, and then there is a continuous record right into the Jurassic, giving an unparalleled understanding of this lineage of animals.

The therapsids split into two groups: a predominantly carnivorous group and an herbivorous group. By about 260 million years ago the ice was gone in South Africa, but we can assume that the relatively high latitude of this part of the supercontinent Pangaea (about 60 degrees south latitude) remained cool. It was still a time of high oxygen, certainly higher than now, but that was changing. As the Permian period progressed, oxygen levels were dropping. Seemingly two great radiations of forms occurred, among both carnivores and herbivores. From perhaps 270 to 260 million years ago the dominant land animals were the dinocephalians, and these great bulky beasts reached astounding size: not dinosaur sized, but certainly approaching any land mammal today save, perhaps, elephants, and some of the largest of the dinocephalians certainly must have weighed as much as elephants.
Moschops
, for instance, a common and well-known genus from South Africa, was five meters high, with an enormous head and front legs longer than the back. It was hunted by a group of similarly sized carnivores.

The dinocephalians and their carnivores were hit by a great extinction, still very poorly understood, that occurred some 260 million years ago. There is still little range data for both the dinocephalians and their immediate successors in terrestrial dominance, the earliest
dicynodonts and their predators. Until new fossils from South Africa and Russia are obtained, this uncertainty will remain. Sadly, there are few fossils of this age and fewer paleontologists studying them, so we may not know for generations, assuming that future generations continue to hunt fossils.

Gorgonopsian skull from Late Permian deposits, South Africa. (Photo by Peter Ward.)

The dicynodonts were the dominant herbivores of the time from 260 to 250 million years ago. They were almost eliminated from the planet in the Permian extinction, which we will describe in more detail in the next chapter. They were hunted by three groups of carnivores: the gorgonopsians, which died out at the end of the Permian, the slightly more diverse therocephalians, and the cynodonts, which ultimately evolved into mammals during the Triassic.

ANIMAL SIZE AND OXYGEN LEVELS

The rise of atmospheric oxygen to unprecedented values of over 30 percent was accompanied by the evolution of insects of unprecedented
size. The giant dragonflies and others of the late Carboniferous through the early Permian were the largest insects in Earth history. Perhaps it is just coincidence, but most specialists agree that the high oxygen would have enabled insects to grow larger, since the insect respiratory system requires diffusion of oxygen through tubes into the interior of the body, and in times of higher oxygen, more of this vital gas could penetrate into ever larger-bodied insects. So if insects got larger as oxygen rose, what about vertebrates? New data indicates that this is true as well.

In 2006, paleontologist Michel Laurin measured fossil skull lengths and body lengths of various reptiles ranging from the Carboniferous through the Permian, from about 320 million years ago until about 250 million years ago. Both of the size descriptors closely tracked oxygen levels. As O
2
levels rose in the Late Carboniferous, so too did the size of the reptiles increase, and, as O
2
began to drop in the mid Permian, size began to trend downward. As we will return to in the chapter on Cenozoic mammals, study on (much) later mammals, by Paul Falkowski and his colleagues, demonstrated a very similar phenomenon during the Early Cenozoic, when oxygen levels have been modeled to have risen significantly, while at the same time, the mean size of mammal species also increased.

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