by Peter Ward
Reefs, in fact, are very ancient evolutionary inventions,1 and their rise to prominence mirrors the rise to high diversity that followed the Cambrian explosion. In a way a hydrogen bomb is a good analogy. Thermonuclear fusion and the enormous explosion that ensues only take place in the immense heat of an atomic explosion. That is how a hydrogen bomb works: an atomic (fission) bomb with plutonium is ignited, which in turn creates sufficient heat and pressure to start the fusion reaction—and fusion explosion. In similar fashion the Cambrian explosion of diversity was the heat and fuel that led to the far greater Ordovician diversification, and one of the most important of the products of this huge run-up in species numbers was the invention of the coral reef.
The first reefs—and by reef, we mean a wave-resistant, three-dimensional structure built by organisms—date all the way back to the earliest Cambrian period. They were not coral reefs, but composed of archaic, now long-extinct sponges called Archeocyathids.2 Coral reefs are slightly younger; the first of these are found in the Ordovician period, and they really increase in distribution, size, and diversity by the Devonian period. They remained a rather constant and ecologically recognizable ecosystem until the end of the Permian—when the reefs and so much else were decimated by the Permian mass extinction.
Let us imagine that we were capable of going back into time and take a dive on a Paleozoic coral reef, one that is 400 million years in age. At first glance there is a surprising similarity to the reefs of today. Corals dominate the reefs; they are the bricks of the 3-D structures that are reefs, and like a brick house, are held together by many kinds of biological mortar, mostly encrusting species that serve to cement and bind the many heads and coral fronds into enormous and complex ramparts and foundations of limestone. But on closer view, the 400-million-year-old corals can be seen to be entirely different in basic appearance, and certainly in taxonomic composition. The massive coral heads are composed of a family that while building overall shapes similar to the corals of today are actually very different in their finer morphology: these are the tabulate corals, and these filled the same niches as are held today by scleractinian corals, the common corals of our modern reefs. Between these broadly branching and hemispherical tabulate coral colonies are other “framework builders,” other bricks in the wall. Many of these are stromatoporoids, a strange, carbonate-producing sponge still living today, but never in the sizes or diversity of the Paleozoic era. Scattered among these two massive inhabitants are a second kind of coral, solitary in nature, called rugose corals, solitary species that look like the horns of a bull, but in this case the pointed end of the “horn,” the calcium carbonate skeleton of these rugose corals, are cemented to the substrate, and the widest end, facing up, is the seat for a single broad sea-anemone-looking animal.
Like our modern scleractinian corals, no matter how large, and composed of how many of the small, tentacled bodies that are the basic body plan of a coral, the tabulates were a single “individual”—at least genetically. But in fact all corals, surely then as well as now, are vast colonies of tiny sea-anemone-like polyps, each a ring of poison-tipped tentacles surrounding a small central mouth. But unlike a seashore rock covered with a smattering of the small, common sea anemones (which are solitary polyps) found the world over, each of these tiny polyps linked to others around it by a thin sheet of tissue. Every part of these sometimes-vast colonies is genetically identical. But this is not just one animal. In fact, any coral supports a vast and diverse assemblage of plants within its tissues. Throughout both the coral’s polyp-to-polyp connecting tissue, as well as in the polyp itself, are untold numbers of tiny plants—single-celled dinoflagellates that live in symbiotic bliss with the corals. It is a great deal for both: the tiny plants get the four things they most want: light, carbon dioxide, nutrients (phosphates and nitrates), and protection within the coral flesh, protection from the many organisms that would love to dine on a tasty if tiny plant.
ORDOVICIAN DIVERSIFICATION: BUILDING ON THE CAMBRIAN EXPLOSION
The Cambrian period came to an end because of a mass extinction, one that affected many of the more successful members of what has come to be known as the Cambrian fauna—sea life composed of such early animal entrants in the overall history of animal life as trilobites, brachiopods, and many of the very exotic arthropods of the Burgess Shale, such as Anomalocaris (although in 2010 a new fossil deposit of Ordovician age has yielded the youngest Anomalocaris of all, and thus perhaps the Late Cambrian mass extinction was kinder to some of the odd Burgess Shale fauna than previously considered). This particular extinction has long been known, but it is not listed as “major,” in that less than 50 percent of marine forms died out. This acted like gasoline on the open fire of diversification, perhaps, in that those forms that were less adaptive died out, opening the way for new innovation and new species in the same manner that ridding a garden of weeds leads to a rapid proliferation of new growth from the nonweeded.
It was also as if the biological world discovered entirely new ways for animals and plants to make a living, as well as finding entirely new places to live: areas that were poorly populated in the Cambrian, such as brackish water and freshwater, as well as both deeper and shallower areas in the sea, right into the surf zones themselves, became ripe for colonization by animals. Many of these were still sedentary, spending their entire lives sitting in one place, filtering the ever-richer and more nutritious marine plankton. But species numbers and biomass numbers alike climbed.3
Many kinds of animals were present in the Ordovician that had not yet evolved in the Cambrian, and many of these appeared soon after the end of the Cambrian mass extinction. The result was an assemblage of animals that is markedly different than most of the Cambrian faunas. Trilobites are still there, but compared to the Cambrian oceans, when they may have been the most commonly encountered animal at most depths, they were overwhelmed in numbers as well as numbers of species of animals with shells—the brachiopods and more than a few mollusks as well. The biggest winners were animals that had evolved an entirely novel way of living—animals that were colonial. While colony formation was something that had been used by other biology far simpler in body plan, including many kinds of plants, microbes, and protozoa, in the Ordovician the leitmotif of colonial life dominated and drove the relentless diversification that is the hallmark of the Ordovician: corals, bryozoans, and new kinds of sponges among many others.
The reasons for this great diversification go back to oxygen.4 Our view is that the true effects of oxygenation in the sea can be seen from this point. Here, then, we will make an interpretation that historians do, one that is as yet still new enough in science that it cannot be considered as hard truth, but one that has enormous explanatory power. It also lets us look, quite appropriately at this point in the book, at an overview of animal diversification. We will argue that it was oxygen levels more than any other factor that has left us with the diversity curve of animals through time, results that are hard science and accepted.
The Ordovician period can be regarded as the second part of the two-part initiation of animal diversity on Earth, with the first being the Cambrian explosion,5 and in both cases, rising oxygen was the driver. Like the Cambrian, it was a time when new species as well as new kinds of body plans appeared at a faster rate than was characteristic of more recent times. This high rate of evolution and innovation was partly in response to filling up the world with animals for the first time. The history of life in the Cambrian was a filling of the seas with many experiments. The post-Cambrian history was one where many of these early and clearly primitive and inefficient evolutionary designs were replaced in what became a rocketing increase in biodiversity as competition ruthlessly killed off the less fit. Evolution became a means of exploring the engineering excellence of body plans.
THE HISTORY OF THE HISTORY OF BIODIVERSITY
The history of biodiversity, which can be thought of as the assembly and numbers of the various categories of organisms (especially anima
ls, because they leave the most abundant and recognizable fossils), was first presented by the English geologist John Phillips, who is also credited with subdividing the geological time scale through the introduction of the concepts of Paleozoic, Mesozoic, and Cenozoic eras. Phillips, who published his monumental work in 1860 both defining these new eras and discerning the largest-scale pattern of evolutionary change that can be found in the fossil record, recognized that major mass extinctions in the past could be used to subdivide geological time, since the aftermath of each such event resulted in the appearance of a new fauna as recognized in the fossil record. But Phillips did far more than recognize the importance of past mass extinctions and define new geological time terms: he proposed that diversity in the past was far lower than in the modern day, and that the rise of biodiversity has been one of wholesale increases in the number of species, except during and immediately after the mass extinctions. His scheme recognized that mass extinctions slowed down diversity, but only temporarily. Phillips’s view of the history of diversity was completely novel. Yet a century passed before the topic was again given scientific attention.
In the late 1960s, paleontologists Norman Newell and James Valentine again considered the problem of exactly when and at what rate the world became populated with species of animals and plants.6 Both wondered if the real pattern of diversification was of a rapid increase in species following the so-called Cambrian explosion of about 530 to 520 million years ago (using the revised dates, not those favored in the 1960s), followed by an approximate steady state. Their arguments rested on the importance of preservation biases in older rocks. Perhaps the pattern of increasing diversification through time seen by Phillips was in reality the record of preservation through time, rather than the real evolutionary pattern of diversification. According to this argument, the change of species is reduced in ever-older rocks, so that sampling bias is the real agent producing the so-called diversification he saw. This view was soon after echoed by paleontologist David Raup in a series of papers7 that forcefully argued that there are strong biases against older species being discovered and named by scientists, since older rocks experience more alteration through recrystallization, burial, and metamorphism; entire regions or biogeographic provinces have been lost through time (therefore reducing the record for older rocks); and there is simply more rock of younger age to be searched.
The argument as to whether diversity has shown a rapid increase through time or achieved a high level early on and has stayed approximately steady ever since dominated paleontological research for much of the latter part of the twentieth century. In the 1970s, massive data sets derived from library records began to be assembled by Raup and the late Jack Sepkoski8 of the University of Chicago along with his colleagues and students. These data, compiling the record of marine invertebrates in the sea, as well as other data sets for both terrestrial plants and for vertebrate animals, seemed to vindicate Phillips’s early view. In particular the curves discovered by Sepkoski showed a quite striking record, with three main pulses of diversification carried out by different assemblages of organisms.
The first was seen in the Cambrian (the so-called Cambrian fauna, composed of trilobites, brachiopods, and other archaic invertebrates), followed by a second in the Ordovician that led to an approximate steady state through the rest of the Paleozoic era (the Paleozoic fauna, composed of reef-building corals, articulate brachiopods, cephalopods, and archaic echinoderms), culminated by a rapid increase beginning in the Mesozoic and accelerating in the Cenozoic to produce the high levels of diversity seen in the world today through the evolution of the modern fauna, composed of gastropod and bivalve mollusk, most vertebrates, echinoids, and other groups.
The net view of biodiversity over the last 500 million years was thus about the same as that of John Phillips in 1860: there are more species on the planet now than at any time in the past. Even more comforting, the trajectory of biodiversity seemed to show that the engine of diversification—the processes producing new species—was in high gear, suggesting that in the future the planet would continue to have ever more species. While not at the time viewed in any sort of astrobiological context, these findings certainly do not suggest that planet Earth is in any sort of planetary old age. All in all, the 130-year belief, from the time and work of John Phillips to that of John Sepkoski—that there are more species now than any time in the past—remained a comforting view. This long-held scientific belief suggested to many that we are in the best of biological times (at least in terms of global biodiversity), and there is every reason to believe that better times, an even more diverse and productive world, still lie ahead, even without weird contributions from biotechnology.
Competing hypotheses about disparity and the Cambrian Explosion. Diversity refers to the number of species, whereas disparity refers to the number of different kinds of anatomies, or body plans. Stephen Jay Gould thought that there were many more body plans (high disparity) during the Cambrian Explosion than now. He referred to many of the strange fossils from the Burgess Shale as “weird wonders” and thought that they were phyla now entirely extinct. The opposite view was held by Simon Conway Morris, who advocated that disparity has slowly increased through time.
While the Sepkoski work seemed to show a world where runaway diversification is a hallmark of the Late Mesozoic into the modern day, worries about the very real sampling biases described by earlier workers persists, and a series of independent tests of diversity were conducted. Of most concern was a phenomenon dubbed the “pull of the recent”—that the methodology used by Sepkoski would undercount diversity in the deep past, making it look like there were ever more species in more recent times. Because of this very real concern, new tests were devised to examine biological diversity through time. In the early part of the new millennium the issue was reexamined9 by a large team headed by Charles Marshall of Harvard (now at Berkeley) and John Alroy, then at the University of California at Santa Barbara. This team assembled a more comprehensive database, based on actual museum collections rather than using Sepkoski’s method of simply tabulating the number of species recorded in the scientific literature for given intervals of past geologic time. To virtually everyone’s surprise, the first results of this effort were radically different from the long-accepted view.
The analyses of the Marshall-Alroy group found that diversity in the Paleozoic was about the same as in the mid-Cenozoic. The dramatic run-up of species that had so long been postulated for diversity through time was not evident in this new study. The implications are stark: we may have reached a steady state of diversity hundreds of millions of years ago. It may be that diversity peaked early in the history of animals, and in contrast to all views since the time of Phillips, it has remained in an approximate steady state since, or perhaps may already be in decline. While many new innovations, such as the adaptation allowing the evolution of land plants and animals, surely caused there to be many new species added to the planet’s biodiversity total, it may be that by late in Paleozoic time the number of species on the planet has been approximately constant.
Thus, following an initial burst of diversification in the lower Cambrian, animal diversity increased exponentially to reach equilibrium during the Paleozoic and then crashed at the end of the Permian, followed by an overall trend of increasing diversity, but importantly interrupted by short intervals of diversity decreases—the mass extinctions—of which five were particularly consequential. While these mass extinctions each led to substantial loss of taxa, all were followed by increased rates of species formation that led to levels not only equaling but in each case exceeding the original diversity prior to the extinction event.
This history suggests that a complex array of factors causing both diversification and extinction are responsible for the observed pattern of Phanerozoic diversity. Among the many potential factors that have been invoked to explain the observed increases in diversity are evolutionary innovation, the colonization of previously empty or unobtainable
habitats, and the occurrences of new resources, while the major factors cited for diversity drops are changes in climate, reduction of resources or habitat area, new biological competition or predation, or external events such as asteroid impact.
Geochemists have long known that CO2 levels and atmospheric oxygen levels show trends that are inversely related to one another: when oxygen levels rise, CO2 is usually dropping. While it is difficult to understand how changing levels of CO2 at concentrations that have little or no direct biological effect on individual organisms could somehow promote or inhibit diversification, it is quite plausible to suggest that it was not the changing CO2 but in fact a combination of changing oxygen levels, with that change being affected by global temperature rates.
Top graph: The trajectory of marine invertebrate animal diversity from the Cambrian Period onward, as discovered by Jack Sepkoski. His findings, based on long and prodigious library research, indicated that the numbers of genera rose quickly in the Paleozoic and then plateaued, only to be cut down by the Permian Mass Extinction. Afterward, he saw a great rise in generic numbers to the present day. Bottom graph: Here we show the levels of oxygen, as modeled by Robert Berner, with newer (than Sepkoski) estimates of animal generic numbers published by John Alroy and others. Notice the strong correlation between peak oxygen levels (both high and low) and the trajectory of animal numbers. (From Peter Ward, unpublished results.)
